INTEGRATED PEST MANAGEMENT OF ONION THRIPS AND FOLIAR FUNGAL 
PATHOGENS IN ONIONS 

By 

Natalie Constancio 

A DISSERTATION 

Submitted to 
Michigan State University 
in partial fulfillment of the requirements   
for the degree of 

Entomology – Doctor of Philosophy 

2024 

 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
ABSTRACT 

An integrated pest management (IPM) program is reliant on a thorough understanding of 

the biology and ecology of the target pest and incorporates multiple management tactics to 

reduce pest pressure. Management can be further complicated when multiple pest species, such 

as insect vectors and plant pathogens, interact in the field. Onion thrips (Thrips tabaci) are the 

main insect pest of onions and are well documented vectors of many different types of plant 

pathogens. The co-occurrence of onion thrips and facultative plant pathogens in the field is well 

documented, but it remains unclear how these pests interact, and whether the integration of 

multiple management tactics can provide synergistic control of these pests. This dissertation 

begins to fill that gap, exploring the relationship between onion thrips and Colletotrichum 

coccodes, a fungal pathogen of onion, and testing IPM strategies for multiple pest management. 

I first examined how C. coccodes influenced onion thrips behavior and physiology by 

conducting preference and performance experiments in the lab. By manipulating host plant 

health, I found that onion thrips can discriminate between multiple hosts and prefer hosts that 

were infected with C. coccodes compared to healthy hosts. Furthermore, adult onion thrips 

survived longer and reproduced at higher rates on plants infected with C. coccodes. Preference 

for an infected host can alter pathogen spread and increases in insect vector abundance often lead 

to more severe pathogen outbreaks. Therefore, I explored how onion thrips spread C. coccodes in 

the lab, examining density dependent and independent factors, such as temperature. At high 

temperatures, onion thrips reproduction increased, and they dispersed more often from an 

inoculated to a non-inoculated plant, leading to an increase in disease spread in the experiment. 

These results suggest that disease spread is likely density dependent, and that conditions favoring 

onion thrips outbreaks may also lead to more severe disease symptoms. Onion thrips and C. 

 
coccodes exhibit a mutually beneficial relationship; with onion thrips reproducing at higher rates 

on C. coccodes inoculated plants, and subsequently disease spread increased concurrently with 

increased vector abundance. 

I then focused on testing various IPM tactics in the field to reduce onion thrips and foliar 

fungal pathogens. Plastic mulches were tested as a non-chemical control method aimed at 

delaying onion thrips infestation in the field. I found that mulches are viable season-long 

alternative to conventional pesticides. Furthermore, the addition of conventional pesticides 

provided synergistic onion thrips control. Finally, I tested organic and conventional pesticide 

programs to develop a sustainable season-long control program for onion thrips and foliar fungal 

pathogens. Organic pesticides were not sufficient for onion thrips control, highlighting the need 

for alternative control methods and more sustainable conventional practices. To address this, I 

tested various action thresholds which reduced the number of pesticide applications throughout 

the season without compromising onion thrips control. 

This dissertation begins to fill the gaps in our existing knowledge of insect-plant-

pathogen interactions and suggests that the role of insects as vectors of facultative pathogens 

should not be overlooked. The mutually beneficial relationship between these pests further 

highlights the need to develop a comprehensive IPM program that focuses on managing both 

pests rather than focusing on a single species. By testing several IPM tactics, this work offers 

new insight into multiple pest management strategies that could be implemented in the field. 

 
 
 
 
This dissertation is dedicated to my husband, Joseph, and my family for their unwavering love 
and support throughout this journey.

iv 

 
ACKNOWLEDGEMENTS 

I would first like to thank my incredible advisor, Zsofia Szendrei, for giving me the 

opportunity to join the Vegetable Entomology Lab and guiding me through my time at MSU. 

Zsofia is an excellent mentor, but more importantly, an exceptional person. I would also like to 

thank my committee members, Mary Hausbeck, Doug Landis, and Ashley Leach who have all 

challenged me to be a better scientist. 

Thank you to all the Vegetable Entomology members for your support and feedback 

throughout the years: Logan Appenfeller, Eli Bloom, Kayleigh Hauri, Laura Marmolejo, Elizeth 

Cinto Mejía, Ray Rantz, Jen Roedel, Josh Snook and Patrick Stillson. Without you, this would 

have been a quiet and lonely journey. I would also like to thank DeShae Dillard, Joseph Taylor, 

Nayeli Carvajal, and Dan Turner for your friendship. Special shoutout to my debate teammates 

for teaching me to be confident in my knowledge and ability to express myself. Thank you to all 

the undergrads who spent hours counting thrips in the field, and many more hours smelling like 

onions afterwards. Thank you to my family, your support was felt from over 2,000 miles away. 

Finally, thank you to my husband for believing in me, even when I didn’t believe in myself. 

Thank you to all the growers who allowed me onto their farms to complete my research, 

and the incredible crew at SWMREC for their support in maintaining my field plots. I would also 

like to acknowledge my many funding sources for this research: USDA NIFA Organic 

Transitions Program, MSU Project GREEEN, MDARD Specialty Crop Block Grant and the 

Michigan Onion Committee. 

v 

 
 
 
TABLE OF CONTENTS 

CHAPTER 1: INTRODUCTION TO INSECT-PLANT-PATHOGEN INTERACTIONS AND 
MANAGEMENT STRATEGIES ……………………………………………………..………......1 
LITERATURE CITED …………………………………………………………..……..12 

CHAPTER 2: ONION THRIPS (THYSANOPTERA: THRIPIDAE) HOST PLANT 
PREFERENCE AND PERFORMANCE ARE MEDIATED BY A FACULTATIVE PLANT 
PATHOGEN OF ONION …………………………..…………………………………..……......18 
LITERATURE CITED ……………………………………………………………...…..42 
APPENDIX 1: CHAPTER 2 SUPPLEMENTARY MATERIALS…………..…………47 

CHAPTER 3: ENVIRONMENTAL CONDITIONS CAN INDIRECTLY AFFECT 
FACULTATIVE DISEASE SPREAD BY ALTERING INSECT VECTOR DISPERSAL ……51 
LITERATURE CITED ……………………………………………………...…………...79 

CHAPTER 4: PLASTIC MULCHES PROVIDE ALTERNATIVE MANAGEMENT OPTIONS 
FOR ONION THRIPS …………………………………………………………………………...84 
LITERATURE CITED …………………………………………………………………110 

CHAPTER 5: MANAGING INSECT AND PLANT PATHOGEN PESTS WITH ORGANIC 
AND CONVENTIONAL PESTICIDES IN ONION …………………………………………..116 
LITERATURE CITED ..………………………………………………………………..135 
APPENDIX 2: CHAPTER 5 SUPPLEMENTARY MATERIALS ………………..…..139 

CHATPER 6: CONCLUSIONS AND FUTURE DIRECTIONS ……………………………...145 
LITERATURE CITED …………………………………………………………………151 
APPENDIX 3: VOUCHER SPECIMEN RECORD ………………….………………..154 

vi 

 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
CHAPTER 1: INTRODUCTION TO INSECT-PLANT-PATHOGEN INTERACTIONS 
AND MANAGEMENT STRATEGIES 

Onion industry 

In 2020, China led the world in onion production (~40%), followed by India (~18%), the 

United States of America (~3%) and Egypt (~2.5%) (FAOTSTAT 2020). Globally, people 

consume about 6.35 kg of onions per person per year, with Americans consuming around 8.6 kg 

per person per year (NOA 2020). In the United States, the onion industry is valued at $1.5 billion 

(USDA/NASS 2024), and Michigan produces 1% of all the onions in the United States, making 

the value of the onion industry in the state worth around $10 million (USDA/NASS 2024). 

Onion thrips 

Onion thrips, Thrips tabaci Lindeman (Thysanoptera: Thripidae), are a major insect pest 

of onions found throughout the world and can cause significant yield loss if unmanaged (Gill et 

al. 2015; Lewis 1991). They cause indirect damage in onions by feeding on the plant foliage 

while also creating alternative entry points for plant pathogens (Lemmetty and Lindqvist 1993; 

Lewis 1997; McKenzie et al. 1993; Dutta et al. 2014). Currently, conventional insecticides are 

the primary management strategy for onion thrips control, and maintaining insecticide efficacy is 

a priority for onion growers. This can be achieved through reducing the risk of resistance 

development by rotating insecticide class and using action thresholds to determine when to make 

applications (Siegwart et al. 2015). However, onion thrips are resistant to many different active 

ingredients and action thresholds are difficult to implement (Nault and Hessney 2008, 2010, 

2011; Gill et al. 2015; Pedigo et al. 1986; Diaz-Montana et al. 2011). Therefore, non-chemical 

control methods must be explored, and a thorough understanding of onion thrips and their 

interactions with other organisms is necessary. 

1 

 
 
 
 
Onion thrips biology 

Onion thrips can reproduce sexually and asexually via thelytokous parthenogenesis, 

causing populations to quicky increase (Nault et al. 2006). Generations of onion thrips can 

switch between the different modes of reproduction, and often exist in the same field 

simultaneously, but it is unknown what factors determine the reproductive mode (Li et al. 2014; 

Nault et al. 2006). 

Onion thrips are holometabolous with distinct life stages. Eggs are laid by the female 

superficially into the plant tissue and, in laboratory studies, incubate for about 4 days, at 25 ± 

1℃ (Bhonde et al. 2016; Cranshaw 2004; Gill et al. 2015). Once hatched, onion thrips have two 

distinct, active feeding instar larval phases before pupating in the soil (Bhonde et al. 2016; 

Cranshaw 2004). Onion thrips are the most mobile during their adult stage due to their ability to 

fly and can migrate using wind currents (Lewis 1991). Adults overwinter in or around fields, and 

emergence is dependent on latitude and regional temperatures (Larentzaki et al. 2007; North and 

Shelton 1986). In Texas, onion thrips emerge as early as February, while in New York, most 

emerge in May (Edelson et al. 1986; Larentzaki et al. 2007). Post emergence, adult onion thrips 

colonize weeds and volunteer onion plants before infesting commercial onion fields. 

Feeding damage 

Onion thrips feed on the plant foliage with unique mouthparts consisting of a single 

mandible and a pair of stylets (Diaz-Montano et al. 2011; Chisholm and Lewis 1984). The 

mandible probes along the surface of the foliage for a feeding site, before puncturing the 

epidermis and consuming the cell contents (Chisholm and Lewis 1984; Cranshaw 2004; Lewis 

1991). This unique form of feeding is referred to as the “punch and suck” method and feeding 

can last anywhere from a few seconds to 30 minutes (Chisholm and Lewis 1984; Lewis 1991). 

2 

 
 
 
 
The punch and suck method of feeding leaves distinct, silvery scarring on the onion 

foliage due to the loss of chlorophyll (Boateng et al. 2014). Chlorophyll loss reduces the onion’s 

ability to photosynthesize, resulting in smaller bulbs and yield loss for growers (Boateng et al. 

2014). Even light amounts of feeding leave distinct scarring, allowing growers to identify onion 

thrips infestations (Chisholm and Lewis 1984). Onion thrips feed at the proximal end of the 

onion leaf, impacting the onions’ ability to transfer nutrients to the bulb (Parrella and Lewis 

1997). Feeding during the bulbing stage of onion development reduces bulb size and can cause 

economic loss for growers while also allowing for pathogen entrance into the plant tissue 

(Kendall and Capinera 1987).  

Thrips as vectors of plant diseases 

In addition to creating entry points for plant pathogens via feeding, onion thrips vector 

diseases. While larval onion thrips cause the majority of feeding damage seen on plants, adults 

are more mobile and thus more likely to vector pathogens over long distances (Lewis 1991; 

Bailey 1935). Onion thrips are well known vectors of Orthtospoviruse, but can also spread 

bacterial, and fungal plant pathogens (Cortes et al. 1998; Dutta et al. 2014; Leach et al. 2020; 

Lemmetty and Lindqvist 1993). 

Onion thrips can transmit at least two economically important Orthotospoviruses: the 

tomato spotted wilt virus and the iris yellow spotted virus (Lemmetty and Lindqvist 1993; Cortes 

et al. 1998). Othrotospoviruses are persistent, circulative pathogens, acquired during the larval 

stage, where the virus has a latency period before being transmitted (Ullman et al. 1992). While 

it is possible that larval onion thrips can spread the virus, adults are more likely to be vectors due 

to their high mobility (Lewis 1991; Ullman et al. 1992). 

Onion thrips can vector bacterial pathogens within the Pantoea genus, such Pantoea 

3 

 
 
 
 
ananatis, the causal agent of center rot in onion (Dutta et al. 2014). The infection begins as 

blotching or spotting on the foliage before spreading to the bulb and causing infections during 

storage (Carr et al. 2013; Coutinho and Venter 2009). The bacteria are acquired by feeding on an 

infected host and spread via feces (Dutta et al. 2014; Dutta et al. 2016). High onion thrips 

infestations exacerbate symptoms of bacterial leaf blight and bactericides are not effective at 

reducing necrotic spread (Grode et al. 2017; Grode et al. 2019). Often, the most efficient way to 

reduce disease spread is by managing onion thrips populations with insecticides (Grode et al. 

2019). 

High infestations of onion thrips can also exacerbate symptoms of fungal disease (Leach 

et al. 2017; McKenzie et al. 1993; Marullo 1995). Stemphylium leaf blight (Stemphylium 

vesicarium) is a fungal disease first reported on onion crops in Texas in 1978 and had been 

reported sporadically but has recently become a dominant pathogen in the Eastern United States 

production region (Miller et al. 1978; Hausbeck and Werling 2018; Hay et al. 2019; Hay et al. 

2021). Disease symptoms are characterized by foliar lesions ranging from light yellow to brown, 

and generally occur on the side of the leaf facing the prevailing winds (Miller et al. 1978). 

Anthracnose (Colletotrichum coccodes) is another onion fungal disease that was found in 

Michigan in 2012 and has persisted at low levels since (Rodriguez-Salamanca et al. 2012). The 

lesions appear tan or salmon-colored, and then dark spores begin to develop (Rodriguez-

Salamanca et al. 2018). Both pathogens, if left uncontrolled, can cause significant economic loss 

for growers (Rodriguez-Salamanca et al. 2012; Leach et al. 2020). Developing management 

plans that can reduce onion thrips and pathogen pests simultaneously is a high priority for onion 

growers. However, understanding how these pests interact is critical to creating an effective 

integrated management plan. 

4 

 
 
Integrated pest management for multiple organisms 

Integrated pest management requires a thorough understanding of the biology and 

ecology of the target pests, and the integration of multiple control tactics to create a cohesive 

plan (Kogan 1998). For onion thrips and fungal pathogens, such as C. coccodes, understanding 

how these pests interact with one another is critical before implementing a management program. 

Currently, insecticide applications are used to reduce onion thrips populations while reducing 

disease spread more efficiently than applying bactericides or fungicides alone (Grode et al. 2019; 

Leach et al. 2020). However, tank mixing insecticides and fungicides can reduce insecticide 

efficacy, highlighting the difficulties of multiple pest management (Nault et al. 2013). Therefore, 

it is important to first examine the interaction between pests, test non-chemical management 

strategies to delay infestation, and finally, develop a pesticide program that can target both pests. 

Insect-plant-pathogen interactions 

Insect pests and plant pathogens interact when they colonize the same host plant. The 

interactions between obligate pathogens and their vectors are well described, but these 

interactions are more obscure for facultative pathogens (Jeger 2020; Lowery et al. 2015; Shaw et 

al. 2017). Facultative pathogens do not rely on insects for dispersal, but insects can contribute to 

pathogen spread in multiple ways via mechanical vectoring or by creating alternative entry 

points through feeding (Tiberi et al. 2016; Eigenbrode et al. 2018). Plant pathogens can also 

affect insect behavior or physiology, and understanding the outcomes of these interactions is 

important for pest management (Daugherty et al. 2011; Ingwell et al. 2012). 

Behavioral modifications can include changes in vector preference for or discrimination 

against an infected host, which can alter the rate of disease spread (Maris et al. 2004; Abe et al. 

2012; Shrestha et al. 2012). However, preference is variable, and can change based on host 

5 

 
 
 
infection stage, and may also change after pathogen exposure (Daugherty et al. 2011; Ingwell et 

al. 2012; Mauck et al. 2018). The vector manipulation hypothesis (VMH) suggests that insect 

behavior, specifically preference, changes throughout the insect’s life to increase the rate of 

disease spread (Ingwell et al. 2012). Insects may prefer an infected host, but after pathogen 

exposure that preference may change and the insect may move to a healthy plant, thus spreading 

the pathogen (Ingwell et al. 2012; Daugherty et al. 2011; Blua and Perring 1992). Conversely, if 

an insect discriminates against an infected host, the contact between the insect and the pathogen 

is reduced, and disease spread should be decreased. The VMH was first documented in aphids, 

but thrips spp. exhibit preference for hosts infected with Orthotospoviruses, and a similar 

mechanism may be occurring (Ingwell et al. 2012; Maris et al. 2004; Abe et al. 2012). 

Physiological modifications can occur when insect performance is affected by host plant 

infection status, such as increased reproduction or higher survival. Onion thrips on grape leaves 

or roses infected with downy mildew perform better than on healthy leaves (Yarwood 1943). 

Interestingly, preference and performance may not be linked traits, and are likely to be species 

specific. For example, western flower thrips (Frankliniella occidentalis) prefer and perform 

better on infected hosts, and tobacco thrips (Frankliniella fusca) prefer infected hosts but 

perform poorly on those same hosts (Maris et al. 2004; Abe et al. 2012; Shrestha et al. 2012). It 

is difficult to predict the effect of host plant infection status on preference and performance, 

therefore, species specific studies on economically important pathogens and thrips are necessary. 

Non-chemical control methods 

Within an integrated pest management program, the inclusion of non-chemical control 

methods is encouraged to reduce pest populations below economically damaging levels. Physical 

control methods, such as plastic mulches have been used by growers for many reasons including 

6 

 
 
increased yield and soil moisture retention, weed reduction, and microclimate control (Kasirajan 

and Ngouajio 2012; Greer and Dole 2003). Plastic mulches are also used for pest control, but the 

efficacy is variable and dependent on the crop, target pest, and mulch color. 

Silver reflective mulches are often used to reduce insect colonization but have had 

variable success in reducing thrips populations, and the effectiveness may change throughout the 

season (Iglesias et al. 2021; Momol et al. 1999). Western flower thrips in pepper cropping 

systems alighted less on peppers planted in reflective mulch beds, but by the end of the season, 

the peppers had higher thrips populations compared to the control (Reitz et al. 2003). It is likely 

that the temporal variation is due to increased canopy cover reducing the amount of exposed 

mulch, thus making the mulch ineffective (Reitz et al. 2003). However, in tomatoes, western 

flower thrips populations were deterred by reflective mulches, and the tomato plants had a lower 

disease incidence compared to the control (Anderson et al. 2012). The discrepancies within the 

literature make it difficult to predict how onion thrips will react to reflective mulches, but since 

mulches are used by some onion producers it is important to consider how they may directly or 

indirectly affect onion thrips populations. 

There are multiple theories describing the mechanisms behind plastic mulches, either 

focusing on the indirect or direct effects (Andreotti et al. 2010; Gordon et al. 2008; Ham et al. 

1993; Mathejczyk and Wernet 2017; Kelber 1999). Plastic mulches may indirectly affect thrips 

populations through alterations in microclimate (Andreotti et al. 2010; Gordon et al. 2008; Ham 

et al. 1993). Dark mulches, such as blue or black mulches, increase the air and soil temperature, 

potentially creating an inhospitable environment (Gordon et al. 2008). Mulches may directly 

affect thrips populations by reducing host finding ability. Sunlight reflected off plants can 

become polarized, which insects, such as butterflies, can then use to orient themselves towards a 

7 

 
 
host (Kelber 1999). Highly reflective plastic mulches or colored plastic mulches may alter the 

wavelength and polarization of light, thus disorienting an insect (Mathejczyk and Wernet 2017). 

To better understand the mechanisms behind repellency it is important that researchers measure 

changes in the microclimate in the field, and the effect of different colored mulches on host plant 

selection. While plastic mulches can reduce both insect abundance and disease spread, they 

become less effective later in the season. Therefore, it is important to combine colored mulches 

with a curative measure, such as action threshold-based insecticide applications. 

Chemical control of onion thrips 

Insecticides are currently the cornerstone for onion thrips management despite problems 

with resistance to several different conventional insecticide classes (Yadav et al. 2018; Martin et 

al. 2003; Nault and Shelton 2010; Diaz-Montano et al. 2011; Adesanya et al. 2020). To reduce 

insecticide resistance development, the rotation of insecticide classes is recommended (Gill and 

Garg 2014). However, insecticide class rotation can be difficult because there are relatively few 

highly effective active ingredients for onion thrips management (Gill et al. 2015; Nault and 

Hessney 2008, 2010, 2011). Maintaining the efficacy of the available insecticides is a top 

priority for growers and can be achieved through implementing action thresholds to reduce the 

number of applications per season (Siegwart et al. 2015; Gill et al. 2015; Leach et al. 2017). 

However, for onion thrips, action thresholds vary depending on the insecticide being applied, 

indirect damage on leaves, field location and weather conditions, thus regular scouting of fields 

throughout the season is essential (Pedigo et al. 1986; Fournier et al. 1995; Rueda et al. 2007; 

Nault and Shelton 2010; Diaz-Montana et al. 2011). The lack of available insecticides as well as 

the difficulty in implementing action thresholds make resistance management a challenge for 

growers if appropriate extension-based education programs are not available for growers (Leach 

8 

 
 
et al. 2019). 

Further complexities occur when multiple pests, such as onion thrips and pathogens, co-

occur in fields, requiring growers to manage both pests simultaneously. However, tank mixing 

insecticides with certain fungicides lowers the efficacy of insecticides, indicating that an 

integrated plan is necessary (Nault et al. 2013). Insecticide applications are more effective at 

reducing pathogen spread than fungicide or bactericide applications, indicating that insect 

management is critical for reducing disease spread (Grode et al. 2017; Leach et al. 2020). 

Therefore, developing new action thresholds that consider the interaction of onion thrips and 

plant pathogens is critical for pest management. 

Organic insecticides or biopesticides have fewer non-target impacts, thus these may be 

more amenable for use in an IPM program. Multiple organic insecticides, including spinosyns 

and azadirachtin, have been tested for onion thrips control (Dively et al. 2020; Iglesias et al. 

2021). However, whether the addition of an organic bactericide or fungicide reduces insecticide 

efficacy has not been tested. Organic pesticides are short lived relative to conventional pesticides 

and are less effective later in the season when pest pressure is high (Golec et al. 2020; Dively et 

al. 2020). Developing a season long organic program that manages onion thrips and fungal 

pathogens would require careful consideration of application timing and efficacy testing. 

Research objectives 

My research aimed to create an IPM program for onion thrips and fungal pathogen 

management, focusing on understanding the relationship between these pests, testing methods to 

reduce pest infestation, and finally exploring sustainable chemical control methods (Figure 1.1). 

The relationship between onion thrips and C. coccodes was explored in laboratory-based 

experiments. In objective 1, host plant selection was documented with paired preference and 

9 

 
 
 
performance experiments, giving insight into how C. coccodes inoculated plants altered onion 

thrips behavior and physiology. It was unclear if onion thrips contribute to the spread of C. 

coccodes, therefore disease spread experiments were conducted to determine whether they are 

vectors in objective 2. By manipulating onion thrips populations and then altering environmental 

conditions, both density dependent and density independent factors affecting pathogen spread 

were tested. For objective 3, plastic mulches were tested in the field to determine if onion thrips 

infestations could be reduced with non-chemical control methods. Changes in plant growth and 

microclimate were monitored throughout the season to determine whether mulches directly or 

indirectly affected onion thrips populations. Finally for objective 4, organic pesticides were 

evaluated for their efficacy against onion thrips and pathogen spread, and the action thresholds of 

conventional pesticides were assessed. 

10 

 
 
11 

 
 
 
 
 
LITERATURE CITED 

Abe H, Y. Tomitaka, T. Shimoda, S. Seo, T. Sakurai, S. Kugimiya, S. Tsuda, and M. Kobayashi. 

2012. Antagonistic plant defense system regulated by phytohormones assists interactions 
among vector insect, thrips and a tospovirus. Plant Cell Physiol. 53: 204–212. 

Adesanya, A. W., T. D. Waters, M. D. Lavine, D. B. Walsh, L. C. Lavine, and F. Zhu. 2020. 
Multiple insecticide resistance in onion thrips populations from Western USA. Pestic. 
Biochip. Physiol. 165: 104553. 

Andersen, P. C., S. M. Olson, M. T. Momol, and J. H. Freeman. 2012. Effect of Plastic Mulch 

Type and Insecticide on Incidence of Tomato Spotted Wilt, Plant Growth, and Yield of 
Tomato. HortScience. 47: 861–865. 

Andreotti, C., D. Ravaglia, and G. Costa. 2010. Effects of Fruit Load and Reflective Mulch on 
Phenolic Compounds Accumulation in Nectarine Fruit. Eur.J. Hort.Sci.75(2): 53-59. 

Bailey, S. F. 1935. Thrips as Vectors of Plant Disease. J. Econ. Entomol. 28: 856–863. 

Bhonde, B. N., D. B. Pawar, D. P. Nikam, and M. Phule Krishi Vidyapeeth. 2016. Biology of 
onion thrips, Thrips tabaci (Lind.) (Thysanoptera:Thripidae) on onion Allium cepa 
(Linnaeus), Adv. Life Sci. 5(19): 8789-8971. 

Blua, M. J., and T. M. Perring. 1992. Effects of zucchini yellow mosaic virus on colonization 

and feeding behavior of Aphis gossypii (Homoptera: Aphididae) alatae. Environ. Entomol. 
21: 578–585. 

Boateng, C. O., H. F. Schwartz, M. J. Havey, and K. Otto. 2014. Evaluation of Onion 

Germplasm for Resistance to Iris Yellow Spot and Onion Thrips, Thrips tabaci. Southwest. 
Entomol. 39: 237–260. 

Carr, E. A., A. M. Zaid, J. M. Bonasera, J. W. Lorbeer, and S. V. Beer. 2013. Infection of onion 

leaves by Pantoea ananatis leads to bulb infection. Plant Dis. 97: 1524–1528. 

Chisholm, I. F., and T. Lewis. 1984. A new look at thrips (Thysanoptera) mouthparts, their 
action and effects of feeding on plant tissue. Bull. Entomol. Res. 74: 663–675. 

Coutinho, T. A., and S. N. Venter. 2009. Pantoea ananatis: an unconventional plant pathogen. 

Mol. Plant Pathol. 10: 325–335. 

Cranshaw, W. 2004. Garden Insects of North America. Princeton University Press, Princeton. 

Daugherty, M. P., A. Rashed, R. P. P. Almeida, and T. M. Perring. 2011. Vector preference for 

hosts differing in infection status: Sharpshooter movement and Xylella fastidiosa 
transmission. Ecol. Entomol. 36: 654–662. 

12 

 
 
Diaz-Montano, J., M. Fuchs, B. A. Nault, J. Fail, and A. M. Shelton. 2011. Onion thrips 

(Thysanoptera: Thripidae): A global pest of increasing concern in onion. J. Econ. Entomol. 
104: 1–13. 

Dutta, B., A. K. Barman, R. Srinivasan, U. Avci, D. E. Ullman, D. B. Langston, and R. D. 

Gitaitis. 2014. Transmission of Pantoea ananatis and P. agglomerans, Causal agents of 
center Rot of Onion (Allium cepa), by onion thrips (Thrips tabaci) through feces. 
Phytopath. 104: 812–819. 

Dutta, B., R. Gitaitis, A. Barman, U. Avci, K. Marasigan, and R. Srinivasan. 2016. Interactions 
Between Frankliniella fusca and Pantoea ananatis in the Center Rot Epidemic of Onion 
(Allium cepa). Phytopath. 106: 956–962. 

Edelson, J. V., B. Cartwright, and T. A. Royer. 1986. Distribution and Impact of Thrips tabaci 

(Thysanoptera: Thripidae) on Onion. J. Econ. Entomol. 79: 502–505. 

Eigenbrode, S. D., N. A. Bosque-Pérez, and T. S. Davis. 2018. Insect-Borne Plant Pathogens and 
Their Vectors: Ecology, Evolution, and Complex Interactions. Annu. Rev. Entomol. 63: 
169–191. 

FAOSTAT: Food and Agriculture Organization of the United Nations. Accessed March 2024. 

https://www.fao.org/faostat/en/#home  

Fournier, F., G. Boivin, and R. K. Stewart. 1995. Effect of Thrips tabaci (Thysanoptera: 

Thripidae) on Yellow Onion Yields and Economic Thresholds for Its Management. J. 
Econ. Entomol. 88: 1401–1407. 

Gill, H. K., H. Garg, A. K. Gill, J. L. Gillett-Kaufman, and B. A. Nault. 2015. Onion thrips 

(Thysanoptera: Thripidae) biology, ecology, and management in onion production systems. 
J. Integr. Pest Manag. 6: 1–9. 

Gill, H. K., and H. Garg. 2014. Pesticides: Environmental Impacts and Management Strategies. 

In Larramendy, M., Soloneski, S. (eds.), Pesticides- Toxic Aspect. InTechOpen. 

Golec, J. R., B. Hoge, and J. F. Walgenbach. 2020. Effect of biopesticides on different 

Tetranychus urticae Koch (Acari: Tetranychidae) life stages. Crop Prot. 128: 105015. 

Gordon, G. G., W. G. Foshee, S. T. Reed, J. E. Brown, E. Vinson, and F. M. Woods. 2008. 

Plastic mulches and row covers on growth and production of summer squash. Int. J. Veg. 
Sci. 14: 322–338. 

Greer, L., and J. M. Dole. 2003. Aluminum foil, aluminium-painted, plastic, and degradable 
mulches increase yields and decrease insect-vectored viral diseases of vegetables. 
HortTechnol. 13: 276–284. 

13 

 
 
Grode, A., S. Chen, E. D. Walker, and Z. Szendrei. 2017. Onion Thrips (Thysanoptera: 

Thripidae) Feeding Promotes Infection by Pantoea ananatis in Onion. J. Econ. Entomol. 
110: 2301–2307. 

Ham, J. M., G. J. Kluitenberg, and W. J. Lamont. 1993. Optical Properties of Plastic Mulches 
Affect the Field Temperature Regime, J. Amer. Soc. Hort. Sci. 118(2): 188-193. 

Hausbeck, M., and B. Werling. 2018. Protect onions against Stemphylium leaf blight. 

Hay, F. S., S. Sharma, C. Hoepting, D. Strickland, K. Luong, and S. J. Pethybridge. 2019. 

Emergence of Stemphylium Leaf Blight of Onion in New York Associated with Fungicide 
Resistance. Plant Dis. 103: 3083–3092. 

Hay, F., S. Stricker, B. D. Gossen, M. R. McDonald, D. Heck, C. Hoepting, S. Sharma, and S. 

Pethybridge. 2021. Stemphylium Leaf Blight: A Re-Emerging Threat to Onion Production 
in Eastern North America. Plant Dis. 105: 1–15. 

Iglesias, L., M. J. Havey, and B. A. Nault. 2021. Management of onion thrips (Thrips tabaci) in 

organic onion production using multiple IPM tactics. Insects. 12: 1–16. 

Ingwell, L. L., S. D. Eigenbrode, and N. A. Bosque-Pérez. 2012. Plant viruses alter insect 

behavior to enhance their spread. Sci. Rep. 2. 

Jeger, M. J. 2020. The epidemiology of plant virus disease: Towards a new synthesis. Plants. 9: 

1–50. 

Kasirajan, S., and M. Ngouajio. 2012. Polyethylene and biodegradable mulches for agricultural 

applications: A review. Agron. Sustain. Dev. 32: 501–529. 

Kelber, A. 1999. Why “false” colours are seen by butterflies. Nature. 402: 251. 

Kendall, D. M., and J. L. Capinera. 1987. Susceptibility of Onion Growth Stages to Onion Thrips 
(Thysanoptera: Thripidae) Damage and Mechanical Defoliation. Environ. Entomol. 16: 
859–863. 

Kogan, M. 1998. Integrated pest management: Historical perspectives and contemporary 

developments. Annu. Rev. Entomol. 43: 243-270. 

Larentzaki, E., A. M. Shelton, F. R. Musser, B. A. Nault, and J. Plate. 2007. Overwintering 

Locations and Hosts for Onion Thrips (Thysanoptera: Thripidae) in the Onion Cropping 
Ecosystem in New York. J. Econ. Entomol. 100: 1194–1200. 

Leach, A., S. Reiners, M. Fuchs, and B. Nault. 2017. Evaluating integrated pest management 

tactics for onion thrips and pathogens they transmit to onion. Agric. Ecosyst. Environ. 250: 
89–101. 

14 

 
 
Leach, A., C. Hoepting, B. Nault. 2019. Grower adoption of insecticide resistance management 

practices increase with extension-based program. Pest Manag. Sci. 75: 515-526. 

Leach, A., F. Hay, R. Harding, K. C. Damann, and B. Nault. 2020. Relationship between onion 

thrips (Thrips tabaci) and Stemphylium vesicarium in the development of Stemphylium leaf 
blight in onion. Ann. Appl. Biol. 176: 55–64. 

Lemmetty, A., and I. Lindqvist. 1993. Thrips tabaci (Lind.) (Thysanoptera: Thripidae), another 

vector for tomato spotted wilt virus in Finland. Agric. Food Sci. 2: 189–194. 

Lewis, T. 1991. Feeding, flight and dispersal in thrips. Toward understanding. Thysanoptera. 

Proc. Int. Conf. Thrips. 63–70. 

Li, X.-W., J. Fail, P. Wang, J.-N. Feng, and A. M. Shelton. 2014. Performance of Arrhenotokous 

and Thelytokous Thrips tabaci (Thysanoptera: Thripidae) on Onion and Cabbage and Its 
Implications on Evolution and Pest Management. J. Econ. Entomol. 107: 1526–1534. 

Lowery, D. T., P. M. Vickers, L. A. Bittner, L. W. Stobbs, and R. G. Foottit. 2015. Aphid 

transmission of the Ontario isolate of plum pox virus. J. Econ. Entomol. 108: 2168–2173. 

Maris, P. C., N. N. Joosten, R. W. Goldbach, and D. Peters. 2004. Tomato spotted wilt virus 
infection improves host suitability for its vector Frankliniella occidentalis. Phytopath. 
jo94: 706–711. 

Martin, N. A., P. J. Workman, and R. C. Butler. 2003. Insecticide resistance in onion thrips 
(Thrips tabaci) (Thysanoptera: Thripidae). New Zeal. J. Crop Hortic. Sci. 31: 99–106. 

Marullo, R. 1995. Possible Dissemination of Pest Fungi by Thrips. Thrips Biol. Manag. 201–

202. 

Mathejczyk, T. F., and M. F. Wernet. 2017. Sensing Polarized Light in Insects, Oxford Res. 

Encycl. Neurosci. 

Mauck, K. E., Q. Chesnais, and L. R. Shapiro. 2018. Evolutionary Determinants of Host and 

Vector Manipulation by Plant Viruses, 1st ed, Adv. Virus Res. Elsevier Inc. 

McKenzie, C. L., B. Cartwright, M. E. Miller, and J. V. Edelson. 1993. Injury to Onions by 

Thrips tabaci (Thysanoptera: Thripidae) and Its Role in the Development of Purple Blotch. 
Environ. Entomol. 22: 1266–1277. 

Miller, M., R. Taber, and J. Amador. 1978. Stemphylium leaf blight of onion in South Texas. 

Plant Dis. Report. 62: 851–853. 

Momol, M. T., J. E. Funderburk, S. Olson, and J. Stavisky. 1999. Management of TSWV on 

tomatoes with UV-reflective mulch and acibenzolar-S-methyl. Education. 111–116. 

15 

 
 
Nault, B. A., and M. Lou Hessney. 2011. Onion thrips control in onion – Trial I, 2010. 

Arthropod Manag. Tests. 36. 

Nault, B. A., and M. Lou Hessney. 2010. Onion thrips control in onion, 2009. Arthropod Manag. 

Tests. 35. 

Nault, B. A., and M. Lou Hessney. 2008. Onion thrips control in onion, 2006. Arthropod Manag. 

Tests. 33. 

Nault, B. A., C. L. Hsu, and C. A. Hoepting. 2013. Consequences of co-applying insecticides and 
fungicides for managing Thrips tabaci (Thysanoptera: Thripidae) on onion. Pest Manag. 
Sci. 69: 841–849. 

Nault, B. A., and A. M. Shelton. 2010. Impact of insecticide efficacy on developing action 

thresholds for pest management: A case study of onion thrips (Thysanoptera: Thripidae) on 
onion. J. Econ. Entomol. 103: 1315–1326. 

Nault, B. A., A. M. Shelton, J. L. Gangloff-kaufmann, M. E. Clark, J. L. Werren, J. C. Cabrera-la 
Rosa, and G. G. Kennedy. 2006. Reproductive Modes in Onion Thrips (Thysanoptera: 
Thripidae) Populations from New York Onion Fields. Environ. Entomol. 35: 1264–1271. 

NOA: National Onion Association. Accessed March 2024. https://www.onions-usa.org/all-

about-onions/retail/consumer-
trends/#:~:text=Onions%20represent%20the%20third%20largest,increase%20in%20consu
mption%20since%201970.  

Parrella, M., and T. Lewis. 1997. Integrated pest management (IPM) in field crops, pp. 595–614. 

In Lewis, T. (ed.), Thrips as Crop Pests. CAB International, Wallingford. 

Pedigo, L. 1986. Economic Injury Levels in Theory and Practice. Annu. Rev. Entomol. 31: 341–

368. 

Reitz, S. R., E. L. Yearby, J. E. Funderburk, J. Stavisky, M. T. Momol, and S. M. Olson. 2003. 
Integrated management tactics for Frankliniella thrips (Thysanoptera: Thripidae) in field-
grown pepper. J. Econ. Entomol. 96: 1201–1214. 

Rodriguez-Salamanca, L. M., T. B. Enzenbacher, M. L. Derie, L. J. du Toit, C. Feng, J. C. 

Correll, and M. K. Hausbeck. 2012. First Report of Colletotrichum coccodes Causing Leaf 
and Neck Anthracnose on Onions (Allium cepa) in Michigan and the United States. Plant 
Dis. 96: 769–769. 

Rodriguez-Salamanca, L. M., R. P. Naegele, L. M. Quesada-Ocampo, and M. K. Hausbeck. 
2018. Inoculation method, temperature, and relative humidity affect leaf and neck 
anthracnose, a new onion disease in Michigan. Plant Heal. Prog. 19: 64–68. 

16 

 
 
Rueda, A., F. R. Badenes-Perez, and A. M. Shelton. 2007. Developing economic thresholds for 

onion thrips in Honduras. Crop Prot. 26: 1099–1107. 

Shaw, A. K., A. Peace, A. G. Power, and N. A. Bosque-Pérez. 2017. Vector population growth 
and condition-dependent movement drive the spread of plant pathogens. Ecology. 98: 
2145–2157. 

Shrestha, A., R. Srinivasan, D. G. Riley, and A. K. Culbreath. 2012. Direct and indirect effects of 
a thrips-transmitted tospovirus on the preference and fitness of its vector, Frankliniella 
fusca. Entomol. Exp. Appl. 145: 260–271. 

Siegwart, M., B. Graillot, C. B. Lopez, S. Besse, M. Bardin, P. C. Nicot, and M. Lopez-Ferber. 

2015. Resistance to bio-insecticides or how to enhance their sustainability: A review. Front. 
Plant Sci. 6: 1–19. 

Tiberi, R., T. Panzavolta, M. Bracalini, A. Ragazzi, B. Ginetti, S. Moricca, R. Tiberi, T. 

Panzavolta, M. Bracalini, A. Ragazzi, B. Ginetti, and S. Moricca. 2016. Interactions 
between insects and fungal pathogens of forest and ornamental trees. Ital. J. Mycol. 45: 54–
65. 

Ullman, D. E. 1992. A Midgut Barrier to Tomato Spotted Wilt Virus Acquisition by Adult 

Western Flower Thrips. Phytopath. 82. 

USDA/NASS: United States Department of Agriculture, National Agricultural Statistics Service. 

Accessed March 2024. https://www.nass.usda.gov/Data_and_Statistics/index.php  

Yadav, M., R. Prasad, P. Kumar, and C. Pandey. 2018. A review on onion thrips and their 

management of bulb crops A review on onion thrips and their management of bulb crops. J. 
Pharmacogn. Phytochem. Ctry. 7(1S): 891–896. 

Yarwood, C. E. 1943. Association of Thrips with Powdery Mildews. Mycologia. 35: 189–191. 

17 

 
 
 
 
CHAPTER 2: ONION THRIPS (THYSANOPTERA: THRIPIDAE) HOST PLANT 
PREFERENCE AND PERFORMANCE ARE MEDIATED BY A FACULTATIVE PLANT 
PATHOGEN OF ONION 

Acknowledgement of prior publication 

This chapter is a reprint of an original peer-reviewed published article in Environmental 

Entomology in 2022, volume 51(6). It can be found at doi: 10.1093/ee/nvac086. The author has 

been permitted to republish the article in this dissertation via the Copyright Clearance Center 

Rightslink® (Figure S2.4).  

Abstract 

Insect vector and phytopathogen interactions are mediated by host plants. Insects interact 

with pathogens directly or indirectly and they may prefer host plants based on infection status. 

Performance on infected hosts varies depending on the type of pathogen involved. Species 

specific studies of economically important insects and phytopathogens are needed to understand 

how these interactions impact crop yields. Onion thrips, Thrips tabaci Lindeman, is an 

economically devastating insect pest of onions (Allium cepa L.) worldwide and it co-occurs 

simultaneously with many different pathogens. Colletotrichum coccodes (Wallr) is a generalist 

fungal pathogen that attacks onion foliage, causing tan lesions and decreasing yield. Onion thrips 

and C. coccodes represent two important pests of onions, but the relationship between onion 

thrips and C. coccodes infected onions has not been studied, and it is unclear if onion thrips 

contribute to the spread of C. coccodes in onion fields. A four-choice test with control, 

artificially injured, artificially injured + symptomatic, and inoculated-symptomatic onion 

suggests that onion thrips distinguish between hosts based on health status. Furthermore, a two-

choice test with control, inoculated-asymptomatic, and inoculated-symptomatic onion pairings 

revealed that onion thrips distinguish between hosts based on infection status and prefer 

18 

 
 
 
 
inoculated-symptomatic hosts. In a no-choice test, onion thrips numbers increased on inoculated-

symptomatic plants compared to control or inoculated-asymptomatic plants. Overall, we found 

that onion thrips preferred and performed best on C. coccodes infected plants. 

Introduction 

Herbivorous insects interact with phytopathogens when they colonize the same host. For 

example, insects can interact with plant pathogens through obligate and facultative vectoring 

(Gonella et al. 2019; Franco et al. 2017). While the relationship between insect vectors and 

obligate pathogens is often well defined, facultative pathogen vectoring is more ambiguous. 

Predicting the outcomes becomes difficult because facultatively vectored pathogens are spread 

by insects in multiple ways, such as creating entry points via feeding, spreading through feces, or 

carrying on the integument (Eigenbrode et al. 2018; Tiberi et al. 2016). In addition, plant 

pathogens can interact with insect vectors by modifying their behavior, physiology, and fitness 

(Simon and Hilker 2003). For example, a host plant’s infection status can have profound impacts 

on an insect vector’s preference and performance (Daugherty et al. 2011; Ingwell et al. 2012). 

Whether an insect prefers or discriminates against a host based on infection status is especially 

important for pest management. 

Many thrips (Thysanoptera: Thripidae) species are plant pathogen vectors and are known 

for their role as tospovirus vectors; they also contribute to the spread of several fungal and 

bacterial plant pathogens (Ananthakrishnan and Dhileepan 1984; Whitfield et al. 2005; Diaz-

Montano et al. 2011). Thrips can be obligate vectors of pathogens, for example, western flower 

thrips, Frankliniella occidentalis Pergande (Thysanoptera: Thripidae), vector the tospovirus 

tomato spotted wilt virus (TSWV) and onion thrips, Thrips tabaci Lindeman (Thysanoptera: 

Thripidae), vector iris yellow spot virus (Wijkamp et al. 1995; Kritzman et al. 2001; Pozzer et al. 

19 

 
 
 
1999).Thrips can also vector pathogens facultatively as in the case of the New Zealand flower 

thrips, Thrips obscuratus Crawford (Thysanoptera: Thripidae), which mechanically vector 

Botrytis cinerea when conidia become attached to the integument (Fermaud and Gaunt 1995). 

Onion thrips are potential facultative vectors of powdery mildew (Erysiphe polygoni) with higher 

thrips numbers resulting in increased powdery mildew incidence (Yarwood 1943). Similarly, 

western flower thrips contribute to the spread of Fusarium rot (Fusarium verticillioides) (Farrar 

and Davis 1991). In cotton, flower thrips (Frankliniella spp.) were associated with F. 

verticillioides, and exposure to flower thrips and F. verticillioides resulted in severe damage 

(Mailhot et al. 2007). Onion thrips can mechanically vector Stemphylium leaf blight 

(Stemphylium vesicarium) (Leach et al. 2020) and bacterial leaf blight (Pantoea agglomerans) 

(Grode et al. 2017; 2019) in onions (Allium cepa). In onions, onion thrips are critical to the 

proliferation of purple blotch (Alternaria porri) and prior thrips feeding damage renders the crop 

susceptible to infection (Bhangale and Joi 1983; McKenzie et al. 1993). 

Thrips interact with a variety of plant pathogens through vectoring, but plant pathogens 

also interact with thrips by modifying their behavior and fitness by affecting host plant 

preference and performance (Abe et al. 2012; Maris et al. 2014; Shrestha et al. 2012; Yarwood 

1943). Western flower thrips, for example, prefer and perform better on TSWV-infected plants 

when compared to healthy plants (Abe et al. 2012; Maris et al. 2004). In contrast, tobacco thrips, 

Frankliniella fusca (Hinds) preferred TSWV infected host plants, but larval performance was 

decreased on them (Shrestha et al. 2012). While obligate pathogens such as TSWV influence 

thrips preference and performance, facultative pathogens can also affect thrips. For example, 

onion thrips on grape leaves or roses infected with powdery mildew (Erysiphe polygoni) had 

increased survival compared to those on healthy plants (Yarwood 1943). Preference and 

20 

 
 
performance of thrips on infected plant tissues is dependent on the thrips species and the 

pathogen involved. Therefore, it is important to study the relationships between economically 

important thrips species and cooccurring plant pathogens. 

Onion thrips are a major insect pest of onions, they are often found in fields concurrently 

with fungal pathogens such as Colletotrichum coccodes (Wallr) Hughes, the causal agent of leaf 

and neck anthracnose (Gill et al. 2015; Rodriguez-Salamanca et al. 2012). In tomatoes, C. 

coccodes inoculum is spread by splash dispersal, which may come from rainfall or overhead 

irrigation (Sanogo et al. 1997). In onions, the most effective C. coccodes inoculation methods 

included the use of a conidial spray that targets the foliage, while soil drenches are not as 

effective as foliar sprays, indicating that C. coccodes infects onions primarily through the leaf 

tissue (Rodriguez-Salamanca et al. 2018). For lesions to develop on tomato fruit, C. coccodes 

requires 10 or more hours of continuous leaf wetness and temperatures between 25-31℃ (Dillard 

1989). On onions, C. coccodes causes dry, tan to salmon colored, oval lesions on the foliage, that 

turn dark as the pathogen sporulates (Rodriguez-Salamanca et al. 2012; Rodriguez-Salamanca et 

al. 2018). Onion plots infected with C. coccodes that are not treated with a fungicide had 

significantly lower yield when compared to those treated with a fungicide (Rodriguez-Salamanca 

2013). In addition to dissemination via splashing, disease can be increased through damage 

caused by onion thrips feeding (Dutta et al. 2014; McKenzie et al. 1993; Leach et al. 2020; 

Yarwood 1943; Bhangale and Joi 1983). 

Onion thrips feed through a punch and suck method, destroying the epidermal plant 

tissues (Chisholm and Lewis 1984). The loss of integrity of the plant host’s epidermis increases 

its vulnerability as pathogens may enter the plant through wounds (Gill et al. 2015; Childers and 

Achor 1995). Disease incidence and severity is positively correlated with onion thrips 

21 

 
 
 
populations and feeding damage, suggesting that onion thrips feeding contributes to pathogen 

infection (Grode et al. 2017; McKenzie et al. 1993; Yarwood 1943; Leach et al. 2020; Dutta et 

al. 2014). For some pathogens, such as Alternaria porri (Ellis), onion thrips feeding wounds 

provide entry points for the pathogen, facilitating infection (McKenzie et al. 1993). Other 

pathogens, such as Pantoea ananatis (Serrano) Mergaert may be spread through contaminated 

onion thrips feces deposited directly on feeding wounds (Dutta et al. 2014). While it is 

understood that onion thrips feeding promotes the infection of onion plants by some pathogens 

(Dutta et al. 2014; Grode et al. 2017; McKenzie et al. 1993), it is unclear how pathogen infection 

may mediate onion thrips behavior, such as host plant preference or performance. 

We examined the effects of varying host plant health status (control, artificially injured, 

artificially injured + symptomatic, and inoculated-symptomatic) on onion thrips preference in a 

laboratory setting using a four-choice test. The pathogen chosen for all experiments was C. 

coccodes, a relatively new pathogen in onions first found in Michigan in 2012, and more recently 

found in Ohio in 2014, and New York in 2016 (Rodriguez-Salamanca et al. 2012; Baysal-Gurel 

et al. 2014, Hay et al. 2016). After 13 days, the number of adult and larval onion thrips were 

recorded on each plant. To better understand the effect of C. coccodes on host plant selection, we 

examined the effects of varying host infection status (control, inoculated-asymptomatic, 

inoculated-symptomatic) on onion thrips preference in a two-choice test. In both the four-choice 

and two-choice tests, we assessed the correlation between the number of onion thrips per plant 

and estimated damage severity (%). In previous research, other thrips species preferred infected 

hosts but whether host preference was indicative of insect performance varied based on the thrips 

species (Abe et al. 2012; Maris et al. 2004; Shrestha et al. 2012). Therefore, to understand the 

implications of the four-choice and two-choice tests, a no-choice test was conducted, and the 

22 

 
 
 
number of onion thrips in the adult and larval life stage was recorded. We hypothesized that in 

the four-choice test, onion thrips would prefer inoculated-symptomatic plants, in the two-choice 

test, onion thrips would prefer inoculated-asymptomatic plants when compared to control or 

inoculated-symptomatic plants, and that preference would be indicative of performance. 

Materials and Methods 

Onion thrips colony 

Onion thrips collected from a commercial onion field (Grant, MI) managed with 

conventional pesticides and fertilizer were used to start a colony at Michigan State University 

(East Lansing, MI) in May 2021. The onion thrips colony was maintained in a mesh cage (50 

cm3; MegaView, Taichung, Taiwan), and kept at room temperature with ambient humidity and a 

16h:8h L:D cycle. Onion thrips were maintained on plants grown from certified organic onion 

seeds (A. cepa cv. ‘New York Early’; Johnny Seeds, Winslow, ME) and allowed to feed ad 

libitum. Three to four onions at the 5-7 leaf stage were added to the cage every week to provide 

fresh foliage for continuous rearing. The onion thrips colony was maintained for 8 weeks prior to 

the initiation of experiments. 

Colletotrichum coccodes inoculation 

Colletotrichum coccodes was isolated from a conventional onion field (Allegan County, 

MI) in August 2020. The isolate was maintained on 25% potato dextrose agar (PDA) media and 

morphologically identified based on key characteristics including sclerotia and conidia shape 

(Cano et al. 2004). Isolate identity was confirmed using the ribosomal internal transcribed spacer 

region in a nested PCR (Cullen et al. 2002). DNA was extracted using the DNeasy Total DNA 

Isolation Kit (Qiagen, Hilden, Germany) following the manufacturer’s protocols. A total volume 

of 25 µl PCR mixture contained PCR grade H20 (Ambion, Austin, TX), 10x PCR Buffer 

23 

 
 
(Invitrogen, Waltham, MA), 50 mM MgCl2 (Invitrogen), 10 mM dNTP (Promega, Madison, WI), 

10 µM of each primer (Invitrogen), 5 u/µl Taq polymerase (Invitrogen) and 6.44 µg/ml of the 

template DNA. The PCR reactions were conducted in a Mastercycler Pro thermocycler 

(Eppendorf, Hauppauge, NY) with the genus specific primers (Cc1F1/Cc2R1) conditions set to 

an initial denaturation at 95℃ for 2 minutes, followed by 35 cycles of denaturation at 95℃ for 

45 seconds, annealing for 61℃ for 1 minute and extension at 72℃ for 90 seconds, and a final 

elongation step at 72℃ for 5 minutes (Cullen et al. 2002). The product of the first PCR was used 

as template in the second PCR with species-specific primers (Cc1NF1/Cc2NR1). This had an 

initial denaturation at 95℃ for 2 minutes, followed by 35 cycles of denaturation at 95℃ for 45 

seconds, and annealing and extension at 72℃ for 135 seconds, with a final elongation at 72℃ 

for 5 minutes (Cullen et al. 2002). PCR products were then visualized on a 1% agarose gel to 

confirm identification. 

Prior to creating the inoculum, C. coccodes isolates were morphologically assessed for 

possible cross contamination by other pathogens (Cano et al. 2004). C. coccodes inoculum was 

grown on a full-strength PDA for 7 days after which the petri dish was flooded with double 

distilled water and the conidia removed by scraping a sterile tongue depressor across the top of 

the media. Onion plants were inoculated with a conidial suspension (2.5 x 105 conidia / ml) 

sprayed onto the foliage until it was fully wetted (i.e. dripping) (Rodriguez-Salamanca et al. 

2018). The spray applications were made using a 250 ml plastic hand spray bottle (Meijer Inc., 

Grand Rapids, MI). C. coccodes conidial sprays were made without abrasive agents because they 

do not increase disease progression for this disease (Rodriguez-Salamanca et al. 2018). 

Four-choice test 

Organic onion (cv. ‘New York Early’) seeds were planted in a 50-cell seedling starter 

24 

 
 
tray filled with perlite soil mix (Suremix Perlite, Michigan Grower Products Inc., Galesburg, MI) 

and kept in an environmental chamber (25℃, 50% RH, 16h:8h (L:D)). Plants were fertilized (2-

3-1 N-P-K, Ocean Crest Seafood’s Inc., Gloucester, MA) once a week at a rate of 74 ppm N and 

watered as needed. After 4 weeks, four onion seedlings at the 3-5 leaf stage were transplanted 10 

cm apart into a rectangular aluminum tray containing slits in the bottom for drainage that were 

filled with perlite soil mix (30 cm x 25 cm x 8 cm, Handi-Max®, Wheeling, IL). Seedlings were 

then returned to the environmental chamber for 1 week and watered every other day.  

A cylindrical plastic cage constructed out of transparency film (School Smart, Greenville, 

WI; 26 cm tall, 15 cm wide) was placed over all arenas and buried 2-3 cm into the soil (Figure 

1A-C). The top of the cage was covered with a nylon mesh material (160 µm, MegaView, 

Lehigh Acres, FL) that allowed ventilation and prevented onion thrips from moving out of the 

arenas. The aluminum trays were placed randomly within the environmental chamber under 

condition as described for onion planting. Each tray was watered to saturation every other day. 

Each of the four plants in a tray was randomly assigned one of four treatments: 1) control 

(sprayed with water until runoff), 2) artificially injured, 3) artificially injured + C. coccodes 

inoculated-symptomatic and, 4) C. coccodes inoculated-symptomatic (Figure 2.1A). Trays (N = 

34) were arranged randomly on the shelves in the environmental chamber. To ensure that C. 

coccodes inoculated plants presented symptoms at the time of exposure to onion thrips, they 

were inoculated 7 days prior to onion thrips exposure. Plants were inoculated in the aluminum 

trays. To prevent cross contamination of treatments, conidial sprays were applied from the top to 

individual onion plants surrounded by a narrow cylindrical-plastic tube made of transparency 

film (26 cm tall x 6 cm wide). Early inoculation resulted in the development of small tan lesions 

with a 1-9% disease severity rating (Figure S2.1). One day before onion thrips exposure, plants 

25 

 
 
assigned to the artificially injured or artificially injured + symptomatic treatments were pricked 

10 times in a vertical line with a size 1 insect pin (Hamilton Bell Co, Montvale, NJ) on each leaf 

to differentiate between mechanical and biological damage. Additionally, three trays that 

contained only control onions were used to assess if there was a directional bias within the 

environmental chamber that may influence onion thrips’ choice. 

Five randomly selected adult onion thrips from the colony were placed in a 1.7 ml 

microcentrifuge tube (Thomas Scientific, Swedesboro, NJ) with a 3 cm piece of fresh onion leaf 

for nourishment. The vials with onion thrips were kept in a cooler until they were released into 

the arenas. After all onion thrips were collected, one vial was randomly assigned to each arena, 

and opened, allowing onion thrips free movement within the arena. The number of onion thrips 

per plant and plant damage severity (%) were recorded 13 days after onion thrips exposure. 

26 

 
 
 
Onion thrips numbers were counted by destructively sampling each arena by removing the 

cylindrical cages and uprooting the onions to pull apart the leaves to check the neck for onion 

thrips. After removing the plant from the arena, we counted the number of larvae and adult onion 

thrips on each plant. Thirteen days after thrips exposure, all plants that received C. coccodes 

inoculum were exhibiting disease symptoms. Damage severity was visually rated on each plant 

from 0 to 100% by estimating the amount of green vs. necrotic tissue caused by both onion thrips 

feeding and C. coccodes. To account for inherent observer bias when taking visual assessments 

(James 1974), all plants within the arenas were assigned an identification number that was used 

for data collection and the observer did not know which treatment they were observing. 

Two-choice test 

Onions for the two-choice test were grown following the procedure described above for 

the four-choice test. After 4 weeks, two onions in the 3-5 leaf stage were transplanted 10 cm 

apart into rectangular aluminum trays and covered with transparent cylindrical plastic cages 

(Figure 2.1B). Aluminum trays were considered the experimental unit and were placed in a 

randomized design within an environmental chamber under the same conditions previously 

described. 

All onion seedlings were randomly assigned a treatment: 1) control, 2) C. coccodes 

inoculated-asymptomatic, and 3) C. coccodes inoculated-symptomatic. Seedlings were then 

placed in pairings so that each tray held one of the following combinations of seedlings: 1) 

control vs. inoculated-asymptomatic (n = 30), 2) control vs. inoculated-symptomatic (n = 30), or 

3) inoculated-asymptomatic vs. inoculated-symptomatic (n = 30). To check for directional bias 

within the environmental chamber, 23 aluminum trays contained a pairing of only control plants. 

A C. coccodes conidial suspension was applied to each inoculated plant as described above using 

27 

 
 
the same conidia concentration as above. Inoculated-symptomatic plants were inoculated 7 days 

before onion thrips exposure. Inoculated-asymptomatic plants were inoculated 3 days before 

onion thrips exposure. Inoculation timing was staggered so that plants would be at different 

stages of symptom progression when they were exposed to onion thrips. At the time of onion 

thrips exposure, inoculated-symptomatic seedlings had early disease symptoms of small tan 

lesions ranging from 1-7% symptom severity.  

Onion thrips were added to the experimental units following the same procedure used in 

the four-choice test. Onion thrips per plant and the percentage of damage severity (onion thrips 

feeding and C. coccodes symptoms) were recorded 13 days after the onion thrips were added as 

described in the four-choice methods.  

No-choice test 

Onions were grown following the same procedure as described in the four-choice test. 

After 4 weeks, individual plants were transplanted into plastic pots (8.5 cm deep, 10 cm wide; 

The HC Companies: ITML, Middlefield, OH) and maintained in the growth chamber under the 

same conditions as described above for one week. An experimental unit consisted of one potted 

onion plant surrounded by a cylindrical-plastic cage made from transparency film (26 cm tall x 6 

cm wide) with nylon mesh on top to allow airflow while preventing escape of the onion thrips 

(Figure 2.1C). Each experimental unit received one of the following treatments: 1) control, 2) C. 

coccodes inoculated-asymptomatic, and 3) C. coccodes inoculated-symptomatic onion plants. 

Experimental units were then placed in a randomized complete block design within the 

environmental chamber with 30 blocks. Inoculation methods and timing were the same as 

described in the two-choice test. Onion thrips were added following the same procedures as in 

the four-choice test. After 13 days, the arenas were destructively sampled as described in the 

28 

 
 
 
four-choice methods and onion thrips numbers and life stage were recorded for each plant.  

Data analysis   

To determine onion plant preference, Chi-square tests were performed on the total 

number of onion thrips per plant for the four- and two-choice tests. The observed number of 

onion thrips per plant was compared to the expected number of onion thrips per plant specified 

by the null hypothesis (i.e., the number of onion thrips per plant between treatments is the same) 

(Franke et al. 2012). For the four-choice test, significant Chi-square tests with Bonferroni 

adjustment for multiple comparison were used to determine significant differences between 

treatments (α = 0.01) (Sharpe 2015). To determine damage severity differences among 

treatments an analysis of variance (ANOVA) was performed for the four- and two-choice tests. 

R-squared values were used to determine if there was a correlation between onion thrips numbers 

and damage severity. For the no-choice experiment, to determine the effect of treatment (control, 

C. coccodes inoculated-asymptomatic, and C. coccodes inoculated-symptomatic) on onion thrips 

performance, the mean larval and adult onion thrips per plant were compared using an ANOVA 

with treatment as a fixed factor and block as random factor (Quinn and Keough 2002). The 

dependent variables met the assumptions of ANOVA. Tukey’s HSD test (α = 0.05) was used to 

determine the differences between treatment means. All data analyses were completed in R 

(RStudio Team 2021). 

Results 

Four-choice test 

Overall, there were significantly more onion thrips on artificially injured plants and 

inoculated-symptomatic plants when compared to control plants or artificially injured + 

symptomatic plants (χ2 = 101.23, df = 3, p-value < 0.001; Figure 2.2). Compared to control 

29 

 
 
 
plants, there were twice as many onion thrips on artificially injured + symptomatic plants (χ2 = 

25.04, df = 1, p-value < 0.001), approximately three times more onion thrips on artificially 

injured plants (χ2 = 64.51, df = 1, p-value < 0.001), and four times as many onion thrips on 

inoculated-symptomatic plants (χ2 =93.44, df = 1, p-value < 0.001). There were 50% more onion 

thrips on artificially injured plants compared to artificially injured + symptomatic plants (χ2 = 

10.82, df = 1, p-value < 0.001) and twice as many onion thrips on inoculated-symptomatic plants 

compared to artificially injured + symptomatic plants (χ2 = 26.04, df = 1, p-value < 0.001). There 

was no difference between the number of onion thrips on artificially injured plants compared to 

inoculated-symptomatic plants (χ2 = 3.44, df = 1, p-value = 0.064). 

30 

 
 
The damage severity (%) on each plant varied by plant treatment (F = 30.21, df = 3, 132, 

p-value < 0.001; Figure 2.3). There was a weak positive correlation between damage severity 

(%) and onion thrips numbers on control plants (R2 = 0.09, p-value = 0.028), on inoculated-

symptomatic plants (R2 < 0.01, p-value = 0.027) and on artificially injured plants (R2 = 0.31, p-

value < 0.001). There was no correlation between damage severity (%) and onion thrips numbers 

on artificially injured + symptomatic plants (R2 < 0.01, p-value = 0.091). 

31 

 
 
 
 
Two-choice test 

The number of onion thrips did not differ on inoculated-symptomatic and inoculated-

asymptomatic onions (χ2 = 2.61, df = 1, p-value = 0.106; Figure 2.4). When given a choice, there 

were 61% more onion thrips on inoculated-symptomatic onion compared to control plants (χ2 = 

30.72, df = 1, p-value < 0.001). There were approximately 66% more onion thrips on inoculated-

asymptomatic onions when compared to control onions (χ2 = 19.08, df = 1, p-value < 0.001). 

32 

 
 
 
The damage severity (%) on each plant varied by plant treatment (F = 55.80, df = 2, 181, 

p-value < 0.001; Figure 2.5). There was a positive correlation between the number of thrips and 

damage severity (%) on control plants (R2 = 0.22, p-value < 0.001). There was no correlation 

between onion thrips numbers and damage severity (%) on inoculated-asymptomatic plants (R2 

=0.18, p-value = 0.095), or inoculated-symptomatic plants (R2 < 0.01, p-value = 0.089). 

33 

 
 
 
 
No-choice test 

Across all life-stages, onion thrips had the greatest survival and reproduction on 

inoculated-symptomatic plants (F = 13.84; df = 2, 87, p-value < 0.001; Figure 2.6). Adult onion 

thrips survival rate was twice as high on inoculated-symptomatic plants (53%) than control 

plants (21%) (t-value = 3.02, df = 87, p-value =0.009). There was no difference in adult onion 

thrips survival rate when comparing control to inoculated-asymptomatic plants (t-value = 1.51, 

df = 87, p-value = 0.291) or inoculated-symptomatic to inoculated-asymptomatic plants (t-value 

34 

 
 
 
 
 
= 1.51, df = 87, p-value = 0.291). Inoculated-symptomatic onion plants had over twice as many 

larvae than control onion plants (t-value = 5.933, df = 87, p-value < 0.001) and 1.5 times more 

larvae than inoculated-asymptomatic plants (t-value = 3.567, df = 87, p-value = 0.006). There 

was no difference in the number of larvae on control and inoculated-asymptomatic plants (t-

value = 2.109, df = 87, p-value = 0.094). 

35 

 
 
 
 
Discussion 

Onion thrips are an economically devastating pest of onions, and along with plant 

pathogens, cause major crop losses (Gill et al. 2015). The relationship between onion thrips and 

plant pathogens, such as A. porri and P. ananatis, is well documented, with onion thrips feeding 

often leading to increased pathogen spread and severity (McKenzie et al. 1993; Dutta et al. 2014; 

Grode et al. 2017, 2019). However, the impact of facultatively vectored pathogens on onion 

thrips behavior and fitness has not been well described compared to obligately vectored 

pathogens. Onion thrips can distinguish between onion plants based on phenotypic and 

biological attributes (Basri and Ansari 2021; Mo et al. 2008; Pobozniak et al. 2021). Our results 

further demonstrate that onion thrips can distinguish between onion plants based on plant health 

and infection status and they perform best on inoculated-symptomatic plants. These results 

suggest that onion thrips do not randomly transfer and open plants for pathogens to enter, but 

they may accelerate plant damage by preferentially feeding on plants that are already stressed by 

pathogens and then spread the pathogen to healthy plants. 

In the four-choice test, onion thrips exhibited a strong preference for artificially injured 

onions and C. coccodes inoculated-symptomatic onions. Artificially injured + symptomatic 

onions were secondarily preferred, and control onions were the least preferred. The reasons for 

this may be due to changes in plant chemistry as many pathogens are known to induce defensive 

pathways that make plants more attractive to insects (Franco et al. 2017). Pathogens within the 

Colletotrichum genera are hemibiotrophic, and when infecting plant cells, they develop 

biotrophic hyphae that induce the salicylic acid pathway, but the hyphae become necrotrophic 

after successful colonization (Mendgen and Hahn 2002). Necrotrophic hyphae can trigger the 

jasmonic acid pathway (Boddy 2016) which is also induced by mechanical damage and onion 

36 

 
 
thrips feeding (Abe et al. 2008; Howe and Jander 2008). Onion thrips may prefer artificially 

injured onions and inoculated-symptomatic onions because they induce the same response in 

onions as thrips feeding, thus signaling that the plant is an appropriate host. Onion thrips may 

have not preferred artificially injured + symptomatic plants when compared to artificially injured 

and inoculated symptomatic plants because the combination of multiple stressors may have 

primed plant defense responses thus making the plant an inadequate host. In addition, the 

artificial injury may be preferred because the injury itself causes increased stress responses and 

allows the pathogen to enter the plant more quickly than without any injury to the plant. 

In the two-choice tests, onion thrips preferred C. coccodes inoculated host plants when 

compared to control plants but did not differentiate between inoculated-symptomatic and 

inoculated-asymptomatic hosts. This lack of difference may have been because by the end of the 

experiment all plants inoculated with C. coccodes exhibited signs of disease. Preference for 

infected hosts may be explained by both chemical and visual cues (Harris and Miller 1983; 

Visser 1988). While we did not measure changes in plant metabolites, all the inoculated plants 

looked visibly different than control plants towards the end of the experiments. However, there 

was no visible difference in damage severity between the inoculated-asymptomatic and 

inoculated-symptomatic plants (Figure S2.2). Plants inoculated with C. coccodes exhibited 

phenotypic changes like leaf necrosis, the development of tan lesions on leaves, had begun to 

sporulate and were visually different from the control plants (Supp. Figure S2.3). Changes in the 

plant phenotype may be important for host selection as some species of thrips orient based on 

visual cues (Teulon et al. 1999). For example, onion thrips prefer sticky traps that are blue or 

yellow, indicating that visual cues are important in pre-alighting behavior (Devi and Roy 2017). 

Thus, the change in leaf color in our study may have made the plant more attractive to onion 

37 

 
 
thrips. In the future, increasing the frequency of sampling experimental units throughout the 

duration of the experiment to estimate the effect of disease progression on insect preference will 

be important in understanding the impact of time on their interaction. 

In our four-choice test, there was a weak positive correlation between onion thrips 

numbers and damage severity (%) on control plants, artificially injured plants and inoculated-

symptomatic plants. Similarly, in the two-choice tests, there was a positive correlation between 

onion thrips numbers and damage severity (%) on control plants, but a weak correlation on 

inoculated-asymptomatic and inoculated-symptomatic plants. In both experiments, all plants that 

were inoculated with C. coccodes were exhibiting signs of leaf necrosis 13 days after onion 

thrips exposure. It is possible that the pathogen is driving damage severity symptoms on leaves, 

while masking thrips damage.  

The results from our no-choice experiment demonstrated that onion thrips survival and 

reproduction increased on inoculated-symptomatic plants. These results support the preference-

performance hypothesis which suggests that adult preference regarding oviposition, correspond 

with larval performance (Jaenike 1978). Larval thrips have low mobility compared to adults, thus 

host plant selection by the mother is critical to larval growth (Gill et al. 2015; Clark et al. 2011). 

It is unclear why onion thrips development increases on inoculated-symptomatic onions 

compared to the control onions, but it may be due to food quality. In general, thrips are 

polyphagous feeders, and some consume pollen and fungal spores (Ananthakrishnan and 

Dhileepan 1984). It is possible that the increased performance on inoculated-symptomatic plants 

may be due to onion thrips consuming the C. coccodes mycelium, which may have provided an 

alternative food source. Onion thrips have been reported potentially feeding on fungal material 

from plants infected with powdery mildew, while it was not confirmed whether fungal material 

38 

 
 
 
was ingested, onion thrips appeared to have destroyed established mildew colonies (Yarwood 

1943). In our experiments, onion thrips may be consuming C. coccodes conidia or mycelia, 

resulting in overall increased performance, but we do not have evidence that such feeding 

behavior occurs in this species. Onion thrips are often associated with fungal pathogens (Leach 

et al. 2020; McKenzie et al. 1993; Yarwood 1943; Fermaud and Gaunt 1995), and when fungal 

pathogens infect host plant tissue, changes in metabolic profiles occur (Medina-Melchor et al. 

2022). Future research that focuses on the relationship between onion thrips performance and 

facultatively vector pathogens, should investigate whether onion thrips are mycophagous and 

compare the metabolic profiles of healthy hosts to inoculated hosts. 

Epidemiological theory suggests that vector preference based on host infection status 

may have a direct impact on pathogen spread (Kingsolver 1987; Sisterson 2008). For example, 

once Rhopalosiphum padi Linnaeus (Hemiptera: Aphididae) acquire Barley yellow dwarf virus 

(BYDV), the infective aphid prefers to feed on healthy plants, promoting transmission (Ingwell 

et al. 2012). Another aphid, Myzus persicae Sulzer (Hemiptera: Aphididae), orient towards 

cucumber mosaic virus infected plants, but after feeding, disperse and prefer to feed on a non-

infected plant (Ziebell et al. 2011). In both cases, the insect vectors initially orient towards 

infected plants until they acquired the virus, and then exhibit a feeding preference for healthy 

plants, thus increasing the probability of disease transmission. Onion thrips are not obligate 

vectors of C. coccodes, yet they exhibit a preference for infected and injured hosts. Previous 

studies regarding onion thrips and facultative pathogens (Leach et al. 2020; Yarwood 1943; 

McKenzie 1993; Fermaud and Gaunt 1995; Grode et al. 2017; Dutta et al. 2014) indicated a 

close association between pests, thus further experiments investigating how onion thrips 

preference affects fungal pathogen spread in the field should be conducted. While we observed a 

39 

 
 
 
preference for and increased performance on C. coccodes inoculated plants, different fungal, 

bacterial, or viral pathogens may interact with onion thrips differently. Therefore, we cannot 

assume that results with one fungal pathogen are generally applicable, and research should 

continue to look at insect vectors and pathogens on species specific levels. 

In conclusion, a clear understanding of the relationship between host preference and 

disease dynamics may provide valuable insight into pest management for growers. When 

considered independently, both onion thrips feeding and foliar plant pathogens reduce the 

amount of photosynthetic tissue, resulting in lower onion yields, but in the field, it is difficult to 

differentiate between damage types as they occur simultaneously (Kendall and Capinera 1987; 

Fournier et al. 1995; Diaz-Montano et al. 2010; Rodriguez-Salamanca 2013; Gill et al. 2015). 

Therefore, to maximize onion yields, we need to develop a pest management strategy that 

considers the interactions between pests, rather than focusing on managing pests in isolation. 

Possible management strategies could include the disruption of host plant selection by the insect 

through either chemical or visual cues, therefore reducing how frequently the insect and the 

pathogen are in contact. Additionally, the development of new pest management thresholds 

which consider multiple pests simultaneously may also help increase crop yield. Understanding 

the interactions between multiple pests is key to optimizing integrated pest management 

strategies.  

Acknowledgements 

We collectively acknowledge that Michigan State University occupies the ancestral, 

traditional, and contemporary Lands of the Anishinaabeg – Three Fires Confederacy of Ojibwe, 

Odawa, and Potawatomi peoples. We recognize, support, and advocate for the sovereignty of 

Michigan’s twelve federally-recognized Indian nations, for historic Indigenous communities in 

40 

 
 
Michigan, for Indigenous individuals and communities who live here now, and for those who 

were forcibly removed from their Homelands. By offering this Land Acknowledgement, we 

affirm Indigenous sovereignty and will work to hold Michigan State University more 

accountable to the needs of American Indian and Indigenous peoples. This research was funded 

by the Organic Transitions Program Grant #2019-03518 from the USDA National Institute of 

Food and Agriculture. We would like to thank members of the MSU Vegetable Entomology lab 

for their feedback and support. 

41 

 
 
 
 
LITERATURE CITED 

Abe, H., J. Ohnishi, M. Narusaka, S. Seo, Y. Narusaka, S. Tsuda, and M. Kobayashi. 2008. 

Function of jasmonate in response and tolerance of Arabidopsis to thrip feeding. Plant Cell 
Physiol. 49: 68–80. 

Abe, H., Y. Tomitaka, T. Shimoda, S. Seo, T. Sakurai, S. Kugimiya, S. Tsuda, and M. 

Kobayashi. 2012. Antagonistic plant defense system regulated by phytohormones assists 
interactions among vector insect, thrips and a tospovirus. Plant Cell Physiol. 53: 204–212. 

Ananthakrishnan, T. N., and K. Dhileepan. 1984. Thrips-fungus association with special 
reference to the sporophagous Bactrothrips idolomorphus (Karny). (Tubulifera: 
Thysanoptera). Proc. Anim. Sci. 93: 243–249. 

Basri, R., and M. S. Ansari. 2021. Analytical study of phenotypic and biochemical attributes of 
onion cultivars in relation to infestation of onion thrips, Thrips tabaci. J. Asia. Pac. 
Entomol. 24: 529–535. 

Baysal-Gurel, F., N. Subedi, D. P. Mamiro, and S. A. Miller. 2014. First report of anthracnose of 

onion caused by Colletotrichum coccodes in Ohio. Plant Dis. 98: 1271–1271. 

Bhangale, G. T., and M. B. Joi. 1983. Role of thrips in the development of purple blotch of 

onion. J. Maharashtra Agric. Eniversities. 8: 299–300. 

Boddy, L. 2016. Pathogens of autotrophs, pp. 245–292. In S.C. Watkinson, L. Boddy and N.P. 

Money (eds.), The fungi 3rd edition. Academic Press, Cambridge, MA. 

Cano, J., J. Guarro, and J. Gené. 2004. Molecular and morphological identification of 

Colletotrichum species of clinical interest. J. Clin. Microbiol. 42: 2450–2454. 

Chisholm, I. F., and T. Lewis. 1984. A new look at thrips (Thysanoptera) mouthparts, their 
action and effects of feeding on plant tissue. Bull. Entomol. Res. 74: 663–675. 

Childers, C.C., D.S. Achor. 1995. Thrips feeding and oviposition injuries to economic plants, 

subsequent damage and host responses to infestation, pp. 31-51. In B.L. Parker, M. Skinner 
and T. Lewis (eds), Thrips biology and management. Springer, New York, NY. 

Clark, K. E., S. E. Hartley, and S. N. Johnson. 2011. Does mother know best? The preference-
performance hypothesis and parent-offspring conflict in aboveground-belowground 
herbivore life cycles. Ecol. Entomol. 36: 117–124. 

Cullen, D. W., A. K. Lees, I. K. Toth, and J. M. Duncan. 2002. Detection of Colletotrichum 

coccodes from soil and potato tubers by conventional and quantitative real-time PCR. Plant 
Pathol. 51: 281–292. 

Daugherty, M. P., A. Rashed, R. P. P. Almeida, and T. M. Perring. 2011. Vector preference for 

42 

 
 
hosts differing in infection status: Sharpshooter movement and Xylella fastidiosa 
transmission. Ecol. Entomol. 36: 654–662. 

Devi, M. S., and K. Roy. 2017. Comparable study on different coloured sticky traps for catching 
of onion thrips, Thrips tabaci Lindeman. J. Entomol. Zool. Stud. JEZS. 5: 669–671. 

Dillard, H. R. 1989. Effect of temperature, wetness duration, and inoculum density on infection 

and lesion development of Colletotrichum coccodes on tomato fruit. Phytopathology. 79 
(10): 1063-1066 

Diaz-Montano, J., M. Fuchs, B. A. Nault, and A. M. Shelton. 2010. Evaluation of onion cultivars 
for resistance to onion thrips (Thysanoptera: Thripidae) and Iris Yellow spot virus. J. Econ. 
Entomol. 103: 925–937. 

Diaz-Montano, J., M. Fuchs, B. A. Nault, J. Fail, and A. M. Shelton. 2011. Onion thrips 

(Thysanoptera: Thripidae): a global pest of increasing concern in onion. J. Econ. Entomol. 
104: 1–13. 

Dutta, B., A. K. Barman, R. Srinivasan, U. Avci, D. E. Ullman, D. B. Langston, and R. D. 

Gitaitis. 2014. Transmission of Pantoea ananatis and P. agglomerans, causal agents of 
center rot of onion (Allium cepa), by onion thrips (Thrips tabaci) through feces. 
Phytopathology. 104: 812–819. 

Eigenbrode, S. D., N. A. Bosque-Pérez, and T. S. Davis. 2018. Insect-borne plant pathogens and 
their vectors: ecology, evolution, and complex interactions. Annu. Rev. Entomol. 63: 169–
191. 

Farrar, J. J., and R. M. Davis. 1991. Relationships among ear morphology, western flower thrips, 

and Fusarium ear rot of corn. Phytopathology. 81 (6): 661-666. 

Fermaud, M., and R. E. Gaunt. 1995. Thrips obscuratus as a potential vector of Botrytis cinerea 

in kiwifruit. Mycol. Res. 99: 267–273. 

Fournier, F., G. Boivin, and R. K. Stewart. 1995. Effect of Thrips tabaci (Thysanoptera: 

Thripidae) on yellow onion yields and economic thresholds for its management. J. Econ. 
Entomol. 88: 1401–1407. 

Franco, P., D. S. Moura, and J. M. Vivanco and M. C. Silva-Filho. 2017. Plant-insect-pathogen 
interactions: a naturally complex ménage á trois. Curr. Opin. Microbiol. 7: 54–60. 

Franke, T. M., T. Ho, and C. A. Christie. 2012. The chi-square test: often used and more often 

misinterpreted. Am. J. Eval. 33: 448–458. 

Gill, H. K., H. Garg, A. K. Gill, J. L. Gillett-Kaufman, and B. A. Nault. 2015. Onion thrips 

(Thysanoptera: Thripidae) biology, ecology, and management in onion production systems. 
J. Integr. Pest Manag. 6: 1–9. 

43 

 
 
Gonella, E., R. Tedeschi, E. Crotti, and A. Alma. 2019. Multiple guests in a single host: 

interactions across symbiotic and phytopathogenic bacteria in phloem-feeding vectors – a 
review. Entomol. Exp. Appl. 167: 171–185. 

Grode, A., S. Chen, E. D. Walker, and Z. Szendrei. 2017. Onion thrips (Thysanoptera: 

Thripidae) feeding promotes infection by Pantoea ananatis in onion. J. Econ. Entomol. 
110: 2301–2307. 

Grode, A. S., E. Brisco-McCann, P. Wiriyajitsonboom, M. K. Hausbeck, and Z. Szendrei. 2019. 
Managing onion thrips can limit bacterial stalk and leaf necrosis in Michigan onion fields. 
Plant Dis. 103: 938–943. 

Harris, M. O., and J. R. Miller. 1983. Color stimuli and oviposition behavior of the onion fly, 

Delia antiqua (Meigen) (Diptera: Anthomyiidae). Ann. Entomol. Soc. Am. 76: 766–771. 

Hay, F. S., D. Strickland, E. Maloney, C. Hoepting, and S. J. Pethybridge. 2016. Anthracnose of 
onion caused by Colletotrichum coccodes in New York. Plant Dis. 100: 2171–2171. 

Howe, G. A., and G. Jander. 2008. Plant immunity to insect herbivores. Annu. Rev. Plant Biol. 

59: 41–66. 

Ingwell, L. L., S. D. Eigenbrode, and N. A. Bosque-Pérez. 2012. Plant viruses alter insect 

behavior to enhance their spread. Sci. Rep. 2: 1-6. 

Jaenike, J. 1978. On optimal oviposition behavior in phytophagous insects. Theor. Popul. Biol. 

14: 350–356. 

James, W. C. 1974. Assessment of plant diseases and losses. Annu. Rev. Phytopathol. 12: 27–48. 

Kendall, D. M., and J. L. Capinera. 1987. Susceptibility of onion growth dtages to onion thrips 

(Thysanoptera: Thripidae) damage and mechanical defoliation. Environ. Entomol. 16: 859–
863. 

Kingsolver, J.G., 1987. Mosquito host choice and the epidemiology of malaria. Am. Nat. 130 

(6): 811-827.  

Kritzman, A., M. Lampel, B. Raccah, and A. Gera. 2001. Distribution and transmission of Iris 

yellow spot virus. Plant Dis. 85: 838–842. 

Leach, A., F. Hay, R. Harding, K. C. Damann, and B. Nault. 2020. Relationship between onion 

thrips (Thrips tabaci) and Stemphylium vesicarium in the development of Stemphylium leaf 
blight in onion. Ann. Appl. Biol. 176: 55–64. 

Mailhot, D. J., J. J. Marois, and D. L. Wright. 2007. Influence of flower thrips on Fusarium 

hardlock severity. Plant Dis. 91: 1423–1429. 

44 

 
 
Maris, P. C., N. N. Joosten, R. W. Goldbach, and D. Peters. 2004. Tomato spotted wilt virus 

infection improves host suitability for its vector Frankliniella occidentalis. Phytopathology. 
94: 706–711. 

McKenzie, C. L., B. Cartwright, M. E. Miller, and J. V. Edelson. 1993. Injury to onions by 

Thrips tabaci (Thysanoptera: Thripidae) and its role in the development of purple blotch. 
Environ. Entomol. 22: 1266–1277. 

Mo, J., S. Munro, A. Boulton, and M. Stevens. 2008. Within-plant distribution of onion thrips 

(Thysanoptera: Thripidae) in onions. J. Econ. Entomol. 101: 1331–1336. 

Medina-Melchor, D. L., D. H. Zapata-Sarmiento, E. Becerra-Martínez, M. Rodríguez-Monroy, 
L. G. Z. Vallejo, and G. Sepúlveda-Jiménez. 2022. Changes in the metabolomic profiling 
of Allium cepa L. (onion) plants infected with Stemphylium vesicarium. Eur. J. Plant 
Pathol. 162: 557–573. 

Mendgen, K., and M. Hahn. 2002. Plant infection and the establishment of fungal biotrophy. 

Trends Plant Sci. 7: 352–356. 

Pobożniak, M., M. Olczyk, and T. Wójtowicz. 2021. Relationship between colonization by onion 
thrips (Thrips tabaci lind.) and leaf colour measures across eight onion cultivars (Allium 
cepa L.). Agronomy. 11. Article 963. 

Pozzer, L., I. C. Bezerra, R. Kormelink, M. Prins, D. Peters, R. O. De Resende, and A. C. De 
Ávila. 1999. Characterization of a tospovirus isolate of iris yellow spot virus associated 
with a disease in onion fields in Brazil. Plant Dis. 83: 345–350. 

Quinn, G. P., and M. J. Keough. 2002. Comparing groups or treatments- analysis of variance, pp. 
173–206. In Experimental design and data analysis for biologists. Cambridge University 
Press, Cambridge, ENG. 

Rodriguez-Salamanca, L. M., T. B. Enzenbacher, M. L. Derie, L. J. du Toit, C. Feng and M. K. 

Hausbeck. 2012. First report of Colletotrichum coccodes causing leaf and neck anthracnose 
on onions (Allium cepa) in Michigan and the United States. Plant Dis. 96: 769-769. 

Rodriguez-Salamanca, L. M. 2013. Characterization, virulence, epidemiology, and management 
of Colletotrichum spp. causing anthracnose in onion and celery (Doctoral dissertation). 

Rodriguez-Salamanca, L. M., R. P. Naegele, L. M. Quesada-Ocampo, and M. K. Hausbeck. 
2018. Inoculation method, temperature, and relative humidity affect leaf and neck 
anthracnose, a new onion disease in Michigan. Plant Heal. Prog. 19: 64–68. 

Sanogo, S., S. P. Pennypacker, R. E. Stevenson, and A. A. MacNab. 1997. Weather variables 
associated with infection of tomato fruit by Colletotrichum coccodes. Plant Dis. 81: 753–
756. 

45 

 
 
Sharpe, D. 2015. Your chi-square test is statistically significant: now what? Pract. Asses. Res. 

Eval. 20: 1–10. 

Shrestha, A., R. Srinivasan, D. G. Riley, and A. K. Culbreath. 2012. Direct and indirect effects of 
a thrips-transmitted tospovirus on the preference and fitness of its vector, Frankliniella 
fusca. Entomol. Exp. Appl. 145: 260–271. 

Simon, M., and M. Hilker. 2003. Herbivores and pathogens on willow: do they affect each other? 

Agric. For. Entomol. 5: 275–284. 

Sisterson, M. S. 2008. Effects of insect-vector preference for healthy or infected plants on 

pathogen spread: insights from a model. J. Econ. Entomol. 101: 1–8. 

Teulon, D. A. J., B. Hollister, R. C. Butler, and E. A. Cameron. 1999. Colour and odour 

responses of flying western flower thrips: wind tunnel and greenhouse experiments. 
Entomol. Exp. Appl. 93: 9–19. 

Tiberi, R., T. Panzavolta, M. Bracalini, A. Ragazzi, B. Ginetti, S. Moricca.2016. Interactions 

between insects and fungal pathogens of forest and ornamental trees. Ital. J. Mycol. 45: 54–
65. 

Visser, J. H. 1988. Host-plant finding by insects: orientation, sensory input and search patterns. 

J. Insect Physiol. 34: 259–268. 

Whitfield, A. E., D. E. Ullman, and T. L. German. 2005. Tospovirus-thrips interactions. Annu. 

Rev. Phytopathol. 43: 459–489. 

Wijkamp, I., N. Almarza, R. Goldbach, and D. Peters. 1995. Distinct levels of specificity in 

thrips transmission of tospoviruses. Phytopathol. 85: 1069-1074. 

Yarwood, C. E. 1943. Association of thrips with powdery mildews. Mycologia. 35: 189–191. 

Ziebell, H., A. M. Murphy, S. C. Groen, T. Tungadi, J. H. Westwood, M. G. Lewsey, M. Moulin, 
A. Kleczkowski, A. G. Smith, M. Stevens, G. Powell, and J. P. Carr. 2011. Cucumber 
mosaic virus and its 2b RNA silencing suppressor modify plant-aphid interactions in 
tobacco. Sci. Rep. 1: 1–7. 

46 

 
 
 
 
APPENDIX 1: CHAPTER 2 SUPPLEMENTARY MATERIALS 

Supplementary material 

47 

 
 
 
 
48 

 
 
 
 
 
 
49 

 
 
 
 
 
 
50 

 
 
 
 
 
CHAPTER 3: ENVIRONMENTAL CONDITIONS CAN INDIRECTLY AFFECT 
FACULTATIVE PATHOGEN SPREAD BY ALTERING INSECT VECTOR DISPERSAL 

Abstract 

Climate change impacts agriculture through shifts in regional environmental conditions, 

significantly altering insect vector and plant pathogen interactions. These pests often have a 

positive density dependent relationship, but for pathogens that do not rely on insect vectors, the 

relationship can be more difficult to predict. Furthermore, environmental conditions, such as 

temperature and relative humidity, can indirectly alter pathogen spread by impacting vector 

reproduction or behavior. Therefore, studies examining the interactions between pathogens and 

insect vectors under varying environmental conditions are critical to understanding pathogen 

spread. Onion thrips, Thrips tabaci Lindeman (Thysanoptera: Thripidae) are the main insect pest 

of onion (Allium cepa) and co-occur with many pathogens including Colletotrichum coccodes 

Wallr (Glomerellales: Glomerellaceae), a fungal pathogen of onion. We conducted experiments 

to understand how different densities of onion thrips and environmental conditions affect 

pathogen spread. To determine how onion thrips density affects pathogen spread, we released 0, 

5 or 25 onion thrips on C. coccodes inoculated plants, that were symptomatic for disease, and 

allowed them to move between the symptomatic and healthy plants. To determine the effects of 

environmental conditions on pathogen spread, we altered temperature and relative humidity and 

added either 0 or 5 onion thrips to the experiment. Onion thrips dispersal, damage distribution, 

and pathogen spread 13 d after onion thrips were released were assessed for each study. Our 

results indicate that C. coccodes was only disseminated in the presence of onion thrips and that 

onion thrips dispersed more at high population densities. Pathogen spread also increased at high 

temperatures, regardless of relative humidity. Overall, our study highlights how changes in insect 

abundance, which can be directly affected by environmental conditions, can alter pathogen 

51 

 
 
spread. 

Introduction 

Environmental conditions can have a significant influence on insect vector and plant 

pathogen interaction (Jones & Barbetti 2012; Peters et al. 2022). One impact of climate change 

on agriculture is a shift in regional environmental conditions that can alter pathogen-vector 

dynamics. However, studies that investigate these interactions in agricultural systems are 

lacking, particularly for facultative pathogens (Anderson et al. 2020; Peters et al. 2022; Jones & 

Barbetti 2012; Jones 2016). Depending on the pathosystem, climate change features like 

unpredictable changes in temperature and relative humidity, are expected to have a significant 

influence disease severity, which could have a direct impact or indirect impact on pathogen 

spread by altering vector traits, including abundance. 

An increase in insect vector abundance often leads to increases in disease severity and 

incidence through direct density dependent mechanisms (Grode et al. 2017, 2019; Leach et al. 

2020; Yarwood 1943). For obligate plant pathogens, the positive relationship between vector 

abundance and pathogen spread is predictable (Jeger 2020; Lowery et al. 2015; Shaw et al. 

2017). In the case of facultative pathogens that do not exclusively rely on insect vectors, this 

density dependent relationship between insects and pathogen spread is less predictable because 

the pathogen can be disseminated with or without the vector. For example, insect feeding 

wounds provide entry points for infection and insects can mechanically vector pathogens; in the 

absence of an insect vector, mechanical wounding by soil particles and spread via rain splash 

provide an alternative infection route (Tiberi et al. 2016; Eigenbrode et al. 2018). Thus, reducing 

insect vector numbers will reliably reduce disease severe and occurrence when pathogen spread 

is insect dependent. However, when pathogens do not rely on insect vectors, it is less clear how 

52 

 
 
much insects contribute to pathogen spread and disease severity. In agricultural studies, 

controlling insect vector populations through insecticides often leads to reduced pathogen spread 

and disease severity; this has been demonstrated for some fungal pathogens, highlighting the 

importance of understanding the strength of the relationship between vector and pathogen 

(Constancio et al. 2023; Leach et al. 2020; Grode et al. 2019; Mailhot et al. 2007). The addition 

of a fungicide along with the insecticide treatments often further reduces disease symptom 

severity and incidence without further reducing insect populations, suggesting that while insects 

contribute to pathogen spread, there are other factors contributing to increased disease 

occurrence and severity within these systems (Constancio et al. 2023; Mailhot et al. 2007). While 

insect population dynamics are important for determining plant pathogen dynamics, the role of 

factors that impact insects and their relationship with the pathogen needs further investigation. 

As ectotherms, insect development is dependent on ambient temperature, with warmer 

temperatures leading to positive changes in growth, developmental rates, increased plant material 

consumption, and reduced time between generations (Cornelissen 2011; Jamieson et al. 2012; 

Lemoine et al. 2013). Consequently, in agroecosystems, higher temperatures may indirectly lead 

to pathogen spread via increases in insect vector abundance. Moreover, temperature and 

humidity often increase concurrently, with high relative humidity often creating conditions that 

may favor high disease severity (Velásquez et al. 2018; Singh et al. 2023). For some fungal 

pathogens, moisture is necessary for conidial release from the acervulus, and splashing rain can 

spread conidia to nearby susceptible plants (Dillard 1989). Additionally, high relative humidity is 

important for increased fecundity and pupation success of some insects (Steiner et al. 2011; 

Garrick et al. 2016). Therefore, increased relative humidity may have an indirect effect on 

pathogen spread by altering the vector reproduction. Overall, the importance of relative humidity 

53 

 
 
and temperature in the case of plant pathogens, like foliar fungal pathogens, is not well 

understood and studies examining its indirect impact on pathogen spread are lacking. 

The fungal pathogen, Colletotrichum coccodes, is a pathogen of potatoes and tomatoes, 

and more recently has been found in onions (Allium cepa) (Rodriguez-Salamanca et al. 2012). It 

was first identified in Michigan onion fields in 2012, since then it has continued to occur and was 

later identified in Ohio and New York (Rodriguez-Salamanca et al. 2012; Baysal-Gurel et al. 

2014; Hay et al. 2016). Colletotrichum coccodes is spread through water-splash, which can occur 

during rain events or overhead irrigation, both events leading to increases in disease severity 

(Dillard 1989). Onion thrips, Thrips tabaci (Thysanoptera: Thripidae), are the main insect pests 

of onions, and vector many different plant pathogens (Yarwood 1943; Bhangale & Joi 1983; 

Ulman et al. 1997; Dutta et al. 2014; Eigenbrode et al. 2018). While onion thrips and C. 

coccodes may be found concurrently in onion fields, it is unclear how onion thrips contribute to 

the spread of C. coccodes and the impact of environmental conditions. 

We determined the effects of onion thrips populations and environmental conditions on 

disease dynamics using laboratory-based experiments by first manipulating initial onion thrips 

densities and then altering temperature, and relative humidity. To better understand the density 

dependent relationship between onion thrips and C. coccodes transmission, we placed 0, 5 or 25 

adult onion thrips in experimental units consisting of one C. coccodes inoculated onion and three 

non-inoculated onions. We hypothesized that more onion plants would become infected by C. 

coccodes at higher onion thrips intial densities due to increased mechanical vectoring of C. 

coccodes conidia. To address how a change in environmental conditions affects onion thrips 

behavior and pathogen spread, we used a similar experimental design and released 0 or 5 adult 

onion thrips on one C. coccodes inoculated onion and two non-inoculated onions, while 

54 

 
 
manipulating temperature and relative humidity. We hypothesized that increased temperature 

and high relative humidity would lead to increased pathogen transmission among the non-

inoculated plants. 

Methods and materials 

Onion thrips colony 

Onion thrips from a commercial, conventionally managed onion field (Allegan, MI) were 

collected and used to start a colony at Michigan State University (East Lansing, MI) in August 

2022. The colony was maintained in a mesh cage (50 cm3; MegaView, Taichung, Taiwan), and 

kept at 22℃ and a 16:8 hr L:D cycle. Onion thrips were allowed to feed ad libitum on onion 

grown from certified organic onion seeds (A. cepa cv. ‘New York Early’; Johnny Seeds, 

Winslow, ME). Each week, ten onions at the 5-7 leaf stage were added to the cage to provide 

fresh foliage for continuous rearing. The onion thrips colony was maintained in these conditions 

prior to the experiment initiation. 

Colletotrichum coccodes inoculation 

Colletotrichum coccodes was isolated from plants grown in the same field (Allegan, MI) 

in August 2020. Prior to the experiments, the isolate was maintained on 25% strength potato 

dextrose agar (PDA) media. The isolate was first identified morphologically based on sclerotia 

and conidial shape (Cano et al. 2004) and confirmed using the ribosomal internal transcribed 

spacer region in a nested PCR (Cullen et al. 2002). The culture plates were visually assessed for 

cross contamination by other pathogens (Cano et al. 2004). Isolates were grown on full-strength 

PDA for 7 d prior to inoculation. The Petri dish was flooded with double distilled water and 

conidia were dislodged from the media by scraping a sterile tongue depressor across the top. The 

onion seedlings were then inoculated with the suspension (2.5 x 105 conidia/ml) 7 d prior to 

55 

 
 
onion thrips exposure. The conidial suspension was sprayed onto the onion foliage until run off 

(Rodriguez-Salamanca et al. 2018). All applications were made with a 250 ml plastic hand spray 

bottle (Meijer Inc., Grand Rapids, MI). 

Experiment 1: Effect of onion thrips initial density on pathogen spread 

Organic onion seeds (cv. ‘New York Early’) were planted in a 50-cell seedling tray and 

fertilized (125 ppm, 20-20-20 N-P-K, Jack’s General Purpose Water-Soluble Fertilizer; JR 

Peters, Inc., Allentown, PA) once a week. The seedlings were grown for 4 wk, until the 3-leaf 

stage. Four seedlings were transplanted into aluminum trays (30 x 25 x 8 cm, Handi-Max, 

Wheeling, IL) approximately 10 cm apart in a straight line, arranged so that the foliage was not 

touching, and assigned a location from 1 to 4 (1 = first seedling in the line; 4 = last seedling) 

(Figure 3.1). After transplanting to aluminum trays, seedlings were allowed to grow for an 

additional 14 d, until the 5-leaf stage, prior to onion thrips exposure to ensure survival. 

56 

 
 
A large cylindrical plastic cage made from transparency film (School Smart, Greenville, 

WI; 26 cm tall, 15 cm radius) was placed over each tray so that onion thrips could move freely 

among plants within a tray but not between trays. To prevent onion thrips movement between the 

aluminum trays but still allow air movement, the top of the cage was covered with a nylon mesh 

(160 µm, MegaView, Lehigh Acres, FL). Each tray was assigned to one of four treatment 

combinations: 1) mock inoculated + 5 onion thrips (N = 20), 2) mock inoculated + 25 onion 

thrips (N = 20), 3) inoculated + 5 onion thrips (N = 20), 4) inoculated + 25 onion thrips (N = 20), 

5) mock inoculated + 0 onion thrips (N = 10) and, 6) inoculated + 0 onion thrips (N = 10) (Table 

3.1). Aluminum trays were placed in a randomized unbalanced block design in the 

environmental chamber with a reduced number of control treatments (treatments 5 and 6 in Table 

57 

 
 
 
 
3.1, N = 10) and watered every 3 d. The 5-onion thrips initial density corresponds to the action 

threshold (one onion thrips/leaf) for most insecticides used for onion thrips management (Rueda 

et al. 2007; Nault & Shelton 2010; Atia et al. 2021). For treatments that included inoculated 

plants (treatments 3 and 4), 7 d before onion thrips exposure, onion plants in location 1 were 

inoculated with C. coccodes, and visually assessed disease symptomatic when exposed to onion 

thrips. To prevent pathogen exposure to the remaining three plants within the tray, the onion 

plant was isolated within a cylindrical plastic tube (30 cm tall, 3 cm radius) with an open top, and 

the inoculum was applied to the onion foliage through the top of the tube. The mock-inoculated 

plants were sprayed with double distilled water until the foliage was fully wetted. 

58 

 
 
 
 
Table 3.1: List of treatments in each onion thrips experiment. The temperature column is the 
temperature of the growth chamber the experiment took place in, RH is the relative humidity 
within the experimental arenas, inoculation status is whether the plant in location 1 was 
inoculated with C. coccodes and the onion thrips added column is the number of onion thrips 
added at the start of the experiment. N represents the total number of replicates for each 
treatment. 

Onion 
thrips 
added 
5 
25 
5 
25 
0 
0 
5 
5 
5 
5 
0 
5 
0 
5 
0 
5 
0 
5 

N 

20 
20 
20 
20 
10 
10 
20 
20 
20 
20 
5 
5 
5 
5 
5 
5 
5 
5 

Experiment 

Treatment 
number 

Temperature 
(℃) 

RH 

Inoculation 
status 

Inoculated 
Inoculated 

NA  Mock 
NA  Mock 
NA 
NA 
NA  Mock 
NA 
Low 
High 
Low 
High 
Low 
Low  Mock 
High 
High  Mock 
Low 
Low  Mock 
High 
High  Mock 

Inoculated 
Inoculated 
Inoculated 
Inoculated 
Inoculated 
Inoculated 

Inoculated 

Inoculated 

Inoculated 

Effect of onion 
thrips initial 
density on 
pathogen spread 

Effects of 
environmental 
conditions on 
pathogen spread 

1 
2 
3 
4 
5 
6 
1 
2 
3 
4 
5 
6 
7 
8 
9 
10 
11 
12 

25 
25 
25 
25 
25 
25 
22 
22 
33 
33 
22 
22 
22 
22 
33 
33 
33 
33 

59 

 
 
 
 
Five or 25 adult onion thrips were randomly selected from the colony and placed in a 1.7 

ml microcentrifuge tube (Thomas Scientific, Swedesboro, NJ) with a fresh piece of onion foliage 

(3 cm) for nourishment. The onion thrips vials were kept in a cooler for a maximum of 1 h prior 

to being released into the aluminum trays. Vials with onion thrips were randomly assigned to 

treatments, empty vials were placed in treatments without onion thrips. All vials, regardless of 

treatment, were placed at the base of plants in location 1, and opened, allowing onion thrips free 

movement. Adult and larval onion thrips per plant and estimated damage severity (i.e. amount of 

tissue damage per plant, rated 0-100%) was recorded 13 d after onion thrips exposure. To count 

the number of adult and larval onion thrips per plant, the cages were removed, the onions were 

uprooted, and the foliage was pulled apart to check the neck of the plant for onion thrips. 

Damage severity was visually estimated on a scale of 0-100% by estimating the amount of 

necrotic tissue on the plant caused by onion thrips feeding and pathogen damage. 

To determine whether onion thrips had spread C. coccodes from the inoculated onions to 

the non-inoculated onions, experimental units were randomly selected for pathogen testing 

(N=5). A small portion of damaged onion foliage (3 cm) was removed from the onion and 

surface sterilized by placing in a 10% bleach solution for 20 s and then placed in double distilled 

water for 20 s to rinse the bleach. Each onion sample was surface sterilized twice to ensure that 

only pathogens within the onion tissue were being sampled. After surface sterilizing, onion tissue 

was placed on 25% strength PDA Petri dish and any fungal growth that occurred was isolated 

and placed on a fresh Petri dish to create pure cultures. Pure cultures were then assessed for the 

target pathogen by visually comparing the culture morphology to a known C. coccodes isolate to 

confirm pathogen identity. The presence or absence of C. coccodes was then recorded for each 

plant that was sampled. 

60 

 
 
 
 
Experiment 2: Effects of environmental conditions on pathogen spread 

Onion plants were grown from seed as previously described. Three seedlings were 

transplanted in the same aluminum trays as described above and assigned location numbers 1-3. 

After transplanting to the trays, the seedlings were grown for 14 d prior to onion thrips exposure 

and covered with cylindrical plastic cages. The trays were placed in a randomized unbalanced 

block design with treatments 1-4 replicated 20 times and treatments 5-12 replicated five times 

(Table 3.1). 

Temperature and relative humidity (RH) were modified using two environmental 

chambers set to either a high (33℃) or low temperature (22℃). To mimic fluctuating 

temperatures throughout the day, each growth chamber was set to the following schedule: 0801-

2000 hr hold at 33 or 22℃, 2001hr – 2200 hr decrease to 23 or 12℃, 2201-0600 hold at 23 or 

12℃, 0601-0800 increase to 33 or 22℃. Relative humidity was increased by covering the top of 

the cage with a plastic film to retain high moisture levels. Relative humidity was monitored by 

placing a hygrometer (AikTryee; Shenzhen Youkeshu Technology, Shenzhen, China) within the 

cages and recording the value every 48 hr. The high relative humidity treatments fluctuated 

between 80-95%, and the low relative humidity treatments fluctuated between 30-50%, 

regardless of temperature. 

There were 12 treatments which varied in temperature, relative humidity, inoculation 

status and onion thrips presence or absence (Table 3.1). The following treatments were included: 

1) low temperature + low RH, 2) low temperature + high RH, 3) high temperature + low RH, and 

4) high temperature + high RH. Each treatment had 0 or 5 thrips. Treatments without onion 

thrips served as a control. Plants in location 1 were inoculated or mock inoculated as previously 

described. Including inoculated and mock inoculated controls allowed the differentiation of plant 

61 

 
 
 
 
damage due to onion thrips feeding or the pathogen. Any damage observed on mock inoculated 

plants was attributed to onion thrips feeding. 

Thirteen d after onion thrips exposure, adult and larval onion thrips numbers and the 

estimated damage (%) per plant were recorded following the same procedure as above. 

Additionally, C. coccodes presence or absence was recorded for all plants from each treatment 

by collecting the plants and following the same protocol as described above to identify the 

pathogen in culture.  

Data Analysis 

To determine how varying onion thrips density or environmental conditions affect onion 

thrips movement and estimated plant damage among plants, we used Generalized Linear Mixed 

Models (GLMMs). All models were created in R (R Core Team 2023) using the glmmTMB 

package (Brooks et al. 2017), and the ‘drop1’ function for evaluating significant main and 

interactive fixed effects. For models with significant interactive effects (α = 0.05), the ‘lstrends’ 

function (Lenth et al. 2024) was used to determine if there were significant differences between 

treatments by comparing the slopes of the lines. Slopes closer to 0 indicate that the distribution 

of the dependent variable is more evenly distributed among plants. 

Effect of onion thrips initial density on pathogen spread 

Thrips dispersal — We first tested whether onion thrips distribution is different between 

life stages by creating two models, with either adult or larval onion thrips per leaf as the 

dependent variable. We then compared models with the onion thrips initial density (0, 5 or 25 

adult onion thrips) and inoculation status interacting with plant location as the fixed effects to 

determine whether initial density changed thrips distribution among the four plants. Additionally, 

including a variable representing inoculation status interacting with plant location allowed us to 

62 

 
 
 
determine if pathogen presence or absence altered onion thrips distribution among the four 

plants. Finally, we included a fixed effect that was an interaction between inoculation status and 

initial onion thrips density to determine whether pathogen presence or absence affected onion 

thrips distribution at varying onion thrips numbers. For all models, block was used as a random 

effect, and a negative binomial distribution was used. 

Pathogen spread and plant damage — A Chi-square test was performed to determine if 

there were differences in the total number of plants positive for C. coccodes at varying onion 

thrips densities. The total number of plants positive for C. coccodes was compared to the 

expected number of plants positive (the total amount of plants positive for C. coccodes was the 

same between treatments). 

To assess how varying onion thrips initial density impacted the plant damage, we built a 

model that compared how the damage per plant varied by plant location interacting with onion 

thrips initial densities or inoculation status, as well as an interaction between onion thrips initial 

density and inoculation status. For the model, block was the random effect, and we used a beta 

distribution. 

Effects of environmental conditions on pathogen spread 

To understand how varying environmental conditions affected onion thrips distribution, 

we evaluated models with adult or larval onion thrips per leaf as the dependent factor and plant 

location interacting with temperature or relative humidity as the independent factors. 

Additionally, we included inoculation status (inoculated or mock inoculated) as a fixed factor, 

interacting with plant location to assess whether C. coccodes presence or absence significantly 

affected the dispersal of adult or larval onion thrips. For both models, block was used as the 

random factor, and we used a negative binomial distribution. 

63 

 
 
 
To assess whether varying environmental conditions impact the damage distribution 

among plants within experimental arenas, we evaluated models with estimated damage as the 

dependent factor and plant location interacting with temperature or relative humidity as the 

independent variables. We also included inoculation status interacting with plant location to 

determine if C. coccodes presence or absence affected the damage distribution among the three 

plants. Finally, we assessed whether onion thrips presence or absence affected damage 

distribution by comparing models with or without onion thrips interacting with plant location. 

For all models, block was used as the random factor, and we used a beta distribution. 

A Chi-square test was performed to determine if there were differences in the total 

number of C. coccodes positive plants at varying temperatures and relative humidity. The total 

number of C. coccodes positive plants was compared to the expected number of plants positive. 

For each Chi-square, the first plant (i.e., the inoculated plant) was removed from the analysis 

because that plant was experimentally inoculated with C. coccodes and positive for C. coccodes.  

Results 

Effect of onion thrips initial density on pathogen spread 

Increasing onion thrips initial density significantly changed the dispersal patterns of 

onion thrips among the four plants (Table 3.2, Models 1, 2). In treatments where 5 adult onion 

thrips were released on the first plant (i.e. low onion thrips initial density), the adult onion thrips 

dispersed evenly across all plants (slope = 0.02), while in treatments with 25 onion thrips 

released, adult onion thrips moved away from the release plant and colonized plants in locations 

2, 3, and 4 (slope = 0.32) at a three times higher rate comparatively (Figure 3.2A; t-value = -

1.978, df = 80, p-value = 0.048). Interestingly, the opposite patterns were observed for the larval 

onion thrips. In low onion thrips initial density treatments, larval onion thrips were distributed 

64 

 
 
 
primarily on plants in the first location, and the larval populations were reduced by as much as 

60% on the fourth plant (slope = -0.40). In contrast, in the high onion thrips initial density 

treatments, larval onion thrips were relatively evenly distributed among all four plants (Figure 

3.2B; slope = -0.05; t-value = -3.897, df =80, p-value < 0.001). Inoculation status did not 

significantly affect onion thrips dispersal among plants within the trays, and the interaction 

between inoculation status and onion thrips initial density was not significant (Table 3.2, Models 

1,2). 

65 

 
 
 
There were significant differences in the distribution of plant damage among the four 

plants within the experimental arenas based on onion thrips initial density (Table 3.2, Model 3). 

Treatments that received no onion thrips (pathogen only) had the most damage on the first plant 

and no damage on the remaining plants (slope = -0.24). Treatments with five onion thrips had 

about 50% damage reduction between the first and second plants, and almost a 65% reduction in 

damage on third and fourth plants when compared to the plant in the first location (slope = -

0.88). The damage distribution of the treatment without onion thrips was 72% more evenly 

distributed compared to the damage distribution of the five onion thrips treatment, indicating a 

more even damage distribution among plants in the treatment without thrips (Figure 3.3A; t-

value = 6.153, df = 60, p-value < 0.001). Similarly, the same pattern was observed in the high 

onion thrips density compared to the no onion thrips treatments, with damage more evenly 

distributed among plants in treatments without thrips (t-value = 4.057, df = 60, p-value < 0.001). 

Damage was about 33% more evenly spread among all four plants at the 25 onion thrips initial 

density (slope = -0.66) compared to plants in the 5 onion thrips treatments (t-value = -2.545, df = 

80, p-value = 0.030). 

66 

 
 
 
67 

 
 
 
 
 
Table 3.2: The models considered in the analysis of varying onion thrips initial density in the first experiment. Fixed effects included: 
1) location: location of plant within the aluminum tray, 2) inoculation: inoculation status with/without C. coccodes, and 3) initial 
density: initial number of onion thrips added. The full model was compared with the model resulting from the single term deletion (i.e. 
removal of the specific interactive effect). The AIC (Akaike information criterion), Chi square, and P value (α = 0.05) were used to 
determine significant interactions. 

Model # 

Full model 

1 

2 

3 

Adult thrips ~ location*inoculation + 
location*density+ inoculation*density + (1|block) 

Larval thrips ~ location*inoculation + 
location*density + inoculation* density + (1|block) 

Damage ~ location*inoculation + location*density 
+ inoculation*density + (1|block) 

Fixed effects single term 
deletion 

AIC 

Chi square 

P value 

Location*inoculation 
Location*density 
Inoculation* density 
Location*inoculation 
Location*density 
Inoculation*density 
Location*inoculation 
Location* density 
Inoculation* density 

827 
831 
827 
1850 
1863 
1850 
-2801 
-2766 
-2800 

0.12 
3.89 
0.00 
2.29 
14.73 
1.78 
0.06 
37.06 
2.52 

0.72 
0.04 
0.98 
0.13 
< 0.01 
0.18 
0.80 
< 0.01 
0.28 

68 

 
 
 
 
 
There were approximately three times more plants positive for C. coccodes in the high 

initial density treatments compared to the low density treatments (Figure 3.3B; χ2 = 5.2, df = 2, 

p-value = 0.07). In all treatments, 100% of the inoculated plants tested positive for C. coccodes, 

indicating a successful inoculation. When onion thrips were absent, none of the plants were 

positive for C. coccodes. When 5 onion thrips were added, 4% of the plants were positive for C. 

coccodes compared to the 14% of plants that were positive when 25 onion thrips were added.  

Effects of environmental conditions on pathogen spread 

Relative humidity and inoculation status were not significant factors in adult or larval 

onion thrips distribution among the three plants (Table 3.3, Model 1). Temperature significantly 

affected adult onion thrips distribution (Table 3.3, Model 1; t-value = 4.032, df = 120, p-value < 

0.001). At the high temperature, there were similar numbers of adult onion thrips on location 1 

plants when compared to location 2 plants, and about 30% less onion thrips on plants in location 

3 compared to locations 1 and 2 (Figure 4A; slope = -0.08). At the lower temperature, adult 

onion thrips remained primarily on plants in location 1 and a few dispersed to the plants in 

locations 2 or 3 (Figure 3.4A; slope = -0.75). Temperature also had a significant impact on larval 

onion thrips distribution among the three plant locations (t-value = 7.493, df = 120, p-value < 

0.001). At high temperatures, larval onion thrips were dispersed evenly across all plant locations 

(Figure 4B; slope = -0.09). At low temperatures, larval onion thrips were found primarily on 

location 1 plants, with an 80% reduction in the number of larval onion thrips on location 2 plants 

compared to location 1, and a 90% reduction on location 3 plants compared to location 1 (Figure 

3.4B; slope = -1.33). 

69 

 
 
Relative humidity and inoculation status did not significantly affect damage distribution 

among the three plants (Table 3.3, Model 3). Additionally, temperature did not significantly 

affect the distribution of damage among the three plants (Table 3.3; Figure 3.5A). However, 

onion plants in the high temperature treatments had an increased incidence of C. coccodes 

positive plants when compared to plants in the low temperature treatments (Figure 3.5B; χ2 = 

4.76, df = 1, p-value = 0.03). In all temperature treatments, 100% of plants in the first location 

(i.e., the experimentally inoculated plant) were C. coccodes positive. In the high temperature 

treatments, 56% of subsequent plants were C. coccodes positive compared to 37% of plants in 

70 

 
 
 
 
the low temperature treatments. There was no difference in the number of C. coccodes positive 

plants at differing humidity levels (χ2 = 0.44, df = 1, p-value = 0.51). 

71 

 
 
 
 
 
Table 3.3: The models considered for testing the effect of varying environmental conditions on onion thrips dispersal. Fixed effect 
included: 1) location, location of plant within aluminum tray, 2) inoculation: inoculation status with/without C. coccodes, 3) relative 
humidity (RH), and 4) temperature. The full model was compared with the model resulting from the single term deletion (i.e. removal 
of the specific interactive effect). The AIC (Akaike information criterion), Chi square, and P value (α = 0.05) were used to determine 
significant interactions. 

Model # 

Full model 

Fixed effects single term 
deletions 

AIC 

Chi Square 

P value 

1 

2 

3 

Adult thrips ~ location*RH + location*temperature 
+ location*inoculation + (1|block) 

Larval thrips ~ location*RH + location*temperature 
+ location*inoculation + (1|block) 

Damage ~ location*RH + location*temperature + 
location*inoculation + location*population + 
(1|block) 

Location*RH 
Location*temperature 
Location*inoculation 
Location*RH 
Location*temperature 
Location*inoculation 
Location*RH 
Location*temperature 
Location*inoculation 
Location*population 

1342 
1360 
1343 
1799 
1855 
1799 
-708 
-709 
-709 
-702 

0.23 
18.37 
0.81 
0.20 
56.20 
0.30 
1.49 
0.04 
0.15 
7.50 

0.63 
< 0.01 
0.37 
0.65 
< 0.01 
0.58 
0.22 
0.84 
0.70 
<0.01 

72 

 
 
Onion thrips presence or absence (C. coccodes only) significantly affected the damage 

distribution among the three plants within the experimental arenas (Figure 3.6; t-value = 2.762, 

df = 120, p-value = 0.006). When onion thrips were present, damage was distributed across all 

three plants, with the most damage present in the first location with a ~60% and 75% reduction 

in the amount of damage on the second and third plants, respectively, compared to the first (slope 

= -0.89). In treatments that did not receive onion thrips (C. coccodes only), damage was isolated 

on plants in location 1, and no subsequent plants were damaged (slope = -0.39). 

Discussion 

Our results demonstrated that the foliar pathogen C. coccodes can be spread by onion 

thrips and could be indirectly modified by a high temperature, potentially via an increase in the 

73 

 
 
 
vector population, which may be injuring the plant tissue or mechanically vectoring conidia. 

Plants at high temperatures had increased disease incidence (i.e., number of plants positive for C. 

coccodes) and more onion thrips at the end of the experiment than plants at low temperatures. 

Relative humidity did not affect pathogen spread in our experiment. 

Increasing the initial density of onion thrips altered adult and larval distribution patterns. 

Adults are more mobile than larval onion thrips and in our experiments, adults moved more 

among plants than immatures, especially when their initial densities were high (Gill et al. 2015). 

In treatments with high onion thrips initial densities, 9% of adult onion thrips were found on the 

first plant, compared to 25% of adults in the low initial density treatment. Western flower thrips 

(Frankliniella occidentalis) density similarly influences dispersal rate, and subsequent pathogen 

dispersal (Shaw et al. 2017; Rhainds & Messing 2005). Larval onion thrips distribution was 

likely reflective of adult onion thrips dispersal; in high density treatments, larval thrips were 

distributed relatively evenly across all plants, while they were primarily on the first plant in the 

low-density treatments. Larval onion thrips are the most damaging life stage and may be good 

predictors of where disease is likely to develop due to increased feeding damage (Coudriet et al. 

1979; Leach et al. 2017). It’s likely that at high densities, the increase in pathogen spread is due 

to higher larval populations on the healthy plants increasing the entry points for the pathogen, 

and increased adult dispersal to the healthy plants increasing mechanical vectoring rate. 

Previously, we found that onion thrips adults prefer C. coccodes inoculated onions over non-

inoculated onions, but the high initial density may trigger dispersal away from the inoculated 

onion (Rhainds & Messing 2005; Constancio et al. 2022). Vector dispersal from an infected to a 

healthy plant has been documented to increase disease incidence in other systems as well 

(Daugherty et al. 2011; Ingwell et al. 2012). 

74 

 
 
 
In our bioassays, C. coccodes spread exclusively in the presence of onion thrips, and 

although a statistical difference was not detected, pathogen spread was reduced with lower onion 

thrips populations. In field-based studies, insecticide applications reduced necrotic tissue in 

onions, but it was unclear if this was due to reduced pathogen spread or feeding damage because 

of the difficulty in differentiating between damage types (Constancio et al. 2023; Leach et al. 

2020; Grode et al. 2019; Mailhot et al. 2007). Our models indicated that the damage distribution 

was predicted by onion thrips densities interacting with plant location (Table 3.3, Model 3), 

regardless of C. coccodes suggesting that onion thrips feeding is the primary damage type. 

However, it is unknown how in a field setting, where precipitation or overhead irrigation often 

associated with severe disease outbreaks, this outcome would change (Tiberi et al. 2016; 

Rodriguez-Salamanca et al. 2018; Eigenbrode et al. 2018). Conversely, high precipitation and 

overhead irrigation lead to a reduction in onion thrips populations due to being washed away 

from the plants, potentially leading to a decreased amount of feeding damage on plants (North 

and Shelton 1986). In the future, it will be important to understand how the differing effects on 

onion thrips populations and disease severity affect pathogen spread. 

We predicted that relative humidity would influence pathogen spread indirectly by 

altering vector reproduction. We found that relative humidity did not affect onion thrips, likely 

because temperature was more important in influencing their development (Bergant et al. 2005). 

However, it is also possible that the relative humidity in our experiment was not outside of onion 

thrips’ tolerance range (Shipp & Gillespie 1993). Onion thrips are thigmotactic and may have 

been able to move to microclimates where relative humidity was favorable, thus avoiding the 

extreme conditions we created (Childers & Achor 1995; Kirk 1997). In onions, larval onion 

thrips are often found in the neck of the onion, where the leaves are close together, potentially 

75 

 
 
exposing them to high relative humidity (Mo et al. 2008). Finally, to prevent plant desiccation 

within our experiment units, our plants were watered every 3 d by soaking the soil around the 

experimental unit to prevent water from splashing onto the plant foliage. In the field, C. coccodes 

conidia are spread via water splash, and in our experiment, we avoided overhead watering to 

prevent pathogen spread (Dillard 1989). Thus, the only way for C. coccodes conidia to move 

among plants was through mechanical vectoring by onion thrips. Therefore, because relative 

humidity did not affect onion thrips reproduction or dispersal, we did not observe effects on 

pathogen spread. 

Increasing temperature altered both adult and larval onion thrips dispersal among the 

plants, likely due to increased densities and dispersal rates at high temperatures. At high 

temperatures, about 37% of adult onion thrips remained on the first onion plants, compared to 

nearly 100% of adult onion thrips in the low temperature treatment. High temperatures increase 

the rate of aerial adult onion thrips dispersal in the field, and a similar pattern was observed in 

our experiment (Smith et al. 2016). Additionally, although both temperatures had the same onion 

thrips initial densities (5 onion thrips per leaf), high temperature treatments had more adults at 

the end of the experiment than at the beginning, indicating a positive change in the development 

rate. At 30℃, onion thrips take approximately 10 d to develop from egg to adult, compared to 17 

d at 21℃, so at our high temperatures, the development rate increased, and onion thrips 

completed their full lifecycle during the experiment (Jamieson et al. 2012; Mound 1997). Larval 

onion thrips followed a similar distribution pattern as adults, with approximately 30% of larval 

onion thrips found on the first plant at high temperature, compared to nearly 100% on the first 

plant in the low temperature. There were more larval onion thrips found at low than high 

temperature, further supporting that onion thrips at low temperatures had not yet completed a full 

76 

 
 
lifecycle (Cornelissen 2011; Jamieson et al. 2012). Likely corresponding with increased onion 

thrips populations at high temperatures, we found more plants positive for C. coccodes at high 

temperatures. These results together indicate that onion thrips density is an important factor in 

pathogen spread, therefore altering developmental rate, decreasing generation time, and 

increasing dispersal rate via increased temperature indirectly affected pathogen spread in our 

experiments. 

Neither temperature nor relative humidity affected the damage distribution. Without 

thrips, damage was found only on the first (inoculated plant), but in the presence of thrips, 

damage occurred on all plants, similar to our results in the first experiment. Relative humidity 

did not alter onion thrips dispersal; therefore, it also did not indirectly alter damage distribution, 

nor did it affect disease incidence (i.e., the number of plants positive for C. coccodes). Yet, in the 

field, relative humidity may increase with precipitation and overhead irrigation, facilitating 

conidial dissemination, potentially altering pathogen spread (Dillard 1989; Tiberi et al. 2016; 

Eigenbrode et al. 2018). Temperature altered onion thrips dispersal but did not alter damage 

distribution, but we found that more plants were positive for C. coccodes at high temperatures. 

This may be due to the increased development rate at high temperatures (Cornelissen 2011; 

Jamieson et al. 2012). The larvae we recorded were second instar and had not spent enough time 

feeding on subsequent plants to significantly alter damage patterns. It’s possible that if the 

experiment had continued, the damage distribution pattern would have been reflective of the 

larval onion thrips distribution. 

The interactions between fungal pathogens and insects can be overlooked because insect 

vectors are not necessary for pathogen spread to occur. However, we found that temperature, but 

not relative humidity, indirectly affected C. coccodes spread by affecting insect behavior and 

77 

 
 
reproduction. Our results provide important information about how environmental changes may 

indirectly affect pathogen spread in a controlled setting, but field-based experiments are needed 

to investigate this further. Understanding the effect of changing environmental conditions on 

pathogen spread is critical for agriculture, especially as climate change causes unpredictable 

shifts in regional environmental conditions. 

Acknowledgments 

We thank the undergraduate students who assisted with data collection, insect rearing, 

fungal colony maintenance, and onion growing. This work was funded by the USDA Specialty 

Crops Block Grant Program. The authors acknowledge that Michigan State University occupies 

the traditional, ancestral, and contemporary lands of the Anishinaabeg- Three Fires Confederacy 

of Ojibwe, Odawa, and Potawatomi peoples. We advocate for the sovereignty of Michigan’s 12 

federally recognized Indian nations, for historic Indigenous communities in Michigan, for the 

individuals and communities who live here now, and for those who were forcibly removed from 

their homeland. By offering this land acknowledgement, we affirm indigenous sovereignty, and 

we will work to hold Michigan State University accountable to the needs of American Indians 

and Indigenous peoples. 

78 

 
 
 
 
LITERATURE CITED 

Anderson, R., P. E. Bayer, and D. Edwards. 2020. Climate change and the need for agricultural 

adaptation. Curr. Opin. Plant Biol. 56: 197–202. 

Atia, A. H. A., N.S. Mandour, M.F. Mahmoud, and M.M.A. Ibrahim. 2021. Assessment of 
Economic Threshold and Economic Injury Levels of Thrips tabaci on Onion Plants. J. 
Applied Plant Prot. 10: 109–117. 

Baysal-Gurel, F., N. Subedi, D. P. Mamiro, and S. A. Miller. 2014. First report of anthracnose of 

onion caused by Colletotrichum coccodes in Ohio. Plant Dis. 98: 1271–1271. 

Bergant, K., S. Trdan, D. Žnidarčič, Z. Črepinšek, and L. Kajfež-Bogataj. 2005. Impact of 

climate change on developmental dynamics of Thrips tabaci (Thysanoptera: Thripidae): 
Can it be quantified? Environ. Entomol. 34: 755–766. 

Bhangale, G. T., and M. B. Joi. 1983. Role of thrips in the development of purple blotch of 

onion. J. Maharashtra Agric. Univ. 8: 299–300. 

Brooks, M.E., K. Kristensen, K.J. van Bethem, A. Magnusson, C.W. Berg, A. Nielsen, H.J. 

Skaug, M. Maechler, and B.M. Bolker. 2017. glmmTMB balances speed and flexibility 
among packages for zero-inflated generalized linear mixed modeling. R. Journal. 9(2) 378-
400. 

Cano, J., J. Guarro, and J. Gené. 2004. Molecular and morphological identification of 

Colletotrichum species of clinical interest. J. Clin. Microbiol. 42: 2450–2454. 

Childers, C. C., and D. S. Achor. 1995. Thrips Feeding and Oviposition Injuries to Economic 

Plants, Subsequent Damage and Host Responses to Infestation. Thrips Biol. Manag. 31–51. 

Constancio, N., D. Higgins, M. Hausbeck, and Z. Szendrei. 2022. Onion Thrips (Thysanoptera: 

Thripidae) Host Plant Preference and Performance are Mediated by a Facultative Plant 
Pathogen of Onion. Environ. Entomol. 51: 1158–1165. 

Constancio, N., D. Higgins, M. Hausbeck, and Z. Szendrei. 2023. Managing insect and plant 

pathogen pests with organic and conventional pesticides in onions. J. Econ. Entomol. 116: 
2116–2123. 

Cornelissen, T. 2011. Climate change and its effects on terrestrial insects and herbivory patterns. 

Neotrop. Entomol. 40: 155–163. 

Coudriet, D. L., A. N. Kishaba, J. D. McCreight, and G. W. Bohn. 1979. Varietal Resistance in 

Onions to Thrips. J. Econ. Entomol. 72: 614–615. 

79 

 
 
Cullen, D. W., A. K. Lees, I. K. Toth, and J. M. Duncan. 2002. Detection of Colletotrichum 

coccodes from soil and potato tubers by conventional and quantitative real-time PCR. Plant 
Pathol. 51: 281–292. 

Daugherty, M. P., A. Rashed, R. P. P. Almeida, and T. M. Perring. 2011. Vector preference for 

hosts differing in infection status: Sharpshooter movement and Xylella fastidiosa 
transmission. Ecol. Entomol. 36: 654–662. 

Dillard, H.R. 1989. Effect of temperature, wetness duration, and inoculum density on infection 
and lesion development of Colletotrichum coccodes on tomato fruit. Phytopath. 79: 1063-
1066. 

Dutta, B., A. K. Barman, R. Srinivasan, U. Avci, D. E. Ullman, D. B. Langston, and R. D. 

Gitaitis. 2014. Transmission of Pantoea ananatis and P. agglomerans, Causal agents of 
center Rot of Onion (Allium cepa), by onion thrips (Thrips tabaci) through feces. 
Phytopathology. 104: 812–819. 

Eigenbrode, S. D., N. A. Bosque-Pérez, and T. S. Davis. 2018. Insect-Borne Plant Pathogens and 
Their Vectors: Ecology, Evolution, and Complex Interactions. Annu. Rev. Entomol. 63: 
169–191. 

Garrick, T. A., O. E. Liburd, and J. Funderburk. 2016. Effect of Humidity on Fecundity and Egg 
Incubation of Frankliniella bispinosa and Frankliniella occidentalis (Thysanoptera: 
Thripidae). Florida Entomol. 99: 505–508. 

Gill, H. K., H. Garg, A. K. Gill, J. L. Gillett-Kaufman, and B. A. Nault. 2015. Onion thrips 

(Thysanoptera: Thripidae) biology, ecology, and management in onion production systems. 
J. Integr. Pest Manag. 6: 1–9. 

Grode, A. S., E. Brisco-McCann, P. Wiriyajitsonboom, M. K. Hausbeck, and Z. Szendrei. 2019. 
Managing onion thrips can limit bacterial stalk and leaf necrosis in Michigan onion fields. 
Plant Dis. 103: 938–943. 

Grode, A., S. Chen, E. D. Walker, and Z. Szendrei. 2017. Onion Thrips (Thysanoptera: 

Thripidae) Feeding Promotes Infection by Pantoea ananatis in Onion. J. Econ. Entomol. 
110: 2301–2307. 

Hay, F. S., D. Strickland, E. Maloney, C. Hoepting, and S. J. Pethybridge. 2016. Anthracnose of 
onion caused by Colletotrichum coccodes in New York. Plant Dis. 100: 2171–2171. 

Ingwell, L. L., S. D. Eigenbrode, and N. A. Bosque-Pérez. 2012. Plant viruses alter insect 

behavior to enhance their spread. Sci. Rep. 2. 

Jamieson, L. E., A. Chhagan, and M. Griffin. 2012. Temperature development and damage rates 

of onion thrips. New Zeal. Plant Prot. 65: 126–132. 

80 

 
 
Jeger, M. J. 2020. The epidemiology of plant virus disease: Towards a new synthesis. Plants. 9: 

1–50. 

Jones, R. A. C. 2016. Future Scenarios for Plant Virus Pathogens as Climate Change Progresses, 

1st ed, Adv. Virus Res. Elsevier Inc. 

Jones, R. A. C., and M. J. Barbetti. 2012. Influence of climate change on plant disease infections 

and epidemics caused by viruses and bacteria. CAB Rev. Perspect. Agric. Vet. Sci. Nutr. 
Nat. Resour. 7. 

Kirk, W. D. J. 1997. Distribution, abundance, and population dynamics, pp. 217–257. In Lewis, 

T. (ed.), Thrips as Crop Pests. CAB International, New York. 

Leach, A., F. Hay, R. Harding, K. C. Damann, and B. Nault. 2020. Relationship between onion 

thrips (Thrips tabaci) and Stemphylium vesicarium in the development of Stemphylium leaf 
blight in onion. Ann. Appl. Biol. 176: 55–64. 

Leach, A., S. Reiners, M. Fuchs, and B. Nault. 2017. Evaluating integrated pest management 

tactics for onion thrips and pathogens they transmit to onion. Agric. Ecosyst. Environ. 250: 
89–101. 

Lemoine, N. P., W. A. Drews, D. E. Burkepile, and J. D. Parker. 2013. Increased temperature 

alters feeding behavior of a generalist herbivore. Oikos. 122: 1669–1678. 

Lenth, R.V., B. Bolker, P. Buerkner, I. Giné-Vázquez, M. Herve, M. Jung, J. Love, F. Miguez, 
H. Rieble, and H. Singmann. 2024. Estimated marginal means, aka least-squares means. 
Amer. Statistician. 34(4): 216-221. 

Lowery, D. T., P. M. Vickers, L. A. Bittner, L. W. Stobbs, and R. G. Foottit. 2015. Aphid 

transmission of the Ontario isolate of plum pox virus. J. Econ. Entomol. 108: 2168–2173. 

Mailhot, D. J., J. J. Marois, and D. L. Wright. 2007. Influence of flower thrips on fusarium 

hardlock severity. Plant Dis. 91: 1423–1429. 

Mo, J., S. Munro, A. Boulton, and M. Stevens. 2008. Within-plant distribution of onion Thrips 

(Thysanoptera: Thripidae) in onions. J. Econ. Entomol. 101: 1331–1336. 

Mound, L. A. 1997. Biological diversity, pp. 197–215. In Lewis, T. (ed.), Thrips as Crop Pests. 

CAB International, New York. 

Nault, B. A., and A. M. Shelton. 2010. Impact of insecticide efficacy on developing action 

thresholds for pest management: A case study of onion thrips (Thysanoptera: Thripidae) on 
onion. J. Econ. Entomol. 103: 1315–1326. 

North, R.C., and A. M. Shelton. 1986. Ecology of Thysanoptera within cabbage fields. Envi. Ent. 

15 (3): 520-526. 

81 

 
 
Peters, J. S., B. A. Aguirre, A. Dipaola, and A. G. Power. 2022. Ecology of Yellow Dwarf 

Viruses in Crops and Grasslands: Interactions in the Context of Climate Change. Annu. 
Rev. Phytopathol. 60: 283–305. 

Rhainds, M., and R. H. Messing. 2005. Spatial and temporal density dependence in a population 
of melon aphid, Aphis gossypii Glover (Homoptera: Aphididae), on established and sentinel 
taro plants. Appl. Entomol. Zool. 40: 273–282. 

R Core Team. 2023. R: A Language and Environment for Statistical Computing. R Foundation 

for Statistical Computing, Vienna, Austria. 

Rodriguez-Salamanca, L. M., T. B. Enzenbacher, M. L. Derie, L. J. du Toit, C. Feng, J. C. 

Correll, and M. K. Hausbeck. 2012. First Report of Colletotrichum coccodes Causing Leaf 
and Neck Anthracnose on Onions (Allium cepa) in Michigan and the United States . Plant 
Dis. 96: 769–769. 

Rodriguez-Salamanca, L. M., R. P. Naegele, L. M. Quesada-Ocampo, and M. K. Hausbeck. 
2018. Inoculation method, temperature, and relative humidity affect leaf and neck 
anthracnose, a new onion disease in Michigan. Plant Heal. Prog. 19: 64–68. 

Rueda, A., F. R. Badenes-Perez, and A. M. Shelton. 2007. Developing economic thresholds for 

onion thrips in Honduras. Crop Prot. 26: 1099–1107. 

Shaw, A. K., A. Peace, A. G. Power, and N. A. Bosque-Pérez. 2017. Vector population growth 
and condition-dependent movement drive the spread of plant pathogens. Ecology. 98: 
2145–2157. 

Shipp, J. L., and T. J. Gillespie. 1993. Influence of temperature and water vapor pressure deficit 
on survival of Frankliniella occidentalis (Thysanoptera, Thripidae). Environ. Entomol. 22: 
726–732. 

Singh, B. K., M. Delgado-Baquerizo, E. Egidi, E. Guirado, J. E. Leach, H. Liu, and P. Trivedi. 
2023. Climate change impacts on plant pathogens, food security and paths forward. Nat. 
Rev. Microbiol. 21: 640–656. 

Smith, E.A., E. J. Shields, and B. Nault. 2016. Impact of abiotic factors on onion thrips 

(Thysanoptera: Thripidae) aerial dispersal in an onion ecosystem. Envi. Entomol. 45(5): 
1115-1122. 

Steiner, M. Y., L. J. Spohr, and S. Goodwin. 2011. Relative humidity controls pupation success 

and dropping behaviour of western flower thrips, Frankliniella occidentalis (Pergande) 
(Thysanoptera: Thripidae). Aust. J. Entomol. 50: 179–186. 

Tiberi, R., T. Panzavolta, M. Bracalini, A. Ragazzi, B. Ginetti, S. Moricca, R. Tiberi, T. 

Panzavolta, M. Bracalini, A. Ragazzi, B. Ginetti, and S. Moricca. 2016. Interactions 

82 

 
 
between insects and fungal pathogens of forest and ornamental trees. Ital. J. Mycol. 45: 54–
65. 

Ulman, D. E., J. L. Sherwood, and T. L. German. 1997. Thrips as vectors of plant pathogens, pp. 

539–565. In Lewis (ed.), Thrips as Crop Pests. CAB International. 

Velásquez, A. C., C. D. M. Castroverde, and S. Y. He. 2018. Plant–Pathogen Warfare under 

Changing Climate Conditions. Curr. Biol. 28: R619–R634. 

Yarwood, C. E. 1943. Association of Thrips with Powdery Mildews. Mycologia. 35: 189–191. 

83 

 
 
 
 
CHAPTER 4: PLASTIC MULCHES PROVIDE ALTERNATIVE MANAGEMENT 

OPTIONS FOR ONION THRIPS 

Abstract 

An integrated pest management program (IPM) relies on multiple management methods 

to reduce pest populations. In particular, onion thrips (Thrips tabaci) have relatively few 

effective control methods, and especially non-chemical management methods, like plastic 

mulches, need to be developed. We tested 7 different plastic mulches in the field, including 3 

silver mulches, to determine their effect on thrips populations. A subset of the mulches was 

tested in a second field trial with or without a pesticide program. Thrips populations were 

recorded once a week for both field trials and spectral data was collected using a 

spectrophotometer. Plant growth, temperature above and below the mulch were recorded for the 

second field trial. Finally, we conducted a no-choice lab experiment to determine the potential 

mechanisms of mulches on thrips population regulation. Thrips numbers, mulch and soil 

temperature, and plant growth were recorded after 13 days. In the first field trial, we found that 

not all the silver mulches were equally effective at reducing thrips populations. In the second 

field trial, red and diamond silver mulch reduced thrips populations similar to the pesticide 

program. Furthermore, the addition of a pesticide program provided synergistic control in most 

treatments. Finally, the no-choice experiment revealed that mulches likely affect thrips 

populations through wavelength-specific induced changes. Overall, we found that silver and red 

mulches suppressed thrips populations as effectively as a season-long pesticide program, 

providing options for an integrated pest management program. 

Introduction 

Integrated pest management (IPM) requires the synergistic use of available techniques, 

such as biological, cultural, physical, and chemical control methods, to manage a pest (Ehler and 

84 

 
 
Bottrell 2000). Within an IPM framework, chemical control should only be used as a last resort 

with resistance management guidelines, such as pesticide class rotation and action thresholds, 

guiding their use (Siegwart et al. 2015). Especially in the case of insect pests, such as onion 

thrips (Thrips tabaci Lindeman, Thysanoptera: Thripidae), that rapidly develop resistance to 

insecticide classes, increasing the number of effective non-chemical management options is 

paramount (Sparks 2013; Pedigo et al. 1986; Ehler and Bottrell 2000; Devi and Roy 2017). 

Plastic mulches are used as a physical control method in IPM, they can be deployed 

either alone or in combination with other pest control options. Historically, plastic mulches have 

been used to increase soil moisture retention and plant yield, control the microclimate around 

plants, and reduce weed pressure (Ham et al. 1993; Greer and Dole 2003; Job and Bhakar 2018). 

Plastic mulches are also used as a physical control strategy for insect pests, but they have had 

mixed success in reducing pest populations. Reflective mulches have had some success in 

reducing aphids (Aphidae), whiteflies (Aleyrodidae), spotted-wing drosophila (Drosophila 

suzukii) and pear psylla (Cacopsylla pyricola) (Brown et al. 1993; Csizinszky et al. 1995, 1999; 

Greer and Dole 2003; Nottingham and Beers 2020; McIntosh et al. 2022). However, silver or 

reflective mulches have had variable success in deterring onion thrips, either reducing numbers 

or having no effect (Lu 1990; Csizinszky et al. 1995; Greer and Dole 2003; van Toor et al. 2004; 

Iglesias et al. 2021). The reason for variable success is unclear, and pest population patterns may 

be driven either indirectly through changes in the microclimate around mulches which may make 

the area inhospitable to pests, or by wavelength-specific color preferences which can affect 

behavior (Andreotti et al. 2010; Gordon et al. 2008; Ham et al. 1993; Larentzaki et al. 2008; 

Bégin et al. 2001; Vincent et al. 2003; Diaz and Fereres 2007). Therefore, it is important to 

evaluate the indirect and direct effects of mulches both on the crop and on the insect. 

85 

 
 
Mulches alter the microclimate around plants throughout the growing season, and these 

changes can also affect insect populations (Andreotti et al. 2010; Gordon et al. 2008; Ham et al. 

1993; Larentzaki et al. 2008). For example, dark-colored mulches, such as black or red, are 

recommended in the early season because they increase soil temperature around the plant (Job 

and Bhaker 2018; Csizinszky et al. 1995; Aguyoh et al. 1999; Greer and Dole 2003). These 

increases may potentially push insects to the upper limits of their thermal tolerance, thus 

reducing pest populations (Gordon et al. 2008; Job and Bhakar 2018). However, dark mulches 

are not recommended for summer or fall crops because high heat retention may be detrimental to 

plant health (Aguyoh et al. 1999; Lai et al. 2024). Conversely, light mulches, such as white or 

highly reflective silver mulches, decrease temperature around the plant and are recommended for 

cool weather crops to reduce soil temperatures (Ham et al. 1993; Greer and Dole 2003; Lai et al. 

2024). However, white mulch can increase pest numbers, for example, it is highly attractive to 

onion thrips, and therefore may not be suitable for fields with historically high onion thrips 

infestations (Brown and Brown 1992; Iglesias et al. 2021; Scott et al. 1989). Mulch color not 

only affects microclimate and potentially indirectly insect physiology but may also affect insect 

behavior (Bégin et al. 2001; Vincent et al. 2003; Diaz and Fereres 2007). 

Plastic mulches reflect different wavelengths of light based on their color, providing 

additional photobiological benefits to plants while potentially inducing wavelength-specific 

behaviors in onion thrips (Decoteau et al. 1988, 1989; Csizinszky et al. 1995; Lopez-Reyes et al. 

2022). Light within the UV range (300 – 400 nm) increases leaf pigmentation and thickness, but 

many thrips species prefer light within that range (Csizinszky et al.1995; Lopez-Reyes et al. 

2022). Red and near-infrared light (620 – 800 nm) increases photosynthesis and yield in onion 

plants but is one of the least attractive colors to thrips, likely due to their low sensitivity to 

86 

 
 
wavelengths within that range (Walker 1974; Alam et al. 2007; Egri et al. 2020; Lopez-Reyes et 

al. 2022). White mulch reflects across the entire visible spectrum (400 – 800 nm) and therefore 

should provide multiple photobiological benefits (Csizinszky et al. 1995; Courbier and Pierik 

2019; Dănăilă-Guidea and Delian 2020). Conversely, black mulch reflects minimal light, thus 

plants may not receive additional photobiological benefits but it is attractive to thrips (Csizinszky 

et al. 1995; Ham et al. 1993; Streck et al. 1995). In addition to composition, wavelength intensity 

(i.e., amount of light reflected) can also alter insect behavior. For example, increasing the 

intensity of blue light often correlates with increased attractiveness for western flower thrips 

(Franklinella occidentalis), and onion thrips prefer highly reflective colors within the same hue 

(Otani et al. 2014; Otieno et al. 2018; Westmore et al. 2019; Stukenberg et al. 2020). Due to the 

varying and potentially conflicting effects of plastic mulches on plants and insect pests, it 

remains unclear whether mulches in their associated colors are a viable alternative management 

strategy. 

The goal of our study was to test various plastic mulches to determine which colors were 

most effective in controlling onion thrips populations and to determine if plastic mulches could 

be a viable management strategy to reduce insecticide sprays. Onion thrips are a significant pest 

of onions (Allium cepa L. Aspragales: Amaryllidaceae) and can cause substantial economic 

losses if left uncontrolled (Kendall and Capinera 1987; Fournier et al. 1995; Waiganjo et al. 

2008). In our first field experiment, we tested 7 different treatments, including 3 silver mulches, 

to identify the most promising colors for onion thrips control. We hypothesized that all 3 silver 

mulches would be equally effective in reducing onion thrips populations when compared to the 

control. In our second field experiment, we investigated the level of onion thrips control 

provided by a subset of mulches from the first experiment alone or combined with pesticide 

87 

 
 
programs. We hypothesized that mulches alone would not be as effective as a grower-standard 

pesticide program for onion thrips control, but the addition of a pesticide program to the mulch 

treatments would provide synergistic control. To determine the potential mechanisms of mulch 

effects on onion thrips, we conducted a no-choice experiment in an environmental chamber to 

determine thrips performance in response to mulch color. 

Methods 

Field mulch trials 

We conducted two field experiments with different colored mulches to evaluate their 

effectiveness in deterring onion thrips. The first field experiment took place at Michigan State 

University’s Entomology Research Farm (Lansing, MI) in a mowed grassy area in the summer of 

2022. The plastic mulch treatments included: 1) control (mowed grass), 2) black mulch, 3) 

reflective silver mulch, 4) metallic silver mulch, 5) diamond silver mulch, 6) red mulch, and 7) 

white mulch (N = 15, Table 4.1). All mulches were cut into 1.2 m x 1.8 m sections and laid in a 

randomized complete block design in the field. To secure the mulch to the ground, each side of 

the rectangular sheet was rolled around a rebar and held in place with yard staples (High Tech 

Pet, Ventura, CA). Onions (cv. ‘New York Early’) were grown by placing one seed in a plastic 

pot (8.5 cm deep, 10 cm wide; ITML Horticultural Products Inc., Brantford, Ontario) filled with 

a perlite soil mix (Suremix Perlite, Michigan Grower Products Inc., Galesburg, MI). The 

seedlings were maintained in an environmental chamber (25°C, 50% RH, 16:8 h (L:D)) and were 

covered during germination to prevent soil dehydration. The cover was removed 7 days after 

seeding once germination occurred in > 75% of seedlings. The seedlings were watered 3 times a 

week and fertilized at 75 ppm N (20-20-20 Jack’s General Purpose Water-Soluble Fertilizer, JR 

Peters Inc., Allentown, PA) once a week. 

88 

 
 
Table 4.1: The mulches selected for testing to determine their effectiveness in reducing onion thrips populations in 2022 and 2023.  

Thickness 

Manufacturer 

Light reflection 

Mulch color  Experiment 

Control 

Field experiment 1,2 

(bare ground) 

Lab experiment 

(mil) 

Location 

Mulch description 

Range 
(nm) 
300 – 800 

Reflectiveness 
(%) 
< 10 

Black 

Field experiment 1,2 

1.0 

Ken-Bar, Rochester 

Black 

300 – 800 

< 5 

Lab experiment 

NY 

Reflective 

Field experiment 1 

1.25 

Ken-Bar, Rochester 

Metallic plastic 

300 – 800 

~ 30 

silver 

NY 

Metallic 

Field experiment 1 

Not provided  Dubois Agrinovation, 

Metallic reflective 

300 – 800 

~ 65 

silver 

ON 

Diamond 

Field experiment 1,2 

6.0 

Viagrow, East Point, 

Mylar diamond film 

300 – 800 

~ 85 

silver 

Red 

Lab experiment 

GA 

Field experiment 1,2 

1.0 

Ken-Bar, Rochester 

Red 

620 – 800 

~ 35 

Lab experiment 

NY 

White 

Field experiment 1,2 

1.25 

Ken-Bar, Rochester 

White on black 

400 – 800 

~ 35 

Lab experiment 

NY 

89 

 
 
 
 
 
 
 
 
Onions were placed into the field when plants were approximately 8 weeks old. Small 

holes were dug into the ground beneath the mulch and slits were cut in the mulch through which 

pots were inserted, ensuring that the tops of the pots were flush with the mulch surface. Three 

seedlings per plot were positioned in the center of the mulch sheets, equidistant (36 cm) from 

each other, and watered 2-3 times a week. Each week from 4 August to 8 September 2022, onion 

thrips were counted by visually inspecting all the leaves, and the number of leaves per plant was 

also recorded. 

In the second field experiment, we tested a subset of the plastic mulches from 2022, in 

combination with a pesticide program. This experiment took place at the Southwest Michigan 

Research and Extension Center (SWMREC; Benton Harbor, MI) on Spinks Loamy Fine Sand 

(USDA Soil 13B). To prepare the soil for mulches, the ground was rototilled to 15 cm depth, 

raised beds (0.6 m wide) were created using a tractor-mounted bed shaper, and a drip fertigation 

line was laid in the center of the beds. After mulches were laid, approximately 2 cm diameter 

holes were cut into the mulch every 20 cm so that onion transplants (cv. ‘Ailsa Craig’; Dixondale 

Farms, Carrizo Springs, TX) in the 2-4 leaf stage could be transplanted. After transplanting, 

fertilizer was immediately applied at 125 ppm N (20-20-20 N-P-K, Jack’s General Purpose 

Water-Soluble Fertilizer), and reapplied 3 times throughout the growing season (9, 30 June, and 

21 July), onions were watered once a week. 

All treatments were set up in a randomized complete block design on 17 May 2023. Split 

plot factors were the presence or absence of a pesticide program, initiated when the 1 thrips/leaf 

threshold was reached on 6 June 2023, for a total of 10 treatments. Full plots measured 0.6 m x 

10 m and subplots were 0.6 m x 5.0 m. The treatments were: 1) bare ground (no mulch) + no 

pesticide, 2) bare ground + pesticide, 3) black mulch + no pesticide, 4) black mulch + pesticide, 

90 

 
 
5) red mulch + no pesticide, 6) red mulch + pesticide, 7) diamond silver mulch + no pesticide, 8) 

diamond silver mulch + pesticide, 9) white mulch + no pesticide, 10) white mulch + pesticide (N 

= 4). The pesticide program consisted of two back-to-back applications 7 days apart of 

spirotetramat (Movento; 0.78ml/l, Bayer Crop Science, Leverkusen, Germany) tank mixed with 

pydiflumetofen and fludioxonil (Miravis Prime; 1.8ml/l, Syngenta, Basel, Switzerland) on 6 and 

14 June 2023, and two back-to-back applications 7 days apart of abamectin and cyantraniliprole 

(Minecto Pro; 1.5ml/l, Syngenta) on 11 and 18 July 2023. Each insecticide was tank mixed with 

a nonionic surfactant (1% v:v, Syl-Tac, Wilbur-Ellis, Aurora, CO). All insecticides were applied 

as a foliar spray with a CO2 backpack sprayer equipped with a single nozzle boom with an 

XR8003 flat-fan nozzle (TeeJet Technologies, Wheaton, IL), calibrated to 241 kPa to deliver 246 

l/ha.  

Each week, the field was scouted for onion thrips by randomly selecting 10 plants per 

subplot and recording the total number of onion thrips per plant. Additionally, 5 plants per 

subplot were randomly selected to record plant height and the total number of leaves each week. 

For height measurements, a ruler was placed on the soil surface, and height was measured from 

the base of the plant to the tip of the tallest leaf. We used a probing digital thermometer 

(Sovarcate, Hunan, China) to record soil temperature 2.5 cm below the soil surface, at the base of 

5 onions per subplot. Temperature on the surface of the mulch was measured by aiming an 

infrared thermometer (Sovarcate) near the base of 5 randomly selected onions in each plot, 

approximately 5 cm from the top of the mulch. All temperature, plant and insect measurements 

were taken each week between 24 May and 8 August 2023. 

No-choice lab experiment 

An onion thrips colony was established at Michigan State University (East Lansing, MI) 

91 

 
 
beginning in August 2022. Onion thrips were collected from a commercial onion field (Grant, 

MI) where conventional pesticides and fertilizers were used. Mesh cages (50 cm3, MegaView, 

Taichung, Taiwan) were kept at room temperature with ambient humidity and a 16:8 h L:D 

cycle. To sustain continuous rearing, 6-8 onions at the 5-7 leaf stage, grown from certified 

organic onion seeds (cv. ‘New York Early’; Johnny’s Selected Seeds, Winslow, ME) were added 

into each cage every week so onion thrips could feed ad libitum. 

To evaluate the impact of different colored mulches on onion thrips performance, a no-

choice laboratory experiment was conducted. Experimental units consisted of one 6-week-old 

onion seedling grown as described in the previous section. One seedling was transplanted into a 

rectangular aluminum tray (30 cm x 28 cm x 8 cm, Handi-Max, Wheeling, IL) filled with perlite 

soil mix (Suremix Perlite) to a depth of 6 cm with drainage slits along the bottom and was 

watered immediately after transplanting. There were five different treatments: 1) control – no 

mulch, 2) black mulch, 3) diamond silver mulch, 4) red mulch, and 5) white mulch (N = 27). 

Mulches were cut into squares (30.48 cm x 30.48 cm) to cover the entire surface of the 

experimental units, small slits were made in the center of each mulch square for inserting the 

onion seedling into the soil in the tray, and the edges were tucked underneath the soil to hold the 

mulch in place. Cages made of transparency film (School Smart, Greenville, WI; 26 cm tall x 28 

cm x 26 cm) and topped with a nylon mesh (160 m mesh size) were placed over each tray to 

prevent onion thrips from moving between experimental units while allowing ventilation. 

Experimental units were organized within environmental chambers (25°C, ambient RH, 16:8 h 

L:D) in a randomized complete block design. 

Three adult onion thrips were removed from the colony and transported in a 1.7 ml 

microcentrifuge tube (Thomas Scientific, Swedesboro, NJ) to the environmental chamber; a 3 cm 

92 

 
 
 
piece of fresh onion foliage was provided to thrips during handling and transportation. The 

experimental units were set up approximately 1 hour before introducing onion thrips into the 

experiment. Onion thrips vials were randomly assigned to experimental units; vials were then 

opened and placed at the base of the onion seedling to allow thrips to move to the plants. The 

transparent cage was then placed over the arena, and additional soil was added between the 

bottom of the plastic cover and the aluminum tray to prevent onion thrips from escaping. After 6 

days, the experimental units were watered by immersing the bottom of aluminum trays into 

water for approximately 40 s, allowing water to soak the soil through the slits in the tray. After 

13 d the number of adult and larval onion thrips, estimated feeding damage severity (%), plant 

growth (height and number of leaves), temperature on the surface of the mulch, and soil 

temperature were recorded for each plant. Destructive sampling was used to count the number of 

onion thrips; the onions were uprooted so that the neck of the onion could be examined for onion 

thrips. Feeding damage severity was visually rated by estimating the amount of damaged tissue 

per plant between 0 to 100%. Mulch surface temperatures were measured with an infrared 

thermometer (Sovarcate) 5 cm from the mulch surface, and soil temperatures were measured 

with a digital probe thermometer (Sovarcate) at a depth of 2.5 cm once at the end of the 

experiment. 

Spectrophotometry 

A handheld spectrophotometer (FLAME-T-UV-VIS-ES; Ocean Insight, Orlando, FL) 

was used to measure the light reflectance (%) of mulches between 300 and 800 nm. Each 

measurement averaged 20 readings with a scan time of 3 s each, and a resolution of 0.2 nm, in 

the ultraviolet–visible light (UV-VIS) range. The spectrophotometer was connected to a pulsed 

xenon lamp as the light source (PX-2; Ocean Insight) so that light conditions remained 

93 

 
 
consistent. In the field, the reflectance of the mulches was measured with a handheld probe 

(QR400-7-SR; Ocean Insight) positioned perpendicular 10 cm from the mulch surface. 

Reflectance readings were obtained in the field on 28 July 2022, 17 July, and 14 August 2023, 

and in the laboratory experiment on 21 August 2023. 

Data analysis 

In our first field experiment, to determine how different mulch colors affected onion 

thrips populations, we constructed generalized linear mixed models (GLMMs) using the 

‘glmmTMB’ package with onion thrips per leaf as the response variable and mulch color as the 

fixed factor (Brooks et al. 2017). Block and date were random factors, and a negative binomial 

distribution was used. In all models, the ‘drop1’ function was used to identify significant fixed 

effects of mulch color compared to the null model (α = 0.05). When the model had a significant 

fixed effect, Tukey’s HSD test was conducted using the ‘multcomp’ package (Hothorn et al. 

2008) to determine significant differences (α = 0.05) among treatments. 

In our second field experiment, we were interested in how mulch color combined with an 

insecticide program affected onion thrips populations, plant growth, soil temperature and 

temperature of the surface of the mulch. We used GLMMs to determine if there was an 

interactive effect of mulch color and spray program on onion thrips populations, with block and 

date as the random factors, and a negative binomial distribution. The ‘drop1’ function was used 

to determine significant treatment interactions, followed by a Tukey’s HSD to determine 

significant differences among treatments (α = 0.05). For plant growth data, leaf number and plant 

height were analyzed only from the date when plants were at their peak growing stages. To 

determine how treatment affected the number of leaves per plant and plant height, we created 

linear mixed effects models with the ‘lme4’ package (Bates et al. 2015) with both mulch color 

94 

 
 
 
and spray treatment as fixed effects, and block as the random factor. To determine how mulch 

treatment affected temperature at the mulch surface and below the soil, we compared the mean 

temperatures above and below the mulch to the mean ambient temperature (MSU Enviroweather, 

2024). Linear mixed effects models were created for both soil and mulch surface temperature 

with mulch color as the fixed factor and date as the random factor. To determine significant 

treatment effects in models for onion thrips per leaf, leaves per plant, average plant height, and 

temperature, the ‘drop1’ function was used, followed by a Tukey’s HSD to determine significant 

differences among treatments (α = 0.05). 

In our no-choice lab experiment, we were interested in how mulch color affected onion 

thrips populations, plant growth, and temperature around the plants under controlled conditions. 

We used GLMMs to determine the effect of mulch color on onion thrips numbers, with block as 

a random factor and a Poisson distribution. To determine how mulch color affected plant growth, 

we used linear mixed-effects models with block as the random factor. Finally, for soil and mulch 

surface temperature, we created linear mixed-effects models with mulch color as the fixed factor 

and block as the random factor. Models were checked for significance in the same way as 

described in the first experiment. 

Results 

Field mulch trials 

In 2022, mulch color had a significant effect on onion thrips numbers (Figure 4.1A; χ2 = 

161.56, df =6, p-value < 0.01). Compared to the control treatment, there were about twice as 

many onion thrips per leaf in the diamond silver mulch (t-value = 6.05, df = 180, p-value < 0.01), 

the red mulch (t-value = 7.36, df = 180, p-value < 0.01) and the white mulch (t-value = 5.07, df = 

180, p-value < 0.01). Onion thrips per leaf tripled on the black mulch (t-value = -9.58, df = 180, 

95 

 
 
 
p-value < 0.01), the reflective silver mulch (t-value = 8.99, df = 180, p-value < 0.01) and the 

metallic silver mulch (t-value = 10.16, df = 180, p-value < 0.01) compared to the control 

treatment. Among the silver mulches, the reflective silver and metallic silver mulch performed 

similarly to each other (t-value = 1.44, df = 180, p-value = 0.79), but the diamond silver mulch 

significantly reduced onion thrips populations compared to the reflective silver mulch (t-value = 

3.33, df = 180, p-value = 0.01) and the metallic silver mulch (t-value = 4.70, df = 180, t-value < 

0.01). 

In the 2022 field experiments, all 3 silver mulches reflected light within the UVA range 

(300-400 nm), but none of the other mulches reflected light within this range (Figure 4.1B). The 

3 silver mulches reflected light within the same range (UV-VIS), but the amount of light 

reflected was different between each silver mulch. The diamond silver mulch was the most 

reflective (70-90% reflectance), reflective silver mulch was in the middle (60%), and metallic 

silver mulch reflected the least amount of light (25%). White mulch did not reflect any light in 

96 

 
 
 
the UV range but reflected between 65-70% of light in the visible range, similar to the reflective 

silver mulch in the visible range. Red mulch reflected less than 10% of light within the UV and 

400 – 600 nm range, but reflectance increased to about 20% in the 600-800 nm range. Black 

mulch reflected less than 10% of light across the UV-VIS spectrum. 

In 2023, there was a significant interactive effect between mulch color and insecticide 

treatment on onion thrips populations (Figure 4.2; χ2 = 25.83, df = 4, p-value < 0.01). In general, 

across most mulch treatments, adding a spray program provided significant additional onion 

thrips suppression when compared to the mulch alone (t-value > 3.29, df = 80, p-value < 0.03), 

except for the diamond silver mulch where thrips numbers were similar between the insecticide-

treated and untreated plots (t-value = 2.76, df = 80, p-value = 0.15). White mulch was the least 

effective treatment overall, regardless of the presence of an insecticide program, with about 

twice as many thrips per leaf than in the other treatments (t-value < -7.41, df= 80, p-value < 

0.01). The addition of a pesticide program on the white mulch significantly reduced onion thrips 

populations (t-value = 3.29, df = 80, p-value = 0.03), but there were still 2.5 times more thrips 

when compared to the bare ground control treatment with an insecticide program (t-value = -

14.29, df = 80, p-value < 0.01). The red mulch without an insecticide had similar numbers of 

onion thrips as the control treatment with insecticides (t-value = -2.15, df = 80, p-value = 0.49). 

Red mulch with an insecticide program was the most effective at reducing onion thrips 

populations, with 62% fewer onion thrips when compared to the control and black mulch with 

insecticide (t-value > 8.88, df = 80, p-value < 0.01), and 20% fewer onion thrips compared to the 

diamond silver with an insecticide program (t-value = -4.84, df = 80, p-value < 0.01). Black 

mulch, with or without a pesticide program, performed similarly to the control treatment, with or 

without a pesticide program (t-value < 1.25, df = 80, p-value > 0.97). 

97 

 
 
Mulch color had a significant effect on the average number of leaves (Figure 4.3A; F= 

5.93, df = 4, 191, p-value < 0.01), but insecticide treatment did not influence leaf numbers (F = 

0.08, df = 1, 191, p-value = 0.77). There were more leaves on plants grown on the black, red, and 

white mulch compared to plants in the control treatment (t-value > 2.86; df = 8, p-value < 0.03). 

There were similar numbers of leaves per plant in the diamond silver mulch and the control 

treatments (t-value = -0.08, df = 8, p-value = 0.99). Mulch color also significantly affected plant 

height (Figure 4.3B; F = 3.37, df = 4, 191, p-value = 0.01), but insecticide treatment did not (F = 

0.67, df = 1, 191, p-value = 0.41). Onions grown on the black and red mulches were significantly 

98 

 
 
 
 
taller than plants on the diamond silver mulch (black: t-value = -2.89, df = 8, p-value = 0.03, red: 

t-value = -3.09, df = 8, p-value = 0.02). 

The temperature of the mulch surface was significantly altered by mulch color (Figure 

4.4A; F = 301.94, df = 5, 129.47, p-value < 0.01). Black mulch was the only treatment to 

significantly increase the mulch surface temperature compared to the ambient temperature, (14℃ 

above ambient, t-value = 4.00, df = 18, p-value < 0.01). When compared to the bare ground 

control, black, red, and white mulch significantly increased the temperature at the surface of the 

mulch by approximately 9℃, 3.5℃, and 2℃ respectively (t-value > 2.79, df =18, p-value < 

0.05). Diamond silver mulch significantly reduced the temperature at the surface of the mulch 

compared to the bare ground treatment by 9℃ on average (t-value = -17.09, df = 18, p-value < 

0.01). Mulch color also significantly affected soil temperature (Figure 4.4B; F = 366.57, df = 5, 

99 

 
 
 
 
78.86, p-value < 0.01). The diamond silver mulch was the only treatment where the soil 

temperature was not significantly higher compared to the ambient temperature (t-value = 2.26, df 

= 18, p-value = 0.18). Red and black mulch significantly increased the soil temperature 

compared to the bare ground control treatment by 2℃ (t-value > 15.58, df = 18, p-value < 0.01). 

Compared to the bare ground control, both diamond silver and white mulch reduced soil 

temperature by approximately 2℃ (t-value > -9.41, df =18, p-value < 0.01). 

In the 2023 field trials, we found similar reflectance patterns than in 2022 (Figure 4.5). 

Within the UV range, diamond silver mulch reflected approximately 65% of light, significantly 

more than any other mulch color (t-value > 86.29, df = 956, p-value < 0.01). Within the visible 

range, the diamond silver mulch reflected 70% of light across the spectrum, and white mulch 

100 

 
 
 
reflected 40% of light, significantly less than diamond silver (t-value = -195.17, df = 4190, p-

value < 0.01). Black mulch and the control treatment only reflected 4% of light across the VIS 

spectrum and were not significantly different from each other (t-value = 2.44, df = 4190, p-value 

= 0.11). Red mulch reflected significantly less light (approximately 8%) within the 400 - 620 nm 

range (VIS excluding red) spectrum compared to diamond silver and white mulch (t-value < -

453.49, df = 2190, p-value < 0.01). However, within the red range (620 – 800 nm), red reflected 

approximately 35% of light, which was significantly more than the white mulch (30% of light 

reflected; t-value = 70.93, df = 2000, p-value < 0.01), but significantly less than diamond silver 

mulch (66% of light reflected; t-value = 363.98, df = 2000, p-value < 0.01). 

No-choice lab experiment 

In our no-choice experiment, mulch color significantly affected larval onion thrips 

101 

 
 
 
numbers (χ2 = 22.67, df = 4, p-value < 0.01) but not adult numbers (Figure 4.6; χ2 = 1.91, df = 4, 

p-value = 0.75). There were no significant differences in larval onion thrips numbers between 

any of the mulch treatments compared to the no mulch control treatment (t-value < 2.34, df =54, 

p-value > 0.13). However, there were approximately half as many larval onion thrips on the red 

(2.44 larval onion thrips/leaf) compared to the black mulch (4.75 larval onion thrips/leaf; t-value 

= -3.25, df = 54, p-value = 0.01), and the white mulch (4.25 larval onion thrips/leaf; t-value = 

2.89, df = 54, p-value = 0.03). Mulch color did not significantly affect plant growth (F = 0.92, df 

= 4, 104, p-value = 0.46). 

Mulch color significantly affected mulch surface temperature (F = 25.4, df = 4, 104, p-

value < 0.01). All treatments increased the mulch surface temperature compared to the control 

102 

 
 
 
treatment by approximately 1℃ (t-value > 6.09, df = 54, p-value < 0.01). There were no 

significant differences between the different colored mulches when compared to each other (t-

value < -2.5, df = 54, p-value > 0.09). Soil temperature was significantly affected by mulch color 

(F = 7.18, df = 4, 104, p-value < 0.01). All mulch treatments significantly increased soil 

temperature compared to the control treatment by approximately 2℃ (t-value > 2.86, df = 54, p-

value < 0.03). There were no significant differences in soil temperature between the mulches 

when compared to each other (t-value < -2.50, df = 54, p-value > 0.08). 

Discussion 

Our results demonstrate that some plastic mulches can be used as an effective alternative 

management strategy for onion thrips. Red mulch and diamond silver mulch without a pesticide 

program were as effective at managing onion thrips populations as a pesticide program, 

potentially offsetting spray application costs and the negative impacts associated with 

conventional pesticide use. Furthermore, we found that combining a pesticide program with 

plastic mulches can provide additional onion thrips control. Our lab-based performance 

experiment suggests that mulch impacts thrips directly, rather than through indirect effects, such 

as changes in the microclimate. 

In our first field experiment, we tested various plastic mulches to determine which colors 

were most likely to be successful in reducing onion thrips populations. All of our mulch 

treatments had increased onion thrips populations compared to the control, but this could be due 

to the lack of color contrast between the grassy background and onion foliage, or associational 

resistance provided by the grass (Barbosa et al. 2009). Western flower thrips are attracted to 

objects that have contrasting background, and this might be the case for onion thrips as well 

(Vernon and Gillespie 1995; Mainali and Lim 2010). We expected that all tested types of silver 

103 

 
 
 
reflective mulches would be equally effective at reducing onion thrips numbers on onions, but 

this was not the case, with inconsistent performance across silver reflective mulches, as reported 

in previous studies (Lu 1990; Csizinszky et al. 1995; Greer and Dole 2003; van Toor et al. 2004; 

Iglesias et al. 2021). Although the reflectance range was similar across the silver reflective 

mulches in our experiment, the amount of reflected light (% reflectiveness) was different 

depending on the mulch brand. Alterations in the reflectiveness or intensity of light change the 

attractiveness/repellence of mulches, and this could be why our silver reflective mulches 

performed differently from one another, with the most reflective mulch, diamond silver, 

performing the best for onion thrips suppression (Otani et al. 2014; Otieno et al. 2018; 

Stukenberg et al. 2020). The results highlight the need to investigate spectral information so that 

the differences between wavelength composition (chromatic) and reflectiveness or intensity 

(achromatic) cues can be identified. 

In our second field experiment, we selected a subset of the mulches and tested them with 

and without a pesticide program, with the goal of understanding if the integration of a pesticide 

program could provide synergistic control. Surprisingly, we found that red (without a pesticide 

program) and diamond silver mulch (with or without a pesticide program) alone achieved similar 

levels of onion thrips control compared to the control (bare ground) with a pesticide program. 

Onion thrips are notorious for developing insecticide resistance to the limited number of active 

ingredients available for their control (Martin et al. 2003; Shelton et al. 2006; Nault and Shelton 

2010; Diaz-Montano et al. 2011; Adesanya et al. 2020) and having non-insecticide-based 

management options, such as mulches, that can suppress their populations to the same levels as a 

season-long pesticide program can be an important tool in their integrated pest management 

program. 

104 

 
 
The integration of a pesticide program with the mulches provided synergistic control in 

all our treatments, except for the diamond silver mulch. Onion thrips numbers in these plots were 

already some of the lowest across our treatments, well below the action threshold of 1 onion 

thrips/leaf for the seasonal average and below the economic injury level of 2.2 onion thrips/leaf 

(Fournier et al. 1995). With the addition of a pesticide program, the black mulch (0.85 onion 

thrips/leaf) and the control treatment (0.84 onion thrips/leaf) suppressed onion thrips populations 

below the threshold. The red mulch with a pesticide program was the most effective in 

suppressing onion thrips populations (0.33 onion thrips/leaf). Although the diamond silver mulch 

with a pesticide program reduced onion thrips (0.5 onion thrips/leaf) below the action threshold, 

the addition of the pesticide program did not provide additional control. In our study, the 

diamond silver mulch was the only mulch that reflected light within the UV range, and since 

pesticides can degrade in the presence of UV light, it’s possible that this led to decreased 

pesticide efficacy (Leach et al. 2017; Lakshmipathy et al. 2024). 

Mulches may directly impact onion thrips; for other thrips species, the irradiation of red 

light in a greenhouse reduced the density of adults (Katai et al. 2015; Shibao and Tanaka 2015; 

Murata et al. 2018a). Although we did not directly irradiate the onions, it’s possible that the 

increase in red light reflecting off the red mulch was enough to deter onion thrips from landing 

on the plants. The diamond silver mulch has a broad range wavelength composition, and it is 

possible that this combined with high reflectiveness reduced thrips colonization and population 

growth (Lopez-Reyes et al. 2022). Interestingly, in the first field experiment, white mulch 

performed similarly to the red and diamond silver mulch but was not effective in reducing onion 

thrips populations in subsequent experiments. In the second field experiment white mulch had 

the greatest onion thrips pressure in our plots (2.2 onion thrips/leaf in the untreated plots; 1.9 

105 

 
 
onion thrips/leaf in the pesticide treated plots); these results are supported by other studies 

although it is unknown why this occurs, it may be because it does not reflect light within the UV 

range (Iglesias et al. 2021; Teulon and Penman 1992). The differences in the effectiveness of the 

white mulch between experiments are potentially due to manufacturing changes, changes in 

latitude and timing, or differences in the length of the experiments. It’s been suggested that white 

mulch degrades throughout the season, or becomes dirty, causing it to appear more yellow which 

attracts thrips (Mutetwa and Mtaita 2014). However, our spectral data suggests that the white 

mulch continued to reflect within the entire spectrum rather than just the yellow range (570 – 580 

nm), therefore it is unlikely that this alone explains the increases in onion thrips populations 

compared to the other mulches. 

In addition to affecting onion thrips populations, mulch color affected plant growth and 

microclimate. Onion plants grown on the red and black mulches had more leaves compared to 

the control plants. Red and black mulches are recommended to increase early season growth 

because they increase the temperature around the plants, and our data supports these findings 

(Job and Bhaker 2018; Csizinszky et al. 1995; Greer and Dole 2003). Interestingly, onions 

growing on white mulch had a similar number of leaves compared to those on the red and black 

mulch, despite a low soil temperature and having about twice as many onion thrips on average. 

In tomatoes, white mulch induces foliage growth and similar patterns are seen in our experiment 

(Decoteau et al. 1989). In contrast to the red and black mulch, white mulch had a lower soil 

temperature compared to the control treatment, so it is unlikely that for the white mulch, 

microclimate changes were the mechanism behind plant growth. Onions grown on the diamond 

silver mulch were the smallest, had fewer leaves than those grown on the red, black, and white 

mulch, and were shorter than onions grown on the red and black mulch. The surface of the 

106 

 
 
 
diamond silver mulch was cooler than the ambient temperature, and the soil temperature was 

lower compared to the other mulches, thus it’s possible that the lower temperatures on the 

diamond silver mulch reduced plant growth (Daymond et al. 1997). Although we were unable to 

measure yield, leaf number and plant height are positively correlated with bulb size (Nourbakhsh 

and Cramer 2022), suggesting that there is a potential for reduced yields when using diamond 

silver mulch. Overall, the effects of mulches on plant growth and microclimate were variable, 

and they did not translate into predictable changes in onion thrips densities, indicating that direct 

rather than indirect mulch effects modulate onion thrips numbers on plants. 

Our no-choice lab experiment also suggested that mulch color directly affects onion 

thrips, especially the immature stages. Although there were no differences in adult populations at 

the end of our lab experiment, there were significant differences in the number of larval onion 

thrips which could be a result of changes in fecundity or survival. Other insects, such as 

predatory pirate bugs (Orius sauteri Poppius; Hemiptera: Anthocoridae), have reduced fertility 

and fecundity and took longer to lay eggs under red (678.5 nm) light, and it’s possible we were 

observing a similar pattern with onion thrips (Wang et al. 2013). In the field, the red and the 

diamond silver mulch had the lowest onion thrips populations, but it is unclear whether that was 

due to physiological changes causing reductions in population growth. Melon thrips, Thrips 

palmi (Thysanoptera: Thripidae), do not exhibit an adverse physiological response when exposed 

to different wavelengths of light, including red light (660 nm), suggesting that responses to light 

are likely species-specific (Murata et al. 2018a). However, melon thrips exhibit behavioral 

changes and disperse away from plants irradiated with red light to search for alternative hosts 

(Murata et al. 2018b). In our lab experiment, alternative hosts were not available, which may 

explain similar adult numbers across treatments in the lab experiment, but they may have spent 

107 

 
 
 
less time on the plants, resulting in lower larval numbers. In the field, it’s possible that adult 

onion thrips either avoided plants in the red and diamond silver mulches, or they landed on 

plants within those treatments but quickly dispersed; in future experiments, we need to determine 

if mulches provide pre- or post-alighting cues. Overall, it is unclear whether the changes in 

populations are due to wavelength-induced physiological or behavioral changes, or a 

combination of both. All the mulch treatments had significantly higher temperatures on the 

mulch surface and in the soil compared to the control, but there were no differences between the 

mulch treatments. This further supports our field experiments indicating that mulches directly 

affect onion thrips populations through wavelength-specific induced changes rather than 

indirectly through changes in the microclimate or host plant quality. 

In conclusion, our results suggest that mulches can be a viable alternative management 

strategy to pesticide programs, and the combination of mulches with a pesticide program can 

provide further onion thrips suppression resulting in reduced reliance on insecticides. 

Furthermore, we found that silver reflective mulches are not equally effective against onion 

thrips, the diamond silver mulch being the most effective, likely due to the differences in 

achromatic (i.e. % reflectiveness) cues. In the field, mulches had inconsistent effects on onion 

thrips populations, plant growth, and microclimate, therefore growers should consider how these 

affect plant growth before selecting a mulch. Finally, wavelength likely had a direct effect on 

onion thrips, especially apparent in a reduction in immature stages in the lab. Overall, our study 

highlighted how multiple IPM tactics, such as chemical and cultural control, can be combined to 

create an integrated pest management program for onion thrips.  

Acknowledgments 

The authors would like to thank the field crew at SWMREC for assisting with plot setup 

108 

 
 
 
and maintenance. Thank you to the undergraduates who assisted with data collection. The 

authors acknowledge that Michigan State University occupies the traditional, ancestral, and 

contemporary lands of the Anishinaabeg- Three Fires Confederacy of Ojibwe, Odawa and 

Potawatomi peoples. We advocate for the sovereignty of Michigan’s 12 federally recognized 

Indian nations, for historic Indigenous communities in Michigan, for the individuals and 

communities who live here now, and those who were forcible removed from their homeland. By 

offering this Land Acknowledgement, we affirm indigenous sovereignty, and we will work to 

hold Michigan State University accountable to the needs of American Indian and Indigenous 

peoples. 

109 

 
 
 
 
LITERATURE CITED 

Adesanya, A. W., T. D. Waters, M. D. Lavine, D. B. Walsh, L. C. Lavine, and F. Zhu. 2020. 
Multiple insecticide resistance in onion thrips populations from Western USA. Pestic. 
Biochem. Physiol. 165: 104553. 

Alam, M.N., M.S. Islma, M.K. Ali, M.A.B. Barkotulla, and S.M.A.T. Khandaker. 2007.  

Aguyoh, J., H. G. Taber, and V. Lawson. 1999. Maturity of fresh-market sweet corn with direct-
seeded plants, transplants, clear plastic mulch, and row cover combinations. HortTechnol. 
9(3): 420-425. 

Andreotti, C., D. Ravaglia, and G. Costa. 2010. Effects of fruit load and reflective mulch on 

phenolic compounds accumulation in nectarine fruit. Eur. J. Hortic. Sci. 75: 53–59. 

Barbosa, P., J. Hines, I. Kaplan, H. Martinson, A. Szczepaniec, and Z. Szendrei. 2009. 

Associational resistance and associational susceptibility: Having right or wrong neighbors. 
Annu. Rev. Ecol. Evol. Syst. 40: 1–20. 

Bates, D., M. Mächler, B. M. Bolker, and S. C. Walker. 2015. Fitting linear mixed-effects 

models using lme4. J. Stat. Softw. 67. 

Bégin, S., S. L. Dubé, and J. Calandriello. 2001. Mulching and Plasticulture, pp. 215–223. In 
Vincent, C., Panneton, B., Fleurat-Lessard, F. (eds.), Phys. Control Methods Plant Prot. 
Springer Berlin Heidelberg, Berlin, Heidelberg. 

Brooks, M. E., K. Kristensen, K. J. van Benthem, A. Magnusson, C. W. Berg, A. Nielsen, H. J. 

Skaug, M. Mächler, and B. M. Bolker. 2017. glmmTMB balances speed and flexibility 
among packages for zero-inflated generalized linear mixed modeling. R J. 9: 378–400. 

Brown, J. E., J. M. Dangler, F. M. Woods, K. M. Tilt, M. D. Henshaw, W. A. Griffey, and M. S. 
West. 1993. Delay in mosaic virus onset and aphid vector reduction in summer squash 
grown on reflective mulches. HortSci 28(9): 895-896. 

Brown, S. L., and J. E. Brown. 2018. Effect of Plastic Mulch Color and Insecticides on Thrips 

Populations and Damage to Tomato. HortTechnol. 2: 208–211. 

Courbier, S., and R. Pierik. 2019. Canopy Light Quality Modulates Stress Responses in Plants. 

iScience 22: 441-452. 

Csizinszky, A. A., D. J. Schuster, and J. E. Polston. 1999. Effect of ultraviolet-reflective mulches 

on tomato yields and on the silverleaf whitefly. HortSci. 34(5): 911-914. 

Csizinszky, A. A., D. J. Schuster, and J. B. Kring. 1995. Color mulches influences yield and 

insect pest populations in tomatoes. J. Am. Soc. Hortic. Sci. 120(5): 778–784. 

110 

 
 
Dănăilă-Guidea, S.M., E. Delian. 2020. An overview on blue light benefits on plants 

physiological performances and on plant products qualities. Sci. Papers. Series B, 
Horticulture. 64(1): 643-652. 

Daymond, A. J., T. R. Wheeler, P. Hadley, R. H. Ellis, and J. I. L. Morison. 1997. The growth, 
development and yield of onion (Allium cepa L.) in response to temperature and CO2. J. 
Hortic. Sci. Biotechnol. 72: 135–145. 

Decoteau, D. R., M. J. Kasperbauer, D. D. Daniels’, and P. G. Hunt. 1988. Plastic Mulch Color 
Effects on Reflected Light and Tomato Plant Growth. Sci. Hortic. 34(3-4): 169-175. 

Decoteau, D. R., M. J. Kasperbauer, and P. G. Hunt. 1989. Mulch Surface Color Affects Yield of 

Fresh-market Tomatoes, J. Amer. Soc. Hort. Sci. 14(2): 216-219. 

Devi, M., and K. Roy. 2017. Comparable study on different coloured sticky traps for catching of 

onion thrips, Thrips tabaci Lindeman. J. Entomol. Zool. Stud. 5: 669–671. 

Diaz, B. M., and A. Fereres. 2007. Ultraviolet-Blocking Materials as a Physical Barrier to 

Control Insect Pests and Plant Pathogens in Protected Crops. Pest Technol. 1(2): 85-95. 

Diaz-Montano, J., M. Fuchs, B. A. Nault, and A. M. Shelton. 2010. Evaluation of onion cultivars 
for resistance to onion thrips (Thysanoptera: Thripidae) and Iris Yellow spot virus. J. Econ. 
Entomol. 103: 925–937. 

Egri, Á., P. Farkas, B. Bernáth, P. M. Guerin, and J. Fail. 2020. Spectral sensitivity of L2 biotype 

in the Thrips tabaci cryptic species complex. J. Insect Physiol. 121. 

Ehler, L. E., and D. G. Bottrell. 2000. The Illusion of Integrated Pest Management, Sci. Technol. 

16(3): 61-64. 

Fournier, F., G. Boivin, and R. K. Stewart. 1995. Effect of Thrips tabaci (Thysanoptera: 

Thripidae) on Yellow Onion Yields and Economic Thresholds for Its Management. J. 
Econ. Entomol. 88: 1401–1407. 

Gordon, G. G., W. G. Foshee, S. T. Reed, J. E. Brown, E. Vinson, and F. M. Woods. 2008. 

Plastic mulches and row covers on growth and production of summer squash. Int. J. Veg. 
Sci. 14: 322–338. 

Greer, L., and J. M. Dole. 2003. Aluminum foil, aluminium-painted, plastic, and degradable 
mulches increase yields and decrease insect-vectored viral diseases of vegetables. 
Horttechnology. 13: 276–284. 

Ham, J. M., G. J. Kluitenberg, and W. J. Lamont. 1993. Optical Properties of Plastic Mulches 

Affect the Field Temperature Regime, J. Amer. Soc. Hort. Sci. 118(2): 1-16. 

111 

 
 
Hothorn, T., F. Bretz, and P. Westfall. 2008. Simultaneous inference in general parametric 

models. Biometrical J. 50(3): 346-363. 

Iglesias, L., M. J. Havey, and B. A. Nault. 2021. Management of onion thrips (Thrips tabaci) in 

organic onion production using multiple IPM tactics. Insects. 12: 1–16. 

Job, M., R. Bhakar. 2018. Field evaluation of plastic mulch film for changes in its mechanical 

properties and retrieval mechanism for its reuse under onion crop. In: Nzihou A, Thomas S, 
Kalarikkal N, Jibin KP (eds.) Re-Use and Recycling of Materials, 1st edn. River Publishers, 
New York, pp 345-355 

Katai, Y., R. Ishikawa, M. Doi, and S. Masui. 2015. Efficacy of Red LED Irradiation for 

Controlling Thrips palmi, in Greenhouse Melon Cultivation. Japanese J. Appl. Entomol. 
Zool. 59: 1–6. 

Kendall, D. M., and J. L. Capinera. 1987. Susceptibility of Onion Growth Stages to Onion Thrips 
(Thysanoptera: Thripidae) Damage and Mechanical Defoliation. Environ. Entomol. 16: 
859–863. 

Lai, P. C., E. A. Grundberg, T. Rusinek, and B. A. Nault. 2024. Evaluation of reflective mulch 
and insect exclusion coverings for allium leafminer (Diptera: Agromyzidae) management 
in allium crops. J. Econ. Entomol. 117: 259–267. 

Lakshmipathy, K., S. Sindhu, A. Singh, S. Chikkaballapur Krishnappa, and C. Duggonahally 

Veeresh. 2024. A review on pesticides degradation by using ultraviolet light treatment in 
agricultural commodities. eFood. 

Larentzaki, E., J. Plate, B. A. Nault, and A. M. Shelton. 2008. Impact of straw mulch on 

populations of onion thrips (Thysanoptera: Thripidae) in onion. J. Econ. Entomol. 101: 
1317–1324. 

Leach, H., J. C. Wise, and R. Isaacs. 2017. Reduced ultraviolet light transmission increases 

insecticide longevity in protected culture raspberry production. Chemosphere. 189: 454–
465. 

Lopez-Reyes, K., K. F. Armstrong, R. W. H. M. Van Tol, D. A. J. Teulon, and M. J. Bok. 2022. 
Colour vision in thrips (Thysanoptera). Philos. Trans. R. Soc. B Biol. Sci. 377(1862). 

Lu, F. M. 1990. Color preference and using silver mulches to control the onion thrips, Thrips 

tabaci Lindeman. Chinese J. Entomol. 10: 337–342. 

Mainali, B. P., and U. T. Lim. 2010. Circular yellow sticky trap with black background enhances 
attraction of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). Appl. 
Entomol. Zool. 45: 207–213. 

112 

 
 
Martin, N. A., P. J. Workman, and R. C. Butler. 2003. Insecticide resistance in onion thrips 
(Thrips tabaci) (Thysanoptera: Thripidae). New Zeal. J. Crop Hortic. Sci. 31: 99–106. 

McIntosh, H., A. Atucha, P. A. Townsend, W. B. Hills, and C. Guédot. 2022. Plastic mulches 

reduce adult and larval populations of Drosophila suzukii in fall-bearing raspberry. J. Pest 
Sci. (2004). 95: 525–536. 

MSU Enviroweather: Michigan State University. 2024. [accessed 2024 January]. 

https://enviroweather.msu.edu/  

Murata, M., T. Hariyama, Y. Yamahama, M. Toyama, and I. Ohta. 2018. Effects of the range of 

light wavelengths on the phototactic behaviour and biological traits in the melon 
thrips,Thrips palmi Karny (Thysanoptera Thripidae). Ethol. Ecol. Evol. 30: 101–113. 

Murata, M., T. Hariyama, Y. Yamahama, M. Toyama, and I. Ohta. 2018. In the presence of red 
light, cucumber and possibly other host plants lose their attractability to the melon thrips 
Thrips palmi (Thysanoptera: Thripidae). Appl. Entomol. Zool. 53: 117–128. 

Mutetwa, M., and T. Mtaita. 2014. Effect of different mulch colors on cucumber production. J. 

Glob. Innov. Agric. Soc. Sci. 2: 178–184. 

Nault, B. A., and A. M. Shelton. 2010. Impact of insecticide efficacy on developing action 

thresholds for pest management: A case study of onion thrips (Thysanoptera: Thripidae) on 
onion. J. Econ. Entomol. 103: 1315–1326. 

Nottingham, L. B., and E. H. Beers. 2020. Management of Pear Psylla (Hemiptera: Psyllidae) 

Using Reflective Plastic Mulch. J. Econ. Entomol. 113: 2840–2849. 

Nourbakhsh, S. S., and C. S. Cramer. 2022. Onion Plant Size Measurements as Predictors for 

Onion Bulb Size. Horticulturae. 8. 

Otani, Y., M. Wakakuwa, and K. Arikawa. 2014. Relationship between Action Spectrum and 

Spectral Sensitivity of Compound Eyes Relating Phototactic Behavior of the Western 
Flower Thrips, Frankliniella occidentalis. Japanese J. Appl. Entomol. Zool. 58: 177–185. 

Otieno, J. A., N. Stukenberg, J. Weller, and H. M. Poehling. 2018. Efficacy of LED-enhanced 

blue sticky traps combined with the synthetic lure Lurem-TR for trapping of western flower 
thrips (Frankliniella occidentalis). J. Pest Sci. (2004). 91: 1301–1314. 

Pedigo, L. 1986. Economic Injury Levels in Theory and Practice. Annu. Rev. Entomol. 31: 341–

368. 

Scott, S. J., P. J. Mcleod, F. W. Montgomery, and C. A. Hander. 1989. Influence of reflective 
mulch on incidence of thrips (Thysanoptera: Thripidae: Phlaeothripidae) in staked 
tomatoes. J. Entomol. Sci. 

113 

 
 
Shelton, A. M., J. Z. Zhao, B. A. Nault, J. Plate, F. R. Musser, and E. Larentzaki. 2006. Patterns 

of insecticide resistance in onion thrips (Thysanoptera: Thripidae) in onion fields in New 
York. J. Econ. Entomol. 99: 1798–1804. 

Shibao, M., and H. Tanaka. 2015. The Effects of Eggplants Illuminated by Red LED (Light 

Emitting Diode) on the Population Density of the Melon Thrips, Thirps palmi 
(Thysanoptera: Thripidae). Japanese J. Appl. Entomol. Zool. 59: 7–9. 

Siegwart, M., B. Graillot, C. B. Lopez, S. Besse, M. Bardin, P. C. Nicot, and M. Lopez-Ferber. 

2015. Resistance to bio-insecticides or how to enhance their sustainability: A review. Front. 
Plant Sci. 6: 1–19. 

Sparks, T. C. 2013. Insecticide discovery: An evaluation and analysis. Pestic. Biochem. Physiol. 

107: 8–17. 

Streck, N. A., F. M. Schneider, G. A. Buriol, and A. B. Heldwein. 1995. Effect of polyethylene 

mulches on soil temperature and tomato yield in plastic greenhouse. Sci. Agric. 52: 587–
593. 

Stukenberg, N., M. Pietruska, A. Waldherr, and R. Meyhöfer. 2020. Wavelength-specific 

behavior of the western flower thrips (Frankliniella occidentalis): Evidence for a blue-
green chromatic mechanism. Insects. 11: 1–15. 

Teulon, D. A. J., and D. R. Penman. 1992. Colour preferences of New Zealand thrips 

(Terebrantia: Thysanoptera). New Zeal. Entomol. 15: 8–13. 

Van Toor, R. F., C. M. Till, D. E. James, and D. A. J. Teulon. 2004. Evaluation of UV reflective 
mulches for protection against thrips (Thrips tabaci) in onion (Allium cepa) crops, New 
Zeal. Plant Prot. 

Vernon, R. S., and D. R. Gillespie. 1995. Influence of Trap Shape, Size, and Background Color 
on Captures of Frankliniella occidentalis (Thysanoptera: Thripidae) in a Cucumber 
Greenhouse, J. Econ. Entomol. 

Vincent, C., G. Hallman, B. Panneton, and F. Fleurat-Lessard. 2003. Management of 
Agricultural Insects with Physical Control Methods. Annu. Rev. Entomol. 

Waiganjo, G. M., and M. Afr. 2008. Effects of weather on thrips population dynamics and its 

implications on the thrips pest management. J. Hort. Sci. 

Walker, W.F. 1974. Responses of selected Thysanoptera to colored surfaces. Envi. Entomol. 

3(2):295-304. 

Wang, S., X. L. Tan, J. P. Michaud, F. Zhang, and X. Guo. 2013. Light intensity and wavelength 
influence development, reproduction and locomotor activity in the predatory flower bug 
Orius sauteri (Poppius) (Hemiptera: Anthocoridae). BioControl. 58: 667–674. 

114 

 
 
Westmore, G. W., G. R. Allen, and C. R. Wilson. 2019. Colour preference and potato cultivar 
oviposition choice by onion thrips, Thrips tabaci (Thysanoptera: Thripidae). J. Asia. Pac. 
Entomol. 22: 25–32. 

115 

 
 
 
 
CHAPTER 5: MANAGING INSECT AND PLANT PATHOGEN PESTS WITH 

ORGANIC AND CONVENTIONAL PESTICIDES IN ONION 

Acknowledgement of prior publication 

This chapter is a reprint of an original peer-reviewed article published in Economic 

Entomology in 2023, 116(6). The original article can be found at doi: 10.1093/jee/toad201. This 

an open-access article that allows the article to be downloaded, reused, modified, distributed, 

and/or copied as long as the original creators are credited via citation. 

Abstract 

Onion thrips (Thrips tabaci Lindeman, Thysanoptera: Thripidae) is a significant insect 

pest of onions (Allium cepa L., Asparagales: Amaryllidaceae). In addition to feeding on onion 

foliage, they may spread plant pathogens. Currently, onion thrips and pathogens are managed as 

separate pests with insecticides and fungicides. It may be beneficial to manage these pests 

simultaneously as limiting onion thrips may reduce pathogen damage. We tested combinations of 

bio- and conventional pesticides in a season-long management program in Michigan onion 

fields. From 2020-2022, we counted onion thrips weekly and visually estimated plant foliage 

necrotic damage (%) in experimental plots each year. In 2020, we tested six treatment programs 

including: azadirachtin, spinosad, a copper-based fungicide, azadirachtin + copper-based 

fungicide, spinosad + copper-based fungicide, and an untreated control. The thrips populations 

were not significantly reduced compared to the control, but necrotic damage was reduced 

significantly in spinosad-treated plots. In 2021, we tested a combination of 8 bio- and 

conventional pesticide programs. Compared to the control, the bioinsecticides did not reduce 

onion thrips populations, but the conventional pesticide programs reduced both onion thrips 

numbers and necrotic damage. In 2022, we tested only conventional insecticide programs but 

included three different action thresholds for initiation and applied them with or without a 

116 

 
 
fungicide, for 8 treatments. All insecticide programs reduced onion thrips compared to the 

control, the action threshold did not impact thrips numbers significantly. Overall, the use of 

action thresholds can lead to fewer insecticide applications and lower incidence of leaf damage. 

Introduction 

Overreliance on pesticides in agriculture has numerous negative effects related to public 

health, non-target impacts, and pesticide resistance (Pimentel 2005; Rolim et al. 2020; Serrao et 

al. 2022; Silva et al. 2020). Despite these negative impacts, pesticides continue to be one of the 

most effective tools used in Integrated Pest Management (IPM) to control pests (Reddy 2016), 

and the incorporation of biopesticides into conventional agricultural practices could lead to 

greater sustainability. In organic agriculture, pesticides are limited to those approved by the 

Organic Materials Review Institute (OMRI) and can only be used if all other management 

options have been exhausted (USDA 2023). The sustainable use of pesticides in both 

conventional and organic management systems relies on strategies that limit their use. These 

strategies include the use of action thresholds, a thorough understanding of the biology and 

ecology of the system, the correct timing and dose of applications, and the use of appropriate 

active ingredients for specific pest species (Siegwart et al. 2015). 

The complexities of pest management are exacerbated when different pest species co-

occur and affect each other on the host plant. Management tactics that focus on a single pest may 

compound other pest problems, or in some instances, the suppression of one pest leads to a 

decrease of another. When plant pathogens are transmitted by insect pests, controlling the insect 

may reduce pathogen symptoms because insect feeding can provide entry points for plant 

pathogens (Grode et al. 2017, 2019; Leach et al. 2017; McKenzie et al. 1993). Action thresholds 

developed for one pest may not apply to multiple interacting pests and thresholds may need to be 

117 

 
 
revised to optimize management.  

Farmers are facing new pest management challenges, including the overall rising costs of 

pesticides, partially due to increases in the cost of development of pesticides that favor highly 

selective products, which are safer for non-target organisms (Sparks 2013). Overall, there are 

few active ingredients to control insects, increasing the need to understand the biology of the pest 

complex (Sparks 2013). Prophylactic applications of insecticide are increasingly unsustainable 

and action thresholds are a critical part of many insect management programs (Anon., 2001; 

Leach et al. 2017, 2019; Ternest et al. 2020). Farmers are increasingly interested in incorporating 

IPM tools to reduce reliance on pesticides and delay pest resistance (Iglesias et al. 2021b; Leach 

et al. 2017). Generally, biopesticides are short-lived and more effective against immature than 

adult insects (Golec et al. 2020). If biopesticides are to be adopted more widely in agriculture, 

their efficacy and application timing must be carefully evaluated as they do not perform well 

when insect population pressure is high (Dively et al. 2020). 

Onion thrips (Thrips tabaci Lindeman, Thysanoptera: Thripidae) is a significant insect 

pest of onions, (Allium cepa L., Asparagales: Amaryllidaceae), and if not controlled, can result in 

severe crop loss (Diaz-Montano et al. 2011; Fournier et al. 1995; Gill et al. 2015; Lewis 1991). 

Onion thrips is resistant to several classes of insecticides; rotating active ingredients and using 

action thresholds sustain insecticide efficacy (Adesanya et al. 2020; Diaz-Montano et al. 2011; 

Leach et al. 2019; Martin et al. 2003; Nault and Shelton 2010; Shelton et al. 2006). One of the 

most effective insecticides for onion thrips control is spinetoram (Gill et al. 2015; Moretti et al. 

2019). Onion growers consider it a high priority to maintain its efficacy (Leach et al. 2017, 

2019). Despite efforts to adopt IPM strategies for onion thrips management, insecticides remain 

the cornerstone for management (Devi and Roy 2018; Iglesias et al. 2021a, b; Leach et al. 2017, 

118 

 
 
 
2020, Yadav et al. 2018). Among the bioinsecticides, spinosad is the most effective for onion 

thrips control (Dively et al. 2020; Iglesias et al. 2021a, b; Nault and Hessney 2005) and it has the 

same mode of action as spinetoram (spinosyns). Other biopesticides such as azadirachtin and 

pyrethrin have been tested for onion thrips control with and without adjuvants (Dively et al. 

2020; Iglesias et al. 2021b)  

Onion thrips damage the onion foliage by feeding and transmitting plant pathogens 

(Bhangale and Joi 1983; Dutta et al. 2014; Leach et al. 2017; McKenzie et al. 1993). Two 

important fungal pathogens of onion in Michigan include Colletotrichum coccodes (Wallr) 

(Glomerellales: Glomerellacaea), first identified in 2012 (Rodriguez-Salamanca et al. 2012), and 

Stemphylium vesicarium (E.G. Simmons) (Pleosporales: Pleosporaceae) a destructive pathogen 

of the eastern production region (Hausbeck and Werling 2018; Hay et al. 2022). The relationship 

between facultative onion pathogens and onion thrips has been the focus of various studies 

(Constancio et al. 2022; Grode et al. 2017, 2019; Leach et al. 2020) but the influence of bio- and 

conventional pesticides on onion foliage and yields is not well understood. Managing two 

organisms simultaneously may be complicated by tank mixing insecticides and fungicides which 

may reduce insecticide efficacy (Nault et al. 2013). The action thresholds used to control onion 

thrips (Nault and Shelton 2010) have been developed without considering the interaction 

between thrips and onion plant pathogens. 

The goal of this study was to evaluate the efficacy of bio- and conventional pesticides in 

a season-long program to control multiple onion pests and develop a combined onion thrips and 

Stemphylium leaf blight management pesticide program, with resistance management practices 

in mind. Our first goal was to broaden the insecticide options currently used in onion thrips 

management by testing bioinsecticides. In 2020 we evaluated the efficacy of biopesticide 

119 

 
 
programs by comparing six different treatments. Building off these results in 2021, we then 

compared eight different bio- and conventional pesticide programs side-by-side. We repeated 

some of the biopesticide programs from 2020 and added two new conventional pesticide 

programs to address the differences in the efficacy of bio- and conventional pesticides. The 

conventional pesticide programs we evaluated in 2021 follow the recommended pesticide 

programs but are not appropriate for insecticide resistance management. Therefore, we made the 

decision to change pesticide programs to address the overarching goal of our study. In 2022, we 

tested varying thrips action thresholds of the conventional pesticide program from 2021. We did 

this to reduce the total number of applications of conventional pesticides and allow better 

coherence to insecticide resistance management guidelines. To measure the impact of our 

treatments on onion pests, we counted onion thrips per leaf weekly, and visually estimated leaf 

necrosis to measure foliar health. 

Materials and Methods 

Field Site  

Experiments were conducted on muck soil, previously cropped to celery, from June to 

August from 2020 to 2022 on a commercial conventional onion farm located in Allegan County, 

MI. Onions are rotated to a new field every year and experimental plots were moved to a new 

location within the same farm each year. ‘Bradley’ onions were direct seeded in early April of 

each year on raised plant beds at a density of approximately 625,000 seeds/ha. Each plant bed 

was comprised of 8 rows spaced 0.15 m apart; onions were direct seeded 5 cm apart. 

Fertilization, herbicide application, and irrigation were managed by the grower cooperator, and 

weeds were removed manually to supplement commercial practices. Herbicide treatments were 

applied to the whole field by the grower using a broadcast sprayer prior to experimental 

120 

 
 
applications. Treatment plots (6 m long x 1.5 m wide) were separated by a 0.6 m buffer and 

arranged in a randomized complete block design, with 4 replicates. All pesticides were applied as 

a foliar spray with a CO2 backpack sprayer and a broadcast boom. The boom was equipped with 

three XR8003 flat-fan nozzles (TeeJet Technologies, Wheaton, IL) spaced 45 cm apart, 

calibrated to 241 kPa to deliver 467 L/ha. 

Onion Thrips 

Onion thrips counting began on 8 July 2020, 14 June 2021, and 14 June 2022 and 

included counting all thrips on 10 randomly selected plants per plot from the center 6 rows of the 

beds. Selected plants including the neck of the onion were visually assessed in a non-destructive 

manner for the total number of adult and larval onion thrips. Thrips were counted weekly until 

27 July 2020, 9 August 2021, and 8 August 2022. In addition to recording onion thrips numbers, 

the number of leaves was counted weekly for 20 plants randomly selected from the center 6 rows 

of the field plots. 

Necrotic Plant Tissue  

Necrotic plant tissue was assessed by visually estimating the percentage of necrotic tissue 

(0 – 100%) per plot on 28 July, and 3 and 10 August in 2020; 23 and 30 July and 6 and 17 

August in 2021. In 2022, plots were assessed weekly from 20 June to 29 August, for a total of 10 

assessments except for the first week of August. If there were signs of Stemphylium leaf blight, 

the pathogen was isolated from 50 plants and identified based on conidial morphology 

(Woudenberg et al. 2017). 

Pesticide Treatments 

Treatments in 2020 included: 1) untreated control, 2) azadirachtin (neem oil), 3) spinosad 

(Entrust SC), 4) azadirachtin + copper (Kocide 3000), 5) spinosad + copper, and 6) copper 

121 

 
 
(Table 5.1). Pesticides were applied weekly from 9 July until 4 August, and were tank mixed 

with a nonionic surfactant (Dyne-Amic, 0.05% v/v), for a total of 5 pesticide applications. 

122 

 
 
 
 
Table 5.1: Pesticides used in the onion thrips and onion disease management field experiments, 2020-2022. Group number refers to 
the mode of action of the pesticide. 
Group 
# 
UN 
UN 

Chemical 
type 
Insecticide 
Insecticide 

OMRIa 
certified 
Yes 
Yes 

Year 
applied 
2020 
2021 

Platonix 
Certus Biologicals 

Azadirachtin 
Azadirachtin 

Active ingredient 

7.8 ml/L 
7.8 ml/L 

Manufacturer 

Rate 

Product 
name 
Neem oil 
Neemix 
4.5 
Entrust 
SC 
Kocide 
3000-O 
23 
Movento 
6, 28  Minecto 

5 

Corteva 

DuPont 

Bayer CropScience 
Syngenta 

5 

1 

Corteva 

Pro 
Radiant 
SC 
Lannate 
LV 
Warrior II  Syngenta 
Agri-Mek  Syngenta 
Syngenta 

Corteva 

3 
6 
7, 12  Miravis 

M5 

Adama Agricultural 
Solutions 

Prime 
Bravo 
Weather 
Stik 
Dyne-
Amic 90 
Activator 
90 
Syl-Tac  Wilbur-Ellis 

Helena Chemical 
Company 
Loveland 

Spinosad 

1.1 ml/L 

Insecticide 

Yes 

2020, 2021 

Copper hydroxide 

Spirotetramat 
Abamectin, 
Cyantraniliprole 
Spinetoram 

3.6 ml/L 

0.78 ml/L 
1.5 ml/L 

Bactericide/ 
Fungicide 
Insecticide 
Insecticide 

1.5 ml/L 

Insecticide 

Methomyl 

7.5 ml/L 

Insecticide 

Lambda-cyhalothrin 
Abamectin 
Pydiflumetofen, 
Fludioxonil 
Chlorothalonil 

0.3 ml/L 
0.5 ml/L 
1.8 ml/L 

Insecticide 
Insecticide 
Fungicide 

3.8 ml/L 

Fungicide 

Methylated seed oils 
Organisilicone non-ionic surfactant 
Non-ionic surfactant 

0.05% v/v 

Surfactant 

0.05% v/v 

Surfactant 

Organosilicone surfactant 
Modified vegetable oil concentrate 

0.10 % v/v 

Surfactant 

Yes 

2020, 2021 

No 
No 

No 

No 

No 
No 
No 

No 

No 

No 

No 

2021, 2022 
2021, 2022 

2021, 2022 

2021 

2021 
2021 
2021, 2022 

2021, 2022 

2020 

2021 

2022 

aOMRI: Organic Materials Review Institute 

123 

 
 
 
 
 
 
Treatments in 2021 included: 1) untreated control, 2) azadirachtin (Neemix 4.5), 3) 

spinosad, 4) azadirachtin + copper, 5) spinosad + copper, 6) copper, 7) conventional insecticide 

program + copper (CI + copper), and 8) conventional insecticide and fungicide programs (CI + 

CF). All pesticides were tank-mixed with a nonionic surfactant (Activator 90, 0.05% v/v). 

Conventional insecticide treatments 7 and 8 contained the following applied twice, 7 days apart 

before rotating to the next insecticide: spirotetramat (Movento), abamectin + cyantraniliprole 

(MinectoPro), spinetoram (Radiant SC), methomyl + lambda-cyhalothrin (Lannate LV + Warrior 

II), and a single application of abamectin (Agri-Mek) (Table 5.1). The conventional fungicide 

program consisted of pydiflumetofen + fludioxonil (Miravis Prime) and chlorothalonil (Bravo 

Weather Stik), applied 7 days apart and rotated weekly for 6 weeks, before applying 

chlorothalonil. All pesticide programs began on 15 June and continued until 10 August. 

In 2022, pesticide treatments were applied according to various thrips action thresholds 

and included: 1) untreated control, 2) fungicide only, 3) low threshold + fungicide, 4) moderate 

threshold + fungicide, 5) high threshold + fungicide, 6) low threshold, 7) moderate threshold, 

and 8) high threshold. Pesticides were tank mixed with an organosilicone surfactant (Syl-Tac, 

1% v/v). All programs containing fungicides alternated between pydiflumetofen + fludioxonil 

and chlorothalonil weekly, starting on 5 July. The low action threshold was 0.5 thrips/leaf (6 

applications) and included: spirotetramat, abamectin + cyantraniliprole, and spinetoram; each 

applied twice, 7 days apart. Spirotetramat’s recommended action threshold for onion thrips is 0.6 

onion thrips per leaf, therefore, to test the efficacy of the low threshold and to ensure all 6 

pesticide applications could be applied to the field, we reduced the action threshold to 0.5 onion 

thrips per leaf. The moderate threshold was 0.6 onion thrips/leaf (4 applications) and included 

abamectin + cyantraniliprole and spinetoram; each applied twice, 7 days apart. Abamectin + 

124 

 
 
 
cyantraniliprole is typically the second product used in onion thrips management (applied after 

spirotetramat), however, the moderate threshold did not receive a spirotetramat application, and 

so abamectin + cyantraniliprole was applied using the action threshold commonly recommended 

for spirotetramat. The high threshold was 1.0 thrips/leaf (2 applications) and included spinetoram 

applied 7 days apart. The low, moderate, and high threshold programs began on 5 July, 26 July, 

and 9 August, respectively. 

Data Analysis  

Data from each year were analyzed separately. To determine the effect of treatment on 

onion thrips populations and the estimated necrotic plant tissue, the mean number of onion thrips 

per leaf was log-transformed, and the estimated percent necrotic plant tissue was logit-

transformed to meet the assumptions of an analysis of variance (ANOVA) and compared with 

the ‘lme4’ package (Bates et al. 2015) using treatment as the fixed factor and date and plot as a 

random factor. Tukey’s HSD test (α= 0.05) was used to determine the differences between 

treatment means using the ‘multcomp’ package (v1.4-22; Hothorn, Bretz and Westfall, 2023). 

All analyses were completed in R (R Core Team 2023).  

Results 

2020 

Onion Thrips  

In the control treatment, onion thrips numbers averaged 9.4 per leaf and ranged from 7.6 

to 6.9 onion thrips per leaf in the treated plots. Although numerically different, there were no 

statistically significant differences in onion thrips numbers among the treatments (F = 0.53, df = 

5, 77.49, p-value = 0.76; Figure 5.1A). 

125 

 
 
 
Necrotic Plant Tissue 

In adjacent experimental plots, the first plant with Stemphylium-like conidia was 

observed on 7 July. There was a significant effect of treatment on necrotic damage on 3 August 

2020 (F = 12.33, df = 5, 15, p-value < 0.01, Fig. 5.1B; Fig. S5.1). Compared to the control 

treatment, there was an approximately 20% reduction in necrosis in plots treated with spinosad 

(t-value = 5.73, df = 6, p-value < 0.01) and spinosad + copper (t-value = 6.09, df = 6, p-value < 

0.01). There was no difference among the control, azadirachtin, azadirachtin + copper, and 

copper-only treatments. 

126 

 
 
 
2021 

Onion Thrips  

Onion thrips numbers were significantly different among pesticide treatments (F = 5.34, 

df = 7, 27.85, p-value < 0.01; Fig. 5.2A). Compared to the control (1.4 onion thrips per leaf), 

there was no significant difference in the mean number of onion thrips per leaf in any of the 

biopesticide programs (ranging from 1.0 to 1.5 onion thrips per leaf). The conventional 

insecticide + fungicide program (0.5 onion thrips per leaf) reduced onion thrips numbers by 65% 

when compared to the control (t-value = 4.64, df = 72, p-value < 0.01). There was no statistical 

difference in onion thrips numbers between the conventional insecticide + copper treatment (0.7 

onion thrips per leaf) and the conventional insecticide + fungicide program (t-value = -1.91, df = 

72, p-value = 0.54). 

Necrotic Plant Tissue 

In adjacent experimental plots, the first plant with Stemphylium-like conidia was 

observed on 24 June and the pathogen was isolated and identified from 50 plants. A moderate 

incidence of pink root rot and low incidence (<10%) of anthracnose was also observed in 

adjacent experimental plots. We found that the estimated necrotic damage was significantly 

different among treatments on 17 August 2021 (F = 9.76, df = 7, 21, p-value < 0.01; Fig. 5.2B; 

Fig S5.2). Compared to all treatment programs, the fully conventional (insecticide + fungicide) 

program significantly reduced the amount of necrotic tissue in the field (t-value > 3.84, df = 8, p-

value < 0.02). There were no significant differences in necrotic tissue among the other 

treatments. 

127 

 
 
2022 

Onion Thrips  

Overall, treatment had a significant effect on onion thrips numbers (F = 4.33, df = 7, 21, 

p-value < 0.01; Fig. 5.3A). Treatments with or without fungicides had similar numbers of onion 

thrips throughout the growing season (0.81 onion thrips per leaf vs 0.63 onion thrips per leaf). 

All insecticide-only treatments, regardless of action threshold, reduced onion thrips populations 

by about 54% when compared to the control (1.2 onion thrips per leaf; t-value < -3.44, df = 56, 

128 

 
 
 
p-value < 0.02). When comparing treatments across all insecticide programs, with or without 

fungicide, all of them reduced onion thrips similarly, regardless of the action threshold. 

Necrotic Plant Tissue  

There was a significant effect of treatment on necrotic damage on 29 August (F = 5.93, df 

= 7, 24, p-value < 0.01; Fig. 5.3B, Fig. S5.3). When compared to the control treatment the low 

action threshold + fungicide significantly reduced the amount of necrotic tissue (t-value = 5.2, df 

= 21, p-value < 0.01). Similarly, the low action threshold + fungicide treatment also significantly 

reduced necrotic tissue in the field when compared to the high action threshold without fungicide 

(t-value = -4.14, df = 21, p-value < 0.01). When compared to the control treatment, the moderate 

action threshold without a fungicide and the high action threshold without a fungicide did not 

reduce the amount of necrotic tissue. 

129 

 
 
Discussion 

Our results demonstrated that the bioinsecticides we tested cannot reduce onion thrips 

sufficiently to keep their populations below the commonly used action threshold of 1 thrips/leaf 

(Nault and Shelton 2010) even under different pest pressures observed in 2020 (7-10 thrips/leaf) 

and 2021 (1-1.5 thrips/leaf). We expected the bioinsecticides to perform better in the low insect-

pressure year (2021), but this was not the case. The 2021 growing season had nearly twice as 

much rainfall as 2020 (average rainfall June-August: 18.4 cm = 2020, 34.8 cm = 2021, MSU 

Enviroweather), so bioinsecticides or onion thrips may have washed off the plants. Biopesticides 

130 

 
 
 
are often more susceptible to extreme weather conditions than conventional pesticides (Fenibo et 

al. 2021; Fronk 2022; Gill et al. 2015). Our results represent the best-case scenario for the 

performance of biopesticides: there were 5 and 9 weekly applications in 2020 and 2021, 

respectively. These types of calendar-based applications are not representative of typical organic 

pest management programs, indicating that even these frequent applications were not able to 

provide sufficient thrips control.  

Interestingly, azadirachtin and spinosad performed similarly in both years for thrips 

suppression relative to the control. Based on previous research, we expected that spinosad would 

perform significantly better than azadirachtin for onion thrips suppression (Dively et al. 2020; 

Iglesias et al. 2021a). The reason that spinosad did not perform as expected (Dively et al. 2020) 

is unlikely to be the result of the surfactant used as two different products were used in 2020 and 

2021, and adjuvants were not a significant factor in onion thrips numbers in a previous study 

(Iglesias et al. 2021a). The sensitivity of onion thrips to spinetoram has been evaluated in New 

York due to concerns that thrips are developing resistance to this insecticide (Moretti et al. 

2019). Despite a variation in LC50 levels among different field populations, New York growers 

reported that spinetoram performed as expected. This is supported by spray trial results, 

including our 2022 results which indicate that it remains effective in the field (Moretti et al. 

2019). In Michigan, spinetoram has been used by growers extensively for the past >10 years so 

the lack of efficacy for spinosad could be due to an increase in resistance to spinosyn insecticides 

(Siegwart et al. 2015). It is possible that low levels of resistance are detected when applying the 

bioinsecticide formulation of this insecticide which may have lower longevity and thus efficacy 

in the field than the conventional version. Monitoring onion thrips susceptibility to spinosyns 

using appropriate bioassays should be a focus for geographic regions that rely on these 

131 

 
 
insecticides for onion production (Yannuzzi et al. 2021). 

Copper alone did not reduce the amount of necrotic tissue, but the amount of necrotic 

tissue was lower in spinosad + copper-treated and spinosad-treated plots in 2020. In the case of 

spinosad-treated plots, the average thrips numbers were similar to those in other treatments that 

did not reduce necrotic tissue. We did not count adult and immature thrips separately, but it is 

possible that spinosad was more effective against immature than adult stages, which has been 

observed for some bioinsecticides (Dively et al. 2020). Overall, copper did not contribute to 

reducing necrotic tissue and it is possible that the presence of onion thrips feeding reduced the 

efficacy of copper to control diseases (Stumpf et al. 2021). In 2021, the conventional treatment 

(CI + CF) had lower amounts of necrotic tissue relative to the other treatments. Leaf necrosis and 

thrips action thresholds increased in concert from low to high, in 2022, thus the measure of leaf 

necrosis better predicted our expected thrips performance than average thrips numbers. This may 

have been because we were measuring relatively small differences among treatments that may 

have been masked by the variability in insect numbers on plants but were captured in data that 

reflects cumulative season-long effects. In the future, it will be important to increase sample size 

and reduce variation. 

The conventional insecticide programs significantly reduced the average number of thrips 

in both years below the action threshold, regardless of tank mixing with fungicides. However, 

chlorothalonil can interfere with insecticide efficacy in some instances (Nault et al. 2013). In 

2022, thrips levels were numerically higher when insecticides were applied with rather than 

without a fungicide. In 2022, the conventional fungicide-only treated plots significantly reduced 

necrotic tissue relative to the control, while the average numbers of thrips were similar to the 

untreated plots. This is likely due to the fungicides providing control against common leaf blight 

132 

 
 
pathogens. The different thresholds we tested in 2022 did not significantly influence average 

thrips numbers; insect pressure overall was low in 2022 and our thresholds were relatively 

similar to each other therefore it was difficult to separate these treatments statistically. In the 

future, thresholds that span a larger range should be tested for their efficacy to determine how 

thrips and onion diseases could be managed together effectively.  

In conclusion, our results suggest that biopesticides have low efficacy for controlling 

onion pests and their relatively high cost may hinder their adoption in large-scale agriculture. We 

were not able to conclusively determine in this study if tank mixing of fungicides and 

insecticides lead to reduced amounts of necrotic tissue, but this issue and the different action 

thresholds should be further tested in years when onion thrips pressure is high. In addition, using 

the recommended action threshold is likely to lead to significant savings for growers. In a year 

when onion thrips pressure was low (2022), two insecticide applications were as effective as six 

at managing onion thrips, indicating that a threshold-based management program could 

significantly contribute to reducing economic inputs and insecticide resistance risks (Leach et al. 

2018). Indeed, onion growers who adopted threshold-based onion thrips management reduced 

their insecticide use by 1 to 4 applications leading to appreciable savings (Leach et al. 2018). 

Acknowledgments 

The authors would like to thank our grower cooperators who allowed us access to their 

fields. Many thanks to members of the Hausbeck lab for their help with hand-weeding the fields. 

Thank you to the undergraduates and graduate students who assisted with data collection. This 

work was funded by the Michigan Onion Committee, USDA Specialty Crops Block Grant 

Program and MSU Project GREEEN. The authors acknowledge that Michigan State University 

occupies the traditional, ancestral, and contemporary lands of the Anishinaabeg- Three Fires 

133 

 
 
Confederacy of Ojibwe, Odawa and Potawatomi peoples. We advocate for the sovereignty of 

Michigan’s 12 federally recognized Indian nations, for historic Indigenous communities in 

Michigan, for the individuals and communities who live here now, and those who were forcible 

removed from their homeland. By offering this Land Acknowledgement, we affirm indigenous 

sovereignty, and we will work to hold Michigan State University accountable to the needs of 

American Indian and Indigenous peoples. 

134 

 
 
LITERATURE CITED 

Adesanya, A. W., T. D. Waters, M. D. Lavine, D. B. Walsh, L. C. Lavine, and F. Zhu. 2020. 

Multiple insecticide resistance in onion thrips populations from Western USA. Pestic. 
Biochem. Physiol. 165. 

Anonymous. 2001. Government Accountability Office, Management improvements needed to 
further promote integrated pest management (GAO Publication No. 01–815). U.S. 
Government Printing Office, Washington, D.C. 

Bates, D., M. Maechler, B. Bolker, S. Walker. 2015. Fitting linear mixed-effects models using 

lme4. J. Stat. Softw. 67 (1): 1-48.  

Bhangale, G. T., and M. B. Joi. 1983. Role of thrips in the development of purple blotch of 

onion. J. Maharashtra Agric. Universities. 8: 299–300. 

Constancio, N., D. Higgins, M. Hausbeck, and Z. Szendrei. 2022. Onion thrips (Thysanoptera: 
Thripidae) host plant preference and performance are mediated by a facultative plant 
pathogen of onion. Environ. Entomol. 51: 1158–1165. 

Devi, M. S., and K. Roy. 2018. An integrated approach for management of Thrips tabaci 

Lindeman in rabi onion under Gangetic plains of West Bengal. Int. J. Curr. Microbiol. Appl. 
Sci. 7: 2865–2877. 

Diaz-Montano, J., M. Fuchs, B. A. Nault, J. Fail, and A. M. Shelton. 2011. Onion thrips 

(Thysanoptera: Thripidae): A global pest of increasing concern in onion. J. Econ. Entomol. 
104: 1–13. 

Dively, G. P., T. Patton, L. Barranco, and K. Kulhanek. 2020. Comparative efficacy of common 
active ingredients in organic insecticides against difficult to control insect pests. Insects. 11: 
1–31. 

Dutta, B., A. K. Barman, R. Srinivasan, U. Avci, D. E. Ullman, D. B. Langston, and R. D. 

Gitaitis. 2014. Transmission of Pantoea ananatis and P. agglomerans, causal agents of 
center rot of onion (Allium cepa), by onion thrips (Thrips tabaci) through feces. 
Phytopathology. 104: 812–819. 

Fenibo, E. O., G. N. Ijoma, and T. Matambo. 2021. Biopesticides in sustainable agriculture: a 

critical sustainable development driver governed by green chemistry principles. Front. 
Sustain. Food Syst. 5: 1–6. 

Fournier, F., G. Boivin, and R. K. Stewart. 1995. Effect of Thrips tabaci (Thysanoptera: 

Thripidae) on yellow onion yields and economic thresholds for its management. J. Econ. 
Entomol. 88: 1401–1407. 

135 

 
 
Fronk, L. 2022. Are you using biopesticides? PennState Extension. https://extension.psu.edu/are-

you-using-biopesticides  

Gill, H. K., H. Garg, A. K. Gill, J. L. Gillett-Kaufman, and B. A. Nault. 2015. Onion thrips 

(Thysanoptera: Thripidae) biology, ecology, and management in onion production systems. 
J. Integr. Pest Manag. 6: 1–9. 

Golec, J. R., B. Hoge, and J. F. Walgenbach. 2020. Effect of biopesticides on different 

Tetranychus urticae Koch (Acari: Tetranychidae) life stages. Crop Prot. 128: 105015.  

Grode, A., S. Chen, E. D. Walker, and Z. Szendrei. 2017. Onion Thrips (Thysanoptera: 

Thripidae) feeding promotes infection by Pantoea ananatis in onion. J. Econ. Entomol. 110: 
2301–2307. 

Grode, A. S., E. Brisco-McCann, P. Wiriyajitsonboom, M. K. Hausbeck, and Z. Szendrei. 2019. 
Managing onion thrips can limit bacterial stalk and leaf necrosis in Michigan onion fields. 
Plant Dis. 103: 938–943. 

Hausbeck, M., and B. Werling. 2018. Protect onions against Stemphylium leaf blight. Michigan 
State University Vegetable Extension. https://www.canr.msu.edu/news/protect-onions-
against-stemphylium-leaf-blight  

Hay, F., D. Heck, S. Sharma, A. Klein, C. Hoepting, and S. Pethybridge. 2022. Stemphylium 

Leaf Blight of Onion. Plant Heal. Instr. 22. 

Hothorn, T., F. Bretz, P. Westfall. 2023. Simultaneous inference in general parametric models. 

Biom. J. 50(3): 346-363. 

Iglesias, L., R. L. Groves, B. Bradford, R. S. Harding, and B. A. Nault. 2021a. Evaluating 

combinations of bioinsecticides and adjuvants for managing Thrips tabaci (Thysanoptera: 
Thripidae) in onion production systems. Crop Prot. 142: 105527 

Iglesias, L., M. J. Havey, and B. A. Nault. 2021b. Management of onion thrips (Thrips tabaci) in 

organic onion production using multiple IPM tactics. Insects. 12: 1–16. 

Leach, A., S. Reiners, M. Fuchs, and B. Nault. 2017. Evaluating integrated pest management 

tactics for onion thrips and pathogens they transmit to onion. Agric. Ecosyst. Environ. 250: 
89–101.  

Leach, A. B., C. A. Hoepting, and B. A. Nault. 2019. Grower adoption of insecticide resistance 

management practices increase with extension-based program. Pest Manag. Sci. 75: 515–
526. 

Leach, A., F. Hay, R. Harding, K. C. Damann, and B. Nault. 2020. Relationship between onion 

thrips (Thrips tabaci) and Stemphylium vesicarium in the development of Stemphylium leaf 
blight in onion. Ann. Appl. Biol. 176: 55–64. 

136 

 
 
Lewis, T. 1991. Feeding, flight and dispersal in thrips. Towar. Underst. Thysanoptera. Proc. Int. 

Conf. Thrips. 63–70. 

Martin, N. A., P. J. Workman, and R. C. Butler. 2003. Insecticide resistance in onion thrips 
(Thrips tabaci) (Thysanoptera: Thripidae). New Zeal. J. Crop Hortic. Sci. 31: 99–106. 

McKenzie, C. L., B. Cartwright, M. E. Miller, and J. V. Edelson. 1993. Injury to onions by 

Thrips tabaci (Thysanoptera: Thripidae) and its role in the development of purple blotch. 
Environ. Entomol. 22: 1266–1277. 

Moretti, E. A., R. S. Harding, J. G. Scott, and B. A. Nault. 2019. Monitoring onion thrips 

(Thysanoptera: Thripidae) susceptibility to spinetoram in New York onion fields. J. Econ. 
Entomol. 112: 1493–1497. 

MSU Enviroweather: Michigan State University. Accessed March 2023. 

https://enviroweather.msu.edu/  

Nault, B. A., and M. Lou Hessney. 2005. Onion thrips control in onion. Arthropod Manag. Tests. 

31: 1–2. 

Nault, B. A., and A. M. Shelton. 2010. Impact of insecticide efficacy on developing action 

thresholds for pest management: A case study of onion thrips (Thysanoptera: Thripidae) on 
onion. J. Econ. Entomol. 103: 1315–1326. 

Nault, B. A., C. L. Hsu, and C. A. Hoepting. 2013. Consequences of co-applying insecticides and 
fungicides for managing Thrips tabaci (Thysanoptera: Thripidae) on onion. Pest Manag. 
Sci. 69: 841–849. 

Pimentel, D. 2005. Environmental and economic costs of the application of pesticides primarily 

in the United States. Environ. Dev. Sustain. 7: 229-252. 

R Core Team. 2023. R: A language and environment for statistical computing. R Foundation for 

Statistical Computing. Vienna, Austria. https://www.R-project.org/ 

Reddy, P.P. 2016. Sustainable crop protection under protected cultivation. Singapore: Springer. 

Rodriguez-Salamanca, L.M., T.B. Enzenbacher, M.L. Derie, L.J. du Toit, C. Feng, and M. K. 

Hausbeck. 2012. First report of Colletotrichum coccodes causing leaf and neck anthracnose 
in onions (Allium cepa) in Michigan and the United States. Plant Dis. 96: 769-769. 

Rolim, G. da S., A. Plata-Rueda, L. C. Martínez, G. T. Ribeiro, J. E. Serrão, and J. C. Zanuncio. 

2020. Side effects of Bacillus thuringiensis on the parasitoid Palmistichus elaeisis 
(Hymenoptera: Eulophidae). Ecotoxicol. Environ. Saf. 189: 109978. 

Serrão, J. E., A. Plata-Rueda, L. C. Martínez, and J. C. Zanuncio. 2022. Side-effects of pesticides 

on non-target insects in agriculture: a mini-review. Sci. Nat. 109: 17 

137 

 
 
Shelton, A. M., J. Z. Zhao, B. A. Nault, J. Plate, F. R. Musser, and E. Larentzaki. 2006. Patterns 

of insecticide resistance in onion thrips (Thysanoptera: Thripidae) in onion fields in New 
York. J. Econ. Entomol. 99: 1798–1804. 

Siegwart, M., B. Graillot, C. B. Lopez, S. Besse, M. Bardin, P. C. Nicot, and M. Lopez-Ferber. 

2015. Resistance to bio-insecticides or how to enhance their sustainability: A review. Front. 
Plant Sci. 6: 1–19. 

Silva, W. M., L. C. Martínez, A. Plata-Rueda, J. E. Serrão, and J. C. Zanuncio. 2020. 

Respiration, predatory behavior and prey consumption by Podisus nigrispinus (Heteroptera: 
Pentatomidae) nymphs exposed to some insecticides. Chemosphere. 261: 127720. 

Sparks, T. C. 2013. Insecticide discovery: An evaluation and analysis. Pestic. Biochem. Physiol. 

107: 8–17. 

Stumpf, S., L. Leach, R. Srinivasan, T. Coolong, R. Gitaitis, and B. Dutta. 2021. Foliar chemical 
protection against Pantoea ananatis in onion is negated by thrips feeding. Phytopathology. 
111: 258–267. 

Ternest, J. J., L. L. Ingwell, R. E. Foster, I. Kaplan, and A. Nielsen. 2020. Comparing 

prophylactic versus threshold-based insecticide programs for striped cucumber beetle 
(Coleoptera: Chrysomelidae) management in watermelon. J. Econ. Entomol. 113: 872–881. 

United States Department of Agriculture. Economic Research Service. 2023. National Organic 

Program Standards Code 205.206 (e). (https://www.ams.usda.gov/rules-
regulations/organic). 

Woudenberg, J. H. C., B. Hanse, G. C. M. van Leeuwen, J. Z. Groenewald, and P. W. Crous. 

2017. Stemphylium revisited. Stud. Mycol. 87: 77–103. 

Yadav, M., R. Prasad, P. Kumar, and C. Pandey. 2018. A review on onion thrips and their 
management of bulb crops. J. Pharmacogn. Phytochem. Ctry. 7(1S): 891–896. 

Yannuzzi, I. M., E. A. Moretti, and B. A. Nault. 2021. Comparison of bioassays used to 

determine onion thrips (Thysanoptera: Thripidae) susceptibility to spinetoram. J. Econ. 
Entomol. 114: 2236–2240. 

138 

 
 
 
 
APPENDIX 2: CHAPTER 5 SUPPLEMENTAL MATERIALS 

METHODS: AREA UNDER THE DISEASE PROGRESSION CURVE (AUDPC) 

To compare how the pesticide programs affected the amount of necrotic onion tissue, 

we calculated the area under the disease progress curve (AUDPC) for each year. The AUDPC is 

used to combine multiple observations of the necrotic tissue progression throughout the season to 

compare across treatments using a single value (Jeger and Viljanen-Rollinson 2000). The 

AUDPC values were compared with an ANOVA with treatment as the fixed factor using the 

‘lme4’ package. The ‘multcomp’ package was used for separating treatment means (Tukey’s 

HSD test, α = 0.05). The AUDPC was calculated using the ‘agricolae’ package (v1.3-5; de 

Mendiburu, 2022) in R (R Core Team 2023). 

RESULTS 

In 2020, there was a significant effect of treatment on disease progression (F = 8.03, df 

= 5, 18, p-value < 0.01). Compared to the control, treatments with spinosad (t-value = 4.19, df = 

6, p-value < 0.01) and treatments with spinosad + copper (t-value = 4.48, df = 6, p-value < 0.01), 

significantly reduced disease progression throughout the season. 

There was a significant effect of treatment on disease progression (F = 9.96, df = 7, 24, 

P < 0.01) in 2021. Compared to the control, the conventional insecticide + copper (CI + copper) 

(t-value = 4.79, df = 8, p-value < 0.01) and the combined conventional insecticide and 

conventional fungicide program (CI + CF) (t-value = 6.36, df = 8, p-value < 0.01) significantly 

reduced disease progression throughout the season. There was no difference in disease 

progression between spinosad and conventional insecticide + copper spray programs, but the 

fully conventional (insecticide + fungicide) spray program significantly reduced disease 

progression compared to the spinosad treatment (t-value = 3.23, df = 8, p-value = 0.016). There 

139 

 
 
 
 
 
was no significant difference in disease progression in the conventional insecticide + copper and 

the fully conventional program. 

In 2022, treatment significantly affected disease progression (F = 4.3, df = 7, 24, p-

value < 0.01). Compared to the control treatment, the low action threshold + fungicide 

significantly reduced disease progression throughout the season (t-value = 4.15, df = 14, p-value 

< 0.01). The low action threshold + fungicide also significantly reduced disease progression 

compared to the moderate action threshold without fungicide (t-value = -3.43, df = 14, p-value = 

0.04) and the high action threshold without fungicide (t-value = -4.19, df = 14, p-value < 0.01).  

140 

 
 
 
FIGURES AND FIGURE CAPTIONS 

141 

 
 
 
 
142 

 
 
 
 
 
 
143 

 
 
 
 
 
LITERATURE CITED 

de Mendiburu, F. 2022. Agricolae: Statistical Procedures for Agricultural Research. R package 

version 1.3-5, https://CRAN.R-project.org/package=agricolae 

Jeger, M. J., and S. L. H. Viljanen-Rollinson. 2001. The use of the area under the disease-

progress curve (AUDPC) to assess quantitative disease resistance in crop cultivars. Theor. 
Appl. Genet. 102: 32–40. 

R Core Team. 2023. R: A language and environment for statistical computing. R Foundation for 

Statistical Computing. Vienna, Austria. https://www.R-project.org/ 

144 

 
 
 
 
 
 
CHAPTER 6: CONCLUSIONS AND FUTURE DIRECTIONS 

In this dissertation, I examined insect-plant-pathogen interactions, first investigating how 

Colletotrichum coccodes influences onion thrips host preference and performance, then 

investigating how onion thrips contribute to C. coccodes spread with density dependent and 

independent mechanisms. I tested an integrated pest management (IPM) program to determine 

potential synergistic methods for onion thrips control and established a multiple pest 

management pesticide program to reduce onion thrips and foliar fungal pathogens in the field. 

The occurrence of thrips and facultative pathogens are well documented in the field (Bhangale 

and Joi 1983; Farrar and Davis 1991; McKenzie et al. 1993; Fournier et al. 1995; Fermaud and 

Gaunt 1995; Marullo 1995; Mailhot et al. 2007; Leach et al. 2020), but there is a gap in the 

understanding of how these pests directly influence each other and how these interactions affect 

pest management. My research has begun to fill that gap, providing a better understanding of 

insect-plant-pathogen interactions and potential IPM strategies for multiple pest management. 

In Chapter 2, my research focused on the influence of C. coccodes on onion thrips host 

preference and performance, manipulating host health through artificial damage or infection 

stage (asymptomatic or symptomatic). The effect of host plant infection on preference and 

performance has been documented for obligate pathogens and their insect vectors, and the vector 

manipulation hypothesis (VMH) suggests that obligate pathogens alter vector behavior to 

increase disease spread (Abe et al. 2012; Shrestha et al. 2012; Maris et al. 2004; Daugherty et al. 

2011; Ingwell et al. 2012). This relationship has not been well studied with facultative 

pathogens, such as C. coccodes, despite previous work indicating that powdery mildew 

(Erysiphe polygoni) increases onion thrips survival rate (Yarwood 1943). I determined that 

plants infected with C. coccodes or plants that were artificially injured, were preferred over 

145 

 
 
 
healthy plants or plants that were both infected and artificially injured. Furthermore, onion thrips 

preferred C. coccodes infected plants compared to healthy plants but did not differentiate 

between hosts at different infection stages (asymptomatic vs symptomatic). Finally, onion thrips 

performed best on symptomatic hosts compared to healthy hosts. This chapter demonstrated that 

C. coccodes affects onion thrips preference and performance, indicating that facultative 

pathogens may also manipulate vector behavior. 

Epidemiological theory suggests that the preference for C. coccodes infected hosts will 

directly impact pathogen spread, likely increasing the rate of disease spread (Kingsolver 1987; 

Sisterson 2008). Preference for infected hosts may increase the rate at which onion thrips and C. 

coccodes conidia or mycelia are in contact with one another, thus if onion thrips disperse away 

from these infected plants, they may be moving propagative material to healthy hosts. 

Furthermore, higher reproductive rates and survival on C. coccodes infected onions indicate that 

there is potential for simultaneous pest outbreaks, particularly because these pests already 

cooccur. Increases in survival rate and reproduction may be due to consumption of fungal 

material as an alternative food source, or changes in the metabolic profile due to the infection 

(Yarwood 1943; Medina-Melchor et al. 2022). Future research should focus on determining the 

mechanisms of preference and performance, as better understanding may help disrupt host plant 

selection in the field, providing alternative control methods for onion thrips. 

In Chapter 3, I focused on understanding how onion thrips spread C. coccodes in the lab, 

examining potential density dependent and independent mechanisms. Increasing onion thrips 

populations often correlates with increases in disease spread and severity within the field 

(Yarwood 1943; Grode et al. 2017, 2019; Leach et al. 2020). However, because C. coccodes 

does not rely on an insect vector for dispersal, it is unclear how much onion thrips contribute to 

146 

 
 
 
 
disease spread, and whether environmental conditions alter the rate of disease spread. I 

determined that onion thrips are vectors of C. coccodes, and that temperature, but not relative 

humidity can indirectly alter disease spread. At higher temperatures, onion thrips reproduced 

more rapidly and were more likely to disperse from a C. coccodes inoculated plant to a healthy 

plant, increasing the rate of disease spread in the experiment. 

This chapter provided novel insight into how environmental changes can affect onion 

thrips behavior and reproduction, indirectly affecting disease spread. The controlled conditions 

in the environmental chamber allowed me to better understand the indirect effect, but field-based 

experiments will be necessary to better understand how these patterns change under realistic 

conditions. For example, relative humidity did not affect disease spread in my experiment, but in 

the environmental chamber, airflow and water-splash were reduced. However, in the field, 

relative humidity corresponds with precipitation, and disease can be spread through wind and 

rain-splash, therefore, it is likely that disease spread patterns will change under field conditions 

(Tiberi et al. 2016; Eigenbrode et al. 2018). Understanding the indirect effect of climate on 

pathogen-vector dynamics is important as climate change causes shifts in regional environmental 

conditions (Anderson et al. 2020; Peters et al. 2022). Furthermore, increases in the number of 

onion thrips at high temperatures compared to low temperatures, and the corresponding higher 

disease spread, likely indicates that disease spread is density dependent. These findings, along 

with the previous chapter, suggest that there may be a mutually beneficial relationship between 

onion thrips and C. coccodes, which will have significant impacts on pest management. 

Therefore, the remainder of my research focuses on reducing pest populations in the field. 

In chapter 4, I focused on the comparison of plastic mulches to the grower standard 

pesticide program, and tested onion thrips performance on the mulches in the lab to determine 

147 

 
 
 
 
potential mechanisms. Silver or highly reflective mulches have been used to reduce pest 

populations, with success for aphid, whitefly, spotted-wing drosophila, and pear psylla control in 

field-based studies, but the success has been variable for thrips control (Wolfenbarger and Moore 

1968; Powell and Stofella 1990; Csizinszky et al. 1995, 1999; Nottingham and Beers 2020; 

McIntosh et al. 2021; van Toor et al. 2004; Iglesias et al. 2021). I first tested various colored 

mulches, including 3 different silver mulches. I found that silver mulches performed 

inconsistently, with a certain type of silver mulch outperforming the others. Furthermore, when 

comparing mulches to the standard grower pesticide program, I determined that mulches are a 

viable alternative management strategy, and the addition of a pesticide program to the mulch 

treatments provided synergistic control of onion thrips. Finally, a lab-based performance test 

suggested that mulch color impacts onion thrips directly, likely through wavelength specific 

behavioral changes. 

The results of this chapter provides growers with an effective non-chemical control 

strategy for reducing onion thrips populations. Onion thrips are resistant to many different 

insecticides, therefore having a season long, non-chemical control method is critical to their 

integrated pest management program. Furthermore, it was unclear whether mulches affect pest 

populations directly through behavioral changes, or indirectly through changes in physiology due 

to changes in the microclimate around plants (Bégin et al. 2001; Vincent et al. 2003; Diaz and 

Fereres 2007). The findings from this chapter provide support to suggest that mulches are 

directly altering insect behavior and potentially physiology. It remains unclear whether mulches 

reduced onion thrips populations by being unattractive to onion thrips, reduced population 

growth on certain colors, or if they landed on the least preferred mulches at the same rate as the 

others but then dispersed away afterwards. Future field research could focus on the differences in 

148 

 
 
 
adult and larval onion thrips numbers on each mulch to determine if the population patterns are 

driven by adult color preference or larval survival. 

Chapter 5 focused on testing sustainable chemical control methods for onion thrips and 

foliar fungal pathogens. Onion thrips and foliar fungal pathogens are primarily managed with 

pesticides despite the negative impacts on non-target organisms, and the development of 

pesticide resistance (Pimentel 2005; Rolim et al. 2020; Silva et al. 2020). Pesticides will likely 

remain a critical component of pest management, therefore, it is important that both conventional 

and organic pesticides are used sustainably within the guidelines of resistance management 

(Reddy 2016). I determined that organic pesticides, despite weekly applications, did not reduce 

onion thrips populations compared to the control treatments, but plant necrosis was reduced in 

some treatments. Furthermore, a side-by-side comparison of organic and conventional pesticide 

programs revealed that organic pesticides cannot be used to reduce onion thrips populations or 

necrotic damage, but conventional pesticides reduced both pests simultaneously. I tested various 

action thresholds for the conventional pesticide program to determine whether the number of 

pesticide applications per season can be reduced. I found that using an action threshold did not 

significantly affect onion thrips populations, although the seasonal onion thrips populations were 

lower than expected, which may have made treatment effects difficult to separate. 

In this chapter, organic pesticides were not successful in reducing onion thrips 

populations despite weekly applications. Organic pesticides are expensive in comparison to 

conventional ones, and the low efficacy indicates that organic growers need to consider other 

control methods, like silver or red plastic mulches, to reduce onion thrips and necrotic damage. 

Using the action thresholds for the conventional pesticide program is likely to reduce the amount 

of pesticides applied in the season, as 2 pesticide applications were as effective as 6 when onion 

149 

 
 
 
 
thrips populations were low. Reducing the number of applications throughout the season can lead 

to reduced economic input for growers and a lower risk of resistance development. Future 

research should focus on continuing to test action thresholds in years when onion thrips 

populations and disease pressure are high to determine how these pests can be effectively 

managed together. 

Overall, this dissertation explored insect-plant-pathogen interactions for facultative 

pathogens and economically important insect vectors, and tested IPM programs in the field to 

manage both pests. When considered together, Chapters 2 and 3, suggest that onion thrips and C. 

coccodes exhibit a mutually beneficial relationship. Onion thrips prefer C. coccodes infected 

plants and reproduce at higher rates on these hosts; subsequently, C. coccodes spread appears to 

be density dependent, and higher onion thrips populations increased disease spread. The 

relationship between onion thrips and obligate pathogens is well studied, but this research 

highlights the importance of conducting facultative pathogen studies as well. Chapters 4 and 5 

focused on developing sustainable management practices for onion thrips and foliar fungal 

pathogens. Red and diamond silver plastic mulches without pesticide programs were as effective 

as conventional pesticide programs in managing onion thrips populations below the action 

threshold, and implementing action thresholds reduced the number of pesticide applications 

throughout the season. Grower adoption of these IPM tactics is going to be important for 

sustainable and long-term onion thrips and pathogen management. Overall, future research 

should continue to explore insect-plant-pathogen interactions, particularly for facultative 

pathogens that have been historically overlooked. Many of the experiments in this dissertation 

focused on insect behavior and future work could focus on manipulating these behaviors to 

enhance integrated pest management. 

150 

 
 
 
LITERATURE CITED 

Abe, H., Y. Tomitaka, T. Shimoda, S. Seo, T. Sakurai, S. Kugimiya, S. Tsuda, and M. 

Kobayashi. 2012. Antagonistic plant defense system regulated by phytohormones assists 
interactions among vector insect, thrips and a tospovirus. Plant Cell Physiol. 53: 204–212. 

Anderson, R., P. E. Bayer, and D. Edwards. 2020. Climate change and the need for agricultural 

adaptation. Curr. Opin. Plant Biol. 56: 197–202. 

Bégin, S., S. L. Dubé, and J. Calandriello. 2001. Mulching and Plasticulture, pp. 215–223. In 
Vincent, C., Panneton, B., Fleurat-Lessard, F. (eds.), Phys. Control Methods Plant Prot. 
Springer Berlin Heidelberg, Berlin, Heidelberg. 

Bhangale, G. T., and M. B. Joi. 1983. Role of thrips in the development of purple blotch of 

onion. J. Maharashtra Agric. Univ. 8: 299–300. 

Csizinszky, A. A., D. J. Schuster, and J. E. Polston. 1999. Effect of Ultraviolet-reflective 
Mulches on Tomato Yields and on the Silverleaf Whitefly. HortSci. 34(5): 911-914. 

Csizinszky, A. A., D. J. Schuster, and J. B. Kring. 1995. Color mulches influences yield and 

insect pest populations in tomatoes. J. Am. Soc. Hortic. Sci. 120: 778–784. 

Daugherty, M. P., A. Rashed, R. P. P. Almeida, and T. M. Perring. 2011. Vector preference for 

hosts differing in infection status: Sharpshooter movement and Xylella fastidiosa 
transmission. Ecol. Entomol. 36: 654–662. 

Diaz, B. M., and A. Fereres. 2007. Ultraviolet-blocking materials as a physical barrier to control 

insect pests and plant pathogens in protected crops. Pest Technol. 1(2): 85-95 

Eigenbrode, S. D., N. A. Bosque-Pérez, and T. S. Davis. 2018. Insect-Borne Plant Pathogens and 
Their Vectors: Ecology, Evolution, and Complex Interactions. Annu. Rev. Entomol. 63: 
169–191. 

Farrar, J. J., and R. M. Davis. 1991. Relationships Among Ear Morphology, Western Flower 

Thrips, and Fusarium Ear Rot of Corn. Phytopathology. 81(6): 661-666. 

Fermaud, M., and R. E. Gaunt. 1995. Thrips obscuratus as a potential vector of Botrytis cinerea 

in kiwifruit. Mycol. Res. 99: 267–273. 

Fournier, F., G. Boivin, and R. K. Stewart. 1995. Effect of Thrips tabaci (Thysanoptera: 

Thripidae) on yellow onion yields and economic thresholds for its management. J. Econ. 
Entomol. 88: 1401–1407. 

Grode, A. S., E. Brisco-McCann, P. Wiriyajitsonboom, M. K. Hausbeck, and Z. Szendrei. 2019. 
Managing onion thrips can limit bacterial stalk and leaf necrosis in Michigan onion fields. 
Plant Dis. 103: 938–943. 

151 

 
 
Grode, A., S. Chen, E. D. Walker, and Z. Szendrei. 2017. Onion Thrips (Thysanoptera: 

Thripidae) Feeding Promotes Infection by Pantoea ananatis in Onion. J. Econ. Entomol. 
110: 2301–2307. 

Iglesias, L., M. J. Havey, and B. A. Nault. 2021. Management of onion thrips (Thrips tabaci) in 

organic onion production using multiple IPM tactics. Insects. 12: 1–16. 

Ingwell, L. L., S. D. Eigenbrode, and N. A. Bosque-Pérez. 2012. Plant viruses alter insect 

behavior to enhance their spread. Sci. Rep. 2. 

Kingsolver, J. G. 1987. Mosquito host choice and epidemiology of Malaria. 811–827. 

Leach, A., F. Hay, R. Harding, K. C. Damann, and B. Nault. 2020. Relationship between onion 

thrips (Thrips tabaci) and Stemphylium vesicarium in the development of Stemphylium leaf 
blight in onion. Ann. Appl. Biol. 176: 55–64. 

Mailhot, D. J., J. J. Marois, and D. L. Wright. 2007. Influence of flower thrips on fusarium 

hardlock severity. Plant Dis. 91: 1423–1429. 

Maris, P. C., N. N. Joosten, R. W. Goldbach, and D. Peters. 2004. Tomato spotted wilt virus 

infection improves host suitability for its vector Frankliniella occidentalis. Phytopathology. 
94: 706–711. 

Marullo, R. 1995. Possible Dissemination of Pest Fungi by Thrips. Thrips Biol. Manag. 201–

202. 

McKenzie, C. L., B. Cartwright, M. E. Miller, and J. V. Edelson. 1993. Injury to Onions by 

Thrips tabaci (Thysanoptera: Thripidae) and Its Role in the Development of Purple Blotch. 
Environ. Entomol. 22: 1266–1277. 

Medina-Melchor, D. L., D. H. Zapata-Sarmiento, E. Becerra-Martínez, M. Rodríguez-Monroy, 

L. G. Z. Vallejo, and G. Sepúlveda-Jiménez. 2022. Changes in the metabolomic profiling of 
Allium cepa L. (onion) plants infected with Stemphylium vesicarium. Eur. J. Plant Pathol. 
162: 557–573. 

Nottingham, L. B., and E. H. Beers. 2020. Management of Pear Psylla (Hemiptera: Psyllidae) 

Using Reflective Plastic Mulch. J. Econ. Entomol. 113: 2840–2849. 

Reddy, P.P. 2016. Sustainable crop protection under protected cultivation. Singapore: Springer. 

Peters, J. S., B. A. Aguirre, A. Dipaola, and A. G. Power. 2022. Ecology of Yellow Dwarf 

Viruses in Crops and Grasslands: Interactions in the Context of Climate Change. Annu. 
Rev. Phytopathol. 60: 283–305. 

Pimentel, D. 2005. Environmental and economic costs of the application of pesticides primarily 

in the United States. Environ. Dev. Sustain. 7: 229-252. 

152 

 
 
Powell, C., and P. Stofella. 1990. Endosulfan and silver reflective mulch effects on sweet potato 
whitefly populations and yields of zucchini squash and tomatoes. Proc. Florida State Hortic. 
Soc. 103: 117–119. 

Rolim, G. da S., A. Plata-Rueda, L. C. Martínez, G. T. Ribeiro, J. E. Serrão, and J. C. Zanuncio. 

2020. Side effects of Bacillus thuringiensis on the parasitoid Palmistichus elaeisis 
(Hymenoptera: Eulophidae). Ecotoxicol. Environ. Saf. 189. 

Shrestha, A., R. Srinivasan, D. G. Riley, and A. K. Culbreath. 2012. Direct and indirect effects of 
a thrips-transmitted tospovirus on the preference and fitness of its vector, Frankliniella 
fusca. Entomol. Exp. Appl. 145: 260–271. 

Silva, W. M., L. C. Martínez, A. Plata-Rueda, J. E. Serrão, and J. C. Zanuncio. 2020. 

Respiration, predatory behavior and prey consumption by Podisus nigrispinus (Heteroptera: 
Pentatomidae) nymphs exposed to some insecticides. Chemosphere. 261. 

Sisterson, M. S. 2008. Effects of insect-vector preference for healthy or infected plants on 

pathogen spread: Insights from a model. J. Econ. Entomol. 101: 1–8. 

Tiberi, R., T. Panzavolta, M. Bracalini, A. Ragazzi, B. Ginetti, S. Moricca, R. Tiberi, T. 
Panzavolta, M. Bracalini, A. Ragazzi, B. Ginetti, and S. Moricca. 2016. Interactions 
between insects and fungal pathogens of forest and ornamental trees. Ital. J. Mycol. 45: 54–
65. 

Van Toor, R. F., C. M. Till, D. E. James, and D. A. J. Teulon. 2004. Evaluation of UV reflective 
mulches for protection against thrips (Thrips tabaci) in onion (Allium cepa) crops, New 
Zeal. Plant Prot. 

Vincent, C., G. Hallman, B. Panneton, and F. Fleurat-Lessard. 2003. Management of 

Agricultural Insects with Physical Control Methods. Annu. Rev. Entomol. 48(1): 261-281. 

Yarwood, C. E. 1943. Association of Thrips with Powdery Mildews. Mycologia. 35: 189–191. 

153 

 
 
 
 
APPENDIX 3: VOUCHER SPECIMEN RECORD 

RECORD OF DEPOSITION OF VOUCHER SPECIMENS 

The specimens listed below have been deposited in the named museum as samples of those 
species or other taxa, which were used in this research. Voucher recognition labels bearing the 
voucher number have been attached or included in fluid preserved specimens. 

Voucher Number: 2024-04 

Author and Title of thesis: 
Author: Natalie Constancio 
Title: Integrated pest management of onion thrips and foliar fungal pathogens in onions 

Museum(s) where deposited: 
Albert J. Cook Arthropod Research Collection, Michigan State University (MSU) 

Specimens:  

Table S.1: Voucher specimens deposited at the Albert J. Cook Arthropod Research Collection 
(Michigan State University).  

Family 

Genus-Species 

Life Stage   Quantity 

Preservation 

Thripidae 

Thrips tabaci   

Adult   

10 

ethanol 

154