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Utilization of the trophic structure of small pond ecosystems by helminths of frogs, Rana catesbeiana and Rana utricularia.

ABSTRACT. -- One hundred and thirty-three adult Rana catesbeiana (bullfrogs), 86 adult R. utricularia (southern leopard frogs) and 200 tadpoles of both species were collected from September 1975 through September 1977 in Brazos County, Texas and examined for endohelminths. Adult R. catesbeiana were infected with 31 species of helminths, adult R. utricularia were infected with 28 helminth species and 17 species of helminths were found in tadpoles. The life cycles of all helminths encountered were verified for south-central Texas through laboratory experiments and/or field observations, and the laboratory and field data collected were used to develop trophic diagrams for the analysis of the role of helminth life cycles in these aquatic ecosystems. Key words: trophic structure; ecosystems; helminths; frogs; Rana.

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Small pond ecosystems are an important resource for many ranches and farms in North America. In south-central Texas these small stock ponds are generally permanent, man-made ecosystems supporting a variety of aquatic and semiaquatic organisms which apparently orginated from the more complex oxbow lake ecosystems. Stock ponds may range in age from those established in pioneer times to those of recent origin. Despite the ubiquity of such ecosystems, there appears to be no synthetic studies on the role of helminth parasites in such ecosystems.

Frogs, Rana catesbeiana Shaw, 1802 (bullfrogs) and Rana utricularia Collins, 1990 (southern leopard frogs) were universally present in these ponds and were therefore chosen for this study. The purpose was to examine how the helminth parasites of these two species of frogs utilize, through their life cycle strategies, the trophic structures of permanent stock ponds.

MATERIALS AND METHODS

A total of 133 adult R. catesbeiana, 86 adult R. utricularia and 200 tadpoles of both species were collected from six permanent stock ponds in Brazos County, Texas from September 1975 through September 1977 and examined for adult and larval helminth parasites. Counts were made of adult and pre-adult helminths, but no counts of larvae were made. Although at least some aspects of the life cycles of most of these helminths had been reported previously (Tables 1 and 2), life cycles were verified for south-central Texas through laboratory experiments and/or field studies. Data collected were used to develop life cycle diagrams (Figs. 1 through 5) and to determine how the life cycle strategies of these helminths utilize the trophic structures of these small stock ponds.

Diagrams which were developed to depict the life cycle strategies of helminths infecting these two species of frogs as definitive hosts (Figs. 1, 2, 3, and 4) are basically composed of three trophic level boxes: 1) C-1, representing the first consumer level (herbivores); 2) C-2, representing the secondary consumer level and 3) C-3, representing the tertiary consumer level (frogs). The area external to the first consumer level box (P) represents those aspects of the primary production level used by the helminths. The diagram depicting the life cycle strategies of helminths utilizing frogs as intermediate hosts (Fig. 5) includes an additional trophic level box (C-4) which represents those consumers which ingest frogs and serve as definitive hosts for frog-borne helminths. Placement of hosts used by the helminths into their respective trophic positions is represented by secondary boxes which are labeled with the category of the host (genus or general group designation) and the helminth life cycle stage established in the host category. Abbreviated designations used for helminth stages are defined in the figure legends. Secondary boxes representing host categories which occupy more than one trophic level are placed overlapping those trophic level boxes in which the particular host category participates. Interactions of helminth life cycles within the different trophic levels of these aquatic ecosystems are displayed as coded lines with directional arrow points which illustrate the pathways used by helminths to move from one host to the next in the pond ecosystems. Coded lines are defined at the top of each figure. A directional arrow point by itself without an adjoining coded line represents helminth egg hatching. Species of helminths utilizing these different pathways are identified by arabic numbers which are defined at the bottom of figures.

RESULTS AND DISCUSSION

Platyhelminths (Figs. 1 through 5) and nematodes (Figs. 4 and 5) were the only helminth groups which utilized these two species of frogs as definitive hosts (Table 1) or intermediate hosts (Table 2). Representative literature citations for known life cycles of helminths encountered in this study are given in Table 1.

Adult R. catesbeiana were infected with a total of 31 species of helminths (12 species represented by adult helminths, 19 species represented by larval helminths), while R. utricularia were infected with 28 species (9 species represented by adult helminths, 19 species represented by larval helminths). Eight species represented by adult helminths (4 flukes, 1 cestode, 3 nematodes) and all 19 species represented by larval helminths (15 flukes, 4 nematodes) found in R. utricularia were shared with adult bullfrogs. Each species of frog was infected by a different species of Haematoloechus, while adult Gorgodera sp., Spinitectus sp. and Camallanus sp. were not found in R. utricularia. Of the 12 species represented by adults found in mature bullfrogs; six were flukes and five were nematodes. Five species of flukes and three species of nematodes represented by adults were found in R. utricularia. Ophiotaenia gracilis (mature cestode) was occasionally present in adults of both species of frogs. Prevalences and intensities are given in Table 1. There were no detectable differences in prevalences or intensities between male and female frogs.

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

[FIGURE 3 OMITTED]

Tadpoles had 14 species of helminths represented by larvae which were shared with adult frogs but larvae of Glypthelmins sp., Clinostomum sp., Contracaecum sp., Eustrongylides sp. and two species of Spiroxys were not found in tadpoles. Two species of Ophiotaenia (one maturing in turtles, one in water snakes) and the metacercaria of Cephalogonimus vesicaudus (maturing in turtles) were found in tadpoles but not in adult frogs. Gyrinicola batrachiensis (nematode) was the only adult helminth in tadpoles and was not found in either species of adult frogs. Of the 19 larval helminths found in adult frogs; two mature in fish, two in amphibians, 10 in reptiles (6 in turtles, 4 in snakes), 4 in piscivorous birds and one in both reptiles (turtles) and amphibians (frogs) (Table 2).

Life Cycle Strategies

Platyhelminths, primarily represented by Digenea (flukes), were the most prevalent helminths found. The neascus encountered was Posthodiplostomum sp. Molluscan first intermediate hosts for flukes became infected either by ingestion of eggs from bottom debris, as in Cephalogonimus sp., Glypthelmins sp., Haematoloechus spp., Halipegus sp., macroderoidids, ochetosomatids and telorchids; or by direct penetration of free-swimming miracidia hatched from eggs deposited in the bottom debris, as in Allassostomoides sp., Clinostomum sp., Gorgodera sp., Megalodiscus sp. and Neascus sp. (Posthodiplostomum sp.). In species of flukes where ingestion of eggs was required, eggs hatched in the intestines of molluscan hosts and the released miracidia penetrated the intestinal epithelium. In either method of snail infection, miracidia became the first germinal masses which initiated polyembryony in this host category. The end product of this reproductive process in molluscan hosts was free-swimming larvae, the cercariae, which left snail hosts to infect the next hosts in their respective life cycles, or to encyst upon appropriate substrates. Life cycle strategies of flukes using these two species of frogs as definitive hosts (Figs. 1 through 3) or intermediate hosts (Fig. 5) can be divided into three general types: 1) cercariae formed metacercariae on a substrate external to a host (Fig. 1; Allassostomoides sp., Megalodiscus sp.); 2) cercariae penetrated into a second intermediate host forming metacercariae (Figs. 2 and 5; Cephalogonimus sp., Clinostomum sp., Glypthelmins sp., Haematoloechus spp., macroderoidids, ochetosomatids, Posthodiplostomum sp., telorchids) and 3) cercariae were directly ingested by a second intermediate host, forming metacercariae or mesocercariae (unencysted metacercariae) within the host (Fig. 3; Gorgodera sp., Halipegus sp.) In the first strategy, definitive hosts became infected by ingesting the substrate on which metacercariae had become established (vegetation, exoskeletons of invertebrates, skin of vertebrates, etc.). In the latter two strategies, definitive hosts were generally infected by eating infected second intermediate hosts, but some infections occurred by autoinfection (digestion of their own infected skin), as seen in Glypthelmins sp.

[FIGURE 4 OMITTED]

[FIGURE 5 OMITTED]

Proteocephalid tapeworms generally used two intermediate host levels (Figs. 4 and 5): 1) copepods were infected by ingestion of eggs deposited in the bottom debris producing procercoid larvae (first larval stage) in the hemocoel of these hosts and 2) tadpoles ingested these infected copepods and plerocercoid larvae (second larval stage) developed in the body cavity and associated tissues of these hosts. Definitive hosts became infected by eating infected second intermediate hosts (tadpoles).

Nematodes were the second most prevalent group of helminths (Figs. 4 and 5), being represented by three basic life cycle strategies: 1) the definitive hosts were directly infected by ingestion of eggs or infective larvae, as in Rhabdias sp. and Gyrinicola sp. (Fig. 4); 2) a first intermediate host only was utilized, as in Spinitectus sp., Camallanus sp. and Cosmocercoides sp. (Figs. 4 and 5) and 3) eggs or larvae were ingested by first intermediate hosts and these hosts were in turn ingested by second intermediate hosts, as in Contracaecum sp., Spiroxys spp. and Eustrongylides sp. (Fig. 5). In the first strategy parasites were able to bypass intermediate trophic levels and adults developed directly in the definitive host without passing through intermediate hosts, while in the latter two strategies the ingestion of intermediate hosts was required.

Trophic Diagrams

The diagrammatic representations (Figs. 1 through 5) show how the life cycle stages of the helminths of leopard frogs, R. utricularia, and bullfrogs, R. catesbeiana, utilize the trophic structures of small pond ecosystems. Generally, the youngest larval stages in these life cycles use the lower trophic level represented by the largest of the concentric boxes (C-1), while the more advanced larval stages are found in the intermediate trophic levels (C-2, C-3), ultimately becoming adults in the highest trophic levels (C-3, C-4). Advancement from lower trophic levels to higher trophic levels is generally achieved through using the food chains of the trophic structure. To insure success in these hazardous transfers, helminths typically display a high reproductive potential to offset a low infection efficiency at each stage of their life cycles. Dronen (1978) provided estimates of the efficiencies of Haematoloechus coloradensis (one of the species encountered in this study) over a two year period and found low efficiencies at all levels of the life cycle: eggs producing miracidia which successfully infected snails (0.02%); cercariae realized from total eggs produced (3.9%); metacercariae actually produced from available cercariae (0.09%) and immature flukes realized from metacercariae available (0.5%). Relatively little is known concerning the amount of energy required to support the high reproductive potential of helminths. With the current resurgence of interest in food chain analyses (Yodzis, 1989), such studies should consider both the amount of energy consumed by parasites and the rates of parasite transmission through food chains.
TABLE 1. Infection levels of adult helminths from Rana catesbeiana and
Rana utricularia in south-central Texas and representative literature
citations for the life cycles previously reported for helminths
encountered.

 Rana catesbeiana Rana utricularia
Helminths Prevalence Intensity Prevalence

Trematodes:
 Allassostomoides 9% 2.8 (1-5) 4%
 chelydrae
 Glypthelmins quieta 33% 6.1 (1-32) 53%
 Gorgodera amplicava 23% 10.2 (1-17) 0
 Haematoloechus 29% 5.8 (1-25) 0
 breviplexus
 Haematoleochus 0 0 32%
 coloradensis
 Halipegus occidualis 8% 2.3 (1-7) 1%
 Megalodiscus 42% 4.7 (1-18) 51%
 intermedius

 6 species 5 species

Nematodes
 Camallanus pipientis 2% 3.0 (1-11) 0
 Cosmocercoides dukae 39% 76.8 (10-211) 21%
 Gyrinicola 55% 9.5 (4-26) 70%
 batrachiensis (1)
 Rhabdias ranae 8% 6.3 (1-21) 9%
 Spinitectus carolini 2% 2.7 (1-5)

 6 species 5 species

Cestodes:
 Ophiotaenia gracilis 3% 1.6 (1-4) 4%

 1 species 1 species

 Rana utricularia
Helminths Intensity Citations

Trematodes:
 Allassostomoides 3.0 (1-5) Beaver, 1929; Byrd & Reiber,
 chelydrae 1940; Krull, 1933a
 Glypthelmins quieta 5.7 (1-25) Leigh, 1946; Rankin, 1944
 Gorgodera amplicava 0 Goodchild, 1945, 1948; Krull,
 1935a
 Haematoloechus 0 Schell, 1965; Smith, 1959
 breviplexus
 Haematoleochus 8.4 (1-45) Dronen, 1975; Underwood &
 coloradensis Dronen, 1977
 Halipegus occidualis 3.0 (1-4) Krull, 1933b, 1935b; Macy &
 Demott, 1957; Macy, Cook, &
 Demott, 1960; Thomas &
 Johnson, 1934
 Megalodiscus 4.0 (1-11) Cary, 1909; Herber, 1938, 1939
 intermedius
 Krull & Price, 1932; Smith,
 1959, 1967

 5 species

Nematodes
 Camallanus pipientis 0 Crites, 1976; Moorthy, 1938;
 Stromberg & Crites, 1974
 Cosmocercoides dukae 15.9 (1-59) Anderson, 1960; Baker, 1978
 Gyrinicola 11.0 (1-30) Adamson, 1981
 batrachiensis (1)
 Rhabdias ranae 8.0 (2-21) Baker, 1979a, 1979b
 Spinitectus carolini 0 Gustafson, 1939; Jilek &
 Crites, 1982a, 1982b

 5 species

Cestodes:
 Ophiotaenia gracilis 2.0 (1-3) Herde, 1938; Magath, 1928;
 Thomas, 1934, 1941

 1 species

(1) Found only in tadpoles.

TABLE 2. Prevalence of larval helminths from adults and tadpoles of Rana
catesbeiana and Rana utricularia, including a list of their definitive
hosts in south-central Texas.

 Rana catesbeiana Rana utricularia
Helminths Adult Tadpole Adult Tadpole

Trematode metacercariae:
Cephalogonimidae
 Cephalogonimus vesicaudus 16% 66% 22% 72%
Clinostomatidae
 Clinostomum sp. 14% 0% 21% 0%
Diplostomatidae
 Neascus sp. 2% 1% 1% 5%
Macroderoididae
 Glypthelmins quieta 0% 0% 26% 0%
 Macroderoides typicus 37% 40% 12% 62%
 Paramaroderoides echinus 23% 47% 13% 36%
Ochetosomatidae 18% 37% 9% 72%
 Dasymetra conferta
 Ochetosoma aniarum
 Ochetosoma ellipticum
 Pneumatophilus variabilis
Paramphistomatidae 8% 3% 5% 2%
 Allassostomoides chelydrae
 Megalodiscus intermedius
Telorchidae 15% 8% 10% 80%
 Auridistomum chelydrae
 Protenes angustus
 Telorchis clavi
 Telorchis corti
Nematode Larvae:
Dioctophymidae
 Eustrongylides sp. 24% 0% 11% 0%
Hetrocheilidae
 Contracaecum sp. 5% 0% 2% 0%
Spiruridae 12% 0% 29% 0%
 Spiroxys contortus
 Spiroxys amydae
Cestode Pleroceroids:
Proteocephalidae 0% 27% 0% 7%
 Ophiotaenia perspicua
 Ophiotaenia testudo

Helminths Definitive Hosts

Trematode metacercariae:
Cephalogonimidae
 Cephalogonimus vesicaudus Trionyx spiniferus
Clinostomatidae
 Clinostomum sp. Bulbulcus ibis, Casmerodius albus
 (probably other piscivorous birds)
Diplostomatidae
 Neascus sp. Piscivorous birds (species not known)
Macroderoididae
 Glypthelmins quieta Rana catesbeiana, Rana utricularia
 Macroderoides typicus Lepisosteus oculatus
 Paramaroderoides echinus Lepisosteus oculatus
Ochetosomatidae
 Dasymetra conferta Nerodia erythrogaster, Nerodia fasciata,
 Nerodia rhombifera
 Ochetosoma aniarum Heterodon platyrhinos, Lampropeltis
 getula, Nerodia erythrogaster, Nerodia
 fasciata, Nerodia rhombifera
 Ochetosoma ellipticum Agkistrodon contortrix, Agkistrodon
 piscivorous, Heterodon platyrhinos,
 Masticophis flagellum
 Pneumatophilus variabilis Nerodia erythrogaster, Nerodia fasciata,
 Nerodia rhombifera
Paramphistomatidae
 Allassostomoides chelydrae Rana catesbeiana, Rana utricularia,
 Chelydra serpentina, Trachemys scripta
 Megalodiscus intermedius Rana catesbeiana, Rana utricularia
Telorchidae
 Auridistomum chelydrae Chelydra serpentina
 Protenes angustus Trachemys scripta
 Telorchis clavi Chelydra serpentina
 Telorchis corti Pseudemys concinna, Sternotherus odoratus
Nematode Larvae:
Dioctophymidae
 Eustrongylides sp. Piscivorous birds (species not known)
Hetrocheilidae
 Contracaecum sp. Piscivorous birds (species not known)
Spiruridae
 Spiroxys contortus Trachemys scripta, Pseudemys concinna
 Spiroxys amydae Trionyx spiniferus
Cestode Pleroceroids:
Proteocephalidae
 Ophiotaenia perspicua Nerodia erythrogaster, Nerodia fasciata,
 Nerodia rhombifera
 Ophiotaenia testudo Trionyx spiniferus


ACKNOWLEDGMENTS

I thank the Texas Parks and Wildlife Department without whose cooperation this study could not have been possible. I am also indebted to B. Lang, Eastern Washington State University, for getting me interested in the role of helminths in the trophic dynamics of ecosystems, M. Sweet, Texas A & M University, for suggestions in the preparation of this manuscript, and K. Vaughan, Texas A & M University, for help in identifying amphibians.

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_____. 1979b. Seasonal population changes in Rhabdias ranae Walton, 1929 (Nematoda:Rhabdiasidae) in Rana sylvatica of Ontario. Can. J. Zool., 57:179-183.

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NORMAN O. DRONEN

Laboratory of Parasitology, Department of Wildlife and Fisheries Sciences, College of Agriculture and Life Sciences, College Station, Texas 77843-2258
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Author:Dronen, Norman O.
Publication:The Texas Journal of Science
Geographic Code:1U7TX
Date:May 1, 1994
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