Ecology and Phylogeny of Amphibian Coccidia: A Review

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Ecology and Phylogeny of Amphibian Coccidia A
Review

• Matthew G. Bolek, and Chris Whipps
• Department of Zoology, Oklahoma State University,
• and Environmental and Forest BiologySUNY College
  of Environmental Science Forestry

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6,433 Extent Species of Amphibia (Frost, 2009)
Anura Caudata
Gymnophiona
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Amphibian Coccidia

• Coccidia of frogs and toads, salamanders and
  newts, and caecilians are the least known of all
  the tetrapod vertebrate classes.

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Generalized Life Cycle of a Coccidian
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3
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Generalized Life Cycle of a Coccidian
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Generalized Life Cycle of a Coccidian
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Generalized Life Cycle of a Coccidian
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The Frogs and Toads(Anurans)
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Anurans

• 5,679 extant species of frogs and toads in 395
  genera and 47 families.

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Anurans

• Of the 5,679 anuran species, only 1.2 (67/5,679)
  of species in 7.6 (30/395) of the genera and 30
  (14/47) of the families have ever been examined
  for coccidia.

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Anurans

• 19 species of Eimeria, 3 species of Goussia, 1
  species of Hyaloklossia and 9 species of Isospora
  have been described.

4 X 2 4 X 2
2 X 4 2 X 4
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Anuran Coccidia World Distribution
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7
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Eimeria spp. of Anurans
Ovoidal Irregular
Spherical
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Variation in Oocyst Morphology
Stieda body Oocyst Residium
Micropile Cap Micropile
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Variation in Endogenous Development
Extranuclear Intranuclear
Bolek unpublished Jirku and Modrý 2005
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Variation in Sporulation
Exogenous Endogenous
Bolek unpublished Duszynski et al., 2007
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Caudatans

• 580 extant species of salamanders and newts in 64
  genera and 9 families.

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Caudatans

• Of the 580 caudatan species, only 7.7 (45/580)
  of species in 28 (18/64) of the genera and 67
  (6/9) of the families have ever been examined for
  coccidia.

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Caudatans

• 20 Eimeria and 2 Isospora species have been
  described from the 560 described caudatan
  species.

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Caudatan Coccidia World Distribution
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6
3
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20 Eimeria spp. of Caudata
Elliptical Spherical
Micropile Cap
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Gymnophionans

• 121 extant species of caecilians in 14 genera and
  3 families.

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Gymnophionans

• Only 1 Eimeria species has been described from
  caecilians.

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Eimeria dermophis Asmundsson, Campbell and
Duszynski, 2000
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Ecology of Amphibian Coccidia
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Ecology of Amphibian Coccidia

• Very little work has been done on the ecology of
  amphibian coccidia (Duszynski, Bolek and Upton
  2007).

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Ecology of Amphibian Coccidia

• Very little work has been done on the ecology of
  amphibian coccidia (Duszynski, Bolek and Upton
  2007).
• Upton and McAllister, 1988 Upton et al., 1993,
  suggested that amphibian coccidia are rare, with
  low prevalence and few species of hosts infected.

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Recent Ecology Studies of Amphibian Coccidia

• Bolek, et al., 2003 Jirku et al., 2009a, b on
  Eimeria spp., Isospora spp., and Goussia spp. in
  anurans and caudatans from Europe and North
  America.

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Ecology of Anuran Coccidia
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• How do amphibians become infected with these
  coccidia species?

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• Examination of field collected tadpoles of
  western chorus frogs indicated that they shed
  oocysts of Eimeria streckeri, Isospora cogginsi
  and Isospora delicatus.

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Prevalence of Isospora cogginsi, Eimeria
streckeri and Isospora delicatus in Adults,
Tadpoles, and Metamorphosed Western Chorus Frogs
N 102 N 44 N 47 N
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We collected western chorus frog eggs, brought
them into the laboratory, and reared tadpoles.
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Experimental Infections We exposed these tadpoles
to coccidia oocysts.
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90 (18/20) of experimentally exposed tadpoles of
western chorus frogs shed oocysts of Isospora
delicatus.
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Tadpoles shed oocysts 9-10 days post exposure,
and continued shedding oocysts for 7 days, and
did not retain the infection before
metamorphosis.
Sporulation Exogenous.
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Tadpole and metamorphosed frog digestive system.
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European Eimeria ranae Jirku et al, 2009
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499 Frogs and Toads of 7 Species from 7 locations
in the Czech Republic.
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3,703 Tadpoles of 7 Species from 7 locations in
the Czech Republic.
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Only adults and tadpoles of the Common Frog and
Agile Frog were infected with Eimeria ranae.
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Prevalence of Eimeria ranae in adults and
tadpoles of the Common and Agile Frog from the
Czech Republic
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Exposed 6 species of Frogs and Toads to Eimeria
ranae.
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Only adult and tadpoles of the Common and Agile
Frogs became infected with Eimeria ranae.
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Cross infected adults and tadpoles of the Common
Frog and the Agile Frog with Eimeria ranae.
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Other Anuran Coccidia

• Hyaloklossia liberkuehni infects tadpole and
  metamorphosed anuran kidneys and survives
  metamorphosis (Modrý et al., 2001).

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Other Anuran Coccidia

• Goussia spp. only infect tadpoles and are lost
  during metamorphosis, but sporulated oocysts are
  found in the liver sinuses of metamorphosed
  anurans (Jirku et al, 2009).

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Ecology of Caudatan Coccidia
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Salamander larvae feed on live prey in the open
water column and therefore few should be infected
with coccidia
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N 20 N 19 N 20 N 14
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100 (9/9) of metamorphosed tiger salamanders
shed oocysts of Eimeria ambystomae.
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How Persistent are Amphibian Coccidia Populations
in Anuran and Caudatan Hosts?
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Eimeria fitchi
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Prevalence of Eimeria fitchi in Adult Wood frogs
from Wisconsin
N 15 N 15
N 17
Year
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Prevalence of Eimeria ambystomae, and E. urodela
in larval Tiger Salamanders from Nebraska
N 39 N 25
N 20
Year
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Phylogeny

• What is the relationship of amphibian coccidia to
  coccidians of other animal groups?

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Amphibian Coccidia Phylogeny

• Jirku et al, 2009 recently sequenced the partial
  SSU rDNA of Eimeria ranae, Goussia noelleri,
  Goussia neglecta, and Goussia sp. from European
  tadpoles and frogs.

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Jirku et al, 2009 Bayesian Phylogenetic tree as
inferred from partial SSU rDNA sequences
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North American Anuran Coccidia
Eimeria strecheri Isospora
cogginsi Isospora delicatus
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Sarcocystidae
Eimeridae
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Sarcocystidae
Eimeridae
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Sarcocystidae
Eimeridae
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Conclusion

• Most species of amphibians have not been examined
  for their coccidia species their ecology is
  poorly known.

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Conclusion

• Most species of amphibians have not been examined
  for their coccidia species their ecology is
  poorly known.
• Goussia spp. exhibit stadial host specificity in
  tadpoles, whereas Eimeria, Hyaloklossia and
  Isospora species can infect larval and adult
  amphibians.

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Conclusion

• Most species of amphibians have not been examined
  for their coccidia species their ecology is
  poorly known.
• Goussia spp. exhibit stadial host specificity in
  tadpoles, whereas Eimeria, Hyaloklossia and
  Isospora species can infect larval and adult
  amphibians.
• Amphibian Goussia spp. and Eimeria spp. with a
  stiedia body are basal among the Eimeridae
  whereas amphibian non stiedia body Isospora spp.
  are more closely related to Hyaloklossia, than
  stiedia body Isospora spp.

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Acknowledgments

• R. S. Seville UW
• Miloslav Jirku (University of Vet Pharm Scie,
  Czech Republic)
• Dr. Armando Irizarry-Rovira (Eli Lilly and Co.)
• Cedar Point Biological Station
• UNL, UNK, NIH BRIN, and Department of Zoology OSU

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Questions