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1977 A Seasonal and Ecological Survey of Freshwater Limpet Snails and Their Digenetic Trematode Parasites in Southeastern Louisiana. Hugh Michael Turner Louisiana State University and Agricultural & Mechanical College

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Recommended Citation Turner, Hugh Michael, "A Seasonal and Ecological Survey of Freshwater Limpet Snails and Their Digenetic Trematode Parasites in Southeastern Louisiana." (1977). LSU Historical Dissertations and Theses. 3140. https://digitalcommons.lsu.edu/gradschool_disstheses/3140

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University Microfilms international 300 North Zaeb Road Ann Arbor, Michigan 4B106USA St. John’s Road, Tyler's Green High Wycombe, Bucks, England HP10 8HR TURNER, Hugh Michael, 1942- A SEASONAL AND ECOLOGICAL SURVEY OF FRESHWATER LIMPET SNAILS AND THEIR DIGENETIC TREMATODE PARASITES IN SOUTHEASTERN LOUISIANA. The Louisiana State University and Agricultural and Mechanical College, Ph.D., 1977 Zoology

Xerox University Microfilmsf Ann Arbor, Michigan 48106 A SEASONAL AND ECOLOGICAL SURVEY OP FRESHWATER LIMPET SNAILS

AND THEIR DIGENETIC TREMATODE PARASITES

IN SOUTHEASTERN LOUISIANA

A Dissertation

Submitted to the Graduate Faculty of the Louisiana State University and Agricultural and Mechanical College in partial fulfillment of the requirements for the degree of Doctor of Philosophy

in

The Department of Zoology and Physiology

by Hugh M. Turner B.S., Georgia Southern College, 1965 M.S., Georgia Southern College, 1972 August, 1977 ACKNOWLEDGEMENT

I would like to thank the members of my Graduate

Committee, Drs. G. H. Lowery, Jr., W. J. Harman, J. M.

Fitzsimons, and E. H. Weidner for the guidance they provided throughout my graduate program. Special thanks are due my Major Professor, Dr. K. C. Corkum, for his help.

I wish also to extend thanks to Dr. R. F. McMahon of the university of Texas at Arlington for confirming identi­ fication of limpets; to Dr. F. G. Thompson of the Florida

State Museum for sharing his knowledge of Florida ancylid snails; to the LSU Foundation, the LSU Student Government

Association, and the LSU Department of Zoology and

Physiology for providing funds for travel in support of this research. TABLE OF CONTENTS

Page

Acknowledgement...... ii

Table of Contents...... ill

List of Appendix F i g u r e s ...... iv

A b s t r a c t ...... vi

Introduction ...... 1

Materials and Methods ...... 16

Results and Observations ...... 22

D i s c u s s i o n ...... 53

Literature C i t e d ...... 61

V i t a ...... 89 LIST OF APPENDIX FIGURES

Page

69 FIGURE 1. 69 f i g u r e 2. Cercaria type II . . . 69 FIGURE 3. carcaria type III . . • 69 FIGURE 4. 69 f i g u r e 5. Cercaria type„V . . . . 69 f i g u r e 6. Cercaria type VI . . . 69 f i g u r e 7. Cercaria type VII . . . 71 FIGURE 8. Cercaria type VIII . . 71 FIGURE 9. Cercaria type IX . . . 71 FIGURE 10. 71 FIGURE 11. Cercaria type XI . . 71 FIGURE 12. Cercaria type XII . . 71 FIGURE 13. Cercaria type XIII 71 FIGURE 14. Cercaria type XIV . . 73 FIGURE 15. Cercaria type XV . . 73 FIGURE 16. Cercaria type XVI . . 73 FIGURE 17. Cercaria type XVII 73 FIGURE 18. Cercaria type XVIII . 73 FIGURE 19. Cercaria type XIX . .

FIGURE 20. Monthly incidence of infection, popula­ tion structure, and index of relative abundance for limpets occurring at Ben 75 Hur Farm ......

iv Page

FIGURE 21. Percent Ben Hur Farm Hebetancylus excentricus in either septate or post-septate phases ...... 77

FIGURE 22. Septate Hehetancylus excentricus exhibiting various degrees of septum formation ...... 77

FIGURE 23 . Post-septate Hebetancylus excentricus...... 77

FIGURE 24. Monthly incidence of infection, population structure, and index of relative abundance for limpets occurring at Beaver Pond Br a n c h ...... 79

FIGURE 25. Monthly incidence of infection, population structure, and index of relative abundance for limpets occurring at Head of Island Pond .... 81

FIGURE 26. Monthly incidence of infection, population structure, and index of relative abundance for limpets occurring at R a m a h ...... 83

FIGURE 27. Monthly incidence of infection, population structure, and index of relative abundance for limpets occurring at Sorrento ...... 85

FIGURE 28. Southeastern Louisiana ancylid species as circles encompassing hosted cercariae...... 87

FIGURE 29. Southeastern Louisiana ancylid species as overlapping circles encompassing "shared,r and exclusively hosted cercariae...... 87

v ABSTRACT

An 18-month survey involving almost 20,000 freshwater limpet snails of the family Ancylidae revealed three species, each representing a different genus, occurring in southeastern Louisiana.

Laevapex fuscus was collected only from lentic habitats, where it exhibited, at most, a bivoltine pattern of repro­ duction with two successive generations per year; in habitats of low primary productivity a single annual generation was produced. Ferrissia fragilis was collected from lotic and lentic habitats and produced a single annual generation. Hebetancylus excentricus also displayed a broad habitat preference but exhibited up to a trivoltine pattern of reproduction.

Southeastern Louisiana ancylid snails play a major role in the ecology of digenetic trematodes, as evidenced by the observation that 19 species of larval trematodes were found developing in three ancylid species. Hosts, descriptions, seasonality of incidence, and possible identity of these cercariae are given.

Seasonality of trematode intramolluscan stages was closely related to seasonality of the ancylid snail hosts.

Bivoltine patterns of reproduction for H. excentricus were

vi reflected in two generations of cercarial production.

On the basis of comparative ecology, anatomy, and hosted trematodes, I propose that Hebetancylus occupies

an intermediate phylogenetic position between Ferrissia

and Laevapex. Ferrissia is least specialized in terms

of its hosted trematode fauna, which bears similarity

.to that hosted by snails of the family Planorbidae.

vii INTRODUCTION

Purpose of Study

The objectives of this study are: (1) to determine the freshwater limpet (Ancylidae) fauna of southeastern

Louisiana, (2) to investigate its ecology including habitat, seasonality, and population biology, (3) to investigate its role in the ecology of digenetic trematode parasites, (4) to provide descriptions and figures of trematode cercariae developing in southeastern Louisiana ancylids, (5) to identify cercariae by life cycle studies and/or survey of trematode life history literature, and

(6) to postulate a phylogenetic relationship for south­ eastern Louisiana ancylids based upon ecology, certain anatomical features, and similarities and differences in hosted trematodes.

Anatomy, Distribution, and Phyloqeny of North American

Ancylids

Freshwater limpet snails of the family Ancylidae are pulmonate gastropods that have become entirely aquatic in their respiration. Although members of the order Basom- matophora, they have lost the mantle-cavity lung and instead evolved a secondary gill, the pseudobranch, as an evagina- tion of the mantle wall near the anus (McMahon, 1975). Basch (1963) noted that the term "limpet" is descrip­ tive of general shell shape and does not imply an affinity between marine limpets and ancylid snails. In fact, authorities on the family (Hubendick, 1955; Basch, 1963) believed it to be derived from the coiled basommatophoran family Planorbidae. Ancylids, however, evolved an uncoiled, and in some species, almost bilaterally symetrical, conical shell. Shis arrangement leaves the entire ventral surface as the shell aperture and causes much of the "soft-parts" to be exposed to desiccation during periods of drought

(Boss, 1974) .

Presumably as an adaptation to desiccation, some individuals of certain species form a septum that serves as a functional epiphragm partially closing the aperture (Basch, 1963; Boss, 1974) . Richardot et al.

(1972) reported that under certain undetermined environ­ mental conditions and among certain individuals in popu­ lations of the European ancylid Ferrissia wautieri

(Mirolli) peripheral shell growth ceased and a septum or thin, horizontal, calcareous shelf was formed. This septum was deposited by the posterior margin of the mantle and was of the same composition and crystalline structure as the shell. Later, when peripheral shell deposition resumed, growth was from the margin of the constricted 3 aperture and resulted in what Parodiz (1957) called the

"post-septate" phase.

Septate ancylids were assigned to the genus Gundlachia

Pfeiffer; however, Basch (1959), in reviewing the 3tatus of

Gundlachia, questioned its validity. Basch (1963) later concluded that North American septate ancylids were refer­ able to Ferrissia fragilis (lyron). Burch and LoVerde (1974) noted that the apical shell sculpturing of G. californica

Rowell, as seen by scanning electron microscopy, was identical with F. fragilis and thus confirmed their synonomy.

Basch (1963) further noted that septum formation by some individuals in a population represented the only case of conspicuous dimorphism among the Basommatophora.

Dimorphism had not been reported for other North

American ancylids, nor had there been reports on the genetics or seasonality of septum formation in natural or laboratory populations. As a result of my research,

I noted the seasonal occurrence of septum formation in the freshwater limpet Hebetancylus excentricus (Morelet) in Louisiana (Turner, 1977).

Basch (1963), in his monograph on North American ancylids, recognized the following five living genera and 12 species: Acroloxus coloradensis (Henderson);

Ferrissia fragilis, F. mcneilli Walker, F. parallela 4

(Haldeman), F . rivularis (Say) and F. walkeri (Pilsbry and

Ferriss); Hebetancylus excentricus; Laevapex fuscus (Adams)

and L. diaphanus (Halderaan); also Khodacmea elatior

(Anthony); R. f ilosa (Conrad) and R. hinkleyi (Walker).

Acroloxus Beck is dextral; other living ancylids are

sinistral. For this and other reasons, Hubendick (1962)

suggested Acroloxus has greater affinities with the family

Latiidae and therefore should be placed in a distinct

family. The collection of A. coloradensis from Endora

Lake, Colorado, (Walker, 1925) represents the only record

from the United States. There exist two other records; both from lakes in Alberta, Canada (Mozley, 1954) . The

apparent rarity of this species was indicated *dien Basch

(1963) noted that extensive collecting by himself and

others, including Dr. Robert Pennak, failed to yield

additional specimens from the Colorado locality.

According to Basch (1963), Hhodacmea Walker was res­

tricted to the mountain drainages of Kentucky, Tennessee,

and Alabama; however, he believed the genus was approaching

extinction because of dams and pollution rendering habitats

unsuitdsle. In his survey only R. elatior could be collect­

ed and then only from the Cahaba River near Helena, Alabama.

Extinction seems to have been the fate of the coiled genera

Neoplanorbis Pilsbry and Amphigyra Pilsbry, which were 5 restricted to the Coosa River in Alabama and are included among the Ancylidae by some workers (Clench, 1959; Basch,

1963).

Hebetancylus excentricus has a Caribbean distribution, but has been reported in North America from southern

Florida, coastal Georgia (Basch, 1963), south central Texas

(Pilsbry, 1889; Walker, 1903), north central Texas

(McMahon and Aldridge, 1976), southern Oklahoma (McMahon, et al., 1976) and southeastern Louisiana (Turner, 1977).

Laevapex fuscus is distributed throughout the tJhited

States and southern Canada east of the Rocky Mountains

(Basch, 1963; Clarke, 1973). L. diaphanus, according to

Basch (1963), had a wide distribution extending from

Georgia to Delaware and west to Arkansas; however, he

found specimens only in the South Fourche River, Perry

County, Arkansas, and suggested that the species was under­ going a reduction in range.

Taxonomic treatment of the genus Ferrissia Walker,

as given by Basch (1963), drew criticism (Dr. Fred G.

Thompson, 1976 per. comm.), and his scheme has not been

adopted by such recent workers as Malek and Cheng (1974) .

More than 24 names have been included in North American

Ferrissia, however, Basch noted great variability and plasticity in shell morphology with production of 6 ecotypes. He reduced the genus to five North American species.

F. fracilis is widely distributed throughout the united States, but has not been reported from Canada or

Mexico (LaRocque, 1953; Basch, 1963; Clarke, 1973).

Ranges for other species are either unknown or of limited extent. F. mcneilli is an example of the latter, and has been reported only from the Mobile, Alabama, area (Walker,

1925).

As concerns phylogeny of the family Ancylidae, Basch

(1963) compared radulae of several living genera and suggested two major lines derived from a proto-ancylid, planorbid derived ancestor. One line led to Rhodacmea and Ancvlus Mueller, which presently has a Eurasian-North

African distribution. The other led to a hypothetical ancestor that in turn gave rise to three stems; one leading to Ferrissia, one to Hebetancylus Pilsbry and Laevapex

Walker, and the third to Burnupia Walker, which has an

African distribution. Burch (1974) used scanning electron microscopy to compare apical shell sculpturing among

several ancylid genera. He noted great similarity between

Hhodacemea and Ancvlus, and thus suggested an affinity and

confirmed part of Basch's phylogenetic scheme. 7

Ancylid Ecology and Population Dynamics

There have been few long term field studies on ancylid populations. Geldiay (1956) investigated the life cycle, growth, reproduction, and bioenergetics of the European stream limpet Ancylus fluvuatilis Muller in England. He noted a one year life span for this species, with one generation being produced and death occurring soon after reproduction. No differences were reported in growth rate or reproduction schedule of A. fluviatilis transferred and caged in natural aquatic habitats of different ecological character than their native habitat. Russell-Hunter et al.

(1967) studied several populations of the stream limpet

F. rivularis in New York State. Significant interpopulation differences were noted in calcium uptake during growth.

These differences were unrelated to environmental differ­ ences and were suspected to involve genetically determined physiological races. Burky (1971) continued this investiga­

tion of F. ~ ivularis in New York and noted that populations

from eutrophic habitats produced two generations per year.

Life spans were 11 and three months for spring and summer hatched adults respectively. Populations from mesotrophic environments produced only one generation per year with a life span of 13 months. Egg production was greater in

limpets from the eutrophic habitat. Burky attributed 8

this partly to the greater primary productivity in a

eutrophic environment, but suggested that genetic

differences between populations might be. involved.

McMahon (1975) reported similar results for populations

of the pond limpet L. fuscus in New York. Cage transfer

experiments between two populations (one from a mesotrophic

and the other from a eutrophic environment) revealed cir­

cumstantial evidence of physiological races. When limpets

from mesotrophic environments were transferred and caged

in a eutrophic environment they demonstrated greater

efficiency in assimilation and/or in the cellular metabolic processes than caged L. fuscus native to the eutrophic habitat. Reciprocal transfers failed to the extent that

limpets from a eutrophic environment caged in a mesotrophic

environment died within two months after transfer.

Recently, McMahon (1976) measured changes over a two year period in mean aperture length among three north

central Texas populations of H. excentricus and L. fuscus.

He noted a bivoltine pattern of reproduction (two succes­

sive generations per year) with recruitment occurring in

spring and fall for all three H. excentricus populations

and for two L. fuscus populations. One L. fuscus population

produced three generations per year with recruitment occur­

ring in the spring, summer, and fall. 9

Ancylids as Hosts for Digenetic Trematodes

Molluscs exhibit not only a species specific, physiologically determined, susceptibility to certain species as well as strains of larval digenetic trematodes, but this susceptibility is extended to geographic strains within a molluscan species (Abdel-Malek, 1950; Newton,

1953). In addition, some workers (Abdel-Malek, 1958;

James, 1968) have evidence suggested age susceptibility, i.e., some molluscan species can be infected only during a certain period of their life. Therefore, consideration of ancylid life cycles and possible genetically controlled physiological races within a species is a necessary pre­ requisite to studying their roles as first intermediate hosts for digenetic trematodes.

Literature on parasitization of ancylid snails is meager, with less being known than for other major families of freshwater gastropods (Malek and Cheng, 1974).

Smith (1967) reviewed the literature on cercariae develop­ ing in ancylids. The six reports from 1827 to 1953 were incomplete in description with no indication of specific or generic identity. None was from North America.

Smith (1953) first noted trematode infections in

North American ancylids. He described and reported on the life cycle of Megalodiscus ferrissianus. which 10

developed in F. fragilis from southeast Michigan, encysted

on pieces of frog skin, and matured as adults when fed to

laboratory reared Rana clamitans. Smith proposed the name

M. ferrissianus in the abstract of his doctoral disserta­

tion, without issuing a supporting paper, and therefore

created a nomen nudum. Yamaguti (1971, 1975), however,

recognized M. ferrissianus as a valid species, and cited

Smith's dissertation.

Smith (1959), in a report footnoted as being a

revised portion of his dissertation, noted the occurrence

of M. temperatus (Stafford) in F. fragilis from Michigan.

There was no mention of M. ferrissianus nor was there a

report confirming identification of M. temperatus by

life cycle studies. Therefore one may assume that he

considered the original material to be M. temperatus and

since M. ferrissianus was a nomen nudum it could not be

a synonym of M. temperatus. The life cycle of this rectal

amphistome of frogs was elucidated by Krull and Price

(1932), vho implicated Helisoma trivolvis (Say) as a

natural snail host.

Smith further reported an unidentified Haematoloechus

Looss cercaria developing in F. parallels from marsh ponds

in Michigan. No description was given; however, he noted

that cercariae appeared identical to xiphidiocercariae 11 developing in the snail Planorbula armigera (Say) located

in a nearby roadside ditch.

Gadgil and Shah (1956) reported F. tenuis (Bourguignat) as an experimental host for the human blood fluke Schisto­ soma haematobium (Bilharz) in India. These investigators noted high mortality for limpets exposed to £!. haematobium miracidia, with those surviving four weeks post exposure shedding few cercariae. There are no reports of natural schistosome infections in F. tenuis nor has its role as an experimental host been verified. According to Malek and Cheng (1974), this report by Gadgil and Shah has been accepted with reservation by many.

Peters and Self (1963) reported an ophthalmoxiphidio- cercaria of the family Allocreadiidae Nicoll developing

in L. fuscus from southeastern Oklahoma and encysting in the mantle of unionid clams and limpets, including limpets hosting the rediae. These investigators believed the

cercaria to be that of Allocreadium ictaluri Pearse, an

intestinal parasite of catfish. They noted that miracidia, hatched from eggs obtained from infected catfish, penetrated

and remained in the tissues of L. fuscus. Seitner (1951) had published what he believed to be the life history of A.

ictaluri; however, he described an oculate trichocercous 12

cercaria/ without penetration stylet/ as the cercaria of

A- ictaluri. Peters (1961) noted the variance of this

cercarial morphology with that of all known allocreadiid

life cycles, which, incidentally involve a lamellibranch

mollusc as first intermediate host. Peters suggested

that Seitner's cercaria was that of the deropristiid

Skriahinopsolus manteri Cable from sturgeon.

Basch (1963) noted that of 150 ancylid collections

made during the summer of 1961, from 23 states, about

15% were heavily infected with one or more species of

trematode. Smith (1967) collected and examined 10,400

JF. fragilis, 2,000 F. parallela, and 9,500 L. fuscus from

13 marsh pond, stream, and river localities in southeastern

Michigan. Fifteen different trematode species were found

to use one or more of the three limpet species as first

intermediate hosts. Unfortunately Smith did not figure

or otherwise describe these cercariae except to note that

M. temperatus developed in all three limpet species.

Identification of the other 14 cercariae was only to the

level of superfamily or family, with no attempt made to

place the xiphidiocercariae in any taxon.

In addition to M. temperatus. Smith noted a heavily

pigmented amphistome developing in F. parallela; a strigeoid

in F. fragilis? another in F. parallela; an echinostomatid 13

in P. fragilis? two others in F. parallela? a fourth in

L. fuscus? a spirorchiid in P. fragilis, P. parallela, and

L. fuscus? a lissorchiid and cyanthocotylid in L. fuscus?

and three xiphidiocercariae in F. parallela. Significance of the apparent specificity exhibited by most cercariae is tempered by the fact that Smith failed to note the occur­ rence of sympatry among the limpet hosts. He did, however, report on experimental infections of M. temperatus

in F. fragilis. Size of these cercariae was compared with those developing in experimentally infected Helisoma trivol- vis, and Smith noted that those in the ancylid were

approximately 30% smaller at maturity.

Smith (1968) reported that the lissorchiid cercariaeum

(a tailless cercaria), previously reported (Smith, 1967) in

L. fuscus from Michigan, also parasitized P. rivularis in

southeastern Michigan. According to Smith, this cercariaeum

was identical to Cercariaeum mutabile described by Cort

(1918) and reported by Wallace (1941) to be the larva of

Triganodistomum mutabile (Cort), an intestinal parasite of

catostomid fishes. Wallace reported H. trivolvis and H.

campanulatum (Say) as natural snail hosts with the planarian

Dugesia sp. and the snail commensal annelid, Chaetogaster

limnaei serving as second intermediate hosts. Smith

reported to have confirmed Wallace's observations, while 14

using cercaria from naturally infected limpets. He noted

that starved Ducresia sp. ingested cercariae that developed

as unencysted metacercariae in the planarian's parenchyma.

Adult T. mutahile developed in chubsuckers, Erimyzon sucetta

fed infected Dugesia. Although Smith noted that the chub­

suckers were lissorchiid parasite-free prior to feeding

experiments, according to Dr. Dominic L. DeGiusti (1975,

pers. comm.) these fish were obtained from a commercial bait

shop and may not have been lissorchiid-free. Smith did not

report any attempts at experimental infection of limpets or

annelids nor did he figure or redescribe Cercariaeum muta­ bile. He did, however, synonymize Triganodistomum Simer

with Lissorchis Magath and thus created L. mutabile comb. n.

Duncan and DeGuisti (1976) produced evidence that the

lissorchiid cercariaeum, thought by Smith (1968) to be

Cercariaeum mutabile, was in fact a complex of three

cercarial species. These cercariaea differed in size,

arrangement of tegumental papillae, tegumental spination

pattern, and species of intermediate hosts. Since Duncan

and DeGiusti believed them to be larval stages of described

lissorchiids, they did not formally describe them as new

species. They did, however, provide full descriptions

while designating them as Cercariaeum types I through

III. Cercariaeum type I utilized L. fuscus as first 15 intermediate host with Chaetogaster limhaei as second intermediate. Cercariaeum types II and III utilized L. fuscus and P. rivularis respectively, while Chaetogaster,

Dugesia tigrina and D. dorotocephala served as second intermediates. They also noted that Cercariaeum type II could use L. fuscus, its first intermediate, as second intermediate. Metacercariae were found encysted in the limpet's hemocoel, pseuddbranch, and foot musculature.

underwood and Dronen (1977) reported an unidentified species of Texas Ferrissia as an experimental host for the frog lung fluke Haematoloechus breviplexus Stafford. These investigators noted that xiphidiocercariae obtained from .

Ferrissia sp. were about 40% smaller at maturity than H. breviplexus cercariae described by Schell (1965) and reported as developing in the planorbid snail Gyraulus similaris (Baker). This observation could be significant since Smith (1967) reported M. temperatus cercariae developing in ancylids were smaller than those in the planorbid Helisoma trivolvis.

As a further result of my research I have reported

F. fragilis as a natural snail host for the turtle blood fluke Spirorchis scripta Stunkard in Louisiana (Turner and Corkum, 1977).

In summary, only M. temperatus and £1. scripta have been demonstrated by published, undisputed life cycle studies as naturally occurring in ancylid snails. Minimum require­ ments for demonstration are the experimental rearing of limpet infecting cercariae to identifiable adults, vfaile using parasite free or laboratory reared second intermediate and/or definitive hosts.

MATERIALS AND METHODS

Field Collections

Limpets were collected biweekly, for up to 18 consecu­ tive months, from five ecologically dissimilar field locali­ ties in southeastern Louisiana. Collecting sites, with survey period in parentheses, were as follows: drainage ditch on LSU experimental farm, 1 mi S of LSU Baton Rouge campus (June 1975 through November 1976); roadside swamp,

2 mi SE of Sorrento on Rt. 61 (June 1975 through July 1976); pond, 2 mi E of Head of Island on Rt. 22 (June 1975 through

August 1976); Beaver Pond Branch, 3 mi SE of Livingston on

Interstate 12 (July 1975 through November 1976); and borrow pit on west side of Atchafalaya floodway levee at Ramah on Interstate 10 (July 1975 through August 1976).

Collections were made by removing, with a sharp scalpel blade, limpets attached to submerged or floating debris as

16 17 well as leaves and stems of floating or submerged vegetation.

Specimens were placed in glass finger bowls containing water from the collecting site. Bowls rested on an inverted styrofoam ice chest that served as a floating work table.

Collecting time for each of the 156 collections was a multi­ ple of 15 minutes duration. This was done to establish an index of relative abundance by noting number of limpets collected during 15 minutes. To roughly determine popula­ tion structure, all individuals seen, regardless of size, were collected.

Examinations of Limpets and cercariae

Snails were maintained in their collection containers until identified, graded into sizes, and examined for larval digenetic trematodes, which was usually done within 24 hours after collection. Limpets were identified with keys and descriptions provided by Basch (1963).

Identification was confirmed by Dr. Robert F. McMahon

(1976, pers. comm.). Voucher specimens of all limpet

species were deposited in the mollusc collection of the

Delaware Museum of Natural History.

The smaller species of limpet, Ferrissia fragilis

(DMNH No. 119530) was graded into three size classes based upon shell length: <2mm, 2-4 mm, and >4 mm.

Laevapex fuscus (DMNH No. 119532) and Hebetancylus 18 excentricus (DMNH No. 119531) were graded into classes:

<3 mm, 3-5 mm, and >5 mm. I believed that changes, over the course of my survey, in relative numbers of each class should reflect population dynamics, including reproduction, recruitment, and death. Although collections were biweekly, data on limpet populations were pooled for each month.

Specimens were examined under a direct lighted dissect­ ing microscope for presence of larval trematodes. Species, size class of limpet, and cercaria type were recorded.

Early in the study I dissected each limpet with a pair of fine insect pins to determine whether it was parasitized.

Unfortunately, four cercarial types were collected only during this early phase. A specimen of each type was, however, photographed and measured even though not naturally emergent or necessarily mature. Later I was able to screen specimens and isolate in individual Stender dishes containing dechlorinated -^ap water those with rediae or sporocysts. Visual screening was possible since much of the limpet's "soft-parts", including the digestive gland, were exposed to inspection when the snail was inverted. After some experience I could often identify cercarial types by observing their parent germinal sacs in situ; however, identification was determined by dissec­ tion or by allowing cercariae to emerge from live, isolated individuals. Limpets not hosting evident germinal sacs were dissected and examined for immature larval stages and/or metacercariae.

Biweekly data on incidence of infection, like those for population biology, were pooled for each month. Only those individuals of H. excentricus and L. fuscus greater than 3 mm total shell length were considered when comput­ ing monthly incidence. Parasitization with cercariae or germinal sacs was not evident among the smaller individuals however, this was not true for P. fragilis, all sizes of which were considered in computing incidence.

Cercariae, designated as types I-XIX {Figures 1-19), were studied live unstained, vitally stained with nile blue, or fixed in hot 10% formalin. Measurements were taken from preserved or live specimens under light cover- slip pressure and are expressed in microns unless other­ wise noted. Drawings were composites made from live and preserved specimens, either free hand, with aid of a microprojector, or from photomicrographs.

Laboratory Maintenance of Hosts

Among the limpets, only F. fragilis was amenable to long term maintenance in the laboratory. Specimens were placed in finger bowls containing dechlorinated tap water 20

and provided with small sheets of alga encrusted plastic.

Small bits of chalk were added as a calcium source and bowls were placed under a lamp for at least eight hours daily to insure growth of alga on which the limpets grazed.

Ten hatchling turtles Chrysemys scripta, reared in

the laboratory from eggs, were obtained from Dr. R. J.

Siebling, LSU Department of Microbiology. Turtles were maintained five each in five-gallon aquaria and were fed

crickets, lettuce, and bits of freshwater clam and fish.

Other experimental definitive hosts included a pair of golden hamsters obtained from a colony maintained by the

LSU Department of Zoology and Physiology, a pair of

gerbils and a pair of albino guinea pigs from the LSU

Department of Veterinary Science, and one captured white­

footed mouse, Peromvscus leucopus from woods 1 mi W of

Mississippi River bridge on Interstate 10. Paired rodents were maintained together in 42 x 39 x 26 cm wire cages with sawdust floors. The mouse was caged alone but other­ wise under identical conditions. Guinea pigs were fed

guinea pig chow and lettuce? others were fed laboratory

rat chow.

Experimental Infections

Each of the 10 turtles was placed in a finger bowl 21 with dechlorinated tap water and exposed to 10 recently- emerged apharyngeate, brevifurcate cercariae (Cercaria type VII) . Cercariae were pipetted from a Stender dish containing an F. fragilis with a naturally acquired infec­ tion. Turtles were necropsied at intervals from 90 to 180 days post exposure. Each organ of the host was isolated and dissected in a solution containing 0.5% sodium chloride and 0.2% sodium citrate. Dissected organs were minced with fine scissors, sealed and shaken for three minutes in a small jar containing the above solution, and allowed to settle for 10 minutes. The supernatant was decanted in small aliquots and each examined for adult trematodes.

Worms recovered by this method or the abovementioned dissection procedure were relaxed in distilled water before fixation in hot AFA. They were not, however, flattened under coversiip pressure because they tended to adhere firmly to any glass surface. Permanent mounts were prepared by staining worms in Semichon's carmine, clearing in methyl salicylate, and mounting in Permount.

Heavily pigmented amphistome cercariae (Cercaria type XVII) were allowed to encyst on pieces of lettuce or short blades of grass placed in finger bowls with naturally infected F. fragilis. Potential definitive hosts were fed green vegetation with encysted metacercariae.

Guinea pigs were each given 270 metacercariae in small

numbers, almost daily, over a two month period. Hamsters,

gerbils, and the mouse were each given 30 metacercariae.

All animals were necropsied and examined for trematodes

within 30 days after being last fed metacercariae.

RESULTS AND OBSERVATIONS

Ecology of Southeastern Louisiana Ancylids

After 18 months of collecting and examining almost

20,000 ancylid specimens, three species, each representing a

different genus, were found to occur at my study areas.

Laevapex fuscus was collected from submerged stems of

emergent vegetation and from submerged debris at three

localities exhibiting a lentic character. Ferrissia

fragilis and Hebetancylus excentricus occurred on emergent

and floating vegetation at all five collecting sites, which along with the seasonality and population dynamics of their ancylid snail faunas, are characterized below.

1. Ben Hur Farm

This 3 m wide, mud-bottom ditch, although never dry,

had an intermittent flow and drained the LSU experimental

22 23 farm and 20 shallow ponds for experimental rearing of

catfish and crayfish. During the 18-month survey at this locality, 3,774 H. excentricus and 172 F. fragilis were collected exclusively off submerged leaves and stems of alligator weed Alternathera sp.. L. fuscus was not seen or collected.

Population dynamics and seasonal abundance of both

F. fragilis and H. excentricus are presented in Figure 20.

JE* fragilis was collected intermittently and in small numbers during the course of the survey at Ben Hur Farm.

Usually less than two individuals were collected per

15 minutes collecting effort. A peak in numbers occurred in April, when about 10 limpets were collected per 15 minutes. This peak was followed by a gradual decline to zero in August. Even though collected intermittently,

JE* fragilis may have been present year round. Recruitment occurred in mid spring as evidenced by the observation that individuals of the small size class (<2 mm length) comprised an increasingly greater percentage of the population during this period. Individuals of the large size class (>4 mm length), which probably represented the post-reproductive segment of the population, were collected only at this time. The fact that Basch (1963) noted a 24 maximum length of 4 mm for F. fragilis may substantiate a post-reproductive role for those large size class individuals. In the case of L. fuscus and H. excentricus, noted by Basch to have maximum lengths of 7.75 and 5.8 mm respectively, individuals >5 mm length would not neces­ sarily be in the post-reproductive segment.

H. excentricus was present throughout the study and exhibited two distinct population peaks: one in November, and another in May. OSiis species displayed a bivoltine pattern of reproduction with two successive generations per year as evidenced by the observation that peaks in the index of relative abundance coincide with or closely follow periods of increase in percentage of small size class individuals (<3 mm length). H. excentricus repro­ duction and recruitment are preceded by a build up in percentage of the large size class sector of the popula­ tion.

Another observation, concerning the H. excentricus population, involved the seasonal occurrence of septum formation by some members of the fall generations. In

October 1975 septate individuals (DMNH No. 108368), anatomically identical in "soft-parts" to nonseptate forms, appeared in the population. By December and January they comprised 23% of the sampled population (Figure 21). 25

In February there occurred a transition from septate to post-septate phase (Figures 22 and 23). This phase per­ sisted until July and was replaced by nonseptate forms.

During November 1976# the last month of the study# septate forms reappeared with 5% of the population involved.

Dimorphism, vfoen present in a population, formed a conven­ ient "tag" for tracing the life span of a generation. This phenomenon was not observed among the F. fragilis population.

Little evidence suggested seasonal partitioning of the habitat by either species; however, an April peak in index of relative abundance of F. fragilis that corres­ ponded with an April low for H. excentricus may be significant.

2. Beaver Pond Branch

This narrow stream, with a continuous flow originates near Livingston, Louisiana, and empties into Hog Branch, a larger, sand-bottom stream forming part of the drainage for the so-called Florida parishes of southeastern

Louisiana. During periods of high water in Hog Branch, which occurred twice during my survey, Beaver Pond Branch received backwater from Hog Branch. This condition per­ sisted for several days before normal flow returned in both streams.

H. excentricus and F. fragilis were collected from 26 floating vegetation and from emergent Sagittaria sp.. As at the previous study area L. fuscus was not encountered.

Figure 24 shows population biology and seasonal abundance of 1,294 H. excentricus and 1,853 F. fragilis collected during 17 months. There is evident seasonality and perhaps a case for seasonal partitioning of the habitat by the two limpet species. From January to July

1976, F. fragilis was present in large numbers at a time when H. excentricus was all but absent from the habitat. H. excentricus became the predominant limpet species during the fall.

Septum formation by H. excentricus was not observed during the fall of 1975; however, 16% of the October and

6% of the November 1976 sampled population were septate.

As at Ben Hur Farm there was no evidence of septum forma­ tion by F. fragilis. On the basis of changes in population structure and abundance, I believe that each species pro­ duces a single generation each year.

3. Head of Island Pond

This permanent pond has a shallow margin at its north end lined with emergent vegetation. The remaining margin was deep and without emergent vegetation. Much sunken debris; sheets of plastic, metal cans, glass, etc., was found along the front or south margin. L. fuscus occurred 27 on this debris, however, because of depth, collecting was difficult. For this reason, L. fuscus was not included among the ancylids studied at this locality. I mention the occurrence because it demonstrates habitat selection by the three ancylid species, since L. fuscus was found only on this deep water debris, while H. excentricus and

F. fragilis occurred only on debris and emergent vegetation along the shallow margin.

Population biology and seasonal abundance for 1,836

H. excentricus and 182 F. fragilis collected during my 15 month survey are shown in Figure 25. F. fragilis was abundant only in February and March. Presence of large size class individuals, accompanied by an increasing percentage of the small class sector, indicates recruit­ ment at this time.

H. excentricus occurred year round with production of three generations; one in the summer, another in the fall, and the third in the spring. Septum formation by either species was not observed.

4. Ramah

'Hiis site is a borrow pit of the Atchafalaya River

Basin subjected to large fluctuations in water level.

Because of fluctuations, emergent vegetation that consisted mainly of Sagittaria sp. was seasonal, and 28

occurred mostly in the summer and fall. Although no mea­

surement of dissolved oxygen was taken during the study, this habitat would probably be classified as mesotrophic

if the criteria of McMahon (1975) were used.

All three limpet species were sympatric at Ramah.

L. fuscus was collected from submerged and floating debris, water hyacinth, and emergent Sagittaria sp. F. fragilis

and H. excentricus were similarly collected; however,

H. excentricus was seldom found on debris. Limpet popula­ tion biology and seasonal abundance for 3,663 L. fuscus,

557 F. fragilis. and 425 H. excentricus collected during my 14-month survey are presented in Figure 26.

As at Beaver Branch, H. excentricus and F. fragilis displayed a pronounced seasonality interpreted as seasonal partitioning of the habitat. However, seasonality of limpets may also reflect seasonal absence of vegetation on which H. excentricus was most often collected. F. fragilis, like the Beaver Branch population, was abundant in early spring through summer, while H. excentricus was most abundant during the fall. Data indicate production of a single H. excentricus generation per year.

Fifty percent of the February F. fragilis collection was in the post-septate phase, tfhis phase disappeared from 29

the population in March; however, individuals in the sep­

tate phase appeared in May and persisted through the end

of the survey in August. Therefore, indications are that

a single generation is produced annually and that some

individuals overwinter in the septate phase and become part of the reproductive base for the spring generation.

Septum formation was not observed among the other ancylid species at Ramah, and its occurrence in p. fragilis was nearly out of seasonal phase with that noted for H. excentricus (Figure 21).

L. fuscus was the predominant limpet species at Ramah and was collected in relative high numbers almost year round. The low fall-winter index of relative abundance may have been due to L. fuscus burrowing into the mud, where they were unavailable for collection by my methods.

Indications are that a single generation is produced annually. Recruitment certainly began in April because population structure for that month demonstrates an expanding population.

5. Sorrento

This roadside swamp, with a shallow depth and mud- bottom, was the last of my study sites. Water level was main­ tained at about .5 m during the first 12 months of the survey; however, in June 1976 the level began to drop and the site was 30

completely dry by August 1976. The 100 m long by 30 m wide

area, which had been cleared several years earlier as right

of way for an underground pipeline, was free of trees. As

a result, a luxurant growth of emergent grass, Paspalunt sp. was maintained almost year round and gave the locality a marsh appearance. This swamp, with its shallow depth,

abundant emergent vegetation, and high primary productivity, probably fits the criteria of a eutrophic environment

(McMahon, 1975).

All three ancylid species occurred at this locality; however, as seen in Figure 27 the scale for relative abun­ dance of L. fuscus is 10 fold greater than for H. excen­

tricus and 100 fold greater than for fragilis. Total

numbers collected were 4,960, 352, and 40, respectively.

F. fragilis was collected in too small numbers for any

determination of population dynamics; however, a pronounced

seasonality was noted. H. excentricus appears to have a

single generation each year with recruitment in the spring.

Septum formation was not observed in either species.

L. fuscus produced a fall and a spring generation.

Egg hatching and recruitment from one biannual cycle ex­

tended into the next, and thus gave the appearance of year

round reproduction. Another observation concerning the

L. fuscus population was the predominance of large size 31 class individuals in most pooled monthly samples. Predomi­ nance of large individuals indicates a rapid growth rate, probably attributable to the eutrophic environment, and is striking when compared to the pooled monthly population structures at the less eutrophic Ramah (Figure 26). As will be shown later, apparent differences in productivity have considerable implications for the ecology of the respective ancylid-hosted digenetic trematode populations.

Digenetic Trematodes in Southeastern Louisiana Ancylids

After 18 months of collecting and examining almost

20,000 ancylid specimens, cercariae representing 19 trematode species were found developing in one or more of three ancylid species. Hosts, descriptions, season­ ality of incidence, and possible identity of these larvae are given below.

Cercaria Type I (Figure I)

L. fuscus collected from Sorrento, F. fragilis from

Beaver Pond Branch, and both species from Ramah were found to harbor infections with xiphidiocercariae of the armatae group and designated Cercaria type I. Measurements in the following description were taken from 20 specimens killed and preserved in hot 10% formalin.

Description: Body 228-276(254) long by 84-112(99) 32 wide and densely covered with small spines that become less dense at the posterior end. Caudal pocket present. Tail

184-228(205) long by 29-35(32) wide at base. Oral sucker

53-63(58) long by 56-64(61) wide. Acetabulum 45-51(47) long by 44-53(50) wide. Stylet shouldered, 28-33(31) long.

Five pairs of pre-acetabular penetration glands with ducts that empty near stylet. Ceca extend to post-acetabular level. Excretory bladder cellular and Y-shaped. Flame cell formula or number not determined.

Incidence and seasonality of infection with Cercaria type I at Beaver Pond Branch are presented in Figure 24.

F. fragilis harboring these cercariae were collected only during July of the second summer and comprised 1% of the sampled population. Infection occurred in 0.8% of the sampled F. fragilis population during the same month at

Ramah (Figure 26) . L. fuscus from this locality, however, harbored infection throughout spring and summer. At

Sorrento (Figure 27) Cercaria type I was present in L. fuscus almost year round with a peak seasonal incidence of 8.5% in August.

Cercaria Type II (Figure 2)

Amphistome cercariae of the diplocotylea type, designated Cercaria type II, were found developing in both L. fuscus and F. fragilis collected at Sorrento. 33

P. fragilis from Ben Hur Farm# Head of Island Pond, and

Beaver Pond Branch also harbored infections. Measurements were based upon 20 specimens killed and preserved in hot

10% formalin.

Description: Body 230-292(260) long by 102-144(123) wide. Tail 415-450(432) long by 35-46(40) wide. Oral sucker 118-147(128) long. Acetabulum 40-77(57) long by

113-149(131) wide. Ceca thick walled, extend posteriorly to near level of excretory bladder. Paired excretory trunks contained many small concretions. Flame cell formula or number not determined.

Cercaria type II, although smaller, fits the descrip­ tion given by Krull and Price (1932) for the cercaria of

Megalodiscus temperatus, and by Smith (1967) for larvae of that species developing in Michigan L. fuscus and F. fragi­ lis . Smith reported an overall incidence of 14% for F. fragilis. whereas an incidence of only 1% was noted for infections in L. fuscus. Cercarial production in F. fragi­ lis was in two distinct waves, one in spring and the other in autumn (Smith, 1967).

Data for seasonality and incidence of infection at four localities are presented in Figures 20, 24, 25, and 27.

Like Smith, I noted a disparity in incidence of infection among the two limpet species. Of almost 5,000 L. fuscus 34 examined from Sorrento, only one harbored infection with

M. temperatus, while eight of 40 P. fragilis were infected.

Two waves of cercarial production were observed. However, one began in late fall and continued until early spring, while the other began in early summer.

Cercaria Type III (Figure 3)

Longifurcocercous, apharyngeate, monostome cercariae, with small eyespots, were found developing in all three limpet species and were collected at all localities except

Beaver Pond Branch. Measurements of Cercaria type III were based upon 20 specimens killed and preserved in hot 10% formalin.

Description: Body 179-207(194) long by 31-39(34) wide, with 12 annulations between oral sucker and acetabular anlagen. QVo pairs of lateral setulae on posterior body near junction of tail stem. Tail stem 202-246(232) long by 26-37(31) wide, with five pairs of lateral setulae grouped near junction with body, and six or seven pairs grouped near bifurcation. Caudal bodies not observed in tail stem. Furcae 161-207(196) long by 16-23(17) wide, with delicate finfolds originating at level of excretory pores, which emptied on anterior surface of furcae. Oral

sucker 37-55(46) long by 17-28(21) wide. Three pairs of penetration glands between eyespots and excretory bladder. 35 with acetabular anlagen located immediately posterior to anterior pair. Genital primordium between posterior penetration glands and excretory bladder. Extent of ceca not determined. Eleven pairs of flame cells located in body and two pairs in tail.

Cercaria type III resembles the larva of Posthodiplo- stomum minimum (MacCallum), a parasite of the great blue heron Nycticorax nycticorax. Itoo morphologically different cercariae have been described for P. minimum. Miller (1954) described Cercaria minimum, which bears similarity to

Cercaria type III, however. Miller noted the presence of five pairs of caudal bodies in the tail stem, "setae” arranged in three groups on the tail stem, and 10 pairs of flame cells in the body and tail. Cercaria minimum developed in naturally infected Physa heterostropha Say in Michigan. More recently, Bedinger and Meade (1967) reported on the life cycle of Posthodiplostomum minimum? the cercaria of which developed in naturally infected

Physa halei Lea in Texas. Those cercariae lack caudal bodies, have "flagellets" in two groups on the tail stem, and have 13 pairs of flame cells in the body and tail.

On morphological grounds Cercaria type III, although somewhat larger, more nearly resembles the cercaria des­ cribed by Bedinger and Meade, however, in size, it resembles 36

Cercaria minimum. Data on seasonality and incidence of

infection are presented in Figures 20, 25, 26, and 27.

Cercaria I^pe IV (Figure 4)

Longifurcocercous, pharyngeate, distome cercariae were

found developing in all three species of limpets and were

collected at all five localities. Measurements of Cercaria

type IV were based upon 20 specimens killed and preserved

in hot 10% formalin.

Description: Body 119-178(151) long by 41-62(51)

wide, with anteriorly directed needle-like spines extend­

ing posteriorly to level of pharynx, and with three pairs

of lateral papillate setulae. Tail stem 228-384(316) long by 72-98(77) wide, with four pairs of lateral setulae.

Furcae 180-292(239) long by 32-48(39) wide, with excretory

pores opening at mid-length of posterior surface. Oral

sucker 35-44(39) long by 25-32(28) wide. Pharynx 9-12(10)

long by 22-28(26) wide, with a single circle of inwardly

directed, needle-like spines. Number and arrangement of

penetration glands not determined. Ceca extend to post-

acetabular level. Six pairs of flame cells in body and

two pairs in tail.

Seasonality and incidence of infection for Cercaria

type IV are presented in Figures 20, 24, 25, 26, and 27. 37

Cercaria Type V (Figure 5)

An echinostome cercaria, with spiny collar, was found developing only in H. excentricus from Ben Hur Farm.

Measurements of Cercaria type V used in the following description were taken from a single live specimen.

Description: Body 176 long by 148 wide, with an unde­ termined number of small collar spines. Tail without fin- fold, 392 long. Oral sucker 44 long by 44 wide. Acetabulum

50 long by 50 wide. Extent of ceca not determined. Many small concretions restricted to middle and anterior portion of paired excretory trunks. Flame cell formula or number not determined.

Cercaria type V was collected only during June of the first summer and comprised 4.1% of the sampled H. excentri­ cus population (Figure 20).

Cercaria Type VI (Figure 6)

Echinostome cercariae, without spiny collars, were found developing in all three limpet species at all locali­ ties except Head of Island Pond. Measurements of Cercaria type VI were based upon 20 specimens killed and preserved in hot 10% formalin.

Description: Body 168-196(184) long by 86-116(102) wide. Tail without finfold, 364-416(393) long by 43-53

(46) wide, with pair of short flagellets near tip. Oral 38 sucker 35-43(39) long by 38-43(40) wide. Acetabulum 37-50

(43) long by 51-58(54) wide. Extent of ceca not determined.

Paired excretory trunks each contain three or four large concentric concretions restricted to pre-acetabular region.

Thirteen pairs of flame cells present in body.

Cercaria type IV may be a species of Echinochasmus

Dietz, since cercariae of this genus often lack collar spines, have few and large excretory concentrations, and have short flagellets on the tail (Yamaguti, 1975). Season­ ality and incidence of infection are presented in Figures

20, 24, 26, and 27.

Cercaria Type VII (Figure 7)

A brevifurcocercous, apharyngeate, distome cercaria of the turtle blood fluke family Spirorchiidae Stunkard was found developing only in F. fragilis from Ben Hur Farm,

Beaver Pond Branch, and Ramah. Measurements used in the following description of Cercaria type VII were based upon

20 specimens killed and preserved in hot 10% formalin.

Description: Body 192-256(219) long by 58-72(64) wide at acetabulum, with three pairs of lateral setulae. Anterior third of oral sucker covered with dense, fine spines. Spines around acetabulum large and numerous. Remainder of body covered with minute, sparse spines. Tail stem attached subterminally, 568-680(590) long by 52-67(60) wide. Short 39 lateral setulae on tail stem arranged in two groups of nine pairs each. Anterior group all nonpapillate. Post­ erior group with last three pairs papillate. Furcae 200-

268(227) long, with finfolds along margin. Oral sucker

44-69(60) long by 28-37(34) wide. Acetabulum protrusible,

24-30(28) long by 26-32(28) wide. Eyespots in second quarter of body. Five pairs of penetration glands from posterior margin of eyespots to fourth quarter of body.

Sixth pair of fused glands in fourth quarter. Ceca extend to level of acetabulum. Five pairs of flame cells in body and one pair of large flame cells in tail. Under laboratory conditions cercariae emerged mostly at night.

Goodchild and Kirk (1960) described the larval stages of Spirorchis eleqans Stunkard from experimentally infected

Helisoma anceps (Menke) as well as naturally infected planorbid snails, Menetus dilatatus (Gould) in Georgia.

Holliman and Fisher (1968) described the larval stages of J3. scripta, emended the species description, and reported the planorbid H. anceps as a natural host in Virginia.

Goodchild and Martin (1969) synonomized _S. eleqans and

S. picta Stunkard with ^S. scripta, which had priority.

As noted earlier, Smith (1967) reported unidentified spirorchiid trematode infections in Michigan F. fragilis,

parallels, and L. fuscus. 40

Cercaria type VII resembles the cercaria of ,S. scripta*

as described by Holliman and Pisher (1968), however, it

differs in number and arrangement of setulae, as well as

size of tail stem and furcae, which are larger in Cercaria

type VII.

Twelve adult spirorchiid trematodes, which fit the

emended description of .S. scripta given by Holliman and

Fisher (1968), were recovered from hearts, arteries, and

veins of six experimentally infected turtles. No worms were recovered from two turtles necropsied at 180 days post exposure, however, spirorchiid eggs were abundant

throughout their tissues.

Limpets harboring spirorchiids were collected only

during the months of April through July, with a peak inci­

dence occurring in the last month (Figures 20, 24, and 26).

Cercaria Type VIII (Figure 8)

A xiphidiocercaria of the armatae group parasitized

only F. fragilis from Ramah. Measurements from the follow­

ing description of Cercaria type VIII were taken from a

single living specimen.

Description: Body 252 long by 140 wide. Tail 203

long by 42 wide. Oral sucker 69 long by 64 wide. Stylet

unshouldered, 25 long. Acetabulum 53 long by 64 wide.

Extent of ceca not determined. Excretory bladder Y-shaped. 41

Arrangement and number of flame cells or penetration glands not determined.

Cercaria type VIII was collected only in July of the first summer of the survey (Figure 26) .

Cercaria Type IX (Figure 9)

An ophthalmoxiphidiocercaria of the family Allocreadi- idae was found developing only in L. fuscus collected at

* Ramah. Measurements for the following description of

Cercaria type IX were taken from a single living specimen.

Description: Body 328 long by 228 wide at acetabulum.

Tail 270 long by 43 wide. Oral sucker, with five rows of small, blunt spines forming a semicircle below mouth, 56 long by 69 wide. Acetabulum, with two alternating circles of small, blunt spines, 64 in diameter. Stylet short and blunt. Eyespots in first quarter of body. Extent of ceca not determined. Number and arrangement of flame cells or penetration glands not determined.

According to Dr. Lewis E. Peters (1975, pers. comm.),

Cercaria type IX appears "very similar to the cercaria that [he and Dr. J. Teague Self] studied in Oklahoma in the early 1960's". Peters also noted that he and Dr.

Raymond Cable had confirmed identity of the cercaria, which also occurred in Indiana L. fuscus. to be that of

Allocreadium ictaluri. Although Peters and Self (1963) 42 reported L. fuscus as one of several second intermediate hosts, I was unable to find any harboring allocreadiid raetacercariae among the 3,663 L. fuscus examined from Ram ah.

Seasonality and incidence of infection for Cercaria type IX are presented in Figure 26.

Cercaria TyPe x (Figure 10)

A small xiphidiocercaria of the armatae group, desig­ nated Cercaria type X, was found developing only in L. fuscus at Sorrento. Measurements in the following descrip­ tion were based upon 10 specimens killed and preserved in hot 10% formalin.

Description: Body 152-182(169) long by 74-90(86) wide.

Caudal pocket present. Tail 106-140(123) long by 30-37(35) wide.. Acetabulum 24-28(26) long by 23-28(25) wide. Stylet slightly shouldered, 23-27 (26) long. Extent of ceca not determined. Excretory bladder Y-shaped. Flame cell formula or number not determined. Penetration gland number and arrangement not determined. Pharynx, although present, was not observed.

Cercaria type X was collected only during July and

August of the first summer and comprised 0.8 and 0.6% of the sampled population, respectively (Figure 27).

Cercaria Type XI (Figure 11)

Tailless cercariae (cercariaea) of the family 43

Lissorchiidae Poche were found developing in L. fuscus and

P. fragilis collected at Ramah. Measurements given in the

followjjig description of Cercaria type XI were obtained

from 20 specimens killed and preserved in hot 10% formalin.

Description: Body 324-392(358) long by 80-128(101)

wide, with nine pairs of lateral papillate satulae.

Pharynx 24-28(26) long by 26-31(29) wide. Oral sucker

50-64(54) long by 51-61(57) wide, with mouth surrounded

on three sides by two alternating rows of small, inwardly

directed spines. Acetabulum 58-69(63) long by 58-71(64)

wide, with two alternating circles of small, inwardly

directed spines surrounding inner rim, and a third row

present on anterior quadrant of inner rim. Tegument with

larger spines directed posteriorly, however, spines absent

from area between oral sucker and acetabulum. Ceca extend

to near base of excretory bladder. Excretory bladder

cylindrical and thick walled. Flame cell and penetration

gland number and arrangement not determined.

Cercaria type XI resembles Cercariaeum type I described by Duncan and DeGiusti (1976), however, it differs in host

specificity (not restricted to L. fuscus) t in size (slight­

ly larger than Cercariaeum type I); in arrangement of

lateral papillate setulae; and in number and arrangement

of small spines on the oral sucker and acetabulum. 44

Duncan and DeGiusti (1976) noted that papillae pattern

and number were variable, however, tegumental spination pattern was fixed. Differences in size may be attributable

to techniques used by these authors, since they first relaxed emergent cercariae in menthol solution prior to fixing in hot 10% formalin. They also measured cercariae in groups of twenty under a "floating" coverslip.

Data on seasonal incidence of infection are presented

in Figure 26.

Cercaria Type XII (Figure 12)

A longifurcocercous, pharyngeate, distome cercaria was found developing only in H. excentricus from Beaver

Pond Branch. Measurements of Cercaria type XII used in the following description were obtained from 20 specimens killed and preserved in hot 10% formalin.

Description: Body 108-156(131) long by 62-99(83) wide. Tail stem 108-200(149) long by 83-150(108) wide.

Furcae 104-163(124) long. Oral sucker 35-48(41) long by

29-39(34) wide. Acetabulum 23-29(25) long by 23-30(26) wide. Ceca surround acetabulum and extend to post-

acetabular position. Tail, as seen in lateral view,

appears as a pair of empty, pressed trousers with excretory pores opening on inner surface of furcae. Number and

arrangement of flame cells and penetration glands not 45 determined.

Data on seasonality and incidence of infection of H. excentricus with Cercaria type XII are presented in Figure

24.

Cercaria iype XIII (Figure 13)

A longifurcocercous, pharyngeate, distome cercaria parasitized only F. fragilis from Head of Island Pond and

Ben Hur Farm. Measurements used in the following descrip­ tion of Cercaria type XIII were taken from 20 specimens killed and preserved in hot 10% formalin.

Description; Body 164-220(193) long by 41-58(46) wide. Tail stem 288-316(297) long by 172-196(186) wide at bifurcation. Furcae 220-268(248) long by 40-60(48) wide. Oral sucker 44-58(51) long by 25-39(38) wide.

Pharynx 12-14(13) long by 14-18(17) wide. Acetabulum with three circles of blunt concentrically placed spines,

25-32 (30) long by 30-35(32) wide. Three pairs of penetra­ tion glands, two pre- and one post-acetabular. Several smaller pairs of cells scattered throughout body. Genital primordium between posterior penetration glands and excre­ tory bladder. Extent of ceca not determined. Anterior body to level of pharynx covered with small dense spines.

Flame cell formula or number not determined. Tegument on tail stem at bifurcation formed into loose, bladder-like 46

"skirt" continuous with furcae. "Skirt" most evident vfcen cercariae were placed under coverslip pressure. Figure 13 was drawn without coverslip pressure and shows "skirt" in folded configuration.

Figures 20 and 25 show seasonality and incidence of infection of F. fragilis with Cercaria type XIII.

Cercaria lype XIV (Figure 14)

A longifurcocercous, pharyngeate, distome cercaria was found developing only in F. fragilis from Ben Hur Farm.

Measurements used in the following description of Cercaria type XIV were taken from 10 specimens killed and preserved in hot 10% formalin.

Description: Body 112-153(127) long by 32-51(44) wide, with small dense spines to level of mid-oral sucker.

Tail stem 187-220(207) long, with nine pairs of lateral setulae. Furcae 162-189(179) long by 14-18(16) wide.

Oral sucker 32-41(37) long by 26-34(30) wide. Acetabulum

18-21(20) long by 19-25(23) wide, with two alternating circles of small, blunt spines. Two pairs of penetration glands, one pre-acetabular the other post-acetabular.

Genital primordium between posterior pair and excretory bladder. Extent of ceca not determined. Five pairs of flame cells in body and two pairs in tail.

Data on seasonality and incidence for Cercaria type 47

XIV are presented in Figure 20.

Cercaria Type XV (Figure 15)

A single F. fragilis collected at Head of Island Pond was found to harbor infection with a longifurcocercous, pharyngeate, distome cercaria. Measurements used in the following description of Cercaria type XV were obtained from 20 specimens killed and preserved in hot 10% formalin.

Description: Body 132-188(161) long by 34-52(41) wide, with small dense spines to level of mid-oral sucker, less densely spined to level of gut bifurcation. Tail stem

280-336(305) long by 124-152(140) wide. Furcae 220-276

(252) long by 28-46(35) wide. Oral sucker 35-52(45) long by 20-30(25) wide. Acetabulum 25-30(27) long by 28-32(30) wide, with three alternating circles of short, blunt spines.

Ceca extend to mid-acetabulum. Two pairs of penetration glands, one pre- and the other post-acetabular. Muscle fibers from median portion of each fiber tract in tail stem contralateral in furca and form a chiasma anterior to bifur­ cation. Lateral fibers ipsilateral. Two pairs of flame cells in tail. Flame cell number or arrangement for body not determined.

According to Dr. Fred W. Beckerdite (1976, pers. comm.),

Cercaria type XV resembles the cercaria of Pharyngostomoides adenocephala Beckerdite et _al., a parasite of the raccoon 48

Procvon lotor. Beckerdite et al. {1971) reported the cercaria of this species to develop in experimentally infected planorbid snails Menetus dilatatus in North

Carolina.

Seasonality and incidence of infection of J?. fragilis with Cercaria type XV are presented in Figure 24.

Cercaria Type XVI {Figure 16)

A single j?. fragilis collected at Ben Hur Farm was found to harbor infection with a small xiphidiocercaria of the ornatae group and designated Cercaria type XVI.

Measurements used in the following description were taken from 10 specimens killed and preserved in hot 10% formalin.

Description; Body 108-150(130) long by 58-72(64) wide.

Tail with finfold, 90-122.(108) long by 18-23 (20) wide. Oral sucker 32-35(33) long by 30-35(32) wide. Acetabulum 18-23

(21) long by 21-23(22) wide. Stylet shouldered 16-21(19) long. Five pairs of penetration glands and ceca extend to mid-acetabular level. Excretory bladder cellular and Y- shaped. Flame cell formula or number not determined.

Cercaria type XVI may be the larva of the frog lung fluke Heamaetoloechus breviplexus. In size of body and tail it appears intermediate between that noted by Schell

(1965) for H. breviplexus larvae developing in experiment­ ally infected Gyraulus similaris in Idaho, and that reported 49 by Underwood and Dronen (1977) for those in an unknown

species of experimentally infected Texas Ferrissia. All

other measurements/ however, agree with those of Schell.

Seasonality and incidence of infection are presented in

Figure 20.

Cercaria Type XVII (Figure 17)

Heavily pigmented amphistome cercariae of the pigment-

ata group, designated Cercaria type XVII, were found devel­ oping in F. fragilis from Beaver Pond Branch, and L. fuscus from Ramah. Measurements used in the following description were taken from 20 specimens killed and preserved in hot

10% formalin.

Description: Body 256-352(281) long by 160-273(233) wide, with 12 pairs of lateral setulae arranged along anterior half. Tail 506-800(702) long by 48-68(57) wide.

Oral sucker 51-72(61) long by 48-69(54) wide. Acetabulum subterminal, 58-83(73) long by 62-101(85) wide. Eyespots large and oval, located in anterior quarter of body. Extent of ceca not determined. Paired excretory trunks filled with concretions and extending anteriorly with several coils until reaching level of oral sucker before turning posteriorly. Flame cell formula or number not determined.

Cercariae maintained under laboratory conditions emerged only in morning, within five mins after exposure to light, 50

and quickly encysted on green vegetation.

Cercaria type XVII most nearly resembles the cercaria

of Stichorchis subtriquetrus (Rudolphi), a cecal parasite

of beaver Castor canadensis. Bennett and Humes (1939) reported on the pre-cercarial development of this species

in experimentally infected lymnaeid snails Lymnaea parva

Lea in Louisiana. Bennett and Allison (1958) later obtained cercariae from experimentally infected L. parva, however, these authors suggested that this snail was not a satisfact­ ory host because of high mortality among infected indivi­ duals.

Except for a slightly shorter tail, Cercaria type XVII fits the description for _S. subtriquetrus given by Orloff

(1941) for cercariae obtained from naturally infected

Planorbis vortex (Linnaeus), Lymnaea ovata (Draparnaud), the operculate hydrobiid Bithynia tentaculata (Linnaeus),

and the terrestrial snail Succinea putris (Linnaeus) in

Russia.

Results of feeding metacercariae to various experiment­

al definitive hosts were negative. Seasonality and inci­ dence of infection are presented in Figure 24.

Cercaria Type XVIII (Figure 18)

A single F. fragilis from Head of Island Pond was

found to harbor infection with a longifurcocercous, 51

pharyngeate, distome cercaria. Measurements used in the

following description of Cercaria type XVIII were taken

from 20 specimens killed and preserved in hot 10% formalin.

Description: Body 150-184(166) long by 48-62(56) wide, with two pairs of lateral setulae, one pair near

mouth and another papillate pair at level of excretory bladder. Anterior body to level of mid-oral sucker covered with small dense spines. Tail stem 240-316(297) long by

128-172(160) wide, with two groups of lateral setulae,

two pairs near junction with body and four pairs near bifurcation. Furcae 208-268(243) long, with excretory pores opening on anterior surface of mid-length. Oral

sucker 40-44(42) long by 28-35(30) long by 30-35(33) wide, with several alternating circles of small, blunt, concen­ trically placed spines. Extent of ceca not determined.

Number and arrangement of penetration glands not determined, however, one pair pre-acetabular. Genital primordium be­

tween acetabulum and excretory bladder. Nine pairs of

flame cells in body and three pairs in tail. Tegument on tail stem at bifurcation formed into loose, bladder-like

''skirt” continuous with furcae.

Presence of three pairs of flame cells in the tail

stem seems to be a deviation from a maximum of two pairs noted for other cercariae of this type (Yamaguti, 1975). 52

Since only nine pairs were observed in the body, perhaps one pair in the tail may have originally been derived from the body complement. Seasonality and incidence of infection are presented in Figure 25.

Cercaria Type XIX (Figure 19)

A single F. fragilis from Head of Island Pond was found to harbor infection with, a longifurcocercous, pharyn­ geate, distome cercaria. Measurements of Cercaria type XIX used in the following description were taken from 10 speci­ mens killed and preserved in hot 10% formalin.

Description: Body 148-204(170) long by 56-96(76) wide.

Tail stem 248-284(256) long by 80-101(90) wide, with 10 pairs of lateral setulae. Furcae 208-220(213) long by

22-32(27) wide, with excretory pores opening on posterior surface. Oral sucker 39-51(45) long by 30-39(35) wide.

Pharynx 12-15(14) long by 14-17(16) wide. Acetabulum

48-57(52) long by 46-62(51) wide, with six circles of small, blunt spines around inner rim. Extent of ceca not determined. Two pairs of penetration glands, one pre- and the other post-acetabular. Ten pairs of flame cells in body and two pairs in tail.

Seasonality and incidence of infection are presented in Figure 25. DISCUSSION

Ecology of Southeastern Louisiana Ancylids

Although F. fragilis accounted for only 15% of the total ancylids collected and examined, it occurred at all sampled habitats, and thus exhibited the least ecological specificity. In contrast, L. fuscus, which comprised 45% of the ancylids studied, was restricted to lentic habitats, and thus displayed greater ecological specialization. H. excentricus was intermediate in ecological specificity as indicated by the fact that, although occurring at all habitats, it was not as successful, in terms of abundance, as F. fragilis at lotic Beaver Pond Branch or L. fuscus at lentic Sorrento. McMahon (1976) stated this relationship when he noted, "representative species of these three limpet genera form the progressively less euryoecic ser ies: Ferrissia-Hebetancylus-Laevapex. "

Bivoltine and trivoltine reproductive patterns with overlapping generations, as exhibited by L. fuscus and

H. excentricus, partially account for their predomin­ ance over F. fragilis at most habitats. Although

McMahon (1976) noted a trivoltine pattern for a Texas

L. fuscus population, I found no more than a bivoltine

for southeastern Louisiana populations. Even at eutrophic

53 54

Sorrento the reproduction-recruitment cycle occurred only twice during the 14-month survey.

Expression of the seasonal phenomenon of septum formation is more easily understood in F. fragilis, which produced a single generation per year, than in hivoltine

H. excentricus. Among the latter species septum formation hy the fall generations has its closest parallel in, and perhaps involves much the same genetic mechanism as, cyclomorphosis among rotifers and cladocerans.

Dr. Robert F. McMahon (1975, pers. comm.) collected thousands of Texas and Oklahoma H. excentricus and did not observe this phenomenon. Dr. Fred G. Thompson (1975, pers. comm.) has collected extensively in Florida, which is near the eastern extreme of the North American range, yet has not observed septate forms. Louisiana habitats for this species differ from those reported for other

North American populations. Basch (1963) reported their occurrence on floating and deep submerged debris in canals and ditches in Florida, while McMahon and Aldridge (1976) collected them on the surface of rocks in fast flowing streams in Texas.

Physiological changes, which surely accompanied septum formation in H. excentricus, seemed to have had little or no effect on parasitization. The period during which 55

septate forms comprised the greatest percentage of the population (Figure 21) corresponded to a discontinuity

in incidence of infection in both forms (Figure 20), however, septates harboring infections were collected during this period.

Role of Southeastern Louisiana Ancylids in Trematode Ecology

Southeastern Louisiana ancylids play more than a minor role in trematode life cycles, as indicated by the observa­ tion that collectively they host at least 19 different cercariae, which in turn utilize every class of vertebrates as definitive hosts.

Expectedly, the ecology of trematode intramolluscan

stages was closely related to the ecology of the limpet hosts. Nowhere was this more evident than Ben Hur

Farm (Figure 20), where the bivoltine reproduction of H. excentricus was reflected in two cycles of cercarial pro­ duction. Ihe aforementioned winter discontinuity repre­ sented an interim between cycles. Seasonality of those cercariae developing in F. fragilis did not demonstrate biannual patterns. Rather, individual trematode species were seasonal with discrete annual periods of cercarial production.

At Beaver Pond Branch (Figure 24) the annual generation of each limpet species is reflected in an annual generation 56

of cercaria production. Cercaria type XVII (probably

Stichordhis subtricruetrus) , from this locality, demon­

strated a pronounced seasonality, which must also relate to the life history of the beaver. Lowery (1974J noted

that, although little is known about reproduction in

Louisiana beaver, young are thought to be born in April or May. If true, June cercarial emergence and encystment on aquatic vegetation may be correlated with feeding habits of recently weaned beaver, and thereby insured infection of

a presumably more susceptible individual.

A similar seasonal correlation between cercarial emergence and life history of definitive host may exist

for Cercaria type VII (Spirorchis scripta) and the turtle

Chrysemys scripta. Cagle (1950) reported egg hatching in

Louisiana C. scripta to occur from early July to early

September. Peak cercarial emergence in July probably

insures infection of young, susceptible individuals, not previously exposed or harboring a current infection with this blood fluke.

Differences in population biology of L. fuscus at

Ramah and Sorrento were earlier attributed to putative differences in primary productivity between these habitats.

As shown in Figures 26 and 27, these differences are in turn reflected in the ecology of the respective ancylid- 57

hosted, trematode faunas. Seasonality of infection in L.

fuscus at Ramah was indicative of a single, annual host

generation; however, two cercarial species were maintained

essentially year round in Sorrento L. fuscus. and thus

reflected relative stability in the L. fuscus population.

Head of Island Pond (Figure 25) was productive enough

to permit a trivoltine pattern for H. excentricus, but was

faunistically poor in ancylid hosted, digenetic trematodes.

Only seven host-parasite combinations were observed, as

compared to 12 at Ben Hur Farm. Five of the seven

involved the single generation of F. fragilis.

Differences in species composition of ancylid hosted,

trematode faunas, at different habitats, can be explained

on the basis of ecological differences in the habitats,

i.e., absence or presence of suitable definitive or other hosts. There was no evidence of different physiological

strains of limpets incapable of hosting certain trematode

species.

Phylogeny of Southeastern Louisiana Ancylids

Basch (1963) noted a general similarity in radular

patterns among Ferrissia, Laevapex, and Hebetancylus.

He also compared anatomy of certain "soft-parts" and noted

a similar verge (male genitalia) for Hebetancylus and

Ferrissia •. however, the Hebetancylus pseudobranch 58

(respiratory organ) was bilobed like Laevapex. Basch thus

proposed that Hebetancylus had greater affinity with

Laevapex, which he believed to be more advanced. Hebe tan-

cylus and Ferrissia were suggested to have evolved independ­

ently from a common ancestor that was in turn derived from

the family Planorbidae.

Based upon the occurrence of septum formation in

Hebetancylus and Ferrissia* and the comparative ecology

of all three genera* X believe Hebetancylus occupies an

intermediate phylogenetic position between Ferrissia and

Laevapex.

Digenetic trematodes generally exhibit greater host

specificity for their molluscan first intermediate host

than for subsequent hosts, perhaps because of a longer

host-parasite evolutionary association (Pearson, 1972).

In light of this generalization, I compared the trematode

faunas hosted by each southeastern Louisiana ancylid

species. Similarities and differences between respective

faunas should reflect the emended phylogeny X have proposed.

Figure 28 depicts each of the three species as a

circle encompassing hosted cercariae, which for convenience have been assigned arabic rather than conventional roman

numeral designations. Figure 29 demonstrates overlap or

"sharing" of cercarial species. 59

Only an echinostome (type VI), a longifurcocercous distome (type IV), and Cercaria type III, tentatively identified as PosthodiplOBtomum minimum, were "shaded" by all three limpet species. None were "shared" jointly by

Hebetancylus and Laevapex, or by Hebetancylus and Ferrissia.

Ferrissia and Laevapex jointly "shared" xiphidiocercaria

(type I), Megalodiscus temperatus (type II), Lissorchis sp.

(type XI), and Stichorchis subtriquetrus (type XVII).

Ferrissia seems to be the least specialized. Even though sympatric with the other genera, Ferrissia maintained the ability to host exclusively four times as many cercar­ iae. This fact becomes more significant when noted that

F. fragilis comprised only 15% of all limpets examined.

Relative nearness of Ferrissia to the planorbid ancestral stock is suggested by the observation that at least five cercariae, hosted exclusively by F. fragilis or "shared" jointly with L. fuscus, are also hosted by planorbids.

The relative positions of Laevapex and Hebetancylus are less clear. Laevapex and Ferrissia have more cercariae in common than Hebetancylus and Ferrissia; however, one cercaria (type XVII) is so broad in host specificity as to develop in prosobranch and both orders of pulmonate gastropods. Furthermore, on the basis of my study, and that of Smith (1967), L. fuscus does not appear to be as 60

suitable host for Megalodiscus temperatus as does P.

fragilis.

The explanation for this "sharing" of cercariae by

Ferrissia and Laevapex can be found in the long sympatric

association of these limpets in North America. Hebetancylus

is Caribbean with its historical, ecological associations

in Central and South America.

Finally, the fact that Laevapex hosts an allocreadiid

(type IX), all others of which are hosted by spheriid clams, would tend to separate it from other ancylids.

Thus, a heretofore neglected group of molluscs is now known to have a major role in the bionomics of the local trematode fauna. LITERATURE CITED

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host to certain trematodes with notes on ancylids as

a new host for Mecralodiscus and Haematoloechus - Trans.

Am. Micro. Soc. 78 (2):228-231.

Smith, R. J. 1967. Ancylid snails as intermediate hosts

of Mecralodiscus temperatus and other digenetic

trematodes. J. Parasit. 53 (2):287-291.

Smith, R. J. 1968. Ancylid snails as first intermediate

hosts of Lissorchis mutaibile comb. n. (Trematoda:

Lissorchiidae). J. Parasit. 54 (2):283-285.

Turner, H. M. 1977. Distribution record for Hebetancylus

excentricus (Morelet) (Pulmonata:Ancylidae) in Louisiana

and a report of septum formation. Nautilus. (in

press) .

Turner, H. M. and K. C. Corkum. 1977. New snail host for 68

Spirorchis scripta Stunkard, 1923 (Digenea:Spirorchi-

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Soc. Wash. (in press).

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1899 (Digenea:Plagiorchiidae) from raniid frogs of

Texas. J. Parasit. 63(1):122.

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and Lancidae. Occ. Pap. Mus. Zool. Univ. Michigan.

165:1-13.

Wallace, H. E. 1941. Life history and embryology of

Triganodistomum mutabile (Cort) (Lissorchiidae:

Trematoda). Trans. Am. Micro. Soc. 60:309-326.

Yamaguti, S. 1971. Synopsis of the digenetic trematodes

of vertebrates. Keigaku Publ. Co., Ltd., Tokyo. 1800 p.

Yamaguti, S. 1975. A synoptical review of life histories

of digenetic trematodes of vertebrates. Keigaku Publ.

Co., Ltd., Tokyo. 1100 p. 69

Figures 1-7. Cercariae developing in southeastern Louisiana ancylid snails. Scale in microns.

1. Cercaria type I

2* Cercaria type II

3. Cercaria type III

4. Cercaria type IV

5. Cercaria type V

6* Cercaria type VI

7. Cercaria type VII 100 71

Figures 8-14. Cercariae developing in southeastern Louisiana ancylid snails. Scale in microns.

8. Cercaria type VXII

9. Cercaria type IX

10. Cercaria type X

11. Cercaria type XI

12. Cercaria type XII

13. Cercaria type XIII

14. Cercaria type XIV 72

8

11 100

12 14 Figures 15-19. Cercariae developing in southeastern

Louisiana ancylid snails. Scale in microns.

15 . Cercaria type XV

16. Cercaria type XVI

17 . Cercaria type XVII

18. Cercaria type XVIII

19. Cercaria type XIX 74 100 75

Figure 20. Monthly incidence of infection, population

structure, and index of relative abundance for (H.)

Hebetancvlus excentricus and (F.) Ferrissia fragilis

at Ben Hur Farm. Small, medium, and large refer to size

classes of limpets. Cercarial type and limpet host

combinations are indicated by various symbols. Relative

abundance is indicated by circle with unbroken line. % population incidence of infection£ 100 100 0 6 20 20 0 4 0 8 0 6 20 0 3 20 0 4 0 8 10 I 5 I 0 I O I5 0 0 0 0 0 5 5

9 J JAS0NDJ F M A M J J A S O N ~ ® - T Y P E V I (F) — T Y P E Vlf (F) ° T Y P E XIII E (F) P Y ° T ) H ( V I E P (F) Y Vlf T - o E - P Y T 111 E (H) P — Y T I (F) V E P Y T - ® ~ II (F.) E P Y • T - • - T Y P E I V (F.) • T Y P E V (H.) T Y P E VI (H.) VI E P Y T (H.) V E P Y T • (F.) V I E P Y T - • - XIV F) F • XVI I (F) V X E P Y • T (F) V X E P Y T • (F.) V I X E P Y T ® . excentricus H. - E G R A L - - - M U I D E M — L L A M S month Y \ s 8 ft-. - t f 8 ■s' . fraqilis F. ---o K -- * —"—o "O— o— 20 1 0 0 3 0 4 0 6 1 0 0 5 0 2 6 4 8 0

no. collected 76 per 15 man/mins. 77

Figure 21. Percent Ben Hur Farm Hebetancylus excentricus population in either septate or post-septate phases.

Figure 22. Septate Hebetancylus esccentricus exhibiting various degrees of septum formation. Pseudobranch visible

on middle specimen. Scale above in mm.

Figure 23. Post-septate Hebetancylus excentricus.

Scale above in mm. POPULATION JJASOHDJFMAUJOASON MONTH ETT PHASE SEPTATE ■ OTSPAE PHASE POST-SEPTATE ~ 78 79

Figure 24. Monthly incidence of infection, population

structure, and index of relative abundance for (H.)

Hebetancylus excentricus and (F.) Ferrissia fragilis

at Beaver Pond Branch. Small, medium, and large refer to size classes of limpets. Cercarial type and limpet host combinations are indicated by various symbols.

Relative abundance is indicated by circle with unbroken

line. /o population incidence of infection 100 100 60 80 40 80 20 40 60 20 4 0 6 8 9 2 3 4 0 7 2 3 5 0 0 I 1

J J ♦ T Y P E VI (H.) VI E P Y T ♦ . s u c i r t n e c x e H. I (F.) E P Y T + ■ T Y P E XII (H.) XII E P Y T ■ ASON O S J A J M A M F J D N O S A . fragilis F. L L A M S J Month

♦ T Y P E VI(F.) • T Y P E VII VII (F) E P Y T • VI(F.) E P Y T ♦ TYPE TYPEXVII(F) E P Y T • ) . F ( V X E P Y T ® II E (F.) P Y T • M U I D E M — ' O - TYPE ) H ( V I E P Y T E G R A L —

0 20 30 40 50 20 30 0 40 50 10 10 no. collected per 15 Man/Mins. 80 81

Figure 25. Monthly incidence of infection, population structure, and index of relative abundance for (H.)

Hebetancylua excentricus and (F.) Ferrissia fragilis at Head of Island Pond. Cercarial type and limpet host combinations are indicated by various symbols. Relative abundance is indicated by circle with unbroken line. 82

SMALL— MEDIUM - LARGE • TYPE ll (F.) ® T Y P E III (H.) o T Y P E I V (H.) ° T Y P E XIII (F) ® T Y P E XIV( F ) + T Y P E XVIII (F.) |f T Y P E X I X (F.)

2 0

o c " c o 0 ” 2 5 " O O 2 0

6 0 K excentricus

100 5 0 8 0 4 0 6 0 3 0 4 0 20 20

■

100 F fragilis 25 Man/Mins. 8 0 20 6 0 4 0 no. no. collected 2 0 per 15 per 15

JJASONDJFMAMJJA Month 83

Figure 26. Monthly incidence of infection, population structure, and index of relative abundance for (L.)

Laevapex fuscus, (H.) Hebetancylus excentricus, and

(F.) Ferrissia fragilis at Ramah. Small, medium, and large refer to size classes of limpets. Cercarial type and limpet host combinations are indicated by various symbols. Relative abundance is indicated by circle with unbroken line. population ° / o incidence of M ■ a o

4 0 0 0 0 0 0 2 3 8 2 0 I

a T Y P E V I (F.) o T Y P E V I ( L ) • T Y P E VII (F) VII E P Y T • ) IV(H.) L ( I V E P E Y P o T Y III T E (L.) o P Y (F.) I T V E * P Y Ia (F.)T E P Y T + ® T Y P E VIII (F) 8 T Y P E I X (L.) e T Y P E X I (L.) I X E P Y T e (L.) X I E P Y T 8 VIII (F) E P Y T ® SMALL MEDIUM = I (L) E P <=> Y T E G R A L — M U I D E M — L L A M ■ S JASONDJFMAMJJA —0 0— . s u c i r t n e c x e H. i R_ fragilis R_ .fuscus u c s u f L. month J i t a / I lit t J 1 iLltll N; 1

0 0 3 0 2 0 4 8 20 0 6 4 8 0 4 1 2 0 5 20 I 2 I 6 I6 I0

0

o c

. collected per 15 man/mins. 84 Figure 27. Monthly incidence of infection, population

structure, and index of relative abundance for (L.)

Laevapex fuscus, (H.) Hebetancylus excentricus, and

(F.) Ferrissia fragilis at Sorrento. Small, medium, and large refer to size classes of limpets. Cercarial type and limpet host combinations are indicated by various symbols. Relative abundance is indicated by circle with unbroken line. population ° / o incidence of 100 100 100 2 0 4 0 8 0 4 0 6 0 8 2 0 4 0 6 20 20 0 4 0 6 8

0 0 0

(. ®TYPE I(. •TYPE II (F.) E P Y T • II (L.) E P Y T ® I (L.) E P Y T o TYPE IV H) V (. <© (L.) X E P Y T © < (L.) VI E P Y T • T E (H.) P Y T ® III E ) P L ( Y T - J JAS0NDJ F M A M J J . s u c s u f L. fragilis . s u c i r t n e c x e H. month - M U I D E M ES G R A L L L A M 0.8 100 0.2 0 0.0 0.6 6 0 4 . 0 8 20 0 4 0 6 4 0 8 1 0 2 I

no. collected per 15 man/mins. 86 87

Figure 28. Southeastern Louisiana ancylid species as circles encompassing hosted cercariae.

Figure 29. Southeastern Louisiana ancylid species as overlapping circles encompassing "shared" and exclusively hosted cercariae. L aevapex fuscus

Laeygpex tll£-CLlLS, VITA

Hugh M. Turner was b o m September 20, 1942 in Marianna,

Florida. He was graduated from Statesboro High School,

Statesboro, Georgia in 1960, obtained a Bachelor of Science degree from Georgia Southern College in 1965 and served four years in the United States Marine Corps. He received a Master of Science degree from Georgia Southern College in

1972. He is presently a candidate for the Doctor of

Philosophy degree in the Department of Zoology and

Physiology, Louisiana State university.

89 EXAMINATION AND THESIS REPORT

Candidate: Hugh M, Turner

Major Field: in v e rte b ra te Zoology

Title of Thesis: a SEASONAL AND ECOLOGICAL SURVEY OF FRESHWATER LIMPET SNAILS

AND THEIR DIGENETIC TREMATODE PARASITES IN SOUTHEASTERN

LOUISIANA

Approved:

Major Professor and Chairman

Dean of the Graduate School

EXAMINING COMMITTEE:

L

“S - 7 (/J/LkJLvjl/o

Date of Examination:

July 13, 1977