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sones on THE LIFE HISTORY AND “ECOLOGY OF— ~
° cursaeau ‘sn‘p. OCCURRING In ‘
; MICHIGAN corroutAILs wm—I-

Ti ‘ SYSTEMATIC STUDIES ON CUTE‘REBRINE'LARVAE .FRQM' °
I OTHER MAMM 1 ALS " ‘

I MisfwmmdPh.-D.

I MICHIGAN STATE UNIVERSITY

' Rudolph Joup‘h Boisvanua
1.955

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This is to certify that the

thesis entitled

"Studies on the life history and ecology of
Cuterebra sop. occurring in Hichigan cottontails
with systematic studies on cuterebrine larvae

from other mammals."

 

presented by

Rudolph Joseph Boisvenue

has been accepted towards fulfillment
of the requirements for

_Eh.D_._ degree in _Mic;nobj_ology
and Public Health

 

STUDIES on THE LIFE HISTORY AND sconce: or CUTEREBRA SPP.
OCCURRING IN MICHIGAN COTTONTAILS WlTH SYSTEMATIC
SIUDIES ON CUTEREBRINE LARVAE FROM OTHER MAMMALS

3!
Rudolph Joseph Boiavenue

A THESIS

Submitted to the School for Advanced Graduate Studies of
Michigan State University of Agriculture and Applied Science
in partial fulfillment of the requirements
for the degree of
DOCTOR OF PHILOSOPHY
Department of Microbiology and Public Health

1955

DEDICATION

The author wishes to dedicate this thesis
to those dear ones, Michelle and Mary Denise,
and to Mrs. Mary Boisvenue whose belief led to

this accomplishment.

 

8'!)

 

v.albii
I
, I -

ACKNOWLEDGEMENTS

The author wishes to convey his appreciation to Dr.
Hilliam.D. Lindquist of the Department of Microbiology and
Public Health whose guidance and constructive eriticism.made
this project possible.

Sincere thanks are extended to Dr. D. Douglass, Game
Division, Michigan Department of ConServation for supplying
the opportunity to collect wild mammals. To the following
persons thanks are also expressed: Dr. William.Jellison,
Rocky Mountain Laboratory, U. 8. Public Health Service, Hamil-
. ton, Montana, who generously contributed literature and speci-
mens for this work; Dr. Curtis Sabrosky, U. S. Department of
Agriculture, for his identifications of adult cuterebrid flies;
Dr. Roland Fischer, Department of Entomology, Michigan State
University, for his help in taxonomdc matters; Dr. Elton Han-
sens, Department of Entomology, Rutgers University, for his
specimens; Mr. Aelred Geis, graduate student in Fisheries and
Wildlife, Michigan State University, who furnished bot material
from ccttontails captured at the Kellogg Bird Sanctuary and
the Kellogg Forest near Battle Creek, Michigan; Mr. William
Youatt, Bacteriologist, Michigan Department of Conservation,
whose photographs enhanced the presentation of this work; Mr.
Glenn Bowers, Pennsylvania Department of conservation for his
.bot examples; and to Michigan State University veterinary

students for their Cuterebra specimens.

Acknowledgement is also due Michigan State University
for providing the author with the opportunity to make these

studies.

TABLE OF CONTENTS

I. INTRODUCTION AND HISTORICAL REVIEW
A. Life History . . . . . . . .

B. Ecology . . . . . . . . . .

C. Systematics . . . . . . . . .

II. MATERIAL AND METHODS . . . . . . .
A. Field Studies . . . . . . . .

B. Laboratory Studies . . . . . .

C. Systematic Studies . . . . . .

III. RESULTS . . . . . . . . . .
A. Life History . . . . . . . . .

l. Obvious Appearance of Larvae

in Their Hosts

2. Anatomical Locations of Larvae Infections .

3. Field Pupation Experiments
h. Field Notes on Pupation

5. Autopsies . . . . . . . .
6. Duration of Instars . . .
7. Air Hole Diameters . . .
8. Mode of Infection Studies

BQE30108y eeeeeeeeee

1. Incidence of Infected Rabbits on Mason Game

Farm 0 O O O O O O O O O

2. Incidence of Infected Rabbits on Kellogg
Station 0 O O O O O O O O O O O O O O O O O

3. Incidence of Larvae in Sex of Rabbits . . .

. 10
. 18
. 19

. 25
. 27
. 27
. 27
. 28
. 28
. 29
. 30
. 31
. 31
. 32

h.
5.
6.
7.
8.
9.
10.
11.

TABLE OF CONTENTS (Cont.)

Page

Seasonal Periodicity of First Stage Larvae . . 58

Seasonal Periodicity of Second Stage Larvae
Seasonal Periodicity of Third Stage Larvae .
Studies on Adult Flies . . . . . . . . . . .
Fly-baiting Experiment . . . . . . . . . . .
Laboratory Pupation Experiments . . . . . .
Factors of Soil and Vegetation on Cuterebra

Effects of Larvae on Cottontails . . . . . .

C. Systematic Studies . . . . . . . . . . . . . .

1.

2.

3.

h.

S.
6.

7.

Definition Of {Instara e e e e e e e e e e e

Hosts smdiod ‘ C C O O O O O O O O O O O O O

cutOPObra in F6118 domeatlca e e e e e e e e

a. Q; horripilum. . . . . . . . . . . . . .
b..Q. buccata . . . . . . . . . . . . . .
Cuterebra in.§gni§_familiaris . . . . . . .
a. Q, buccata . . . . . . . . . . . . . .
Cuterebra in £2225,californicugIQgggrticola
Cuterebra in'Perogyscus leucopus . . . . . .
a.‘Q. fontinella . . . . . . . . . . . . .
Cuterebra in Sylvilggus fgggidanug mallurus.
a. Q, buccata . . . . . . . . . . . . . .
Cuterebra in Sylvilagug floridanus mearnsii.
a..Q, horripilum; . . . . . . . . . . . . .

b._§, buccata . . . . . . . . . . . . .

ii

60
61
62
63
6h
65
67
73
73
77
80
80
91
95
95
98
108
108
117
117
119
119
120

TABLE OF CONTENTS (Cont.)
. Page
IV. DISCUSSION . . . . . . . . . . . . . . . . . . 123
A. Life History . . . . . . . . . . . . . . . . 123

B. Ecology . 125

C. Systematics . . . . . . . . . . . . . . . . . 131
V. SUMMARY . . . . . . . . . . . . . . . . . . . . . 1&9
BIBLIOGRAPHY . . . . . . . . . . . . . . . . . ... . . 153
APPENDIX . . . . . . . . . . . . . . . . . . . . . 160

iii

 

1 I In I I- I I] ll: l i I'll. i.

LIST OF FIGURES

 

 

 

 

 

 

 

 

FIGURE Page
1. Effects of Cuterebra on Nevada jack-rabbits 72
2. First stage larva of Cuterebra 7h
3. Second stage larva of Cuterebra 75
h. Third stage larva of Cuterebra 76
5. Posterior Spiracular plates of a mature Q, fontinella
larva 78
6. Posterior spiracles of a second stage 9, fontinella
larva 79
7. Multipointed spines of a‘Q, horripilum first stage
larva 81
8. Posterior spiracular plates of a first stage larva
Q. horripilum 8h.
9. Cephalopharyngeal apparatus from a first instar of
9.- haaaiailm - 35
10. Cephalopharyngeal apparatus from a second stage
larva of‘Q, horripilum. 88
11. Posterior spiracular plates of a second stage larva
of.§. horripilum 90
12. Posterior spiracular plates of a third stage larva
of 2. horripilum. 92
13. Cephalopharyngeal apparatus from a.g, horripilum third
stage larva 93
1h. Posterior spiracular plates of a third stage larva
of E. buccata 9h
15. Cephalopharyngeal apparatus of a‘g. buccata third
stage larva 96
16. Cephalopharyngeal apparatus of a E, buccata second
stage larva 97
17. Posterior spiracular plates of a second stage larva
of g. buccatg 99

iv

18.

19.

20.

21.

22.

23.

25.
26.

27.

28.

29.

30.

31.

32.

33.

3h-

Posterior spiracular plates of a second stage larva
obtained frmm Nevada jack-rabbits

Cephalopharyngeal apparatus of a second stage larva

from.Nevada jack-rabbits

Posterior spiracular plates of a third stage larva

from Nevada Jack-rabbits

Cephalopharyngeal apparatus
from.Nevada jack-rabbits

of

Cephalopharyngeal apparatus of

of _C_. fontine lla

Multipointed spines of a third

fontinella

Cephalopharyngeal apparatus

of

A pupal case of E, fontinella

Posterior spiracular plates
of C. horripilum

Cephalopharyngeal apparatus
of Q. horripilum

 

Posterior spiracular plates
of E. buccata

Cephalopharyngeal apparatus
°f£~ 12112232

Posterior spiracular plates
of g, horripilum

Cephalopharyngeal apparatus
of Q, horripilum

Posterior spiracular plates
of the Nevada jack-rabbits

Cephalopharyngeal apparatus
of the Nevada jack-rabbits

Posterior spiracular plates
of 2. fontine 11a

of

of

of

of

of

of

of

of

of

a third stage larva

a first stage larva

stage larva of E.

a is fontine 113

 

a first instar larva

a first instar larva

a second instar

a second instar

a second instar

a second instar

a second instar

a second instar

a second instar

larva

larva

larva

larva

larva

larva

larva

102

103

106

107

111

112
115
116

E

E

E

E E

E

35.

36.

37.

38.

39.

#0.

I11.

Posterior spiracular plates
of §:.horripilum

 

Cephalopharyngeal apparatus
instar of E. horripihmn

 

Posterior spiracular plates
of Q. buccata
Cephalopharyngeal apparatus
instar of.Q. buccata

Posterior spiracular plates
from.the Nevada Jack-rabbit

Cephalopharyngeal apparatus
from.the Nevada jack-rabbit

Posterior spiracular plates
larva of 9, fontinella

Cephalopharyngeal apparatus

larva of E. fontinella

vi

of a mature third instar

from a mature third

of a mature third instar

from a mature third

of a third stage larva

of a third stage larva

of a mature third stage

of a mature third stage

1116
1116
1116
1117
1117
117

1h?

LIST OF GRAPHS

GRAPH

1.
2.

3.
h.

S.

6.

7.

8.

9.

Mason Trapping Record,

Incidence of Cuterebra
Cottontails, 19537

Mason Trapping Record,

Incidence of Cuterebra

 

Rabbits, 1951;‘

Incidence of Cuterebra
Cottontails, 19§l

Incidence of Cuterebra
Cottontails, l9 2

Incidence of Cuterebra
Cottontails, l9 3

Incidence of Cuterebra

Cottontails firom 19§l

1953

Larvae in Mason Game Farm

195a

Larvae in Mason Game Farm
Larvae in Kellogg Station
Larvae in Kellogg Station
Larvae in Kellogg Station

Larvae in Southern Michigan
to 1953

Growth Curve of Kellogg Station Cottontails, 1951

vii

Page
38

no
u3

#5
us
52
53

57
68

TABLE

I.
II.
III.
IV.
V.
VI.
VII.

VIII.

X.
5:1.
XII.
XIII.

XIV.

XV.

LIST OF TABLES

Page

A Laboratory Air Hole Diameter Study on Phases
of Third Instar Cuterebra, 1953. . . . . . . . . . . 33

A Laboratory Air Hele Diameter Study on Phases
of Third Instar Cgtezebga, 195h . . . . . 3h

A Laboratory Air Hole Diameter Study on Phases
of Third Instar Cuterebra, l95h . . . . . . 35

Incidence of Cuterebra Larvae in Mason Game Farm

COttontaila, 19§3 e e e e e e e LL]-

Incidence Of Cuterebra Larvae in Mason Game Farm
Cottontails, l . . . . . . . h2

Number of Marbles Per Infected Rabbit Mason.Game
Farm, 1953 . . . . I16

Number of Marbles Per Infected Rabbit Mason Game
Pam, 195“. e e e e e ”.7

Incidence of Cuterebra Larvae in Kellogg Station
Cottontails, 19 . . . . h9

Incidence of Cuterebra Larvae in Kellogg Station

COttontailsg 19;: e e e e e e e e e 5].

Incidence of Cuterebra Larvae in Kellogg Station

Cottontails,—95*“ 3 . . . SII

Number of Marbles Per Infected Rabbit Kellogg
Station, 1951, 1952 . . . . . . 56

Incidence of Cuterebra Larvae in Sex of Mason
Cottontails, 19;} and 195‘... e e e e e e e e e e 59

Weight Measurements on a Cuterebra Infected Juvenile
Cottontail Confined in the Laboratory, 195h . . . . 69

A Comparison of First Instar Cuterebra Species
Characteristics With Measurements Obtained by
Taxonomloworkers..................131.|.

A.Comparison of Second Instar Cuterebra Species
Characteristics With Measurements Obtained by
Taxonomic Workers

eeeeeeeeeeeeeeeee135

viii

TABLE Page
XVI. A Comparison of Third Instar Cuterebra Species

Characteristics Hith Measurements Ubtained by
Tuonomicworkers eeeeeeeeeeeeeee136

ix

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1r.

I

 

INTRODUCTION AND HISTORICAL REVIEN

The purpose of this study was (1) to investigate the
phases of the life history of Cuterebra sp. as they occur
under natural conditions, (2) to elucidate the ecology of
the cuterebrid flies in relation to vegetation, soil and
host, the Michigan cottontail, Sylvilaggs floridanus
mearnsii, and (3) to clarify the systematics of cuterebrine

larvae collected from certain mammals.

A. LIFE HISTORY

At present the biological knowledge of the Cuterebra
species is rather scant. The paucity of material is noticed
in the problem of the life cycle, which Cameron (1926)
states may be attributed to the shy habits of the cuterebrid
adult flies. Reviews by Hadwen (1915), Townsend (1917),
Crawley (1923) suggest that the possible mode of infection
in carnivores may be thrOugh the ingestion of rodent car-
casses, having immature larvae. From the stomach these lar-
vae migrate to the skin in the new host and there complete
their development. Parker and Wells (1919) offered partial
evidence in support of this idea by finding subcutaneous in-
festations in prairie dogs orally given young larvae. Hall
(1925) states that this mode of infection might explain

the finding of a last stage cuterebrid larva in the nostrils
of a cat. The cat in the process of feeding on an infected
carcass may have had a ”grub" entering the nostrils. Evi-
dence of carnivores swallowing cuterebrid larvae was presented
by the above author in cases of late stage larvae found in the
stomach and fecal samples of carnivores.

Other contingencies mentioned in the papers of Cameron
(1355. £13.), 3.11 (133. 21.3.), Dalmat (19113) are that the
infestation of the carnivores may be direct, i.e. that the
adult female fly deposits its eggs on the host. Dalmat (122.
gig.) further states that the host licks the eggs off the body
hairs, and swallows the infective eggs. As a modification of
the above possibility, the deposited eggs hatch into first
stage larvae and may penetrate the skin of the host.by means
of strong oral hooks, and burrow into the subcutis. The mor-
phology of the egg reflects the possibility of a strong attach-
ment to the hairs of the heat by a glutinant ventral groove
(Hadwen, 122..gi§.; Parker g§.gl., loc. cit.).

Townsend (1935) offered the probability that the eggs
are laid on feed plants of the host and when the animal
feeds, the eggs are ingested. Once in the stomach of the
host, the eggs excyst releasing the active larvae, which
through some unknown migration route reach the subcutaneous
region of the body.

The fact that hosts are highly infested in the throat

and neck regions may be explained by their frequent brushing

against vegetation.having first stage larvae (Allison, 1953).

Townsend (1915) suggested that the eggs are probably ,
deposited in burrows or runways of the rodents. Adult cutere-
brids, according to Chandler (l9h9), lay great quantities of
eggs in areas rabbits frequent. Beamer's observation (1950)
supports this evidence, in that female flies were seen laying
eggs in.the runways of the host.

Townsend (1935) observed that cuterebrid flies fre-
quented rockpiles, brushpiles, and rock recesses that could
be rodent habitats. Dalmat (19h3) conjectured on the above
observation that it seemed likely to find cuterebrine eggs
deposited in nests and burrows used by hosts. Consequently,
hatched first stage larvae would probably come in contact
with the habitant host, attach to it, wander and burrow in
when a suitable site was reached. In the subcutis they would
continue developing to mature larvae. Beamer and associates
(l9h3) supported the above conjecture by discovering eggs
around the burrows of pack rats. The eggs were found ran-
domly on logs, under stones, sticks in or over the entrance
of the nests. Hall (1925) offered the possibility of pre-
natal infection, which is demonstrated in the case of para-
sites, having larvae that wander through the host tissues.
That author stated further that there is no evidence of this

migration as yet, in Cuterebra species. This hypothesis
might clarify some questions on early infections of nursing

animals cited by Dalmmt (loc. cit.).

Thus from the data on the life cycle of Cuterebra sp.
there appears to be two hypotheses; the direct ingestion
'mode,and the skin penetration mode of infection.

Observations by Dalmat (19113) on the oviposition of
female cuterebrid flies showed that numerous eggs were laid
("more than 1000 eggs have been taken from.one Outagebra").
Measurements of the eggs resulted in an average length and
width of l.h mm. and 0.3 mm. respectively. A total time of
oviposition for hSO eggs was hS hours. The female fly exp
hibited a sporadic egg-laying two days after it had emerged.
The pattern of the deposited eggs on a twig revealed eggs
singly-laid in a row. Characteristics of the eggs such as a
very heavy chorion, a ventral groove, a sticky substance on
the posterior end, and an operculated anterior end were re-
corded by the above author. These features corroborated
Hadwen's findings (1915). Dalmat (122.1213.) goes on to
relate that oviposition probably does not happen on the
host owing to the numerous eggs laid. Thus a high mortality
rate would result because of the reduced number of first
stage larvae reaching a suitable host. Parker and Wells
(1919) determined the longevity of collected viable eggs
to be six months.

Whether the operculum of the egg is Opened by the fric-
tion and moisture in the mouth (Townsend, 1935) or if the

larvae emerge from eggs without mechanical aid (Moilliet,

l9h3; Ferris, 1920), the first stage larvae actively leave
the eggs to establish themselves in the host. Moilliet
(122. gig.) retained one unfed larva for ten days.

With the establishment of the first stage larva in the
host, Knipling and Brody (19h0) found that a molting period
follows at the end of which a Second stage larva evolves.

The metamorphosis to the third stage larva is proceeded by

an intermediate melting period. Mature larvae are usually
defined as those found in the late third stage (Dalmat,
l9h2). After some time the mature larva drops from the

host, burrows in the ground, and changes into a pupal stage
(Ryckman, 1953). The pupa overwinters in the soil, according
to Dalmat (lgg.‘gi§.) and in late spring or early summer,
depending on date of pupation, an adult fly emerges from

the puparium. In southern Georgia, Knipling and Brody

(123. gig.) found that two generations a year may exist.

In the investigation of the cuterebrid parasites a
problem confronting workers is that of the length of larval
development in the host. Reviews by Vorhies and Taylor (19h0),
Moilliet (l9h3), relate that the larval period of rodent I
Cuterebra species is from three to four weeks in duration.
These observations compared with those of Scott and Snead
(l9h2) in their finding of a larval infection period as ap-
proximately one month. One observation suggests that the
developmental period of cuterebrid species is relatively

much shorter than those of Hypoderma and Gastergphilus

(Knipling 2§_gl., 19h0). These authors stated further that
the duration of the secondstage larvae was determined to be
h to 5 days. This duration began at the appearance of an
Opening in the host's skin until the molt to the third stage.
The third or mature stage required 10 days.. No specific data
could be found on the time of the first stage larvae to es-
tablish itself in the host or its melting to the second instar.
Parker and'wells (1919) however, reported that the first ap-
pearance of "grubs" under the skin was 9 to 12 days after
oral infection. They go on to say that the skin was punc—
tured two dayslater. At no point in their experimental
descriptions do they state the stage of these ”grubs". The
valid interpretation of their experiments as to the duration
of the first stage larvae cannot be Obtained.

. Under laboratory conditions, Parker and Wells (123.
21;.) found the pupal period to range between h? and 173
days. Hewever, Meilliot(lgg. gig.) obtained a pupal period
of 11 1/2 months in an outdoor insectary.- Another example
of a natural pupal period was from.8 to 10 1/2 months (Dal-
mat, l9h3). The above workers claim that the large range
of the pupal stage may be due to the existing moisture,
temperature, amount of food stored in the puparia, and the
time of year in which the pupation happened. Cases of a
short pupal period may be during the mid-summer and a.long
example if started in the fall or winter.

B. ECOLOGY

As stated above the pupation of Cuterebra species may
depend on environmental factors. These factors consequently
could give rise to one or two generations a year, owing to
the geOgraphic location of cuterebrid flies. One approach
to the problem of environmental factors has been the signi-
ficance of soil in relation to pupation. Experiments carried
out by Haugen (l9h2), Knipling and Brody (l9h0) employed
sand as the soil surrounding the puparium. Methods employed
by other workers (Parker 23.21., 1919 ; Cameron, 1926; Del-
mat, 19LI2) did not classify the soil used in artificial
pupation. The need for further investigation in this respect
is warranted due to the paucity of specific data.

The factor of temperature in artificial pupation is
another problem.deserving attention. Knipling and Brody
(192. git.) state "after the larvae had pupated, the jars
in which they lay were placed in a cool closet.” Many pupa-
tion experiments were carried out by workers without relating
the conditions conducive to emergence. One substantial
record of soil temperature, taken during pupation, was be-
tween 26 to hl° F (Dalmat, l9h3). This temperature was re-
flective of a situation wherein the pupal jars were kept in
an outdoor subterranean basement during the winter.

Moisture, according to Johnson (1930) is believed to

be the prime factor necessary for pupation. He reported in

his study on the rearing of Cuterebra pupae that water was
added intermittently to insure a moist condition. Others
state that no water was added at any time prior to emergence
(Greene, 1935; Hall, 1925)., The different methods undertaken
for pupation have created a need for further study on the
factors affecting pupation.

vegetation as an agent in the ecology of Cuterebrg
species has been mentioned in papers dealing with the life
history of these flies. Townsend (1935) stated that eggs
are laid on bark of trees and shrubs or stems of herbaceous
plants which the hosts visit for feeding. Beamer (1950) ob-
served an adult female laying eggs on the tips of celery
grass near a rabbit runway.

Pertinent to the habitat of the adult flies, Cameron
(1926) offered the information that the flies preferred dark
situations, exmmples of which were outbuildings, summer kit-
chens and ground burrows of rodents. The females of Cutere-
bgg, according to Townsend (129. gig.) are frequently encoun-
tered_flying close to the ground in open woodlands or perched
on herbage in wooded lowlands. .

Adult flies have been observed in flight from June to
September (Cameron, 129..gi§.)._ cuterebrid larvae were found
by Knipling and Brody (129..gi§.) in cottontails during June
and November. However, records from.the Kellogg Station show
that hunters have reported the warbles in rabbits during other
months of the year. Harkema (1936) discovered in his findings

of Cuterebra infestations in North Carolina cottontails that
the percenteg? of hosts infested were highest in October,
June and January respectively. e

Curran (193k) indicated that these flies have been reared
from.rabbits, rats, mice and squirrels. Occasionally, they
invade such animals as the cat and the dog, and even hogs,
cattle, mules, opossum.and man. Knipling and Bruce (1937)
relate that larger animals, pigs, cows and mules, are_not
frequently found infected with cuterebrids and states that
these infections are accidental.
_ f Cuterebrid 1arvae_have been found in various locations
of their hosts.. Examples_of sites recorded were the neck,
back, shoulders, belly, head and scrotum, especially in areas
where the skin was thin. Cameron (1926) discovered that in
the deg larval sites were particularly noted in the scapula-
humeral region. _ ' _

in important problem.arising in the study of the cutere-
brid parasites is the effect of the larvae on their hosts.
These effects range from.no effect to cause of death. Be-
cause of certain species locating in the scrotum.of the
host, Haugen (l9h2) claimed that the cuterebrid larvae may
cause sterility. Scott and Snead (l9h2) found a relationship
between the peak in Cuterebra infections to a definite de-
crease in mouse populations. Gray squirrels in the North
Carolina study of Allison (1953) were greatly affected in‘a

like manner. Of economic importance is Lindquist's study (1937)

10

that Cuterebra species were the main predisposing agent of
primary screworm infections in cottontail rabbits. Knipling and
Bruce (192..gi§.) presented a similar situation in a mule.
These same authors offered a case wherein the direct cause
of death in a pig was due to a cuterebrid larva which was
lodged in the trachea. Juvenile cottontails, have been found
by Bruna (1952) to be greatly debilitated and.weakened so
that secondary effects such as predation or pneumonia may
cause death. “Cameron (193.'gi§.) cited an example of ana-
phylactic-ahock in a dog undergoing extraction of larvae.
During the extraction a larva was accidently crushed under
the skin and shock ensued. Symptoms prevailed for seven
hours and the animal recovered. _ ..

These robust bot flies are restricted to the western
hemisphere. The Appendix offers the distribution ranges,
the localities and bibliographic references of Cuterebra
species concurrently with their hosts. These notes were
summarized from papers of Townsend (l935),Knipling and
Bruce (1937), Hall (1921), and Harkemm (1936).

C. SYSTEMATICS

Townsend (1917) in his synoptic revision of the family
Cuterebridse states "certain species of the older authors
have been misidentified, certain valid species names have

been put in synonymy, certain synonyms have been used as

11

valid names, and certain aberrant specimens of old species
have been described as new species." This statement reflects
the confusing early history of the systematics of Cuterebra
species. The subsequent history is still uncertain due to
the ”lumpers" and ”splinters” views on taxonomy. Also the
above author presented a key which separated the genera of
the family. VExmmples of genera were Pseudogametes, Dermatobig,
Bo eria, Hogenhofera and Cuterebra. 4 .
The first reported note on Quterebra was that of Fabricius
(1776) in his reference of Oestrus buccatus. Oestrus was
believed to be the original Cuterebra genus as later recorded
by Brauer (1863). Fabricius' taxonomic description was main-
tained until 1815 when Clark designated it as Cuterebra
purivora. Latreille (1816) changed the species to buccata
which remained unchanged until Wiedemann (1830), through a
misidentification, placed it in the genus Trypoderma. Macquart
(1835) re-established it in itsprOper genus, that of Cutere-
225. This final partition was confirmed by Joly (18h6), and
had held since. An error was noticed by Mik (1895) on the
use of the name ”gutitergbra" in some reviews. Fortunately,
this error was apprehended before confusion reigned again.
Another taxonomic example of unstableness was in the
Cuterebra horripilum species. Clark (123. gig.) in his study
on bots maintained that Cuterebra cuniculi and.§. horripilum

were two distinct species. However, various other subsequent

12

taxonomists (Erauer, 1863; Townsend, 1917) offered evidences
identifying the two species as horripilum. At present, the
contention among contemporary taxonomists is that‘g, cuniculi
is a synonym.for Q, horgipilum. Townsend (lgg,'gi£.) also
presented the synonym.of'g, abdominalis for Q, horripilum.
Dalmat (19h2) distinguished‘g. pergmysci from_§. fontinella
Clark and the former species fromwg. fasciata Swank. All
above divisions have been accomplished by taxonomic studies
on adult flies. For adult species identification, the reader
is referred to reviews by Clark (1815), Brauer (1863), Swank
(1905), Jones (1906), and Townsend (1917).. Supporting bibf
liographic references may be found in Appendix I. However,
interests in this systematic study were in the investigation
of larval forms.

a'contemporary taxonomic studies of Cuterebra larvae are
mainly those dealing with second and third stages. This is A
due to the insufficient sampling of first stage larvae neces-
sary for valid characters (Knipling ggngf, l9h0). Examples
of first stage larval studies are_those of Ferris (1920),
Beachley and Bishopp (19h2) and.Da1mat (19h2).

The general approach to a systematic study of cuterebrid
larvae is the study of the following features: (1) the rela-
tive size and shape of spines, (2) the number and distribution
of spines, (3) the structure and size of the posterior spir-

acles,and (h) general appearance of the larva. Knipling and

13

Brody (19h0) stated that there were other characters of lesser
importance, namely the size and shape of the larva, the gener-
al structure of the cephalopharyngeal mechanism, and the size
and shape of the anterior spiracles.

'The body of the first stage larva was shown to be fusi-
form, tapering at both ends and measurements on the early
instars have been recorded by Ferris (lgg.‘gi§.) and.Dalmat
(leg..gi§.) as l.h to h.2 mm. in length and 3.2 mm. for the
width. The latter author discovered that 12 segments were
visible in this stage, and demonstrated cone-shaped dermal
appendages. On the twelfthsegment the posterior spiracular
plate was found with each spiracle terminating in two slits.
Records of the color of the stage were not given in the text
of these authors.

. However, in his study of the second instar, Dalmat (191(2)
stated that the body was white. The average length and width
was 9.5 mm. and 3 mm. respectively. Cone-shaped and scale-
like spines were seen covering the segments. Some cone-
shaped spines pointed posteriorly and others pointed anter-
ierly. These spines were situated on the anterior and pos-
terior aspects of a segment, and the direction of the spines
was the reverse of their location. Cone-shaped spines, ac-
cording to Cameron (1926), may be single or multipointed in
certain larval species. Specific spinal characteristics for
each of the twelve segments were presented by Dalmat (leg.

cit.), along with measurements on the posterior spiracles.

11L

The spiracles measured 0.12 mm. in length and 0.18 mm. in
width. Knipling and Brody (l9h0) found in their investi-
gations that the length and width of the spiracles was 0.30
mm. and 0.26 mm. It is probable that the latter authors

had a later phase of that stage. After internal examination
they found that the average length and width of the cephalo-
pharyngeal skeleton was 1.6 and 0.75 mm. No measurements of
spines were carried out in the studies cited above.

In studying the third instar, the degree of pigmenta-
tion of certain spines was recorded (Knipling gt gl., log.
.233.). They stated that pigmentation distinguished the rela-
tive age of the larvae, that is a newly melted larva from
a mature larva. There was a lack of pigment in the former
larva, and the more mature a bot became the darker the larva.
Lengths of mature larvae ranged from 20 to Q3 mm. and widths
approximately equal to one-half the lengths. Spines were
measured from base to tip to obtain lengths ranging from
0.36 to 0.80 mm. Base measurements for width ranged from
0.25 to 0.65 mm. These range variances were reflected in
larvae of different Cuterebra species. A comparison of lar-
val characteristics was presented by Knipling and Brody
(l9h0) using Cuterebra buccata and Q. cuniculi=(horr1p11um) as
the bot examples.

The sampling material of cuterebrid larvae employed in

the descriptions of the above workers was here discovered

 

1.1(lluluil

II..()A

15

to be rather limited. Thus need of a greater bot sample is
necessary in order to achieve more finite characteristics.

The systematic study of pupae has been neglected by
workers, probably because of the immediate fixing of mature
larvae for future investigation. The puparium is essentially
a dried hardened third stage larval skin, which has a more
spherical shape, reflecting a stouter condition in the middle
and posterior (Dalmat,-l9h2). Due to the shrinking effect,
only ten segments are visible as the cephalic and spiracular
segments are so retracted that they are not discernible.
Anterior spiracles, everted during pupation, may be found
between segments 2 and 3 of the puparium.as two light brown,
column-like tubercles projecting from.the integument (Knip-
ling and Brody, 19h0). It was possible to retrogress by
studying the morphology of a puparium.with mature larval
features, from.which an identified adult fly emerged.

Dalmat (lgg.|git.) stated that the emergence of the
fly was brought about by the detaching of the dorsal aspect
of the first 5 segments in a single piece often referred to
as a cap. This method of ecdysis is typical of the dipteran
suborder Cyclorrhapha.

Among the families of Diptera, and particularly in the
Oestridae, a structure termed the "button" may be present in
the mid-line of the posterior spiracular plate. This struc-

ture is essentially an accumulation of scars produced by the

l6

discarded spiracles of the preceding stage. Greene (1925)
stated that the Cuterebra larvae lack the button in the
spiracular plates. However, papers by Knipling and Brody
(l9h0) and Dalmat (l9u2) showed posterior spiracular plates
with buttons present in the third instar. The resolution of
this problem will be discussed later.

Of morphological significance is the length and width of
the posterior spiracles and of the spiracular plate itself.
In a third instar example cited by Dalmat (l9h2) the length
and width of the posterior spiracle were 1.1 mm. and 0.5 mm.
respectively. Two kidney-shaped spiracular plates, each
containing three well defined sinuses, were 0.91 mm. long
and 0.33 mm. wide.

It was heped in this work that the various inquiries on
the life cycle of cuterebrid species would be clarified. In-
stars of larvae were studied in the hosts to determine the
seasmal periodicity, duration and incidences of the larvae.
In these studies some effects of the larvae on the hosts were
ascertained.

As a consequence of the life history study, ecological
data was determined. Ecological factors such as soil and
vegetation were examined in relation to the environment of
Cuterebra. Modes of infection were studied from the above
investigations.

Systematic investigations on cuterebrine larvae were

carried out with the object of separating various Quterebra

l7

instars. Morphological similarities and differences of the
larvae were discovered which were used in their species
identification.

Confirmation of the larval species was accomplished in
the taxonomic studies of pupal cases from which identified

adult flies emerged.

 

). (I: -.l Ital-ll;

5.0. 11.!)selnbf . Tm.” ..l
lbs I

 

18

MATERIALS AND METHODS

The choice of a cuterebrid infected host was founded on
the facility of capture and handling as well as obtaining
substantial numbers of hosts and'parasites. Michigan cotton-
tails, Sylvilaggs floridanus mearnsii, reasonably fulfilled
the study prerequisites.

Subsequent observations were made on individual hosts
in order to follow the course of infection. In the contin-
uous recapture of hosts, some questions on the life history

of Cuterebra were clarified. (However, these periodic studies
were not so frequent as to interfere with the natural habits
Of the cottontails. The study area was carefully analyzed
Previous to the onset of trapping, and also while in the
course of the project. Proposed areas for analyses were host
burrows, nests, runways, and feeding areas.

Tabulation of data was done while in the field in order
not to, lose the freshness of ideas. Infected animals were
brought into the laboratory under conditions similar to their
habitat, and more complete studies were carried out. They
were released into the study area as soon as possible to ob-
sex-Va re-infection. Situations peculiar to the procurement
of ad:Lllt flies and larvae were established in the field.
The approach to the problem of the life history and ecology

 

..a a. ‘ v

 

19

of Cuterebra was adapted as nearly as possible to natural
conditions.

For the systematic study the collection of larval

material gave an adequate sample of various instars. Inas-

much as larvae obtained from cottontails were allowed to
complete pupation, additional larval specimens had to be ob-

tained. Larvae were obtained from road kills, rabbits killed

by hunters and trap-killed cottontails. Various other repre-

sentative instars of larvae were collected from other hosts.

Other sources of these examples were veterinarians and state

' conservation departments .

A . FIELD STUDIES

Of first concern was the mapping of the study area, in

II'hlrl. ch vegetation, topography and soil was graphically recor-
dod

The area under investigation was the state game farm

nee—1‘ Mason, Michigan. The game farm functions principally

as a. pheasant farm, covering an area of 250 acres. However,

the area offers excellent habitat for rabbits.

Trapping investigations began May 5, 1953. Thirty-two

"1P6 live traps were set in areas thought to be of rabbit use.

Daily visits to the trap line were made from May 5 to November
214., 1953. and observations were recorded. A normal run of

the trap lines would consist) of an early morning inspection

or the traps for captures, closely scrutinizing the vegetation

 

 

 

20

bordering rabbit runways for cuterebrid eggs, observations
from a hidden area in the swales and wheat fields for adult
flies and noticing rabbit movements. closely. Wheat plants
found on the edges of the fields were inspected for eggs.
Beamer (1950) stated that the eggs were seen with the naked
eye. '

Six o'clock in the morning proved a fruitful hour to
study rabbit movements. Field observations on the adult
flies were made later in the day when the temperature was
warmer.

Upon capture the rabbit was moved from the wire trap
into a cloth bag and weighed. Rabbits were then immediately
tagged in the ears. The tag number, age, sex of host, and
area of capture were recorded. Cuterebrid larvae examina-
tions were accomplished in the field while the animal was
5171 11 in the bag. Areas of the neck, back, scrotum and

8hOnlders were examined for warble formation, cuterebrid
9838 and larval air holes. This examination consisted of a
°1°3e scrutiny of the skin and a detailed palpation of. the
mentioned areas. Other areas of the body were generally ob-
served.

The location, stage and number of bets on infected cotton-
taila were noted, along with measurements of air holes when
found - I If ~the "bot" stage in the rabbit happened to be a
8°°°hd or a third instar, the infected rabbit was brdught to

t
he university laboratory for further study. A cottontail

21

with a mature larva was placed in an outdoor wire pen and ob-

served. Dropped mature larvae were collected and effects on

the host were summarized. Infected rabbits were released

into nature a few weeks later, being temporarily held in
order to study whether latent original infections would reach
their final location.

The other method employed in the collection of cotton-

tails was that of collecting highway killed specimens. This

was carried out in the spring of the years 1953 and l95h by
means of early morning observations‘of various highways.
Counties of Michigan studied were Ingham, Kalamazoo and Barry.
Samples of cottontails at this time of the year'were suffi-

cient as rabbit movements were intensive during mating season.

Autopsy protocols were carried out on these cottontails,
in which the animals were first externally observed for war-

bles. Then the specimen was skinned in order to check sub-

mltaneous larvae or remnants of larval scars. Nasal and oral

caVities were examined as possible larval migratory routes.

Internal examinations were made of the body cavities, mesen-

tepics of the abdomen, the digestive tract and the musculature

or the back, neck, fore and hind limbs. Scrota of males

were dissected for larval stages. specimens submitted by
hunters in the fall at the Kellogg Forest, near Battle Creek,
Michigan, were handled in the same manner. However, in the

ma3°rity of the hunting cases, the larvae were extracted from

22

the hosts. These larval examples, depending on the stage of
the parasite, were either kept for pupation or for mode of
infection studies.

Mature larvae collected for pupation outdoors were placed
in soils of various ecological situations. Fly traps were
planted over the pupation sites. Thirteen sites were established
by November 21;, 1953 at which time rabbit trapping was termi-
nated. These sites were routinely examined throughout the
winter and spring to prevent damage or disturbance.

Fly traps were also employed during the summer of 1953
for the procurement of adult cuterebrid flies. Various baits

were placed under the traps in the hepe of luring and even-
tually capturing adult flies. Baits used were gasoline,
Vinegar and commercial rabbit lure. The above bait solutions

were applied to the sponge of a "sweat band”, and the band was
Wra~£3ped around the trap, placinghthe soaked-sponge under the
flu“115181 of the trap. Every three days the sponges were re-
soaked with the solutions. Fly traps were set in areas where
“an 1t flies might habit.

Mode of infection studies were carried out in the field

during the summer of 19514,. Inasmuch as areas of high

W infection were discovered from the previous year's
Stud-3. bait pens, containing live cottontails were established

there. Cottontails used in these studies were isolated for

one month prior to placement in the bait pens in order to

 

 

 

23

insure a negative pre-experimental condition. Different
ecological effects, such as experimental exposure to vege-
tation, lack of vegetation, field borders, swale edges, brush
piles, outbuildings were individually attempted. Domestic
white rabbits were also employed as controls in these out-
door situations. Bait animals exposed to vegetation were
allowed to eat the prevailing vegetation. However, cotton-
tails not having vegetation were fed commercial rabbit feed
only. . All animals were given water in an inverted animal
cage drinking tube, for the purpose of avoiding possible
cuterebrid egg contamination. Routine procedure of bait
Pens consisted of semiweekly examinations of the host and of
the pen for phases of the life cycle of Cuterebra.
Concurrent with the Mason game farm study, asimilar
trapping program was started on August 10, 1953, under the
BuPer-vision of Mr. Aelred Geis, at the Kellogg Station, near
Batt 1e Creek, Michigan. .Though the program was later than
the Mason area, it was partially compensated by the use of
seventy-five live traps on 1150 acres. -
A duplicate cottontail study was again'started at Mason
°n May 20, 1951;, employing fifty live traps. This last
trapDing project terminated on November 20, 1951+.

 

 

 

B. LABORATORY STUDIES

Cottontails with second or third stage larvae were
brought into the laboratory, and were placed in animal cages.
The fecal trays were filled with sand to a depth of )4. inches,
in order to allow pupation of dropped mature larvae. Periodic
investigations, every two days, consisted of recording the
weight, the 'air hole diameter of the larva, the appearance or
disappearance of larvae, and the time of healing of larval
cysts after the mature larva dropped. Cottontails were
held for one month in the laboratory to check for possible

latent original infections. ‘ The hosts were then released
into the study area and closely studied in subsequent cap-
tures for reinfections.

Some collected mature larvae were allowed to pupate in

Jars containing depths of sand. The depth varied from 1 1/2
to 5 inches. Observations on pupation were recorded. At
the end of £311 trapping 1951i, thirty-nine pupation jars with
gauze or muslin tops had been set up. Sixteen Jars were
placed in a cool damp basement at the game farm on September
10’ 1951+. Temperature was recorded throughout the winter
lint; 1 January 16, when the pupae were brought to the labora-

tepy and left at room temperature. The remaining pupation

Jars were individually brought into the laboratory as soon

a
a the pupae were established.

 

 

|.|Il|.‘|l|alli III.

 

 

25

C. SYSTEMATIC STUDIES

The primary objective in this study was to collect
mature larvae, allow them to pupate and to identify the adult
flies obtained. Once the adults were known, the puparia were
studied for larval taxonomic characteristics. In this man-
ner known types could be established for future reference.
However, inasmuch as the possibility of procuring success-
ful pupations was rather small, larvae from various hosts
were collected. In general, these latter larvae were received
from outside sources in a preserved condition.

Hosts recorded from sariples in fixative were dog, cat,
white-footed mouse and Jack-rabbit, Also they were from
cottontails, peculiar to the states of Michigan, New Jersey,
Pennsylvania and Wisconsin. These bots were segregated ac-
°°rding to host and studied separately. Features studied were
simi lar to those suggested by authors in the introduction.

Measurement of the larger spines, posterior spiracles and
Ora-1 skeletons were taken with a compound microscope at 100

magnifications, using an ocular micrometer.

The method of preparing the stigmata for identification
Was

carried out in the following manner. Since the larvae
Were hardened in alcohol for a number of days prior to re-
c6119 1;, the Stigmata were rather firm and. could be 01115 0‘11“
T1118 disection was best accomplished under the stereoscope

w
ith the aid of two microneedles and a pair of microscissors.

26

Anchoring the bot specMen firmly in a paraffin mold, the
stigma was teased with the microneedles and excised intact
with the microscissors. Stigmata from the first and second
instars could then be passed through two 5-minute changes of
70 percent and absolute alcohol. The section was rinsed
well in diaphane and a coverslip placed on a glass slide

‘ ‘usingdiaphane as the mounting medium. Due to their. dense

- pigmentation the stigmata of third stage larvae and puparia
had to be cleared first in a boiling _10 percent KOH solution.
Boiling was usually continued for an hour or two in order
to obtain clear spiracular plates. After removal from the
KGB solution, the stigmata were washed in water thoroughly,
dehydrated in the usual manner and mounted in diaphane.

‘ A similar protocol was used for the preparation of
Cephalopharyngeal skeletons. However, in order to obtain ex-
cellent view of the specimen, the skeleton was cut with micro-
scissors at the hypostomal bridge and each section was
mCurated showing an outer lateral and inner lateral surface.

Areas of segments showing the shape and multipoints
of Spines were excised and mounted in diaphane.
The segments of the bots were closely studied for dif-

repel-'1 tiating characteristics to separate the larvae as to

spec-’1 es.

27

RESULTS
A. LIFE HISTORY
l. Obvious Appearance of Larvae in Their Hosts

_ It seemed that with the continuous recapturing of cot-
tontails the development of larval-stages in the hosts could
be studied. ‘Data gathered on the, trapping of Mason rabbits
in 1953 revealed the percent of recaptured rabbits to be 35
by November 7. 'With this recapturing certain facts on the

timely appearance of larvae were noted. On August 1, 1953,

a recaptured adult cottontail which was previously diagnosed
externally as negative for W July 10, 1953, was found
to have an early third instar in the neck. Thus, it was only
22 days from a probable negative condition to an apparent
third stage. This larval time period occurred in three in-
fected recaptures. Another cottontail previously captured
on July 21, 1953. and externally determined as negative for
W larvae, was recaptured on August 5 with an early
third instar larva. Time for this larval exanmle was 15
days- Various other examples of larval growths were: from
nfigatfixe to an early third instar, 26 days; from negative to
a Well healed larval wound (dropped mature larva), 39 days.

The Presented data reflected an obvious internal larval ap-

peeu:‘aa'ice in cottontails approximating the time of 22 days.

 

I ....I .l.’i‘JLr.. 1 ' .

 

28

2. Anatomical Locations of Larvae Infections

Of forty-nine rabbits infected with Cuterebra larvae
during the two year study at Mason, only one example diverted
from the neck region. This single example was in the left
front leg over the suprascapular region of the shoulder bone.
In the Kellogg Station data of 1953 W0 cottontails were
foxmd showing unusual infection sites. One cottontail with
four cuterebrid larvae had two of the larvae in the cheek
region and two in the neck. The other had one larva on its
back and another larva in the scrotum. The primary site of
Cuterebra infections in 187 “southern Michigan infected cotton-
tails captured at the Kellogg Station and Mason Farm was in

the 11 00k.

3. Field Pupation Experiments

V-IEleven outdoor pupation sites were established in 1953
to determine times of emergences of adultgcuterebrids. These
“tea were investigated throughout the winter and spring in
”961' to maintain the fly-traps. In the late spring 01' 1951+
the locations were frequently checked for newly emerged
8.6.1111; flies. Only one fly-trap had a positive result. The
larva - used in this trap was taken from a white-footed field
mouse

a Peromyscus leuco us, on August 27 . 1953. On the very
da
y °r capture the mature larva pupated in the sandy soil

29

of the pupation site. A densely vegetated sumac border was
the site of this fly trap. Date of emergence was July 25,
1951;, which offered a pupation time of nearly 11 months.
Dr- Sabrosky later identified the fly as a female Cuterebra

 

fontinella. Longevity of this fly was only one day in a
laboratory container. No studies on the modes of infection
could be carried out with this cuterebrid fly. The remaining
ten unsuccessful‘pupation sites were retained in thefield
until the spring of 1951;. Though the pupae were discovered
to be intact in the fall of 1953, no flies emerged the spring
of 1951... Thus, the Cuterebra appeared in this study not to
show a two-year cycle. Also it was found that one generation

a year existed in Michigan.

h. Field Notes on Pupation

_Mature thirdstage larvae were studied outside their
hosts for times of survival. This extraneous situation was
thrice recorded as 9, 10, 13 days before any serious changes
began. This range of 9 to 13 days may be beneficial to the
dropp ed mature larva in awaiting a suitable pupation.

Upon dropping on similar soil, mature third instars
were noted to react in two ways. One manner was the immedi-
ate burrowing of the larva in the soil. .On the other hand,
othe}? mature larvae merely laid on the soil surface with

1 .
1 ti: 1e locomotive action.

30

Burrowing time was noted to be in relationship with the
type of soil. In sandy soil, five mature larvae revealed an
average of 10 minutes. However, in sandy loam the average
time for six mature larvae was 15 minutes. Edaphic areas
recorded were solely those of light types such as sand and
loan. Depths recorded on 27 burrowing larvae revealed
ranged from 1 1/2 to 2 1/2 inches. There was no evidence of
subterranean lateral migration by larvae during burrowing

in three dozen soil Jar containers used for pupation experi-

ments .

5. Autopsies

Sixty-two cottontails were examined during the two-year
rabbit study. These rabbits were autopsied throughout the
Possible Cuterebra cycle, that is from May to December. For
°Xternal investigations examination areas for cuterebrid
°888 were the lips, nose, neck, shoulders, abdomen, scrota,
and heels of the hosts. Also in these areas the skin was
c1089 1y examined for perforations which might be larval entry
Bites - Larval migratory routes, larval. cysts or representa-
tive larval atagsswere sought in the internal investigations.
The only positive prosecting was adiscovery of a first instar
cuterebrid larvae on June 28, 1953. which is discussed under
til-'31? stage larvae seasonal periodicity. There were no other
Oxtgphal or internal evidences of any phase of the W

11
rg history in the autopsied animals.

31

6. Duration of Instars

Captured rabbits, having Cuterebra Ag gig were taken
to the laboratory for further observation. Twelve examples
were observed intermittently from July 25 to September 25,
1953. An animal which reflected the general time of cuterey-
bridlarval stages‘was an adult female cottontail. Primary
cap ture was ~on July 10, 1953, at which time the rabbit was
not obviously infected. However, on August 1, 1953, it was
infected by a mid third instar and in Just eight days the '
matme larva dropped and a pupa was formed. Another eprle,
an adult female rabbit, whose primary capture examination
was negative on June 30, 1953, had an early third stage infec-
tion July 25. A mid third stage infection was recorded on
July 31. The mature larva had dropped out and formed a pupa
on August 8. Summarizing the laboratory larval data for
1953 and 19514. it was discovered that about 6 days elapsed
from an early third stage to a mid third stage. Nine days

"as noted for the duration of a mid third instar to a pupao

7. Air Hole Diameters

It was noted that upon checking cuterebrid larvae in the
h
081;, the. air hole-diameters gave significant data as to the
at
age orthe larva. For example, air hole diameters for the

e
arly third stage larvae ranged from 3 mm. to 9 mm. No

32

dimeters below 3 mm. were found in this study. Confirmation
of this stage at the minimum point was made by excising the
larva and identifying it. The larvae which were light brown
in color had incomplete spiracular plates and intermediate
sp zines which were low and not completely developed (see
descriptions under Systematics). In the mid-third stage
larvae the air hole range was from 10 mm. to 13 m. At the
13 rum. diameter the larvae were observed in the laboratory
specimens to be one-quarter out of their "larval cyst or
bag”. Diameters at the time of mature larval dropping‘were
between 114 mm. and 16 nan. Usually the 17 mm. diameter showed
a vacancy of the larval bag and a healing process beginning.
No first or second stage larval air hole diameters were ob-
served throughout the study. These larval air hole diameter
8”erages were taken from sixty infected cottontails of which

three- cases are presented in Tables I, II, and III.

8. Mode of Infection Studies

With the trapping project of 19514. came the knowledge
of wInert areas had the highest infestation of cuterebrid
larvae . In these determined areas 22 live bait pens were
eatablfished to discover the mode of infection. Two positive
cuteI‘Bbrid infestations were obtained. One location "88 a
combination lumber and fence wire salvage dunnp. This sal-

Va .
8e dump was bordered on the sides by a cornfield, evergreen

33

 

 

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emoH .«mmmmmepo maamzH omHsa mo
mmm<ma zo women mmemzaHo egos mHa mmoe<momao <

2 SE

 

35

TABLE III

A LABORATORY AIR HOLE DIAMETER STUDY ON PHASES
or THIRD INSTAR CUTEREBRA, 1951;

_h m j

__ Host 19911034101: Juvenile Male Cofit-tontail
_Date 8-5-51 8-8-51 8-11-51; Ban-511 8-18-51; 8-19-51; 8-2u-5u

 

 

 

 

 

 

Earn” 1 1 1 1 1 1 1
Larval early early early mid late
jugs 3rd 3rd 3rd 3rd 3rd pupa “3'
Air Hole ’ 1

9184111111. ) 3 5 6 12 16 17 scar
Rabbit

wt. (oz. ) 23 23 2h 21, 2h 26 29

 

 

E” 0 3 3 3 u 1 s

.—

36

hillside and willow swale which had greenbriar and sumac
intermingled on its border. It was in this swale that an
adult cuterebrid was observed—in the summer of 1953. The

' wire cage, measuring 8' x 3' x 3', was placed in the middle
of the dump and was supported three feet'off the ground.

On June 10, 19514.. a wild cottontail previously determined
35 negative by palpation and isolation was placed in the
pen and was observed semiweekly for cuterebrid larvae. At
no time was the animal in contact with natural vegetation.
518° Periodically {examined for cuterebrid eggs were the
nesting box and the rabbit cage. An early instar was dis-
covered in the left side of the neck on July 11, 19511. with
an 311‘ hole diameter of 3 mm. No eggs were found on the
ho“ nor in the pen. A mid third instar was reached July
289 19514.. The larva dropped from the host July 30, 1951+. and
was Placed. in a pupation jar where it pupated the next day.
An autoI)sy carried out on the host revealed no evidence of
migratory routes or other larval stages.

Lo(:ation of the other positive bait experiment was in
an area having a high larval incidence in 1953. This perma-
nent C}&1’ne Farm pen measured 50' x 15' x 8' and was exposed
to natural vegetation. A rabbit burrow was supplied in the
pen. Simultaneously, two adjacent pens containing white
domestic rabbits were Similarl" established as controls.
0n J- J U

11118 17, 19511, two male juvenile cottontails originally
dete

I‘n'lined as negative, again by palpation and L1 weeks

37

isolation. were placed in the cage. These were checked as in
the previous bait experiments.

An early third instar was discovered in one juvenile
cottontail on August 19, 19511. Previous to this date no
P081t1V3 signs of larval infection were noticed. Larval
development was followed until maturity which was on August
27. 19514.. The larva dropped from the host three days later
and Pupatedon September 1.‘ After the infection the host
was sacrificed and autopsied, revealing no larval stages or
migratory routes. No Cuterebra larvae were discovered in
th" dOme stic rabbits which were held in the cages until Octo-
her 5, 195,4. 6

B. ECOLOGY

It was discovered that spring and sumer trappings of
Mason cottontails were rather difficult due, in part, to
the availability and abundance of existing natural vegeta-
tion. (Gt-aph I). This vegetation was more appealing as food than
‘th° fie 1d corn used as bait in the traps. Thus, the sampling
data 01‘ wild cottontails was not great compared to numbers
Obtained in fall and winter. Later in the year there was
an increase in captured rabbits due to the juveniles and a

la
ck 01‘.“ natural vegetation which favors trapping.

 

 

 

Number of Rabbits Captured

38

Graph 1

Mason Trapping Record
1953

Total Rabbits

20* ....... Total Juvenile Rabbits

19'
181

17'
161

ES

131

P‘h’
~953teru

 

:.

I n

 

 

OHNw-l—‘U‘ owgco
F‘

I
D
«in

June July ' Aug. Sept.‘ Oct.i‘ Nov.
Time of Captures

39

1. Incidence of Infected Rabbits on Mason Game Farm

The first trapping project began May 5 and ended November
214., 1953', at which time 138 captured cottontails resulted in
212 captures and recaptures. Because the curve of larval in-
Icidence occurred between July 19 and October 17 ”(Graph 21. only
those rabbits captured during that time, were considered, within
this time range 113 rabbits were trapped of which 29 had a
cuterebrid infection (Table IV). Therefore the percentage
of bot infestation was. 26. In general, the infections were
slightly greater in adults than in‘juvenil'es, however the
Periodicity of infections varied according to age groups.
Juveniles had an incidence peak from August 2 to 15 whereas
the adu 1t pattern reflected "up and down" cycles throughout
the project. The summer of 1953 was markedly and constantly
high in temperature offering what was believed to be favorable
conditions for cuterebrid infestations. '

Incidence of Cuterebra larvae in the Mason game farm
cottontails captured in 1951.1 was 29 percent. Number ofrabbits
handled during the infective period were only 57 (Table V).
In Part because of biological knowledge of the study area.
Obta1ne‘d from the previous year‘s investigation, there was
a high Spring collection of rabbits (Graph 3). However. as
the— trapping continued low numbers of cottontails were ob-
tained due to, the high juvenile mortality observed in the

fig '
1dr Inclement summer weather was believed'contributory

 

filial]! lat/win

#0

Graph 2
Incidence of Cuterebra larvae

in Mason Game Farm Cottontails 1953

 

Adult Rabbits
_ —— - -- Juvenile Rabbits
100T

901' '

(bx!
00

U1

0

e
‘.—-..l_~

‘5

 

Percent Infected

Lu
0
e

 

 

 

July Aug. Sept. 0613 0
Time of Captures

 

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m o o o H o o o o o H o o o cho ooHon noH: ooHHooosH *
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mm 0 0H m H m H m N ,H o m m o eooooecH poe ooHsoo *
m o o o H m o H o o o o o o aHoo ooHon ooH: ooHsoo *
m H o o o o o H H o o m H m oaoooH soH: moHooo %
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o o o o NN o o oo mm o oo mm oooooH an: Hopop a
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o o o o o o o o o o o o o sHeo ooHon anz .oHHooosH *
o o o o N o o H o o H o o oo>ooH noH: ooHHaooaH *
N N H H N m N H o o H o H oopooecH poo opHsoo %
o o o o H m o H o m o o o sHeo ooHon.anz ooHsoo %
o o o o o o o H H o H H H oooooH noH: opHsoo *
H N N N o H H H H m H N H opHooon oHHcoosH %
N N H H m 0H N N N m N H N ooHooan pHsoo *
m z m m a HH m m m o m m m ooHocos *
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Graph 3

Mason Trapping Record

1951;

Total Rabbits

Total Adult Rabbits

 

 

 

 

0

Time of Captures

to this situation. Additional factors were changing ecolo-
gical and agricultural conditions which were believed due,
in part, to the farm crops program established at the Mason'
Farm that summer.

The peak of incidence of juvenile rabbits in 19Sh
(Graph h) was found to be on August 2 which would correlate
with the peak obtained in 1953. Also comparatively similar
were the incidence peaks relative to adult rabbits. In the
later phases of the curves, minor peaks were noted indicating
the appearance of emergent adult flies which continually
arose from puparia during the summer and fall. These newly

emerged Cuterebra adults would propagate new larval infec-

tions resulting in new minor cycles and peaks.

The number of warbles per‘ infected rabbit was generally
found to correspond with the peak of incidence (Tables VI and
VII). This is explained by the concentration of larvae at
that time which would lead to greater infections on individual

rabbits.

2- Incidence of Infected Rabbits on the Kellogg Station

All larval material presented from the Station was

carried out by A. Geis. Cuterebrid larvae infections in

the Kellogg cottontail sample of 1951 were highest on
'J““'<szulo rabbits during August 11 and 31 (Graph S)- Adult
cottontails showed a peak in bots between September 1 and 10.
TenOle VIII relates the percent. of cuterebrid larval infections

Percent Infected

100?

A:
9L

 

1&5

Graph h
Incidence of Cuterebra larvae

in Mason Game Farm.Rabbits l95h

Adult Rabbits
------ Juvenile Rabbits

49.---

. July Aug.- Sept.
Time of Captures

no

TABEE VI

NUMBER OF‘WARBLES PER INFECTED RABBIT
MASON GAME FARM, 1953

W
Adults Juveniles

 

 

Number of Warbles Number of Warbles
Date (1953) or Holes or Holes

2 3 Aver. 2 3 Avon
l

 

 

 

July 19-25

Aug. 2—8

Aug 0 9'15

Aug 0 16-22

Aug. 23-29

Aug 0 30-Sept e 5
Sept. 6-12
Sept. 13’19
$61) to 20-26
Sept. 27-Oct. 3
Get 0 (4-10

Get 0 11-17

Total
W

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0‘ CHDCDPNDCDCHDP‘PHVFJC} F‘
l“ (DCDCHJCDCHDCDPHHPJPND

P‘
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n)
F:
pa
0

#7

TABLE VII

NUMBER OF WARBLES PER INFECTED RABBIT
MASON GAME FARM, l9Sh
W
' Adults Juveniles

 

 

Number of‘Harbles Number of Warbles
Date (195h) or Holes or Holes

2 Average 1 2 Average

 

 

 

July 19-25
July 26-Aug. 1
Aug. 2-8

Aug. 9-15
Aug. 16-22 1
Aug. 23-29 1
Aug. 30-Sept. 5
Sept. 6-12
Sept. 13-19
Sept. 20-26
Sept. 27-Oct. 3
OCte ““10

Get. 11'17

Total

HHHH H

owoowwo
m OHOOHHONNHHHH

3 1 1.3

H
O
N
....I
e

Percent Infected

AB

Graph 5

Incidence of Cuterebra larvae in

Kellogg Station Cottontails, 1951*

lOO«» Adult Rabbits

90., AK ' “““ Juvenile Rabbits
80 ‘r
704L
60"
so 4%
hO‘
30-

V

f

204»

10 n

 

 

 

July— . Aug. rSept. 9' Oct. Nov.
Time of Captures

*From A. Geis

 

 

 

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so on>ama npaz Hepop R
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mmH NN Hm HN NN NN HH N H N m : oBooNoH poo 33:23. A,
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oNN 4N Nm NN 0: mm HN : 0H NH NH : .sbeeo oHHeopsH a
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Hench. $02 doo doc :30 .paom .pnom .pnom .93. .34 .93 ASE.

 

 

 

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HHH> mum<a

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....a’. A, kl. mm

 

 

 

50

to be 29. This was determined from a total rabbit pOpulation
of 272 which revealed larval infections in 79 cottontails.
In this survey more juveniles had larvae than did adults.

In Table Ix.the larval incidences for 1952 give a total
percentage of larval infections as 19 which is quite low
compared to results in 1951. The rabbit sample for the later
year was 191 of which 38 cottontails were infected. There
was no evidence in Graph 6 of a definite peak of larval in-
cidence for juvenile rabbits. However, itdid appear that
the juvenile curve was in the late phase of its infection,
‘that is, it may show only the tail end of the curve. The
adult cycle related a peak during September 1 and 5 which
did compare chronologically with the data for 1951 on the
same area.

A situation similar to the above seems to exist for the
juvenile curve of the 1953 Cuterebra larval incidence (Graph
7). This curve exhibited a downward trend phase. Though
the adult example did not show a peak as high as the past
years, nevertheless there was a peak occurring between Sep-
tember 1 and 10 which did approximate the condition found in
1952. Twenty-one cottontails from a total population of
1&9 were infected with Cuterebra resulting in a lh percent
infection. This percent infection recorded in Table I
was the lowest obtained in all the larval studies under-

taken at the Kellogg Station. Essentially, the number of

TABLE IX

51

INCIDENCE OF CUTEREBRA LARVAE IN KELLOGG STATION

OTTON AILS, 1952*

 

Time of Captures

 

 

 

Aug. Sept.Sept. Sept. Oct. Oct. Total
26-31 1-5 17-20 21-30 1-10 11-20
# handled 16 17 15 52 51 no 191
# adult rabbits 6 2 2 8 h 3 25
# juvenile rabbits 10 15 13 NN h? 37 166
# adults with larvae l 1 o o o o 2
# adults with holes 1 l O O O 0 2
# adults not infected h 0 2 8 h 3 21
# Juveniles with larvae 3 ll 5 7 2 l 22
# juveniles with holes 1 O l 5 h l 12
# juveniles not infected 6 ll 7 32 lil 35 132
% total with larvae 25 29 33 13 h 2 12
% total with larvae or
holes 38 35 no 23 12 5 19
% adult with larvae 17 50 O O O O 8
% adult with larvae or
holes 33 100 O O O O 16
% juveniles with larvae 3O 27 38 IN N 3 13
% juveniles with larvae
or holes no 27 N6 16 13 5 12

 

 

*From A. Geis.

52

Graph 6

Incidence of Cuterebra larvae in

Kellogg Station Cottontails, 1952*

100'

Adult Rabbits
--..— - Juvenile Rabbits

T

90*

co
9?

I
U1
<3

roe
a:
c:

 

Pe
w
O

 

 

 

-4

I
T7

Aug. Sept. Oct.

Time of Captures

*From A. Geis

53

Graph 7

Incidence of Cuterebra larvae in

Kellogg Station Cottontails, 1953*

100 T

 

Adult Rabbits
90‘“ ------- Juvenile Rabbits

1

80‘

ts70-"

r

86%)?

00
;r
<3

  

 

. -. 4:11
Aug. Sept. Oct.
Time of Captures

—v—

*From A. Geis

TABLE I

St

INCIDENCE OF CUTEREBRA LARVAE IN KELLOGG STATION

WARS , 1953*

 

Time of Captures

 

 

 

Aug. _Aug. Sept.3ept. Sept. Oct. Total
11-20 21-30 1-10 11-20 21-30 1-10

# handled 16 15 13 15 36 SN 1119
# adult rabbits h 2 5 2 8 6 27
I juvenile rabbits 12 13 8 13 28 NB 122
# adults with larvae l O O O 2 O 3
# adults with holes 0 O l O O O l
# adults not infected 3 2 h 2 6 6 23
# juveniles with larvae 5 3 l l l l 12
# juveniles with holes 1 O O 2 l l 5
# juveniles not infected 6 lO 7 10 26 no 105
% total with larvae 38 20 8 7 8 2 10
% total with larvae or

holes M1 20 15 20 11 Ii 11;
% adults with larvae 25 O O 0 25 O 11
% adults with larvae or .

holes 25 0 20 0 25 0 11
% juveniles with larvae h2 23 13 8 h 20 10
% juveniles with larvae

or holes 50 23 13 20 7 h 1h

 

”From A. Geis.

55

warbles per infected rabbit shown in Table XI was greatest
when there was a peak in the incidence of Cuterebra larvae
among the cottontails.

Graph 8 represents a composite picture of the averages
obtained from.the larval incidence studies carried out at
the Kellogg Station and the Mason Game Farm. This was accome
plished by chronologically tabulating the incidence percen-
tages resulting from.the individual studies and finding the
percent averages therefrom. These results mainly strengthen
the previously presented fact that the peak of larval inci-
dence among southern Michigan juvenile cottontails is found
between August 1 to 20. Also that the adult rabbit incidence
curve presents an opposite condition wherein the major peak
of incidence occurs between July 20 to 30, along with the
secondary peak between September 1 to 10. Slight variances
in peak incidences between the two study areas and various
years are probably due to fluctuations brought about by
sampling material and ecological factors.

The period before a peak incidence in larval infections
as seen in Graphs 1 and 3 showed that few juvenile cotton-
tails were captured. Field observations during this time
revealed cottontails hixiing during the hot July days
in dark densely vegetated areas and in nests<n~burrows.
After this Tperiodic hiding" the percentage of Cuterebra

infected young cottontails captured is quite high. Perhaps

NUMBER OF WARBLES PER INFECTED RABBIT
KELLOGG STATION, 1951, 1952

TABLE XI

r

 

 

56

 

 

 

 

 

 

Adults Juveniles ‘_
Number of Warbles Number of Warbles

Date (1951) or Holes or Holes
1 2 3 #0:: Aver. l 2 3 35:: Aver.
A1180 1'10 1 1.0 2 2 200
Aug. 11-20 1 1 1.5 2 h 3 1.9
Aug. 21-31 2 100 2 1 had 8 202
Sept. 1-10 1 100 1 3 205
Sept. ll-20 2 1.0 6 3 1 had h 1.6
sept. 21-30 1 1.0 7 3 l 1.5
Oct. 1-10 2 1.0 10 l 1.1
Oct. 11-20 0 O 6 1.0
Oct. 21-30 0 O l 1.0
NOV. 1-10 0 0 2 1.0
Total ‘11 1 1.1 us 11 11 {-3‘ 1.6

(1952)

Aug. 26-31 1 1 105 3 1 102
Sept. 1-5 2 1.0 u. 1.0
Sept. 17-20 0 O 5 l 1.3
Sept. 21-30 0 O 9 l l 1 had A 1.5
Oct. 1-10 0 o S 2 1.3
Oct. 11-20 0 O 2 1.0
TOtal 3 1 102 28 (4. 2 1."; 103

 

 

Percent Infected

57

Graph 8

Incidence of Cuterebra larvae in Southern Michigan

Cottontails from.l951 to 1953

1001- -—--—-—- Adult Rabbits
----- " Juvenile Rabbits

70 o

4? U1 o~
G» <3 :3

Lu
0

2017

 

 

0 AA- A: :LLA' LJ‘AL:
July Aug. Sept. Oct. Nov.
Time of Captures

58

this hiding may be conducive to Cuterebrid infections inasmuch
as adult flies prefer dark situations and nesting areas

(Cameron, 1926).

3. Incidence of Larvae in Sex of Rabbits

Results tabulated in this survey showed that the male
cottontails have an incidence of cuterebrid larvae approxi-
mately,twice as high as the female rabbits (Table XII). _The
month of August is the primary month of infection which
would compare with the seasonal larVal incidences. This
higher occurrence in male rabbits may be partly explained
by the activity of males in searching for mates during
breeding seasons,thus offering a greater captured sample.
Also in all probability more female cottontails, either
pregnant or with young in nests, are less likely to wander

under those conditions.

h. Seasonal Periodicty of First Stage Larvae

There is no mention in the literature relative to the
periodicity of first instar larvae in Michigan cottontails.
The first example of a cuterebrid infection in rabbits was
a highway kill that was found in Ingham county near Mason,
on June 28, 1953. Upon skinning, a first instar was dis-

covered in the region of the neck immediately under the

59

TABLE XII

INCIDENCE OF CUTEREBRA LARVAE IN sax OF
MASON CONTENTKTESI 1953 and 1951

 

 

 

 

 

 

1953 195M
Date
Male Female . Male 3 Female

July 5 3 3 2
August 7 3 6 2
September 6 3 5 2
October 1   l O 0

Total 19 10 1h 6

 

60

skin enclosed in a nodule approximately 11 mm. in diameter.
Close observation of the infected area revealed no larval

bag or air hole.' Measurements on the larva were 5 mm. long
and 2 mm. wide. Length of larval life was one day in a Petri
dish.

Examples of other first instar larvae were from preserved
material sent in to the laboratory. These were from veterinary
sources and the hosts were domesticated cats. Dates of col-
lection were recorded in the months of January, August and

September.

5. Seasonal Periodicity of Second Stage Larvae

The first recorded second instar in.Mason cottontails
was on July 25, 1953. A swelling under the neck was pal-
pated in an adult rabbit and the warble was extricated from
the bag by a scalpel. The nodule measured 15 mm. in diameter
Iand the larval measurements were 10 mm. long and h mm. wide.
Upon microscopic examination it was determined to be a late
second stage cuterebrid larva. No air holes were
discernible. In Table II there is noted a cottontail which
revealed subsequent larval infection not originally recorded.
On July 23 the host was found to have an early third instar .
on the left side of its neck. The animal was brought into
the laboratory and isolated in a clean cage. A large.

swelling, measuring 25 mm. in diameter was observed on

inl

'61

July 30 on the right side of the neck. No internal investi-
gation of the swelling was carried out for fear of damaging
the parasite. Larval development was allowed to continue
through August 8 when two'early third stage larvae with air
holes appeared in the region of the tumor. It was believed
that the stage of the larvae within the tumor was that of a
second instar. The reasonsfor this conjecture were due to
the measurements of the tumor and palpation of the larvae,
supported by the fact that in the two-year screening study
of approximately h50 cottontails for cuterebrid larvae, no
air holes were ever found for second stage larvae.

Second instar periods recorded in preserved specimens,
having Eglig_domestica as hosts, were in January, February,
March and in June, besides the normal months described in
cottontails. These stages were collected by veterinary
students and.were submitted with limited history on their
hosts. Previous geographic locations of the hosts that may
have determined unseasonal acquisitions of cuterebrid infec-

tions were not obtained.

6. Seasonal Periodicity of Third Stage Larvae

Recorded in Table I are examples of third instars in

‘Mason rabbits which were discovered on July 2h, 1953. Perio-

dical development of these larval examples were followed in

days relative to the growth of the phases (early, mid or late)

62

in the same table. The majority of third stages occurred
during the middle of August and early September when the lar-
vae were obvious as indicated in Graphs 2, h, 5, 6 and 7.
However, third instar examples in Kellogg Station cottontails
were seen as late as November and December. Larval material

from.cats had representatives in nearly every month of the

year c

7. Studies on the Adult Fly

The first adult cuterebrid was seen on July h, 1953.
At 10 A.M. the yellow-sided Cuterebra was observed flying low
over a clover field. Unable to apprehend the fly, a thorough
search of the clover plants under the flight area was carried
out in the hope of finding eggs. Results were negative. A
small white-sided Cuterebra was noticed in a thick willow
swale on July 11 at 11 A.M. The fly appeared to be resting
not quite a foot off the ground on young willows. Lazily
it flew from willow to willow, intermittently resting on
grass leaves. Upon approaching the fly, which was only a few
feet away, with an open insect net, it swiftly darted into
the dark core of the swale. The area revealed no eggs. On
August 11, l95h, at 2 P.M. a yellow-sided cuterebrid was seen
in a dense sumac area. The fly was captured and placed in a
laboratory container for study. Three days was the length of
life of this fly. It was later identified as an adult male

63

Cuterebra horripilum.by Dr. C. W. Sabrosky. A significant fact

afterwards discovered was that the three observation areas re-

flected a high incidence of Cuterebra infections.

8. Fly-baiting Experiment

Fly traps with bait were set near swales or other areas
of suspected cuterebrid habitat in order to capture adult
flies. Hindered by adverse weather conditions, baiting was
practically ineffective. ‘Baits would either be washed off
by rain or evaporate after a few days exposure. Various
baits used were: from.Ju1y'h-6, rabbit lure; July 6-8, honey;
July 8-10, rabbit feces in urine; July 10-12, gasoline; July
12-30, vinegar. Live bait, that is, cottontail rabbits in
cages were employed from July 3-7; July 22-August 14.; September
h-2h in areas believed having a high incidence of Cuterebra.
The end result of all the above experiments carried out that
summer of 1953 at the Mason farm was negative. No fly-baiting
experiments were undertaken at the Kellogg Station.

However, on July 2h, l95h, an adult cuterebrid fly was
found in a fly-trap that had been placed over a rabbit burrow.
This burrow was in a dark situation under a lumber pile in a

salvage dump. The specimen was sent to Dr. Sabrosky who de-

termined it as Cuterebra horripilum.

9. Laboratory Pupation Experiments

Thirty-nine pupation jars were established during the
late summer and early fall of 195h. Various types of soil
were used in order to study the ecological significance of
soil on pupation. Soils varied from.loamy clay to sand.

By July 6, l95h, five adult flies were obtained through
these experiments. In all five cases sandy soil was involved.

Emergence of these flies was noted to occur in a chrono-
logical manner, that is the first pupated example was also
the first emerging fly. This first example pupated on August
1, 195h. and the date of emergence was March 3, 1955. resul-
ting in a total pupation period of 17k days. Remaining
pupae reflected total pupation periods of 175, 218, 23h,
and 235 days. The amount of water added to these pupation
jars was 25 cc. per month. Four of the five positive pupa-
tion experiments were placed in a damp basement during the
first four months of pupation. Ranges of temperatures during
the winter months in the basement were 32 to 117° F. Past
this time they were in the university laboratory at room
temperature. The remaining pupa was continually in the labor-
atory, but situated on a window ledge partially exposed to
winter conditions. Conditions existing at emergence were
that it occurred during the day and in a very hot sunlight.
Summarizingtimme pupation data, it appeared that a slight

eXposure to cold stimulated the pupae towards an early

65

pupation period. The depth of soil in the pupation jars did
not generally bother pupation as results were obtained in
sandy soil in as little as l to 2 l/2 inches deep. Longevity
of adult flies in laboratory jars was recorded as l, 2, 3, h
and 5 days. Four males and one female fly were identified.
Dr. Sabroskyidentified all Michigan rabbit examples as
Cuterebra horripilum. The remaining fly which.was originally
sent from Pennsylvania was pupated, raised and identified as
Cuterebra buccata. Because the only female fly lived one day,
mode of infection studies could not be carried out. Chrono-
logically, two adult flies, male and female, would have to
emerge at nearly the same time and mate soon thereafter

in order to have laboratory studies on mode of infection es-

tablished through the acquisition of oviposited eggs.

10. Factors of Soil and Vegetation on Cuterebra

Results obtained from the Mason trapping projects indi-
cated higher numbers of Cuterebra infections in areas having
sandy soil. This fact may be explained by the possibility
that the soil in these areas offer optimum pupation condi-
tions. Mature larvae are better able to burrow into this
soil type and thus have higher survival numbers. Inasmuch
as there is better pupation results one may expect a higher
concentration of pupae in these areas and subsequently

greater concentration of emergent adult flies. The greater

66

the concentration of flies, the greater the nwmber of infected
rabbits would be in these areas. Also it was discovered that
more rabbit burrows were situated in the sandy areas, perhaps
allowing for optimum.exposure of the hosts to the flies.
Trapping records of the Michigan Conservation.Department were
summarised from.the Rose Lake Station, Clinton County, Michigan
and corroborated the results obtained at Mason. Sandy sites
on the Station revealed captured cottontails with more lar-
val infections and more larvae per number on rabbits. The
records covered trapping projects dating back to 1950.
Larval incidences on lower areas, such as marshes and clay
soils were distinctly lower than on sandy ridge areas. Also
the cottontail trapping program carried out at the Kellogg
Station in l9Sh supported the above contention. Mr. Aelred
Geis (1955) orally stated: ”the number of Cuterebra larvae
were much lower in cottontails captured in low areas, such
as the marshes found on the Kellogg Station, than on the
sandy ridge sites.“ Because rabbit movement studies were
being carried out on these Station areas during the summer
and fall of l95h, an excellent opportunity arose for selec~
tive ecological studies of cuterebrid larvae on their hosts.
However, due to their trapping procedures at Kellogg, data
relative to seasonal larval incidence in cottontails was
thought to be invalid.'

Vegetative sites such as dense sumac bushes, willow

swales and clover fields were associated with adult cuterebrid

flies.

67

11. Effects of Larvae on Cottontails

Comparing the growth curves of infected juveniles with
that of adult rabbits not infected (Graph 9) demonstrates the
effect on juveniles. Juvenile rabbits 2 to 3 months old,
having larvae, were found, according to Geis (1953) to average
about 20 percent lighter than those non-infected. Infected
rabbits soon regained weight after the warbles dropped out,
and averaged the same as non-infected cottontails by the
fifth and sixth month.

Results of weight measurements taken on fourteen infec-
ted cottontails held in the laboratory, revealed changes in
weight. This offered a good opportunity to closely check weight
fluctuations. Variations in the seven infected adults were
on the average 3 ounces from the original captured weight.
However, the infected juveniles were observed to decrease 3
to 6 ounces from the initial laboratory weight_which could
prove detrimental to young who weighailz or 16 ounces before
larval infections. Table XIII summarizes the course of a
larval infection in a juvenile. This example was chosen from
seven other warble infections because of its completeness and
continuity of infection. The juvenile host in the earlier
phase of the infection showed a debilitated condition, list-
lessness and lack of appetite.‘ No diarrhea or constipation
was noted and at no observed time did the rabbit lick or

gnaw at the larval wound. At the beginning of observation

Weight in Pounds and Ounces

68
Graph 9
Growth Curve of Kellogg Station
Cottontails, 1951*

‘ Rabbits Without Warbles

x Rabbits With warbles
0 Rabbits Formerly Infected

F:
0
e

r—;

2&0‘ )(e >‘

e
X
X

12*

 

A L_ L__ I n l_rl b
‘1— VT I I 1 V I

1 2 3 u. S 6 7
Age in Months

fiFrom A. G618, 1953

 

 

69

TABLE XIII

WEIGHT MEASUREMENTS ON A CUTEREBRA INFECTED JUVENILE
COTTONTAIL CONFINED IK‘TEE“EI§ORATORY, 195k

"--.,m —--—W~___.. vv'c—-——~——"—.’-

Host #hBh-hBS: Juvenile Female, 1 Larva in Neck

   

 

Days Air Hole

 

egg; Date "7:531: 8233:: 13$;sz Dimer
0 9-13-5h 1h 0 early 3rd 3
3 9-16-5h 11 -3 early 3rd 7
7 9-20-51; 10 -li mid 3rd 10
11 9-214-514. ll -3 mid 3rd 12
1h 9-27-5h 12 -2 late 3rd 1h
17 9-30-5h 13 -l late 3rd l6
l9 lO-2-5h 16 e2 pupa healing
23 lO-6-5h 20 +6 negative scar

29 lO-lZ-Sh 2h +10 negative scar

 

70

the infection the host lost h ounces and its morbidity remained
until the mature larva dropped from the rabbit. Once the lar—
va left the host there was an increase in weight and this in-
crease was retained until the tenth day after the larva dropped,
out, whereupon the animal, determined negative, was released
into the study area.

The infected adult cottontails appeared to have more re-
sistance to the effects of the larvae probably due to their
bulk. Whereas the young cottontails which probably have just
recently left their nests are more susceptible because of
their lack of resistance. An autopsy on an emaciated juvenile
rabbit which had been infected in the neck with three larvae
revealed pulmonary congestion (pneumonia) which was thought
to be a secondary effect contributory to death. Erhe primary
cause was believed to be the debilitating effects of the
larvae on the young rabbit which had a dead weight of 15
ounces.

During the two-year cottontail study insouthern Michigan
only three cases of Cuterebra in the scrota of male cotton-
tails were seen. These examples were from.the Kellogg Station.
In post-infection investigations, the resulting scar tissue
from.larval wounds caused severe atrophy of the scrota.
Emasculation would probably ensue from.the above pathology
due to the lack of reproductive tissue._

Effects of multiple infections on rabbits wereobserved

during a cottontail hunting party at Mason, Michigan, in

71

November of l95h. Cottontails were being collected during
the hunting season in order to observe late Cuterebra infec-
tions. An adult female rabbit which appeared to be listless
when first sighted was shot. It was discovered that four lar-
vae had recently infected the host in the neck. Three fresh
larval wounds were seen minus larvae along with one late
third instar. The host appeared emaciated though it was in
early November and the unharvested crops on the area offered
a good food supply. Upon autopsy a pulmonary congestion was
again discovered. This congestion might have been one factor
which slowed the animal. So indirectly the larval infections
may have been contributory to the death of the rabbit by gun.
Chances of winter survival in nature for an animal in this
state are rather low.

Cuterebra larvae have been associated with blindness in
jack rabbits of Nevada during multiple infections (Philip gt
El: 1955). Figure 1 shows a jack rabbit blinded from.bots
under left eye and one under right. There appears to be
numerous bot infections in the cheek area. Source of this
figure was from.Dr. C. B. Philip who also studied ticks in
his paper of 1955 (seen near white cards in photograph).

Fig. l.

 

Three heads of jack-rabbits from Nevada showing
effects of bots on hosts. head on the bottom
has two third stage larvae, one in its "larval
bag," the other out of it. Two air holes are
seen below the free larva. Numerous warbles

~ are found under the jaw of the middle rabbit.

An early third instar is shown out of its bag.
Upper rabbit was blinded because of multi-
infections around the eyes.

72

F180 1

 

73

C. SYSTEMATIC STUDIES
1. Definition of Instars

After surveying 127 cuterebrid larvae it was discovered
that the larval instars would have to be defined in order to
separate the larvae.' Larvae were sorted by external morphology
according to stages prior to taxonomic determination of Cutere-
‘égg species. Criteria for larval segregation were size, shape,
spine distribution, number of rows of spines, structure of the
posterior spiracles, and the color of the larvae. First and
second stage larvae were creamy-white in color (Figures 2 and
3). Larvae peculiar to third instars varied from light brown
to black (Figure h). The next important characteristics
were the arrangement and number of rows of spines on the lar-
val segments. Patterns for the first instar exhibited a
haphazard unorganized assemblage of spines in the four an-
terior segments. Whereas the second stage larvae had some-
what organized anterior rows of spines on the first four
segments. These two stages had spines arranged in several
irregular rows that circumvented the body segments. Third
stage larvae showed a distribution of spines in regular rows
throughout the larval segments. Naturally in relation to
size, the first instars would be the smallest. They ranged
from 2 to 5 mm. in length and from 1 to 2me. in width. Ranges

for second instars were 6 to 16 mm. in length and 2 to 6 mm.

ulna-i ' I.

|
.a;a.€:?£-— A -—..~.r .

Fig. 2.

First stage larva, 5 x 2 mm ., showing 12 vis-
ible segments ventrally, of which the last con-
tains the posterior spiracles. Oral hooks are
seen protruding at the right.

 

r - :
Slang? ;.__ .» __"._~l_;- m

(aim:-

Fig. 3.

A second stage larva measuring lh x 5 mm . taken
from the eyelid of a dog. The distribution and
number of spines are shown on the dorso-lateral
aspect beginning with the anterior segments at
the upper right.

75

F18- 3

 

o .w 4v «vi mun-d“ ‘ M‘

“Li

Fig. u.

A third stage larva from a cottontail showing
the number and distribution of spines on its
dorsal surface beginning with the anterior seg-
ments at the upper right. Note the clear
grooves, having microspines, one on each side
of the dorsum.

76

F180 1..

 

77

in width. Third stage larvae offered examples of lengths
ranging from 11 to 35 mm. and widths from.6.5 to 16 mm.

These measurements would vary according to Cuterebra species,
and are presented here merely to relate the relative sizes

of the three instars. Development of the posterior spiracles
was another feature aiding in the separation of cuterebrid
larvae into the various instars. Posterior spiracles pecu-
liar to third instars (Figure 5) show each plate divided

in three parts and perforated by numerous sinuous spiracular
openings. Spiracular plates for young Cuterebra larvae

were not clearly defined and may have two sinuous spiracular

openings (Figure 6).

2 . Ho 8158 Studi ed

Cuterebrid larval material collected from various sources
was studied separately according to the hosts they infected.
This was done after the larvae were differentiated to various
instars. The host examples included small wild mammals whose
scientific names and general location are as follows: white-
footed.field mouse, Peromyscus leuco us, Michigan; Sylvilagus
floridanus mearnsii, cottontail of Michigan, Pennsylvania
and‘wisconsin; Sylvilagus‘gloridanughmallgggg, cottontail
found in.New Jersey; and the jack rabbit,‘Lgpg§_californicus

deserticola of the state of Nevada. Larvae from domestic

, ":9" t'L

Fig. 5.

Posterior spiracular plates and spiracles of a
mature Q. fontinella larva taken from a white-
footed mouse.

78

F180 5

 

 

‘.' '<-'r~" . ~. -
.4, £235.“ ..-. it..- -44

Fig. 6.

Highly magnified posterior spiracles of second
stage 9, fontinella larva taken from a white-
footed mouse.

 

 

 

80

:mammals were obtained from the dog, Canig familiarig, and the
cat, Felis domestica, whose locations were listed as Wiscon-

sin, Ohio, Michigan and Illinois.

3. Cuterebra in Felis domestica

a. Q. horripilum .

First stage. Five examples of this instar were primarily
studied in respect to arrangement and number of rows of
spines found dorsally and ventrally on the larval segments.
Average 1ength.and width of the larvae were h.75 mm. and 1.75
mm. respectively. These measurements were obtained from
ranges of 3 to 6 mm. for the length and of 1 to 2 mm. for
the width. All representative instars were white in color.
However, the shape of spines varied in one specimen. Four of
the five larvae had predominantly single pointed spines along
with a few multipointed spines (Figure 7). The remaining
larva had only single pointed spines. However, the latter
example was an early first instar and believed to be income
plete for that stage in its spine development. Thus, these
larvae may be all from the same species, but not quite in the
same phase of the first stage. Posterior spiracles added evi-
dence to this question by comparing their structures. Before
the investigation of this question, the pattern of the spines

per segment will be presented below.

Fig. 7.

Multipointed spines of a C. horripilum first
stage larva taken from Fells domestica.

 

82

Cephalic segment. Small and usually partly retracted.

Anterior lobes bear small sensory tubercles. Group of

spines is found ventrally near the mouth.

Segment 2.
Segment :3.
Segment 4;.
Segmenth.
Segment 6.
Segmenth.
Segment 8.
Seggent 2.
Segment 10.

Segment ll.

Anteriorly h rows of caudad pointed spines.

No row of spines posteriorly on segment.
Anteriorly h-S rows of caudad pointed spines.

No row of spines posteriorly on segment.
Anteriorly 4-5 rows of caudad pointed spines.
No row of spines posteriorly.

Anteriorly h~5 rows of caudad pointed spines

No row of spines posteriorly.

Anteriorly h-S rows of caudad pointed spines.
Posteriorly 1 row of cephalad pointed spines.
Anteriorly 3-h rows of caudad pointed spines.
Posteriorly 1 row of cephalad pointed spines.
Anteriorly B-h rows of caudad pointed spines.
Posteriorly 1—2 rows of cephalad pointed spines.
Anteriorly 2-3 rows of caudad pointed spines. .
Posteriorly 1-2 rowsof cephalad pointed spines.
Anteriorly 1 row of caudad pointed spines.
Posteriorly 6-8 rows of cephalad pointed spines.

Anteriorly 1 row of caudad pointed spines.

. Posteriorly h-S rows of cephalad pointed spines.

Segment_12.

More or less truncate behind. Rounded anal
lobes on each side of anus. Posterior spir-

acles in center of segment at the end.

33

Segmental boundaries of the first four segments were
difficult to recognize in preserved specimens due to the
intermingling of the posterior spines of the preceding seg-
ment into the anterior spines of the following segment. In
general, the spines appeared, at first glance, to have a
haphazard pattern in direction. No spines were apparent
between the anterior and posterior spines of a segment.

The length and width of the largest spines ranged from .12

to .lh mm. and .Oh3 to .072 mm. respectively. Patterns of
the posterior spiracles in all_five examples were similar

to that seen in Figure 8. Spiracular plates which.measured
.h8 mm. wide and .36 mm. long were not organized in any de-
fined pattern and showed long moderately convoluted spiracles
which were broken into segments. Each spiracle ended in two
slits and measured .22 and .11 mm. for the length and width.

On the basis of two pointed spines which.Knipling and
Brody (19hO) stated were occasionally seen in Q, horri ilum,
it is believed that these first instar larvae from the cat
were Cuterebra horripilum. Two-pointed spines were occasion-
ally seen on the larval segments, especially in the anterior
rows of the first four segments and in the twelfth segment.

. Oral mouthparts for this instar extended back to the
anterior margin of the third segment. Morphology of the
cephalopharyngeal skeleton is reflected in Figure 9. The

oral skeletons measured .72 mm. for the length and .32 mm.

[J
...... -.....t... ..D

Fig. 8.

Posterior spiracular plates of a first stage

larva, Q. horripilum, obtained from Felis domes-
tica.

3h

Fig.'8

 
    

“/i; a / )de“ /,.~

d] “3
\ ' rP/“I”..,.- 1

‘ :‘e ...“.VA '
.‘ ° . ’. .‘el'V/‘f. 9")!‘I"" I,'“.. ‘(t
'.' <- V;, , . .

‘ ' r
. , , (
it - I \ .

 

..,#m

Fig. 9.

The left side of a cephalopharyngeal apparatus,
dissected from a first instar of Q, horripilum,
with Felis domestica as the host. Note the
foramen In the oral hook sclerite.

3W!

g9,

P180 9

 

85

86

for the width. Determination of the length was arrived at
by measuring the oral apparatus from the oral hook to the
end of the dorsal cornu. .For the width, the distance be-
tween the dorsal and ventral cornu was the measurement.
This procedure was carried throughout the measurements of

the oral skeletons.

Second stage. Twelve larval representatives were col-
lected for taxonomic investigations. They were white in
color and averaged 11.0 and h.5 mm. in length and width.
The shape of the spines was predominantly single pointed,
although two-pointed spines were occasionally seen during
the screening of the segments under a stereoscope. Larger
spines were .35 mm. long and .16 mm. wide. Segment 7 re-
vealed 5 to 7 rows of spines, and the remaining ventral
segments offered an arrangement and number of spines simi-
lar to that situation existing in the second instars from
Peromyscus leucogus. The following is a presentation of
the pattern and number of spines present on the dorsal
surface of second instars collected from cats. Segment 1
was usually retracted and small with two anterior lobes
having small sensory tubercles. Ventrally, near the mouth
a group of spines were found. Segment 12 was truncate behind
and contained the anus. The posterior spiracles are situ-

ated at the end and in the center of the segment.

Segment 2.
Segment 3.
Segment h.
Segment 5.

Segment 6.

Ԥegment 7.

Segment 8.

Segment 2.

87

Anteriorly h-S rows of caudad pointed spines.

No spines posteriorly. . '

Anteriorly h-5 rows of caudad pointed spines.
No spines posteriorly.

Anteriorly h-S rows of caudad pointed spines.

No spines posteriorly.

Anteriorly h-6 rows of caudad pointed spines.
Posteriorly 1 row of cephalad pointed spines.
Anteriorly h-6 rows of caudad pointed spines.
Posteriorly 2 rows of cephalad pointed spines.
Anteriorly h rows of caudad pointed spines.
Posteriorly h-S rows ofcephalad pointed spines.
Anteriorly h rows of caudad pointed spines.
Posteriorly h-S rows of cephalad pointed spines.
Anteriorly 3-h rows of caudad pointed spines.

. Posteriorly h-S rows of cephalad pointed spines.

Segmentglg.

Segment 11.

No row of spines either anteriorly or poster-
iorly. Few scattered spines posteriorly.
Anteriorly few microscpines.

Posteriorly 8-10 rows of cephalad pointed

spines.

However, the size and general shape of the dorsal spines

varied in the two host examples. The oral skeleton for this

stage from the cat was .86 mm. long and .h3 mm. wide (Figure

10.). Spines found dorsally on segment 11 were generally the

a-

Fig. 10.

The right side of a cephalopharyngeal apparatus
dissected from a second stage larva of 9, mg;-
ripilum. Foramen is seen in the oral hook
sclerite.

 

 

88

89

same as the situation on the ventral aspect. Segment 12 had
spines on its anterior segments gradually reduced, whereas
the posterior half of the segment was well armed.

There were three definite slits in the posterior spira-
cles of this instar and the arrangement of the_spiracles
appeared to be approaching a fixed structure typical of third
instars (Figure 11).. Lengthand width of the spiracles were
.65 and .h2 mm. respectively.‘ The spiracular plates were
.2h mm. wide and .h2 mm. long. “No buttons were present in
any of the twelve instar examples. Cuterebra horripilum.

appeared to be the species for these larvae from.the cat.

Third stage, Approximately eighteen larvae were taxo-
nomically studied in this group. Third stage larvae reflected
color variances from light brown to black. A few two pointed
spines were discovered on the larval segments. The larval
examples had an average length and width of 15.0 and 6.25
mm. accordingly. Ranges of the larvae extended from 11 to
20 mm. in length and 6 to 11 mm. in width which were inter-
preted as early and mid third instar larval examples. Larger
spines had a length range of .33 to .h2 mm. and widths ranging
from..28 to .3h mm. respectively. Number of rows of spines
in segment 7 was 12 to 15 which was the average condition
for all segments. Also in segment 7 mature spines were seen
of the first A to 5 rows anteriorly and posteriorly with

haxagonal untipped spines in between these rows. The above

Fig. 11.

Posterior spiracular plates and spiracles of
a second stage larva of g. horripilum obtained
from Felis domestica.

... \\\“., 9
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91

spine pattern was typical of early third stage larval segments.
Tips of these spines were either light brown or black de-
pending on degree of larval maturity.

Posterior spiracles for these two-pointed spine examples
(Figure 12) measured 1.6 to 1.3 mm. in average length and
width. The spiracular plates revealed a diffused pattern of
spiracles not clearly defined by two slits in each plate.
Spiracular plates were 1.h.mm. long and .58 mm. wide. Some
blance of a button may be seen in the mid-line of the spiracle.
Figure 13 revealed the typical morphology of the oral skeleton
which.gave an average length and width of 2.2 and 1.08 mm.
respectively.' The species of Cuterebra determined for these

two-pointed spine larvae was Cuterebra horripilum.

b. 9, buccata

Third stage. Fifteen larvae with single pointed spines
ranged in length from 15 to 30 mm. and in width 8 to 13 mm.
The mdnimum.points of these ranges represented early third
stages and the maximum.points were of the mature larvae.
_Larger spines of mature larvae were .38 to .h5 mm. long and
.28 to .32 mm. wide. The number of spinal rows in segment 7
were 12 to 15. Of significant difference was the structure
of the posterior spiracles which showed two slits clearly
separating three bundles of spiracles in each spiracular

plate (Figure 1h). Average lengths and widths of the posterior

 

9‘

Fig. 120

Posterior spiracular plates and spiracles of
a third stage larva of g, horripilum obtained
from a cat. Note the semb ance of buttons in
the centre of the plates.

 

. . “...—...“-—

 

 

 

92

 

Fig. 13.

The right side of a cephalopharyngeal apparatus
of a{§. horripilum third stage larva obtained
from a cat. Note foramen in the slender oral
hook sclerite.

 

Fig. 13

 

93

F180 1’40

Posterior spiracular plates and spiracles of
a third stage larva of g, buccata obtained
from a cat. Note narrow width of the con-
voluted chains.

 

9h

r13. 1h

 

95

spiracles were 1.04 and 1.314. m.respectively. Spiracular plates
measured 1.00 mm. in length and .50 mm. in width. What

might be interpreted as a button was vaugely seen in

the middle portion of the posterior spiracles.

The oral skeleton was found to be comparatively smaller
than‘Q, horri ilum, measuring 2.04 and .75 mm. in length and
width (Figure 15). All measurements taken on larval examples
are averages and may be interpreted as such. For these lar-

vae Cuterebra buccata Fabricius was the determined species.

h. Cuterebra in Canis familiaris
a.‘g. buccata

Sgcond stggg. Two larval specimens of this instar were
obtained from.the dog. These were studied for taxonomic
differences among the dog, cat, and rabbit species. The
white larvae gave an average length and width of 1h and 5 mm.
respectively. Spines were slender and single pointed with
an average length and width of the larger spines of .32 and
.17 mm. accordingly. The larvae had a pattern and number
of spines similar to that found in the cat, but having their
spines slightly smaller and more delicate in appearance than
the feline examples. Measurements taken on the oral mouth-
parts were smaller compared to those obtained for cats.

The mouthparts were .72 mm. long and .36 mm. wide (Figure 16).

 

dials. ~ ...-

Fig. 150

The left side ofa cephalopharyngeal apparatus
of a Q. buccata third stage larva obtained
from a ca .

Fig . 15

 

96

meet:- an 11.4mm

Fig. 16.

The left side of a cephalopharyngeal skeleton
of a second stage larva of g. buccata obtained
from Canis familiaris.

 

97

 

98

Also the posterior spiracles (Figure 17) were smaller than
the cat sample, measuring..h3 and .32 mm. for the length and
width. By comparison of the posterior spiracles taken from
the cat and the dog Cuterebra, it appeared that the spiracles
on the larvae from.the dog were not fully developed to final
structure and were in the process of maturing so as to array
themselves in similar morphology to spiracles from the cat
Cuterebra larvae. No buttons were discernable.

On the bases of single pointed long delicate spines
smaller oral skeletons and posterior spiracles, these two
second instar examples from the dog are presented as Cuterebra
buccata. The location of infection for these larvae was in
the neck and records do not show the sexes of the dogs, which
might eXplain the site in the neck and not in the scrotum
which is usually associated with this cuterebrid species.

5. Cuterebra in Lepus californicug deserticola

Second stage. Only one larval specimen of this instar
was obtained from Dr. Jellison. This larva of Nevada jack-
rabbits was white in color and measured lhand 6 mm. in
J~et‘1gth and width. Measurements of the larger spines gave
a length and width of .29 and .17 mm. respectively. Survey
Of the spines showed the shape of these spines to be single
and two pointed. Numerous multi-pointed spines were seen

in segments 2 to h and 11. The spine pattern and number

 

Fig. 17.

Posterior spiracular plates and spiracles of
a second stage larva of Q, buccata obtained
from a dog.

 

1.3 of
£1395

99

 

100

of rows was essentially the same as those of the cat, dog
and rabbit arrangements, but less rows were present. Because
of the unusual host and the geographic location of the larva,
the scheme of dorsal spines is presented below for comparison
with those of the cat, dog and rabbit. Segments l and 12

again were similar to previous larval examples of the cat,

dog, and rabbit. 0n the ventral surface there were no rows

of spines posteriorly in segments 2 to 10.

Segment 2. Anteriorly 2-3 rows of caudad pointed spines.
Posteriorly no spines.
Segment 3. Anteriorly 2-3 rows of caudad pointed spines.
Posteriorly no spines.
Segment A. Anteriorly 2-3 rows of caudad pointed spines.
Posteriorly no spines.
Se ent . Anteriorly 2-3 rows of caudad pointed spines.
_ Posteriorly 1 row of cephalad pointed spines.
Segment 6. Anteriorly 2-3 rows of caudad pointed spines.
. Posteriorly 1-2 rows of cephalad pointed spines.
Segment 7. Anteriorly 2-3 rows of caudad pointed Spines.
. Posteriorly 1-2 rows of cephalad pointed spines.
Segment_§. Anteriorly 2-3 rows of caudad pointed spines.
Posteriorly 1-2 rows of cephalad pointed spines.
Segment 9. Anteriorly 2-3 rows of caudad pointed spines.

Posteriorly 1-2 rows of cephalad pointed spines.

101

5

Segmpnt 10. No spines either anteriorly or posteriorly.
Segment ll. No spines anteriorly.
Posteriorly 6-8 rows of cephalad pointed

spines.

Taxonomic differences were noted in this larval example.
The first apparent difference, besides the shape of the spines,
was the structure of the posterior spiracle (Figure 18). Four
vertically arranged spiracles having an average length and
width of .lh and .03 mm. were observed. Individual spiracu-
lar plates were .15 mm. long and .09 mm. wide. Total length
and width of the posterior spiracles was .26 and .15 mm. res-
pectively.” No buttons were present. Comparatively, this
posterior spiracle was quite small and structurally different
than those of Cuterebra horripilum.and Q. buccata. The mor-
phology of the oral mouthparts (Figure 19) showed a differ-
ence in the area.of the oral hook and appeared to be stubbier.
However, the measurements of the oral skeleton were .72 mm.
long and .29 mm. wide.

Proposed cuterebrid species for this larva was rather
difficult inasmuch as the literature is rare on these rabbit
larvae. Yet, the posterior spiracles resemble those peculiar
to the early instars ony. fontinella. Philip'gg‘gl. (1955)
state that Q, ruficrus and Q, jellisoni have been found on
Nevada jack rabbits.

Fig. 18.

Posterior spiracular plates and spiracles of
a second stage larva obtained from Lepus cal-
ifornicus deserticola.

102

Fig. 18

u
\

0"

 

Fig. 19. The right side of a cephalopharyngeal apparatus
of a second stage larva obtained from Lepus cal-

ifornicus deserticola. Note stubby ora hooE
sclerite.

 

 

103

Fig. 19

 

 

10h

Third stage. Eighteen larvae which were collected from
Nevada jack rabbits were sent by Dr. Jellison for study.
These larvae averaged 25.h and 11.2 mm. in length and width.
Averages were taken from larvae ranging 19 to 35 mm. in
length and 9 to 16 mm._in width. The shape of the spines on
these larval segments revealed single, double and triple .

points. Seven larvae exhibited only the single oblique cone-

_ ‘_._ ..

shaped spines.» These long tipped spines gave ranges in length
and width of .38 to .58 mm._and .32 to .Sh mm. respectively.
The number_of rows of spines on these specimens were between
15 and 20. A_typical larval segment such as number 7 would
have the first 5 to 6 rows anteriorly and the last 5 to 6
rows posteriorly with single long obliquely slanted spines and
the intermediate spines were short and stubby. Segment 11
had short sharply pointed spines with black tips. The last
5 to 6 rows of this segment had spines which were orange in
color with black tips.l

Larvae with oblique cone shaped multipointed spines
were essentially the same in length and width as the single
pointed larger spines and similar in rows of spines in seg-
ment 7. However, segment ll was not orange in color. Multi-
pointed spines were found mostly on the first three anterior
and posterior rows. Intermediate spines were seen forming
two-pointedspines. More multipointed spines were seen dor-

sally than ventrally on the larval segments. Spines

105

surrounding the posterior spiracle in segment 12 also re-
vealed multipointed spines.

After examining the posterior spiracles of all the jack
rabbit 1arvae,it was discovered that regardless of whether
the larval spines were single or multipointed the shape of
the spiracles was simdlar (Figure 20). Scrutinizing this
spiracular example, it was compared with that of Q. buccata.
Hewever, the spiracles of buccata were long convoluted unbroken
in character whereas the spiracles of these Nevada cutere-
brid larvae were thicker in diameter and broken up into a
”macaroni” pattern. The macaroni pattern of these spiracles
was the same in the two types of larvae under consideration,
that is, the single and multipointed spine types. Measurements
on the posterior spiracles were .65 to .80 mm. wide and 1.01
to 1.20 mm. long respectively. Oral mouthparts of the two
larval types were also found similar if not identical in mor-
phology and approximate measurements (Figure 21). Lengths
and widths ranged between 2.30 to 2.hh mm. and 1.00 to 1.08
mm. respectively. Two species, namely, Q, ruficrus and‘Q.

ellisoni were recorded in the literature from Nevada Jack
rabbits (Philip 33.31., 1955). Further mention was made in
this reference that both species have been reared from jack
rabbits. In order to definitely identify these it would be
necessary to have the puparial cases related to the Cuterebra
species. At this point one could only present the larval

taxonomic findings sing confirmation of Cuterebra species.

 

Fig. 20. Posterior spiracular plates and spiracles of
a third stage larva obtained from Lepus cal-
ifornicus deserticola.

 

 

106

 

 

 

Fig. 21.

 

The left side of a cephalopharyngeal apparatus
of a third stage larva obtained from Legus
californicus deserticola. Foramen in t e oral
hook sélerite was not discernible.

 

.--—*—

__1-.

 

 

107

 

108

Puparium. ‘With regard to the Cuterebra larval species
described from Nevada rabbits, no puparia were obtained in
order to taxonomically separate the species, namely 9. ruficrug
or Q,_Jellisoni. No relationship could be made to the larval
descriptions rendered. This adult fly-pupa relation will
have to be accmmplished before positive identification of

these larvae can be made.

6. Cuterebra in Peromyscus leucopus

a. ‘2. fontinella

Second stage. Three specimens were collected and studied
according to the taxonomic characteristics of the early in-
stars. Length and width averages for these instars were 9.5
to #03 mm. respectively. These averages were taken from ranges
of 9 to 10 mm. for length and h to 5 mm. for width. All lar-
vae were white in color. Long tipped spines, found on the
segments, exhibited 1 to 3 points upon examination, especially
in segment number eleven. These spines had an average length
and width of .09 and .03 mm. The pattern of spines peculiar
to these instars are described below for each segment.

Segments l and 12 were generally similar to the early
instars previously described, except for a slight increase

in the number of spines on these segments.

Segmentgg.

Segmentg}.

Segment lie

Segmenth.

Segment 6.

8682201113 7 e

W-

Segment 2.

Segment 10.

Want 1:]. e

109

Anteriorly 3-4 rows of caudad pointed spines.
First 2 rows have largest spines.

Anteriorly 3-h rows of caudad pointed spines.

No posterior spines.

Anteriorly 3-u rows of caudad pointed spines.

No posterior spines.

Anteriorly h-S rows of caudad pointed spines.

No posterior spines.

Anteriorly h—S rows of caudad pointed spines.
Posteriorly 1-2 rows of cephalad pointed spines.
Anteriorly h-S rows of caudad pointed spines.
Posteriorly 1-2 rows of cephalad pointed spines.
AnteriorlY'h-S rows of caudad pointed spines.
Posteriorly 2-3 rows of cephalad pointed spines.
Anteriorly h-S rows of caudad pohnted spines.
Posteriorly 2-3 rows of cephalad pointed spines.
No spines anteriorly.

Posteriorly 3-h rows of cephalad pointed spines.
No spines anteriorly.

Posteriorly h-S rows of cephalad pointed spines.

Measurements of the larger spines were .27 mm. long and

.16 mm. wide. Rows of spines taken arbitrarily on segment 7

were between S and 7 in number. This procedure was undertaken

for every larval stage and host. The above three specimens

were located in the neck of the host. No examples of larvae

110

in the scrotum.were obtained for this stage. The cephalopharyn-
geal apparatus measured 1.22 mm. long and .65 mm. wide, but
was otherwise too badly damaged for morphological comparative
study. However, embedded in the larvae, an additional oral
skeleton was found which was smaller in size resembling a
first stage larval oral apparatus (Figure 22). The latter
example was more intact and measured .h8 mm. long and .17 mm.
wide.

Structure of the posterior spiracles (Figure 5) showed

vertical spiracles measuring .10 m. long and .028 mm. wide. P03-

terior spiracular plates measured .17 mm.wide and .114 um. long.
There was no evidence of a button in the posterior spiracles.
The cuterebrid species peculiar to these three similar second
instars was Cuterebra fontinella Clark.

Third stage. Five larval examples of third instars were
collected for the systematic study. Locations of these larvae
at time of the collection were in the neck and in the scrota.
The color of the larvae varied from.light brown to brownish
black. The average length and width of these third stage
larvae was 1h.6 and 7.9 mm. These measurements were taken
from larvae offering ranges of 10 to 22 mm. in length and 6
to 11 mm. in width. Ranges for the length and width of the
larger spines were .28 to .32 mm. and .19 to .21 mm. respec-
tively. One to six points were discovered on the short stubby
spines (Figure 23) and were frequently seen in the larval

segments. In segment 7 the rows of spines were found to be

Fig. 22. The cephalopharyngeal apparatus of a first
stage larva of Q. fontinella, obtained from a

white-footed mouse. #iote the foramen in the
mandibular hook sclerite.

 

 

as

961’“!

rut

Fig. 22

 

111

Fig. 23.

Multi-pointed spines of a third stage larva
of Q. fontinella obtained from a white-footed
mouse.

112

 

113

from 15 to 20. The arrangement and number of rows of multi-

spines per segment is described below.

Segment 1. No multispines present.
Segment g. Anteriorly, multispines present in first 2-3
POW! e

Posteriorly, multispines in last row.

Segmmot 3. Same as 2.
Segment g. Same as 2.

Segent 5. Same as 2.
Segment 6. Anteriorly in first 5 rows.

Posteriorly last 2 rows.
Segment Z. Anteriorly in first 5-6 rows.
Posteriorly last 2-3 rows.
Segment 8. Anteriorly in first 6 rows.
Posteriorly in last 3 rows.
Segment 2. Anteriorly in first 6-7 rows.
Posteriorly in last 2-3 rows.
Segment 10. Anteriorly in first 6-7 rows.
Posteriorly in last 2-3 rows.
Segment 1;. Anteriorly in first 6-7 rows.
Posteriorly in last 3 rows.

Segment 12. Multispines scattered throughout segment.

It was noted upon microscOpical examination of the spines
that the larvae from the white-footed mouse were red in color,

especially in segment 9. The structure of the posterior

11h

spiracles, peculiar to mature larvae, is seen in Figure 5.

Six bundles of greatly convoluted spiracles, each measuring

.36 and .13 mm. in average lengths and width, were obliquely
arranged in their individual spiracular plate. Each kidney—
shaped plate contained two oblique slits which sinuously sep-
arated the spiracles. These plates were .65 mm. long and .M3
mm. wide. Total length and width of the posterior spiracles
was .9h and .65 mm. accordingly. Buttons were recognizable

in the spiracles. Cephalopharyngeal skeletons averaged 1.88
and .68 mm. in length and width (Figure 2h). Cuterebra ggm:
tinella was the proposed species for these larvae. Verification
of the Cuterebra species was carried out from taxonomic features
found on a puparium.which.had given rise to an.2, fontinella

fly.

Pupariumm As was previously mentioned the necessity of
obtaining the puparial cases related to identified adult flies,
was pertinent for confirmation of mature larvae. This con-
firmation process was possible through studies on the pupal
cases which are hardened mature third stage larvae (Figure 25).
Thus, any features discovered on pupal cases are transmittible
to any mature larvae of that species. The determination of
the species Cuterebra fontinella Clark, proposed for the white-
footed mouse, has been verified through similar characteristics

on the known pupal case.-

Fig. 2h. The left side of a cephalopharyngeal apparatus
of a _C_. fontinella third stage larva obtained
from a white-footid mouse.

 

 

 

115

Flee 2h.

 

Fig. 25.

A dorsal view of a pupal case of g, fontinella
after the emergence of a fly. The object
above is the pupal cap which has two everted
anterior spiracles at its kmer border. The
puparium is lined internally with a thin white
silken membrane. Remnants of the cephalo-
pharyngeal apparatus are seen at the top
resting on the venter inside the case.

 

q ..-~.

_ .. -_._-_

 

 

116

 

 

. . liq-1f

117

,Three pupal cases of Cuterebra fontinella, averaging 19.6
mm. in length and 10.6 mm. in width, were obtained from.the
pupation experiments carried out in the laboratory. Emergent

adult flies were sent to Dr. Sabrosky and identification to
the above species was confirmed by him. Upon investigation
of the pupae, it was found that the pattern and shape of the
spines were identical to those proposed for the third instar.
Also similar were the structures and measurements of the pos-
terior spiracles and of the oral skeletons. The only differ-
ence existing between the third instars and the puparia was
the length. It was noted that the pupae had reduced their
length, on the average, by2 mm. because of the process of
shrinking and dehydration necessary for pupation. By retro-
gressing it was possible to survey all the larval stages and
see whether the original species determination was valid or

not. In the case of Cuterebra fontinella it definitely was.

7. Cuterebra in Sylvilagus floridanus mallurus
8- 992.2252;

Third stage. Nine larvae were obtained from Pennsylvania
cottontails of which six larvae were recorded as located in
the scrota of the hosts. The remaining three larval examples
were from the neck. None of the larvae were mature. The.
average length and width of the larvae were 20 and 11. mm.
respectively. After surveying the posterior spiracles of

118

the larvae, their structures resembled those of‘g. buccata.
Therefore, the nine larvae were suspected of belonging to

this Cuterebra species. Studies on the larval segments re-
vealed spines having single and two points. Comparatively
however, the nwmber of two pointed spines was not as great

as the gmterebra horripilumm More two-pointed spines were
found on the dorsal aspect of the larvae than on the ventral.
Larger spines had ranges in length and width of .38 and .50
mm. and .32 to .h2 mm. The nwmber of rows of spines taken in
segment 7 varied from.15 to 20. Oral mouthparts peculiar to
these larvae were quite similar in pattern-and approximate
measurements to those determined as Q, yuccata inԤ. floridanus
mearnsii cottontails. Measurements on these cephalopharyngeal
skeletons were 2.2 mm. long and .98 mm. wide. Posterior
spiracles revealed lengths and widths of 1.08 and l.hh.mm.
Individual spiracular plates measured .98 mm. long and .h8

mm. wide. Thus, with these similarities, the nine larvae

were listed as Cuterebra buccata Fabricius.

Puparium. One pupal case, measuring 21 and 13 mm. in
length and width was obtained by pupation experiments. An
adult fly identified to this species had emerged from the
puparium. Retrogressing it was discovered that the original
species presentations peculiar to third stage larvae found in
cats, dogs, and rabbits were shmilar to pupal features.

Three pupal cases, averaging 22.5 mm. long and 11.6 mm.
wide, from.which adult'Q. buccata had emerged.were submdtted

119

this laboratory by Dr. Sabrosky for study. The previously
determined characteristics presented for the-mature larvae

were confirmed upon examination of the puparia.

8. Cuterebra in Sglvilaggs floridanus mearnsii

a. g. horripilum

First stage. A single example of this instar was obtained
during the Mason game farm study. The length and width of
the early larvawere 5 and 3 mm. respectively. Single and
multipeinted spines were seen on the larval segments. However,
the former spines were more predominant. These spines ranged
from .12 to .17 m. in length and .0113 to .086 mm. in width
using the larger spines as examples. Pattern of the posterior
spiracle was similar to those in Figure 7 which is peculiar
to early instars in 19.133. domestica. The length and width
of the posterior spiracles were .50 and .36 m. respectively.
Individual spiracles measured .19 and .09 mm. for the length
and width. The arrangement and number of spines were similar
to those of larvae found in the cat. Oral mouthparts revealed
a morphology similar, if not identical, to that in Figure 9.
The oral skeleton measured .68 and .36 mm. in length and width.
This example was relegated to Cuterebra horripilum.

120

b. 9, buccata

Second stage. Two sources of larvae from.cottontails
were obtained in this stage; one from.New Jersey rabbits and
the other from.Nichigan cottontails. The color of the larvae
was white and they had an average length and width of lh.0
and 5.0 mm. respectively. Larvae from.New Jersey had long
delicate single pointed spines measuring .35 and .21:mm.
for the average length and width. Further studies on the
spines revealed a pattern and number similar to that found
in the cat. However, the posterior spiracles resembled that
of the dog Cuterebra in size and pattern (Figure 17). The
spiracles were smaller than those of Q, hmmmmilum, having
average length and width of .142 and .29 m. They were nega-
tive for buttons. Also the oral skeleton was discovered to.
be smaller than 9, horripilum.in length and width, measuring
.75 and .36 mm. The oral mouthparts of the New Jersey cotton-
tail larvae resembled that of the Canis species (Figure 16).
Thus, with this comparative presentation it seemed that the
larvae occurring in New Jersey rabbits were Cuterebra buccata.

Second stage larvae collected from Mason rabbits appeared
similar to those of New Jersey cottontails and to those larvae
from.§mml§ familiaris. These similarities are seen in the
shape, measurement and arrangement of spines. Also the oral

skeleton and posterior spiracles were respectively identical

121

in structure and measurements to those of the cat, dog and New
Jersey rabbits. Therefore, these larval stages peculiar to

Michigan cottontails were reported as Q, buccata.
a. Q. horripilum

Third stage. Twenty-five larvae collected fromq§.‘£;ggl-
.gmmmg mearnsii cottontails were determined as E, horripilum.
The greatest length and width was a mature larvae with 32 and
17 mm. respectively. It was noted upon investigations that
one and two pointed spines existed on the larvae. They re-
vealed posterior spiracles and oral skeletons similar to those
of the previously discussed'Q. horripilum in cats. Measurements
on these structures were larger, in average, than these re-
corded in cats. Posterior spiracles were 1.5 mm. long and
.8h mm. wide. The length and width of the posterior spiracular
plates were 1.0 and .h6 mm. accordingly. Oral skeletons re-
vealed an average length and width of 2.6 and .92 mm. Larger
spines found on these larvae gave lengths ranging from..38 to
.50 mm. and widths ranging from..28 to .32 mm. These measure-
ments were greater than those peculiar to third instars in
cats which indicates that these larvae were more mature. How-
ever, the collection of‘Q. horripilum.third instars were dis-
covered to be in their early and mid-phases of that stage. No

mature third stage larvae were studied in.this species.

122

b. 2, buccata

Third stagg. Twenty-two larvae had predomdnantly
single pointed spines on their segments. Approximately one
dozen of these larvae were in the mature state of the third
stage. Ranges for their length and widths were 25 to 30 mm.
and 1h to 18 mm. Larger spines revealed.ranges of .38 to .hS
mm. in length and.28 to.32 mm. in width. The posterior spir-
acles had lengths and widths averaging 1.08 and l.hh mm.‘
Spiracular plates were 1.00 mm. long and .58 mm. wide. Oral
mouthparts revealed an average length and width of 2.5 and
.98 mm, respectively. The previous measurements were taken
from mature larvae which were determined as‘g. buccata and

resembled those discussed in cats.

a. Q. horripilum

Puparium. Five pupal cases, averaging 26 and 17 mm. in
length and width, were obtained from pupation experiments.
The adult flies which emerged from.the puparia were confirmed
by Dr. Sabrosky as Q. horripilum species. Studies on the
pupae revealed species characteristics identical to those pre-
sented for the third instars occurring in cats and cotton;
tails. Segment 11 in the posterior rows of spines had.

intensely orange colored spines.

123

Iv . DISCUSSION

There appears to be no evidence in the literature of
intensive studies on Cuterebra larvae occurring in cottontails,
especially in.Nichigan rabbits. In general, pertinent refer-
ences have been minor observations encountered accidentally
in zoological studies, such as Wildlife and.Mammalogy. Though
these observations are beneficial, they are merely mdnute
fragments of the Cuterebra picture and may be subjected to
various interpretations by different zoological workers. It
is thought that this two-year cuterebrid larval investiga-

' tion of Sylvilagus floridanus mearnsii is, at present, the
most specific in relation to life history, ecology and syste-

matics.

A. LIFE HISTORY

The mode of infection hypothesis that the cuterebrid
eggs are laid on food plants of the host, and when the ani-
'mal feeds, the eggs are ingested (Townsend, 1935) was in
serious doubt because the acquisition of a cuterebrid infec-
tion in a caged cottontail not exposed to natural vegetation.
The probability that the sampling data of Cuterebra were
specifically limited in these mode of infection experiments,
involving 22 bait pen rabbits, was realized. However, with

12h

the obtained data acquired by these studies, it is believed
that the mode of infection does not entail the eating of
cuterebrid egg-infested vegetation by the host. The hypothe-
sis presented by Allison (1953) that rabbits acquire infec-
tions by brushing against vegetation having first Stage larvae
is also deemed invalid on the basis of the above experimental
results.

As a result of the life history study, it is not main-
tained that the adult females lay their eggs on definitely pre-
disposed areas of the hosts such as the neck or scrota. Nor
subsequently, that these eggs hatch into first instars which
dig through the skin, using their oral hooks, and directly
settle subcutaneously in these areas as final infection sites.
Evidences supporting this belief were that no first stage
larval swellings had scars overlying the tumorous areas (indi-
cating larval entry) and that no early instars had air holes
which the larvae would use seemingly to facilitate breathing
by the posterior spiracles. Beamer (1950) stated that the
eggs may be seen with the naked eye. In this study no eggs
were observed on these predisposed areas in 170 Mason Farm
cottontails, especially in those rabbits recaptured within
15 days time between an obvious negative condition and an
obvious third stage larval infections Dalmat (19h3) observed
that as many as h50 to 1000 eggs have been counted from female
cuterebrid flies. It would seem.that oviposition on predis-

posed areas of the host by adult females is unlikely due to

125

the few larval infections found in these areas of the host.
These few infections would infer that the cuterebrid eggs
were quite vulnerable to environmental conditions. To the
contrary, Parker and Hells (1919) discovered that the eggs
lived six months in a laboratory container and even then some
were viable.

Suggestion of cuterebrid larval migration was found in
the study on the duration of instars. Two third instars
appeared in one side of the neck of a cottontail, diagnosed
as negative in that area a week previously. With the possi-
bility of migration in cottontails, it was thought that evi-
dences of migration could be found upon autopsy in infected
dead rabbits. It was known that the larvae of gypoderma
lineatumlshowed migratory routes in the tissues of their hosts
and in this manner larval migrations were anatomically traced.
In sixty-two cottontails autopsied no evidences of migration
such as routes or larval stages were ever seen in.muscles,
mesenteries or other body areas. Hewever, inasmuch as early
instars were found subcutaneously in the neck, it was believed
that the migration to their final infection sites was done by
the first instar. First stage instars were found in this
study melting to the second stage and the second melting to
the third stage all in one infection site. In one case an
early instar was extracted frdm a caseous cyst which was dis-
covered underlying the skin. Externally there was no scar.

Thus, it was maintained that the larva was inactivated by

126

the reactions of the host when the parasite reached its final
location through internal means in the host. Another finding
that suggested migration was that larvae in a.multiple infec-
tion of a rabbit were discovered not to be in the same phase
of larval development. Larvae in the same area of the host
were observed upon maturation to drop during a period of from
one to three days.° This condition, it is believed, would

not be prevalent if eggs were laid by flies in predisposed
areas. Rabbits with.many larvae were held in the laboratory
after the dropping period to see if other larvae would appear
which might indicate more than one infection in the host. No
detained rabbits showed this type of infection.

Because of the shortness of the life cycle, approximately
one month, ascertained by Scott and Snead (l9h2), it was felt
that the migration was a short one. Reason for this belief
was that since the time of the third instar in the host was
determined in this study to be 15 days, few days would be
left in a month to allow for an extensive migration for the
first stage and melting to the second and consequently to
the third stage. Possible areas of short migrations in re-
lation to final infection sites were examined. Oral and nasal
passages were checked in twenty—five rabbits along with eso-
phageal and tracheal areas. Also the soft abdominal skin
adjacent to the scrota of’mmle cottontails were investigated.

Probably due to the’Sampling, negative results were obtained.

127

It was discovered in this study that some cottontails had
larval infections in the areas of the cheek. Records of
anatomical locations of infections in the veterinary samples
submitted to the laboratory were from.the eyelid, nares,
cheeks, chin and neck of domestic mammals. Philip and as-
sociates (1955) found multiple larval infections occurring
in Nevada Jack rabbits (Figure l) in the region of the eyes,
chin and cheeks. It seemed likely from the above examples
of larval infection sites that oral and nasal cavities are
the sites of primary infection initiating a short migration
of first stage larvae to these infection sites. This con-
tention is partially supported by the fact that no evidences
of larval migration were seen in the areas other than the
head and the neck.

The use of air hole diameters in determining the age of
the larvae found in infected cottontails is believed to be
of practical significance. It was discovered and applied in
this study for the first time and was shown to be useful in
inspecting infected cottontails for laboratory studies on
duration of instars. As the larval air hole approached that
diameter peculiar to mature larvae, the host was carefully
watched for the dropping of the mature larvae and their pupa-

tion in the soil trays to record their behavior and time of

pupation.

128

B. ‘ECOLOGY

There is no apparent record in the literature on the
seasonal periodicities of immature cuterebrid larval stages
in.Nichigan cottontails. It was found in this study that
the first appearance of a first instar in a Michigan cotton-
tail was on June 28, 1953. A second instar in a wild rabbit
was recorded on July 25, 1953. Because of the paucity of
.earlier instar larvae, it is felt that these months do not
respectively show the seasonal periodicities of the mentioned
larval stages. In this study it has been determined that the
seasonal peaks of mature larvae were found between August 1
and 20 (Graphs 2, h, 5, 6, 7, 8) and that the length of the
'Cuterebra life cycle in the host was approximately one month.
Thus, it is believed that the seasonal periodicity of the
first instar larvae should occur about one month previous
to the seasonal peaks of mature larvae in the early part of
July. .

Frem.this study it was believed that certain conditions
conducive to cuterebrid infections existed. The best situa-
tion for cuterebrid infections was thought to be the nest or
burrow of the host. This belief was partially supported by
the fact that more larval infections occurred in areas having
the highest density of rabbit burrows. Young cottontails
determined by weight measurements (Petrides, 1951) to have

recently left their nests were discovered infected with

129

Cuterebra larvae. Also adult female rabbits which were in the
process of lactating were found with infections.

Periods of aestivation by cottontails were noted prior
to cyclic peaks of larval infections. Rabbits at these
times were seen in their burrows or shady areas during the
day hiding from.the hot sun rays of July. Perhaps it was due
to the subsequent increase in rabbit captures that these high
numbers of cuterebrid infections occurred. Nevertheless, the
fact that these ”highs" did exist after these aestivations
revealed a possible relation between adult flies and infec-
tions in burrows or shady areas. The capture of an adult fly
atOp a rabbit burrow may or may not add further evidence to
this.

In relation to the high larval incidence of Cuterebrg
in areas having the highest density of burrows, a fact noted
afterwards was that the soil type of these areas was of a
sandy nature. The best example was sandy loam. Results ob-
tained on the influence of soil in pupation experiments re-
vealed that mature larvae burrowed best and fastest in sandy
soils. It was concluded therefrom that the reason for greater
larval infections in areas of greater number of burrows was
that more successful pupations occurred and more cuterebrid
flies emerged in the sandy areas. This ecological situation
is believed to be contributory to more infections of the

rabbits in their burrows.

130

It was felt after the first trapping program.cf 1953
that the sampling data of Cuterebra larvae were rather limited
in number. This was believed due, in part, to the inexperience
'of trapping cottontails on the Mason farm and of interpreting
cuterebrid material. However, comparing results obtained from
the second trapping program.at Mason in l95h and the cotton-
tail studies on the Kellogg Station, it was discovered that
the number of cuterebrid infections in cottontails was nor-
mally small. Added to this fact was the low natural popu-
lation of cottontails encountered during the summer trapping
which decreased the cuterebrid sample material further.
Though.seemingly this was abad time of the year to study
this host-parasite relationship, it was the only valid time
to do so ecologically. Graphs 2, h, S, 6, 7, 8 on the
seasonal incidences of larval infections revealed this eco-
logical situation to be true.

It was thought at the onset of this study that adult
cuterebrids could be lured into fly traps with the use of
various baits. Curran (193h) stated that the adult cuterebrids
have poorly developed mouth parts and that the adult flies
were believed incapable of feeding. Thus, it would appear
that the Quterebra flies were only reproductive in nature.
However, inasmuch as there was no previous work done on
baiting cuterebrid flies, the experiment was established to

observe whether the adult flies would employ baits similar

131

to those used for Diptera, such as horse flies. The results
obtained.in this bait experiment were negative.

Hewever, applying the ecological knowledge of the adult
flies that they frequent the host's burrows (Townsend, 1915),
an adult fly was captured in an unbaited fly trap atop a
cottontail burrow. Thus, it appeared from this study that
the baiting of fly-traps for capture of adult cuterebrids
was not the proper method. By employing ecological situa-
tions pertinent to the fly,results were obtained. The possi-
bility that this capture was merely a chance condition was
realized. However, the chances seemed to be increased by

placing the trap in that ecological site.

C. SYSTEMATICS

Another subject presented for discussion is the presence
or absence of the buttons in the posterior spiracles of outer-
ebrid larvae. The status of the buttons is necessary in
order to classify the Cuterebra posterior spiracles as to
schizotreme or ptychotreme types of stigmata for dipterous
larvae presented by HacGreger (l9lh). Greene (1925) stated
that no buttons were found in the Cuterebridae. The stage
of the larval example described by that author was not speci-
fically given and conclusions therefrom were not obtained.
Knipling and Brody (l9h0) and Dalmat (l9h2) have shown but-

tons in third instarsg_ From.the systematic study of various

132

instar examples of Cuterebra stigmata, it was found that no
distinct buttons as shown by the three above workers were
seen in the early larval instars. In this study, buttons
were observed in the third instar stigmata of Q. horri ilum,
buccata, fontinella and the Cuterebra species of Nevada Jack-
rabbits. MacGregor (1911;) in his definition of a ptychotreme
stigma related that the button was always present and usually
very distinct. The above author also stated that the ptycho-
treme type had alvery marked ring which is the thickened

a...“
{i ”I 'n'- ANr‘.-.‘ _._‘..,

periphery of the stigmal plate. In the present study no
heavy ring was seen peculiar to this type of stigma. How-
ever, one distinct feature pertinent to ptychotreme stigma
was observed. This morphological characteristic was that of
a convoluted chain, either broken into segments or unbroken,
which was situated within the ring. It appeared that the
cuterebrid stigma or posterior spiracle did not distinctly
classify into either type as both types were reflected.in the

Cuterebra. It is believed that an intermediate evolutionary

position exists for the cuterebrid stigma in between the
schizotreme and the ptychotreme types of dipteran stigmata
approaching the ptychotreme stigmata. Evidence of an evolu-
tionary link was seen in the earlier stigma of second stage
larvae of g. fontinella which had straight rods of spiracles
peculiar to the schizotremeexample (Figure 6). It is hoped
that a more complete study on this taxonomic subject will be

carried out in the future.

133

Having a sizeable sample of cuterebrid larvae (127 repre-
sentatives), it was possible to determine new ranges and
larger coverage of morphological characteristics to present
for larval species determinations. It was with this idea
in mind that these results were compared, with those of pre-
vious workers (Tables XIV, xv, XVI). Knipling and Brody ’ s
(l9h0) in their presentation of Q, buccata and Q, cuniculi= 7 I

horripilum.offered procedures and measurements which.were
used in this study. The present work contributed to the

[7—7 "‘2. ...pl vs .. a

taxonomy of the first and second stages of,§. horripilum in ' on;
which new measurements on morphological structures were ob-
tained. The above authors presented in their taxonomic
studies the greatest lengths and widths of the cephalopharyn-
geal skeletons of’Q, horripilum and‘g. buccata as 5.5 mm. and
2.7 mm. and h.mm. and l.8 mm. respectively. Compared to the
measurements obtained in this study (Table XVI) they appear
to be twice asggeat. Oral skeletons here were measured by
recording the dimensions on the heavily chitinized structures,
that is.the oral, hypostomal sclerites and the dorsal and
‘vontral arches. The dorsal and ventral cornua were not con-
sidered in the measurements, as it was believed that these
softer structures would be damaged upon dissection by inex-
perienced workers and would result in abnormal dimensions.

It was discovered that if the dorsal and ventral arches were

measured, the measurements would approximately equal those

TABLE

A COMPARISON OF FIRST INSTAR gg
‘WITH MEASUREMENTS OBTAIN

 

 

‘Q. horripilum ‘Q. 23
Boisvenue Knipling & Boisvenue
(Average of 6) Brody (l9h0)
Aver. length h.88 mm. No No
” width 2.38 mm. First Instars First Instars

—

Spines:
1 and 2 pointed spines
Spine length .12-.17 Me
N Width eOh‘eOB Me

Posterior Spiracles:
Length ehB‘eSO m.
Width .36-.38 mm.

 

0rdl Skeletons:
Length .68-072 Dune
Width e32'e36 Me
M

 

 

13h

XIV

TEREBRA SPECIES CHARACTERISTICS
SE B? TAXONOMIC WORKERS

 

 

 

 

seats 9, fontinella ‘Q. peremysci Cuterebrgggg.

Knipling a Boisvenue Dalmat (l9h2) From.Nevada

Brody (l9k0) Moulting l Larva Jack Rabbits
No First Instar Length.h.2 mm. No

First Instars l larva only ‘width. 3.2 mm. First Instars
in which only
oral skeleton
was obtained

 

Oral Skeleton: Ne record of
Length .h8 mm. oral skeleton
Width .17 mm.

 

 

TABLE

A COMPARISON OF SECOND INSTAR OU
WITH MEASUREMENTS OBTAIfi

 

 

 

 

 

 

 

g. horripilum 5;. pg
Boisvenue Knipling & Boisvenue
(average of 12 larvae) Brody (l9h0) (aver e of 3)
L. 11.0 mm. L. mm.
We lies Me N0 We 5 mm.
Full grown larvae: Second Instars
L. 15 mm,
w. 6 mm.
Spines: Spines:
l and 2 pointed 1 point
Le e35 m. . L0 033 mm.
He e16 mm. W. e19 Me
Posterior spiracles: Posterior
L. .65 mm. Spiracles:
U. ell-2 we Le ens mm.
W. .31 mm.
Oral skeleton: Oral skeleton:
L. .86 we Le e7 Me

U. 014.3 m. We e3 Me

XV

TEREBRA SPECIES CHARACTERISTICS

WAXONOMIO WORKERS

 

1.35

 

 

 

 

 

ccata 'Q; fontinella 'Q. peromysci Cuterebra 32,
Knipling & Boisvenue Dalmat (l9h2) Nevada
Brody (19h0) (average of 3) (average of h) Jack rabbits
(average of 2) L. 9.5 mm. L. 9.5 mm. Boisvenue
L. 10.5 mm. W. h.3 mm. W. 3.0 mm. 1 larva
W. h.5 mm. L. 1 mm.
W. mm.
Spines: Spines: No spines re- Spines:
1 point 1 and multi- corded l and multi-
No record pointed A.pointed
L. .09 mm. L. .29 mm.
We e03 We We e17 mine
He record Spiracular Spiracular Posterior
plate: plate: Spiracles:
Le en)- Me Le e12 Me Le e26 m.-
We e17 We We e18 m. We e15 we
L. 1.6 mm. Oral skeleton: Oral skeleton: Oral skeleton:
W. .75 mm, L. 1.22 mm. L. 1.1 mm. L. .72 mm.
W. .65 mm. Ne width re- 14. .29 mm.

 

corded

 

 

1
’—

TABLE

A COMPARISON OF THIRD INSTAR‘QQ
WITH MEASUREMENTS OBTAIN

 

 

 

 

 

 

C. horripilum C. bu
Boisvenue Knipling & Boisvenue
(average of 33) Brody (l9h0) (average of 37)
L. 32 mm. L(Number?) L. 15-30 mm.
“o 17 me 35‘h3 m. w. 8‘18 mne
Spines: Spines: Spines:
l and 2 pointed 1 point
(rare 2)
LO 038-:5g$ Le 065$0 mm. Le 038'. 1‘5”.
“0 028 " We 055955m W. 028-0323“
Posterior spiracles: Spiracular
plates:
Le 1e6 Me Le 1e]. me Le 1.00 We
W. 081‘. we W. Go; Me W. e58 Imne
Oral skeleton: Greatest Oral skeleton:
L. 2e2’206 m. Le 505 m. Le 200-205 m
U. e92'1008 min. W. 2e? me we e75‘e98 mme

 

 

136

XVI

TEREBRA SPECIES CHARACTERISTICS
ED BY TAXONOMIC WORKERS

 

7-- _. _-_ “—_.—.»—-—.~—b” ——q’.—.~ FW-h,-_

   

 

 

 

 

ccata: 7 ‘Q. fontinellat“ Q, peremysei Cuterebra.52,
Knipling a Boisvenue ~ Dalmat (1913) Jack-rabbits
Brody (1914.0) (average of 5) (average ef16) of Nevada
(average of k). Boisvenue
L. 26-32 m. L. 111.6 m. L. 20-25 mm. (average of 18)
H. one-half I. 7.9 mm. 'U. 7.5-7.8 mm. L. 25.h.mm.
We 11.2 Me

Spines: “Spines: Spines: « - Spines:

1 point (2) 1-6 points l-h points 1-3 points

Le ehOJAS me Le e28‘e32 W Le e36‘eh1 we Le e38'058 m
U. eBO-eBSmme U. 019-e21 Me "a 025-030 M. W. 032-05“. me

 

 

‘ Spiracular' Spiracular Posterior
. plates: plates: epirscles:
Le e88 mm. ' Le e65 Me Le e91 Me Le 1.01-1.20 mm»
W. 0&5 Me U. eu3 mule We e33 Me U. e65-e80 Me
Greatest Oral skeleton: Oral skeleton: Oral skeleton:
Lo ’4. ms Le 1.88 m. Le Zes Me Le 2.30.2. mm.
W. 1.8 m. . w. .68.me ' NO Width re“ We 1.00-1.0 mme

corded

 

 

 

 

137

presented by Knipling and Brody (19h0). Thus, it was main-
tained that the most stable procedure for recording measure-
ments on the oral skeletons was that of considering the heavily
sclerotized structures which make up the skeleton.

Knipling and Brody (19h0) made studies on the anterior A
spiracles which were not used in this study. It was felt
that since measurements of the structures were only recorded,
the anterior spiracles were not significant systematically
‘as posterior spiracles, oral skeletons and spines whose mor-
phology and measurements were determined.

Dalmat (19h2) presented first, second and third stage
larval descriptions of Q, peromysci. The above author stated
that the adults of Q. peromysci closely resemble those of19.
fontinellg. It was found in the larval study of these two
species presented in Tables XIV, XV, XVI, that the larvae
also closely resembled one another. However, differences
were seen in the second instar which.Da1mat (leg. git.) main-
tained had a transverseband.of spines on anterior margins of
all but the first segment of Q, peromysci. Present observa-
tions on‘g. fontinella showed no transverse band of spines
on the anterior margins of segments 10 and 11. The spines
found on the larval segments of the third instar of 9, £22;
tinella had 1 to 6 points, whereas those recorded for Q,
peromqsci by Dalmat (lgg.,gi§.)~were l to h points. Also it

was discovered that the mature larvae of Q. fontinella had a

138

reddish appearance due to the spines being colored red. Dal-
mat (lgg. git.) does not state the color of his mature larvae,
but it is asswmed that it was a normal dark brown or he would
have mentioned it. Measurements recorded on mature larvae
of‘g, fontinella and peromysci (Table XVI) indicated that the
.2. peromysci were generally larger. 8

The predominant species of Cuterebra found on Michigan
cottontails waslg. horripilum, 0f the twenty-five larvae
collected from.the cottontails, 18 were determined to be
9, hgrripilwm. The remaining seven were 9, buccata.

Twenty-six larval specmmens were obtained from Pennsyl-
vania cottontails. This sample contained twenty larvae
classified as 2, buccata. The remaining larvae were 9,
horripilum, Thus, on the material collected it would appear
that Q, buccata is the predominant species occurring in Pennsyl-
vania.

In the white-footed mouse, thirteen larval specimens col-
lected in Michigan were determined as Q,‘£pntigella. Thus,
it is thought that the predominant cuterebrid species occur-
ring in the Michigan Peromyscus leucopus is Q, fontinella.

The most frequent larval species collected fromlzglis
domestica waslg. horripilum. Thirty-five larvae out of fifty
were relegated to this species. 9, buccata were the remaining
species.

Referring to the Appendix, Cuterebra fontinella and
QQEEEEEEEE have been recorded in Michigan. However, the

 

139

incidence of these species in their respective hosts could
not be ascertained from the literature. Records from.Penn-
sylvania have shown that‘Q. buccata has been found there.

New Jersey cottontails were discovered to have‘g. buccata lar-
vae, which was confirmed with the finding of that species in
that state. However, there are apparently no records of‘Q.
horripilum.in that state. Thus, it is presented here that in
the eleven larvae received from Dr. Hansens, four larvae were
identified as Q, horripilum.

As a result of the systematic study, it was felt that
identification of larvae to species should be carried out
through a known adult fly-pupa series. Inasmuch as the taxon-
omy of adults was more stable than the larvae, the prime stand-
ard of verification was the fly. Thus with a definitely iden-
tified adult fly which had emerged from its pupa, it was pos-
sible to study pupal morphological characteristics which simi-
larly reflected the situation in the mature third instars.
With features of the third instars it was not hard to work
back to the second and first stages, assimdlating the charac-
teristics originally determined from the puparium. Through
comparison of these features among various larvae, a key was
constructed (page lul) which distinctly separated three cuter-
,ebrid species, namely fi,‘£gntinella, Q, buccata and‘Q.lhgg;
ripilum. The unidentified cuterebrid species found on Nevada

Jack-rabbits is also presented in the key. In employing this

 

adult fly-pupa series method of identifying the larvae of
Cuterebra to species, it is rather difficult to deny the

validity of the species found in this manner.

mo

1L1

A Key to the Species of Cuterebra Larvae in This Study

1. Body white to cream-colored; spines arranged in several
somewhat irregular rows that encircle the body; posterior
spiracular platesbisinuate; larval length 2-15 mm., width.
1-6 mm. ----Cuterebra s22. (First and Second Stage) 2
Body light brown to black; spines or pointed scales
closely set covering all of the surface of each segment;

posterior spiracular plates divided into three divisions;

larval length 15-h3 mm., width 8-18 mm.-------—--e -----
--------------- --------Cuterebra app. (Third Stage) 6

2. Larval length 2-5 mm., width 1-2 mm.; spines showing a
haphazard arrangement in first four anterior segments;
1 row of anterior spines on segments 10 and 11, no in-
termediate spines; spiracular plates (Fig. 26), .h8 mm.
long and .36 mm. wide; cephalopharyngeal apparatus (Fig.
27) .72 and .32 mm. long and wide (cat, cottontail)----
........................... -9. horripilum (First Stage).
Larval length 6-15 mm. width 3-6 mm.; spines not showing
a haphazard arrangement in first four anterior segments
--- ............. -----0uterebra‘gpg. (Second Stage) 21

28. Transverse row of spines on all but first segment-- 3
Transverse row of spines lacking on segments 1, 10, ll

------ __________________ _ ____________ --- ........... 5

.r N
«as! '1

Fig. 26.

Fig. 27.

Fig. 28.

Fig. 29e

Posterior spiracular plates of a first instar
larva of C. horripilum (reduction of Figure 8).

The left side of the cephalopharyngeal appara-
tus dissected from a first instar larva of C.
horripilum (reduction of Figure 9).

Posterior spiracular plates of a second instar
larva of Q. buccata (reduction of Figure 17).

The left side of the cephalopharyngeal appara-
tus dissected from a second instar larva of C.

buccata (reduction of Figure 18).

 

 

1h3

3. All spines single pointed on larval segments; spiracular

plates .12 mm. long and .18 mm. wide; cephalopharyngeal

apparatus length 1.1 mm. (rodents, Dalmat, l9u2)-------
" """""""" ‘ ’’’’ ’ ----------------- --Q, peromysci

Spines predominantly single pointed with infrequent two
pointed spines on larval segments (larvae not on rodents)
------------- ------ ----- ----- --------— ----- - ------- u
h. Single pointed spines greatly predominate, only rarely
two pointed spines on larval segments; posterior spir-
acles (Fig. 28) .u3 mm. long and .32 mm. wide; cephalo-
pharyngeal apparatus (Fig. 29) .72 mm. long and .36 mm.
wide (dog, cat, cottontail)--§-- ----- ----fig. buccata
Single spines predominate with two pointed spines more
frequent; posterior spiracles (Fig. 30) .65 mm. long and
.h2 m. wide; cephalopharyngeal apparatus (Fig. 31) .86
mm. long and .u3 mm. wide (dog, cat, cottontail)--e—---
-- ------- - ----- --- ------- --- ---------- ----§, horripilwm
5. Three pointed spines infrequent; spiracular plates (Fig.
‘32) .13 mm. long and .09 mm. wide; oral skeleton (Fig.
33) .72 mm. long and .29 mm. wide; larvae found on.Jack-
rabbits of Nevada-- ------ --Cuterebra g2. (unidentified)
Three pointed spines frequent; spiracular plates (Fig.
3h) .lh mm. long and .17 mm. wide; cephalopharyngeal
apparatus 1.22 mm. long and .65 mm. wide (rodents)-----

-- ---------------- II-n- --------------------- 9.. fontinella

Fig. 30o

Fig. 31.

Fig. 32.

Fig. 33.

Fig. 3h.

Posterior spiracular plates of the second in-
star larva of g, horripilum (reduction of

Figure 11).

The right side of the cephalopharyngeal appa-
ratus of the second instar larva of g, horri-
pilum.(reduction of Figure 10).

Posterior spiracular plates of the second in-
star larva of the Nevada jack-rabbit Cuterebra
species (reduction of Figure 18).

The right side of the cephalopharyngeal appa-
ratus of the second instar larva obtained from
Nevada jack-rabbits (reduction of Figure 19).

Posterior spiracular plates of the second in-
star larva of Q. fontinella (reduction of
Figure 6).

N‘s!

(1“-

I."

 

1&5

6. Posterior spiracular plates not distinctly separated
into 3 divisions (Fig. 35); posterior spiracles 1.6
mm. long and .8h mm. wide; cephalopharyngeal appara-
tus (Fig. 36) 2.h mm. long and 1.0 mm. wide; single
and two-pointed spines on larval segments; orange
colored spines on posterior margin of segment ll
(cat, cottontail)--—--------—--- -------- -59, horripilum.
Posterior spiracular plates distinctly separated into
3 divisions----------- --------- - --------- -- ------- - 7
7. Spines predominantly single pointed, very rarely two
pointed on larval segments, .38 - .hS mm. long and .28
- .32 mm. wide; lacking orange colored spines on seg-
ment ll; posterior spiracular plates (Fig. 37) 1.00
mm. long and .58 mm. wide; cephalopharyngeal apparatus
(Fig. 38) 2.2 mm. long and .87 mm. wide (cat, cotton-
tail)---—-- -------- ------ -------------------- g, buccata
Spines commonly multipointed on larval segments---- 8
8. Larvae from.jack-rabbits of Nevada; spines having one
to three points; posterior spiracles with "macaroni"
pattern (Fig. 39) 1.10 mm. long and .7h mm. wide;
cephalopharyngeal apparatus (Fig. hO) 2.37 mm. long and
1.0h mm. wide----- ------- --Cuterebra gp. (unidentified)
Larvae from rodents ---------- - -------- - --------------- 9
9. Spines having one to four points, .36 - .ul mm. long and
.25 — .30 mm. wide; posterior spiracular plates .91 mm.

long and .33 mm. wide; cephalopharyngeal apparatus 2.5

Fig. 35.

Fig. 36.

Fig. 37.

(Fig. 38.

Posterior spiracular plates of a mature third
instar of C. horripilum.(reduction of Figure
12

The right side of the cephalopharyngeal appa-
ratus from a mature third instar of C. horri-
pilum (reduction of Figure 13).

Posterior spiracular plates of a mature third
instar of Q, buccata (reduction of Figure 1h).

The left side of the cephalOpharyngeal appa-
ratus from a mature third instar of C. buc-
cata (reduction of Figure 15).

me

 

Fig. 35
Fig. 36

 

F
is. 3?
F13
. 38

Fig. 39.

Fig. no.

Fig. file

Fig. #2.

Posterior spiracular plates of a third stage
larva from the Nevada Jack-rabbit (reduction
of Figure 20).

The left side of the cephalopharyngeal appa-
ratus of a third stage larva from the Nevada
Jack-rabbit (reduction of Figure 21).

Posterior spiracular plates of a mature third
stage larva of Q, fontinella (reduction of
Figure 5).

The left side of the cepha10pharyngeal appa-
ratus from a mature third stage larva of Q.
fontinella (reduction of Figure 2h).

 

1h?

   

Fig. ho

 

m8

long, no width recorded (white-footed mouse; Dalmat,
l9h2) ----------------------------------- ---C. ero sci

Spines having one to sproints, .28 - .32 mm. long and
.19 - .21 mm. wide; spines red giving larvae a reddish
appearance; posterior spiracular plates (Fig. #1) .65

mm. long and .A3 mm. wide; cephalopharyngeal apparatus
(Fig. 142) 1.88 mm. long and .68 mm. wide (white-footed

mouse)----- --------------- ----- ------------ IQ. fontinella

1&9

SUMMARY

The life history and ecology of Cuterebra species, occur-
ring in Michigan cottontails, were studied in part by means
of a two-year live trapping program of rabbits. Field obser-
vations on adult cuterebrid flies and rabbits were also
carried out. One hundred and seventy rabbits were captured
and were screened for Cuterebra larval infections. Infected
cottontails were brought into the laboratory and studied for
‘phases of the life cycle.

Records on the duration of third stage larvae in the
cottontails related an average of 15 days. Concurrent with
the above study, it was found that the air hole diameters of
larvae reflected the phases of the third stage larvae while
in the host.

Mode of infection studies were made in the field using
twenty-two penned cottontail and domestic rabbits in areas
having high larval incidences. A positive larval infection
was obtained in a penned cottontail whichxwas not exposed to
natural vegetation.

The primary site of Cuterebra larval infections in 187
southern Michigan infected cottontails was in the neck. Other
anatomical areas recorded were the scrota, cheeks, back and

shoulders.

150

Suggestion of larval migration was obserVed when two
third stage larvae appeared on the right side of the neck of
an isolated cottontail which was externally determined negative
in that area a week previously. A large tumor appeared first
in the area followed.by two larval air holes overlying the
tumor. No evidence of extensive larval mdgratior was found
in sixty-two cottontails which were autopsied throughout the
Cuterebra cycle. 8

The time recorded for the obvious appearance of third
stage larvae in cottontails from a negative determination was
22 days.

First, second and third stage larvae were discovered in
the cottontails which gave seasonal periodicities in their
hosts. The seasonal periodieuw'of third stage larvae was de-
termined to be between August 1 to 20. First stage larvae
were believed to have a seasonal periodicity a month previous
to the third stage larvae in the early part of July.

Seasonal incidence of cuterebrid larvae in southern
Michigan juvenile cottontails was determined to be between
August 1 and 20. 'For adults, it was found to be between July
20 to 30. In general, the juvenile cottontails had a higher
incidence of Cuterebra larvae than adult rabbits. Also the
Innnber"of warbles per infected rabbit was found to be the

greatest when there was a peak in the incidence of Cuterebra

larvae among the cottontails.

 

151

Field notes on pupation showed that mature larvae which
had recently dropped from their hosts were able to survive
9.to 13 days before pupating. Depths recorded on 27 burrow-
ing larvae offered-a range of 1 1/2 to‘2 1/2 inches in sandy I
soils. Field pupation experiments revealed that no two-year
cycle existed for the pupae. Also one generation a year was
shown to exist in.Nichigan for Cuterebra, regardless of ex-
posing the pupae to artificial or natural conditions prior
to the emergence of the flies. Longevity of adult flies were
observed in laboratory pupation Jars to range from.l to 5
days.

Higher numbers of Cuterebra infections were recorded

 

in areas having sandy soils. Also these sandy areas showed
greater numbers of rabbit burrows. This situation was believed
conducive to good pupation and consequently, successful emer-
gence of adult flies with excellent conditions for larval
infections in the rabbit burrows.

Vegetative sites such as dense sumac bushes, willow swales
and clover fields were associated with adult cuterebrid flies.

One hundred and twenty-seven cuterebrid larvae, collected
from cottontails, cats, dogs, jack-rabbits, and white-footed
mice, were comparatively studied and taxonomic differences
were presented for each instar of individual Cuterebra species
studied. The results obtained in the systematic study of

larvae were compared with the findings of previous workers.

152

Buttons, peculiar to posterior spiracles of some dipterous
larvae, were seen in the cuterebrid examples investigated.

A key is presented which separates the various instars
of the individual larval species determdned in the systematic
study. Species of Cuterebra determined in this study were
buccata, fbntinella, and horripilum. An unidentified species,
found on.Nevada Jack-rabbits was described and its larval
characteristics are presented for comparison with the known
cuterebrid species. No pupa-adult fly series were obtained
for the identification of the Nevada species. However, they
'were obtained for the three identified species.

Verification of the three Cuterebra species was accomp
plished by means of a puparium.from.which a known identified
adult fly emerged. With the morphological characteristics of
the puparium.it was possible to retrogress to the third in-
star and subsequently to the first instar of that species.

Larval species found in 221;; domestica were 9, buccata
and horri ilum, with a preponderance of the latter species.
Cuterebra buccata was recorded from_§gg;g_familiaris. Michi-
gan cottontails had both cuterebrid species, withug. horripilum
predominating. The only larval species obtained from the
white-footed mouse of Michigan was 9, fontinella.

A check-list of the Cuterebra species of the western
hemisphere is presented with records of their geographic

locations and the scientific names of their hosts.

153

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159

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160

APPENDIX

A Check-list of Cuterebra Hith Their Hosts and-
Geographic Locations

Cuterebra albifrons Swank (= to Q. princepg, Townsend, 1917).
Lepus californicus and Sylvilaggs floridanus; Arizona
Calif., Nevada, Hyo., New Mexico; Townsend, 1917.*

abdominalis Swank (==to Q. horripilum, Townsend, 1917).

'0 '0
e e

aldrichi Austen.
Neotoma fuscipes f.; California; Austen, 1933.

I0
e

almeidai.
Distribution in Brazil; Guimaraes, 19u1.

Q, emericana Townsend.
‘nggg alleni a.; Arizona; Vorhies and Taylor, 1933.
25225 californicus c.; Arizona; ibid.
'Lgpgg alustris; Mexico; Brauer, 1863.
Distribution also in New Mexico; Skinner, 1903.
In California; Ferris, 1920.

‘2. analis Macquart ( = to Q. emasculator, Van Der Wulp,
1888).
Distribution in Mexico; Swenk, 1905. In Brazil, Macquart,
18h3. In Arizona; Austen, 1895. .

‘Q. apicalis = to Q. analis, Guérin-Méneville, 1829).

Distribution in North America and South America; Guerin-

Meneville, 1829.

...(‘l (I .I.

 

161

Q. moximata Ulk. .
Distribution in Arizona; Townsend, 1917. In Mexico and
Guatemala; Van Der Wulp, 1888. In Vancouver, B. 0.;
Austen, 1895. 8 A

9. 52395 Clk. (= to Q. gimilig, Townsend, 1917)..
Distribution in Mexico; Townsend, 31917.

Q. bgég; Shannon and Greens.
Alouatta sp. (red howling monkey); British Guiana and
Panama; Greene, 1925. : '

Q. beameri Hall.
Neotoma glavidiana osagensis Blair;'Kansas; Hall, 19h3.

‘9. buccata Clk. A _ ‘
Citellus tridecemlineatus; United States; Rathron, 1869.
_I_i_qm_9_ sapiens; Mass.; Bequaert, 19h6.
‘Lgpgg spp.; Penn. and Kentucky; Brauer, 1863.
Oryctolagus cuniculus domesticus; Georgia; Knipling and
Brody, 19h0.
Sylvilagus floridanug; Georgia; Knipling and Brody, 19h0.
Michigan; Haugen, l9h2. Oklahoma; Eddy and Emerson, 19h0.
Recorded in Florida, South Carolina, Penn., Kentucky,
New Jersey, Mass., Minn., Nova Scotia; Swenk, 1905.

' Q, cauterium Clark. . '
.Distribution in United States; Joly, 18h6.

Q, Eggghnensis Macquart.

Distribution in Brazil; Patton, 1921.

162

g, cyanella Jones.
Distribution in Nebraska; Jones, 1906.

‘Q. emasculator Fitsch.
$19919. fifemiliaritg; Canada (Montreal); French, 1893.
Peromyscus spp.; California; Riley and Howard, 189k.
Sciurus hudsonicus etulans; United States; Seguy, 192h.
§. 2. hudsonicus; United States, Ban, 1906.
Ԥ. gagglinensis lgucetis; United States; Seguy, 192M.
Sitomys califorggggg; California; Riley and Howard, 1895.
Tamias striatus 1 tori; Canadd; Cameron, 1926. New York,
Arkansas, Mass., and Iowa; Fitsch, 1859.
Recorded in New York; Lintner, 1885. In Mexico, Van Der
Wulp, 1888. In Illinois, Nova Scotia; Swenk, 1905.

Q, ephippium.Latr.
Distribution in French Guiana; Patton, 1921.

‘9. fasciata Swank.
Tamias £22.; South Carolina, Florida, Miss.; Townsend,
1917. Distribution in Nebraska; Swenk, 1905.

Q, fontinella Clark.
£223§‘§22.; New Mexico; Townsend, 1892.

$2225 artemisia; United States; Bau, 1906.

Peromyscus leucopus 1.; North Carolina, Harkema, 1936.

2,‘l. noveboracensis; Boston; Johnson, 1930. Maryland,

Greene, 1935.

Sylvilagus spp.; New Mexico; Townsend, 1892.

163

Sylvilagus floridangg mallurus; Smith, 1908.
§, nuttalli n.; New Mexico; Seguy, 192k. . _
Recorded in British Columbia, Hadwen, 1915. In Illinois;
Clark, 1826. ‘

Q, funebris.
Lonchergg uianae; Trinidad; Bau, 1906.

Q, grisea Coquillet.) I . ‘
Mug musculus; Manitoba, Saskatchewan, Alberta, North-Host
territories, British Columbia; Cameron, 1926.
Citellus tridecemlineatus; Minn.;;Hashburn, 1905.

Q, histrio Coq. - ' I

‘ Distribution in.Nexico; Coquillet, 1903.

Q, horripilum.Clk. (= to Q. cuniculi, Brauer, 1863).
gang familiaris; United States; crane-y, 1923.
Felig domestigug; New York; Bequaert, 1946. Missouri and.
North Carolina; Rileyand Howard, 1893.
'nggg‘ggp. and Sylvilagus £22.; Iowa and California; Os-
born, 1896. Georgia, Florida, Arizona and Colorado;
Virginia and Indiana; Riley and Howard, 1893.
Ogyctolagus cuniculus domesticus; United States; Schwartz
and Shock, 1933.
Sylvilaggs £22.; Georgia; Clark, 1797.
‘S. floridanug; Virginia and Indiana; Riley and Howard, 1893.
'S..gloridanusmearnsii; Michigan, Haugen, 1982.
§. alustris; Georgia; Knipling and Brody, 19h0.
Recorded in Nova Scotia; walker, 18h9.' In Minn.; Lugger, 1896.

g,

2.

16h

Jellisoni Curran.

I‘Leggs californicus; Oregon; Jellison, 19h2.

infulata Lutz.

Distribution in Brazil; Patton, 1921.

latifrons Coq. (== to Q. americana, Townsend, 1911).
Neotoma fuscipes macrotis; California; Ryckman, 1953.
Recorded in Virginia, South Carolina and Georgia; Town-
send, 1917. In California; Coquillet, 1898.

lepivora Coq. (:= to Q. princeps, Townsend, 1917).
Sylvilagus'gpp.; Wyoming and California; Coquillet, 1898. »
Recorded in New Mexico; Johnson, 1902.

lepusculi Townsend (= to Q. princeps, Townsend, 1917).
Lgpgg artemisia; New Mexico; Townsend, 1917..
Sylvilagus muttalli n.; New Mexico; Seguy, 1928.

W m. (= to g. fontinella, Brauer, 1863).
Lgpg§,§22.; South America; Brauer, 1863.

nigricans Lutz.
Distribution in Brazil; Patton, 1921

nigrocincta Austen.
Distribution in Brazil; Patton, 1921.

nitida Coq. (male is = to Q. americana, Townsend, 1917).
Recorded in Virginia, South Carolina and Georgia; Townsend,

1917. In California; Coquillet, 1898. In New Mexico,

165

g. patagona Guerin.(= to Q. bugggtg, Brauer, 1863).

Family Muridae; Patagona, bouth.America; Patton, 1921.
Q, peromysci Dalmat.
' Perdmysgug leucgpus noveboracensig; Iowa; Dalmat, 19h2.

Q, pessoai.‘
Distribution in Brazil; Guimaraes, 19h1.

Q, polita Coq. (==to Q, americana, Townsend, 1917).
1.3233; £22., Virginia, South Carolina, Georgia; Townsend,
1917. )
Recorded in wyoming; Coquillet, 1898.
‘Q. princeps Austen. ,,
£2225 alleni a.; Arizona; Vorhies and Taylor, 1933.
L. californicujg c.; Arizona; Ibid. .
'Lp callotis; United States; Bau, 1906. New Mexico;-
Townsend, 1892. ‘
Sylvilagus floridanus; Arizona, New Mexico, California
and Nevada; Townsend, 1917.
Recorded in Mexico; Austen, 1895.
Q, ruficrus Austen.
Lgpgg californicua; Great Basin Area, U. S.; Curran, 19h2.
IQ. rufiventris Macquart ‘ .
Distribution in Brazil; Patton, 1921.
g, ggrcOQhagoideg Lutz.
Distribution in Brazil; Patton, 1921.
g, schmalzi Lutz.
Distribution in Brazil; Patton, 1921.

166

Q, scudderi Townsend
£22355 californicgg texianug; Texas; Roberts, 1933.
§2i§,§u;§;'Mary1and, Virginia, Tennessee and Texas;
Townsend, 1917.
Sylvilagus floridanus mallurus; Maryland; Townsend, 1917.
C. scuttelaris Brauer (= to Q. emasculator, Townsend, 1917).
Citellus £22. and Tamias £22.; N. E. United States; Town-
send, 1917. 8
Recorded in United States; Brauer, 1863.
Q, similis Johnson.
Recorded in New Mexico; Johnson, 1903.
Q, gterilator Lugger. A ,
Recorded in Minn.; Lugger, 1896.
Q. tenebrosa Coq.
Cynomys ludovicianus; Montana; Parker and wells, 1919.
Neotoma cinereg; Montana; ibid.
Onychomys leuco aster; Montana; ibid.
Recorded in Colorado, Calif., Oregon; Coquillet, 1898.
In South Dakota; Aldrich, 1905.
Q, terrisona Walker ’= to Q. g££2§3 Aldrich, 1905).
Distribution in Guatemala; Walker, 18h9.
Q. thomomurig Jellison.
Thomomyg borealis; Great Basin area; Jellison, 1989.
Q;pworontgowi.

Distribution in Brazil; Guimaraes, 1981.

167

Cuterebgaigpg.
Citellug tridicgglineatus pallidus; Colorado, Hall, 1910.
Didelphys hilander; Brazil; Natterer, 1820 and 1821.
L322; artemisia; New Mexico; Townsend, 1892.
'Lgpg§_pa1ustr;g; Mexico; Coquerel and Sells, 1862.
Neotoma fallax; Colorado, Hall, 1910.
Neotoma fuscipes macrotis; California; Gander, 1929.
Rattus norvegicug; Canada; Cameron, 1926.
Sciurus aestuans; Brazil, Natterer, 1820 and 1821.
Sciurus aureogasteg; Mexico; Coquerel and Sells, 1862.
Sylvilggug floridanus 5122;; Oklahoma; Leonard, 1933.
g. nuttalli a; New Mexico; Tom send, 1892.
.§. palustris‘p.; United States; Brauer, 1863.
Thomomyg borealig; Wyoming; Leidy, 1857.

STUDIES ON THE use HISTORY AND ECOLOGY OF CUTEREBRA SPP.
OCCURRING IN MICHIGAN COTTONTAILS WITH SYSTEMATIC
STUDIES ON CUTEREBRINE LARVAE FROM OTHER MAMMALS

By ,
Rudolph Joseph Boisvenue

AN ABSTRACT

JAISuhmitted to the School for Advanced Graduate Studies of
Michigan State University of Agriculture and Applied Science
in partial fulfillment of the requirements
for the degree of

DOCTOR OF PHILOSOPHY

Department of Microbiology and Public Health
Year 1955

Approved by

 

 

Rudolph Joseph Boisvenue
1

The purpose of this study was (1) to investigate the
phases of the life history of Cuterebra g2. as they occur
under natural conditions, (2) to elucidate the ecology of
the cuterebrid flies in relation to vegetation, soil and
host, the Michigan cottontail, Sylvilagus floridanus mearnsii,
and (3) to clarify the systematics of cuterebrine larvae
collected from.certain mammals.

The life history and ecology of Cuterebra species, oc-
curing in Michigan cottontails, were studied in part by
means of a two-year live trapping program of rabbits. Field
observations on adult cuterebrid flies and rabbits were also
carried out. One hundred and seventy rabbits were captured
and were screened for Cuterebra larval infections. Infected
cottontails were brought into the laboratory and studied
for phases of the life cycle.

Records on the duration of third stage larvae in the
cottontails related an average of 15 days. Concurrent with
the above study, it was found that the air hole diameters
of larvae reflected the phases of the third stage larvae
while in the host.

Mode of infection studies were done in the field using
twenty-two penned cottontail and domestic rabbits in areas
having high larval incidences. A positive larval infection
was obtained in a penned cottontail which was not exposed

to natural vegetation.

Rudolph Joseph Boisvenue
2

The primary site of Cuterebra larval infections in 187
southern Michigan infected cottontails was in the neck.
Other anatomical areas recorded were the scrota, cheeks,
back and shoulders.

Suggestion of larval migration was observed when two
third stage larvae appeared on the right side of the neck
of an isolated cottontail which was externally diagnosed
negative in that area a week previously. A large tumor ap-
peared first in the area followed by two larval air holes
overlying the tumor. No evidences of extensive larval mi-
gration were found in sixty-two cottontails which were autop-
sied throughout the Cuterebra cycle.

The time recorded for the obvious appearance of third
stage larvae in cottontails from.a negative diagnosis was
22 days.

First, second and third stage larvae were discovered in
the cottontails which gave seasonal periodicities in their
hosts. The seasonal periodicity of third stage larvae was
determined to be between.August 1 to 20. First stage larvae
were believed to have a seasonal periodicity a month previous
to the third stage larvae in the early part of July.

Seasonal incidence of cuterebrid larvae in southern
Michigan juvenile cottontails was determined to be between
August 1 and 20. For adults, it was found to be between
July 20 to 30. In general, the Juvenile cottontails had a
higher incidence of Cuterebra larvae than adult rabbits.

Rudolph Joseph Boisvenue
3 .

Also the number of warbles per infected rabbit was found to
be the greatest when there was a peak in the incidence of
Cuterebra larvae among the cottontails.

Field notes on pupation showed that mature larvae
which have recently dropped from their hosts were able to
survive 9 to 13 days before pupating. Depths recorded on
27 burrowing larvae offered a range of 1 1/2 to 2 1/2 inches
in sandy soils. Field pupation experiments revealed that no
two-year cycle existed for the pupae. Also one generation a
year was shown to exist in Michigan for Cuterebra, regardless
of exposing the pupae to artificial or natural conditions
prior to the emergence of the flies. ‘Longevity of adult
flies were observed in laboratory pupation jars to range from
1 to 5 days.

Higher numbers of Cuterebra infections were recorded in
areas having sandy soils. Also these sandy areas showed great-
er numbers of rabbit burrows. This situation was believed
conducive to good pupation and consequently, successful emer-
gence of adult flies with excellent conditions for larval in-
fections in the rabbit burrows.

Vegetative sites such as dense sumac bushes, willow
swales and clover fields were associated with adult cuterebrid
flies.

One hundred and twenty-seven cuterebrid larvae, collected
from cottontails, cats, dogs, jack rabbits and white-footed

mice, were comparatively studied and taxonomic differences

 

 

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Rudolph Joseph Boisvenue

were presented for each instar of individual Cuterebra species
studied. The results obtained in the systematic study of
larvae were compared with the findings of previous workers.
Buttons, peculiar to posterior Spiracles of some dipterous
larvae, were seen in the cuterebrid examples investigated.

A key is presented which separates the various instars
of the individual larval species determined in the systematic
study. Species of Cuterebra determined in this study were
buccata, fontinella, and.horripilum. An unidentified species,
found on Nevada jack-rabbits was described and its larval
characteristics are presented for comparison with the known
cuterebrid species. No pupa-adult fly series were obtained
for the identification of the Nevada species. However, they
were obtained for the three identified Species.

Verification of the three Cuterebra species was accom-
plished by means of a puparium.from which a known identified
adult fly emerged. With the morphological characteristics
of the puparium it was possible to retrogress to the third
instar and subsequently to the first instar of that species.

Larval Species found in.§§l;§.dpmestica were 9. buccata
and horri ilum, with a preponderance of the latter species.
Cuterebra bucgata was recorded from'ggg;g familiaris. Michi-
gan cottontails had both cuterebrid species, with.Q, horripilum
predominating. The only larval species obtained from.the

white-footed mouse of Michigan was‘Q. fontinella.

Eudolph Joseph Boisvenue

A check-list of the Cuterebra Species of the western
hemisphere is presented with records of their geographic

locations and the scientific names of their hosts.

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