Cestoda from Lake Fishes in Wisconsin: The Ecology and...

J. Helminthol. Soc. Wash.59(1), 1992, pp. 76-82

Cestoda from Lake Fishes in Wisconsin: The Ecology and InterspecificRelationships of Bothriocephalid Cestodes in Walleye,Stizostedion vitreum

OMAR M. AMI NDepartment of Biological Sciences, University of Wisconsin-Parkside, Box 2000, Kenosha, Wisconsin 53141

ABSTRACT: A total of 1,812 fishes of 32 species from Silver Lake (Kenosha County) and Tichigan Lake (RacineCounty), southeast Wisconsin, and 1,543 fishes of 27 species from connected waters, were examined for parasites.Only walleye, Stizostedion vitreum, from Silver Lake were infected with both Bothriocephalus formosus (a newhost record) and B. cuspidatus. Green sunfish, Lepomis cyanellus, from Tichigan Lake canal were also infectedwith B. formosus. The description of B. formosus is addended from autumn and spring collections. Availablemuseum specimens were examined critically and some were reidentified. The relationship between growth anddevelopment of B. formosus was related to season (temperaturee) and host species. Bothriocephalus formosuswas more dominant than B. cuspidatus. It was present in walleye all year, but its major recruitment andreproductive seasons were autumn and summer, respectively. Bothriocephalus cuspidatus, which competed withB. formosus for pyloric ceca, was absent from walleye during summer when B. formosus reached its peak intensityof infection and reproductive activity. Peak reproductive season of B. cuspidatus was in the autumn. This isconsidered to be a case of temporal segregation of reproductive niches. Prevalence and intensity of infection ofboth Bothriocephalus species did not appear to be related to host size or sex. Pomoxis annularis, P. nigromacula-tus, S. vitreum, Micropterus salmoides, and Ambloplitis rupestris appear to be paratenic hosts of Bothriocephalusin Silver Lake; the first to be reported.

KEY WORDS: cestodes, Wisconsin, Bothriocephalus, Stizostedion vitreum, morphology, ecology, interspecificrelationships, seasonality, host size and sex, site selection.

This report addresses various ecological rela-tionships between 2 species, Bothriocephalus for-mosus Mueller and Van Cleave, 1932, and Both-riocephalus cuspidatus Cooper, 1917, infectingwalleye, Stizostedion vitreum, from 2 eutrophiclakes in southeast Wisconsin. Early studies offishparasites in various Wisconsin waters includedparsite-host lists, which were occasionally an-notated. Both species of cestodes were previouslyreported in western Wisconsin (Fischthal, 1947;Kuntz and Font, 1984), but B. cuspidatus wasmore widespread elsewhere in northern and east-ern Wisconsin and in other Great Lakes states(see Hoifman, 1967). The fact that both speciesof cestodes utilized the same fish species as thedefinitive host in this study provided a uniqueopportunity to study their interspecific associa-tions, habitat occupancy, host relationships, andvariations in their temporal pattern of repro-duction. Morphological comparisons and eco-logical information contained herein are report-ed in the North American literature for the firsttime.

Materials and Methods

Walleye were examined from Silver Lake (KenoshaCounty), a 188-ha eutrophic land-locked lake, andTichigan Lake (Racine County), a 458-ha lake in an

advanced state of eutrophication on the Fox River(tributary of the Mississippi River). Seasonal biweeklycollections were made from both lakes during spring(April) , summer (June, July, and early August), andautumn (late October and November) between 1977and 1979 and also from Silver Lake during the summerof 1976.

Fish were electro-shocked and dissected shortly aftercapture. The stomach (region A), the first and secondloops of the small intestine (B! and B2) and the firstand second halves of the large intestine (C, and C2)were systematically examined for parasites. Cestodeswere fixed, stained, and mounted as in Amin (1986a)and categorized as juveniles (strobila with no or onlyimmature proglottids), mature adults (posterior pro-glottids sexually mature), and gravid (at least someproglottids with eggs). Mean refers to the number ofworms recovered/number of fish examined, and prev-alence is the number offish infected/number examinedx 100. Representative specimens were deposited inthe U.S. National Museum Helminthological Collec-tion (USNM Helm. Coll.) and in the University ofNebraska State Museum Harold W. Manter Labora-tory Collection (HWML Coll.).

Results

Only walley from Silver Lake were found in-fected with either species of cestodes.

Variability

The morphometrics of B. formosus from wall-eye in Wisconsin were similar in the autumn and

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Copyright © 2011, The Helminthological Society of WashingtonCopyright © 2011, The Helminthological Society of Washington

Table 1. Comparison between major anatomical features of Bothriocephalus formosus from Wisconsin and the type material.4

Wisconsin material Type material

Character Autumn/springN=8

SummerN = 11

Mueller and Van Cleave(1932) description

USNM Helm. Coll. No. 8690 cotypesN=6

Strobilar length (mm)Max. width (mm)

Scolex length (mm)Max. width (mm)

Neck width (mm)Mature seg. length (mm)

Width (mm)Gravid seg. length (mm)

Width (mm)No. of segments

% gravidTestis dimensions (MHI)

No.Cirrus sac dimensionsOvary width (Mm)Egg length (MIH)

Width (/tm)Vitellaria dimensions (M

102.50 (74.00-130.00)f2.06(1.60-2.44)1.16(1.12-1.26)0.45 (0.36-0.52)0.27(0.22-0.31)0.60 (0.36-0.76)2.00(1.37-2.44)0.97(0.72-1.20)1.95(1.60-2.44)

380.2 (277^43)10.7 (8.0-16.0)

120 (106-134) x 110(80-128)50.7 (45-58)

285 (238-350) x 251 (196-336)630 (490-728)55 (48-64)39 (32-45)69 (48-83) x 54 (42-64)

29.50(18.00-38.00)1.11 (0.84-1.37)0.83 (0.70-0.98)0.37 (0.27-0.42)0.18(0.15-0.31)0.40 (0.28-0.49)0.88(0.71-1.09)0.53 (0.42-0.63)1.11 (0.84-1.37)

119.9 (81-158)17.7 (8.0-30.0)89 (76-109) x 76(61-99)44.1 (34-60)

204 (154-238) x 186(140-238)399 (294-560)53 (48-64)38 (32-48)54 (38-64) x 44(35-51)

Rarely exceeding 301.30.32-0.4750.13-0.23Similar to scolex width0.4-0.60.8-1.2

1.3

30-45

53-5933-35

27.15(21.20-34.00)1.05(1.00-1.12)0.46 (0.42-0.49)0.20(0.14-0.25)0.16(0.14-0.17)0.54 (0.40-0.60)0.97(0.88-1.12)0.69 (0.60-0.84)1.03(0.92-1.12)

105.7 (92-120)14.5 (6.0-27.0)81 (70-112) x 68(58-90)41.5 (32-55)t

151 (115-196) x 132 (96-154)§274 (238-322)56 (51-61)41 (38-48)42 (32-51) x 33(26-42)

* All the Wisconsin specimens and the cotypes were gravid.t Mean (range). Two testes, cirrus sacs, ovaries, eggs, and vitelline glands were measured and/or counted in each cestode.$ Only developing testes could be counted until obscured by forming vitellaria. Numbers shown may be underestimates.§ The size of the cirrus sac increases considerably in posteriormost proglottids of complete worms. Indicated size was probably affected by a few missing segments from 3 worms.

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78 JOURNAL OF THE HELMINTHOLOGICAL SOCIETY

Table 2. Prevalence and mean intensity of Bothriocephalus formosus and B. cuspidatus infections in Stizostedionvitreum from Silver Lake, 1976-1979.

B. formosus

Fish inf./exam. (%)Worms (mean/exam, fish) max.

B. cuspidatus

Fish inf./exam. (%)Worms (mean/exam, fish) max.

Autumn(late Oct., Nov.)

15/23(65)313(13.6) 112

5/23 (22)62 (2.7) 47

Spring(April )

20/21 (95)529 (25.2) 93

12/21 (57)415(19.8) 120

Summer(June-early Aug.)

6/10(60)368 (36.8) 285

0/100

Total

41/54(76)1,210(22.4)285

17.54(31)477 (8.8) 120

spring collections; data were combined (Table 1).Summer worms were considerably shorter andmeasured structures were smaller. Meristic andmorphometric features in 19 worms with com-plete strobilae were compared with the incom-plete description of Mueller and Van Cleave(1932), as well as with measured samples of theircotypes (Table 1). Available museum specimensof B. formosus and B. daviceps were also ex-amined for verification of identity.

Seasonality

Prevalence and intensity of infection were con-siderably higher for B. formosus (76%, 22.4) thanfor B. cuspidatus (31%, 8.8) (Table 2). Walleyewere most frequently and heavily infected withB. formosus during summer and with B. cuspi-datus during spring (Table 2). Summer infectionswith B. formosus were influenced by 1 heavilyinfected fish that had 285 worms.

Table 3. Seasonal development of Bothriocephalusformosus and B, cuspidatus in Stizostedion vitreum fromSilver Lake, 1976-1979.

Number and prevalence (%)of worms

Cestode develop-mental stages

B. formosus

Al l stagesJuvenile (%)*Mature (%)Gravid (%)

B. cuspidatus

Al l stagesJuvenile (%)Mature (%)Gravid (%)

No. ofworms

1,21097318453

4773359329

Autumn(lateOct.,Nov.)

313293 (94)

8(2)12(4)

620(0)

41 (66)21 (34)

Spring(April )

529432 (82)

88(17)9(2)

415355 (86)52(13)8(2)

Summer(June-earlyAug.)

368248 (67)88 (24)32(9)

00(0)0(0)0(0)

* The percent prevalence compares data in vertical columns.

Walleye harbored juvenile and gravid B. for-mosus during all seasons; most worms recoveredduring autumn were juveniles (94%), and thehighest proportion of mature and gravid adults(33%) was obtained during the summer (Table3). No B. cuspidatus were found in walleye duringsummer; most spring worms were juveniles(86%), and all autumn worms were mature (66%)or gravid (34%) adults (Table 3).

Host relations

Parameters of B. formosus and B. cuspidatusinfections were not affected by host sex. Preva-lence and mean intensity of B. formosus infec-tions were 79% and 19.0 in 28 male and 73%and 26.0 in 26 female walleye. B. cuspidatus in-fections were 36% and 9.1 and 30% and 8.5 inmale and female walleye, respectively. No par-ticular relationship between rates of infection andfish size was apparent; males and females werenot significantly different in size.

Site of infection

Pyloric ceca of walleye appear to be the pre-ferred sites of infection with both species of Both-riocephalus, particularly B. cuspidatus, during allseasons (Table 4). However, gravid worms oc-curred with similar frequency in both cecal andintestinal sites.

Infections in other hosts

The only adult B. formosus not collected fromS. vitreum were 13 gravid worms from the py-loric ceca of 3 green sunfish, Lepomis cyanellus,captured in Tichigan Lake Canal during the sum-mer of 1979. In addition, 13 larval B. formosus(Bf) and 9 larval B. cuspidatus (Be) were foundduring the spring (20) and summer (2) of 1978on the liver of 6 fishes, 1 Pomoxis annularis (1Be), 2 S. vitreum (3 Bf), 1 Pomoxis nigromacu-latus (1 Be), 1 Micropterus salmoides (11 Bf, 5


OF WASHINGTON, VOLUME 59, NUMBER 1, JANUARY 1992 79

Table 4. Seasonal site selection of Bothriocephalus formosus and B. cuspidatus in Stizostedion vitreum fromSilver Lake, 1976-1979.

Season

B. formosusAutumnspringSummer

B. cuspidatusAutumnSpring

No. ofworms

313529368

62415

Percent of worms in intestinal regions (% of juveniles, adults, gravid worms)*

A

5(100,0,0)1 (83, 17,0)

12(66, 29, 5)f

00

Ceca

59 (90, 5, 5)68 (76, 22, 2)50(68,25,7)

97 (0, 65, 35)85(86, 12,2)

B

32 (97, 0, 3)30(95,4, 1)37(67,20, 13)

1.5(0, 100,0)15(84, 14,2)

c,

4(100,0,0)0.4 (50, 50, 0)1 (50, 0, 50)

1.5(0, 100,0)0

C2

00.4 (100, 0, 0)0

00

* Percent of worms in the stomach (A), ceca, small intestine (B), and first and second halves of large intestine (C, and C2)(percent of juveniles with only immature segments if segmented, adults with sexually mature segments, adults with segmentsgravid with eggs).

t It is possible that regurgitation was a variable affecting this anterior localization of worms.

Be) and 1 Ambloplites rupestris(\) from SilverLake. Cestodes from walleye were 3-22 mm longand with 6-70 segments each. Those from otherhosts were 2-9 mm long and with 2-35 segmentseach. The scolex was well denned in all juveniles.

Discussion

Morphometric and meristic features of B. cus-pidatus were similar in shape and size to thoseoriginally described by Cooper (1917) and sub-sequent observers (Van Cleave and Mueller,1934; Hugghins, 1972). Thus, morphometricanalysis was not warranted. The smaller summerB. formosus from Wisconsin were similar to thosein the original description (Table 1). Mueller andVan Cleave's (1932) specimens were collectedduring the summer. Therefore, their descriptionof B. formosus does not express the full range ofvariation exhibited by B. formosus in this study(Table 1). The scolex of B. formosus from Wis-consin agrees with the text description of Muellerand Van Cleave (1932). However, the scolex ofOneida Lake cestodes (Mueller and Van Cleave,1932, fig. 20) was markedly smaller (Table 1)and its anterior tip was more dome-shaped. Thedome-shaped scolex tip of the 6 cotypes (USNMHelm. Coll. No. 8690) (Table 1) was barely tomoderately pronounced. Observed scolex differ-ences are not considered sufficient to warrantconsidering Wisconsin material as a new species.Proglottids of the Wisconsin material were sim-ilar to those in the original description knownonly from summer material.

Reference specimens made available for studyincluded B. formosus cotypes collected by J. F.Mueller in 1932 from Percopsis omiscomaycus

in Oneida Lake (USNM Helm. Coll No. 8690)and B. formosus from Etheostoma nigrum inChippewa County, Wisconsin (USNM Helm.Coll. No. 78221), which were identical to mymaterial. Misidentifications included "B. for-mosus" from E. nigrum in Ingram County,Michigan (USNM Helm. Coll. No. 76699) andfrom Pimephalus notatus in Posey County, In-diana (HWML Coll. No. 21487), as well as "B.daviceps" (actually B. formosus) from Lepomiscyanellus in Keith County, Nebraska (HWMLColl. Nos. 19827, 19893).

Summer B. formosus and their reproductivestructures (except egg size) were considerablysmaller compared to autumn-spring worms (Ta-ble 1). Number of proglottids/strobila was alsoconsiderably fewer, but percent of gravid seg-ments was greater in summer (Table 1). Clearlythese data represent a seasonal (temperature-re-lated) growth-maturity phenomenon. Growthappears to proceed quickly during the autumn(early in the infection cycle) and large size isretained in the overwintering worms. In the sum-mer, rapid maturation, perhaps of new recruits,leads to small size adults. Musselius (1962 inDavydov, 1978) reported that cestodes in fishintestines at water temperatures of 22-25°C ma-ture and produce eggs almost twice as fast as at16-19°C. It took Bothriocephalus acheilognathiYamaguti, 1934, 12-14 and 22-25 days to attainsexual maturity at 22-25° and 15-18°C, respec-tively (Davydov, 1978). Granath and Esch (1983)noted that development of B. acheilognathi fromNorth Carolina was stimulated by water tem-perature. Growth and fecundity of B. acheilo-gnathi were also found by Davydov (1978) to be


80 JOURNAL OF THE HELMINTHOLOGICAL SOCIETY

dependent on worm size and affected by tem-perature. Moravec (1985) reported that gravidB. daviceps from Czechoslovakia were larger inMay to July than in August. Robert et al. (1988)observed many large segments of Bothriocepha-lus gregarius from France during July comparedto the fewer and smaller segments observed laterin the season. Bona (1983) shed more light onthis phenomenon with his careful biometricalstudy of the dilepidid cestode Dendrouterina pil-herodiae Mahon, 1956. He analyzed differentialrate of growth versus development and proposeda model showing how adult proglottids of dif-ferent sizes can form. He concluded that growthassumes an S-shaped curve with an increasing,then a decreasing, rate. Wisconsin material alsoindicates that this growth-development phenom-enon is additionally affected by host species. The13 gravid B.formosus collected from L. cyanellusin Tichigan Lake Canal during the summer weresimilar in size to the larger autumn-spring wormsobtained from walleye in Silver Lake (Table 1).This may represent an ecological phenomenonrelated to L. cyanellus becoming active and feed-ing on intermediate hosts earlier in the spring,or to its gut size. Riggs et al. (1987) also notedthe relationship between size and fecundity of B.acheilognathi and cyprinid and poecilid fish hostspecies and gut size in North Carolina. The ab-sence of other collections from green sunfish fromWisconsin during other seasons does not allowfurther elaboration on that point.

Bothriocephalus cuspidatus is a common par-asite of walleye (Van Cleave and Mueller, 1934;Hugghins, 1972; Deutsch, 1977; Sutherland andHolloway, 1979; Robinson and Jahn, 1980; andothers). In land-locked Silver Lake, B. cuspidatuswas far less common than B. formosus in walleye(Table 2). Neither species was found in 55 wall-eye examined from Tichigan Lake and its canal.Appropriate intermediate hosts are probablypresent in Tichigan Lake system as indicated byinfection of L. cyanellus from the Tichigan LakeCanal. However, the vagile green sunfish mighthave picked up the infection elsewhere, e.g., theFox River. Other helminth species also found tobe more dominant in Silver Lake fishes com-pared to Tichigan Lake include Proteocephalusambloplitis (Leidy, 1887) Benedict, 1900 (seeAmin, 1990a; Amin and Cowen, 1990), cary-ophyllaeid cestodes (Amin, 1986a), and Neoe-chinorhynchus spp. (Amin, 1986b). The oppositetrend was observed in Pomphorhynchus bulbo-

colli Linkins in Van Cleave, 1919 (see Amin,1987) and similar infection parameters were not-ed for Proteocephalus pinguis La Rue, 1911, inboth lakes (Amin, 1990b). Environmental pe-cularities and ecological variables, relating to dif-ferences in the lif e cycles of each of the parasiticgroups, particularly the intermediate host, mayaccount for the expression of the above patterns.Parasites using cyclopoid copepods are less rep-resented in Tichigan than in Silver Lake.

The similar prevalence and intensity of bothB. formosus and B. cuspidatus infections in maleand female walleye of all sizes over 15 cm appearto reflect a relatively uniform level of infectionin fish paratenic hosts since walleye become pi-scivorous at about 6-8 cm (Niemuth et al., 1972).No second intermediate host is necessary in thecycle of both species of cestodes. This pattern ofinfection with Bothriocephalus was previouslynoted by Essex (1928), Mitchell and Hoffman(1980), and others. In the present study, thestomachs of some larger walleye contained wall-eye and bluegill, Lepomis macrochirus. These preyfish may represent a link in the chain of walleyeinfection in Silver Lake. The increased preva-lence of Bothriocephalus sp. in female yellowperch, Perca flavescens, in Ontario was appar-ently related to increased predation by older fe-males which, unlike males, "showed an increasein food size . . . (crayfish and fish) . . . with in-creasing size . . ." (Cannon, 1973). Similar re-lationships between intensity of infection and hostsize were also reported for B. daviceps from perch,Perca fluviatilis, in Czechoslovakia (Scholz, 1986)and for B. gregarius from turbot, Psetta maxima,in France (Robert et al., 1988).

Of the 54 walleye examined from Silver Lake,41 (76%) were infected with B. formosus and 17(31%) with B. cuspidatus (Table 2). All 17 fishinfected with B. cuspidatus were also concur-rently infected with B. formosus. Both speciesoccupied pyloric cecal sites (Table 4). Site selec-tion, interspecific competition, and/or season-ality of intermediate hosts may have influencedthe reproductive strategy of both cestode speciesin walleye. At the infrapopulation level, individ-ual concurrently infected walleye with high in-tensity of B.formosus infections usually had lightinfections with B. cuspidatus; the opposite wastrue. Bothriocephalus formosus appears to be thedominant cestode species in Silver Lake walleye.Recruitment, maturation, and reproduction of B.formosus occur during all seasons (Tables 2, 3).


OF WASHINGTON, VOLUME 59, NUMBER 1, JANUARY 1992 81

The major recruitment season appears to be au-tumn when 94% of cestodes were juveniles; par-tial generation overlap is indicated. Cestode build-up and maturation increased reaching a maxi-mum intensity (36.8) (Table 2) and proportionof mature and gravid worms (33%) (Table 3)during summer when the highest proportion innonpyloric cecal sites (37%) was noted (Table 4).No collections were made during winter. Theseasonality ofB.formosus has not been reportedin any other location in North America, but com-parable patterns were reported in other bothrio-cephalid cestodes, e.g., B. daviceps from eel (An-guilla anguilld) in Czechoslovakia (Moravec,1985), B. daviceps from perch (Perca fluviatilis)in Czechoslovakia (Scholz, 1986), and B. achei-lognathi from Gambusia affinis in North Caro-lina (Marcogliese and Esch, 1989).

The reproductive cycle of B. cuspidatus in Sil-ver Lake may be related to its decreased com-petitive success compared to B. formosus. Insummer, when B. formosus reached its peakabundance and reproductive activity, B. cuspi-datus was absent. This absence might have beenaffected by sample size of walleye but not its sexor size, which were shown above to be unrelatedto prevalence or intensity of infection. Peak re-productive activity of B. cuspidatus (100% ma-ture and gravid worms) was evident in the au-tumn (Table 3). This is in contrast to evidencefrom other studies of B. cuspidatus in single in-fections, which suggests that the usual breedingseason of B. cuspidatus is summer in its fish de-finitiv e hosts (Van Cleave and Mueller, 1934;Amin, 1975; and others). The seasonal displace-ment of B. cuspidatus and change in its repro-ductive cycle allowed temporal niche sharing inthe pyloric ceca of the same host species. Thepossible involvement of the seasonal distribu-tion of intermediate hosts, or other ecologicalvariables, in this phenomenon is not known.

The recovery of juveniles of both species ofBothriocephalus from the liver of P. annularis,P. nigromaculatus, S. vitreum, M. salmoides, andA. rupestris contrasts with Essex's (1928) originalcontention about the role of small fish as a sourceof infection of the definitive fish host. Essex (1928)originally thought that B. cuspidatus could betransmitted from fish to fish if the prey fish wasrecently ingested and had an infected copepodin its stomach. The fact that walleye of the sizesexamined in this study (15-45 cm) are piscivo-rous suggests that the above species of fish serve

as paratenic hosts in Silver Lake. This is the firstreport of fish paratenic hosts for either speciesof Bothriocephalus. Other sites for paratenic in-fection have, however, been noted, e.g., B. gre-garius metacestodes infected the intestine of goby(Robert et al., 1988).

Deposited Specimens

Bothriocephalus formosus: HWML Coll. Nos.31701-31707 and USNM Helm. Coll. Nos.81264-81268. Bothriocephalus cuspidatus:HWML Coll. Nos. 31708, 31709 and USNMHelm. Coll. Nos. 81269, 81270.

Acknowledgments

Dr. M. H. Pritchard, the University of Ne-braska State Museum, Lincoln, kindly providedinitial identification ofB.formosus. The loan ofvoucher material by Dr. Pritchard and by Dr. J.R. Lichtenfels, Animal Parasitology Institute,U.S. Department of Agriculture, Beltsville,Maryland, is appreciated. I am also grateful toall my former students who helped with fish col-lection and processing of slides, particularly Les-lie A. Burns and the late Robert J. Bauer.

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Cestoda from Lake Fishes in Wisconsin: The Ecology and...

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