From a Frogs Perspective, is a Dragonfly a Dragonfly? Evolutionary Avenues for and Constraints on the Transmission of Frog Lung Flukes (Haematoloechus

From a Frogs Perspective, is a Dragonfly a Dragonfly? Evolutionary Avenues for and

Constraints on the Transmission of Frog Lung Flukes (Haematoloechus spp.).

From a Frogs Perspective, is a Dragonfly a Dragonfly? Evolutionary Avenues for and

Constraints on the Transmission of Frog Lung Flukes (Haematoloechus spp.).

Matthew G. Bolek*, Scott D. Snyder, and John Janovy Jr.School of Biological Sciences, University of Nebraska-

Lincoln

Matthew G. Bolek*, Scott D. Snyder, and John Janovy Jr.School of Biological Sciences, University of Nebraska-

Lincoln

Archetypical and Paradigmatic Life of a Frog Lung Fluke

Real World Lives of Frog Lung Flukes

6 spp.

21 spp.

511 spp.

12 spp.

The Problem of Parasite Flow Through an Ecosystem Actually Looks Something Like This:

(1) Two species are specialists only infecting dragonflies.

The Situation: 2nd Intermediate Host Specificity


(2) One species is intermediate in its host specificity and can infect dragonflies and damselflies.



(2) One species is intermediate in its host specificity and can infect dragonflies and damselflies.

(3) Two other species are generalists infecting dragonflies, damselflies, and other aquatic arthropods.


N. Leopard Frog P. Leopard Frog Bullfrog

Two Generalists X


Two Generalists

One Specialist


XX

Two Generalists

One Specialist

One Intermediate

One Specialist


XX

Two Generalists

One Specialist

One Intermediate

Ecological Host

Specificity

Ecological Host

Specificity

One Specialist

Ecological Host

Specificity

Ecological Host

Specificity


XX

What is the role of second intermediate dragonfly hosts and their parasite

interactions in the transmission of frog lung flukes?

?

Nickol Pond, Cass Co., NE

Eastern Pondhawk teneral

Eastern Pondhawk post-teneral

Prevalence of Lung Flukes Recovered from 75 Larvae and 74 Tenerals of Eastern Pondhawks

0

5

10

15

20

Larva Teneral

Life Stage

Pre

vale

nce

(%

)

P < 0.05

The Eastern Forktail

Prevalence of Lung Flukes Recovered from Larvae, Tenerals, and Aduts of the Eastern Forktail

0

5

10

15

20

25

30

Larva Teneral Adult

Life Stage

Pre

vale

nce

(%

)

N = 80 N = 28 N = 46

P < 0.05

Eastern Forktail larva

Mean Abundance of Lung Flukes Recovered from the Body Cavity of 25 Larvae and Lab Metamorphosed

Tenerals of the Eastern Forktail

0

0.5

1

1.5

2

2.5

3

Larvae Teneral

Life Stage

Mea

n A

bund

ance

+ 1

SD

P > 0.05

Eastern Pondhawk larva

Eastern Pondhawk castskin

0

0.5

1

1.5

2

2.5

3

Larva Teneral

Life Stage

Mea

n A

bund

ance

+ 1

SD

BranchialBasket

Body Cavity

P < 0.001

P > 0.05

Mean Abundance of Lung Flukes Recovered from the Body Cavity and Branchial Basket of 100 Larvae and

Lab Metamorphosed Tenerals of the Eastern Pondhawk

Experimental Infections

• I experimentally infected dragonflies with parasites from lab reared snails infected with four species of lung fluke and examined these dragonflies for the location and survival of these parasites through metamorphosis.

Table I. Prevalence and location of four lung fluke parasites in experimentally exposed eastern

pondhawk dragonflies

Prevalence Head Thorax Branchial Basket

Generalist 1 10/10 Yes Yes Yes

Generalist 2 6/10 Yes Yes Yes

H. varioplexus 5/9 __ __ Yes

H. longiplexus 6/9 __ __ Yes

0

10

20

30

40

Larva Teneral

Generalist 1 N = 10

Generalist 2 N = 10

Haematoloechusvarioplexus N=6Haematoloechuslongiplexus N=9

Mean Abundance of Four species of Frog Lung Flukes in Experimentally Infected Eastern Pondhawk Larvae and

Tenerals M

ean

Ab

un

dan

ce +

1S

D

Life Stage

P < 0.05

Natural History of Frog Hosts

Aquatic Amphibians

Semi-terrestrial Amphibians

Haematoloechus varioplexus

N = 4 N = 4 N = 3 N = 3

N. Leopard Bullfrog P. Leopard Bullfrog Frog FrogN. Leopard Bullfrog P. Leopard Bullfrog Frog Frog

X

Haematoloechus varioplexus

X N = 4 N = 4 N = 3 N = 3

YesYes

N. Leopard Bullfrog P. Leopard Bullfrog Frog FrogN. Leopard Bullfrog P. Leopard Bullfrog Frog Frog

Morphological Studies of the specialist Haematoloechus varioplexus, or, is it really

H. varioplexus?• Haematoloechus varioplexus, a parasite of northern

leopard, was synonymized with five other species of Haematoloechus including H. parviplexus which infects bullfrogs (Kennedy, 1981).

The question arises as to whether Kennedy was justified, or correct, in making this synonymy.

Molecular Studies

H. complexusWI

H. complexNEAF316155

H. complexusMB9

H. complexus

H. complexusNE

H. coloradensisCPBSNE

H. coloradensisCdrCkNE

H. varioplexusWI

H. varioplexusSD

H. varioplexusND

H.abbreviatusAF316156

H. variegatusAF316158

H. parviplexusNE

H. parviplexusWI

H. parviplexusNEAF316262

H. floedaeAF387796

H. breviplexusTX H12

H. medioplexusAF316161

H. longiplexusNEAF316153

H. longiplexusPAWNE

H. longiplexusNEVNEH. asperAF316165

H. similisUK

P. koreanusAF151946

P. vespertilionisAF151952

P. maculaosusAF316152

88

95

100

100

95

86

99

99

100

60

68100

100

96

100

100

58

12 European and North American Species of Frog Lung Flukes from 23 populations (Complete ITS region of rDNA)

261 PICTL = 672CI = 0.81HI = 0.18 RI = 0.88

OutGroupBolek, Snyder, and Janovy In Prep

Implications

• In terms of transmission, depending on the frog species, its habitat, and the trematode species involved, a dragonfly is not a dragonfly.

H. coloradensis (NA)

H. complexus (NA)

H. varioplexus (NA)

H. abbreviatus (E)

H. variegatus (E)

H. floedae (NA)

H. breviplexus (NA)

H. parviplexus (NA)

H. medioplexus (NA)

H. longiplexus (NA)

H. asper (E)

H. similis (E)

Plagiorchiidae OutGroup

North America

Europe

3

2

1

Bolek, Snyder, and Janovy In Prep

Life cycle unknown


H. complexus (NA)

H. varioplexus (NA)

H. abbreviatus (E)

H. variegatus (E)

H. floedae (NA)

H. breviplexus (NA)

H. parviplexus (NA)

H. medioplexus (NA)

H. longiplexus (NA)

H. asper (E)

H. similis (E)

Plagiorchiidae

Various Arthropods, Gastropods, Amphibians

Damselflies

North America

Europe

OutGroup

Damselflies

Life cycle unknown


H. complexus (NA)

H. varioplexus (NA)

H. abbreviatus (E)

H. variegatus (E)

H. floedae (NA)

H. breviplexus (NA)

H. parviplexus (NA)

H. medioplexus (NA)

H. longiplexus (NA)

H. asper (E)

H. similis (E)

Plagiorchiidae


Damselflies and Dragonflies

North America

Europe

OutGroup

Damselflies

Life cycle unknown


H. complexus (NA)

H. varioplexus (NA)

H. abbreviatus (E)

H. variegatus (E)

H. floedae (NA)

H. breviplexus (NA)

H. parviplexus (NA)

H. medioplexus (NA)

H. longiplexus (NA)

H. asper (E)

H. similis (E)

Plagiorchiidae


Specialist

North America

Europe

OutGroup


Damselflies

Life cycle unknown


H. complexus (NA)

H. varioplexus (NA)

H. abbreviatus (E)

H. variegatus (E)

H. floedae (NA)

H. breviplexus (NA)

H. parviplexus (NA)

H. medioplexus (NA)

H. longiplexus (NA)

H. asper (E)

H. similis (E)

Plagiorchiidae


Specialist

Generalists

North America

Europe

OutGroup


What About the Amphibian Host?

Damselflies

Life cycle unknown


H. complexus (NA)

H. varioplexus (NA)

H. abbreviatus (E)

H. variegatus (E)

H. floedae (NA)

H. breviplexus (NA)

H. parviplexus (NA)

H. medioplexus (NA)

H. longiplexus (NA)

H. asper (E)

H. similis (E)

Plagiorchiidae


Dragonfly

Generalists


Damselflies

Small to Medium Frogs

Life cycle unknown


H. complexus (NA)

H. varioplexus (NA)

H. abbreviatus (E)

H. variegatus (E)

H. floedae (NA)

H. breviplexus (NA)

H. parviplexus (NA)

H. medioplexus (NA)

H. longiplexus (NA)

H. asper (E)

H. similis (E)

Plagiorchiidae


Dragonfly

Generalists



Life cycle unknown


H. complexus (NA)

H. varioplexus (NA)

H. abbreviatus (E)

H. variegatus (E)

H. floedae (NA)

H. breviplexus (NA)

H. parviplexus (NA)

H. medioplexus (NA)

H. longiplexus (NA)

H. asper (E)

H. similis (E)

Plagiorchiidae


Dragonfly

Damselflies

Generalists

Large FrogsDamselflies and Dragonflies

Damselflies


Life cycle unknown


H. complexus (NA)

H. varioplexus (NA)

H. abbreviatus (E)

H. variegatus (E)

H. floedae (NA)

H. breviplexus (NA)

H. parviplexus (NA)

H. medioplexus (NA)

H. longiplexus (NA)

H. asper (E)

H. similis (E)

Plagiorchiidae


Dragonfly

Generalists

Medium Frogs

Large Frogs

Large Frogs


Damselflies


Life cycle unknown


H. complexus (NA)

H. varioplexus (NA)

H. abbreviatus (E)

H. variegatus (E)

H. floedae (NA)

H. breviplexus (NA)

H. parviplexus (NA)

H. medioplexus (NA)

H. longiplexus (NA)

H. asper (E)

H. similis (E)

Plagiorchiidae


Dragonfly

Generalists Small to Medium Frogs

Medium Frogs

Large Frogs

Large Frogs


Adult North American Bullfrog and Northern Leopard Frog

M. Bolek

M. Bolek

Bolek and Janovy 2007

Bolek and Janovy 2007

Mean Prey Size and Gape Size of 5 North American Frog Species

0

5

10

15

20

25

30

35

0 10 20 30 40 50

Mean Head Width (mm)

Mea

n P

rey

Siz

e (m

m)

Bullfrog

Bolek unpublished.

M. Bolek

Diet of Bullfrogs

Amphibians and Reptiles 13.9%

Fish 3.1%

Crustaceans 31.6%

Misc. Inverts. 3.5%

Mammals 15.3%

Other 6.2%

Insects 26.4%

Data from various sources.

Conclusion

• Our data on closely related trematode species clearly suggest that their complex life cycles are dynamic and there are numerous avenues for and constraints on transmission to their definitive hosts.

Acknowledgments• Dr. John Janovy Jr.• Dr. Scott Snyder (UNO)• Randy Peterson• Dr. Brent Nickol• Dr. Virginia Leon, and Rosario Mata (UNAM)• Dr. Agustin Jimenez

• Cedar Point Biological Station• UNL School of Biological Sciences Special Funds, Initiative

for Ecological and Evolutionary Analysis UNL, Center for Great Plains Studies

• Jaclyn Helt, Jill Detwiler, Samana Schwank

Questions?

Documents

From a Frogs Perspective, is a Dragonfly a Dragonfly? Evolutionary Avenues for and Constraints on the Transmission of Frog Lung Flukes (Haematoloechus