73-26,921
STROMBERG, Paul Charles, 1945- THE LIFE HISTORY AND POPULATION ECOLOGY OF CAMALLANUS OXYCEPHALUS WARD AND MAGATH, 1916 (NEMATODA:CAMALLANIDAE), IN FISHES OF WESTERN LAKE ERIE.
The Ohio State University, Ph.D., 1973 Zoology
University Microfilms, AXEROX Company , Ann Arbor, Michigan
THIS DISSERTATION HAS BEEN MICROFILMED EXACTLY AS RECEIVED THE LIFE HISTORY AND POPULATION ECOLOGY OF CAMALLANUS
OXYCEPHALUS WARD AND MAGATH, 1916 (NEMATODA:
CAMALLANIDAE), IN FISHES OF WESTERN LAKE ERIE
DISSERTATION
Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University
By
Paul Charles Stromberg, B.Sc.
The Ohio State University 1973
Reading Committee: Approved by
Paul A. Colinvaux
Richard A. Tubb
John L. Crite ACKNOWLEDGMENTS
I am profoundly grateful to my adviser, Professor
John L. Crites, not only for all his advise and help with this study, but for directing my interest and enthusiasm in parasitology during the last 10 years. His kindness, criticism, encouragement, fairness and above all patience, have been of inestimable value to me.
I am also grateful to Professor Paul A. Colinvaux and Professor Rodger D. Mitchell who, knowingly or un knowingly, have stimulated me to think about host-parasite systems as an ecologist.
Dr. Richard A. Tubb and the staff of the Ohio
Cooperative Fisheries Unit and Dr. Loren S. Putnam and the Franz Theodore Stone Laboratory were of great help in providing assistance, facilities and services for this research. Mr. Russell Scholl and the Ohio Division of
Wildlife helped in the collection and aging of fish. I would also “like to thank the commercial fishermen of Lake
Erie, especially Mr. Thomas Smith of the Cold Creek Fish
Company, without whose help this study would not have been possible.
I would also express appreciation to Dr. C. E. Herdendorf of the Center for Lake Erie Area Research, Mr.
Delmar Hanley and the Federal Fish Restoration Act,
Project F-48-R-1, administered by the Ohio Department of
Natural Resources, Division of Wildlife.
In addition, I am thankful for the help and support
I received from several of my graduate student associates; in particular, Mr. Clifford Swanson for his help in the field and laboratory and with the photography; Mr. Richard
Wehnes for his help collecting fishes; Dr. Charles Barans, for his help collecting and maintaining live fish; Mr.
Robert Ashmead, for autopsying fishes; and finally, to
Dr. John E. Zapotosky and Dr. Norton Rubinstein for their ideas and enthusiasm.
I would also like to express special thanks to
Mr. Aaron Supowit, Ms. Patricia Saunders, Mr. Thomas Whitney and the Ohio State University Instruction and Research
Computer Center for all their time and assistance with the handling, programming and analysis of the data. VITA
June 9, 1945...... Born - Morristown, New Jersey
1965-1967 ...... Research Assistant, Ohio Cooperative Wildlife Research Unit; Ohio State University
June, 1967...... B.Sc. with distinction, The Ohio State University
June, 1968-Sept.,1968 . . Ohio Cooperative Fisheries Unit Fellow - Eastern Fish Disease Laboratory, Leetown, West Virginia
1967-19 72 ...... Teaching Associate, Department of Zoology, The Ohio State University
June, 19 70...... Married, Joan Shaw; Worthington, Ohio
1972-1973 ...... Staff Research Biologist, the Center for Lake Erie Area Research
PUBLICATIONS
1970. DDT residues associated with cestodes from Mallard and Lesser Scaup ducks. Bull. Environ. Cont. Tox. 5<1):13-15.
1970. Aspidobothrean trematodes from Ohio mussels. Ohio J. Sci. 70(6):335-341.
19 72. A new nematode Dichelyne bullocki sp. n. (Cucullani- dae) from Fundulus heteroclitus (L.) Proc. Helm. Soc. Wash. 39(1):131-134.
197 3. A description of the male and redescription of the female of Carnallanus oxycephalus Ward and Magath, 1916 (Nematoda:Camallanidae). Proc. Helm. Soc. Wash. 40(2): iv FIELDS OF STUDY
Major Field: Zoology
Studies in Helminthology. Prof. John L. Crites
Studies in Invertebrate Zoology. Prof. John L. Crites
Studies in Ecology. Prof. Rodger D. Mitchell
Studies in Fish Disease. Dr. Glenn L. Hoffman
Y TABLE OF CONTENTS
Page
ACKNOWLEDGMENTS...... ii
VITA ...... iv
LIST OF TABLES ...... viii
LIST OF ILLUSTRATIONS...... x
INTRODUCTION ...... 1
MATERIALS AND METHODS...... 4
HISTORICAL BACKGROUND...... 7
Systematics and Taxonomy...... 7 Geographical Distribution ...... 12 Review of Previous Life History Information...... 14
DESCRIPTION OF CAMALLANUS OXYCEPHALUS...... 20
THE LIFE HISTORY OF CAMALLANUS OXYCEPHALUS .... 26
Description of Larval Stages and Development...... 26 Discussion of the Life History...... 39
STUDIES ON THE BIOLOGY OF THE 1ST STAGE LARVAE . . 47
Survivorship...... 47 Infection of Copepods ...... 48 Activity 5 3 Discussion...... 55
ECOLOGICAL STUDIES OF CAMALLANUS OXYCEPHALUS IN WESTERN LAKE ERIE...... 6 5
Western Lake Erie Ecosystem ...... 65 History of C. oxycephalus in western Lake E r i e ...... 66 Discussion of the History in western Lake E r i e ...... 77
vi Page
Population Structure of C. oxycephalus...... 83 Growth and Development in the Natural P o p u l a t i o n ...... 86
DISTRIBUTION IN WESTERN LAKE ERIE FISH...... 95
Relationship to Fish Sex...... 95 Relationship to Fish S i z e ...... 9 5 Changes in the Infection...... 106
THE LAKE ERIE-CAMALLANUS SYSTEM...... 12U
SUMMARY...... 133
PLATES ...... 138
APPENDIX A ...... 1H8
APPENDIX B ...... 159
REFERENCES CITED ...... 16 2
vix• • LIST OF TABLES
Table Page
1. Distribution of the Species of Camallanids in host groups...... 10
2. Experimental Determination of Inter mediate Host 2 7
3. Determination of the Releaser for Escape Activity ...... 32
4. Observed Molting Sequence of Some Other Camallanids...... 42
5. Life Table for C. oxycephalus 1st Stage Larvae at 20^C...... 49
6. Life Table for C. oxycephalus 1st Stage Larvae at 25°C...... 50
7. Infection of Copepods by 1st Stage Larvae...... 51
8. Potential Production of 3d Stage Larvae from L^ Survivorship at 25 C . . . 59
9. Potential Production of 3d Stage Larvae from L^ Survivorship at 20 C . . . 60
10. Comparison of Frequency of C. oxycephalus in Lake Erie 1927-57-71-72 ...... 71
11. Seasonal Structure of C. oxycephalus Population in Lake Erie . . -...... 85
12. Turnover of Adult C. oxycephalus Population...... 86
13. Relationship Between Female Length, Volume and 1st Stage Larvae Production. . 9 2
14. Frequency of Food Organisms Found in Some Fish Stomachs...... ICO
viii Table Page
15. Frequency Distribution of C. oxycephalus in Centrarchids...... 105
16. Frequency Distribution of C . oxycephalus in Young of the Year Gizzard Shad...... 108
17. Frequency Distribution of C. oxycephalus in Young of the Year White Bass...... 109
18. Frequency Distribution of C. oxycephalus in Young of the Year Freshwater Drum . . . 110
19. Seasonal Changes in the Infection of Adult White Bass in Lake Erie...... 112
20. Seasonal Changes in the Infection of Young of the Year White Bass in Lake E r i e ...... 112
21. Seasonal Changes in the Infection of Adult Yellow Perch in Lake Erie...... 113 LIST OF ILLUSTRATIONS
Text Figure Page
1. Growth of C. oxycephalus in White Bass at 26 C ...... 37
2. Survivorship Curve of 1st Stage Larvae at 20 and 2 5 C ...... 52
3. Penetration Efficiency and Age of the 1st Stage Larva ...... 54
4. Basal and Excititory Activity Rates of 1st Stage Larvae at 25 C ...... 54
5. Effect of Temperature on the Development of the Larvae within the Copepod. . . . 56
6. Relationship Between L-. Activity and Consumption by Cyclopoid Copepod. . . . 64
7. Map of Lake E r i e ...... 6 7
8. Western Basin of Lake Erie with Collection Sites...... 6 7
9. Frequency Changes of C. oxycephalus in Lake Erie Fish...... 69
10. Frequency Changes of C. oxycephalus in Lake Erie Fish...... 69
11. Frequency Changes of C. oxycephalus in Lake Erie Fish...... 70
12. Frequency Changes of C. oxycephalus in Lake Erie Fish...... 70
13. Host Species Importance Curves for Lake Erie Fish Community 19 27-57-71-72 . . . 76
14. General Host-Parasite Population Interaction Model ...... 79
x Text Figure Page
15. Systems Model of C. oxycephalus in Lake Erie...... 81
16. Growth Cruve of C. oxycephalus in the Natural Population ...... 88
17. Relationship Between Dispersal Period of C. oxycephalus and the Seasonal Copepod Density...... 90
18. Relationship Between Intensity of Infection and Fish Length for White Bass, S u m m e r ...... 9 7
19. Relationship Between Intensity of Infection and Fish Length for White Bass, Spring ...... 9 7
20. Relationship Between Intensity of Infection and Fish Length for Yellow Perch, Summer...... 98
21. Relationship Between Intensity of Infection and Fish Length for Yellow Perch, Spring...... 98
22. Relationship Between Intensity in Infection and Fish Length for Fresh water D r u m ...... 99
23. Seasonal Changes in the Mean Infection Intensity of C. oxycephalus in White B a s s ...... 122
24. Summary of the Life History of £. oxycephalus...... 126
25. Flow Diagram of £. oxycephalus Community Relationships...... 127
Plate
I. Development of 1st Stage Larva...... 138
II. Development of 2nd and 3d Stage Larvae. . . 140
xi Plate Page
III. Development of 4th Stage Larva and Adult...... 142
IV. Adult £. oxycephalus...... 144
V. Cross Section of White Bass Intestine with £. oxycephalus in situ...... 146 INTRODUCTION
My interest in this problem resulted from frequently collecting Camallanus during several summers at the Franz
Theodore Stone Laboratory. This research was undertaken because of my interest and at the suggestion of my academic adviser, Professor John L. Crites.
Initially this research was concerned with studying the life history of Camallanus oxycephalus Ward and
Magath, 1916. Several other studies of camallanid life histories have been published, but none had completely elucidated the basic pattern. For instance, there was confusion about the types of intermediate hosts in volved, the number and sequence of molts in the develop mental cycle and the use of transport of "paratenic hosts". However, while searching for the answers to these questions, I began to think about some basic ecological questions. I was particularly interested in why this nematode was so abundant in Lake Erie fish.
Comparison with 2 previous surveys revealed that the incidence in Lake Erie had increased dramatically over the last 45 years. Information gathered in studying the life history was applied to questions generated about the population biology. This in turn generated inquiries about population density and regulatory mechanisms which may be applicable to other host-parasite systems.
The objectives of this study, then have changed periodically, progressing from the elucidation of the life history pattern of a specific nematode to the study of some broad characteristics common to many parasitic species. This progression in though still continues at the time of this writing.
Much of the work done on the Camallanidae has been taxonomic. As a result of this work, knowledge about the distribution and morphological variation of these nematodes is extensive. There are about 119 described species in six genera found in fish, amphibians and reptiles. They occur on every continent except Ant arctica. Most of these are found in the tropical and subtropical latitudes. Only two species are known from
North American freshwater fish, Camallanus oxycephalus and C. ancylodirus Ward and Magath, 1916. Both species have frequently been reported from fish by numerous authors, but no complete description of the species or work on the life history has been attempted. One of the objectives of this study was to clarify the description and elucidate the life cycle.
In addition to the life history, I also intended to study the population biology of this parasite. Several investigators have made such studies of other helminths in fish (Kennedy, 1968; Hopkins, 1959). These studies have been concerned with the number and frequency of worms, seasonal occurrence, sex and size of the fish as well as recruitment and mortality of parasites. It was my objective to measure these parameters in the Lake Erie
Camallanus system and compare my findings with previous investigations.
I was also interested in developing some evolutionary questions about Camallanus in particular and parasite populations in general. Foremost among these was how parasite populations are regulated and the implications of differing types of life cycles. MATERIALS AND METHODS
Examination of fish and specimen preparation
Lake Erie fishes were collected by seine, Fyke net, otter trawl, gill net and hook and line. In addition, fishes were obtained from commercial shore seines, trap nets and the Ohio Division of Wildlife. All fishes were transported on ice to either Franz Theodore Stone
Laboratory or the parasitological laboratory at Ohio
State University in Columbus. The entire intestine was removed from each fish and placed in Ringer’s Solution.
Young of the year fishes were placed into a pepsin digest solution and the residue examined for nematodes.
All worms were killed in hot Ringer’s, fixed for 24 hours in A.F.A. and stored in 10% glycerin alcohol. Nematodes were cleared and mounted in glycerin. Measurements were made with an ocular micrometer, accurate to 1.5 microns.
Portions of fish intestine with worms in situ were fixed in alcoholic Bouin's for sectioning to study pathology. This material was dehydrated and embedded in paraplast and cut on a microtome at 8 microns thickness.
Sections were stained with Mallory's triple stain and hematoxylin and eosin.
4 Experiments
Infective first stage juveniles were obtained by placing gravid female C. oxycephalus in lake water and allowing the worms to rupture, releasing thousands of juveniles. Arthropods for intermediate host determina tion were collected with a plankton net and dip net.
Copepods were maintained in the laboratory in one gallon containers and fed Paramecium 3 times a week. Copepods were infected by exposing single copepods to 10 juveniles in 2 ml of lake water for 2H hours.
Experimental fishes were young of the year fish collected by seine before the dispersal period of
Camallanus. These fishes were brought to the laboratory, placed in 15 gal acquaria, treated with Maracyn and
Malachite Green and maintained on fish meal and spot- tail shiner fry. Shiner fry were periodically sampled and dissected to establish absence of Camallanus. Some experimental Yellow Perch were hatchery raised at
Fender's Fish Hatchery, Baltic, Ohio. All fish infected by copepods were anesthetized in Quinaldine C.025ml/3 gal
HgO) and fed copepods via stomach tube.
Data
Simple mathematical procedures and small sample statistics were handled on a Hewlett-Packard 9100 E desk computer. Data on fish, nematode numbers, lengths, volume conversions, etc., were analyzed by standard FORTRAN XV programs on an IBM 370/165 digital computer. HISTORICAL BACKGROUND
Systematics and Taxonomy
The family Camallanidae was erected in 1915 by
Railiet and Henry for Camallanus lacustris (Zoega, 1776).
This species was first described as Echinorhynchus
lacustris in Muller (1776). Muller observed in 1779 that this species was incorrectly placed and assigned it to the genus Cucullanus which he had created in 1777. It remained in this genus until 1915. Camallanus was the only genus in the family until 19 22 when Baylis and
Daubney set up the genus Camallanides. Baylis (19 23) created the genus Procamallanus the following year. York and Maplestone (1926) added a fourth genus, Paracamallanus, by 1926. Tornquist (19 31) in a complete review of the
family, recognized these four genera and listed about 24
species.
The next major revision within the Camallanidae
occurred when Olsen (195 2) divided the genus Procamallanus
Baylis, 19 2 3 and created Spirocamallanus. There were, at
that time, 24 species described in Procamallanus. Olsen
assigned 16 of these to the new genus on the basis of
the spiral thickenings in the buccal capsule. Ali (1957)
7 erected the genus Neocamallanus and the subgenera
Monospiculus and Isospiculus and in 1960 added a third subgenus, Aspiculus. Campana-Rouget (1961) suppressed
Ali's assignments and supported Olsen's genus, Spiro- camallanus.
Chabaud (1965) created the Superfamily Camallanoidea to include the following three families: Camallanidae
Railiet and Henry, 1915, Cucullanidae Cobbold, 1864, and
Anquillicolidae Yamaguti, 1955. The definition of this grouping is very broad, however, and probably based upon superfiscial morphological similarities. Until more information is made available concerning the biology of the latter two families, the validity of Chabaud's super family is in doubt.
The last major change within the Camallanidae occurred when Yeh (19 60) divided the family into two sub families : the Procamallaninae and the Camallaninae. He placed the genera Procamallanus and Splrocamallanus
Olsen, 1952 in the former, and Camallanus, Camallanides
Baylis and Daubney, 19 22 and Paracamallanus York and
Maplestone, 19 26 in the latter. In addition, he created three new genera; Zeylanema, Piscilania and Serpinema.
The first of these is most likely valid and has been recognized by several authors (Furtado, 1965). Piscilania was created for Camallanus melanocephalus (Rudolphi, 1819) and contains only that species. This species needs re-examination and until that is accomplished, I shall resist separating a new genus out of Camallanus for a single worm. The third genus, Serpinema is also question able. It was created for 10 species of Camallanus which occur in reptiles and based upon a separation of the buccal ridges into dorsal and ventral groups. Examination of North American specimens of C. microcephalus (Dujardin,
1845) revealed that this character appears constant, but specimens of C. octorugatus Baylis, 193 3 from Australia, do not show this separation. Yeh's inclusion of this species into Serpinema is thus incorrect, but whether this invalidates the entire genus or not is questionable.
Since other genera, Carnallanides, in the family occur in fishes, and reptiles, Yeh’s inclusion of all reptilian species of Camallanus into a separate genus may be arti ficial. Until further information is available, I shall recognize only Camallanus as the genus for these species.
The Family Camallanidae at present is comprised of at least 6 genera and approximately 119 species occurring in fishes, amphibians and reptiles. Table 1 summarizes this distribution. It can be seen from this table that the camallanids are primarily parasites of fresh-water fish with approximately equal numbers of species in marine fish, amphibians and reptiles. Nearly 75% of all species occur in fish. The amphibian forms are ex clusively frog and toad parasites. The reptilian species 10 are predominantly from turtles, but a few species occur in snakes and lizards. As a group, the Camallanidae are essentially associated with aquatic vertebrates.
TABLE 1. DISTRIBUTION OF CAMALLANID SPECIES IN HOST GROUPS
Genus Fish Fish Reptiles Amphibians Total (F) CM)
Camallanus 24 3 11 12 50
Procamallanus 24 4 - 2 30
Spirocamallanus 17 7 - 1 25
Zeylanema 6 - - - 6
Camallanides 1 - 3 1 5
Paracamallanus 3 - - - 3
Totals 74 14 14 17 119
% .618 .121 .121 ,142 1.00
F indicated freshwater species;
M indicated marine species.
Description of Family and Genera
Family Camallanidae Railiet and Henry, 1915
Description: Mouth elongate dorsoventrally; buccal
capsule sclerotized, either barrel-shaped, or divided 11 into two lateral shell-like valves; esophagus com posed of anterior muscular portion and posterior glandular portion. Male: Posterior end curved ventrally; caudal alae present; papillae variable in number* mostly pedunculate: spicules dissimilar, equal or unequal. Female: Vulva usually near middle of body; vagina directed posteriorly; uterus with posterior limb ending blindly; one ovary.
Ovoviviparous.
Key to the Genera of Camallanidae
CYeh, 1960)
Buccal capsule barrel-shaped...... Procamallaninae
Buccal capsule smooth...... Procamallanus
Buccal capsule with spiral ridges...Spirocamallanus
Buccal capsule consisting of 2 lateral shell-like,
sclerotized valves...... Camallaninae
1. Buccal capsule with anterior and posterior
divisions of nearly equal size. . . .Paracamallanus
Buccal capsule with posterior division absent or
markedly smaller than anterior division...... 2
2. Buccal valves with deep lateral groove; tridents
modified into monodonts...... Camallanides
Buccal valves without lateral groove...... 3
3. Buccal ridges smooth...... Camallanus
Buccal ridges armed with teeth...... Zeylanema 12
Geographical Distribution
Camallanids have a world-wide distribution, but are most numerous and most diverse in tropical Asia. All six genera and 6 5 (54.0%) species occur there. Two genera,
Zeylanema and Camallanides, are indigenous, and a third,
Paracamallanus occurs outside of Asia only in tropical
Africa. Procamallanus is essentially a tropical Asian genus with 2 3 (79.3%) indigenous species. Two species occur in tropical Africa, one in temperate South Africa and two in Japan. Spirocamallanus also shows a pre dominantly tropical distribution pattern, that is larger than Procamallanus. A center of diversity occurs in both the Old World Tropics and the New World Tropics. Only three species of Spirocamallanus occur in temperate or subtropical latitudes; one in Australia, one in Japan and one in North America. The North American species, S^. pereirai (Annereaux, 1946) is particularly illustrative of how this genus is essentially restricted to warm water.
S. pereirai is known from five species of inshore fish on the southern California coast (Noble and King, 1960).
It also occurs in five species of marine fish from southern Florida (Hutton, 19 64). I have collected it from croakers (Micropogon undulatus) in Alabama and
Overstreet (19 72) reports that it occurs commonly in the
Gulf of Mexico in this fish. Although croakers range from Texas to New Jersey, no reports of this nematode exist anywhere else north of Florida. It would appear
that in this case the range of the nematode is not being
restricted by the host range. Perhaps the worm is
restricted in some way by the climate.
Only the genus Camallanus has apparently been able
to invade the cold temperate regions. Nineteen of the
50 species or almost 40% occur outside tropical areas.
The genus is represented on all the continents except
Antarctica, although the greatest diversity occurs in
tropical Asia. The species of this genus exhibit an
interesting characteristic with respect to latitude.
Tropical Asia has the most species of any geographical region (20). The degree of specialization or host
specificity is high in this region. Frequently, several
species of Camallanus occur in one species of host. The species diversity in North America and Eurasia is low and the degree of specialization is also low. Moravec
(19 69b) stated that C. lacustris was reported from 32 species of fish in nine families found in Eurasia.
Camallanus oxycephalus Ward and Magath, 1916 is known from over 50 fish in North America. Camallanus micro- cephalus occurs in 11 species of turtles in North
America and Europe. It appears, then, that there is a trend toward lower diversity and lower specialization in temperate latitudes.
The evidence suggests that the Camallanidae is 14
essentially a tropical family which parasitizes aquatic
vertebrates. Invasion of temperate regions has been
limited and apparently must be accompanied by special adaptations not widely found in the group. Since few
species has succeeded in establishing populations in
cool water environments, investigations of the life
history and population ecology of species in both tropi
cal and temperate regions might be very useful in
elucidating some of these adaptations.
Review of Previous Life History Information
Leiper in 1910 demonstrated a living Cyclops infected with Cucullanus elegans (= Camallanus lacustris) before
the Zoological Society of London. This represented the
first solid evidence that camallanids utilized copepods
as first intermediate hosts. Since then several in
vestigators have studied the life history phenomena of
camallanids.
Li (19 35) studied the early development of Spiro-
camallanus fulvidraconis (Li, 19 35) in China. He
demonstrated that this worm utilized species of Cyclops
as intermediate hosts. In a series of experiments with
seven species of Cyclops, he discovered that the pene
tration efficiency of the 1st stage larva into the cope-
pod hemocoel was as low as .083 - .133. Li observed a
larval molt on the 8-9th day post-infection (p.i,), but 15 repeated examinations up to 5 weeks revealed no further molts. However, he described the slender tail of this larva as j "...gradually (retreating), leaving an empty sheath behind, until just before the first molt a short tripod tail, similar to that of the female adult, was found, already formed within the old cuticle". It seems clear that Li was describing the mucrones on the tail of the 3rd stage larva and that what he believed was the first molt was, in fact, the second.
The following year, Pereira, Dias and Azevedo (19 36) described Spirocamallanus cearensis from Brazil and in vestigated its life history. They found that the calanoid copepods of the genus Diaptomus were the intermediate host. Natural infections of these crustaceans were as high as 2% and experimental infections low, at 4%. They believed that only one molt occurred in the copepod.
Examination of their description reveals that the larvae which they thought were 2nd stage larvae, possessed three mucrones on the tail and thus were most likely 3rd stage larvae. It is likely too that they observed only the 2nd molt within the copepod. Figure 6 in their manuscript is labeled "3rd stage larva" from the fish and since it possesses a divided buccal capsule and apparently a mucronate tail it seems that this designation is correct.
However, their Fig. 7 is also labeled 3rd stage, and it seems sure that this worm is a 4th stage larva. The tail 16 has no mucrones (which are lost with the final molt in
C. oxycephalus) and the undivided buccal capsule is figured with what appears to be a new and probably adult buccal capsule forming around it. Pereira, et al. noted that when infected copepods were fed to small fish the nema todes continued development. They believed small forage fish served as transport hosts and larger carnivorous species acquired the infection by consuming these small fish.
The next major contribution to the elucidation of the life history of the camallanids was Moorthy (1938), who studied the life history of Paracamallanus sweeti (Moorthy,
1937) in India. This species also used a copepod for the intermediate host. Moorthy noted that the first molt occurred 24-36 hours p.i. and stated that it was extremely difficult to recognize. The second molt occurred on the
8-12th day at 55-70°F. Third stage larvae had divided buccal capsules and three mucrones on the tail. He observed development of the 3rd stage larvae within the final host intestine and although he did not describe the third molt, he saw the final molt. An additional contri bution by Moorthy was the demonstration that fish bile activated the Lg within the copepod and apparently stimu lated it to escape from the crustacean.
Moorthy also believed that large piscivorous fish were infected by consuming smaller, plankton-feeding 17
species. Whether or not this transport host was necessary was enigmatic. He collected adult worms from only one
species, but recovered L^'s from five species of plankton-
feeders. His assumption that the final host was most often infected by eating these small transport hosts is probably correct.
The most recent and most thorough investigation of camallanid development to date was done by Moravec (1969a).
He studied the development of Camallanus lacustris in the laboratory and clarified some of the questions and antago nistic views held by several investigators who had studied this European nematode.
In addition to copepods, Moravec also attempted to infect isopods, amphipods, cladocerans, mayfly, caddisfly, dragonfly and chironomid larvae. The results of these experiments established that only copepods serve as inter mediate host. Four days after infection (20-25°C) the larvae undergo the first molt. Much development occurred during the 2nd stage. The second molt occurred after the ll-12th day p.i. The 3rd stage larvae had a divided,
"Paracamallanus-type11 buccal capsule typical of other camallanid Lg's and three mucrones on the tail. The third molt occurred 13-15 days after infection of the fish with the Lg. The males molted for the Uth time 35 days p.i. and females molt 65 days p.i. Larvae appeared in the female uterus by the 91st day. Moravec (1969b) noted that C. lacustris was known from a wide variety of fish. Based upon infection experi ments, he divided these hosts into the following three groups: one, fish in which normal development occurs, including percids, salmonids and gadids; two, predatory cyprinids in which development occurred, but a-t a slow rate; and three, nonpredatory cyprinids and cobitids in which the larvae remained but showed no further develop ment. Moravec suggested that this latter group acted as a reservoir transmitting the nematode to larger fish when they consumed small infected cyprinids.
Summary of Accumulated Information Concerning the
Camallanid Life History
1. Adult female worms in the stomach of intestine
of an aquatic vertebrate contains infective 1st
stage larvae in the uterus.
2. First stage larvae are released into the water
and consumed by copepods.
3. Larvae penetrate through the gut wall into the
hemocoel where they undergo two molts and become
infective 3rd stage larvae.
H. Copepods eaten by fish are killed and bile
stimulates escape activity of the L^; the worm
molts twice and becomes an adult. Some kind of transport host mechanism appears to be involved but the necessity of it is questionable. Some investigators believe this to be a true 2nd intermediate host. DESCRIPTION OF CAMALLANUS OXYCEPHALUS
WARD AND MAGATH, 1916
Camallanus oxycephalus Ward and Magath, 1916 is a common and widely distributed nematode of fishes in eastern North America. It occurs from Massachusetts
(Sindermann, 1953) westward through the Great Lakes drainage to South Dakota (Hugghins, 1959) and south to
Oklahoma (McDaniel, 1963). It has not been reported west of the Mississippi drainage nor farther north than north west Ontario. The original description is based on female specimens taken from Pomoxis nigromaculatus and
Morone chrysops at Fairport, Iowa. Since that time, C. oxycephalus has been reported from 4 8 species of fishes which are distributed over 32 genera and 17 families. In addition to those fishes listed as hosts for this nematode by Hoffman (1967), we add the following four species from western Lake Erie: Dorosoma cepedianum, Alosa pseudo- harengus, Osmerus mordax and Notropis spilopterus.
Although C . oxycephalus has been collected and identi fied frequently in eastern North America since its description, the male has never been described. This species has been separated from C. ancvlodirus Ward and
20 21
Magath, 1916 the only other indigenous species of
Camallanus described from North American freshwater fishes,
by the orientation of the buccal capsule and esophageal
dimensions of the female. Ward (1918) constructed a key
using the head orientation and vulvar position to dis
criminate between these two species and this has been the
basis for identification of C. oxycephalus since that
time.
The nematodes used in this study were killed in hot
AFA and fixed in AFA for 2M- hours. They were preserved
in 10% glycerin alcohol, cleared and studied in glycerin.
Several en face views were studied in a mixture of gly
cerin jelly and agar. All measurements are in microns
unless otherwise stated.
Camallanus oxycephalus Ward and Magath, 1916
(Plate IV. Figs. 22-27)
Description
Camallanidae Railiet and Henry, 1915. Slender nematodes, widest in middle third of body and tapering
slightly toward tail. Living worms red in color. Head
straight, not bent ventrally. Oral opening elongate.
Buccal capsule divided into two sclerotized lateral valves with smooth longitudinal rib-like thickenings internally; inflation of valves forms sclerotized ring at junction of buccal capsule and esophagus. Two trident
shaped processes present, one dorsal, one ventral, at 22 junction of valves. Three pairs of simple circumoral papillae in outer circle; two pairs in inner circle located at dorsal and ventral ends of oral opening. Esophagus divided into anterior club-shaped muscular portion and posterior cylindrical glandular portion. Intestine straight. Anal lips slightly salient.
Male (10 specimens): Length 4.43mm - 5.20mm (average
4.57), width 120-184 (152). Cuticle with striations barely perceptible. Buccal capsule 9 6-112 (10 3) by 96-
107 (100); tridents 86-104 (94) in length. Muscular esophagus 360-422 (390) long; glandular esophagus 428-
530 (461) long. Nerve ring 168-210 (189) from anterior end. One testis reaching almost to glandular esophagus, then reflexed; reproductive tract with several swollen portions separated by constrictions. Tail 109-136 (121) long, rolled ventrally in mature specimens, ending bluntly without mucrones. Thin caudal alae supported by papillae. Eleven pairs of pedunculate papillae, 6 pairs preanal, 5 pairs postanal; first three pairs of postanal papillae arranged close together. Two spicules, unequal but similar; left spicule weakly sclerotized, right spicule heavily sclerotized, 146-166 (154) in length, no gubernaculum.
Female (10 specimens): Length 15.9 3mm - 25.05mm
(18.18mm); width 206-282 (245). Cuticle with striations barely perceptible. Buccal capsule 128-142 (137) by 136-
165 (151); tridents 134-144 (138) in length. Muscular
esophagus 483-666 (569) long; glandular esophagus 558-748
(652) long. Nerve ring 22 2-300 (262) from anterior end.
Vulva 2.24mm - 3.11mm (2.69) from tip of tail, lips
slightly salient. Vagina very muscular, directed post eriorly. One ovary reaching to level of muscular esopha gus then reflexing; posterior branch of uterus reaching end ot tail, ending blindly in highly muscular sac. Tail
1.5 3mm - 2.21mm (1.87) long, bluntly rounded without mucrones. Ovoviviparous; larvae 629-645 (635) long.
Host: Morone chrysops
Location: Large intestine, rectum
Locality: Lake Erie off Buckeye Point, South Bass Island, Put-In-Bay Twp., Ottawa Co., Ohio
Specimens deposited: USNM Helm. Coll. No. 72457
Discussion
The description of the female of C. oxycephalus by
Ward and Magath (1916) is incomplete. Only the body length and vulvar position as given by Ward and Magath are useful for comparison. The vulva was described as being, "located at the anterior margin of the middle third of the body." My investigation of this character shows that the vulva is situated -much farther posterior, close to the anus (714-918 from the anus). This 24 discrepancy, which Tornquist (19 31) was unable to resolve in his review, cannot be merely ascribed to allometric growth. I examined immature female specimens and the vulva is in approximately the same position, proportion ally, as it is in gravid adults. This position is con sistent in the 1200 female worms examined. Ward and
Magath indicated that females reached 25mm in length, but failed to mention if these worms contained larvae or embryos. My measurements are based upon gravid females containing embryos and larvae and the maximum is con sistent with the original description. Despite the difference in vulvar position, which is an important taxonomic character in this group, we elect to retain our material in the species C. oxycephalus. The absence of a male description and the few good female characters given by Ward and Magath seem to justify this.
Camallanus oxycephalus can easily be separated from
C. ancylodirus Ward and Magath, 1916 although a complete description of the latter is lacking. The head is bent ventrally in C. ancylodirus and the males reach a length of 15mm, which is three times the maximum male length of
C. oxycephalus. Two European species of Camallanus have been reported just once from North American fishes,
(Meyer, 195 4; Maine). Camallanus oxycephalus can be differentiated from both of these species by the number and arrangement of the papillae on the male tails. Camallanus lacustris (Zoega, 1776) posses 13 pairs of caudal papillae. The males of this species reach a maximum length of 2.28mm (Moravec, 1969). Females of C. lacustris reach a maximum length of 7.0 8mm and possess a vulva with two highly elevated lips situated in the middle of the body. The males of C. truncatus (Rudolphi,
181M0 possess 12 pairs of caudal papillae which are arranged differently than on C. oxycephalus. In addition the tridents on both males and females of C. truncatus are very long, reaching more than half way to the nerve ring. THE LIFE HISTORY OF CAMALLANUS OXYCEPHALUS
Females are often seen protruding from the anus of fish. These worms are ovoviviparous. When fully gravid, females placed in lake water rupture and release between
7,000 and 10,000 infective first stage larvae (L1 's) into the plankton.
Description of 1st Stage Larva (Plate I, Figs. 5 and 6)
Slender nematodes: Length 629-645 (Average 635), width 15-17 (16). Cuticle thin with very fine circum ferential striations. Anterior end rounded with minute dorsal spine; stoma very narrow. Esophagus thin-walled
222-246 (235) long. Nerve ring 79-86 (82) from anterior end. Excretory pore indistinct. Intestine with patent sinuous lumen; walls one cell thick, heavily pigmented.
Tail long and attenuated, 160-170 (164), terminating without spines or mucrones. Anus opens through cuticle
465-481 (472) from anterior end. Rectal gland cells present. Cenital primordium composed of 6-8 cells.
Determination of Intermediate Host
Gravid female nematodes were obtained from White Bass and placed in filtered lake water and allowed to rupture.
26 27
Released first stage larvae were collected and exposed to a variety of arthropods to determine which serve as the intermediate host. Several individuals of each species were placed in stender dishes and large numbers of infective larvae were pipetted into the dish. The preparation was then observed under a dissecting micro scope to ascertain if the larvae were eaten. Ten individ uals of each species were isolated in separate dishes as controls and fed nothing. Table 2 summarizes these experiments.
TABLE 2. EXPERIMENTAL DETERMINATION OF THE INTERMEDIATE HOST
Potential Host Larvae Eaten Larvae Penetrated
Gammarus + -
Hyalella + -
Asellus + -
Cyclops + +
Diaptomus + +
Daphnia - -
Bosmina --
Chironomus + -
Cricotopus + -
Stenonema _—
Ostracoda 28
All of the arthropods, except the cladocerans and
the mayfly, were observed readily ingesting the infective
larvae. Penetration through the gut wall into the
hemocoel occurred only in the copepods. This occurred
within 2 hours after ingestion. Active larvae were
frequently observed moving about in the gut of amphipods
and midge larvae but penetration was never observed.
Larvae were allowed to remain with these arthropods for
several days and specimens were dissected periodically,
but no nematodes were found in any animals except copepods.
Controls were negative for the infection in all species.
Development of the 1st Stage Larva
Shortly after penetration into the hemocoel, the
anterior portion of the thin-walled esophagus thickens, becoming more distinct (Plate I, Fig. 6). The posterior
portion becomes lined with cells indistinguishable from
the intestinal cells. The intestinal wall becomes
thicker with more cells and the lumen becomes wider and
straightens out. The genital primordium remains un
changed .
The first molt occurs on the 4th day p.i. at 25°C and on the 5th day p.i. at 20°C. This molt is most
easily observed by examining the cuticle attached over the tail of the emerging 2nd stage larva (Plate II, Fig.
8). The stoma is very small and round and the minute dorsal spine is absent (Plate II, Figs. 7 and 8). The buccal cavity is a narrow tube connecting the stoma to the esophagus. The posterior portion of the esophagus is thickened and differentiated from the intestine but not yet separated from the anterior portion. Two large cells are visible at the base of the posterior esophagus. The tail becomes shorter and thicker, still ending in a point. Cuticular striations are slightly more pronounced than in the 1st stage larva.
Morphological changes occur in the anterior end during development. The buccal cavity lengthens, pushing the esophagus posteriorly and the numerous glandular cells present in the anterior end begin to form the buccal valves. The stoma changes from a circular opening to a dorso-ventral oval.
Description of the 2nd Stage Larva (Plate II, Figs. 7-9)
Living worms with distinct pale orange color.
Shorter and thicker than 1st stage larva; length H16-672
(55*0, width 22-30 (28K Stoma oval shaped. Buccal valves forming around anterior end of esophagus. Buccal cavity becoming enlarged by lateral inflation, pushing esophagus posteriorly. Esophagus 160-20 5 (186) in length; anterior portion becoming muscularized, lining of lumen thickened, posterior esophagus distinct, non- muscular, not separated from anterior portion. Nerve 30 ring 52-60 (54) from anterior end. Excretory pore * indistinct. Intestine filled with granular pigmented
material. Large rectal gland cells visible around rectum.
Genital primordium composed of 10-12 cells. Tail 74-168
(100) in length, shorter than in 1st stage, slightly
thicker, ending in point.
Development of the 3rd Stage Larva
The second molt occurs on the 7-8th day p.i. at 2 5°C and on the 10th day at 20°C. This molt is easily detected since the 3d stage tail with three mucrones can be seen under the molting L2 cuticle (Plate II, Fig. 10). The buccal capsule in the 3d stage larva begins to take on the appearance of the adult form (Plate II, Figs. 11, 12).
It consists of a large anterior chamber and a very small posterior one separated by a slightly sclerotized ring.
Because this capsule resembles the two part capsule found in adults of the genus Paracamallanus, it is often referred to as a "Paracamallanus type" capsule.
Description of the 3d Stage Larva from Copepods (Plate II,
Figs. 11, 12)
Living worms a pale orange color. Length 450-671
(569); width 36-47 (40). Cuticle finely striated. Stoma elongated dorso-ventrally, no circumoral papillae pres ent. Buccal capsule pale yellowish in color; divided into large anterior chamber and small posterior one; anterior chamber 22-2 3 in length, 21-24 (22) in width; formed by two lateral "shell-like" valves with internal oblique ridges; posterior chamber subcylindrical, 7-11
(9) in length, separated from anterior chamber by in completely sclerotized ring, opening directly into sclerotized esophageal cup. Numerous large, peri esophageal glandular cells behind buccal capsule. Esopha gus distinctly divided into two parts; anterior muscular portion 112-147 (135) in length, posterior glandular portion 81-109 (9 6) in length, with two large glandular cells at base. Nerve ring 50-61 (56) from anterior end.
Excretory pore indistinct. Intestine thick walled, filled with dense, granular, pigmented material, opening into thin walled rectum; large rectal gland cells surrounding rectum. Tail short, thick, 51-69 (58) in length; terminating in three mucrones. Genital primordium ventral, composed of 10-12 cells just anterior to anus.
The 3d stage larvae cease activity and lie coiled in the hemocoel, usually dorsal to the intestine. They are infective immediately and presumably remain so for the life of the copepod. Adult copepods experimentally infected have been observed with Lg's for up to 20 days with no apparent change in the nematode.
An experiment was set up to determine if there was a releaser to initiate escape activity by the L^. Table 3 summarizes this experiment. 32
TABLE 3. DETERMINATION OF THE RELEASER FOR ESCAPE ACTIVITY
Ringer's Solution Pepsin-HCL + Ringer's Bile + Ringer's
- Activity + Activity ++++ Activity
Copepods were placed in 1 ml of each solution on separate depression slides. Copepods died quickly in each solution. Larvae remained coiled and motionless in
Ringer's for several hours. The pepsin-HCL solution pro duced some larval activity after 35 minutes and continued for 3 hours, but the worms remained coiled. The bile solution caused larval activity to begin within 5-10 minutes. Larvae uncoiled and moved about so violently that it caused the flexing of the entire dead copepod body. These worms moved throughout the body pushing their heads into appendages and lashing vigorously about the hemocoel. No larvae were observed escaping however although this activity continued for 3 hours.
Young of the year White Bass , Yellow Perch and Small
Mouth Bass and adult Spot-fin Shiners were..collected-- prior to the dispersal period for C. oxycephalus from
Sandusky Bay and maintained in the laboratory holding tanks and acquaira. Approximately 20 specimens of each species were set aside as control fish and an additional 33
20 were dissected to establish that the experimental populations were free of the infection. Experimental fish were anesthetized with Quinaldine and infected copepods were introduced directly into the stomach with a stomach tube. Fish were autopsied after infection to study the development of the worms. All infected fish contained nematodes in various stages of development. All control fish dissected were free of the infection.
Freshly hatched Spot-tail Shiner fry (Notropis hudsonius) were collected from the lake by dip net and a sample of 20 were dissected to establish absence of the worm. These fish were exposed to infected copepods in large finger bowls and allowed to feed on them for three days. A sample of ten fry was removed and dissected and found to be infected with developing 3d stage larvae in the small intestine. Ten Yellow Perch were withdrawn from the uninfected laboratory population divided into two lots of five fish each and placed in separate acquaria. The spot-tail fry experimentally infected with Camallanus was fed to the first lot while the second lot was kept as a control. All of the fish were sacri ficed after 5 days. Four of the five perch in the first lot contained developing 3d stage larvae and all controls were negative for the infection. 34
Description of the 3d Stage Larva from Fish. (Plate III,
Figs. 13-14)
Living worms bright orange in color. Length .6 40-
1.214mm (.963), width 37-45 (40). Cuticle finely striated.
Buccal capsule deep bronze in color, divided into two chambers; total length 37-4 3 (38), width 29-37 (32); buccal valves of 4th stage larva visible, forming around
3d stage capsule. Anterior end of worm filled with numerous glandular cells. Nerve ring 85-90 (86) from anterior end. Excretory pore indistinct. Esophagus divided into anterior muscular portion and posterior glandular portion; muscular esophagus 150-194 (166) in length, glandular esophagus 117-160 (133) in length.
Intestine filled with (pigmented) granular material.
Large rectal gland cells visible around rectum. Tail short, thick 62-88 (73) long, terminating in three mucrones. Genital primordium proliferating anteriorly and posteriorly.
The third molt occurs on the 9-10th day after entry into the fish at 26°C and on the 12-13th day p.i. at 23-
24°C. This molt, like the second one, is easily observed since the mucronate tail of the 4th stage larva can be seen under the molting L^ tail (Plate III, Fig. 14). The most striking changes occur in the buccal capsule which now closely resembles the adult capsule. Circumoral papillae can be seen in the en face view (Plate III, Fig. 35
16). There are two pair of these in the inner circle,
located at the dorsal and ventral regions of the slit
like opening, and three pair in the outer circle. The only other major change from the copepod besides an
increase in length is an increase in the development of the reproductive tract (Plate III, Fig. 18).
Description of the 4th Stage Larva (Plate III, Figs. 15-
19)
Living worms bright orange in color. Length 1.241-
2.559mm, width 56-85. Cuticle finely striated. Stoma a dorsoventral slit. Five pairs of circumoral papillae, 3 in outer circle, 2 in inner circle. Buccal capsule completely sclerotized, deep bronze in color. Length
51-67, width 46-66. Formed by two lateral "shell-like" valves; internal ridges longitudinal. Esophagus divided into anterior muscular portion and posterior glandular portion; muscular esophagus 211-33 3 in length, glandular esophagus 211-306 long. Nerve ring 86-9 3 from anterior end. Excretory pore opening ventrally near middle of muscular esophagus. Intestine thick walled, lumen filled with dense granular pigmented material. Large rectal gland cells present. Tail short in pre-male forms, longer in pre-female forms, 82-204 in length, terminating in three mucrones smaller than L^'s. Reproductive tracts developing, vagina and vulva forming in pre-females, but 36
not patent.
Because the final molts occur at different times for
the male and female worms, there is a difference in the
maximum length obtained by pre-male and pre-female 4th
stage larvae. The pre-males reach a maximum length of
about 1.900mm and molt on the 17-18th day p.i. at 26°C.
The pre-female 1s, however, reach about 2.600mm in
length and do not molt until the 24th day p.i. These
lengths represent about 40% and 10% of the final body
length for males and females respectively. Text Fig. 1
graphically illustrates the growth of the fish parasitic
stages of C. oxycephalus and the molting times. Growth rates for the and L,^ are similar and recently molted males increase their rate of growth only slightly to about .0 875mm/day. Female L^'s increase their rate of growth about 16 days p.i. and at 20 days cease growing until the final molt when their rate of growth increases
greatly. This rate within the first 4 days after the last molt rises to .125mm/day and by the 8th day, the rate is .273mm/day.
Adult worms can readily be distinguished from larvae by the presence of dorsal and ventral trident shaped structures around the buccal capsule (Plate III, Figs. 19-
20). In addition to this, the mucrones on the tail are lost with the final molt and the tail ends bluntly in the female. Spicules and caudal papillae are visible in the 37
E 3-0
at
IK 1.0
Adults
10 3 0 3 0 Days
Text Fig. 1, Growth of C. oxycephalus in White Bass at 26°C. Vertical lines indicate range of body length. 38 male L ^ ’s during the final molt (Plate III, Fig. 15).
Because of the susceptibility of young White Bass to ichthyopthiriasis, gyrodactyliasis and numerous bacterial and fungal diseases, maintenance in the laboratory is difficult. Heavy mortality occurred periodically within the experimental populations and thus prevented me from studying the development during the prepatent period.
Summary of the Experimental Life History
1. Ovoviviparous females exposed to lake water when fully gravid rupture and release from 7*000 - 10,000 infective first stage larvae.
2. Active 1st stage larvae are consumed by a variety of aquatic arthropods, but penetration through the gut wall into the hemocoel and further development occurs only in copepods.
3. Little observable development occurs until the
1st molt, which occurs on the 4th day p.i. at 2 5°C.
4. Many morphological changes begin to take place
in the 2nd stage larva (L2 ). Most notably, the buccal capsule begins to form.
5. The second molt occurs between the 7th and 8th day p.i. at 25°C.
6. Third stage larvae are distinct. The buccal capsule is divided into two chambers, and the tail terminates in three mucrones. The living worm is bright orange in color. 39
7. Escape activity is partially released by Pepsin-
HCL but violent activity is produced by immersion in
fish bile.
8. Infection may be produced in large fish either
by directly ingesting the infected copepod or by consuming
a smaller fish previously infected from copepods.
9. The third molt occurs between the 9-10th day
after introduction into the fish. The 4th stage larva
has a one piece buccal capsule, circumoral papillae and
three mucrones on the tail.
10. The final molt occurs on the 18th day p.i. for
males and the 24th day p.i. for females. Adult nematodes
have dorsal and ventral tridents associated with the
buccal capsule and a blunt tail without mucrones.
11. The growth rate for males remains constant, but
recently molted female worms accelerate their rate of
growth rapidly.
Discussion of the Life History
The experimental determination of the life history of
Camallanus oxycephalus revealed several significant
features. These features allowed an initial investiga
tion of the population ecology of the parasite and the
development of a simple model of this host-parasite system which might apply to other systems.
Other life history studies of camallanids revealed 40 that copepods served as intermediate hosts, and the possibility of a copepod being in the life history of C. oxycephalus was investigated first. However, alternate intermediate hosts must be known in order to develop a model. The establishment of the copepods as inter mediate hosts was important. Equally significant was the failure of other aquatic arthropods to become infected.
Moravec (19 69a) investigated alternate intermediate hosts for C. lacustris, because Leuckart (1876) and
Linstow (19 09) allegedly observed C. lacustris larvae in Asellus and Agrion respectively. All attempts to infect arthropods other than copepods failed. Whether or not these two species are representative of all other camallanids is not certain, but it seems likely that most camallanids use copepods as intermediate hosts. It is clear that if no alternate intermediate hosts are available, the dynamics of parasite movement through the system is a function of nematode-copepod-fish inter action and ancillary trophic relationships between fish and other aquatic organisms can be ignored.
Two molts were observed to occur within the copepod, which is similar to the pattern for C. lacustris and P. sweeti (Moravec, 19 69a, and Moorthy, 1938). Li (19 35) and Pereira et. al (19 36) observed only one molt in the copepod for the species they studied and it might be inferred that fundamental differences exist in the 41 development sequences of various camallanids. However, molts are frequently difficult to see in the early stages of development and can be easily overlooked. I have suggested during the review of the life history informa tion that I believe the first molt was overlooked in both these studies. Comparison of the larval stages from these studies with those of C. oxycephalus and C. lacustris and those studied by Moorthy and Li strongly support my conclusion.
Development depends upon temperature and it is difficult to compare molting times for C. oxycephalus with those in other studies. However, Table 4 reveals that the time required to reach the infective 3d stage larva is short, less than two weeks in all cases. This is significant because copepods have relatively short life spans, and it is advantageous to reduce the develop ment time in hosts and maximize the exposure time to the final host.
A comparison of the larval stages, L-^- L3, between
C. oxycephalus and C. lacustris revealed several similar ities in basic morphology. Except for the body sizes, the gross morphological features distinguishing each larval stage were the same. The first stage larva of
C. lacustris was slightly smaller but grew during develop ment and produced L^'s larger than those of C. oxycephalus. 42
TABLE 4. OBSERVED MOLTING SEQUENCE FOR SOME OTHER CAMALLANIDS
Species Time of M^ Time of M 2 Temperature
P. sweeti 24-36 hrs. 5-6 days 90-10 2°F
8-12 days 55-70°F
C. lacustris 4-5 days 10-11 days 20-25°C 0 CM 0 C. oxycephalus 5 days 10 days 0
4 days 7-8 days 25°C
S. fulvidraconis - 8-9 days -
The induction of escape activity by fish bile suggested that escape of the L^ occurs in the stomach.
The L3's were found actively moving about free in the lumen of the stomach (six hours after introduction of infected copepods). Moorthy (19 38) demonstrated that bile activated P. sweeti larvae. His experiments, and mine, showed larvae were greatly excited by bile, but failed to escape from the copepod hemocoel. Moorthy also noted a slight activation by HCL. It seems likely that activity is initiated in the stomach in the presence of
Pepsin-HCL. The copepod exoskeleton, during this period, is softened if small amounts of bile are regurgitated into the pylorus of the fish, activity is increased. This activity coupled with the partially digested chiti-
nous exoskeleton results in the release of the L3 in the
fish stomach. If no bile is present in the pyloric
stomach, release is probably delayed until the copepod
body reaches the duodenum. Escape, then, depends upon
activation of the larvae and the degree of digestion of
the copepod. This two stage process could easily be
affected by variations in the quality of enzymes and
bile found in different species of fish. Such subtle
differences could be produced by variations in the
genome among different fish species. The efficiency of
escape and survival of the larval stages may be related
to these subtle differences. The ability to escape from
the intermediate host (transfer environments) with a
high efficiency is an important consideration in any host-parasite system and becomes in part an expression of host specialization. Release of highly specialized
parasites is accomplished in only one host. Release of
generalized species can be effected in several hosts, but there is probably an optimal host, since it is un
likely that reaction to a wide variety in the quality of
stimuli would be equal.
A significant finding in this experimental study of the life history of (). oxycephalus was the elucidation of the transport host mechanism or alternate pathway to the final host. The life cycle may be completed by consumption of the infected copepod by the final host. This was the
shortest and seemingly most efficient route. However, frequently in helminth life history studies an additional host may occur on a trophic level between the inter mediate and final host. This host feeds upon the inter mediate host which may not be a principal food item of the final host and so concentrates the infective agents.
When this alternate host is consumed by the final host the life cycle is completed. When this host is optional and no development of the parasite occurs, it is called a "transport host". The ability of helminth parasites to utilize transport hosts has three distinct advantages.
First, it may increase the exposure time of the infective agents beyond the biological longevity of the intermediate host. Hence, the parasite is distributed through a longer period of time resulting in an increase in the probability of contact with the final host. Second, and perhaps most important, the infective agent is distributed in space in such a way that the likelihood of final host contact is maximized. This is particularly true if the transport host is a principal food item of the final host. Third, the transport host serves as a concentrating mechanism, transferring several worms with each contact instead of one or two. Parasites, like other biological variables tend to be concentrated in the food chain.
The distribution in each host population is apt to be slightly different with higher levels of parasites in the higher levels of the chain. This last aspect is critically important for dioecious helminths where popu lation levels are low and the likelihood of mating and reproduction are functions of parasite density.
My experiments show that following introduction into some forage fish the nematode grows, molts and continues development in the same way it does in White
Bass, Yellow Perch and Small Mouth Bass. The life history can be completed in fish such as the Spot-fin shiner (Notropis spilopterus). In the Gizzard Shad and probably other species, the worms molt and development continues through the 4th stage larva but the final molt does not occur and the larvae die. No adult C. oxycephalus was found in Gizzard Shad. These results are similar to Moravec1s (1969b).
Similar patterns of development in the 4th stage larvae occur in C. oxycephalus and C. lacustris. The male in both of these species molts before the female
. There is a disproportionate amount of time between the two molting patterns not attributed solely to the difference in experimental temperatures. Moravec noted that the males molted between 35 days p.i. (20-25°C) but as late as 69 days p.i. Camallanus oxycephalus, in sharp contrast to this molts on the 17-18th day p.i.
Molting was not spread out over a long period of time. The female C. lacustris molts 6 5 days p.i. or almost twice the time after infection that the male does.
Female C. oxycephalus on the other hand undergo their final molt between 2U and 25 days p.i., only about one week after the males.
I was not able to determine the length of the prepatent period due to mortality in the experimental fish population. A comparison of this period between the two species might be interesting, especially since the female C. lacustris molts considerably later and is patent for larvae only 30 days after this molt. Without comparative studies of the two species at the same temperature, conclusions concerning their final develop ment are speculative. It does, however, appear that there are some fundamental differences in the terminal development sequence between these species. STUDIES ON THE BIOLOGY OF THE 1ST STAGE LARVAE
A series of experiments was conducted to investi gate the affect of age and temperature on several important processes of the 1st stage larvae. These processes are related to the ability of the infective larva to penetrate the intermediate host and so produce third stage larvae which may invade the final host.
Temperatures selected were the extreme summer lake water temperatures likely to be encountered by the L^'s. A life table and survivorship curve were constructed for each temperature. When survivorship had been studied, fresh larvae were fed to copepods to determine the penetration efficiency (Pe ) at 0 days age. Larvae were aged in lake water at 20° and 25°C and fed to copepods every 24-48 hours to determine how the P changed with age. An attempt was also made to quantify the activity and movements of the L^ as related to age.
Survivorship of the 1st Stage Larva
Life tables were constructed from experiments to determine the time the dispersal agents remain alive at
20° and 25°C (Tables 5 and 6). The survivorship curve
47 plotted was from the life table data (Text Figure 2). The
general form of both curves is similar. However, it is
clear that survival is favored considerably at the lower
end of the temperature range. Death rates per 1000 (qx)
were essentially zero for 7-8 days at both temperatures,
indicating that initial survival was the same over the
entire temperature range. Following this period,
survival at 25°C dropped sharply. The death rate in
creased rapidly on the 16th day and survivorship termi
nated at 24 days. The death rate at 2 0°C, however,
remained at a constant, low (x = 12.4/10 00) rate for
approximately two weeks, resulting in a straight sur
vivorship curve between one and three weeks. Death rate
after three weeks rose to over 100/1000 individuals
around the 27-30 day and survival terminates on the 40th
day.
Infection of Copepods
Infection experiments with copepods were not species
specific, rather copepods were divided into calanoids
and cyclopoids. All calanoids were of the genus Diaptomus and cyclopoids were Cyclops (principally C. vernalis and
C . bicuspidatus). Larvae 0 days old were exposed to
copepods at the concentration of 10 L^'s to one Cyclops
in 2 ml of water for 24 hours. Table 7 shows a great
discrepancy in the percent of the exposed larvae which 49 TABLE 5 . LIFE TABLE FOR C. OXYCEPHALUS 1ST STAGE LARVAE AT 20°C.
Age Interval in Days dx Xx ^x
0 1 0 1000 0 1 2 0 1000 0 2 — 3 8 1000 8.4 3 — 4 8 992 8.5 4 — 5 0 984 0 5 - 6 0 984 0 6 - 7 0 984 0 7 — 8 0 984 0 8 - 9 8 984 8.6 9 10 8 976 8.7 10 — 11 8 968 8.8 11 — 12 21 960 22.1 12 — 13 13 939 13.6 13 - 14 4 926 4.6 14 - 15 12 922 13,8 15 - 16 21 910 23.4 16 — 17 13 889 14.3 17 - 18 8 876 9.7 18 - 19 8 868 9.8 19 - 20 13 860 14.9 20 — 21 8 847 10.1 21 — 22 47 839 56.1 22 - 23 26 792 32 .4 23 — 24 —- - 24 - 25 56 766 72.6 25 - 26 —- - 26 — 27 73 710 102.4 27 - 28 52 637 82.0 28 - 29 -- - 29 - 30 - - - 30 — 31 171 585 292 .6 31 _ 32 124 414 298 .8 32 - 33 33 290 114.7 33 — 34 43 257 166 .6 34 _ 35 38 214 177.7 35 - 36 52 176 297.3 36 — 37 57 124 461.5 37 - 38 28 67 428 .5 38 - 39 29 39 750 .0 39 — 40 10 10 1000 40 —•
N o . of deaths during age interval ; lx = No. dx = survivors from last age interval; q = death rate/1000 A individuals. 50
TABLE 6. LIFE TABLE FOR C. OXYCEPHALUS 1ST STAGE LARVAE AT 25°C.
Age Interval in Days dx Xx <*x
0 - 1 0 1000 0 1 - 2 14 1000 14.2 2 - 3 0 986 0 3 - 4 0 986 0 4 - 5 0 986 0 5 - 6 0 986 0 6 - 7 0 986 0 7 - 8 0 986 0 8 - 9 7 986 7.2 9 - 1 0 35 979 36 .4 10 - 11 57 944 60 .6 11 - 12 35 887 39 .3 12 - 13 21 852 24.6 13 - 14 49 831 58.8 14 - 15 49 782 62 .5 15 - 16 112 733 152. 3 16 - 17 55 621 89 .8 17 - 18 147 566 259 .3 18 - 19 140 419 333. 3 19 - 20 104 279 375 .0 20 - 21 56 175 320 .0 21 - 22 46 119 384.6 22 - 23 73 73 1000 23 - 24
d = No. of deaths during age interval; 1 = No. of A A survivors from last age interval; qx = death rate/
1000 individuals. 51 were consumed by calanoids and cyclopoids. Although the
data for Diaptomus were insufficient to establish an
efficiency of penetration, the propensity of Diaptomus for Carnal1anus larvae was low and virtually eliminated them from consideration as an intermediate host in Lake
Erie. The efficiency of penetration (Pe) in Cyclops was high (0.709) especially when compared to Li's (19 35) studies on —S. fulvidraconis —--- (P e = .080) and Muller's (1971) work on Dracunculus (P = .375).
TABLE 7. INFECTION OF COPEPODS BY 1ST STAGE LARVAE
No. Lj No. L! No. Li Copepod Exposed Eaten Penetrated
Cyclops 800 508 (.635) 360
P e =.709 Diaptomus 108 1 (.009) 0
Using a Pg of 0.709 as the infection efficiency measured at 0 days age, it was possible to estimate how efficiency changed with larval age under two different temperatures. A significant difference in the decrease of Pe under the two different temperatures was found
(Text Figure 3). Both expressions were fitted to logrith- mic curves. Analysis of variance of the regressions were 1004 \X n\
«00 L,
400-
300-
to 30 30 40 Days
Text Fig. 2. Survivorship Curve of at 20° and 25°C. 53 highly significant in both cases (F = 19.17 > a . 01 = 8.86 for 25°C; F = 14.78 > a .01 = 0.65 for 20°C), The Pe at
25°C begins to decline on the second day and approaches zero by the 16-17 day. At 20°C, however, Pg remained near .709 for five days and was still above .200 on the
28th day.
Activity of the 1st Stage Larvae
First stage larvae exhibited a characteristic "S"- shaped wiggling when free in the water. When in contact with a substrate, these worms "attached" by their tails.
Holding the anterior two-thirds of the body in a broad
"C", they flailed it back and forth by alternate con tractions of the muscle quadrants on either side of the tail. Such behavior can be quantified by allowing larvae to settle to the bottom of a small petri dish and counting the number of contraction cycles in 30 individ uals over a set period of time. Time, unfortunately permitted this measurement to be made at 2 5°C only.
Both the basal and excititory activity rates de clined with age in a linear fashion and the slope of the two lines was almost identical (Text Figure 4). No basal activity was observed after 16 days although activity may be induced by stimulation until 19 days. et i. BsladEcttr ciiyRts of Rates Activity Excititory and . Basal U Fig. Text
Contractions / Min. of Age and (P_) Efficiency Penetration 3. Fig. Text ISO-4 *.*o- 100- - 0 5 ao- o .a 1 .30- . 0 - t 25°C. at s 10 Days ays D 10 ao o uUHay t ta ta ary H U iu ■o Sat* l i « l >o is 30 40 ao
5U Development of Larval Stages
The time required to reach the infective 3d stage
larva was studied at three different temperatures.
Development was most rapid at the higher temperatures
as might be expected (Text Figure 5). Significantly,
development was rapid in the normal summer temperature
range but below 20°C, up to 25 days were required for
development.
Discussion of the Studies on the Biology of the L-^
The ability to survive, move, infect the next host
and develop are all vitally important to dispersal.
Together they can contribute to a meaningful under
standing of the population biology of the parasite in
a particular environmental system, when studied in
relation to the environmental parameters likely to be
experienced by the organism.
The survivorship curves showed that at normal
summer lake water temperatures, infective 1st stage
larvae survived for 24-40 days. Initial survival was
unrelated to the temperature extremes as shown by the
low mortality rates for both temperatures during the first week. Thus effect of tepiperature was delayed, resulting in a maximum survival for approximately one week throughout the entire normal summer temperature range. The adaptive significance is easily understood. w*c «> 3J
m
2 i
5 10 15 20 25 Time in Days
Text Fig. 5. Effect of Temperature on the Development of Larvae within the Copepod 57
Slight flucuations in water temperature have a minimal
effect upon early survival.
The difference in consumption of L^’s by cyclopoids
and calanoids was interesting, particularly in Lake Erie where cyclopoids far outnumbered calanoids in the summer
plankton. Pennak (1953) noted that cyclopoids possessed mouth parts modified for seizing and biting and fed upon
unicellular plants and animals while calanoids were
filter feeders. This difference might easily explain the
low numbers of larvae consumed by calanoids in the
experiments. Calanoids must occasionally ingest the L^’s because on two occasions I have seen Diaptomus with 3d
stage larvae Camallanus. However, the low consumption rate coupled with the relatively small portion of the copepod community they represent essentially eliminated the calanoids from consideration as intermediate hosts.
A significant find was the extremely high efficiency of penetration (Pe) found for freshly liberated 1st
stage larvae. This was a remarkable value when compared to the values known for fulvidraconis and Dracunculus and must be considered as an important factor in the abundance of C. oxycephalus in Lake Erie. The effect of age upon Pe was clearly related to temperature. The ability to infect the copepod was lost more quickly at higher temperature. The magnitude of the difference in the decrease of Pe between the two temperatures was greater than expected at first glance. At 25°C, the P value equalled 0.10 in 14 days. Although the experiments were completed only to 28 days at 20°C, the efficiency had still not declined to the 0.10 level. Thus, the
P£ remained above this value at least twice as long at
20° than at 25°. This efficiency is important from the standpoint of the maintenance of a reservoir of infective larvae in the environment. Perhaps differences in efficiencies are more important when the larvae are young. The P at 25°C began to decline after 2 days reaching a value of .50 by the fourth day and .27 by the eighth day. The P£ at 20° was still around .64 on the eighth day. The significance of these differences is clearer if we construct an additional table.
If the survivorship (1 ) is multiplied by the age specific efficiency (Pe) an estimate of the number of L^1 surviving to a specific age which will be converted into
LQ’s can be derived. This value, labelled m , changed w X with time very differently at 20° and 25°C. Although there is no difference in survivorship during the first week, a distinct difference in the number of larvae potentially converted to L^’s occurred at the two temperatures (Tables 8 and 9)* The potential number of
L^'s which can be converted into L^’s after one week at
25°C is 266/1000, while the same interval at 20°C allowed
620/1000. Unquestionably the affect of temperature on 59
TABLE 8. POTENTIAL PRODUCTION OF 3d STAGE LARVAE FROM L ± SURVIVORSHIP AT 25°C.
Age Interval P in Days e mx
0 - 1 1000 .709 709 1 - 2 1000 .709 709 2 - 3 986 .590 582 3 - 4 986 .510 503 4 - 5 986 .440 434 5 - 6 986 .370 365 6 - 7 986 .320 316 7 - 8 986 .270 266 8 - 9 986 .230 227 9 - 10 • 979 .200 196 10 - 11 944 .170 160 11 - 12 887 .150 133 12 - 13 852 .130 111 13 - 14 831 .100 83 14 - 15 782 .090 70 15 - 16 733 .068 50 16 - 17 621 .060 37 17 - 18 566 18 - 19 419 19 - 20 279 20 - 21 175 21 - 22 119 22 - 23 73 23 - 24
m = No. larvae surviving to age x which can potentially be converted into L^. 60
TABLE 9. POTENTIAL PRODUCTION OF 3d STAGE LARVAE FROM Lx SURVIVORSHIP AT 20°C.
Age Interval m in Days Xx Pe X
0 - 1 1000 .709 709 1 - 2 1000 .709 709 2 - 3 1000 .709 709 3 - 4 992 .709 709 4 - 5 984 .709 709 5 - 6 984 .709 709 6 - 7 984 .671 659 7 - 8 984 .630 620 8 - 9 984 .600 590 9 - 10 976 .573 556 10 - 11 968 .544 523 11 - 12 960 .511 490 12 - 13 939 .480 451 13 - 14 926 .441 407 14 - 15 922 .420 387 15 - 16 910 .390 355 16 - 17 889 .370 329 17 - 18 876 . 360 315 18 - 19 868 . 340 295 19 - 20 860 .320 275 20 - 21 847 .300 254 21 - 22 839 .290 243 22 - 23 792 .270 214 23 - 24 - .260 - 24 - 25 766 .240 199 25 - 26 — .230 - 26 - 27 710 .220 156 27 - 28 637 .210 134 28 - 29
mx = No. larvae surviving to age x which can potentially be converted into Lg. 61 the L-^ population was more important than was initially thought from observing the survivorship curves. These values when compared to similar values for related species may be useful as an indicator of relative fitness to different environments.
The ability of the infective larvae to move is re lated to the ability to penetrate the gut wall of the copepod. Larvae were observed inside the copepod gut and were very active. The result of this activity was that the head of the larva was poked through the gut wall and the worm wiggled'through into the hemocoel. Obvi ously if the larvae cannot move, the gut wall cannot be perforated and migration to the copepod hemocoel and hence development cannot occur. Active movement of the free- living L1 was also used as a criterion of survivorship.
The interrelation of these two functions was evident when the data for 2 5°C was examined. There was no activity or penetration after 17 days. Although larvae survive for several more days, the larvae twitch but there are no whole body contractions. Quantifying this activity, then, may provide an insight into the nature of this relationship.
Both basal and excititory activity rates declined in a linear fashion, suggesting that the worms do not conserve energy to maintain a high excititory rate. This suggests that a high excititory rate is apparently not of 62 great selective value. This poses somewhat of an enigma since logic dictates that the greater the movement, the more likely penetration will occur, if penetration is purely a mechanical process. The fact that Pe declined in a non-linear relationship with age suggests that penetration is not solely dependent upon movement. The more rapid logrithmic decay of Pg probably represents a degradation of some physiological conditions, perhaps enzymatic secretory material, unrelated to activity.
Since the larvae moved more or less continuously, ex pending energy constantly as indicated by Text Fig. 4, there is presumably some value in this.
Active 1st stage larvae must be consumed before development occurs. If the worms can act as a bait by moving, they may increase the likelihood of being con sumed and thus increase the probability of completing the life cycle. Whether or not cyclopoids can actually see images with the eye is uncertain, but they can surely detect differences in light intensity and so they may respond to movement. Hungry copepods quickly found and ingested single, active 1s in 8ml stendor dishes. Even if larvae cannot be seen, copepods should be capable of discriminating moving prey from non-moving prey when grasped. To test this assumption, I analyzed the relation ship between the number of larvae consumed by the experi mental copepods and the mean activity of the larvae as it declined from 0 days to 15 days of age (Text Fig. 6).
The correlation coefficient was highly significant (F =
8.0 6 > 8 .02).
When the larvae were dead and showed no movement, copepods consumed slightly more than 50% of the worms exposed. This could be expected since cyclopoids are alleged to be scavengers. However, the relationship indicates that copepods "prefer" actively moving larvae.
The result is that active worms, which are younger and therefore possess a higher Pe , are more likely to be consumed than older worms with a low probability of penetrating the gut wall and developing into L^'s. Text Figure 6. Relationship Between Larval Activity and Activity Larval Between Relationship 6. Figure Text
900 O /1000 Consumption by Cyclopoid Copepods. Cyclopoid by Consumption 40 otatos/Min. / Contractions to 120 64 ECOLOGICAL STUDIES OF CAMALLANUS OXYCEPHALUS
IN WESTERN LAKE ERIE
The Western Lake Erie Ecosystem
Lake Erie, the shallowest, southernmost and warmest of the Great Lakes, is geologically divided into three basins. The western basin, comprising only 13% of the total surface area and 5% of the volume, is the smallest of the three basins (Hartman, 1972). It is by far the shallowest portion of the lake with a mean depth of only
7.4 meters and a maximum depth of 20.4 meters. There are many reefs, shoals and islands in the area and it is considered to be an important fish-spawning ground and nursery (Hartman, 1972). Because of the latitude (42° t 15 N), there is a marked seasonal flucuation in temp erature. Air temperature in July averages 21-24°C and in February -5 to -2°C. The western basin generally freezes over in mid-December with water temperatures near
1°C. The ice thaws around the end of March and water temperature begins to rise, reaching near 10°C by May 1.
The temperature by June is near 15°C and reaches as high as 24-26°C by early August before gradually cooling until the ice cover in December. Because of the shallowness of the basin wind and water currents tend to keep the water
65 66 isothermal in the summer.
The entire lake but especially the western end harbors a rich and diversified fish fauna. Van Meter and
Trautman (19 70) listed 138 species as having been reported from Lake Erie. Studies on the abundance of plankton by
Chandler (1940) and Davis (1968) revealed a large number of rotifers, cladocera and copepods.
Because of the seasonal flucuation of environmental parameters, population levels of copepods in the western basin change throughout the year. Chandler (1940) noted that cyclopoid copepod density remained low during autumn and winter, increased in May and reached a peak in late June and July. Davis (19 69) observed that the zooplankton in July consisted mostly of daphnids and copepods, while in October it was dominated by rotifers and small cladocerans with very few copepods. The most abundant species in 19 67 were Cyclops bicuspidatus and
C. vernalis, (Davis, 1968). Furthermore, diaptomids were distinctly less abundant than cyclopoids.
History of Camallanus oxycephalus in western Lake Erie
The first record of C. oxycephalus in Lake Erie was from 1927 (Bangham and Hunter, 1939). They reported 28 species of fish from nine families as host for this nematode. Bangham (1972) in a resurvey of the fish parasites done in 1957 reported C. oxycephalus from 26 67
Lake Ontario
It.CM* C.
I L a k e OetroilQ^^ 1S t.C la u
Lake Erie Erie Pa.
loledo
Cleveland
Text Figure 7, Lake Erie
ONTARIO D etroit i R iver MICHIGAN Point
0-
WESTERN LAKE ERIE
Maumee Bay
Toledo • ll.
h .
OHIO
Text Figure 8. The Western Basin of Lake Erie. Stars indicate Collection Sites 68 species of fish. These studies provide a basis for comparison of the frequency of occurrence with the present study. The two previous surveys were conducted during the summer and autumn. Although the present study spans
27 months, only the data for summer and autumn 1971 and
19 72 are utilized for comparison. All of the most com monly infected fish were sampled and compared except those species which have disappeared or decreased in abundance so much that collection of an adequate sample was not possible. To offset differences in the sample sizes of some fish among the three studies, some related species were pooled together and compared as a group.
For example, minnows, darters and sunfish were all compared as a group. Text Figures 9-12 show the relative infection frequencies in some fish among the three years and Table 10 summarizes the data. Fre quencies were tested with chi-square to determine whether a significant change had occurred.
These data indicated that the frequency of occur rence of C. oxycephalus in Lake Erie fish increased greatly since 1927. The fish most commonly infected in all years was the White bass, Morone chrysops. The inci dence remained the same between 1927 and 1957, but since then has increased almost 100%. In addition, there were indications that the intensity of infection has also risen. Bangham and Hunter did not keep precise records 69
I I W27 l.O-i 1957
1971
. 7 5 -
F - 5 0 - r f P
.2 5 — #I
2 k W. Bass F. Drum JY. Perch
Text Figure 9. Frequency Changes of C. oxycephalus in Lake Erie Fish. i I I W27 l.0- n I H 1957
1972 . 7 5 -
F .5 0 —
.25- D W.Crappie Bl.Crappie Rockbaaa
Text Figure 10. Frequency Changes of C . oxycephalus in Lake Erie Fish. 70
1.0
.75
F .5 0
.25
S. Mouth Sunlieh
Text Fig. 11. Frequency Changes of C. oxycephalus in Lake Erie Fish.
1 .0 - 1 F 11927
M l 1957
.75
F .50 —
.2 5 -
n _ F 7 i Minnow* Smelt Alewlfe Gizzard Shad
Text Fig. 12. Frequency Changes of C . oxycephalus in Lake Erie Fish. TABLE 10. COMPARISON OF FREQUENCY OF C. OXYCEPHALUS IN LAKE ERIE FISH
• 1927 1957 1971 Fish Species F N F NF N x2
Morone chrysops (Adult) .469 32 .472 53 .952 83 8.25**
M. chrysops (YOY) .220 9 - - .641 170
Aplodinotis grunniens .400 45 .143 88 .507 67 9.99**
A. grunniens.(YOY) ---- .500 300
Perea flavescens (Adult) .022 45 .054 93 .475 114 303.02**
P. flavescens (YOY) .000 15 - - .016 64
Pomoxis annularis .231 17 .396 53 .708 48 7.69**
P. nigromaculatus .111 9 .310 29 .730 37 8.87**
Ambloplites repestris .116 12 .107 75 .273 22 3.82
Leporais spp. .061 33 .194 144 .107 28 3.16
Micropterus dolomieui .125 80 .078 55 .375 40 13.29**
M salmoides .023 129 .175 40 - - • 11.70** TABLE 10. CONT’D. COMPARISON OF FREQUENCY OF C. OXYCEPHALUS IN LAKE ERIE FISH
1927 1957 1971 Fishr Species F N FNF N X2
Stizostedion spp. .104 48 .212 33 —- 1.62
Etheostoma/Percina spp. .161 93 .102 127 -- 1.48
Percopsis omiscomaycus . 369 69 .032 63 .077 13 11.29**
Ictalurus spp. .034 29 .026 39 .167 57 6.00
Notropis spp. .055 274 .017 287 .027 264 7.22
Osmerus mordax - - .000 61 .040 50
Dorosoma cepedianum -- .000 27 .533 360
Alosa pseudoharengus .000 14 .121 190
2 ** denotes significant X value. 73
of infection intensity in each fish. They did, however,
define three classes of intensity; 1-9, 10-49 and over 50
worms per fish. They noted that 82% of their adult White
bass contained less than 10 worms per fish and only 18%
carried 10-49. No data are available for 1957 but in
1971-72, the percentage of fish containing 1-9 worms had
dropped to 55%, while 45% carried over 10 worms. This
45% includes 4% with over 50 worms. The frequency has
significantly increased in young of the year as well.
The frequency in Freshwater drum has flucuated but was
high for 1971-72. No data for young of the year was
available from the previous surveys. The YOY and adult
portions of the population in 1971-72 have very similar
frequencies of occurrence. The increase of Camallanus
in perch is restricted to adult fish. Young of the year
perch harbor few worms. The two species of Crappies,
Pomoxis annularis and P. nigromaculatus, have undergone a great increase in the frequency of the nematode. This
increase is seemingly parallel in the two fish and was
evident between 1927 and 1957. Since 1957, however, the
frequency has risen to such an extent that Crappies are
now the second and third most commonly infected fish in the western end of the lake. The frequency values for
Ambloplites rupestris and the Lepomis spp. were not
significantly different among the three studies. The
data for Micropterus dolomieui and M. salmoides indicated 74 that the frequency has increased in both of these fish.
Current information for large mouth bass is lacking since
I was unable to collect them, but the 1927 to 19 57 in crease was significant. Insufficient data for walleyes and darters precluded comparison of the values among the three studies. Although the walleye sample was small
(12 fish) the frequency value was very high (.700) in dicating that further study of the walleye population is necessary. The only fish in which the frequency declined was the troutperch. The data show that this decline occurred between 19 2 7 and 1957. The value has remained essentially the same since 1957. The data for catfish indicated that the frequency of Camallanus has not increased.
The incidence of C. oxycephalus in planktivorous forage fish was both interesting and instructive. No change has occurred in the frequency in minnows among the studies. The 19 71-72 study, though, revealed that three additional species of forage fish, Smelt, Alewife and Gizzard shad, not previously reported with Camallanus, were infected. The latter two species have only recently been known from Lake Erie in large numbers. Gizzard shad very frequently infected.
Seventeen fish or groups were investigated and the frequency of infection with C. oxycephalus compared with the previous data. The occurrence of this nematode has increased significantly in 10 of these, remained unchanged
in 6 and decreased in only one. If the frequency of
infection values from Table 10 for each study are plotted
in sequence from the highest frequency to the lowest, a
curve is generated describing the distribution of the
nematode within the fish community. A comparison of
curves (Text Figure 13) indicated the nature of the
change in the occurrence of this parasite. The curves
for 1927 and 195 7 were very similar. No significant
difference between them was indicated by chi-square.
Although the occurrence of Camallanus in some fish (i.e.
Crappies and Troutperch) changed significantly between
- these two studies, the overall distribution within the
fish community was unchanged. Since the 195 7 study,
however, the distribution has changed greatly. The 19 27/
19 57 curves were characterized by three species with a
frequency above 0.30 but none higher than 0.50. The
majority of values (6) fell between 0.10 and 0.20 and
a large number (5) were under 0.10. Three species were
of great importance as host and the remainder were
occasional hosts. The 1971-72 curve, however, had seven
fish above the 0.30 level, with five above 0.50. The
shape of the curve strongly suggests that a dispropor
tionate increase of C. oxycephalus occurred in the com
monly infected species of fish. In occasional fish
hosts, the frequency showed only a marginal increase. 76
1.00
9 0
8 0
7 0
O . 6 0
50
4 0
U. .20
Host Sequence
Text Fig. 13. Host Species Importance Curves for Lake Erie Fish Community 19 27-195 7- 1971-72. 77
Discussion of the Histoyy of C. oxycephalus in western
Lake Erie.
The frequency and abundance of a parasite within a host population depends upon a number of factors.
Kennedy (1970) listed host diet, behavior, physiological resistance and the availability of infective larvae as important determinants. The occurrence of a parasite is the result of input and output in the host population.
Input is a function of contact between the host and para site affected by the density of individuals in both populations. For endoparasitic species transmitted through a food web, host diet is extremely important. A high density of infective agents may increase the likelihood of host-parasite contact, but feeding habits ultimately determine the rate of contact. Output is related to the conversion or transfer efficiency, or the number of in fective agents successfully transferred from one environ ment to the next divided by the number of infective agents contacted by the host (see Text Fig. m ) . When the conversion efficiency (E) is low, many of the in fective agents contacting the host are not transferred.
Infection and development do not occur and output is considered high. Once the transfer and establishment of the parasite is accomplished, output is related to sur vivorship of the parasite population within the host.
The factors affecting this are complex but probably 78 include host immune response, temperature and longevity of the parasite. It is possible that in some systems survival may be related to the density of parasites or the amount of parasite biomass within a host.
Clearly, the abundance of a parasite increases within a host population when the input is greater than the output. A change in the system resulting in in creased host-parasite contact, transfer efficiency, sur vivorship or all of these factors should produce an increase in the frequency and abundance of the parasite.
A preliminary analysis of the Camallanus-Lake Erie system is possible by adapting the general host-parasite population interaction model to the life cycle. Text
Figure 15 is a systems model of C. oxycephalus in Lake
Erie. P represents the probability of contact between two boxes and the output function, E is the conversion of transfer efficience. The frequency of occurrence in any box, is predicted by
Finf - (P x E)
(from Text Figure 14).
Fish populations declining in a particular system and under stress, might reasonably be expected to be more susceptible to infection. An expression of this might be an increase in E. However, the greatest increases of
C. oxycephalus in Lake Erie have been in populations of fish not declining perceptably, such as White bass, P host /parasite contact
INPUT HOST f« = (p
E conversion efficiency
OUTPUT
Text Figure 14. General Host-Parasite Population Interaction Model 80
Crappies, Freshwater drum, Black basses and Shad (Hartman,
1972). Such increases might logically be explained by a greater frequency of contact between fish and parasite.
The question becomes what changes in the lake have probably produced a higher fish-parasite contact fre quency .
An increase in the abundance of copepods theoreti cally raises the probability of contact between infective
1st stage larvae (L^) and the intermediate host. Bradshaw
(1964) pointed out that such an increase has occurred in western Lake Erie. Comparing data from Chandler (1940) and Hubschman (19 60), he noted that total copepods in creased from 70,000/m3 to 165,0QQ/m3. If this rise in copepod density increased the P of contact with copepods, the frequency of infected copepods might be expected to be greater. No data were available to indicate such an increase. A greater frequency of in fected copepods might be indicated by a rise of Camallanus in planktivorous fish, although this might also be due to a greater predation on copepods. The incidence of
Camallanus in minnows which feed heavily upon cladocerans but not copepods (Price, 1963) has not increased signifi cantly. Young of the year White bass, which feed heavily upon copepods, appear to have a higher infection fre quency in 1971-72. The relationship between increased copepod density and the rise in C. oxycephalus is not 81
copepod
planktivorous fish
piscivorous fish
Text Figure 15, Systems Model of C, oxycephalus in Lake Erie 82 clear and the evidence indirect. Conclusions, then, based upon these data are uncertain.
The highest infection frequencies and greatest in creases of C. oxycephalus have occurred in adult, pisci vorous fish. These fish become infected by consuming smaller, infected plankton-feeding species. This pathway was experimentally proven. Higher infection frequencies suggest an increased consumption of infected forage fish or higher frequencies of Camallanus within forage fish populations, or both. The data indicate that the fre quency of Camallanus in minnows has not risen suggesting that another group of forage fish may be responsible for the increase of this nematode in large fish. The dis covery of C. oxycephalus in Alewife and Gizzard shad in
1972 was particularly significant in this regard, since
Gizzard shad have very high frequencies of Camallanus
(over .70) during some portions of the summer. Gizzard shad and Alewife were rare enough in 19 27 that Bangham and Hunter were unable to collect adequate samples. The
1957 samples were very small and the worms were absent from both species. Gizzard shad and Alewife were known from Lake Erie prior to 1927, but Miller (19 60) believed the species have only become numerous since about 1950.
Both have become particularly abundant in the western end of Lake Erie (Bodola, 1964). I frequently found both species in the stomachs of White bass and Crappies during 83 the study, suggesting that the increase in these fish has been and is being exploited by several piscivorous species.
This exploitation has caused an increased frequency of contact between infected plankton-feeding species and large piscivorous ones, resulting in an increase in flow of Camallanus to the adult, piscivorous portion of the fish community.
The great increase of C. oxycephalus in western Lake
Erie appears to be related to the rise in the abundance of
Gizzard shad and Alewife in this region. The reasons for the increase in clupeids is uncertain, but the affect upon the Camallanus population has been great. The in crease in the Camallanus population results in a greater input of L-^'s into the system. If no regulation of worm numbers is accomplished, the greater parasite frequency and perhaps greater infection intensities, increase the probability of stress and disease within the fish com munity .
Population Structure
Continuous sampling of the C. oxycephalus for 26 months revealed a distinct seasonal cycle in the popu lation structure. The population was composed of male and female nematodes in a 1:1 ratio throughout the entire year with the exception of July and August. The majority of worms during these two months were larval stages, principally 4th stage larvae. The sex ratio changed with males outnumbering females 2 to 1. Table 11 summarizes the seasonal structure of the population and indicates that in western Lake Erie, C. oxycephalus produces one generation per year. The table also shows that the nematodes live for only one year and the generations barely overlap. Because immature and senescent adults can easily be distinguished from one another by size, the longevity can be accurately determined. Table 12 indi cates that a great mortality of year old adult worms occurred during July and August, and by September the new generation represented 100% of the population.
The sex ratio deviated from 1:1 during the summer.
There was a greater mortality of females than males be tween June and September. This was due to the protrusion of gravid females from the fish rectum, their rupture liberating larvae, and their subsequent death. Mechanisms of death for senescent males are unknown, but generally the mortality rate was not as high and males usually outlived the females by several weeks, creating an un balanced sex ratio. The sex ratio was also initially unbalanced in the new generation, but by September, it is essentially 1:1. Males outnumbered females initially because the final molt transforming L^’s to adults occur red within 18 days for males, while it takes 24 days for females. Thus, males are recruited into the new generation 85
TABLE 11. SEASONAL STRUCTURE OF THE C. OXYCEPHALUS POPULATION IN LAKE ERIE
Month % Males % Females % L^'s % L.3»:
June 1+8.2 51.8 0 0
July 16.6 10.2 58.4 14.3
August 30.1 17.5 43.1 9.2
September 51.6 45.6 3.2 0
October 51.2 48.8 0 0
November 50.5 45.9 0 0
December - - -
January - - - -
February - -- -
March - - -
April 49.2 50.8 0 0
May 47.9 52.1 0 0
June 50.9 49.1 0 0 86
TABLE 12. SEASONAL TURNOVER OF ADULT C. OXYCEPHALUS POPULATION
Old New Old New Month Males Males Larvae Females Females
June 48.2% 0 0 51.8% 0
July 11.6% 5.2% 72.9% 6.4% 3.9%
August 1.0% 29 .1% 52 . 3% 0.1% 17 .5%
September 0 51.6% 3.2% 0 45.6%
more rapidly than females. When all of the larvae have molted, however, the sex ratio is restored to 1:1,
Growth and Development in the Natural Population
Accurate estimates of growth within each generation of Camallanus can be obtained since there is only one generation per year in Lake Erie, which barely overlaps the previous one. These data were collected for two generations and Text Figure 16 reveals that the curves for both years were very similar. The rate of growth for the female was initially higher than for the male. The experimental life history study indicated that shortly after the final molt, the female growth accelerated (Text
Figure 1). The females, in the natural population, were approximately 8.0mm long by November, while the males were only 4.0mm in length. These lengths represent about 80% of the total length for males, but only about 35% for females. Comparison between samples taken in November and the first week in April showed no significant difference in female body length (t = ,003 < t« = .05 = 1.645).
Similar comparison for male worms, however, revealed significantly larger males in the April sample (t = 2.888 > t a = .05 = 1.645). Females stopped growing in November and did not resume until April, but the males apparently continued to grow through the winter. Continued male growth was very slight (Text Figure 16). Female growth resumed in spring at a high rate, doubling the length in
40 days.
There are several very important ecological consid erations connected with this seasonal growth pattern. A fundamental problem for all parasites is contacting the host. Two adaptations used by many species of parasites to increase the likelihood of contacting the required hosts and completing the life cycle are: a great repro ductive effort resulting in large numbers of dispersants
(Baer, 1972), and timing of dispersal to coincide favorably with host activity resulting in a high frequency of con tact between the host and parasite. The classic example of this is the periodicity exhibited in some types of filariasis where microfilariae are found in peripheral blood during the hours when the mosquitoes feed. Text Figure 16. Growth of 0, oxycephalus in the in oxycephalus 0, of Growth 16. Figure Text Worm Length in mm ao.o 10.0 15.0 3.0 5.0 JULY ET C NV E JN PEI JAN DEC NOV OCT SEPT Natural Population Natural 1970-71 MY UKI UY AUO JULY I K JU MAY t p A ogs Males .o-g^s Female* 88 89
A timing mechanism was found in the C. oxycephalus population in western Lake Erie. Text Figure 17, compiled from plankton samples taken three times a week from April to September for two years, shows clearly that the dis persal period for C. oxycephalus coincides with the annual maximum density of cyclopoid copepods. This timing is related to the delay in growth during the winter months (Text Figure 16). Proof is lacking, but the delay , p is apparently not controlled by the worm. It is impressed upon the worm population by the drop in temperature from
25°C to 4°C. This belief is based upon data from the
European species, £. lacustris, which exhibits a similar annual growth cycle (Tornquist, 1931). Moravec (1969a) completed the life cycle of C. lacustris in 90 days under laboratory conditions. Considering the tropical distri bution of most camallanids, it is perhaps not surprising that some growth inhibition occurs at low temperatures.
This delay in growth, however, has several important ramifications.
A more optimal survival tactic would appear to be a constant rate of growth from November through June or even a rapid early growth with the commitment of a large portion of energy into biomass increase. In the spring, energy could then be budgeted into the reproductive effort with a low expenditure for growth. The growth curve is depressed during the winter because the nematodes et iue 7 Rltosi BtenDsesl Period Dispersal Between Relationship 17. Figure Text COPEPODS PEI L I T E ! 1PIA PRO FOi AAAU I WSEN AE E I H LAKE WESTERN IN CANAUANUS i O F PERIOD U1SPEISAL 1971 aalns larvae. Camallanus Cyclopoid Copepod Density. Shaded areas Shaded Density. Maximum Copepod Annual the Cyclopoid and oxycephalus C. of niae h pro f ipra of dispersal of period the indicate IOLY JUNE 197 )
90
91 are apparently unable to maintain a high rate of growth at low temperatures. When egg production begins in
April and presumably energy is budgeted for reproduction a great increase in biomass occurs. This seems to be a rather inefficient way of handling resources.
The reason for this expenditure of energy for growth in the spring becomes evident when egg production and female size are examined. It has already been noted that production of prodigeous numbers of young is apparently a tactic used by many parasitic species. Be cause of the low density of copepods in early spring, production and release of Camallanus larvae continually from April through August would be inefficient and waste ful. Larvae released in April, May and early June would have a very low probability of being contacted and con sumed by copepods. Eggs and developing larvae are stored until late June and then released during the copepod peak.
The number of larvae stored is directly related to the amount of storage space or female body volume.
Table 13 shows the relationship between female body length, body volume and the estimated maximum number of
1st stage larvae which can be stored within that volume.
Volumes were calculated from the length-width function by considering worms as perfect cylinders. Potential larvae was estimated by dividing the mean volume of a single
(.00013mm ) into the calculated female body volume. 92
TABLE 13. RELATIONSHIP BETWEEN FEMALE LENGTH, VOLUME AND THE NUMBER OF 1ST STAGE LARVAE WHICH CAN BE PRODUCED
3 Female Length Volume in mm Maximum #L-, Increase (mm)
8 .1752 1,348 -
9 .2268 1,745 397
10 .2830 2,177 432
11 .3454 2,657 480
12 .4116 3,166 509
13 .4849 3,730 564
14 .5572 4,286 556
15 .6270 4,823 537
16 .6992 5,378 555
17 .7684 5,911 533
18 .8424 6,480 569
19 .9025 6,942 462
20 .9620 7,400 458
21 1.0059 7,738 338
22 1.0450 8,038 300
23 1.0833 8,333 295 33
Actual counts of the number of L^'s in gravid females ranged from 7,800 - 10,000 so the estimated values are reasonable approximations.
If the female do not grow during the spring or re sumed growth at a rate similar to that during the previous autumn, they would attain a length between 8 and 11mm by the time the copepod population reached its maximum.
This limited increase in body volume would allow a total estimated production'of only 1,348 - 2,657. The rapid growth which does occur allows the females to reach a length of 18 - 20mm and produce between 6,480 and 7,400 larvae, approximately three times the number possible with limited growth. Some females reach a length of 25mm, so that production is still greater. In view of this difference in potential larval production, the budgeting of energy into growth during the time of egg production seems to be justified. The yield in terms of larvae is fairly high. Each additional millimeter of body length between 8 and 2 3mm provides a mean increase in volume sufficient for the storage of an additional 466 L^'s.
The real efficiency of this production could be estimated if information was available on energy cost involved in the production of each millimeter of body length.
The stimulus for this rapid female growth is unknown.
It is likely that rising temperature stimulates increase in growth. There may be a threshold below which no growth 9U occurs. But temperature alone may be insufficient to cause such a high rate of growth, especially since growth during comparable autumn temperatures is not as rapid.
Since worms attach to the intestinal wall and feed on blood, a constant supply of energy should be available.
Kennedy (1969) presented evidence that the spring egg production of Caryophyllaeus laticeps in the European dace,
Leuciscus leuciscus was influenced by rising hormone levels in spawning fish. Possibly the spring growth of C. oxycephalus in Lake Erie may be stimulated by rising hormone levels in White bass.
The persistence of males within the fish throughout the entire year is very interesting. Copulation takes place as early as October. If resources were limited, one might expect a sexual competition with selection favoring the females. This would result in an increase in male mortality after copulation. Such a post-copulatory mortality apparently occurs in philometrid nematodes as well as others. Since there is apparently no increase in male mortality, it is assumed that competition between the sexes for resources is not intense. The presence of male worms throughout the year may help to insure that fertilization of a maximum number of females occurs. DISTRIBUTION IN WESTERN LAKE ERIE FISH
Relationship to Fish Sex
The analysis of the incidence and intensity of in
fection in male and female fish revealed no significant
difference. The Mann-Whitney-U statistic was calculated
for summer and spring samples of White bass, Yellow perch
and Freshwater drum and no difference between the sexes was noted at either time of year in any of the three species. All subsequent analyses on fish are based upon mixed samples of male and female fish, since no difference
in their worm burdens was indicated.
Relationship to Fish Size
The distribution of C. oxycephalus was studied in depth within the White bass and Yellow perch populations.
Text Figure 18-21 show the nature of the relationship between fish size and the infection intensity in these two fish. In addition, Text Figure 22 illustrates the relationship between these variables in the Freshwater drum population. White bass have by far the greatest numbers of Camallanus, with the intermediate to large size fish being most heavily infected. Young of the year
95 96
White bass and Freshwater drum exhibited similar patterns of moderately high incidence but low intensity. Young perch were essentially free of the infection. The in tensity of infection and variance were generally higher in the larger fish for all three species.
Kennedy (19 70) suggested that host diet is an important determinant in the distribution of some endo- parasites of fish. Since oxycephalus can be trans mitted by copepods and small forage fish, these elements of the fish diet were examined to see if any correlations could be drawn among changes in diet, worm number and fish size. Price’s (196 3) food study of Lake Erie fish gave some indication of how important copepods and fish were in the diets of different size fish.
Table 14- shows that young of the year fish of all three species feed upon copepods. Part of the difference in magnitude of infection between young White bass and young Freshwater drum may be due to the relatively higher frequency of feeding by bass upon copepods. Although young perch feed heavily upon copepods, C. oxycephalus practically never occurs within this age class. This is the result of two factors which operate to reduce the frequency of Camallanus to zero. One, by the time the infective L^'s are dispersed into the plankton, the mean length of young perch is between 60 and 70 mm. This size class is rapidly approaching a frequency of copepod 97
Summer 70,71
30 ik
o 2 0
0 150 2 5 0 3 0 0 3 5 0 Flili Length In m m
Text Fig. 18. Relationships of Infection Intensity and Fish Length for White Bass-Sununer 19 70,71
so
• 30
S »
«•
ISO 250 300 4 5 0 Fish Length In m m
Text Fig. 19. Relationship of Infection Intensity and Fish Length for White Bass-Spring 1971-72 98
SO- mm w 1970.1971
■c 3 0 -
E £ ao-l
10-
o -i tfpi. H. - r - ■i o SO 190 230 Fish Length m mm
Text Fig. 20. Relationship of Infection Intensity and Fish Length for Yellow Perch - Summer 1970, 1971 Pwrcm imga Sprint 1971,1972
4 0 -
> 30’
10 « i « >
I * e 40 t*l«l M If I il •tri i " p OH T 2 5 0 5 0 100 150 200 Fish Length In mm
Text Fig. 21. Relationship of Infection Intensity and Fish Length for Yellow Perch - Spring 1971, 19 72 99
5 A. qrunnlent 4 0 - .30 1 20 10- Fleh Length in mm Text Fig. 22. Relationship of Infection Intensity and Fish Length for Freshwater Drum - Summer 1971, 1972 100 TABLE 14. FREQUENCY OF FOOD ORGANISMS FOUND IN FISH STOMACHS* Size in White Bass Yellow Perch Drum mm Copepods Fish Copepods Fish Copepods Fis] CM J- LO 00 1 .83 .03 .79 0 . 31 0 50-74 .52 .11 .47 0 .31 0 75-99 .14 .33 .30 0 .24 0 100-150 .16 .56 .16 .02 .06 0 151-202 .03 .41 .03 .05 0 .0 3 203-251 0 .71 .01 .16 0 .01 252-302 0 .82 0 0 0 ,05 303-378 0 .28 0 0 0 .16 ; 379-445 0 0 0 0 0 .27 * Data from Price (1963). 101 consumption of .30, which is considerably less than the .79 found in 25-48mm fish. Thus, contact with the nema tode is reduced. In addition, the E of transfer is very low in perch. This value, experimentally measured, was .022 as opposed to .80 7 for young White bass. This com bination of relatively low contact frequency and extremely low E of transfer explain the absence of Camallanus from young perch. The intensity of infection of C. oxycephalus in 1+age class fish correlates very well with the frequency of fish in the diets of the three species. The mean and variance rise abruptly at about 200mm for White bass then fall around 300mm. Table 14 shows that the frequency of fish in the diet is highest in this size interval. Yellow perch contain very few worms until they reach about 180mm, close to the size at which they begin taking fish. Freshwater drum begin to carry increased numbers of worms around 200mm of length which is also the size at which they begin to consume fish. Several other studies have revealed relationships between infection intensity and fish length that are similar to C. oxycephalus in Lake Erie. Awachie (19 65) showed that the greatest intensity and variance of the acanthocephalan, Echinorhynchus truttae Schrank, 1788, in trout occurred in the intermediate size fish. Later, (Awachie, 196 8) he demonstrated a similar pattern for the 102 trematode Crepidostomum metoecus (Braun, 1900). Kennedy and Hine (1969) demonstrated that the intensity of in fection with the tapeworm Proteocephalus torulosus (Batsch, 1786) in dace generally increased with fish length and had a larvae variance. Feeding habits of fish are known to have a signifi cant affect upon the distribution of various parasites within fish populations. Hopkins (1959) showed a high correlation between infection of young sticklebacks, Gasterosteus aculeatus, with the tapeworm Proteocephalus filicollis (Rudlophi, 1810) and their feeding upon cope pods. Chubb (1964) discovered a similar relationship between the perch, Perea fluviatilis, and the tapeworm Trianenophorus nodulosus (Pallas, 1781). It seems clear that the initial intensity of in fection as well as frequency of any parasite transferred through a food web is highly dependent upon the fish diet. Because the feeding habits of fish often change quite drastically with size and age, the distribution of para sites is seldom similar in different size classes. The frequency and intensity of infection in fish is deter mined by feeding rates, parasite distribution within the trophic level sampled by the fish and the transfer effi ciency. These variables may be different for different size fish. For example, the distribution of Camallanus in the copepod population, the feeding rate of young 103 White bass and the E of transfer from copepod to fish are all likely to be different from distribution values in forage fish, feeding rates of adult bass and the E of transfer from fish to fish. The result is two different patterns of infection in young (under 180mm) and adult White bass (over 180mm) (Text Figures 18-19). Whatever factors combine to produce the distribution of C. oxycephalus within the White bass population, the result is interesting. The greatest infection intensity is found in the 1+age class fish (180 - 2 80 mm). These fish are the optimal size since they have the greatest likelihood of surviving for the 12 months necessary for the nematode to complete development and reproduction. Large, senescent fish may perish before these vital pro cesses are complete. Likewise, young of the year fish are most likely to be consumed by birds or other predators unsuitable as a host for the worm. The concentration of Camallanus in these optimal size fish groups minimizes the risks of host destruction before parasite reproduction. One of the major factors in the production, of this optimal size distribution is the ability of C. oxycephalus to utilize a transfer host such as Gizzard shad and Alewife. This was the advantage to transferring packets of worms instead of single units. Analysis of the distri bution of the worm within young of the year and adult portions of the White bass population showed that the mean infection was 1.27 worms and 14.8 worms respectively. The probability of finding at least one male and female in each fish can be estimated by expanding the binomial (p + q)n with p = .5 and q = .5 representing the 1:1 sex ratio, and n equalling the number of worms in the fish. Since pn + q11 equals the probability of finding either all males or females, the probability of finding a mixture is equal 1 - (pn + q11). The probability of finding a mixture of male and female Camallanus approaches 1.0 only when the number of worms is equal to or greater than 4. Reproduction is assured in large fish because the mean intensity of infection is sufficiently high to get a mixture. However, the mean intensity for young of the year bass is very low = 1.94 worms). This means approximately one half of the infected fish will contain either all male or all females and thus will not contribute to reproduction. Data for young Freshwater drum = 1*47) and young Gizzard shad = 1.76) are similar. Thus reliance upon copepods alone in the life cycle would produce much lower frequencies and in tensities of infection and limit the nematode population to a higher risk host group. Table 15 shows the frequency distribution of C. oxycephalus in other species of fish. It is evident that the level of infection is not sufficiently high in most of the other species to assure a mixture of worm sexes and TABLE 15. FREQUENCY DISTRIBUTION OF C. OXYCEPHALUS IN CENTRARCHIDS No. Fish With X Worms N o . Worms Pumpkin- X W. Crappie S . Mouth Bl.Crappie Rockbass seed 0 2 24 9 16 25 1 5 5 11 3 2 2 3 6 5 2 1 3 4 2 5 1 0 ' 4 4 0 4 0 5 3 0* 0 6 3 0 1 7 3 1 0 8 1 0 9 1 1 10 2 0 >10 2 No. Fish 33 39 35 22 28 N o . Worms 159 39 58 10 4 4.82 1.00 1.66 0.45 0.14 % inf 94 38 74 27 11 2.60 1.67 1.33 Xinf 5.13 2.23 X,. = mean number of worms for all fish w X. -r = mean number of worms for infected fish only. 106 hence reproduction. These species, however, do represent a maintenance mechanism if a catastrophe strikes the principal host population. Such circumstances would un doubtedly reduce the population of Camallanus, but repro duction in these other fish might be sufficient to main tain the parasite population until the principal host population recovered. This mechanism probably contributes to the stability of the population and dampens any tend ency to flucuate greatly. Changes in the Infection Intensity Although the initial level of parasitism is a function of parasite distribution, fish diet and behavior, the level frequently changes through time. Comparison be tween Text Figures 18-19 and 20-21 clearly demonstrate much greater infections during the summer than the follow ing spring. Kennedy (1970) indicated that output in host-parasite systems was a function of failure of para sites to establish themselves, rejection of established parasites and natural mortality at the termination of a parasite's life span. These functions are influenced by such biotic factors as overcrowding and interspecific competition and abiotic factors like temperature. The population level at any moment is the difference between input and output, or recruitment and mortality. If the level of infection remains stable throughout the year, the 107 two functions balance. Frequently, however, parasite levels flucuate (Hopkins, 1959; Chubb, 19 63; Kennedy, 1968), with a rise indicating periods of infection and a fall indicating periods of mortality. It was determined that the Camallanus population in western Lake Erie produces a single generation each year and further that this is dispersed during July and early August. Adults die shortly after this dispersal. Thus, a distinct mortality was observed followed by a rapid rise in the intensity of infection by the new generation. The nature of this recruitment and mortality in plankto- vorous fish was studied in Gizzard shad, young White bass and young Freshwater drum. Tables 16-18 show the sequential changes in the frequency distributions of C. oxycephalus in these fish. The percentage of infection in Gizzard shad dropped quite rapidly 71% to 43% in only three weeks. This value for the Freshwater drum and White bass, however, remained somewhat stable over four months. The mean intensity of infection decreased in all three species. These data suggest that the nematodes did not survive for a long period of time in the Gizzard shad population. The absence of any adult worms indicates that development ceases before the last molt and the worms die. This limits the time any single worm can remain in the Gizzard shad population to only a few weeks. This reduction in 108 TABLE 16. THE FREQUENCY DISTRIBUTION OF C. OXYCEPHALUS IN YOY GIZZARD SHAD No. Worms No. Fish With X Worms X August 5 August 13 August 2 3 Total 0 23 34 46 10 3 1 27 23 21 71 2 18 15 10 43 3 8 5 1 14 4 2 0 1 3 5 1 1 0 2 6 0 2 0 2 > 6 1 0 0 1 No. Fish 80 80 79 239 % inf 71.2 57.9 42.5 57.1 No. L3 's 78 49 14 141 % L3 72.2 57.6 29 .2 N o . L ^ 's 30 36 34 100 % L,. 27.8 42.4 70.8 No. Adults 0 0 0 0 I Worms 108 85 48 241 1.350 1.060 .608 1.008 Xw 2 1.851 1.706 .729 1.513 1.890 1.840 1.410 1.760 Xinf s^/x, 1.371 1.609 1.19 9 1.501 w 109 TABLE 17. THE FREQUENCY DISTRIBUTION OF C. OXYCEPHALUS IN YOY WHITE BASS N o . Worms No. Fish With X Worms X Aug 16 A u g . 2 8 Sept. 12 Oct. 4 Tota: 0 20 13 16 12 61 1 12 15 13 17 57 2 6 7 6 5 24 3 5 4 4 4 17 4 5 0 0 1 6 5 1 1 0 1 3 > 5 1 0 1 0 2 No. Fish 50 40 40 40 170 % inf 60.0 67.5 60.0 70.0 64.1 No. L g ’s 35 10 9 0 54 % Lg 44.9 21.7 20.9 No. L^'s 40 24 7 7 78 % l 4 51.3 52.2 16.3 15.6 No. Adults 3 12 27 38 80 % Adults 3.8 26.1 62.8 84.4 £ Worms 78 46 43 45 212 1.56 1.15 1.08 1.12 1.26 s2 5.31 1.31 1.61 1.45 2 .59 2.60 1.70 1.79 1.64 1.94 *inf 2 . - 1.49 1.29 2.04 8 /xw 3.41 1.14 110 TABLE 18. THE FREQUENCY DISTRIBUTION OF C. OXYCEPHALUS IN YOY FRESHWATER DRUM N o . Worms No. Fish With X Worms To X Aug. 16 Aug., 22 A u g . 2 8 Sep. 12 Oct. 4 tal 0 47 20 22 24 18 131 1 33 10 13 11 15 82 2 13 7 2 4 6 32 3 4 2 1 1 1 9 4 2 1 2 0 0 5 5 1 0 0 0 0 1 No. Fish 100 40 40 40 40 260 % inf 53.0 50 .0 45.0 40.0 55 .0 49 .6 No. Lg’S 26 6 3 2 0 36 29 .8 17.6 10.7 9.5 % L3 No. L^'s 54 23 8 7 1 93 64.3 67.6 28.6 33. 3 3.0 % L4 No. Adults 5 5 17 12 29 56 % Adults 6.0 14.7 60.7 57.1 96 .7 I Worms 84 34 28 21 30 19 7 .84 .85 .70 .55 .75 .76 2 s 1.09 1.11 1.09 .61 .65 1.58 1.70 1.55 1. 31 1.37 1.53 *inf s2/;w 1.29 1.30 1.55 1.11 .87 Ill the number of Camallanus contracts the period of time in which nematodes can be recruited into large piscivorous fish from shad. Clearly, the infection of copepods is seasonal. The incidence of Camallanus in Gizzard shad is also apparently seasonal, meaning that recruitment of the nematode into large fish (White bass) probably occurs only during summer and autumn. Tables 19-21 show the changes in the infection of White bass and Yellow perch within the 1971-72 worm gen eration. The mean intensity of infection was highest and most variable during•late summer when recruitment into fish was occurring at a high rate. The mean dropped sharply between late summer and early autumn, then appear ed to remain stable through November. The mean appeared to drop over winter but remains stable until the post- reproductive mortality. The mean intensity of infection in young of the year White bass did not drop, but appeared to rise slightly from late summer to the follow ing spring. Unfortunately, these data could not be anlayzed statistically due to the large variance. It is particularly significant that the variance/mean ratio 2 — (s /*w ) in almost all of these samples is greater than one, indicating overdispersion of the parasite population. The data for White bass, Yellow perch, Freshwater drum and Gizzard shad were fit to the negative binomial distribution, a form of overdispersed distribution 112 TABLE 19. SEASONAL CHANGES IN THE INFECTION OF ADULT WHITE BASS Jul- Sep- Mar- Aug Oct Nov Apr May Jun No. Fish 48 20 8 23 26 21 No. Inf 39 20 8 22 26 21 17.57 11.45 11.50 8.04 9 .38 8.00 18.03 11.45 11.50 8.41 8.00 *inf 9 .38 s2 1191.12 36.47 26.00 24.41 28.49 23.50 2.- 6 /x« 67.79 3.19 2.26 3.04 3.04 2.94 TABLE 20. SEASONAL CHANGES IN THE INFECTION OF YOY WHITE BASS Jul- Sep- Mar- Aug Oct Nov Apr May Jun No. Fish 63 11 17 18 No. Inf 51 11 17 14 2.46 3.09 4.76 3. 56 K 3.04 3.09 4.76 4.57 *inf 2 s 5.28 2.89 10.19 8.85 2.15 .94 2.14 2.49 s2/xw 113 TABLE 21. SEASONAL CHANGES IN THE INFECTION OF ADULT YELLOW PERCH Jul- Sep- Mar- Aug Oct Nov Apr May Jun No. Fish 46 64 9 25 33 19 No. Inf 37 41 6 18 17 3 6.80 2.13 2.89 1.16 1.09 .21 8.46 3.32 4.33 1.61 2.12 1.33 *inf S2 69.09 7.76 10.61 1.64 2.52 .29 3.64 3.67 1.41 2.31 1. 38 s2/5w 9. 82 resulting from the expansion of The mean y is given by y = pk and the variance,a , by a = pkq The general equation is [k+x-l]! Rx ** ~ x! [k-l]! qk where Px is the probability that a host will be infected - . 2 with x parasites. The sample mean, x, and variance s can be calculated directly and substituted for Mu and Sigma. 114. R = p/q. The estimation of k, however, can be very diffi cult and time consuming. I used the maximum likelihood estimate of Bliss and Fisher (1953). The observed and expected values produced by the computer program were compared by Chi-square and not found to be significantly different. This means that the negative binomial ade quately described the distribution of C. oxycephalus in the Lake Erie fish. The reduction of the mean worm numbers per fish could be caused by either of two factors. One, heavily para sitized fish could die, or two, nematodes within the fish could die. If all worms in all fish had an equal chance of dying, mortality in single worm infections would be equal to mortality in multiple infections, that is, mortality would be density-independent. Some single worm infections, in this case might be expected to be lost during the year, resulting in an increase in parasite free fish. The adult White bass data, however, showed no such increase in the 0 parasite class (Table 19). It would be reasonable to assume then, that mortality may be related to infection intensity or worm density and that greater mortality of worms occurs in more intense infections. Comparison of Tables 19 and 20 suggests that the dif ferences in mortality between heavily infected adult fish and lightly infected young of the year may be a function of worm density. The proof of such a density-dependent 115 parasite regulation can be found only after rigorous experimentation, but these data clearly indicate that such experiments may prove fruitful. Crofton (19 71a) redefined parasitism according to modern ecological theory. He noted that parasitism was an ecological relationship between two populations. Furthermore, this relationship is characterized by the following four features which are: 1) the parasite is physiologically dependent upon the host; 2) the infection process tends to produce an overdispersed distribution of parasites within the'host population; 3) heavily infected hosts are killed; and 4) the parasite has a higher biotic potential than the host. Crofton stated that the use of frequency distributions was one of the few methods of expressing quantitative relationships between hosts and parasites. Williams (196M-) obtained good fits to the log-series distribution with data primarily on ecto parasites. Cassie (19 62) believed that the negative bi nomial presented an acceptable picture of overdispersion. This distribution was favored by Crofton because the mathematical basis and hypothetical situations generating it were translatable into parasitological terms. He stated that parasites could be distributed as a negative binomial as a result of a series of independent and random exposures or if the infective agents were not distributed randomly. It could also be generated if infection either 116 increased or decreased the chances of further infection, or if variation in individual hosts made the chances of infection unequal. Whatever form the distribution takes, overdispersion means that a large number of parasites will be found in a small number of hosts. Large numbers of parasites pre sumably begin to stress the host at some point and, according to Crofton*s definition, kill the host. Over- dispersion, then, is a method of population control for both parasite and host. Death of such heavily infected hosts is a greater loss to the parasite population than to the host population. This difference is compensated by the higher biotic potential of the parasite. Crofton (19 71b) created a deterministic model based upon his definition of parasitism and simulated it with a digital computer. By varing, arbitrarily, values for the lethal level of infection, k, the exponent of the nega tive binomial distribution and the acheivement factor, which was a measure of infection potential and repro ductive rate, Crofton showed that stability within a host-parasite system could depend upon the ability of parasites to kill hosts. , The logic of Crofton*s model cannot be denied. There is an upper limit to the number of parasites any animal (or plant) can carry. When this limit is approached, host animals begin to die. The problem is defining or 117 estimating this upper limit in any given host-parasite system. This largely depends upon the biology of the parasite. For large parasites or those which cause severe damage, pathology or disease, the lethal level might be low. Conversely, for those parasites causing little damage or those which are very small, the lethal level might be very high. Camallanus oxycephalus is a relatively small nematode which produces some pathology by burrowing through the intestinal mucosa, attaching to the submucosa and feeding upon tissue fluid and blood (Plate V, Figs. 28 and 29). When the worms are most numerous, they are primarily L^’s and 's and are very small. It might be expected that large White bass could tolerate relatively large numbers of these small worms, and indeed they do for a short period of time. Analyzing the frequency distribution for spring, it was found that no White bass carried more than 32 worms. If the lethal level were close to that, as might be expected by the lack of fish with more intense infections, then 34% of the nematodes during the previous summer were found in fish with a lethal load. Thus, 34% of the Camallanus were lost when their hosts died. This attrition from the nematode population seems high and it should be possible for the parasite population to exploit ways to avoid this severe method of population control. 118 A density-dependent mechanism operating on hosts with a near lethal or just lethal worm load might reduce the numbers of parasites sufficiently to avoid host death and thus retain a large portion of the population which would otherwise be lost. Roberts (1961) showed that population density of the rat tapeworm, Hymenolepis diminuta Rudolphi, 1819, effected the metabolism of the parasite. In dense infections, the germinative capacity, carbohydrate and lipid concentrations and metabolism were altered. Larger species or strains of rats were found by Read and Voge (1954) to have larger tapeworms. Ractliffe, et al (19 71) showed that the mean size of the nematode, Haemonchus contortus (Rudolphi, 1830), in lambs tended to be smallest in the more heavily parasitized animals. Com petition for resources between individuals then appears to be one density-dependent mechanism by which parasite biomass may be limited. Holmes (19 62) presented evidence that carbohydrate is an important resource and that competition resulted in depressed rates of growth. Such a depression presumably reduces the rate at which the parasite biomass at high levels stresses the host. The depression of growth and reduction of parasite biomass, however, does not remove parasites which may be harmful even at low biomass levels. A population regu lation mechanism reducing the numbers of parasites would be more efficient. Such mechanisms are probably complex, 119 involving environmental parameters and host-parasite inter action. Hopkins (1959) presented evidence that in natural populations of stickleback, maturation of the tapeworm Proteocephalus filicolis, was inhibited season ally and undeveloped individuals passed out of the fish. Whitlock (19 66) noted that Haemonchus populations were controlled by inhibition of molting in entering individ uals. These are examples of mechanisms tending to reduce the numbers of parasites within a host, and retarding the approach to the lethal level. Although such mech anisms are clearly operable, Whitlock (1966) correctly noted that the literature is generally lacking in data concerning parasite population control. The affect of such regulatory mechanisms upon the Crofton model is unknown. However, if such a mechanism could be incorporated into the model, simulation might indicate the effect upon the host-parasite system. In deed, it in perhaps possible that equilibrium states can be reached by replacing host death with a density-de pendent parasite regulation. The regulation of parasite biomass below a lethal level cannot be considered by itself. The particular strategy of the parasite species or life history stage must also be considered. If the parasite must remain within a host for a long period of time before reproduc tion, it Is advantageous to reduce the stress on host 120 resources far below the lethal level. If, on the other hand} the strategy is to predispose the host to predation by another animal, some stress is advantageous. This means that parasite biomass must be regulated at a level approaching the lethal level. Pennycuick (1971) noted that the plerocercoids of Schistocephalus solidus (Mueller, 1778) in sticklebacks, impaired the fish's swimming and feeding ability thus increasing the likelihood that they will be consumed by the parasite's final host. Walkey and Meakins (19 70) experimentally determined the energy budget in this system. They demonstrated a considerable depletion of host food reserves and weight loss in para sitized fish. Petrushevski and Shulman (195 8) presented evidence that the metacercaria of Diplostomum spathecum (Rudolphi, 1819) caused blindness in sticklebacks, thus inhibiting their feeding ability and increasing the likeli hood of their being eaten. Pennycuick (1971) noted that the acanthocephalan Echinorhynchus clavula caused no damage in the sticklebacks. Since the fish is the final host, it is advantageous to cause as little damage as possible until reproduction has occurred. Because large White bass and Yellow perch are final hosts for C. oxycephalus in western Lake Erie and the development period within the fish is relatively long, reduction of stress on the host would seem to be a favor able tactic. The reduction of the mean worm load in 121 large White bass appears to occur during late summer and early fall (Text Fig. 23) when the worm loads are very high. There is also an apparent reduction during the winter months. If mortality of fish occurs, it is likely to be during the late summer when infection intensities are highly variable but very high in some fish. However, a density-dependent regulatory mechanism would most likely operate at this point too, since the density of the para site is greatest. A large portion of the Camallanus are larvae which must molt to continue development and growth. Prevention of this molt, as in Haemonchus, would be one way to lower mean worm loads. Such a mechanism may be at work in Gizzard shad (Table 16) since no adult worms were ever found. Whether this is a function of worm density or an unsuitable host is uncertain. The latter appears most likely to me, but failure to molt as a result of some feedback stimulated by large numbers of worms is a distinct possibility. The winter reduction of parasite levels is unlikely to be due to fish death, because the mean and variation of the infection intensity is very much lower and only slightly higher than during the following spring. The drop in mean infection intensity, then appears to be the result of real mortality of nematodes. The mechanisms causing this mortality are undetermined, but temperature, host nutri tion or worm biomass are possible factors. et i. 3 Saoa Cags nteMa Infection Mean the in Changes Seasonal 23. Fig. Text M No. Worm*/Fish 20 0 1 Jut A uq Sop Bass in Western Lake Erie. Lake White in Western in Bass oxycephalus C. of Intensity Apr May May Apr JunJon Ooc Nov Oct 122 123 The possibility that worm biomass was involved in the mortality of nematodes was investigated by converting worm lengths to worm volume. This was done by considering nema- 2 todes to be perfect cylinders (V = r h). The radius for each worm was derived from the allometric growth equation for length and width. Conversions were performed on a digital computer. Analysis of the mean amount of parasite biomass per infected fish throughout the year revealed that the mortality of worms was not great enough to keep the increase in biomass due to worm growth at a constant level. The mean amount of worm volume increased from .1824mm in August to 3.0 2 74mm the following spring. A linear and second degree polynomial regression was performed to test whether there was a relationship between the mean female volume and the infection intensity. The analysis of variance of these regressions yeilded F-values which were not signi ficant. This indicates that no "crowding effect" was ex hibited by the Camallanus population. Thus, it appears that the observed mortality of C. oxycephalus in White bass is unrelated to competition for resources by growing nema todes or more likely that the intensities of infection in this system at present are not sufficient to stress the parasites available resources. THE LAKE ERIE - CAMALLANUS SYSTEM The elucidation of the complete life history, as summarized by Text Figure 24, made possible the creation of a simple model of _C. oxycephalus in western Lake Erie. This model is an expansion of the life history model designed earlier to help explain the increase of Camallanus in the community. The flow diagram, Text Figure 25, illustrates all of the input and outputs in each part of the system. Each transfer within the system has a prob ability (Pv ) and an efficiency (E ) associated with it. X X The conversion or transfer efficiency is considered an out put function since worms are lost from the system when this value is less than 1.0. The mortality rate CD X ) is the number of worms lost within each part of the system for a given unit of time. Based upon the data collected, the total yield of 1st stage larvae per fish was estimated for both young of the year and adult White bass. The relative productivity of the direct (copepod-bass) and alternate (copepod-shad-bass) pathway to the final host was compared. The higher frequency and intensity of in fection in adult White bass results in the production of approximately 3 3, 3 33 L-^*s per fish, while the low level of 124 125 infection in young bass produces slightly over 14,8 32 L^'s. Thus, the alternate pathway produces twice as many larvae despite the additional transfer and the relatively higher mortality. This increase in the parasite productivity may in crease the density of the worm throughout the entire community. The number of L^'s available for copepod con sumption is initially very high, however, the great majority of these larvae in the open lake probably fall through the water column and are lost in the sediments. The situation in littoral zones is slightly different. Rooted aquatic vegetation provides a substrate that in fective larvae can adhere to and so remain viable. The experiments on the biology of these larvae revealed that survivorship, depending upon temperature, may last for a considerable period of time. Although the transfer effeciency decreased sharply with age, the L^'s retained their ability to infect the copepod for several weeks. Rooted aquatic plants such as Potamogeton, Myriophyllum and Valisneria are very common in littoral zones of western Lake Erie and probably have a periphytonic fauna associated with them that includes cyclopoid copepods. The result should be a build up of infective L^'s in these zones with a higher incidence of infected copepods than in the open lake. Watson and Lawler (1964) noted such a distribution for procercoids of Triaenophorus in cyclopoid 126 Ma _ ~ ADULT Whlla B i n M r QKlHd ShM Life History of Camallanus oxycephalus Text Fig. 24. Summary of the Life History of C. oxycephalus. L = larval stage, M =Molts. X X YOY Q . S h a d >■0 14,(33 I, / FISH 33.3331, / FISH Text Fig. 25. Flow Diagram of C. oxycephalus Community Relationships. 128 copepods. The principal forage fish in western Lake Erie, Notropis hudsonius, N. atherinoides, Dorosoma cepedianum and perhaps Alosa pseudoharengus, were shown by Harner (1958) to frequent littoral zones. All of these species were frequently collected in shore seines. The two species of Notropis do not feed heavily upon cyclopoids (Price, 1963; Gray, 1942). However, both species of clupeids were shown by Price to feed extensively upon cyclopoid copepods. The frequency of C . oxycephalus in Dorosoma is extremely high (.5 3 ** .70) and in Alosa it is lower (.12) but still at a frequency to be considered as an important transport system. The frequency in the Notropis spp. was less than .05. All of these fish are closely associated with White bass (Harner, 1958). White bass stomachs, collected while autopsying fish, revealed that from 20-50% of the adult fish during late summer and autumn contained Gizzard shad. Both the direct and alternate pathway to the White bass population would seem to be favored in littoral zones. The close interaction among 1st stage larvae, copepods, forage fish and White bass in this region suggest this. This means that in terms of the flow diagram in Text Figure 25, the P values should all be higher in littoral zones. However, White bass move around the lake to an un determined extent. There is a constant exchange of fish 129 between littoral and open lake regions. Harner found large numbers of White bass in open lake areas. Compari son of White bass from Sandusky Bay and Gr*een Is. revealed no difference in infection frequency or intensity. Until I can find evidence to support this hypothesis, it must remain a speculation. The ramifications of the alternate pathway to the bass population are numerous. Clearly, fish infected via this route have a higher incidence and intensity of Camallanus. Hopkins (19 59) suggested that a relatively high incidence but low intensity is likely to arise if the source of infection is essentially single units. Young White bass, Freshwater drum and Gizzard shad, acquiring the nematode from copepods, have a high incidence and low intensity (Tables 16, 17 and 18). Although the spatial distribution of C. oxycephalus within the copepod population is unknown, data from these fish suggest that the most common infection in copepods is a single worm. The probability that a single copepod will be infected must be very small. The accumulation of larvae in Gizzard shad, even for a short period of time, provides a mechanism whereby the source of infection can be composed of multiple units per exposure. Leyton (196 7) developed a stochastic model which predicted that high incidence and high intensity could be produced from such a source. The increased flow of parasites to the White bass population as well as to other adult piscivorous 130 fish such as Crappies, Small mouth bass and Walleye, would result in more female worms reaching maturity and more 1st stage larvae being put back into the system. The ultimate outcome must be a general rise in the oxycephalus population. Some limitation upon the system must occur. Indeed, we have seen that mortality probably occurs in the worm population and perhaps in the fish population as well according to Croftonfs model. Limitations must also occur on the system level. Because of the complexity of the Lake Erie-Camallanus- system, with its multiple hosts and infection routes, there is probably a great deal of stability. It seems that changes in the P 3\ values up or down, could have a large affect upon the population levels of the nematode. This is particularly true in Lake Erie since the life cycle is seasonally timed. The summer and autumn 19 72 population levels of Camallanus in adult White bass were much lower than in previous years. In addition, the 72-73 nematode generation did not appear in adult fish until about the middle of August. The summer of 19 72 was unusually cold and it seem probable that this lower temperature may have contributed to the population reduction in some way. Examination of the flow diagram (Text Figure 25) helps to locate a point from which to construct a hypothesis for the population drop in adult fish. Temperature depression 131 has a positive effect upon the survivorship and transfer efficiency of the L1 and a direct inhibition of the dis persal agents is ruled out. Although the distribution within the copepods is not known, the discovery of young shad, Alewife, White bass and Freshwater drum with moderate to high frequencies of Camallanus indicates a good flow of parasites from copepods to small fish. Thus, the de pression of the C. oxycephalus in adult White bass suggests an impairment of parasite movement from Gizzard shad and Alewife to White bass. Several factors could be affected by temperature to alter the flow rate of the nematode between these two populations. First, a decrease in temperature might alter the transfer efficiency of larvae. Second, the lower temperature might increase the mortality (D_.) of Camalla- nus in shad. Table 16 reveals that the temporal distri bution of C. oxycephalus in Gizzard shad changed greatly in 18 days. The frequency of infection on August 5 was 0.72 but dropped to o.4 2 by August 23. Whether or not the relatively high mortality was caused by the lower 1972 temperature is not certain. Quite possibly, the Dx function is an expression of incompatability between worm and fish, relatively constant in each generation and in dependent of temperature. The third factor is an alteration in the function. If the lower temperature delayed the feeding by White bass upon shad, the high Dx 132 value of the nematode in the shad might reduce the number of larvae available to the White bass population. Quite possibly, the low seasonal temperature in 19 72 delayed normal shad growth, delaying the attainment of a minimum prey size which adult White bass might select. Predation upon other forage species, such as the Notropis spp. which have very low frequencies of Camallanus, in creased. When shad finally reached the minimum prey size, later than usual, White bass began them. This would explain the late appearance of the 72-7 3 Camallanus gen eration in adult White bass. The increased period of time in which the nematode population remained in shad before predation by White bass began allowed a greater mortality of worms, resulting in fewer nematodes being available for transfer. The difference in the worm distribution in shad changed greatly in just 18 days, so that even a short delay in the feeding by White bass upon shad could result in a very different infection intensity in White bass. The frequency of shad in August White bass stomachs was .20, while in October it was .4-5. Whether or not this is a normal seasonal feeding pattern or it was delayed slightly is unknown. A continuation of this study is planned, and should provide some answers to the questions raised in this hypo thesis . SUMMARY 1. Camallanus oxycephalus Ward and Magath, 1916 has been redescribed completely and is morphologically distinct from other species of the genus. 2. Females are ovoviviparous. When fully gravid, females placed in lake water rupture, releasing between 7,000 and 10,000 infective 1st stage larvae. 3. Larvae are eaten by copepods, penetrate the gut wall within 2 hours and enter the hemocoel. The first molt occurs 4-5 days after infection; the second 8-10 days after infection, at summer lake water temperatures. Third stage larvae within the copepods are characterized by a divided "Paracamallanus type", a partially sclerotized buccal capsule and three mucrones on the tail. No other arthropods are known to act as the intermediate host. 4. When infected copepods are ingested by fish, bile stimulates activity of the 3d stage larva and the worms escape from the copepod body either in the pyloric stomach or the duodenum. The third molt occurs about 10- 12 days after infection. Fourth stage larvae have cir- cumoral papillae, three mucrones on the tail and a com pletely sclerotized buccal capsule without tridents. 134 5. The final molt occurs at 18 days post infection for male larvae and 24 days p.i. for female larvae. Fe males begin to grow very rapidly following the final molt. 6. When infected copepods are experimentally intro duced into forage fish, development of the worms to adult hood may or may not occur, depending upon the species of fish. The worms can be transferred from these forage species to larger, piscivorous species, such as White bass, Yellow perch and probably to Freshwater drum, Black bass, Crappies, Walleye, etc. 7. The use of forage fish as a transport host has three distinct advantages for the parasite: One, it in creases the exposure time of the L3 to the final host; two, it raises the probability of contact between the Lg and a large portion of the final host population; and three, it serves as an accumulating mechanism which transfers multiple units of infection agents with each exposure. 8. Studies on the biology of the 1st stage larvae revealed that temperature affected the survivorship and the rate of decrease in infectivity. The active move ments of the L^’s decreased linearlybut infectivity decreased non-linearly, indicating that penetration of the copepod gut was not entirely a mechanical process. Active L^'s are more likely to be consumed by copepods than inactive ones. Temperature also affected the rate of 135 development of the Lg. 9. The history of Camallanus oxycephalus in Lake Erie since 19 2 7 was reviewed and comparison with this study suggests that the frequency of occurrence has in creased in 10 species of fish, remained stable in 6, and decreased in one. 10. A simple model was constructed and expanded to conform to the life cycle of Camallanus in Lake Erie. Analysis of the Lake Erie-Camallanus system indicates that the increase in Gizzard shad abundance in the lake since the fifties may explain the increase in Camallanus in the fish community. 11. A distinct seasonal cycle occurs in the Lake Erie-Camallanus system. The worms live for only one year and the new generation replaces the old one during July and August. Adults grow until November, then cease growth until the following spring. Females grow very rapidly, reaching full maturity and releasing larvae by late June. This corresponds to the period of maximum cyclopoid copepod density. This timing maximizes the likelihood of copepod-L-^ contact. 12. Rapid growth and simultaneous production of young is not an efficient way to budget resources. How ever, storage capacity (female body volume) is directly related to the number of L^*s which can be produced for the next generation. The great increase in parasite body 136 volume is necessary if a large number of L^'s are to be produced. 13. The distribution of C. oxycephalus in various size classes of White bass is related to the feeding habits of the fish and indicates that there is a general tendency for the intensity of infection to increase with length. A large variation exists in this relationship. 14. Camallanus oxycephalus is overdispersed in the White bass, Yellow perch, Freshwater drum and Gizzard shad populations. The form of the overdispersed distri- bution is the negative binomial, Cq-p) —k 15. The mean intensity of infection in White bass declines from August to the following June. This suggests that either heavily infected fish are being killed according to Crofton's model, or that mortality is occur- ing within the worm population, or both. This mortality occurs in heavily infected adult bass but not in lightly infected young, suggesting that there may be a density- dependent population regulation involved. Male and female worms are equally affected. 16. Biomass estimates were obtained by converting length to volume, employing the length-width relationship. The total amount of parasite biomass within each fish increases from August to June indicating that the increase in parasite volume is not balanced by a reduction of para site numbers. No "crowding effect" was demonstrated by 137 analysis of the relationship between infection intensity and biomass of gravid females. 17. A simple model of the community was constructed to analyze points of high output and compare the relative yield in terms of infective 1st stage larvae between the two routes to the bass population. It is predicted that the infection is more concentrated in littoral zones of the lake. The increased utilization of the transport host mechanism as a result of the increase in Gizzard shad abundance produces higher infection intensities and a greater production of larvae. The result is an increase in the Camallanus population. 18. A hypothesis was constructed to explain the reduction of the 72-73 nematode generation in large White bass. It is believed that the unusually low temperature in the summer of 19 72 delayed Gizzard shad growth, thus delaying bass predation and allowing a greater mortality of worms in the shad population. When predation commensed, the distribution of Camallanus in shad was markedly lower, resulting in later appearance and lower worm loads in adult bass. 138 EXPLANATION OF PLATE I Fig. 1 Fertilized egg from the uterus of the female. Fig. 2 Blastula. Fig. 3 "Sausage stage" developing larva. Fig. 4 Immature first stage larva, within egg membranes. Fig. 5 Infective first stage larva, free-living in water. Fig. 6 First stage larva from the hemocoel of the copepod. PLATE .06 m m .06 m m 7)6mm ' ' 06mm .15mm CO ID .15mm 140 EXPLANATION OF PLATE II Fig. 7. 2nd stage larva, en face view. Fig. 8. 2nd stage larva, tail with molting cuticle. Fig. 9. 2nd stage larva, late, just before 2nd molt. Fig. 10. 3d stage larva with tail of 2nd stage. Fig. 11. 3d stage larva, from copepod, en face view. Fig. 12. 3d stage larva, from copepod, fully developed. w oo ,15mm ,05mm LT I wi IIPLATE ,15mm ,15mm NO 1 .15mm ,05mm 142 EXPLANATION OF PLATE III Fig- 13. 3d stage larva from fish, anterior end with L^ buccal capsule forming underneath. Fig- 14. 3d stage larva, molting to 4th stage, tail. Fig. 15. 4th stage larva, molting to adult, tail. Fig. 16. 4th stage larva, en face view. Fig. 17. 4th stage larva, anterior end. Fig- 18. 4th stage larva, female, posterior end. Fig. 19. 4th stage larva, molting to adult, anterior end with adult buccal capsule visible underneath larval buccal capsule. Fig. 20. Adult, anterior end and buccal capsule, lateral view. Fig. 21. Adult, anterior end and buccal capsule, dorsal view. 15mm LT III PLATE .15mm 1 1 .15mm 1 ' ,15 mm 15m m .15mm 144 EXPLANATION OF PLATE IV Fig. 22. Adult, anterior end of male. Fig. 23. Adult, en face view. Fig. 24. Spicules. Fig. 25. Adult, male tail, ventral view showing alae and caudal papillae. Fig. 26. Adult, male tail, lateral view showing alae and caudal papillae. Fig. 27. Adult, female tail, lateral view, showing vulva, vagina, anus, and distensible, blind sac of uterus. N) r o 1 25mm .15 mm 15m m 25m m ,50mm 1U6 EXPLANATION OF PLATE V Fig. 28. Cross section of White bass intestine with nematode burrowed through mucosa, attached to submucosa. Fig. 29. Cross section of White bass intestine with nematode burrowed through mucosa, attached to submucosa. APPENDIX A THE SPECIES, HOSTS, AND GEOGRAPHICAL LOCATIONS OF THE CAMALLANIDAE 148 149 The Species, Hosts, and Geographical Locations of the Camallanidae Genus Camallanus Raillet £ Henry, 1915 £. lacustris (Zoega, 1776) Acerina cernua, Perea fluviatilis, Lucioperca lucioperca, Lota lota,~Esox lucius, Cottus gobio, Siluris glanis, Alburhus alburnus, Rutilis rutilis, Leuciscus idus, Salmo sp., Coregonus peled, Stenodus leucidfrbhysnelma; Europe and Eurasia. C. truncatus (Rudolphi, 1814) Acerina cernua, Perea fluviatilis, Acerina schraetser, Zingel zingel, Stizostedion volgense, Lucioperca lucioperca, Esox lucius, Lota lota, Siluris glanis, Pelecus cultratus, Natrix tessel- lata; Europe and Eurasia. C. melanocephalus (Rudolphi, 1819) Scomber colias, Thynnus thynnus, Pelamys sarda, Auxis bisus; Italy. C. oxycephalus Ward and Hagath, 1916 Amia calva, Salmo trutta, Dorosoma cepedianum, Alosa pseudoharengus, Hiodon tergisus, Hoxostoma sp., Catottomus commersoni, Osmerus mordax, Rhinichthys cataractae, Carpiodes cyprinus, Semotilus atromaculatus, Notropis heterodon, N. hudsonius, N. atherinoides, N. spilopterus, N. whippliiT, Ericymba buccata, Ictalurus punctatus, I. natalis, I. nebulosus, Noturus flavus, Percopsis omiscomaycus, Horone chrysops, M. mississippiensis, Esox lucius, E. masqumongy, Lota lota, Culea inconstans, Perea flavescens, Stizostedion vitreum, S. canadense, Percina caprodes, P. maculata, Ammocrypta copelandi, A. pellucida, Etheostoma blennioides, E. flabellare, E. exile, E. caeruleum, Poeci1ichthys exi1is, Micropterus dolomieui, M. salmoides, Lepomls macrochirus, L. cyanellus, L. gibbosusT Ambloplites rupestris, Pomoxis annularis, P. ni^romaculatus, Labidesthes sicculus, Aplodmotus grunniens; North America. C. ancylodirus Ward £ Magath, 1916 Carpiodes carpio, C. thompsoni, Cyprinus carpio, Ictiobus bubalus, 1^. cypnnella; North America. C. tridentatus (von Drasche, 1883) Arapaima gigas; Brazil. Emys orbicularis, Clemmys caspica, C. leprosa; Europe. Kmosternonodoratus, sp., Malacoclemys Dermatemys mawii; lesueun, North America. Aromochelys Rana hexadactyla; Europe. Rhinogobius similis, ChaenogobiusMorgurnda obscura,macrognathus, Cottus pollux; Japan. Leuciscus Opsarichthys leuciscus, "unclrostns , Emys, Chelydra sp., Pseuemys sp., Chrysemys sp., Parasiluris asotus, Zacco temmincki, Z. platypus, Barbus sp.; Tanzania Kachuga smithii (Emydidae); India. Salmo sp.; Kashmir. Ptychozoon hemalocephalum; Java. Damonia reevesi, Kinosternon sp.; Europe. Heosemys grandis; Malaya. Kinosternon hirtipes; Mexico. Chrysemys ornata; Mexico. Mastacembelus armatus; India. Hypophthalmichthys melotrix; Northeast Asia. . scabrae. MacCallum, 1918. Syn. C. microcephalus Camallanus . kachugae. Baylis £ Daubney,22 19 . trispinosus. (Leidy, 1852). Syn. C. microcephalus undulatus* Railliet £ Henry, 1915 C. C. microcephalus (Dujardin, 1845) C. C. nigrescens (von Linstow, 1906) C. cotti Fujita, 1927 C. C. kirandensis8 Baylis,2 19 C. C. ptychozoondis MacCallum, 1918 C. octorugatus3 Baylis,3 19 C. C. mastacembeli Agrawal, 1967 C. parvus Caballero,39 19 ol ol ol o! C. magnorugosus Caballero,39 19 C. salmonae Chakravorty, 1942 C. hypophthalmichthys Dogiel £ Achmerov,57 19 151 Cinosternum scorpioides integrum; Bolivia. Wallago attu; Ceylon. Channa striata; Malaya. Clanus batrachus; Malaya. Lissemys punctata; India. unispiculus Khera, 1956. Syn. Zeylanema anabantis Geoclemys reevesi, China. Rana cyanophlyctus; India. Echis carinatus, Rana tirgrina; India and Burma. Ophiocephalus punctatus; India. Rana sp.; South Africa. Rana Northcatesbia'na; America. Mastacembelus armatus; India. Pelecus cultratus; USSR. Zacco temmincki; China. Caranx sp.; Fiji Is. Acipenser sturio; Italy. . sweeti. Moorthy,37. 19 Syn. Paracamallanus papillifer. sweeti Molin, 1858 . C. C. magathi Sprehn, 1932 C. C. ceylonensis Fernando3 & Furtado,6 19 C. C. yehi Fernando 6 Furtado,64 19 C. C. longitridentatus Fernando S Furtado, 1964 C. lissemys0 Cupta 6 S Singh, 19 C. C. intermedius Hsu Hoeppli, S 31 19 C. C. ranae 56 Khera, 19 C. C. baylisi Karve, 1930 C. C. atridentus 56 Khera, 19 C. C. multilineatus 48 Kung, 19 C. C. mazabukae Kung, 1948 C. C. wolgensis Levashov,29 19 C. C. zacconis Li, 1941 ol Ol C. carangis Olsen, 1954 Genus Camallanus 152 Genus Camallanus C. anabantis Pearse, 19 33. Syn. Zeylanema anabantis, Z . pearsei. C. 'ophioc'ephali Pearse, 19 33 'Ophiocephalus striatus; Thailand. C. trichogasterae Pearse, 1933 Trichogaster trichopterus; Thailand. C. amazonicus Ribeiro, 1941 Podocnemis expansas; Brasil. C. nodulosus Sahay, 196 5 Rana cyanophlyctus; Bangla Desh C. marinus Schmidt £ Kuntz, 1969 Caranx affinis, Gazza minuta, Thysanophrys nematophthalmus, Trichiurus haumela; Philippines. C. kaapstaadi Southwell £ Kirshner, 19 37 Xenopus laevis; South Africa. C. multiruga Walton, 19 32 Frog; West Africa. C. pipientis Walton, 1935 Rana pipiens; North America. C. johni Yeh, 1960 Xenopus sp.; Tanzania C. inglisi Agrawal, 196 7 Bufo sp.; India. C. ctenopomae Vassiliades £ Petter, 1972 Ctenopoma kingsleyae; Senegal. C. thapari Gupta, 1959 Rana tigrina; India. Genus Procamallanus Baylis, 19 2 3 P. laeviconchus (Wedl, 1862) Baylis, 1923 Clarius lazera, C. an^uillaris, Synodontis schal, S. batensoda, S_. clarius, S_. gambiensis, S_. nigrita, S^. sorex, Bagrus bay ad , ~B. docmac, Distichodus niloticus, D. rostratus, Mormyrops deliciosus, M. anguilloides, Schilbe mystus, Tetraodon fahaka, Citharinus citharus , Gnathonemus cypnnoides , Malapterurus electricus; Sudan, Ghana, Congo. 153 Genus Procamallanus P. mehrii Agarwal, 19 30 Wallago attu; India P. spiculogubernaculus Agarwal, 19 58 Clarius teysmanni, C. batrachus, Heteropneustes fossilis; India. P. muelleri Agrawal, 19 66 Heteropneustes fossilis; India. P. heteropneusti Ali, 1956 Heteropneustes fossilis; India. P. clarius Ali, 1956 Clarius batrachus; India. P. globoconchus Ali, 1960 Rita hastata; India. P. ophiocephalus Ali, 1960 Ophiocephalus punctatus; India. P. armatus Campana-Rouget S Therezien, 19 6 5 Anguilla australis; Madagascar. ]?. conf us us Fernando £ Furtado, 196 3 Heteropneustes fossilis; Ceylon. P. malaccensis Fernando £ Furtado, 196U Channa lucius; Malaya. P. dacca Gupta, 1959 "Catfish"; India. P. ahiri Karve, 195 2 Anguilla bengalensis, India. P. mysti Karve, 19 5 2 Mystus cavasius; India. P. saccobranchi Karve, 19 5 2 Saccobranchus fossilis; India. P* bagarii Karve £ Naik, 1951 Bagarius bagarius, B. yarrelli, Callichorus bimaculatus, Ophiocephalus sfr'iatus ; 1 ndia . P. planoratus Kulkarni, 19 35 Clarius batrachus, Ophiocephalus punctatus, 0. striatusl India. 154 Genus Procamallanus P. brevis Kung, 19 48 Rana sp.; South Africa. P. hindenensis Lai, 1965 Heteropneustes fossilis; India. P. magurii Lai, 19 65 Heteropneustes fossilis; India. P. attui Pande, Bhatia S Rai, 196 3 Wallago attu; India. P. devendri Sinha £ Sahay, 1966 Heteropneustes fossilis; India. P. sphaeroconchus Tornquist, 19 31 Serranus sp,, Teuthis sp.; Red Sea. P. lonis Yamaguti, 1941 Lo unimaculatus; Okinawa. P. annulatus Yamaguti, 19 54 Siganus sp.; Celebes. P. charkravartyi Fernando £ Furtado, 196 3 Heteropneustes fossilis; India. P. slomei Southwell £ Kirshner, 19 37 Xenopus laevis; South Africa, P. sigani Yamaguti, 19 35 Siganus fuscescens; Japan. Genus Spirocamallanus Olsen, 1952 J3. spiralis (Baylis, 1923) Olsen, 1952 Synodontis schal, J3. batensoda, S. eupterus, Clarius' anguillaris, Heterobranchus occidentalis, Crenidens forskalu, Sargus noct, Cheilinus trilobatus; Egypt. S. monotaxis Olsen, 1952 Monotaxis grandoculis;’Hawaii. olseni Campana-Rouget £ Razarihelissoa, 19 6 5 Echeneis naucrates , Lutjanus doudecimlineatus; Madagascar...... - ^ 155 Genus Spirocamallanus S. chauhani Sahay, 19 67 Mystus cavasius; India. S^. ,vachai Sinha £ Sahay, 196 5 Eutropichthys vacha; India. S. mazabukae Yeh, 1957 "Homa fish"; Northern Rhodesia. S^. parasiluri • (Fujita, 1927) Olsen, 1952 Parasxluris asotus; Japan. S^. inopinatus (Travassos, Artigas £ Pereira, 19 28) Olsen, 1952 Leporinus copelandi, L. elongatus, L. sp., Schizodon nasutus; Brazil. iheringi (Travassos, Artigas £ Pereira, 19 28) Olsen, 1952 Leporinus copelandi, L. elongatus, L. fasciatus, Schizodon nasutus, Salminus hilarii, Hoplias malabarica, Tetragonopterus sp. ; Brazil. S. rarus (Travassos, Artigas £ Pereira, 1928) Olsen, 1952 Pimelodella lateristriga, Rhinodoras dorbignyi; Brazil. S. xenopodis (Baylis, 1929) Olsen, 1952 Xenopodis muelleri, X. spp.; East Africa. S^. kerri (Pearse, 1933) Olsen, 1952 Glossogobius giurus; Thailand. §.• amarali (Vaz £ Pereira, 1934) Olsen, 1952 Leporinus sp. ; Brazil. £5. hilarii (Vaz £ Pereira, 1934) Olsen, 1952 Salminus hilarii; Brazil. §.• barroslimai (Pereira, 1935) Olsen, 1952 "Sardine"; Brazil. S. fariasi (Pereira, 1935) Olsen, 1952 Leporinus sp., Pygocentrus sp,; Brazil. S. wrighti (Pereira, 1935) Olsen, 1952 Astvanax sp., Hoplias malabaricus, Leporinus sp., Pygocentrus sp.; Brazil. 156 Genus Spirocamallanus S^. fulvidraconis (Li, 1935) Olsen, 1952 Pseudobagrus fulvidraco, Ophiocephalus argus, Siluris soldatovi, Parasiluris asotus, Liocassis ussuriensis, L. braschnikowi, Siniperca chua-tsi, Ery thro cult er mongolicus ; North East AsiaTi S. cearensis (Pereira, Vianna 6 Azevedo, 19 36) Olsen, 1952 Astyanax bimaculatus vittatus; Brazil. S. murrayensis (Johnston £ Mawson, 1950) Olsen, 1952 Pseudophritis urvillei, Percalates colonorum, Plectroplites ambiguus; Australia. J3. istiblenni Noble, 1966 Istiblennius zebra; Hawaii. S. pereira (Annereaux, 1946) Olsen, 1952 Athennopsis calif orniensis , Gillichthys mirabilis , Leptocottus armatus, Fundulus parvipinnis, Athennops affins , Girella nigricans, Bairdiella chrysura, Leiostomus xanthrurs, Symphurus plagiusa, Achirus lineatus, Hycteroperca microlepis, Micropogon undulatus; Lower California and Gulf of Mexico. S. singhi (Ali, 19 56) Campana-Rouget & Razarihelissoa, 1965 Callichrous bimaculatus; India. S. viviparus (Ali, 1957) Campana-Rouget 6 Razarihelissoa, 1965 Mystus microphthalmus; India. S. gubernaculus (Khera, 19 55) Campana-Rouget £ Razarihelissoa, 1965 Rita rita; India. S. hyderabadensis (Ali, 19 57) Campana-Rouget £ Razarihelissoa, 1965 Mystus seenghala; India. Genus Zeylanema Yeh, 1960 Z. pearsi Yeh, 1960 ~ Rasbora daniconius\ India. 157 Genus Zeylanema Z. anabantis (Pearse, 1933) Yeh, 1960 Rasbora daniconius, Anabass testudineus, Puntius filameritosus, Ophiocephalus punctatus; Ceylon. Z. kulasirii Yeh, 1960 Ophiocephalus punctatus, Anabas testudineus; Ceylon. Z.* fernandoi Yeh, 1960 Ophiocephalus punctatus, 0. striatus; India. Z. spinosa Furtado, 1965 Betta picta; Singapore. Z. mastacembeli Sahay £ Sinha, 19 66 Mastacembelus armatus; India. Genus Camallanides Baylis £ Daubney, 19 22 C. prashadi Baylis £ Daubney, 19 22 Bungarus fasciatus, Naja hannah, Ptyas mucosus, Rana tigrina, R. cyanophlyctis, Calotes versicolor; India. C, piscatori Khera, 1956 N a t n x piscatori; India. C. ptyas Khera, 1956 Ptyas mucosus; India. C. dhamini Deshmuth, 19 68 Ptyas mucosus, India. C. hemidenta Majumdar, 19 6 5 Channa striatus; India. Genus Paracamallanus York £ Maplestone, 19 2 6 P. cyathopharynx (Baylis, 192 3) York £ Maplestone, _ 1926 Heterobranchus anguillaris, Clarius lazera, C. parvimanus; Egypt, Isreal. £• ophiocephali Karve, 1 9 m Ophiocephalus gachua; India. 158 Genus Paracamallanus P. sweeti (Moorthy, 19 37) Campana-Rouget, 19 61 Ophiocephalus gachua, 0. striatus, 0. punctatus, Anabas testudineus, Rasbora daniconius, Lepidocephali'chthys thermal is , Barbus , sp. , Gambusia sp.; India, APPENDIX B COMPUTER PROGRAM FOR FITTING THE NEGATIVE BINOMIAL DISTRIBUTION 159 160 / / GGX040, 'ST ROM BERG, P. ' , / / CLA SS = A / / EXEC PROC=FORTRUN ,T IME = ( ,3 0 ) //CM P. SYS IN on * CC NEGATIVE BINOMIAL DISTRIBUTION PROGRAM DIMENSION X ( 5 0 0 ) , F ( 5 0 0 ) , A (5 0 0 ) , EF (5 0 0 ) , E FN (500) READ 9 9 ,M 99 FORMAT (13) M4 = M + 4 DO 10 I = 1, M4 F ( I )=0. 10 X (I ) = 1-1 READ (5, 100) (F(I), I = 1, M) 100 FORMAT (2 4 F 3 .0 ) XN ~ 0 . 0 XM = 0 .0 XS = 0 . 0 - XK a 0 .0 DO 12 1 = 1 ,M XN = XN + F ( 1 ) XM = XM + F ( I ) * X ( I ) 12 XS = XS + F(I ) * X(I ) * * 2 .0 XM E = XM / XN XSE = ( XS - XM * XME ** 2I/IXN - 1 .0 ) XK = XME ** 2 . 0 /(XSE - XME) A(l) = XN - F ( 1) DO 13 1 = 2,M 11 - 1 - 1 13 A ( I ) = A ( I I ) - F {I ) JS = 0 TO SUM 1 = 0 JS = JS+1 IF (JS.EQ.20) STOP 50 SUM 2=0 DO 14 I a 1 ,M ADD 2 =A D IFF = XNUM /DEMON XKP=XK-D IFF IF (ARS (I) 1FF/XK ) . LT ..OOOOl) GO TO 16 XK= XKP GO TO 70 16 P = XMF/XK Q = 1 .0 + P R = P/0 B = 1.0/0**XK EF I 1) = B EFM(l) = B*XN DO 17 I = 2, N4 IJ = I - 1 EF (I ) = EF (IJ )*R*(XK + X(IJ))/X(I) 17 EFM U ) = EF ( I )*XN WRITE (6 ,1 0 3 ) 103 FORMAT Cassie, R. M. 196 2. 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