cestoda from lake fishes in wisconsin: the ecology of...
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J. Helminthol. Soc. Wash.57(2), 1990, pp. 120-131
Cestoda from Lake Fishes in Wisconsin: The Ecology ofProteocephalus ambloplitis and Haplobothrium globuliforme inBass and Bowfin
OMAR M. AMI N AND MARSHA COWENDepartment of Biological Sciences, University of Wisconsin-Parkside, Box 2000, Kenosha, Wisconsin 53141
ABSTRACT: Findings on Proteocephalus ambloplitis (Leidy) from bass in 2 southeastern Wisconsin eutrophiclakes show the importance of critical temperatures and host size in the parenteric recruitment of this tapewormduring the spring. The effect of latitudinal differences in the seasonal development of P. ambloplitis in southeasternWisconsin compared with collections from elsewhere in North America are also noted. Enteric worms survivedfor up to 8 mo but lived and reproduced for longer periods in bowfin (Amia calvd) in which recruitment wasonly dependent on the ingestion of plerocercoid-infected fish intermediate hosts. In southeastern Wisconsin,bowfin appeared to be the important host in which the majority of the P. ambloplitis population circulates. Thetapeworm's initial establishment, maturation, and reproduction occurred in anteriormost digestive tract locationsin both bass and bowfin. Establishment of Haplobothrium globuliforme Cooper, 1914 occurs anteriorly in bowfin,but adult and gravid worms are found only in the large intestine during peak breeding in the summer. Adultslive up to 1 yr in the gut of bowfin. The mud minnow (Umbra limi) is a new intermediate host for H. globuliformeplerocercoids. The 2 tapeworm species had considerably denser populations in the closed system of Silver Lakethan in the larger river-connected Tichigan Lake. The seasonal development of both P. ambloplitis and H.globuliforme in bowfin is reported here for the first time. Notes on concurrent infections with acanthocephalans,other Proteocephalus species, and hyperparasitism are also included.
KEY WORDS: Cestoda, Proteocephalus ambloplitis, Proteocephalus spp., Haplobothrium globuliforme, seasonalecology, recruitment, infectious cycle, site selection, bass, bowfin, Wisconsin, concurrent infections, hyperpar-asitism.
The role of 16 fish species in the ecology ofProteocephalus ambloplitis (Leidy) plerocercoidsin 2 southeastern Wisconsin eutrophic lakes wasreported by Amin (1990). In the same 2 lakes,adults of this cestode species infect largemouthbass, Micropterus salmoides (Lacepede), andsmallmouth bass, M. dolomieui Lacepede, as wellas bowfin, Amia calva Linnaeus, which is alsoinfected with Haplobothrium globuliforme Coo-per, 1914. The ecological relationships amongthese organisms in southeastern Wisconsin areherein reported against a background that lacksany such information on H. globuliforme but in-volves various interpretations of some basic de-velopmental and ecological phenomena uniqueto P. ambloplitis known only from bass.
Cooper (1914, 1917) described H. globuli-forme and the fragmentation of its primary sco-lex. The study of the lif e history of this ancientand intriguing cestode was initiated by Essex(1929) and Thomas (1930) but was completedby Meinkoth (1947), based on material fromMichigan. The most recent work on H. globuli-forme is descriptive in nature, particularly at theultrastructural level, e.g., MacKinnon and Burt(1985a, b, c). This tapeworm infects only A. cal-va, an ancient fish itself, throughout the United
States and southern Canada. Proteocephalus am-bloplitis has a similar distribution range. Cooper(1915,1918) and Bangham (1927) provided ear-ly descriptions of the lif e history of the bass tape-worm, which was more completely investigatedby Hunter (1928) and Hunter and Hunter (1929).Freeman (19 7 3) and Fischer and Freeman (1969,1973), however, provided the first complete ac-count of its lif e history and the actual role ofplerocercoids in bass from Ontario. Subsequent-ly, the Ontario reference line was used to com-pare findings on the same cestode species fromMichigan and South Carolina bass by Esch et al.(1975) and Eure (1976), respectively. Relatedfindings from Wisconsin bass are described andcompared, and those from bowfin are reportedfor the first time. The ecology of//, globuliformein its only host, bowfin, is also reported here forthe first time.
Materials and Methods
The fishes examined were from Silver Lake (Keno-sha County), a 188-ha eutrophic land-locked lake, andfrom Tichigan Lake (Racine County), a 458-ha lake inan advanced state of eutrophication on the Fox River(a tributary of the Mississippi River). Seasonal collec-tions were made from both lakes during the spring(April) , summer (June, July, and early August), and
120
Copyright © 2011, The Helminthological Society of Washington
Table 1. Prevalence and intensity of Proteocephalus ambloplitis and Haplobothrium globuliforme in fishes of Silver and Tichigan lakes proper, 1976-1979.
Cestode species
Proteocephalusambloplitis
Haplobothriumglobuliforme
Fish species
Amia calva
Micropterussalmoides
Micropterusdolomieui
Amia calva
Season
SpringSummerAutumnTotal
SpringSummerAutumnTotal
SpringSummerAutumnTotal
SpringSummerAutumnTotal
N
783
18
28386
72
2204
783
18
Fish
Inf. (%)
7(100)6(75)3(100)
16(89)
26 (93)13(34)
1(17)40(56)
2(100)002(50)
2(29)6(75)1(33)9(50)
Silver Lake
N
84575788
1,690
54367
7617
9009
149305117571
Tichigan Lake
Cestodes
x/fish
120.794.629.393.8
19.41.81.28.57
4.5
——2.25
21.238.139.031.7
Max.
37245140
451
86377
86
6006
12794
117127
N
1355
232
192344
6102
18
1355
23
Fish
Inf. (%)
12(92)5(100)4(80)
21(91)
01(5)5(22)6(14)
0000
2(15)4(80)2(40)8(35)
TV
619218225
1,062
028
10
0000
42624
108
Cestodes
jc/fish
47.643.645.046.17
—0.10.40.27
-—
—0
3.212.40.84.70
Max.
195112112195
0222
0000
4141
341
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122 JOURNAL OF THE HELMINTHOLOGICAL SOCIETY
Table 2. The relationship between the size and sex of Mlcropterus salmoldes and M. dolomieui from Silver andTichigan lakes and infection with Proteocephalus ambloplitis, 1976-1979.
Proteocephalus ambloplitis
Fishspecies
Micropterussalmoldes
Totals
Totals
Micropterusdolomieui
Totals
Fish totalLake length (cm)
Silver 1 1-2021-3031-4041-50
Tichigan 1 1-2021-3031-4041-50
Tichigan 1 8-2028
INO. 01 maie nsn
Exam.
216110
29
6640
16
314
Inf. (%)
2(100)7(41)4(36)0
13(45)
0(0)1(17)0(0)01(6)
1 (33)1 (100)2(50)
N
1015410
66
01001459
x per
Exam.fish
5.00.93.7
—2.3
—0.2
——
0.01
1.35.02.25
INO. 01 lemaie nsn
Inf. fish
5.02.1
10.2—5.1
—1.0—
—1.0
4.05.04.50
Max.
74
180
18
01001455
Exam.
510171143
51283
28
000
Inf. (%)
0(0)6(60)
10(59)11 (100)27 (63)
0(0)2(17)1(12)2(67)5(18)
000
autumn (late October and November) between 1977and 1979 and from Silver Lake during the summer of1976. One thousand eight hundred twelve fishes rep-resenting 32 species and 10 families (Amiidae, 1 species;Catostomidae, 7; Centrarchidae, 9; Cyprinidae, 2;Esocidae, 2; Ictaluridae, 4; Lepisosteidae, 1; Percidae,2; Salmonidae, 2; Serranidae, 2) were captured by elec-troshocking from both lakes. An additional 1,543 fishesrepresenting 29 species and 11 families (Amiidae, 1;Catostomidae, 3; Centrarchidae, 6; Cyprinidae, 5; Cy-prinodontidae, 2; Esocidae, 2; Gasterosteidae, 1; Ic-taluridae, 4; Percidae, 3; Serranidae, 1; Umbridae, 1)were seined or minnow trapped in a channel drainingthe swampy western area of Tichigan Lake during 1978,1979, and 1981.
Fish were systematically dissected shortly after cap-ture. Specimens of parasites were processed as in Amin(1986a). The plerocercoid terminology of Freeman(1973) and Fischer and Freeman (1973) is used here.Representative specimens were deposited in the U.S.National Museum Helminthological Collection (USNMHelm. Coll.) and in the University of Nebraska StateMuseum's Harold W. Manter Laboratory Collection(HWML Coll.).
Results and Discussion
Host distribution
Prevalence and mean intensity of infectionswith P. ambloplitis were considerably greater inA. calva (89%, 93.9) than in either M salmoides(56%, 8.6) or M. dolomieui (50%, 2.2) from Sil-ver Lake. This pattern was consistent and moreextreme than in Tichigan Lake, where infectionswere considerably lighter (Table 1). It is clearthat the bowfin plays a major role in the flow ofthe P. ambloplitis suprapopulation in its fish de-finitive hosts in southeastern Wisconsin; see
Amin (1987) for a discussion of host role changes.Parenteric recruitment of middle plerocercoid IIinto the bass gut, particularly in smallmouth bass,as originally described by Fischer and Freeman(1969) is not relevant to infections in bowfin.The cycle of P. ambloplitis in southeastern Wis-consin was clearly influenced by bowfin preda-tion on plerocercoid-infected fish intermediatehosts, e.g., bowfin are not intermediate hosts ofP. ambloplitis (see Amin, 1990). Accordingly, the"critical" spring temperatures of 7-12°C neces-sary for parenteric recruitment in bass (up from4°C in Ontario and Michigan [Fischer and Free-man, 1969; Esch et al., 1975] and down from26°C in South Carolina [Eure, 1976]) is not rel-evant to bowfin. This may explain why infectionparameters of bowfin in the large river-connectedTichigan Lake were similar in all seasons (Table1). Parameters in bowfin from the smaller land-locked Silver Lake, which shows greater fluctua-tions in seasonal temperature, were probably in-dicative of the higher intensity of fish feedingduring spring and summer compared with au-tumn (Table 1).
Lake distribution
Both tapeworms (Table 1) had larger popula-tions in Silver Lake than in Tichigan Lake, asnoted earlier for P. ambloplitis plerocercoids(Amin, 1990), caryophyllaeid cestodes (Amin,1986a), and some acanthocephalan species(Amin, 1986b). The closed system in the land-locked Silver Lake clearly enhanced the popu-
Copyright © 2011, The Helminthological Society of Washington
OF WASHINGTON, VOLUME 57, NUMBER 2, JULY 1990 123
Table 2. Continued.
Proteocephalus ambloplitis
x per
N
089
303159551
0326
11
000
Exam.fish
_8.9
17.814.512.8
—0.30.32.00.4
—
—-
Proteocephalus ambloplitis
x perloiai no. 01 risn
Inf. fish
14.830.314.520.4
—1.52.03.02.2
——-
Max.
081863286
02255
000
Exam.
726281172
1118123
44
314
Inf. (%)
2(29)13(50)14(50)11 (100)40 (56)
0(0)3(17)1(8)2(67)6(14)
1(33)1 (100)2(50)
N
10104344159617
0426
12
459
Exam.fish
1.44.0
12.314.48.6
—0.20.22.00.3
1.35.02.3
Inf. fish
5.08.0
24.614.415.4_
1.32.03.02.0
4.05.04.5
Max.
781863286
02255
455
lation density of these helminths. Other variablesrelated to the different state of eutrophication inthe 2 lakes may include species composition, dis-tribution and density of the intermediate hosts,and the feeding strategy of the definitive hostsinvolved. The lower visibility in Tichigan Lakecould negatively affect feeding on infected preyby bass (a sight feeder) and contribute to the largedifference in prevalence in the 2 lakes (Table 1).Feeding of the bottom-dwelling bowfin (proba-bly an olfactory and tactile feeder) would not bestrongly affected by decreased visibility .
Host size and sexTwo of 7 M. salmoides below 20.0 cm in total
length (less than 2 yr old; see Pasch [1974]) fromSilver Lake were lightly infected with enteric P.ambloplitis', none of 11 similar fishes from Ti-chigan Lake were infected. Heavier and morefrequent infections were largely confined to ma-ture larger bass (Table 2). The shift from a mi-crocrustacean and insect diet to a fish diet inlarger largemouth bass started in 5-cm long bass(Pasch, 1974, among others). It is not certainwhether these data support the hormone factorhypothesis of Fischer and Freeman (1969) andEsch et al. (1975), who suggested that sex hor-mones of mature bass > 15.0 and >20.0 cm inlength, respectively, may affect the parenteric mi-gration of middle plerocercoid II in the bass gut.The possible contribution of cannibalism to theabundance of enteric P. ambloplitis in bass innot known. In both lakes, female largemouth bass
were considerably more heavily and more fre-quently infected than males (Table 2). Whetherfemale sex hormones have greater effect than malehormones in promoting parenteric recruitmentis not known. Fischer and Freeman (1969) in-dicated that proper rise in temperature and basssize (maturity), but "apparently" not bass sex,were important for penetration. The feeding be-havior of male vs. female bass is not known.
In A. calva, the smallest fish examined wereinfected with P. ambloplitis (Table 3). Althoughvirtually all bowfin were infected, larger fish fromboth lakes had heavier worm burdens, whichwould correspond with the larger volume of food(infected bass) eaten by these fish. Unlike thepattern in bass (Table 2), there appeared to beno marked difference in infection parameters bysex of A. calva (Table 3).
The pattern of//, globuliforme infection in A.calva (Table 4) was similar to that of/5, amblo-plitis from the same host (Table 3) except thatthe increase in H. globuliforme burden by fishsize was smaller, whereas the difference betweenfemale and male host infection parameters wasgreater. The lif e history of H. globuliforme issimilar to that of P. ambloplitis in A. calva butwithout the complication of the different typesof plerocercoids. Bowfin appear to become in-fected by ingesting a second fish intermediatehost, e.g., Lepomis or Ictalurus infected (withextraintestinal plerocercoids) from feeding onplerocercoid-infected copepods. The consider-ably greater intensity and higher prevalence of
Copyright © 2011, The Helminthological Society of Washington
124 JOURNAL OF THE HELMINTHOLOGICAL SOCIETY
Table 3. The relationship between the size and sex of Amia calva from Silver and Tichigan lakes and theintensity of infection with Proteocephalus ambloplitis, 1976-1979.
Proteocephalus ambloplitis
Lake
Silver
Totals
Tichigan
Totals
Fish totallength (cm)
20-2930-3940-4950-5960-69
20-2930-3940-4950-5960-69
INO. 01 maie nsn
Exam.
002507
1
02
110
14
Inf. (%)
002(100)3(60)05(71)
1 (100)02(100)
10(91)0
13(93)
N
00
241100
0341
6304
4500
517
x per
Exam.fish
_—
120.520.0—48.7
63.0—2.0
40.9—36.9
INO. ot icmaie nsn
Inf. fish
_
—120.533.3—68.2
63.0—2.0
45.0—39.8
Max.
00
159440
159
6303
1120
112
Exam.
551140
11
003429
Inf. (%)
55(100)1 (100)1 (100)4(100)0
11 (100)
002(67)3(75)2(100)7(78)
* Nine of these hosts were also infected with Haplobothrium globuliforme.t Eight of these hosts were also infected with Haplobothrium globuliforme.
infection in female than in male bowfin suggestsa larger volume of food intake in females vs.males of the same size. This argument may alsohold for bass.
Seasonal distribution
The distribution of P. ambloplitis in M. sal-moides from Silver Lake shows peak prevalenceand mean intensity in the spring (93%, 19.4),decreasing in the summer and autumn to 34%,1.8, and 17%, 1.2, respectively; the number ofworms from the same host in Tichigan Lake was
much smaller (Table 1). Most of the spring tape-worms were recently recruited immatures (7%plerocercoids and 78% juveniles) (Table 5) thatmust have reached enteric sites during April andMay, and possibly earlier. Some recently recruit-ed plerocercoids in bass and bowfin were con-siderably smaller (occasionally littl e more thana scolex) than many of those infecting body cav-ity organs (particularly ovaries) of fish interme-diate hosts (Amin, 1990). The summer wormsincluded a considerably higher proportion of ma-ture adults (58%) and gravid adults (8%), which
Table 4. The relationship between the size and sex of Amia calva from Silver and Tichigan lakes and theintensity of infection with Haplobothrium globuliforme, 1976-1979.
Haplobothrium globuliforme
Lake
Silver
Totals
Tichigan
Totals
Fish totallength (cm)
20-2930-3940-4950-5960-69
20-2930-3940-4950-5960-69
INO. 01 maie nsn
Exam.
002507
102
110
14
Inf. (%)
000000
1 (100)001(9)02(14)
N
000000
100304
x per
Exam.fish Inf. fish Max.
- - 0000
- 0o
1.0 1.0 1- 0
- - 00.3 3.0 3
00.3 2.0 3
No. of female fish
Exam.
51140
11
003429
Inf. (%)
3(60)1 (100)1 (100)4(100)09(82)
002(67)2(50)2(100)6(67)
* Al l these hosts were also infected with Proteocephalus ambloplitis.
Copyright © 2011, The Helminthological Society of Washington
OF WASHINGTON, VOLUME 57, NUMBER 2, JULY 1990 125
Table 3. Continued.
Proteocephahis ambloplitis Proteocephalus ambloplitis
x per
N
127372451399
01,349
00
11450
230394
Exam,fish
25.4372.0451.099.8—
122.6
_—38.012.5
115.043.8
Inf. fish
25.4372.0451.099.8—
122.6
——57.016.7
115.056.3
Max.
54372451132
0451
00
11227
195195
Total
Exam.
51390
18*
105
152
23f
no. off ish
Inf. (%)
5 (100)1 (100)3 (100)7 (78)0
16 (89)
1 (100)04 (80)
14 (93)2 (100)
21* (91)
x per
N
127372692499
01,690
630
118651230
1,062
Exam,fish
25.4372.0230.7
55.4—93.9
63.0—23.643.4
115.046.2$
Inf. fish
25.4372.0230.7
71.3—
105.6
63.0—29.546.5
115.050.6$
Max.
54372451132
0451
630
112151195195
t One 57-cm-long fish was not sexed. It contained 151 worms. This fish and its parasites were included in the totals but notunder either male or female columns.
disappeared from the dwindling autumn popu-lation in October and November. The abovefindings suggest a major recruitment (possiblymostly parenteric) beginning in late March andextending at least through June (25% of summermaterial were juveniles, Table 5). Maturationproceeded sufficiently fast to produce breedinggravid adults in the summer. By autumn mostworms had already disappeared, leaving only 7adults in 1 out of 6 bass examined. Mature adultsof the autumn were considerably smaller thanthe more robust ones of the summer. Clearly
there is no reason to suspect winter P. ambloplitisin the gut of M. salmoides. The few data fromM. dolomieui (Tables 1, 5) fit the pattern de-scribed in M. salmoides. Findings from bass thussuggest an enteric P. ambloplitis lif e span of nomore than 8 mo in southeastern Wisconsin, whichmay be a few weeks longer than that of the sametapeworm species in M. dolomieui reported inmore northern locations, e.g., Fischer and Free-man (1969) and Esch et al. (1975) from Ontarioand Michigan, respectively. Temperature gra-dient was probably involved in this latitudinal
Table 4. Continued.
Haplobothrium globuliforme Haplobothrium globuliforme
x per
N
1232294
3320
571
009
4352
104
Exam.fish
24.622.094.083.0
—51.9_
—3.0
10.826.011.6
Inf . fish
41.022.094.083.0
—63.4
_
—4.5
21.526.017.3
Max.
512294
1270
127
008
414141
Total
Exam.
51390
18
105
152
23
no. of fish
Inf . (%)
311409*
102328*
(60)(100)(33)(44)
(50)
(100)
(40)(20)(100)(35)
N
1232294
3320
571
109
4652
108
x per
Exam,fish
24.622.031.337.0
—31.7
1.0—1.83.1
26.04.7
Inf. fish
41.022.094.083.0
—63.4
1.0—4.5
15.326.013.5
Max.
512294
1270
12
108
414141
Copyright © 2011, The Helminthological Society of Washington
126
variation. In all other respects, our results fromWisconsin are in agreement with those of theabove authors and are thus supportive of thecritical temperature of parenteric recruitment inbass. The longer lif e span of parenteric P. am-bloplitis plerocercoids in bass or other species offish intermediate hosts (Amin, 1990) classes P.ambloplitis among the semelparous brevipatentone-time seasonal breeders with short adult lif espan (in bass); see Kennedy (1983). The increasein intensity of P. ambloplitis plerocercoids in old-er Lepomis macrochirus body cavity locationswas interpreted by Bailey (1984) as reflectingplerocercoid longevity. Bailey's (1984) obser-vation may also express an increased probabilityof exposure due to greater food intake by largefish. The seasonal maturation in this type of lif ehistory is clearly timed to coincide with the op-timal period for transmission when plankton aremost abundant. Seasonality may thus be moreeffectively determined at the level of the inter-mediate host, its seasonal and spatial availabil-ity, and dormancy.
The seasonal pattern of tapeworm infection inbowfin adds a new dimension to the develop-mental aspects of P. ambloplitis population ecol-ogy that is of major importance because A. calvaappears to be the major definitive host in south-eastern Wisconsin (Table 1). The parenteric re-cruitment and its associated critical spring tem-peratures as well as the potential hormonal factorexcluding recruitment in immature bass are notparts of the bowfin biological system (see Hostdistribution, Host size and sex, above). The mostimportant remaining variable is the feeding be-havior. The prevalence of P. ambloplitis in A.calva from both lakes as well as the mean inten-sity of infection in Tichigan Lake showed noseasonal differences. The mean intensity in SilverLake was, however, lower in the autumn, prob-ably reflecting less feeding activity (Table 1). Thesmaller land-locked Silver Lake probably showsmore extremes of seasonal temperatures. In thatlake, the proportion of mature worms in bowfinin the spring (37%) was considerably higher thanin largemouth bass (15%), was stable through thesummer (38%), and peaked in the autumn (83%)(Table 5). Freshly recruited plerocercoids and ju-veniles as well as gravid worms were also rep-resented in the autumn. These conditions wereeven more pronounced in Tichigan Lake where84% of the spring worms were mature (3 speci-mens were gravid) and 16% of the autumn spec-
imens were gravid. It is clear from the abovefindings, and in the absence of the constraintsoperating on bass, that the recruitment season inbowfin must begin well before April , with egglaying extending well past November. This sig-nificantly increases the length of the breedingseason of P. ambloplitis in A. calva and thusincreases its reproductive potential. It is inter-esting to come across 2 such different reproduc-tive strategies of the same tapeworm infecting 2genera of fish definitive hosts in the same bodyof water.
Infection parameters of H. globuliforme in A.calva were more or less seasonally stable in SilverLake but were less consistent in Tichigan Lake(Table 1). Like P. ambloplitis in bowfin, the lif ecycle of//, globuliforme involves a copepod andfish intermediate hosts whose distribution andseasonal availability may differ in both lakes.Recently recruited H. globuliforme juveniles wererepresented in all collections from both lakes, butin Silver Lake, a high proportion (41 %) was pres-ent during the spring, suggesting more active re-cruitment then. Primary scolices were found onlyon about one-half of the juvenile worms; the restof the juveniles and all other stages had onlysecondary scolices (Table 6). Worms with pri-mary scolices were clearly the youngest and rep-resented the earliest recruitments. MacKinnonand Burt (1985c) also observed a higher propor-tion of H. globuliforme collected from A. calvain Lake Ontario in late June than in late August.In Silver Lake, maturation and breeding in-creased during the warmer months from 36%mature and 19% gravid in the spring to 33% and37% in the summer; no gravid worms were re-covered during the autumn but recruitment con-tinued (Table 6). Worms matured more rapidlyin Tichigan Lake, but both mature and gravidworms disappeared by October. The above ob-servations and the lighter autumn infections,particularly in Tichigan Lake, suggest the ab-sence of//, globuliforme from bowfin during thewinter.
Twenty-four H. globuliforme plerocercoidswere recovered from the body cavity of 19 of 66(29%) mud minnows, Umbra limi (Kirtland), ex-amined from Tichigan Lake canal during thesummer. Most of these were excysted from dou-ble-walled cysts. The outer cyst wall appeared tobe of host origin—a new observation. The plero-cercoids resembled the pyriform ones reportedby Meinkoth (1947, Fig. 1) from the liver of
Copyright © 2011, The Helminthological Society of Washington
Table 5. Seasonal development of Proteocephalus ambloplitis in fishes from Silver and Tichigan lakes, 1976-1979.
Lake Fish species
Silver Amia calvaMicropterus
salmoidesMicropterus
dolomieuiTotal
Tichigan Amia calvaMicropterus
salmoides
Total
* Terminal plerocercoids.
Spring (Apr)
Plero-cercoids* Juvenilesf Mature
845 461(54) 73(9) 311(37)543 40(7) 424(78) 79(15)
9 6(67) 0 3(33)
1,397 507(36) 497(36) 393(28)
619 25(4) 70(11) 521(84)0 0 0 0
619 25(4) 70(11) 521(84)
Summer (Jun-early Aug)
Gravid(%)
00
0
0
3d)0
3(1)
N
75767
0
824
2182
220
Plero-cercoids
248 (33)17(25)
0
265 (32)
3(1)0
3d)
Juveniles
190(25)6(9)
0
196(24)
19(9)0
19(9)
Mature
291 (38)39(58)
0
330 (40)
144(66)0
144(65)
Gravid
28(4)5(8)
0
33(4)
52 (24)2(100)
54 (25)
N
887
0
95
2258
233
Autumn (late Oct, Nov)
Plero-cercoids
(%)
2(2)0
0
2(2)
21(9)0
21(9)
Juveniles(%)
9(10)0
0
9(10)
26(12)1(13)
27(12)
Mature
73 (83)7(100)
0
80 (84)
140(62)7(87)
147(63)
Gravid(%)
4(5)
0
4(4)
38(17)0
38(16)
t Segmented but still small and sexually immature.
OF WASH]NGTON, \
5w„->2ctfl*J
Ci-1
Table 6. Seasonal development of Haplobothrium globuliforme in Amia calva of Silver and Tichigan lakes, 1976-1979.
Lake
SilverTichigan
N
14942
Juv. 1*
29(19)2(5)
Spring (Apr)
Juv. 2f Young:|: Mature Gravid
32(22) 6(4) 54(36) 28(19)0 9(21) 20(48) 11(26)
Summer (Jun-early Aug)
N
30562
Juv. 1 Juv. 2
39(13) 8(3)4(7) 0
Young
44(14)2(3)
Mature
102(33)18(29)
Gravid
112(37)38(61)
N
1174
Autumn (late Oct, Nov)
Juv. 1 Juv. 2
17(15) 11(9)4(100) 0
Young(%)
32 (27)0
Mature Gravid
57 (49) 00 0
* Juveniles with primary scolex.t Juveniles with secondary scolex.i Larger worms but still without sexually mature segments.
Copyrig
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2011, T
he H
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128 JOURNAL OF THE HELMINTHOLOGICAL SOCIETY
Table 7. Seasonal site selection of Haplobothrium globuliforme in Amia calva and Proteocephalus ambloplitisin Amia calva, Micropterus salmoides, and Micropterus dolomieui from Silver and Tichigan lakes, 1976-1979.
Spring (Apr) (%)*
Cestode
Haplobothriumglobuliforme
Proteocephalusambloplitis
Host species
Amia calva
Amia calva
Micropterussalmoides
Micropterusdolomieui
Lake
SilverTichigan
SilverTichigan
SilverTichigan
SilverTichigan
TV
14942
845619
543
9
At
49.126.0
38.3
33.3
Ce Bl
1.3
- 41.9- 38.9
38.7 11.4
11.1 55.6
B2 Cl
23.583.3
1.3 6.9- 33.6
6.6 1.9
— —
C2
33.614.3
0.20.5
3.1
—
C3
41.62.4
0.61.0
—
* % of worms in intestinal regions.t A: stomach; Ce: cecum; Bl , B2: small intestine; C1-C3: large intestine. (Amia calva has no cecum and Micropterus has no
C3.)
guppies, Poecilia reticulata Peters. The Wiscon-sin specimens, however, were more elongate witha distinct long cylindrical neck and a bladder thatwas either abruptly spheroidal (in 1 specimen)or gradually enlarged distally. Umbra limi is anew intermediate host for H. globuliforme.
Seasonal site selection
Data from Table 7 show anteriormost local-ization of H. globuliforme during the summer.During the summer, stomach (A) and small in-testine (Bl, B2) were occupied by 9.2, 32.1, and36.7% of worms, respectively (Table 7). Quickposterior migration would clearly reduce com-petition with P. ambloplitis, which usually oc-cupy anterior locations. Regions A and B in A.calva were practically free of//, globuliforme in-fections during autumn and spring.
Site selection of P. ambloplitis in A. calva didnot show any particular seasonal predeliction.The anteriormost gut regions (A, Bl ) appear tobe the optimum sites for maturation and breed-ing, as they are for initial establishment of P.ambloplitis in A. calva during all seasons.
In bass, different forces appear to be involvedin the seasonal site selection of P. ambloplitis.Here the major parenteric recruitment occurredlargely during the spring, but most of the wormsfrom Silver Lake (the larger sample) were in thestomach (38.3%) and the cecum (38.7%) (Table7). The ceca of bass appear to be optimum forP. ambloplitis maturation and breeding. Thestomach distribution appears to have been anartifact of regurgitation upon capture. Wormsfound in other intestinal locations (also from M.dolomieui) were mostly enteric plerocercoids
(terminal-II) that must have just penetrated thegut wall.
Concurrent infections
Both species of Micropterus were also com-monly infected with Neoechinorhynchus cylin-dratus (Van Cleave, 1913) Van Cleave, 1919 andLeptorhynchoides thecatus (Linton, 1891) Kos-tylev, 1924 (Acanthocephala) and less common-ly with Camallanus oxycephalus Ward and Ma-gath, 1916 (Nematoda) in both lakes. Rareinfections with Neoechinorhynchus prolixoidesBullock, 1963 in both bass species were also not-ed from Silver Lake, and 1 largemouth bass fromTichigan Lake was infected with 1 Pomphorhyn-chus bulbocolli Linkins in Van Cleave, 1919(Acanthocephala). The anterior position of bothP. ambloplitis and L. thecatus did not show sig-nificant seasonal changes, whereas N. cylindratusunderwent marked posterior migration betweenautumn and summer (see Amin [1986b] for de-tails).
Amia calva was also occasionally infected withthe trematodes Azygia longa (Leidy, 1851) inboth lakes, A. angusticauda (Stafford, 1904)Manter, 1926 in Tichigan Lake, and Macro-deroides spiniferus Pearse, 1924 in Silver Lake.Azygia spp. primarily occupied the stomach, andM. spiniferus were confined to the posterior 75%of the gut (Amin, 1982).
Hyperparasitism
One adult P. ambloplitis in the cecum of a 36-cm-long male largemouth bass from Silver Lakeexamined during the spring was penetrated by amale L. thecatus. Similarly, a P. ambloplitis pie-
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OF WASHINGTON, VOLUME 57, NUMBER 2, JULY 1990 129
Table 7. Continued.
Summer (Jun-early Aug) (%)
N
30562
757218
672
A
9.23.2
83.559.2
43.3100.0
Ce Bl B2
- 32.1 36.724.2
- 11.5 1.139.4
23.9 3.0 10.4— — —
Cl
15.872.6
1.4-
3.0—
C2 C3
2.6 3.6-
0.3 2.20.5 0.9
16.4 -— —
N A
117 -4 —
88 80.7225 46.2
1
10 10.0
Autumn (late Oct, Nov) (%)
Ce Bl
-
19.331.1
- 28.620.0 40.0
B2 Cl
- 95.775.0
_ _
9.4
42.9 -20.0 10.0
C2
1.725.0_
13.3
28.5—
C3
2.6-
-
_
—
rocercoid in the liver of a 46-cm-long femalelargemouth bass from Tichigan Lake examinedduring the autumn was penetrated by a femaleL. thecatus. Leptorhynchoides thecatus occasion-ally passes into extraintestinal sites of centrar-chids (Amin, unpubl.)- Both incidents appear tobe chance occurrences. Two other similar asso-ciations were previously reported by Miller (1946)of Echinorhynchus salvelini Schrank, 1788(=Pomphorhynchus laevis) (Zoega in Muller,1776) Van Cleave, 1924 attached to Eubothriumsalvelini (Schrank, 1790) and by Muzzall andRabalais (1975) of Acanthocephalus jacksoniBullock, 1962 (=A. dints (Van Cleave, 1931) VanCleave and Townsend, 1936) attached to Pro-teocephalus sp. The first case was attributed toovercrowding and the second to chance occur-rence.
Other helminths
A few individuals of at least 3 species of Pro-teocephalus Weinland, 1858 were found in thececa and intestines of largemouth bass from bothlakes. One species (1 mature individual 130 mmlong) in a Silver Lake bass had 4 suckers, eachwith pointed apex, and a sizable vestigial fift hsucker in a broad anterior depression. Anotherspecies (6 immature worms 20-40 mm long) fromSilver Lake had 4 large highly muscular suckersdeeply set in an expanded bulbous scolex wellset off from a long neck, with faint segmentation.A third species (7 immatures 1-3 mm long and6 mature adults 9-23 mm long) from both lakeshad a gradually expanded scolex with 4 ovoidlyexpanded suckers and a dome-shaped fifth, al-most equally expanded and not much smaller.
The juveniles and adults of this third species mayactually belong to 2 different species. The abovematerial was not sufficiently informative to as-sign satisfactory specific identifications. Al l spec-imens clearly only accidentally infected bass.
Conclusions
Al l work reported so far on the lif e history anddevelopment of P. ambloplitis since Cooper's(1918) earliest account has reported bass, Mi-cropterus spp., as the definitive host. The morerecent additions to Hunter's (1928) and Hunterand Hunter's (1929) scheme and the understand-ing of parenteric migration of plerocercoids byFischer and Freeman (1969, 1973), Esch et al.(1975), and Eure (1976) were also based on stud-ies of M. dolotnieui. Records of bowfin as a hostof adult P. ambloplitis were noted by Hoffman(1967). This study shows that bowfin, and notbass, is the major host off. ambloplitis in south-eastern Wisconsin This host specificity occurs inthe presence of large populations of bass in thesame waters. This is clearly a matter of morethan "host role change" as explained by Amin(1987) and must involve a certain element ofhost preference. The role of other definitive hosts,e.g., Morone chrysops and M. mississippiensis(Arnold et al., 1968; McReynolds and Webster,1980) in the biology of P. ambloplitis is notknown.
Bowfin become infected by ingesting plerocer-coid (middle-II)-infected fish intermediate hosts.Enteric P. ambloplitis has a longer lif e span anda longer breeding season in bowfin than in bass,even though it also seems to disappear duringthe winter. In bass, P. ambloplitis is present for
Copyright © 2011, The Helminthological Society of Washington
130 JOURNAL OF THE HELMINTHOLOGICAL SOCIETY
no more than 8 mo, with parenteric recruitmentoccurring mostly during the spring and possiblyinfluenced by host size (sexual maturity), as hasbeen reported in Ontario and Michigan by Fi-scher and Freeman (1969) and Esch et al. (1975),respectively. In these 2 locations, the lif e span ofenteric P. ambloplitis appeared to be somewhatshorter than in Wisconsin bass (this study). En-teric infections in the winter (absent betweenSeptember and November) were reported inSouth Carolina (Eure, 1976). The following fac-tors thus appear to influence the seasonal devel-opment of P. ambloplitis: (1) temperature, (2)latitudinal differences, (3) host size (hormonalfactors), and (4) host species. The first 3 factorswere explored earlier (Fischer and Freeman, 1969;Esch et al., 1975; Eure, 1976) in bass and are, atleast partially, supported by this study.
Initial establishment and maturation of P. am-bloplitis appear to occur in the anteriormost lo-cations of both bass and bowfin digestive tracts.These traits were not significantly seasonallyvariable. Although initial establishment of H.globuliformc appeared also to have occurred inthe anteriormost gut locations of the bowfin, fur-ther development and breeding occurred exclu-sively in the large intestine. Metabolic require-ments of maturation and reproduction as well asdecreasing competition with P. ambloplitis, whichconsistently occupied anterior gut regions of thishost, probably influenced the location of//, glob-uliforme. Recruitment of H. globuliforme in A.calva, like that of P. ambloplitis, depended onthe ingestion of plerocercoid-infected fish inter-mediate hosts, involving at least U. limi in Tichi-gan Lake during the summer, with active repro-duction occurring during the spring and peakingin the summer. Adult H. globuliforme appear tolive in A. calva from recruitment of initial ju-veniles in spring and summer to gravid adults inthe same summer. The seasonal ecology of //.globuliforme in its fish definitive host, A. calva,is reported here for the first time.
Both tapeworm species had larger populationsizes in the smaller land-locked Silver Lake thanin the larger river-connected Tichigan Lake. Thedifference in tapeworm distribution and preva-lence between lakes may also have been relatedto differences in eutrophication levels affectingintermediate host population parameters andvisibilit y as well as definitive host feeding strat-egies. The enhancement of population density ofother helminth species in closed systems like Sil-ver Lake has also been demonstrated (Amin,
1986a, b). Seasonal differences in temperature(more extreme in Silver Lake than in TichiganLake) appeared to have affected the feeding be-havior and subsequently the recruitment of tape-worms, e.g., P. ambloplitis, by A. calva.
Of the relatively common helminth associatesin bass, only L. thecatus shared anterior gut lo-cations with P. ambloplitis; neither helminthshowed significant seasonal changes in site se-lection. This clearly provided the opportunity foran accidental (opportunistic?) attachment of 1 L.thecatus to an individual P. ambloplitis.
Deposited Specimens
Haplobothrium globuliforme from A. calvafrom Tichigan Lake (USNM Helm. Coll. Nos.80515-80518) and from Silver Lake (HWMLColl. Nos. 24913-24922). Proteocephalus am-bloplitis from A. calva from Tichigan Lake(USNM Helm. Coll. Nos. 80519-80522) andfrom Silver Lake (HWML Coll. Nos. 24923-24933), and from M. salmoides from TichiganLake (USNM Helm. Coll. Nos. 80523-80525)and from Silver Lake (HWML Coll. Nos. 24934-24946).
Acknowledgments
Dr. Gerald W. Esch, Wake Forest University,Winston-Salem, North Carolina, kindly re-viewed the manuscript.
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