Parasites of amphibians and reptiles from Michigan

33 Pages·2005·0.31 MB·English

by  Muzzall, P. M.

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Number 2077 January 2005
Parasites of Amphibians
and Reptiles from Michigan:
A Review of the Literature 1916–2003
Patrick M. Muzzall
FISHERIES DIVISION
www.michigan.gov/dnr/
RESEARCH REPORT
MICHIGAN DEPARTMENT OF NATURAL RESOURCES
FISHERIES DIVISION
Fisheries Research Report 2077
January 2005
Parasites of Amphibians and Reptiles from Michigan:
A Review of the Literature 1916–2003
Patrick M. Muzzall
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Suggested Citation Format
Muzzall, P. M. 2005. Parasites of amphibians and reptiles from Michigan: A review of the literature
1916–2003. Michigan Department of Natural Resources, Fisheries Research Report 2077, Ann
Arbor.
Michigan Department of Natural Resources
Fisheries Research Report 2077

Parasites of Amphibians and Reptiles from Michigan:
A Review of the Literature 1916–2003

Patrick M. Muzzall

Michigan State University
Department of Zoology
Natural Science Building
East Lansing, Michigan 48824

Abstract.–A summary of the literature on the parasites (protozoans, digenetic trematodes,
monogeneans, cestodes, and nematodes) of amphibians and reptiles (herps) in Michigan is
presented. It is divided into three sections: 1.) a list of the parasite species by taxonomic group
and family followed by their herp hosts and studies, 2.) a list of the herp species in Michigan by
order and family and their parasites, and 3.) a list of body sites occupied by parasites in herps by
order. At least 84 studies (abstracts and articles) have been published on the parasites of herps in
Michigan from 1916 through 2003. These studies include: 49 on frogs, 5 on toads, 19 on
salamanders, 15 on snakes, and 16 on turtles. The more widespread or common herp species have
more parasite species reported from them compared to the less common species. At least 17
protozoan species, 39 adult digenetic trematode species, 12 larval digenetic trematode species, 2
adult monogenean species, 5 adult cestode species, 2 larval cestode species, 15 adult nematode
species, and 3 larval nematode species have been reported from herps in Michigan.
Acanthocephalans have not been reported in Michigan herps. Only two studies have been
published on the parasites of herps in the Upper Peninsula of Michigan. Nineteen (36%) of the 53
herp species in Michigan have not had articles published on their parasites. This study is the first
one to summarize the parasites of herps in a state or province in North America.

The literature on the parasites of herps provided a checklist of helminths in bullfrogs
(defined here as amphibians, snakes, turtles, and Rana catesbeiana in North America. Prudhoe
lizards) in the central United States is extensive, and Bray (1982) discussed the helminth
diverse, and scattered. Historically, studies have parasites of amphibians. Ernst and Ernst (1977)
focused on two major areas, parasite life listed the helminths infecting native turtles of the
histories and taxonomy. Parasite fauna surveys United States. Baker (1987) provided a synopsis
have also received considerable attention. of the nematodes parasitic in herps of the world.
However, many of these surveys are limited in Kuzmin et al. (2003) reviewed and summarized
that only one parasite species or parasite group the literature on the nematode genus Rhabdias
was studied, only one herp species was studied, from herps of the Neartic. Aho (1990) presented
or the number of herps examined was small. and explored mechanisms influencing the
More studies have been performed on the patterns and processes of helminth community
parasites of amphibians than reptiles. Dyer organization in herps.
(1991) listed many of the helminth parasites of Based on discussions with parasitologists
amphibians from Illinois and adjacent and herpetologists as well as reviewing articles
midwestern states. Andrews et al. (1992) on the parasites of herps, it became apparent that
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many investigators were unaware of the synonyms or to review the validity of published
existence of published information on the results. Studies on viruses, bacteria, fungi, and
parasites of Michigan herps. This might be leech parasitism of herps from Michigan were
because titles of some articles do not indicate not included.
that parasites of Michigan herps were studied.
Furthermore, the information in some older
articles is difficult to interpret, often not Results
indicating specifically what species of herps
were examined, where in Michigan the study The parasites found in herps of Michigan, by
was performed, and if the study was actually taxonomic group and family, are listed in Table
done in Michigan. The objective of the present 1. The numbers of parasite species counted,
study was to summarize information on the presented, and reported in the text only involve
parasites of herps in Michigan in an accessible those identified to species, unless only one
form, as the literature on this subject is widely genus or common name was reported in the
scattered in several journals. For investigators original article. A total of 17 protozoan species
interested in these parasites and herp groups, this (1 ameba, 10 flagellates, 2 ciliates, 4
review will provide a basis for a better apicomplexans) in 9 families have been reported
understanding of this subject and for future in herps. Six studies involved some aspect of
study. Cepedietta michiganensis infecting the four-toed
Infectious diseases, such as chytridiomycosis, salamander Hemidactylium scutatum. Only
ranavirus, saprolegniosis, and trematode Entamoeba invadens, Trichomonas sp.,
(Ribeiroia sp.) infection have been discussed as coccidians, and a haemogregarine-like form
causes of mortality leading to amphibian have been reported from snakes. Only one
population declines (Daszak et al. 2003). protozoan Haemoproteus metchinikovi has been
Another objective of this study, therefore, was to reported from a turtle. Flagellates were found in
determine if relationships between helminths ranid frogs and the Eastern American toad Bufo
and amphibian mortalities and malformations a. americanus, based on one study. The rest of
have ever been reported in Michigan. the protozoan species, such as Nyctotherus
Furthermore, it is important to document cordiformis, were reported from ranid frogs,
parasites of herps in Michigan so that changes while the coccidian species Eimeria longaspora
brought about by environmental variation and and Eimeria megaresidua were reported from
the introduction of exotic organisms can be the eastern newt Notophthalmus viridescens.
understood. Thirty-nine species of adult digenetic
trematodes from 13 families have been reported
in Michigan herps (Table 1). A total of 19
Methods digenetic trematode species have been found in
amphibians (18 in frogs, 2 in toads, 5 in
Ten species of salamanders, 13 species of salamanders), 8 species in snakes, 15 species in
frogs and toads, 18 species of snakes, 10 species turtles, and 1 species has been found in both a
of turtles, and 2 species of lizards occur in frog and a turtle. Regarding trematode families,
Michigan (Harding and Holman 1990; Harding members of the Brachycoelidae and
and Holman 1992; Holman et al. 1989; Harding Cephalogonimidae infect amphibians;
1997). Information on the parasites of herps in Gorgoderidae, Haematoloechidae, Hemiuridae,
Michigan was obtained from studies published and Lecithodendriidae primarily infect ranid
since 1916, when the first study was published. frogs; Macroderoididae and Paramphistomidae
Some studies report experimental infections of (except for Allassostomoides parvum) primarily
herps with parasites. Several studies occurred in infect hylid and ranid frogs; Plagiorchiidae
the Douglas Lake and Ann Arbor areas, and infect snakes and turtles; Pronocephalidae infect
have been designated to occur in Cheboygan turtles and a frog; Heronimidae and
County and Washtenaw County, respectively. Spirorchiidae infect turtles; and Telorchiidae
In most situations, no attempt has been made to primarily infect turtles. The families
demonstrate the past complexities of parasite Haematoloechidae and Plagiorchiidae are
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represented by six and seven species, Eight studies have been performed on the
respectively, and the Spirorchiidae and parasites of Notophthalmus viridescens from
Telorchiidae each have five species. Michigan. Five of the 11 species infecting
At least 12 different species of larval newts are digenetic trematodes. Only one study
digenetic trematodes representing 7 families was done on the parasites of the red-backed
have been reported from herps in Michigan salamander Plethodon cinereus. Seven studies
(Table 1). Most species infect amphibians (11 in have been performed on the protozoan species
frogs, 1 in toads, 4 species in salamanders). Cepedietta michiganensis infecting the four-toed
Only larval Alaria intermedia, Alaria salamander Hemidactylium scutatum.
marcianae, and mesocercaria (=Alaria) have Five studies have been performed on the
been reported from snakes. Only one larval parasites of toads with most studies involving
trematode (Cercaria welleri) has been reported Bufo a. americanus. Six parasite species (four
from turtles. protozoans, two digeneans) have been reported
Adult cestodes in three families have been from this toad species. The digenetic trematode
reported from amphibians in Michigan with Cephalogonimus americanus is the only species
Bothriocephalus rarus infecting Notophthalmus reported from the Fowler’s toad Bufo fowleri in
viridescens, Cylindrotaenia americana and one study.
Cylindrotaenia quadrijugosa infecting the Twelve parasite species from eight studies
northern leopard frog Rana pipiens, and have been reported from four hylid frog species.
Proteocephalus saphena infecting green frogs Ten species of parasites have been reported from
Rana clamitans melanota (Table 1). The one the northern spring peeper Pseudacris c. crucifer
report of Proteocephalus sp. infecting the tiger and four species from the striped chorus frog
salamander Ambystoma t. tigrinum and ranid Pseudacris triseriata. Only one parasite species
frogs involves non-gravid worms. Only one has been reported from Blanchard’s cricket frog
cestode species (Proteocephalus perspicua) has Acris crepitans blanchardi and one from the
been reported from snakes. Larvae of two eastern gray treefrog Hyla versicolor.
genera of cestodes (Mesocestoides and Eighteen species of parasites from nine
Proteocephalus) infect ranid frogs. Cestodes studies have been reported from Rana
have not been reported from turtles. catesbeiana. Twenty-eight studies have been
Adults of at least 15 nematode species in 10 performed on green frog parasites with 43
families have been reported from herps in parasite species listed. Twenty-three species are
Michigan (Table 1). Eleven species infect digenetic trematodes with 15 of these being
amphibians with most of them in ranid frogs and adults and 8 species are larvae. Three cestode
three species occur in salamanders. Thelandros species and 10 nematode species are reported
magnavulvaris only infects salamanders. Adult from green frogs. Thirty studies have been
Camallanus microcephalus, Spiroxys amydae, performed on the parasites of the northern
and Spiroxys contortus have been reported from leopard frog Rana pipiens with at least 31
turtles. Dracunculus ophidensis, Rhabdias parasite species listed. At least nine of these
fuscovenosa, unidentified adults, and species are represented as larval trematodes and
microfilariae (larvae) have been found in snakes. six species are adult trematodes.
Encysted larval Spiroxys sp. are common Only one study has been published on the
nematodes of amphibians. parasites of each of the pickerel frog Rana
The parasites found in amphibians and palustris and of the mink frog Rana
reptiles in Michigan by herp order are listed in septentrionalis, and this last one only involved
Table 2. Six species of salamanders in three the blood. Eight studies listing 14 parasite
families have parasites reported from them. species have been done on wood frogs; 7 of
Seven parasite species from three studies have these species are digenetic trematodes.
been reported from the blue-spotted salamander Tadpoles of the following anuran species
Ambystoma laterale. The spotted salamander have been found infected with parasites (in
Ambystoma maculatum and eastern tiger parentheses): Bufo a. americanus
salamander Ambystoma t. tigrinum each have (Cephalogonimus americanus), Bufo fowleri
only had one study on their parasites. (C. americanus), Bufo sp. (C. americanus),
3
Rana catesbeiana (Halipegus eccentricus), Rana trematodes) reported from it involving 14
c. melanota (Alaria marcianae, Alaria mustelae, studies. Three studies on the parasites of the
Caudorchis eurinus, C. americanus, eastern spiny softshell turtle Apalone s. spinifera
Diplostomum micradenum, Echinoparyphium reported five parasite species. Digenetic
flexum, H. eccentricus, Lechriorchis primus, trematodes have been found in four turtle
Megalodiscus temperatus, trematode cysts, species. Of the turtle species, the painted turtle
Proteocephalus perspicua, Proteocephalus is the only one infected with a larval trematode.
saphena, Spiroxys contortus, Spiroxys sp.); Rana Of all the herp species examined from Michigan,
pipiens (A. marcianae, Alaria intermedia, the painted turtle is the only one infected with
A. mustelae, Apharyngostrigea pipientis, monogeneans.
C. eurinus, D. micradenum, E. flexum, The sites occupied by parasites in Michigan
H. eccentricus, L. primus, gorgoderids); Rana amphibians and reptiles by host order are in
sylvatica (E. flexum); Pseudacris c. crucifer Table 3. At least 11 species of parasites occur in
(E. flexum); Pseudacris triseriata (E. flexum); the digestive tract of salamanders from
Hyla versicolor (A. pipientis); species not given Michigan with 8 of these species reported from
(Ribeiroa ondatrae, D. micradenum, Cercorchis the intestine. The gall bladder, lung, blood, and
medius, Telorchis medius). Parasites found in lens of the eye each harbored one parasite
the following larval caudates are: species. Five species of larval parasites
Notophthalmus viridescens (Bothriocephalus occurred elsewhere in the body.
rarus); Ambystoma maculatum (C. americanus); At least 23 species of parasites have been
Ambystoma t. tigrinum (Telorchis corti, reported from the digestive tract of anurans in
Diplostomum sp., Proteocephalus sp.). All these Michigan. Eight species infect the lungs and at
helminth species occurring in tadpoles and larval least four species have been found in the urinary
caudates were larval or immature stages except bladder and kidneys. Six Trypanosoma spp.
for T. corti that was represented by some gravid have been found in the blood. Larval and
stages. immature parasites of all the parasite groups
Eight species of snakes in one family from except the monogeneans occur unencysted or
Michigan have parasites reported from them. At encysted in the body cavity, extra intestinal
least 10 parasite species occur in the northern visceral organs, and muscles.
water snake Nerodia s. sipedon based on 8 Most parasites reported from Michigan
studies. The northern ribbon snake Thamnophis snakes are from the digestive tract and lungs.
sauritus septentrionalis and the common garter Five parasite species are reported from the blood
snake Thamnophis sirtalis have five and eight of turtles, four species from the digestive tract,
species reported from them, respectively. The and one species from the lungs. The sites of
other snake species (brown snake Storeria several species infecting turtles were not given
dekayi, northern red-bellied snake Storeria o. in the original articles.
occipitomaculata, northern ring-necked snake Published studies on the parasites of herps
Diadophis punctatus edwardsi, eastern milk have been performed in 13 counties of
snake Lampropeltis t. triangulum, eastern Michigan. At least 45 studies occurred in
smooth green snake Opheodrys vernalis) had Cheboygan County from 1916 through 1968,
one to three species reported from them due to the investigations of parasitologists at the
involving three studies or less. All snake species University of Michigan Biological Station at
infected with Entamoeba invadens involved Douglas Lake. Washtenaw County has had at
experimental infections in the laboratory. These least 17 studies. Specific locations of six studies
snakes were caught in the Douglas Lake area of in Michigan were not reported. Only two
Michigan. Wild snakes in Michigan have not articles have been published on the parasites of
been found infected with E. invadens. herps in the Upper Peninsula. One of these
Eight species of turtles in four families have involved the occurrence of Cephalogonimus
parasites reported from them in Michigan. americanus in Rana c. melanota and the other
Spiroxys contortus infected all these species. listed blood flagellates found in six species of
The painted turtle Chrysemys picta had 18 anurans. The number of studies (in parentheses)
parasite species (13 of which are digenetic published on the parasites of herps in Michigan
4
in 20-year intervals were: 1910–1929 (11), 1930– The total numbers of parasite species found
1949 (43), 1950–1969 (19), 1970–1989 (2), and in each herp group in parentheses are:
after 1990 (9). Most studies (35) were published salamanders (19), toads (7), hylid frogs (12),
from 1930 through 1939. ranid frogs (at least 50), snakes (15), and turtles
(22). Overall, both toads and hylid frogs were
infected with two parasite groups: toads
Discussion (protozoans 57%; trematodes, 43%) and hylid
frogs (trematodes 67%; nematodes, 33%). The
A survey of the literature on the parasites of percentages (in parentheses) of each parasite
herps in Michigan reveals that most articles deal group (protozoans, trematodes, monogeneans,
with parasite life histories and taxonomy, and cestodes, and nematodes, respectively) for the
parasite surveys of one or more herp species. remaining herp groups are: salamanders (21%,
These studies were not warranted by some 47%, 0%, 11%, 21%), ranid frogs (13%, 57%,
pressing or continuous issue involving parasite 0%, 11%, 19%), snakes (27%, 53%, 0%, 7%,
or herp biology or pathology, but represent the 13%), and turtles (5%, 71%, 10%, 0%, 14%).
interests of specific investigators. At least 84 Excluding toads, trematodes are the most
studies have been published on some aspect of common parasites found in the herp groups.
parasites infecting Michigan herps. Of these Monogeneans have only been reported from
studies, 49 involve frogs, 5 involve toads, 19 turtles. Cestodes have not been found in toads,
involve salamanders, 15 involve snakes, and 16 hylid frogs, and turtles. As more studies are
involve turtles. These numbers are inflated performed on herp species (groups) in Michigan,
because some abstracts and articles by a few more parasite species will be found.
authors involve the same parasites and hosts. Earlier it was mentioned that no attempt was
Many articles present data on the prevalence made to demonstrate the past complexities of
(percentage of a herp species infected with a parasite synonyms. However, it should be
parasite species), mean intensity (mean number pointed out that a few helminth species in some
of parasites per infected herp), and mean families such as Haematoloechidae,
abundance (mean number of parasites per Spirorchiidae, Telorchiidae, and Molineidae
examined herp). A few articles include have undergone name revisions and
information on the diversity of the helminth synonymizations. Therefore, the taxonomic
fauna of a herp species. More parasite species status of some species listed in the tables in this
have been found in amphibians, primarily review article may be uncertain.
anurans, than in reptiles because more studies Several investigators have suggested there is
have examined their parasites, and more a positive correlation between type of habitat
amphibian species and greater numbers of them occupied by the herp species and number of
have been examined. None of the parasites helminth species found, with those species
species reported from Michigan herps are exotic associated with aquatic environments having
species. more parasite species than terrestrial ones. Most
A few species of helminths (e.g., parasite species reported from herps in Michigan
Clinostomum sp., Diplostomum sp., Ribeiroia are digenetic trematodes that utilize molluscs as
ondatrae, Proteocephalus sp., Camallanus sp., intermediate hosts. The presence of more
Spinitectus gracilis, and Spiroxys sp.) found in parasite species in frogs compared to other herp
Michigan amphibians also infect fish. Gravid S. groups in Michigan is likely due to their
gracilis have been found in both ranid frogs and association with aquatic habitats. Frogs eat
centrarchid fish. Larval R. ondatrae occur in many aquatic organisms that serve as
both tadpoles and fish. Larval Clinostomum sp., intermediate hosts for digenetic trematodes and
Diplostomum sp., Proteocephalus sp., other parasite groups, and live in the water
Camallanus sp., and Spiroxys sp. infect where larval parasites (primarily trematodes) can
amphibians and fish in Michigan but it is not directly penetrate and infect them. Other
known if infections in these animals involve the explanations may be that snakes and turtles in
same helminth species. Michigan have not been surveyed for their
parasites as commonly as frogs, or parasites may
5
not be that common in Michigan snakes and They reported that heavy infections in the
turtles. tadpoles caused severe symptoms, producing a
Herps may be infected with either the larval condition that they called “bloat disease,” due to
or adult stage of the parasite species and can the characteristic distension of the abdomen.
serve as either the intermediate or definitive host Studies have not been published on the
or both at the same time. In many cases, the parasites of mudpuppies Necturus maculosus
predator-prey relationships of herps help explain maculosus, western lesser sirens Siren
the transmission of the parasites that infect them. intermedia nettingi, marbled salamanders
Frogs are infected with many species of larval Ambystoma opacum, small-mouthed
parasites indicating they serve as intermediate salamanders Ambystoma texanum, Cope’s gray
hosts for several parasites and are eaten by treefrog Hyla chrysoscelis, Kirtland’s snake
several species of predators. Not enough studies Clonophis kirtlandii, northern copper-bellied
in Michigan have been performed on toads, water snake Nerodia erythrogaster neglecta,
salamanders, snakes, and turtles to determine if queen snake Regina septemvittata, Butler’s
they have many larval parasites. Many herp garter snake Thamnophis butleri, eastern
species in Michigan serve as definitive hosts for hognose snake Heterodon platyrhinos, racer
several parasite species that they acquire by Coluber constrictor foxi, black rat snake Elaphe
eating intermediate hosts. obsoleta obsoleta, eastern fox snake Elaphe
Where the parasitological data comparing gloydi, western fox snake Elaphe vulpina,
herp developmental stages are known, more eastern massasauga rattlesnake Sistrurus
parasite species have been found in adult frogs catenatus catenatus, wood turtle Glyptemys
compared to tadpoles or juveniles. An increase insculpta, red-eared slider Trachemys scripta
in the number of parasite species and their elegans, five-lined skink Eumeces fasciatus, and
numbers in adults can be a function of time, with six-lined racerunner Cnemidophorus sexlineatus,
older (larger) individuals having a longer time to in Michigan. Fowler’s toad, Blanchard’s cricket
acquire parasites, or reflect ontogenetic shifts in frog, eastern gray treefrog, pickerel frog, mink
diet, habitat, or behavior. frog, spotted salamander, eastern tiger
Studies on the parasites of herps sometimes salamander, red-backed salamander, brown
offer some interesting insights on how they snake, northern red-bellied snake, northern ring-
affect their hosts. Two examples in Michigan necked snake, common musk turtle, spotted
will suffice. Brackett (1938) reported that turtle, eastern box turtle, and Blanding’s turtle
gravid females of the nematode Dracunculus each have had only one study published on their
ophidensis are found primarily on the dorsal parasites. Furthermore, before the anecdotal
surface of the snake Thamnophis sirtalis, report of Muzzall et al. (2001) of
producing dermal elevations characteristic of Pneumatophilus foliaformis infecting Nerodia s.
infection. Brackett (1938) stated “The remains sipedon, the last publication on the parasites of
of a female worm which has given off its larvae snakes in Michigan was Yongue (1964). Also,
are in some way disposed of by the snake’s the last report of a parasite infecting a turtle in
tissue, for all traces of the infection disappear by Michigan was the brief mention by Esch and
fall or early winter.” In a letter from Bruce Lang Kocan (1966). The lack of parasitological
regarding D. ophidensis infecting T. sirtalis, it studies on these herp species and the
was stated “The snake’s tail is damaged to the infrequency of studies on other species in
point where portions drop off when an infection Michigan are not surprising and are due to
forms in the area around the blister where the several reasons. These include: the distributions
larvae exit the snake.” And furthermore “This of some herp species in Michigan are restricted;
then could explain the high percentage of T. some species occur in low numbers; some
sirtalis with portions of their tail missing” in the species are threatened or endangered; lack of
Cheboygan area of Michigan. Cort and Brackett interest by investigators; and lack of financial
(1938) reported that the unencysted larval support for studies like this.
diplostomula stages of the trematode, Cercaria Parasites can be found in all the organs of a
ranae, occurred in the body cavity and are herp. If only the digestive tract of the herp is
widely distributed in the tissues of tadpoles. examined, some parasite species (and their
6
numbers), as indicated by this review, would be digenetic trematodes in the genera Procyotrema,
missed and not counted. There may be hundreds Pharyngostomoides, and Strigea.
of larval parasites in the herp. Many of the In general, larval cestodes can be recognized
larval digenetic trematodes, cestodes, and by the presence of calcareous corpuscles. Larval
nematodes infecting herps (especially cestodes generally referred to as tetrathyridia
amphibians) in Michigan are difficult to work may be found and are considered to be of the
with because removing larvae from their cysts genus Mesocestoides. These stages have a
may be difficult. If successfully removed, they deeply invaginated and inverted unarmed scolex
should be examined alive to find characteristics, with four suckers. Schmidt (1970) defined a
if developed enough, that will be useful for tetrathyridium as the cysticercoid of
identification. Larval parasites may also be Mesocestoides that has a solid body and a scolex
identified to species if feeding experiments of not surrounded by special membranes. A
the larvae are performed and adult worms are juvenile cestode in its host can also be called a
found in the animals that were fed the larvae. metacestode.
There are a few terms that describe various Johnson et al. (2002) reviewed information
larval stages of trematodes and cestodes that on larval trematodes producing deformities in
occur in herps, primarily amphibians, that amphibians in North America. They reported
deserve mention for clarification purposes. that the larval trematode Ribeiroia ondatrae was
Several species of cercariae have been described associated with, and functionally related to,
and illustrated in the older literature, being given higher frequencies of amphibian limb
the generic name Cercaria for these species. malformations than found in uninfected
Therefore, the scientific name of these digenetic populations. Gillilland and Muzzall (2002)
trematodes may not be known. Thus, the term reported on the larval helminth parasites
cercaria has been used as a generic name, and infecting amphibians from southern Michigan
more appropriately as a common name for and discussed the lack of deformities in them
certain larval stages of digenetic trematodes. from this area. The earliest article on the larval
Bosma (1934) used the terms, immature trematodes of amphibians in Michigan was Cort
metacercaria and agamodistomum to define the (1918). Although all the animal species (snails,
larval trematode stage that forms from the amphibians and fish, herons, and hawks)
cercaria that penetrates into and occurs in necessary for the completion of the life cycle of
tadpoles and frogs of the trematode genus R. ondatrae occur in Michigan, limb
Alaria. She demonstrated by experiments that malformations of amphibians and the
the so-called agamodistomum of Alaria relationship between larval trematodes and
mustelae is an essential step in the development amphibian malformations were never mentioned
of the next larval stage called the metacercaria. in articles on the larval trematodes of Michigan
She suggested that the name mesocercaria amphibians. If R. ondatrae can produce limb
should be used instead of immature metacercaria malformations in amphibians, might it also be
or agamodistomum. In support of this, Olivier possible that larval cestodes and nematodes can
and Odlaug (1938) employed mesocercaria cause deformities. In Michigan and elsewhere,
(sometimes referred to as the genus unencysted and encysted larval cestodes and
Mesocercaria (=Agamodistomum) in the earlier nematodes are common parasites of amphibians
literature) as the name for these stages of but so far, a relationship between these larval
trematodes with four-host life cycles. The latter helminths and deformities has not been reported.
authors found mesocercaria of Alaria intermedia Beaver (1939) reported on the occurrence of
(=Mesocercaria intermedia) in the muscles and metacercariae of Ribeiroia ( = Psilostomum)
pericardial region of tadpoles and adult Rana ondatrae in the lateral line canal and under the
pipiens and in the fatty tissue of the tail of scales of freshwater fish (experimental and field
Thamnophis sirtalis. Therefore, unencysted infections) from Douglas Lake, Michigan and
mesocercaria can be found in both amphibians the surrounding region. He stated that
and reptiles. Schell (1985) reported that the metacercariae “also develop in the nostrils of
mesocercaria stage can also be produced by tadpoles and fish, and occasionally may be
found in the cloaca and associated ducts after
7