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thesis entitled

The Effects of the Snail Physaigyrina (Say)
on the Structure of an Epiphytic Diatom Community

 

presented by

Nancy L. Winters

has been accepted towards fulfillment
of the requirements for

_M.Si_degree in loology—__

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THE EFFECTS OF THE SNAIL PHYSA GYRINA (SAY) ON THE
STRUCTURE OF AN EPIPHYTIC DIATOM COMMUNITY

 

By

Nancy L. Winters

A THESIS

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

MASTER OF SCIENCE

Department of Zoology

1980

ABSTRACT

THE EFFECTS OF THE SNAIL PHYSA GYRINA (SAY) ON THE
STRUCTURE OF AN EPIPHYTIC DIATOM COMMUNITY

 

By

Nancy L. Winters

The purpose of this study was to determine the potential grazing

role of the freshwater gastropod, Physa gyrina (Say), in structuring

 

the diatom portion of the periphytic community. Effects of intensive
snail grazing on colonized glass substrates was measured in the
laboratory as: (l) periphytic biomass (ash-free dry weight), (2) diatom
species diversity, and (3) alterations in numbers and numeric propor-
tions of specific diatom genera. The response of the periphytic
community two weeks after grazing ceased was also measured using the

same parameters. Grazing effects were also measured jg_situ at lower

 

natural snail densities.

At high densities in the laboratory 3, gyrjng_reduced both the
diatom standing crop and the species diversity, and preferentially
removed Navicula. Two weeks after release from grazing pressure, the
periphyton remained reduced in standing crop but not in species
diversity. At the lower, natural densities of E, gyriga_the diatom
standing crop was increased while the species diversity was not

altered.

ACKNOWLEDGMENTS

I thank Dr. Donald J. Hall for his suggestions and encouragement
throughout the course of this research. Dr. Robert G. Wetzel and Dr.
Donald L. Beaver offered comments on earlier drafts of this thesis.
Dr. Patricia Werner gave guidance in the design and initiation of the
research. I extend my sincerest thanks to Elizabeth Hutchison and
Judith Soule for unending encouragement, suggestions, and comments on
earlier drafts. I am especially endebted to Martin Werner. His
assistance, suggestions, and enthusiastic concern have supported me

throughout the course and completion of this work.

ii

TABLE OF CONTENTS

 

Page
LIST OF TABLES ........................ iv
LIST OF FIGURES ....................... v
INTRODUCTION ......................... 1
THE SYSTEM .......................... 7
Lawrence Lake ...................... 7
Epiphytes ........................ 8
Physa gyrina (Say) ................... 8
MATERIALS AND METHODS .................... 11
Treatment I ....................... ll
Treatment II ...................... 18
Determination of Snail Densities ............ 18
Method of Data Analysis ................. l9
RESULTS ........................... 20
Ash-Free Dry Weight ................... 20
Algal Numbers and Diversity ............... 26
Differential Grazing .................. 30
DISCUSSION .......................... 48
CONCLUSIONS ......................... 60
BIBLIOGRAPHY ......................... 6l

Table

10

11

LIST OF TABLES

Treatment I median, range, and n = numbg; of slides

analyzed for ash-free dry weight (mg/cm

Median number of snails/cm2 on Lawrence Lake macro—

phytes and experimental substrata ...........

Treatment I median, range, and n = number of slides
analyzed for ash-free dry weight from recolonized

slides ........................

Treatment II median, range, and n = number of slides
analyzed for (a) ash-free dry weight, (b) algal
cells/cmz, and (c) diversity index H' = 2 Pi ln

Treatment I median, range, and n = number of slides

analyzed for number of algal cells/cm ........

Treatment I median, range, and n = number of slides
analyzed for number of algal cells/cm from recolo-

nized slides .....................

Treatment I median, range, and n = number of slides
analyzed for species diversity H' = 2 pi ln

Treatment I median, range, and n = number of slides
analyzed for species diversity H' = 2 p1 lnp. from

recolonized slides ............ l .....

Treatment I median, range, and n = number of slides
analyzed for the percent of the community for each

major genus ......................

Treatment II median, range, and n = number of slides
analyzed for the percent of the community for each

major genus ......................

Treatment I median, range, and n = number of slides
analyzed for the percent of the community each genus

represents from the recolonized slides ........

iv

pi . . . .

pi .....

Page

21

24

34

41

LIST OF FIGURES

Treatment I schematic flow sheet ...........

Ash-free dry weight plotted by replicate from
Treatment I .....................

Ash-free dry weight plotted by replicate from
Treatment I recolonized slides ............

Species numbers plotted by replicate from Treat-
ment I ........ . ........... .. . . .

Species numbers plotted by replicate from Treat-
ment I recolonized slides ..............

Shannon Weaver Index plotted by replicate for
Treatment I .....................

Shannow Weaver Index plotted by replicate for
Treatment I recolonized slides ............

Percent of the community plotted by replicate for
Achnanthes, Cymbella, Epjthemia, Eunotia, Fragi-
laria, Navicfla, and Girdle Views of Treatment—I

 

 

Percent of the community plotted by replicate for
Achnanthes, Cymbella, E ithemia, Eunotia, Fragi-
laria, Navicula, and Girdle Views of Treatment I
recolonized slides ..................

 

Page
14

25

33

38

46

INTRODUCTION

The majority of the world's lakes are small, shallow (less than
20 meters deep) bodies of water and therefore provide conditions
necessary for extensive littoral development (Wetzel 1975). Littoral
flora in these shallow lakes may contribute significantly to the
primary productivity of the lakes. Aquatic macrophytes not only con-
tribute to the synthesis of organic material, but also provide an
enormous amount of surface area for colonization by epiphytic primary
producers.

In addition, macrophytes provide structural complexity within
the community which provide a niche dimension along which organisms
may divide habitat space. The multitude of organisms which this
habitat can support creates a potential for complex ecological inter-
actions.

Epiphytes on the surfaces of macrophytes contribute significantly
to the total primary production of many aquatic systems. Periphyton
was determined to be the most important producer in shallow Borax
Lake, California (Wetzel 1964).

A number of mechanisms operate to regulate both the physical
structure and species composition within the periphytic community
such as the surrounding water chemistry (Hutchinson l975), the nature
of the substrata whether organic or inorganic, the length of the

colonization period, and the age and condition of the macrophyte

1

 

2

host (Round l965). The nature and species of the macrophyte host
may determine, in part, which species of epiphytes colonize the

surface. Prowse (l959) found Utricularia to be preferentially

 

colonized by Gomphonema, Najas by Eunotia, and Enhydrias by Oedogonium.

 

Seiburth and Thomas (l973) found decaying eelgrass to be colonized
initially only by Cocconeis and secondarily by other species. In a
study of macrophyte-epiphyte interactions on Lawrence Lake, Michigan,
Allen (l97l) suggested a dissolved organic carbon "pool" is estab-
lished within the marl matrix between the macrophyte host and the
periphyton. He named four sources which may contribute to this
carbonate-muco-organic "pool" including: (a) extracellular release
from the macrophyte, (b) active excretion by the attached algae and
bacteria, (c) decomposition products following autolysis of attached
algae and bacteria, and (d) dissolved allochthonous and autochthonous
carbon within the littoral zone. It is the chemical interactions
proposed (the first three contributors listed) which may, in fact,
determine macrophyte-epiphyte specificity. Further biochemical
analysis is necessary to determine the extent of such specificity.
Morphology of the attachment structure influences the physical
structure of the community. Epiphytes may be attached by (l) branched
or unbranched stalks (e.g., Gomphonema and Cymbella), (2) tight and

 

direct adherence to the host surface (e.g., Cocconeis), (3) a basal
mucilaginous pad (e.g., Synedra and Eunotia); or (4) they may be motile
within the epiphytic structure (e.g., Navicula) (Round 1965). A mat
of the directly adherent diatoms either unispecific (Seiburth and

Thomas l973) or multispecific (Allanson l973) may form a crust upon

3

which other epiphytes colonize. The physical structure of the epi-

phytic community was directly observed on Chara spp. and Potamqgeton

 

ggtgg§_using scanning electron microscopy (Allanson l973). Allanson
noted a loosely woven diatomaceous component held in place by a
stranded matrix formed of the gelatinous epiphytic stalks and under-
lain by a layer of calcite deposits.

Epiphytic community structure may be determined by length of
colonization period. Whitford (l956) outlined a successional pattern
for algae epiphytic on Sagittaria leaves in a hard freshwater spring
in Florida. Cocconeis was found to be a pioneer Species on bare
leaves; Cocconeis colonization was followed by a canopy of Synedra,

Gomphonema, Xenoccus, and Achnanthes; eventually these were overgrown

 

by other diatoms, filamentous green algae and Plectonema.

 

Species composition within the community may be regulated by
seasonal fluctuations in light and temperature. Sullivan (1977)
found species diversity to be greatest in early spring when macrophyte
growth was greatest and competition for space and light was least.

The actual relationships between species composition and physical
structure are yet to be documented.

The structure and composition of the periphytic community may
also be controlled by ecological interactions with other members of
the aquatic system. For example, Batrick and Strawbridge (1963)
hypothesized that diatom species populations were regulated at low
densities by interspecific competition and predation.

Predation or grazing may alter the community in a number of ways.
The density of epiphytes has been demonstrated to be affected by

grazing. For example, a population of chironomids completely depleted

4

the periphyton on old Iyghg_stems by the end of the growing season
(Mason and Bryant 1975). Brook (1975) attributed the increase of
epiphytic algae and diatoms in the winter to a lack of predation by
Tricoptera, Ephemeroptera, chironomids, and fish.

Herbivorous grazing may also alter the primary productivity of
an algal community. C00per (1973) reported that moderate grazing in

microcosms by the herbivorous fish Notropis spjjopterous, increased

 

net primary productivity. Flint and Goldman (1975) also demonstrated
an increase in periphytic primary productivity as a result of grazing
by crayfish. The amphipod, Hyallela, increased epibenthic algal
productivity at densities simulating those in a natural lake (2 to 3
amphipods/20 cmz) (Hargrave 1970a).

Grazing may alter the structure of an aquatic community by
affecting diversity. Paine and Vadas (1969) suggested the sea urchin

Strongytocentrotus spp. enhanced diversity in the epilithic macro-

 

algal community. By grazing on Hedgphyllum, which was the dominant

 

species in the absence of the urchin, Strongytocentrotus indirectly

 

allowed other algal species to persist. Species diversity is not
necessarily enhanced as a result of grazing. For example, the

voracious grazing of the tadpole Rana aurora decreased species

 

diversity in a pond by removing the green algae and desmids from the
periphytic community. Only after the tadpoles metamorphosed, and
thereby eliminated the intense grazing pressure on the periphyton,
did a secondary succession of the community occur accompanied by an
increase in diversity although not comparable to the original

diversity (Dickman 1968).

5

When a predator or grazer feeds preferentially on the competi-
tively dominant member of the community, the diversity of that
community is increased. Lubchenco (1978) demonstrated this point for

the algal and Littorina littorea interactions in intertidal pools.

 

As the snail density increased the algal density also increased.
However, at high snail density algal diversity was reduced.

Grazing, as has been demonstrated, may affect community structure
by altering density, productivity, or diversity. Grazing within the
periphytic community is specifically of interest for three reasons.
First, since periphyton is a contributor to the primary production
of many aquatic environments, any alteration of the productivity is
an alteration of the photosynthetic energy entering the system.
Secondly, organisms which alter density may alter the physical
structure of the community affecting post-grazing colonization of
epiphytes. Thirdly, interactions which alter the populations within
the periphytic community affect the structure of the community and
affect other organisms of the littoral zone.

Physa gyrina (Say). a common freshwater gastropod, grazes on

 

periphyton, primarily on diatoms (Clampitt 1970). Diatoms were the
preponderant component of the gut contents which he studied. Peri-
phyton is a significant contributor to the primary productivity of
shallow freshwater lakes. Stockner and Armstrong (1971) reported that
diatoms represent 60-70% of the epiphytic community, while in a
previous study it was found that they represented 75% of the epiphytic

community on Potamogeton tenufolius in Gull Lake, Michigan, a hard-

 

water lake neighboring Lawrence Lake (Winters, unpublished). Since

6

diatoms are the major food of P, gyrjgg_and since they represent
between 60% and 70% of the epiphytic community, the potential role
of E, gyrjgg_in structuring the diatom portion of the periphytic
community is of ecological interest. The purpose of this study was

to determine the effects of grazing by Physa gyrina on the diatom

 

portion of the periphytic community as measured by: (l) periphytic
biomass, (2) diatom species diversity, and (3) alterations in cell
numbers and numeric proportions of specific diatom genera. In
addition, the post-grazing effects (i.e., the response of the peri-
phytic community after grazing ceased) were measured by the same
parameters. Effects were measured jg_§jtg_at natural densities of
snails simulating densities found in Lawrence Lake, Michigan, and
under laboratory conditions at densities 20 times those found in

Lawrence Lake.

THE SYSTEM

Lawrence Lake

 

Lawrence Lake is a small calcareous lake of glacial origin
located in Barry County, Michigan (85°21'W, 42°27'N). The surface
area of the lake is 4.96 ha.; the maximum depth is 12.6 meters, while
the mean depth is 5.89 meters (Allen 1971). Two small inlets and one
outflow maintain the water level within the lake (Allen 1971). A
portion of the lake's bottom is covered with extensive marl deposits.
It is the calcium carbonate-nutrient interactions which are largely
responsible for the low rate of primary productivity by the limnetic
phytoplankton (41.1 g C/mz/yr) (Wetzel 1975), while allowing a few
adapted macrophytes to dominate the primary production (87.9 g C/mzlyr)
of the lake (Rich gt_gl, 1971). The littoral zone which extends to
a depth of 6 to 7 meters is the site of the major portion (48.3%) of
primary productivity of the lake (Rich gt_gl, 1971). Littoral
macrophytes include: Chg:g_spp., Myriophyllum heterophyllum, Najas
flexilis, Nuphar sp., Nymphaea sp., Potamogeton spp., and Scirgus

 

 

subterminalis. These macrophytes not only function in the capacity

 

of primary producers but also function as available hosts for epi-
phytic colonization and primary production. Allen (1971) found
epiphytic algae on emergent macrophytes in Lawrence Lake synthesized
2.9 g C/mZ/yr and epiphytes on submergent macrophytes synthesized
35.0 g C/mZ/yr. Since a significant contribution to the primary

7

8

productivity is made by the epiphytic algae, the littoral community
of Lawrence Lake provides an ideal site to study interactions such
as occur between herbivorous grazers and epiphytes which may affect

the epiphytic community as a whole.

Epiphytes

The species composition of epiphytes in Lawrence Lake was
followed throughout a growing season by Allen (1971). On the east

shore of the lake within the Najas-Chara beds in which the substrata

 

for this study were colonized, Allen found a meager early summer
colonization by Fragilaria, Tabellaria, and Cymbella. By midsummer
and early fall the Najas and Chara hosts were dominated by Gomphonema

 

with a secondary growth of Eunotia, Cymbella, Fragilaria, and Synedra

 

adherent to the Gomphonema. Navicula, Cyclotella, Oedogonium,

 

 

 

Zygenema, Synedra, and Chlorella were among the dominant genera

 

found attached with holdfasts or growing prostrate on the macrophyte

surface.

Physa gyrina (Say)

 

Physa gyrina (Say) is a pulmonate mollusc of the Order Basommato-

 

phora and Family Physidae. Physids have secondarily returned to the
aquatic environment (Barnes 1963). Therefore, they must either
surface to obtain air (a frequent occurrence in shallow water)
(Clampitt 1970) or obtain oxygen from the water circulated through
the mantle cavity (Barnes 1963). P, gyrigg_is distributed in a broad
array of freshwater habitats (Clark 1973). The snail burrows into

soft mud as temporary ponds dry and remains buried until the water is

9

replenished by autumn rains (DeWitt 1955). E, gyrjgg_is more often
associated with vegetated areas than with bare rock or mud surfaces
(Pip and Stewart 1976).

The life span of E, gyrjgg_is 12 to 13 months in permanent ponds
and lakes in Michigan (DeWitt 1955). Oviposition occurs in April in
Michigan when water temperatures reach 10°C (DeWitt 1955) and is
regulated by water temperature rather than day length (DeWitt 1967).
A single individual may lay from 42 to 1839 eggs (DeWitt 1954b); after
the first two days of oviposition the number of eggs laid per snail
per day is reduced (DeWitt 1954a). Isolated laboratory individuals
of E: gyrjgg_1aid a greater number of eggs per snail (830/isolated
laboratory snail versus 653/field snail) but fewer of the eggs were
successful in reaching maturity (DeWitt 1954a). Although E, gyrjgg_
is monoecious and can be hermaphroditic, individuals do not reproduce
in this fashion for two successive generations (DeWitt 1954a).

Eggs may hatch from 8 to 10 days following oviposition (DeWitt
1955) but development is temperature dependent (Sankurathri and
Holms 1976). Juveniles feed continuously (DeWitt 1955) within
their major period of growth extending from April to June (Clampitt
1970). The often observed midsummer disappearance of mature snails
has been attributed to post-reproductive mortality (Sankurathri and
Holms 1976). E, gyrjgg_may migrate to deeper water in winter as was
determined for their congeners, P, integra, by Clampitt (1974) or
they may undergo estivation as was determined by DeWitt (1955). In
either case, their activity is diminished in winter. Snails reach

sexual maturity at approximately 7 mm in length (DeWitt 1955),

10

except under crowded conditions when they remain smaller (Clark
1973). The life cycle begins again the following April.

£5 gyrjgg_feed by means of the radula. The radula bears a
number of small teeth varying from 95 to 120 oblique teeth on each
side of a larger central tooth (Clark 1973). Gut content analysis has
revealed that snails feed on diatoms, green algae, detritus, vascular
plant tissue, rotifers, microcrustaceans, diptera larvae, and oligo-
chaetes, but that diatoms formed the major portion of the diet
(Clampitt 1970). The assimilation efficiency of food, however, is
about 4% for adult Potamopyrgus jenkinsi, another herbivorous fresh-
water species (Heywood and Edwards 1962) and is probably similar to
the efficiency of E, gyrjgg,

E, gyriga_can detect quantitative differences in food levels
(Warner 1976) locating food either by random movement (Bovbjerg 1965)
or by close range chemoreception (Townsend 1973). A group of snails
will adjust their feeding densities in accord with the amount of
food available (Warner 1976). Further, preferences for the macrophyte

Potamogeton pectinatus have been determined by Pip and Stewart (1976)

 

who hypothesized that E, gyrina responds to the high concentration of
glucose, fructose, and other soluble carbohydrates exuded by the

macrophyte.

MATERIALS AND METHODS

Two experiments were performed in this study to determine the
effects of a high density of grazers (Treatment 1), and the effects
of grazers at densities comparable to those found in Lawrence Lake,
Michigan, in late summer (Treatment II). Treatment I attempted to
simulate in the laboratory the grazing pressure which could exten-
sively impact the periphytic community for a short post-hatching

period in the spring. Each individual of Physa gyrina is capable of

 

laying up to 1800 eggs per season in masses of approximately 100 eggs
each (DeWitt 1954b). The egg mortality ranges from 7-55% (DeWitt
1954b). If only one-half of the eggs in each mass survives until
hatching, 50 young snails would hatch. Although adult snails are
capable of moving from an area at a rate of 7 meters in 24 hours
(Clampitt 1974), the young snails may not be able to move as rapidly
and would be unlikely to do so until the food resource becomes
limiting. Thus, a high density of young snails may impact the peri-

phytic community extensively.

Treatment I

 

Four boxes of 16 glass microscope slides were suspended in
Lawrence Lake, Michigan, for a two-week colonization period. The
boxes were removed to the laboratory where two of the boxes of slides

were placed in battery jars and were exposed to a period of snail

11

12

grazing while the remaining two boxes of slides, also placed in
battery jars, were not exposed to grazing. Following the grazing
eight slides from each jar were removed and analyzed for ash-free dry
weight, species identification, anc cell enumeration. The eight
slides remaining in each of the battery jars were returned to Lawrence
Lake for a two-week recolonization period with no snail grazing.
Thereafter they were removed and analyzed for ash-free dry weight,
species identification, and cell enumeration. A schematic flow chart
outlining the procedure for Treatment 1 is presented in Figure 1.

Much debate has been focused on the use of artificial substrata
in the study of periphytic communities. While data of Tippett (1970)
firmly denies the usefulness of glass slides on the basis of selective
colonization of diatoms and reduced production, Stockner and Armstrong
(1971) determined that slides and denuded substrata were comparable in
the accumulation of epiphytic biomass. Sladecek and Sladeckova (1964)
reported "only small differences in periphyton between natural and
artificial substrata." Patrick (1968) stated that within two weeks
the periphyton colonized on glass was characteristic of natural
communities. Glass slides are convenient as they have a known surface
area and can be colonized for predetermined lengths of time. It is
possible, due to their silica content, that slides may be selectively
colonized by diatoms. However, since diatoms are the main considera—
tion of this study, glass slides would pose no hindrance to coloni-
zation.

The two-week colonization period was selected for this study for

several reasons. Patrick (1968) proposed two-week colonization as the

13

Figure 1. Treatment I schematic flow sheet.

 

 

14

Treatment 1 Schematic Flow Sheet

 

 

 

 

 

 

 

‘- r;.
We slides 16 slides 16 slides 16 slides W
colonized colonized colonized colonized

2 weeks 2 weeks 2 weeks 2 weeks

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

- I _ l s l _ _ I _
16 slides 16 slides 16 slides 16 slides

, 16 snails 16 snails f _

Eslides. .8 slides 8 slides

\ ‘ ‘ 8 slides

slides individually processed tor:

Ash Free Dry Weight
Species Identification
Species Enumeration

 

 

 

 

 

 

 

    
   
 
 

 

 

 

    
   
 

, I I
8 slides 8 slides 8 slides aslides
1 t 1
recolonized recolonized recolonized recolonized
2 weeks 2 weeks 2 weeks 2 weeks

 

 

 

 

 

 

slides individually processed for:
' Ash Free Dry Weight
Species Identification
Species Enumeration

 

 

 

 

Figure l

 

15
best interval for diatoms to settle and grow in a characteristic
pattern. Castenholz (1961b) suggested that with colonization periods
longer than two weeks the substrata are subject to increased predation
and increased sloughing of cells. Kevern, gt_gl, (1966) reported the
rate of periphytic primary production reached a stable plateau by the
13th day of colonization of artificial substrata.

The vertical placement of the slides in the water column was
determined to be most appropriate for this study as only those diatoms
which are actually epiphytic would colonize vertical substrata and
the amount of detritus settling on the slides would be reduced. Casten-
holz (1961b) reported 6 to 12 times more biomass on horizontally
placed slides due to accumulation of detritus and increased ease of
settlement and attachment by epiphytes. While 3, gyrjgg_feeds on
detritus as well as diatoms, detritus does not represent as great a
proportion of the diet as diatoms (Clampitt 1970). Detrital material
is not easily categorized or quantified and was not the major focus
of this study. Since it was desired that the snails graze on diatoms
rather than detritus, vertical placement was deemed appropriate.

The four boxes of 16 glass microscope slides (7.6 x 2.5 x 0.1 cm)
were suspended vertically l7-mm apart from an inflated bicycle inner
tube between 13 and 75 cm from the sediment surface in a water column
1.75 m deep in the littoral zone of Lawrence Lake, Michigan.

The colonized slides were removed and transported to the labora-
tory for the exposure to grazing or control chambers. 0f the four
colonized boxes, two were selected randomly to be subjected to grazing

by Physa gyrina (labeled boxes A and B) and the remaining two were to

 

remain ungrazed as controls (labeled boxes C and D). The 16 slides

16

from each box were held vertically by grooved rubber stoppers (four
slides/stopper) and placed in a two gallon battery jar filled with
water from Lawrence Lake. Sixteen E, gyrjgg_selected at random from a
stock culture and measuring between 4.0 and 9.5 cm in length were
placed in each of battery jars A and B. Snails had access to slides'
by climbing from tank bottom to stopper, then on to the slides. Slide
positioning posed no difficulty in accessibility to snails. The E,
gyrjgg_had not been permitted to feed for 24 hours prior to their intro-
duction to the battery jars. No snails were introduced to battery jars
labeled C and D. The snails in jars A and B were permitted to graze
between 43 and 48 hours and were then removed.

The grazing period in Treatment I was set at approximately 48
hours. Qualitative visual observations after 12, 24, and 36 hours
showed that the periphyton had been disturbed little by the snails,
and few grazing trails were visible. Forty-eight hours permitted the
snails to acclimate and graze a relatively large portion of the peri-
phyton without completely scraping the substrata bare. The remaining
portion of periphyton served to determine selectivity for any parti-
cular diatom genus by the snails.

Eight slides from each aquarium were then randomly selected and
returned to the site of colonization in Lawrence Lake for 14 days of
recolonization to determine changes in species composition of the
diatom community which occur post-grazing (”post-grazing effects").
The remaining 8 slides from each aquarium were processed to determine
the effects of snail grazing. The surfaces of each slide were scraped
using a clean glass slide and washed with distilled water into a jar.

Each jar was stirred for 30 seconds, where upon a known aliquot

17

between 1 and 5 ml (depending on the estimated density of diatoms)

was pipetted. The aliquot was then filtered onto gridded HA Millipore
filters (0.45 um pore size) and the cells preserved with Lugol's
solution. Following McNabb (1960)), the filters were placed on clean
microscope slides, cleared with immersion oil, air dried overnight
(25°C), and made permanent with PermountR. These slides were labeled
and stored for later identification. Four slides from each treatment
were randomly selected for species identification and enumeration.
Identifications of the algae were made to genera at 400x in the case
of diatoms and all other algae were grouped together. One grid

(3 x 3 mm) was selected at random. Since eight slides were identified
from each treatment for each replicate, any non-random distribution
of algae was deemed unimportant. All diatoms within the grid were
identified using Weber (1971) and enumerated. Algae classified as
other algal groups represented less than 7% of the community; most

of these algae were in the division Cyanophyta (e.g., Oscillatoria,

Microcystis). In more densely populated grids enumeration was halted

 

when between 500 and 1000 cells had been counted and the dimensions
of the counted area determined using delineations on the microscope
grid. The total surface of the filter and total dilution were then
calculated.

The remaining portion (known volume 60-70 ml) of each sample in
the jar was filtered onto dried (12 hours at 105°C) and weighed HA
Millipore filters. The filter papers with samples were then dried for
24 hours at 105°C and weighed. They were then placed individually in
crucibles which had been fired to constant weight (12 hours) at 550°C,

cooled to 105°C for one hour, desiccated for 30 minutes, and weighed to

18

the nearest 10 pg. Filter papers in covered crucibles were heated to
550°C for three hours, cooled at 105°C for 30 minutes, desiccated for
30 minutes and weighed to the nearest 10 pg to determine ash-free dry
weight.

The slides which had been returned to Lawrence Lake were removed
after 14 days and were processed in the same manner as described above
for species identification, enumeration and ash-free dry weight.

Treatment I was replicated five times between 7 July and 22

October 1977. Water temperatures ranged between 28°C and 12°C.

Treatment II

 

Nine clean glass slides positioned vertically 17 mm apart were
placed in each of four boxes. The boxes were each enclosed in fiber-
glass screen bags (mesh size 0.46 cm diagonally). In each of two of

the bags were placed five snails (Physa gyrina) ranging between 5.0

 

and 8.5 cm in length. The bags were suspended in Lawrence Lake in a
1.37-meter water column from 17 to 52 cm above the sediments. The
bags remained in the lake for 14 days between 13 August and 27 August
1977, and were removed and processed as above for species identifi-

cation, enumeration and determination of ash-free dry weight.

Determination of Snail Densities

 

Twenty individuals of the following macrophytes -- Myriophyllum

 

heterophyllum, Najas flexilis, Potamogeton pectinatus, E, praelongis,

 

and Scirpus subterminalis -- were removed from Lawrence Lake using

 

SCUBA equipment and taken to the laboratory where determinations of

surface area per unit dry weight were made using the Teepol method

19

(Harrod and Hall 1962). Regression equations were calculated for
each species (Wagner 1978). .

To determine the natural density of snails on macrophytes, 20
individuals of each of the above species were collected using SCUBA,
each plant being carefully placed in a plastic bag which was sealed and
floated to the water's surface. The number of all snail species was
counted, the surface area of the macrophyte determined using dry

weight (24 hours at 105°C) and the regressions discussed above.

Method of Data Analysis

 

The assumptions of normal distribution of the population and
homogeneity of variance which underlie parametric statistical analyses
could not be met. The effects of violated assumptions on parametric
tests have not been determined (Bradley 1968); therefore, distribution-
free non-parametric tests which do not make these assumptions were
deemed most informative and useful.

A Krushkal-Wallis analysis of variance was used to determine the
effects of time of colonization on the Treatment I data. A Friedman
analysis of variance was performed to determine the overall effects
of the grazing in Treatment I. To determine on which dates specifi-
cally grazing caused significant differences Mann Whitney U-tests were
used. A Mann Whitney U-test was also employed in comparing grazed and
non-grazed data in Treatment 1. Medians, rather than means are
appropriate for use with the non-parametric tests employed (Siegel
1956). Data are, therefore, presented as medians with ranges given in

parentheses.

RESULTS

The Krushkal-Wallis analysis of variance was performed on each
set of parameters in Treatment I to determine the effect of time of
colonization. In every case the null hypothesis (t1 = t2 = t3 = t4 =
t5) was rejected (i.e., significant differences at P = 0.05 existed).
Therefore, while Friedman analysis of variance was performed on each
of the parameters to determine the overall effect of the grazing
treatment, a replicate by replicate Mann Whitney U-test for the
effects of grazing was used to establish on exactly which dates
(replicates) the snails had a significant (P = 0.05) effect. Signi-
ficant differences as determined by the Mann Whitney U-tests are
denoted in tables and figures by an asterisk. The overall effects of
grazing as determined by Friedman analysis of variance are those to

which the text refers.

Ash-Free Dry Weight

In Treatment I the ash-free dry weight (AFDW) was found to be
significantly less (Friedman analysis of variance, P = 0.05) on
the grazed slides than on the non-grazed. A list of the medians,
range and number of slides analyzed in each case (n) for the ash-free
dry weights appears in Table 1. The information is presented
graphically in Figure 2. The data indicate that a high intensity of
grazing by Physa gyrina did diminish the periphytic biomass. While

 

20

21

Table 1. Treatment I median, range, and n = number of slides analyzed
for ash-free dry weight (mg/cmz).

 

 

Replicate Grazed Non-Crazed

l 0.19 (0.11 - 0.26) 0.45 (0.16 - 0.86)
n = 5 n = 4

2* 0.04 (< 0.01 - 0.11) 0.14 (0.06 - 0.18)
n = 16 n = 14

3* 0.05 (< 0.01 - 0.18) 0.16 (0.06 - 0.20)
n = 16 n = 16

4 0.07 (< 0.01 - 0.23) 0.08 (< 0.01 - 0.33)
n = 16 n = 16

5 0.03 (< 0.01 - 0.22) 0.05 (0.02 - 0.25)

n = 5 n = 16

 

*Indicates significant differences using Mann Whitney U-test P = 0.05.

22

45-"- NON-GRAZED
+-— GRAZED

ILII

 

ASH FREE DRY WEIGHT (mg/cm2)
(I)

 

 

0.01 l 1 l
O l 2* 3*
REPL I CATES

—l

45-1
(11

Figure 2. Ash-free dry weight plotted by replicate from Treatment I.
* indicates significance using Mann Whitney U-test at
P = 0.05.

23

the number of grazers per unit surface area was an order of magnitude

higher than that determined for Myriophyllum heterophyllum in Lawrence

 

Lake (see Table 2), it may be a realistic grazing pressure during a
spring post-hatching period and prior to decreases in population from
natural mortality and predation although adult snails were used
rather than newborn. Data in Table 2 also indicate a range of
herbivorous snail grazing pressure from a low density of 0.00083

snails per square centimeter on Najas flexilus (or 0.9 snails per

 

plant of a mean surface area of 1078.94 cmz) to 0.02423 individuals/cm2

on Myriophyllum (or 17.1 snails per plant of a mean surface area of

 

706.54 cmz). The snail species included not only Physa gyrina but

 

also all of the following species: Amnicola limosa, A, lustrica,

 

Campeloma decisum, Gyraulus deflectus, g, paruus, and Valvata tri-

 

 

 

carinate. After the slides were returned to the lake for recoloni-
zation, a significantly greater ash-free dry weight (P = 0.05) was
found on the slides which were not subjected to grazing (Table 3 and
Figure 3). (AFDW data from replicates 3 and 4 were accidentally
burned and therefore unavailable.)

When the grazing pressure more nearly approximates that found in
Lawrence Lake (see Table 2), in Treatment II the results reverse them-
selves. The slides in the grazed enclosures had a significantly
(P = 0.05) higher ash-free dry weight (Mann Whitney U-test, P = 0.05)
than the slides within the non-grazed enclosures (Table 4). The data
imply that grazing by snails at natural densities enhances diatom
growth.

The percent of organic matter on the slides was assumed to be

constant throughout treatments. It ranged between 0.57% and 28.03%

24

Table 2. Median number of snails/cm2 on Lawrence Lake macrophytes
and experimental substrata.

 

Substratum Date(s) Sampled Snails/cm2

 

Myriophyllum heterophyllum 8/23/77 9/19/77 0.02423 0.01173

 

 

 

 

 

Najas flexilus 8/20/77 0.00083
Potamogeton pectinatus 9/19/77 0.00531
Potamogeton praelongus 9/17/77 9/19/77 0.00381 0.00917
Scirpus subterminalis 8/23/77 0.00253
Glass slides Treatment I 0.52210
Glass slides Treatment II 0.01431

 

Table 3. Treatment I median, range, and n = number of slides analyzed
for ash-free dry weight from recolonized slides.

 

 

Replicate Grazed Non-Grazed
l 0.90 (0.29 - 11.79) 0.98 (0.81 - 11.67)
0 = 5 n = 4
2* 0.08 (0.02 - 0.54) 0.65 (0.28 - 0.95)
n = 14 n = 15
5* 0.03 (< 0.01 - 0.22) 0.12 (0.03 - 0.30)
n = 13 n = 16

 

*Indicates significant differences using Mann Whitney U-test, P = 0.05.

ASH FREE DRY WEIGHT (mg/cm2)
(I)

0.01

Figure 3.

25

 

 

 

a
1
' 9---. NO'N-CRAZED
_ +-— GRAZED
l I I If 1
0 l 2* 3 4 5*
REPLICATES
Ash-free dry weight plotted by replicate from Treatment I

recolonized slides.
* indicates significance using Mann Whitney U-test at
P = 0.05.

26

with a mean of 13.71%, which is lower than that reported by McIntire

(1966). The discrepancy will be considered in the discussion.

Table 4. Treatment II median, range, and n = number of slides 2
analyzed for (a) ash-free dry weight, (b) algal cells/cm ,
and (c) diversity index H' = 2 pi lnp

i

 

 

Grazed Non-Grazed
(a) AFDW mg/cm2** 0.20 (0.06 - 0.41) 0.02 (< 0.01 - 0.02)
n = 18 n = 17
(b) cells/cm2** 15,147 (6,797 - 17,976) 6,822 (5,155 - 10,750)
n = 8 n = 8
(c) diversity 2.1878 (1.2969 - 2.5001) 2.2709 (2.1799 - 3.3058)
n = 8 n = 8

 

**Indicates grazed treatments are significantly greater than non-
grazed treatments using a Mann Whitney U-test, P = 0.05.

Algal Numbers and Diversity

 

The slides subjected to herbivorous grazing had significantly
(P = 0.05) fewer cells per unit area (Table 5 and Figure 4). After
recolonization the number of algal cells had not increased to the
same extent on the grazed as on the non-grazed slides (Table 6 and
Figure 5). The previously grazed slides were significantly lower
(P = 0.05) in the number of algal cells than the non-grazed. Because
the cell numbers are not consistently significantly different on a
date by date comparison using Mann Whitney U-tests the data imply that
the diminished ash-free dry weight of the grazed slides may be

partially due to biomass other than algae (perhaps bacteria).

27

Table 5. Treatment I median, range, a d n = number of slides analyzed
for number of algal cells/c .

 

 

Replicate Grazed Non-Grazed

1* 32,710 (31,632-33,788) 124,852 (70,601-235,790)
n = 2 n = 5

2* 12,550 (4,048-29,614) 27,997 (15,260-67,788)
n = 8 n = 8

3 7,350 (BBS-26,639) 16,420 (9,475-28,138)
n = 8 n = 8

4 9,882 (1,833-24,104) 11,145 (l,158-79,843)
n = 8 n = 8

5* 1,776 (939-7,283) 36,687 (ll,155-58,951)
n = 8 n = 8

 

*Indicates significant differences using Mann Whitney U-test,
P = 0.05.

Table 6, Treatment I median, range, and n = number of slides analyzed
for number of algal cells/cm2 from recolonized slides.

 

 

Replicate Grazed Non-Grazed

1 372,061 (185,038-599,993) 303,213 (241,072-325,444)
n = 5 n = 5

2* 132,550 (39,324-184,614) 461,352 (135,976-960,009)
n = 8 n = 8

3 59,904 (21,380-412,523) 153,943 ( 4,272-520,277)
n = 8 n = 8

4 68,208 (26,604-165,532) 50,495 (30,739-147,401)
n = 8 n = 8

5* 26,267 (5,314-70,973) 412,967 (311,621-591,992)
n = 8 n = 8

 

*Indicates significant differences using Mann Whitney U-test,
P = 0.05.

1000000:
(<7 ..
E -
3
ID
: 100000:
0 I
m _
a: -
14.1
m -
Z
3
2
10000:
U) a
L” I
8 -
LL] -
0- ..
U)
1000

 

28

'9'“ NON-GRAZED
‘1'— GRAZED

 

 

1* é* 6 3. 6*
REPLICATES

Figure 4. Species numbers plotted by replicate from Treatment I.
* indicates significance using Mann Whitney U-test at

P = 0.05.

29

 

 

 

1000000:
6? _
E -
\°
: 100000:
a) -
(I: _
lu
m1 -
IE
:3
:2
10000:
U) _
L“ I
0 - 45-"- NON-GRAZED
m cl
0- ‘- -+—- GRAZED
a)
1000 r I T .0 r 1
C) 1 2* 3 4 5?

REPLICATES

Figure 5. Species numbers plotted by replicate from Treatment I
recolonized slides. * indicates significance using
Mann Whitney U-test at P = 0.05.

30

In Treatment II the grazed slides have a significantly greater
(Mann Whitney U-test, P = 0.05) number of algal cells/cm2 and ash-free
dry weight than the non-grazed (Table 4).

The Shannon Weaver Information Index (Shannon and Weaver 1949)
was used to determine species diversity (H' = 2 pi 1npi) where pi is
the proportion of all diatom species present represented by species i.
Median indices were compared (Friedman analysis of variance). Egygg.
gyrjgg grazing significantly decreased diversity in Treatment I
(Table 7 and Figure 6) but had no effect on diversity after recoloni-
zation (Table 8 and Figure 7). Grazing had no effect on diversity in

Treatment II (Table 4).

Differential Grazing

 

The diatom community composition was compared for each genus by
calculating the percent which the genus represented of the total cell
count on that slide. Comparisons between grazed and non-grazed
substrata were made using a Friedman analysis of variance for Treat-
ment I (Table 9 and Figure 8) and a Mann Whitney U-test for Treatment
II. All such comparisons assume that each species represented the
same proportion of the community before being subjected to the treat-
ments. Graphical presentation of the Treatment I data is found in
Figure 8.

In Treatment I Navicula was significantly lower (P = 0.05) on
the grazed slides (Table 9). It is noteworthy that the percent of the
girdle views (diatoms not lying with the identifying value in view)
were also significantly lower in the grazed situation. The percentage

of girdle views closely parallels the percentage of Navicula. It is

31

 

 

Table 7. Treatment I median, range, and n = number of slides analyzed
for species diversity H' = 8 pi 1np .
1
Replicate Grazed Non-Grazed
1 1.9175 (1.7768-2.0583) 1.8991 (1.8029-1.9702)
n = 2 n = 5
2 1.6230 (1.2086-l.8338) 1.7569 (1.5707-1.8638)
n = 8 n = 8
3* 1.8280 (1.3584-2.0232) 1.9913 (1.8638-2.0988)
n = 8 n = 8
4* 1.6453 (1.3657-2.0134) 1.8543 (1.6232-1.9887)
n = 8 n = 8
5 1.1369 (0.9016-1.3134) 1.2607 (1.0723-1.4401)
n = 8 n = 8

 

*Indicates significant differences using Mann Whitney U-test,

 

P = 0.05.
Table 8. Treatment I median, range, and n = number of slides analyzed
for species diversity H' = 2 pi 1np from recolonized
slides. i
Replicate Grazed Non-Grazed

 

1

4*

1.6242 (1.5863-1.7124)

n 5
1.3440 (0.9161-1.5977
n = 8
1.5800 (1.1123-l.9167)
n = 8
1.2341 (0.9984-1.4417)
n = 8
0.6990 (0.6282-l.0737)
, n = 8

1.6185 (1.4343-1.7281)

n 5

1.3805 (1.1816—1.6568)
n = 8

1.4461 (1.0274-1.8029)
n = 8

1.4982 (1.0076-l.9004)
n = 8

0.7682 (0.6077-0.8975
n = 8

 

*Indicates significant differences using Mann Whitney U-test,

P = 0.05.

32

 

 

 

200‘
108'
.x 1.6-
1.1.1
:3
Z
a: 1.4-
LIJ
:>
<
Lu
:3
z 102‘
0
Z
Z
«c
3:
CD 1.0-1
em- NON-GRAZED
4—GRAZE0
008'
006 F l r T 1
0 1* 2 3* 4* 5
REPLICATES
Figure 6. Shannon Weaver Index plotted by replicate for Treatment I.

* indicates significant difference using a Mann Whitney
U-test at P = 0.05.

33

 

 

 

23-() n
_ 6m- NON-GRAZED
+——GRAZED
108.1
x 1.6~
Lu
C3
2
a: 1.4d
m ,
.>
4:
Lu
:3
z 102‘
D
Z
Z
«c
I
00 1 .() -
1008‘
0-6 I r T T l
0 1 2 3 4* 5
REPLICATES
Figure 7. Shannon Weaver Index plotted by replicate for Treatment I

recolonized slides. * indicates significant difference
using a Mann Whitney U-test at P = 0.05.

34

 

 

 

Table 9. Treatment I median, range, and n = number of slides analyzed
for the percent of the community for each major genus.
Genus Replicate Grazed Non-Grazed
Achnanthes 1 32.8 (18.1-47.5) 29.3 (13.6-24.7)
n = 2 n = 5
2 41.0 (25.2-53.9) 43.0 (26.9-45.4)
n = 8 n = 8
3** 46.1 (30.5-65.9) 33.2 (25.0-45.3)
n = 8 n = 8
4 52.2 (25.6-65.4) 37.0 (28.9-54 6)
n = 8 n = 8
5 68.9 (58.6-74.5) 70.9 (66.5-74.9)
n = 8 n = 8
Cymbella 1 14.3 (8.2-20.4) 16.2 (14.9-22.3)
n = 2 n = 5
2 7.5 (6.4-13.5) 8.7 (4 9-10.1)
n = 8 n = 8
3 8.3 (3.4-11.1) 8.4 (5.9-10.8)
n = 8 n = 8
4 6.0 (0.8-10.7) 6.6 (4.1-9.2)
n = 8 n = 8
5 1.7 (0.0-6.3) 2.3 (1.8-4.8)
n = 8 n = 8
Epithemia 1 5.6 (4.2-7.0) 4.2 (1.9-8.2)
n = 2 n = 5
2* 0.9 (0.2-6.5) 1.2 (0.7-2.0)
‘ n = 8 n = 8
3 5.7 (1.2-8.2) 7 1 (3.5-9.3)
n = 8 n = 8
4 3.4 (1.8-8.0) 6.1 (3.9-7.7)
n = 8 n = 8
5* 0.8 (0.2-2.2) 1.7 (0.9-5.1)
n = 8 n = 8
Eunotia 1** 4.0 (1.7-2.4) 1.0 (0.1-1.8)
n = 2 n = 5
2 1.2 (0.8-4.3) 1.2 (0.6-1.9)
n = 8 n = 8

35

 

 

 

 

Table 9. (Continued)
Genus Replicate Grazed Non-Grazed
Eunotia 3 3.7 (1.0-8.2) 1.4 (0.4-2.2)
(continued) n = 8 n = 8
4 2.2 (0.7-4.0) 1.2 (0.4-2.2)
n = 8 n = 8
5** 1.3 (0.5-1.8) 1.9 (0.9-2.3)
n = 8 n = 8
Fragilaria l 2.9 (2.3-3.5) 2.6 (l.8-4.8)
n = 2 n = 5
2* 1.6 (0.7-3.1) 3.4 (1.2-5.4)
n = 8 n = 8
3 2.3 (0.4-6.7) 4.9 (3.8-8.2)
n = 8 n = 8
4 5.5 (1.3-7.0) 3.6 (1.7-7.3)
n = 8 n = 8
5* 1.2 (0.3-5.6) 4.2 (2.0-6.0)
n = 8 n = 8
Gomphonema 1 4.1 (4.1) 3.2 (2.1-4.7)
n = 2 n = 5
2 6.0 (2.7-8.5) 5.2 (3.0-7.3)
n = 8 n = 8
3 4.6 (1.9-15.5) 2.9 (1.3-4.0)
n = 8 n = 8
4* 3.4 (1.5-3.8) 5.4 (2.7-9.5)
n = 8 n = 8
5** 14.4 (3.4-22.9) 4.3 (3.7-8.9)
n = 8 n = 8
Navicula 1* 11.5 (10.9-12.2) 17.8 (16.6-22.0)
n = 2 n = 5
2* 11.4 (7.0-16.1) 17.4 (12.3-19.6)
n = 8 n = 8
3* 9.8 (5.4-16.6) 15.0 (12.2-20.2)
n = 8 n = 8
4 11.2 (4.4-19.6) 12.9 (7.7-16 2)
n = 8 n = 8

36

 

 

Table 9. (Continued)
Genus Replicate Grazed Non-Grazed
Navicula 5* 3.4 (2.1-7.6) 5.5 (4.1-7.0)
continued) n = 8 n = 8
Girdle Views 1* 19.0 (13.6-24.3) 26.1 (20.9-30.6)
n = 2 n = 5
2* 15.3 (9.8-20.1) 23.3 (18.5-29.9)
n = 8 n = 8
3* 8.9 (4.1-17.0) 15.7 (10.6-20.8)
n = 8 n = 8
4 11. 9 (4. 3- 26. 0) 17.1 (8.3-19.7)
= 8 n = 8
5* 1. 0 n(0. 5- 4. 8) 3.5 (1.7-4.3)
= 8 n = 8

 

*Indicates grazed treatments are significantly less than non-grazed
using a Mann Whitney U- test at P= 0. 05.

**Indicates grazed treatments are significantly greater than non-

grazed using a Mann Whitney U-test at P =

0.05.

Figure 8.

37

Percent of the community plotted by replicate for

 

Achnanthes, C bella, Epithemia, Eunotia, Fragilaria,
Navicula, and girdle View ofTTreatment I. 7* indicates
significant differences using a Mann Whitney U-test

at P = 0.05; = grazed, ------ = non-grazed.

 

 

38

CYMBELLA

 

r2

EUNOTIA

 

 

 

201-

ACHNANTHES

10"

 

 

 

 

5
0
3..
6

EPITHEHIA

 

 

8C1-

60‘-

 

 

 

20‘-
O
8 .
6

>FHZDZZOQ mo Hzmommm

REPLICATES

Figure 8

PERCENT OF COMMUNITY

39

3. FRAGILARIA 20. communism

 

 

 

 

 

 

4~ lo-
2- s-
o . r r . s o

o l 2* 3 4 5* o
20. NAVICULA 30-

.--.
--.‘

ls~ 23-
lo- 15-
5- e-
0 U r r O

 

 

 

 

 

01*2*3*4?* o

REPLICATES

Figure 8 (Continued)

40

possible that the major portion of the girdle view category was, in

fact, Navicula. Eunotia and Gomphonema on the contrary, were signi-

 

ficantly higher on the grazed slides than on the non-grazed slides

(P = 0.05). In Treatment II (Table 10) Eunotia, Fragilaria, and

 

Gomphonema were found to be a significantly higher proportion of the

 

community under a grazing regime.

Data from the recolonization portion of Treatment I are presented
(Table 11 and Figure 9) in the same manner as data in Table 9 and
Figure 8. These calculations were made to determine if grazing had
any effect on recolonization. Grazing had no effect on the pattern
of recolonizing by the diatoms. No statistically significant

differences were found using a Friedman analysis of variance.

41

Table 10. Treatment II median, range, and n = number of slides
analyzed for the percent of the community for each
major genus.

 

 

 

 

 

Genus Grazed Non-Grazed
Achnanthes 21.1 (17.7-23.1) 16.9 (12.2-34.7)
n = 8 n = 8
Cymbella 9.7 (6.4-11.1) 8.2 (3.4-25.5)
n = 8 n = 8
Egithemia 12.6 (6.8-19.2) 13.9 (9.8-29.0)
n = 8 n = 8
Eunotia** 1.3 (0.5-1.8) 1.9 (0.9-2.3)
n = 8 n = 8
Fragilaria** 6.6 (3.9-8.6) 11.6 (7.4-13.3)
n = 8 n = 8
Gomphonema** 2.5 (2.0-3.8) 4.4 (2.5-8.9)
n = 8 n = 8 ,
Navicula 15.9 (11.8-20.9) 13.8 (11.7-32.6)
n = 8 n = 8
Girdle Views 18.1 (16.4-22.1) 17.2 (15.7-40.0)
n = 8 n = 8

 

**Indicates grazed treatments are significatnly greater than non-
grazed treatments using Mann Whitney U-test at P = 0.05.

42

 

 

 

Table 11. Treatment I median, range, and n = number of slides
analyzed for the percent of the community each genus
represents from the recolonized slides.

Genus Replicate Grazed Non-Grazed

Achnanthe§_ 1 36.7 (31.4-46.2) 44.0 (37.8-58.5)

n = 5 n e 5
2 65.2 (49.2-78.8) 58.6 (41.8-67.2)
n = 8 n = 8
3 56.4 (34.5-71.4) 65.1 (55.4-74.1)
n = 8 n = 8
4** 69.2 (61.2-77.7) 64. (41.9-75 8)
n = 8 n = 8
5 83.3 (70.1-85.4) 82. (78.3-87.5)
n = 8 n = 8
Cymbella l 8.8 (5.1-9.2) 7. (6.5-11.4)
n = 5 n = 5
2 3.9 (l.8-8.4) 4. (2.0-7.9)
n = 8 n = 8
3** 5.6 (2.1-10.7) 3. (l.l-4.8)
n = 8 n = 8
4 2.6 (1.6-4.5) 3. (1.8-5.0)
n = 8 n = 8
5 0.4 (0.2-0.9) 0. (0.2-1.7)
n = 8 n = 8
Epithemia 1 1.2 (0.5-2.4) 1. (1.0-1.8)
n = 5 n = 5
2 1.4 (0.7-2.1) l. (0.4-2.7)
n = 8 n = 8
3** 3.3 (1.7-4.9) 1. (0.6-2.6)
n = 8 n = 8
4 2.8 (1.1-5.0) 3. (1.4-8.2)
n = 8 n = 8
5 0.3 (0.0-0.5) 0. (0.2-1.2)
n = 8 n = 8

43

 

 

 

 

Table 11. (Continued)
Genus Replicate Grazed Non-Grazed
Eunotia 1 1.0 (0.6-1.9) 0.8 (0.4-1.0)
n = 5 n = 5
2** 1.2 (0.0-2.8) 0.3 (0.1-0.7)
n = 8 n = 8
3 0.8 (0.2-2.4) 0.4 (0.0-1.3)
n = 8 n = 8
4* 0.7 (0.3-2.4) 1.2 (0.4-5.3)
n = 8 n = 8
5 0.5 (0.3-2.3) 0.4 (0.1-0.6)
n = 8 n = 8
Fragilaria l 0.8 (0.2-1.6) 1.2 (1.0-1.4)
n = 5 n = 5
2 0.7 (0.3-1.0) 0.6 (0.0-1.6)
n = 8 n = 8
3 2.2 (0.6-3.9) 1.8 (0.0-3.7)
n = 8 n = 8
4 1.9 (1.4-2.8) 2.3 (0.0-3.9)
n = 8 n = 8
5* 1.9 (1.4-2.8) 2.3 (0.0-3.9)
n = 8 n = 8
Gomphonema 1 3.2 (1.7-4.5) 2.4 (2.0-3.6)
n = 5 n = 5
2** 4.3 (1.3-6.7) 2.4 (2.0-3.6)
n = 8 n = 8
3** 2.5 (1.4-4.1) 1.7 (0.7-2.3)
n = 8 n = 8
4 2.0 (1.3-3.3) 2.3 (0.0-12.0)
n = 8 n = 8
5** 4.2 (1.8-6.4) 1.5 (1.0-2.9)
n = 8 n = 8
Navicula 1 17.2 (12.9-21.1) 15.7 (10.9-17.6)
n = 5 n = 5
2* 9.8 (4.5-12.3) 13.0 (8.0-20.2)
n = 8 n = 8

44

 

 

Table 11. (Continued)
Genus Replicate Grazed Non-Grazed
Navicula 3 9. 7 n(4. 3- 17. 6) 10.2 (5.7-14.0)
(continued) = 8 n = 8
4 4. 9 n(1. 78 2) 7.1 (3.3-10.1)
= 8 n = 8
5 1. 8n (1. 1 -.12 8) 2.3 (Ll-7.2)
= 8 n = 8
Girdle Views 1 21.9 (20.6-31.5) 21.0 (13.0-27.9)
n = 5 n = 5
2* 9.0 (2.8-10.7) 11.4 (9.7-17.7)
n = 8 n = 8
3 7.0 (3.3-18.1) 6.3 (3.5-12.6)
n = 8 n = 8
4 4. 3 (2. 0- 8. 4) 5.8 (2.5-12.7)
= 8 n = 8
5 0. 3 n( .0- 1. 0) 0.7 (0.2-2.5)
= 8 n = 8

 

*Indicates previously grazed treatments are significantly less than

non-grazed using Mann Whitney U-test at P =

0.05.

**Indicates previously grazed treatments are significantly greater

than non-grazed using Mann Whitney U-test at P =

0.05.

Figure 9.

45

Percent of the community plotted by replicate for

Achnanthes, C bella, Epithemia, Eunotia, Fragilaria,
N6v1cula, and Girdle Views of Treatment I—reCOTofiized

slides. * indicates significant differences using a
Mann Whitney U-test at P = 0.05; = grazed,
------ = nongrazed.

 

 

 

46

 

ACHNANTHES

 

r2

rel

 

m-
w-
w-

 

»HHZDZZOQ do Hzmommm

EUNOTIA

 

 

8.
REPLICATES

Figure 9

 

EPITHEMIA

 

 

PERCENT OF COMMUN I TY

47
3. FRAGILARIA e- GOMPHONEMA

 

 

 

 

 

 

 

 

 

 

 

20 . mmcuu 30 - GIRDLE VIEW
15-- 23-
10- is-
5- e-
o . . . T . o
o 1 2* 3 4 5 o
REPL I CATES

Figure 9 (Continued)

DISCUSSION

Data from Treatment I indicate that at high densities the grazing
of Physa gyrina (Say) decreased the standing crap (as measured by ash-
free dry weight). Mean algal cell numbers were also significantly
lower when intensively grazed. In other words, over the 48 hour
grazing period the epiphytes did not increase growth to compensate
for lost biomass. Snail densities in Treatment I are likely comparable
to snail densities (50 snails/plant) for a short post-hatching period
in early spring (DeWitt 1954a) prior to dispersal. Young snails,
although smaller than snails used in this study, feed continuously
(DeWitt 1955) and therefore could have a similar impact as the larger
snails less voracious in the laboratory. The results of this study
are similar to those of Hickman and Round (1970) who found that snail
grazing reduced vernal epipelic standing crap. At high densities E,
Igyrigg_may be capable of depleting a major portion of epiphytic
population over a longer span of time, e.g., the growing season, as
determined by Castenholz (1961a) for Littorina spp. Tadpoles have
' been shown to greatly reduce the epibenthic algal population before
metamorphosing (Dickman 1968). High intensity grazing by snails is
unlikely to persist for extended periods of time, however. As peri-
phytic resources were depleted, increased emigration and mortality
should reduce the snail population to the carrying capacity of the

periphytic community. The "tadpole effect" observed by Dickman (1968)

48

49

created intense grazing pressure on the community for a relatively
short time. The algal periphyton, therefore, had a temporal refuge
following metamorphosis of the tadpoles during which the population
could increase. This type of refuge would not be available under
intense E, gyrigngrazing as these snails do not leave the system.
Physa gyrina populations may also be reduced from the early spring

maximum by aquatic predators such as the pumpkinseed (Lepomis gibbosus)

 

whose diet may be composed of as much as 49% gastropods (Keast 1978),
and brown bullhead (Ictalurus nebulosus) (Keast and Harker 1977), or

by avian predators such as the upland plover (Bartramia longicauda)

 

(Purchon 1968) to lower densities comparable to those found in late
summer in Lawrence Lake. At lower snail densities over a longer time
period competition for periphytic food would be lessened; fewer
grazers would remove less of the biomass. Remaining algal cells
would then have time to respond to the more moderate grazing pressure.
Grazing enhanced the growth of periphyton as shown by the ash-free
dry weight and the number of algal cells per square centimeter
(Treatment II). Enhancement may be caused by a number of factors.
One possible mechanism is nutrient regeneration through excretion or
the elimination of fecal material as Flint and Goldman (1975)
suggested for crayfish. Pomeray (1970) emphasized nutrient regenera-
tion through fecal material as a general mechanism for increased
nutrient availability and hence increased productivity. Second,
senescent cells may limit other viable cells from attaining nutrient
or light requirements; cropping would remove the senescent cells as
suggested by Cooper (1973). Thus, light and nutrient limitation would

be reduced by the removal of senescent cells. Third, cropping may

50

increase availability of new patches of substrata for colonization
much as Pisaster opens new patches in the rocky intertidal zone for
invertebrate colonization (Paine 1966). Paine and Vadras (1969) also
report on opening of patches for algal colonization by the sea urchin,

Strongylocentrotus. The urchin removes Hedophyllum, the dominant

 

 

macroalga, and by the urchin's action open spaces are created which
are available to other less competitive algae. Finally, some diatoms
may pass through the digestive system undigested because of inability
of the enzymes to penetrate the diatom frustrule. Nicotri (1977)
suggested that diatoms with less ornamentation (i.e., fewer striae)
were less susceptible to the digestive enzymes since the enzymes enter
the diatoms via performations associated with ornamentation. Thus,
whole live diatoms may pass through the gut surrounded by the high
nutrient feces and diatom growth would thereby be enhanced. Porter
(1973) suggested such a mechanism for the increased growth of some
species of phytoplankton ingested by zooplankton. All of these
suggested mechanisms need further investigation. Collection and
culturing of fecal pellets would give some insight into this problem.
Another more detailed procedure might include actually marking the
precise location of grazed patches to determine if they are differen-
tially recolonized.

After recolonization the slides previously subjected to intense
grazing (Treatment I) had a significantly lower ash-free dry weight
than the control slides. The median number of algal cells per square
centimeter was also significantly lower on grazed slides. These
data lend credibility to the hypothesis that epiphytic algae under

continuous, intense grazing could not respond (i.e., reproduce) as

51

fast as they were cropped. However, the numbers of algal cells per
square centimeter from replicates 1, 3, and 4 were not lower (using a
Mann Whitney U-test) on the previously grazed slides. Consequently,
this interpretation remains in question.

The percentage of organic matter found on the slides was con-
siderably lower than that found by McIntire (1966) and Kehde and
Wilhm (1972) for stream systems. The effects of increasing current
were demonstrated to increase productivity of periphyton (McIntire
1966). Therefore, as lakes do not exhibit high continuous water flow
rates, it is possible that productivity would be lower. A study of
vertically placed glass slides in a reservoir reported a 20% accumu-
lation of organic matter over a two to four week period (Slidecek and
Sladeckové 1964). These results are reasonably similar to the 13%
organic matter found in this study.

Community composition is often quantified by the use of diversity
indices. The Shannow-Weaver Index (Shannon and Weaver 1949) is
commonly employed and is appropriate for determining species diversity
and evenness of distribution within a community such as the periphyton
(Pielou 1966, Wilhm 1970). Grazing significantly lowered the community
diversity in Treatment I. Although not significant, the diversity
indices of Treatment II also tended to be lower when grazed. After
recolonization of the substrata, the diversity was not significantly
lower on the grazed slides. Diversity of a community whether auto-
trophic or heterotrophic may be increased when the dominant competitor
of the community is selectively removed by a predator, and when the
other less dominant species can colonize the resultant patch more

rapidly than the originally dominant species. Paine (1966) demonstrated

52

the validity of this principal in the rocky intertidal zone with
Pisaster. Pisaster's preferential feeding on Mytilus opened space

for other potential substrata colonizers which were otherwise competi-
tively excluded by Mytilus. In another study fish in microcosms
feeding selectively on Ceriodaphnia released other microcrustaceans
from competitive pressure for food. The number of species which could
coexist on the food source was increased by the selective removal of
Ceriodaphnia; diversity was thereby increased (Neill 1975). In the

same manner, the selective feeding of Strongylocentrotus on the

 

dominant alga, Hedophyllum, permitted other epilithic algal species

 

to become established (Paine and Vadras 1969). Conversely, the
unselective browsing of the marine snail, Patella, decreased the
macroalgal diversity by removing many small algal species and spare-
1ings before they could become established (Jones 1946). Addicott
(1974) determined that while the species diversity of protozoans in

the leaves of the pitcher plant was reduced by predation, the species
evenness was enhanced. He postulated that the abundance of species was
controlled by the relative rates of increase of the various prey
species rather than by the predator.

Recently Lubchenco (1978) demonstrated the importance of under-
standing grazer food preferences, as well as interspecific competitive
relationships among the consumed species and the changing relationships
between physical regimes and microhabitats. She determined that a
unimodal relationship existed between algal Species diversity and

Littorina littorea density in rocky intertidal pools. SpeCies

 

diversity was highest at moderate Littorina grazing levels because

the snail's preferred food was competitively dominant in the tidal

53

pools examined. Grazing reduced the dominant species, as in the other
aforementioned studies, and allowed competitively inferior species to

persist. In my study the competitively dominant species, Achnanthes,

 

was not selectively removed by P, gyrjgg, Therefore, it is not
surprising that species diversity was reduced in the presence of
3- 9.171199-

As information concerning individual genera was not apparent
from the diversity indices, the percent of the community which each
of the major species represented was examined. A consistent pattern
is seen with Navicula which represented a significantly smaller
portion of the total community on the grazed slides than on the non-

grazed slides. Reduced proportions imply that Physa gyrina selec-

 

tively removed this epiphyte, assuming the proportion of Navicula on
grazed and non-grazed slides to be approximately equal prior to
treatment. In addition, the category labeled "Girdle Views" repre-
sented a significantly lower portion of the community. I suspect
that the majority of the girdle view cateogry was, in fact, Navicula,
based not only on the correlation but also on the morphology of the
cells. This further supports the contention of selection for
Navicula by E, gyrjgg,

Food preferences or selectivity have been recognized in inverte-
brates by numerous authors. These preferences can function to struc-
ture a community. Pisaster was shown to prefer Mytilus when offered
numerous two-way choices (Landenberger 1968). Douglas (1958)
reported preferences for epibenthic algal species by a stream caddis-

fly. Calow (1973, 1974) reported a pulmonate snail, Angylus fluvia-

 

tilis, ingested a variety of periphyton but preferred the diatom

54

genus Gomphonema. However, due to the low density of the snails, the

 

grazing disturbance had little effect in altering the proportion of

Gomphonema in the comnunity or the periphytic calmlunity as a whole.

 

Selectivity may be based on (1) nutritional value and palata-
bility (neither of which is in the scope of this study), (2) abun-
dance, or (3) ease of attainment. As Navicula was not the most
dominant member of the community, representing from 9 to 19% of the

total number of cells, while Achnanthes represented from 19 to 72%,

 

one would suspect the snail would select Achnanthes if selection were

 

based an abundance. Therefore, the availability hypothesis based on
simple abundance is unlikely. It is more probable that Navicula is
a less energetically costly food to attain. There is support for
this hypothesis in the growth form of Navicula. According to Round
(1965), members of the genus Navicula which are epiphytic are motile
and move about.through,and on the surface of the periphyton. Other
species of Navicula are reported to be stalked and attached in
chains (Round 1965). Since Navicula is above the periphytic mat of
diatoms, either motile or in chains, the snail would have to merely
skim the surface of the mat with the radula involving less resistance
to the scraping and presumedly less energy.

Other members of the periphytic community adhere more tightly to

the surface of the substrata. Achnanthes is a very small, short-

 

stalked epiphyte projecting only a small distance above the surface.
While no definite trend to select against it (or ignore it) can be
determined from the data, the significantly higher portion of

Achnanthes on the grazed slides in replicate 3 of Treatment I, using

 

6 Mann Whitney U-test, might imply that the snails do not scrape it

55

off in proportion to its abundance. However, this datum point is
more likely an artifact of the variation between boxes of slides.

Eunotia, on the other hand, represented a significantly greater
portion on the grazed slides; it is attached via a basal mucilaginous
pad which adheres to the surface of the substratum (Round 1965).
Eunotia was also significantly lower in Treatment II, giving support
to the idea that it is not readily available to E, gyrjgg, Since
Eunotia also represented such a small portion of the community further
study would be necessary to distinguish between abundance and ease
of attainment as a reason it was not selected by E, gyrigg, frggi-
lgrig, a large stalked diatom, may be easily attained by Ehygg, But
under less competitive conditions it was taken in less proportion
than its occurrence in the community (Treatment II). Since both
Eunotia and Fragilaria represented just less than 5% of the community,
it is likely that variation due to structural heterogeneity (i.e.,
patchiness) and chance are responsible for what appears to be differ-
ential grazing.

Gomphonema is a stalked and branched diatom (Round 1965); there-
fore, it was potentially available to the snail. But in both Treat-
ment I and Treatment II it accounted for a significantly greater
portion of the grazed slides, implying that the snail either did not
feed on it or that its growth was enhanced by the snails' presence.
Such an enhancement may be due to a higher reproductive rate evolved
to counteract grazing perturbations. Other diatoms are subject to
the same grazing disturbances; if this were the case, it seems likely
that they, too, would have responded by equivalent reproductive rates.

Growth enhancement could be a response to increased specific

56

micronutrients found either within snail fecal material left on the
slides or in slime trails which the snails leave on the substrata.
Gomphonema may also be grazed but remain undigested, acquiring
nutrients while in the gut; in that case, growth could be more rapid

following elimination from the snail's body. Gomphonema has only a

 

moderate amount of ornamentation. Thus the possibility exists for
the snails' digestive enzymes to have less effect on it than on a
more heavily ornamented species (e.g., Epithemia) as Nicotri (1977)
suggested. Food is in the digestive system for three to five hours
(North 1954). This length of time spent in darkness would be insuffi-
cient to kill the cell. Acquisition of micronutrients seems the most
plausible explanation for differential growth by this species.
Preferences for particular diatom genera could be obtained by
offering snails two-way choices of pure cultures on glass slides
placed in finger bowls. A ranking of preference might well be
established from this type of study. Snails may also show greater
selection when not starved prior to preference feeding tests. Landen-
berger (1968) found the starfish, Pisaster, exhibited greater
selectivity when food was not withheld prior to preference tests.
Nicotri (1977) suggested that three species of marine snails and one
species of periwinkle grazed more selectively and assimilated algal
cells less efficiently when food was not limiting. It might, there-
fore, be construed that E, gyrigg_exhibits greater selection when
food is in abundance and hunger levels are reduced. When the snails
were starved (Treatment I), they fed preferentially on a species
which was presumedly easy to obtain (i.e., Navicula). However, when

food was abundant and snail densities were reduced, the preference

57
for Navicula was not observed. The snails did not feed selectively
on any species in Treatment II. Instead, three species, Eunotia,

Fragilaria, and Gomphonema were found in greater abundance on the

 

grazed slides. Two of these species, Eunotia and Gomphonema,were also

 

found in higher abundance on grazed slides in Treatment I. Possibly,
these three species were avoided by the snails. Avoidance of a diatom

species (Cocconeis) by a congener of E, gyrina (P, heterostraphg) was

 

observed (Patrick 1970). Therefore, avoidance is a possibility.

The recolonization data show the response of the periphytic
community after grazing. By again comparing the percent of each
genus in the community, more information can be obtained than by

evaluating the diversity index alone. Achnanthes accounted for a

 

generally increased portion of the community after recolonization
regardless of laboratory treatment (i.e., grazed or control). Perhaps

Achnanthes was an early colonizer in the successional process on

 

apical portions of macrophyte surfaces. As the process continued,

Achnanthes may have become a proportionately less dominant member of

 

the community. But as snails opened new patches by grazing, Achnanthes

 

could have maintained dominance. Or perhaps this species being small
in size can exploit smaller spaces and hence remain the superior
competitor. In Treatment II when grazing extended over a longer

period of time, while Achnanthes was a relatively smaller portion of

 

the community, it was still the dominant species. The data do not
lend support to either hypothesis.

Variation between slides and boxes of slides presented diffi-
culty in the analysis of this study. Variation may have been reduced

by increasing sample size; but analysis, especially enumeration,

58
became unwieldy even for the samples counted in this study. Another
possible way to reduce variation would be to colonize larger glass
plates, sample small sections of the plate prior to treatment, and
allow snails to graze only one-half of the plate. Gut analysis might
help to determine snail preferences, unless cells are differentially
digested. Gut analysis might also prove valuable in analysing data
from the two-way preference tests mentioned earlier. Additionally,
future study might entail varying the densities of snails around
natural macrophytic substrata which would be enclosed.

This study raises several issues. How important is E, gyrigg_
in altering the structure of the periphytic community? Larger more
voracious grazers such as tadpoles are capable of completely removing
a major portion of periphyton during an early phase of their develop-
ment (Dickman 1968). Small grazers may also change the structure of
the periphytic community. For example, the mayfly nymph (ghlgggg),

a cyclopoid copepod, a chydorid, and a chironomid larva have been
observed feeding on epiphytic algae (Allanson 1973). Hyalella
gztegg, an amphipod, feeds predominantly on periphytic algae (Har-
grave l970b); a ciliated protozoan reportedly feeds on diatoms
(Brook 1952) of the same genera as were removed by E, gyrigg_in this
study. These organisms as well as other gastropods influence the
structure of the periphytic community. Which organisms are respon-
sible for the major alterations in comnunity structure has not yet
been determined.

What mechanisms control diatom preferences by Physa gyrina? Is

 

it less energetically costly to graze only diatoms not securely

attached to the surface and therefore to skim only the surface of

59

the periphytic mat? Are certain diatoms (for instance, Gomphonema)

 

differentially digestible; and does ingestion enhance the micro-
nutrient climate surrounding the cells passing viably through the
gut? From this study it appears that P, gyrigg_might function as to
partially regulate the periphytic community by decreasing the algal
population at high densities while increasing it at lower densities.
Selection of Navicula, whether a preference due to palatability,
digestibility, or attainability, does, in fact, alter the structure

of the periphytic community. Enhancement of the growth of Gomphonema,

 

whether the mechanism is an increased nutrient concentration provided
in the gut or by the deposited fecal material, also plays a role in

regulation of the heterogeneity of the periphytic community.

l)

3)

4)

CONCLUSIONS

At high densities of Physa gyrina grazing the periphytic standing

 

crop, the numbers of diatom cells/cm2 of glass substrate and the
community diversity were significantly reduced.

At high densities P, gyrjgg_preferentially removed Navicula.

Two weeks after intense grazing ceased, the previously grazed
substrates were significantly lower in standing crop and cell
numbers. Community diversity was not lower on the previously
grazed slides.

At lower densities snail grazing significantly increased peri-
phytic standing crop, numbers of diatom cells/cm2 of the sub-

strate, and the growth of Gomphonema, Fragilaria, and Eunotia.

 

 

60

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