PowerPoint Presentationfwf.ag.utk.edu/mgray/wfs493/Lectures/Harris.pdf•light intensity and temperature thermoregulation (Stegen et al. 2004) seasonal shifts Acris crepitans Adult

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Amphibian Predation and Defense

By: Katie Harris

“Each stage of development from egg to adult faces it own particular dangers, and at no time of day or night are frogs and their offspring safe from attack.” –Tyler 1976

“almost anything will eat an amphibian.” – Porter 1972

Why Eat Amphibians?

Amphibian Predators

Evolutionary

Response

Future Directions

Summary

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Why Eat Amphibians?

Amphibian Predators

Evolutionary

Response

Future Directions

Summary

1. Egg

2. Larvae

3. Adult

Why eat an amphibian?

• Small, slow-moving, defenseless?

• High population densities

• Good source of protein

• Lack indigestible material






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Common Predators?

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Common Predators?

• Invertebrates

• eggs and larvae

• temporary ponds

• caddisfly larvae

• parasites

• trophic loop

Lethocerus americanus Pseudacris regilla

Common Predators?

• Invertebrates

• eggs and larvae

• temporary ponds


• parasites

• trophic loop

TrichopteraAmbystoma maculatum

Common Predators?

• Invertebrates

• eggs and larvae

• temporary ponds


• parasites

• trophic loop

MacrobdellaLithobates sylvaticus

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Common Predators?

• Invertebrates

• eggs and larvae

• temporary ponds


• parasites

• trophic loop

Common Predators?

• Invertebrates

• Fish

• Eggs, larvae, adults

Common Predators?

• Invertebrates

• Fish

• Reptiles

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Common Predators?

• Invertebrates

• Fish

• Reptiles

• Birds

Common Predators?

• Invertebrates

• Fish

• Reptiles

• Birds

• Amphibians

Common Predators?

• Invertebrates

• Fish

• Reptiles

• Birds

• Amphibians

• Mammals

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Option 1:

Reduce the

likelihood of being

detected

Option 2:

Reduce the chances

of being consumed

once detected

Behavioral

PhysiologicalMorphological

Chemical

Phenological

Ambystoma maculatum

Option 1:

Reduce the

likelihood of being

detected

Option 2:

Reduce the chances

of being consumed

once detected

Behavioral


Chemical

Phenological

Ambystoma maculatum

Option 1:

Reduce the

likelihood of being

detected

Option 2:

Reduce the chances

of being consumed

once detected

Behavioral


Chemical

Phenological

Ambystoma maculatum

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Option 1:

Reduce the

likelihood of being

detected

Option 2:

Reduce the changes

of being consumed

once detected

Behavioral


Chemical

Phenological

Ambystoma maculatum

Eggs: Mechanical and Chemical

• Egg capsule and jelly

• Toxic and distasteful compounds

• Effectiveness depends on predator

• Eggs of R. calmitans & R. catesbianus

• distasteful to newts and larval ambystomatids (Walters 1975)

• readily consumed by leeches (Howard 1978)

Eggs: Oviposition Site

• Areas without fish

• temporary ponds

• on land

• Areas void of predators

• Anaxyrus americanus avoid oviposition in areas that contained Lithobates sylvaticus eggs (Pentranka et al. 1994)

• L. sylvaticus didn’t lay eggs in ponds with predatory sunfish (Hopey and Petranka 1994)

Lithobates sylvaticus

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Eggs: Oviposition Site

• Areas without fish

• temporary ponds

• on land

• Areas void of predators

• Anaxyrus americanus avoid oviposition in areas that contained Lithobates sylvaticus eggs (Pentranka et al. 1994)

• L. sylvaticus didn’t lay eggs in ponds with predatory sunfish (Hopey and Petranka 1994)


Eggs: Timing of Reproduction

• Early spring

• before predatory species reach peak densities

• Synchronized reproduction

• earlier hatchlings consume eggs deposited later

• swamp predators increasing individual survival


Eggs: Timing of Reproduction

• Early spring

• before predatory species reach peak densities

• Synchronized reproduction

• earlier hatchlings consume eggs deposited later

• swamp predators increasing individual survival


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Eggs: Adaptive Plasticity

• Red-eyed tree frog (Agalychnis callidryas)

• egg mass hatches immediately if clutch is attacked (Warkentin 1995, Warkentin 2000,

Warkentin et al. 2001)

• survive by dropping in water

• trade off! small, not very mobile

• wasp predation – single hatching (Warkentin 2000)

• fungus – eggs closet to fungus hatch first

Agalychinis callidryas








Leptodeira










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• Hatching is delayed in the presence of predators (Sih and

Moore 1993, Moore et al. 1996)

• Allows larvae to hatch at a more advanced stage

Ambystoma opacum

Larval Defense:

Lithobates clamitans

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Larval Defense: Color Patterns

• First line of defense

• Drab colors

• Countershading

• Disruptive coloration

• Reflective or transparent

• Deflection marks

Lithobates clamitans



• Drab colors

• Countershading




Lithobates clamitansStorfer et al. 1999



• Drab colors

• Countershading




Lithobates catesbianus

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• Drab colors

• Countershading







• Drab colors

• Countershading




Xenopus longipes



• Drab colors

• Countershading




Acris sp.

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• Drab colors

• Countershading




Clinotarsus alticola

Larval Defense: Phenotypic Plasticity

• Acris• tail tip coloration (Caldwell 1982)

• Hyla chrysoscelis• dragonfly naiads present

• dark orange, deep tail fins, dark (Van Buskirk & McCollum 1999)

• predators absent• Shallow, unmarked tail fins

(Van Buskirk & McCollum 1999)

• early age exposure = gradual development (LaFiandra

& Babbitt 2004)

• direct contact not necessary

dragonfly naiads present

fish present

Acris sp.








& Babbitt 2004)


Present

Absent

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& Babbitt 2004)


Present

Absent








& Babbitt 2004)


Present

Absent

Larval Defense: Behavioral


• Schooling (Rodel and Linsenmair 1997)

• decreases chance of individual capture

• Time of day

• shift active when predators are not active (Sih et al. 1992)

• Ambystoma barbouri – tend to be nocturnal in presence of fish (Taylor 1983)

• Refuge habitats: less food

• water column – Ambystoma talpoideum (Holomuzki 1986)

• trade-offs vulnerability versus foraging efficiency

• Limit activity (Altwegg 2003)

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• Time of day











• Time of day











• Time of day







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(Strangel and Semlitsch 1987)


Larval Defense: Sensory Cues

• Tactile

• Visual

• Chemical

• discrimination between dangerous and less dangerous genetic response-previous exposure is not required (Lefcourt 1996,1998, Gallie et al. 2001, Mathis et al. 2003)

• discrimination between predators of conspecific larvae (Chivers and Mirza 2001)

• not always present, can develop rapidly (Kiesecker and Blaustein 1997)


(Chivers, Kiesecker, Blaustein 1996)

Predatory

Predatory

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Larval Defense: Sensory Cues


• Tactile

• Visual

• Chemical

• discrimination between dangerous and less dangerous genetic response-previous exposure is not required (Lefcourt 1996,1998, Gallie et al. 2001, Mathis et al. 2003)

• discrimination between predators of conspecific larvae (Chivers and Mirza 2001)

• not always present, can develop rapidly (Kiesecker and Blaustein 1997)

Larval Defense: Alarm Responses

• Cues from injured conspecifics (Hews and Blaustein 1985)

• use these cues to avoid areas where predators are likely (Hews 1988)

• increase activity (different than most)

• beneficial if predator has already been detected (Hews 1998))

Lithobates sphenocephalus

Larval Defense: Growth & Development

• Rapid growth

• Predators have limited prey size

• Sprint speed increases with size (Richards and Bull 1990)

• Higher growth rate= higher survivorships (Travis 1983)

• Growth and predator exposure

• Bufo boreas – increased growth rate (Chivers et al. 1999)

• Ambystoma macrodactylum – decreased growth rate

• foraging decreased (Wildy et al 1999)

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Larval Defense: Growth & Development

• Rapid growth

• Predators have limited prey size

• Sprint speed increases with size (Richards and Bull 1990)

• Higher growth rate= higher survivorships (Travis 1983)

• Growth and predator exposure

• Bufo boreas – increased growth rate (Chivers et al. 1999)

• Ambystoma macrodactylum – decreased growth rate

• foraging decreased (Wildy et al 1999)

Larvae Defense: Chemical Defenses

• Distasteful and toxic; particularly anuran tadpoles

• Bufo- palatability varies among predators

• Why not in all species?

Bufo bufo

Larvae Defense: Chemical Defenses

• Distasteful and toxic; particularly anuran tadpoles

• Bufo- palatability varies among predators

• Why not in all species?

• expensive to produce

• temporary ponds: too costly, rapid growth

• permanent ponds: worth the energy costs, slow growth

Bufo bufo

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Adult Defense: Cryptic Coloration

• Matching dorsal coloration to environment (Edmunds

1974)

• Reflect light in visible and infrared spectrum (Schalm et al. 1977,

Emerson et al. 1990)

• Color change (Iga and

Bagnara 1975)

• Cryptic patterning (Cott 1940)

Hyla chrysoscelis



1974)




Bagnara 1975)


Hyalinobatrachium taylori



1974)




Bagnara 1975)


Hyla cinerea

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Ceratobatrachus guentheri - Soloman Island Frog



1974)




Bagnara 1975)

• Cryptic patterning(Cott 1940)

Adult Defense: Color Polymorphism

• Polymorphism = different forms

• Genetically controlled (Merrell 1965, Fogelman et al. 1980)

• can be environmentally influenced (Travis and Trexler 1984, Harkey and

Semlitch 1988)

• Pacific tree frog (Pseudacris regilla)

• color-changing morph (brown/green) (Wente and Phillips 2003)

• slow not effective to immediate predation

• adaptive

• light intensity and temperature thermoregulation (Stegen et al. 2004)

seasonal shifts

Acris crepitans





Semlitch 1988)




• adaptive


seasonal shifts

Acris crepitans

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Semlitch 1988)




• adaptive


seasonal shifts

Acris crepitans

Adult Defense: Predator Avoidance

• Avoid locations where predators present

• Chemical cues• predators

• injured conspecifics

• Newts (Woody and Mathis 1998)

• did not avoid chemical stimuli from fish (Marvin and Hutchinson 1995,

Woody and Mathis 1997)

• avoided chemical stimuli from fish if associated with injured conspecific (Woody and Mathis 1998)

Plethodon vandykei









Plethodon vandykei

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Plethodon vandykei

Adult Defense: Behavioral

• Jumping – slender bodies (Heinen and Hammond 1997)

• Flipping – Plethodontids (Whiteman and Wissinger 1991, Azizi and Landberg 2000)

• Coiling – Mount Lyell salamander Hydromantes playcephalus (Garcia-

Paris and Deban 1995)

• Death feigning – leaf litter frog Ischnocnema aff. henselii (Vaz-Silva et. al

2004)

• Vocalization (Weber 1978)

• Biting (Taylor and Ludlam 2013)

• Tail display – Plethodontidae, Salamandridae (Wake and Dresner 1967)

• Unken reflex (Kuchta 2005)

Rana so.




• Coiling – Mount Lyell salamander Hydromantes playcephalus (Garcia-

Paris and Deban 1995)

• Death feigning – leaf litter frog Ischnocnema aff. henselii (Vaz-Silva et. al

2004)





Plethodon cinereus

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• Coiling – Mount Lyell salamander Hydromantes

playcephalus (Garcia-Paris and Deban 1995)

• Death feigning – leaf litter frog Ischnocnema aff. henselii (Vaz-

Silva et. al 2004)





Ischnocnema aff. henselii







Silva et. al 2004)





Lithobates catesbianus

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Silva et. al 2004)





Amphiuma tridactylum






• Death feigning – leaf litter frog Ischnocnema aff. henselii(Vaz-Silva et. al 2004)





Batrachoseps relictus


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Silva et. al 2004)





Taricha granulosa

Adult Defense: Chemical

• Granular glands• Found in all amphibians, relatively similar structure

• Distributed throughout the skin or concentrated

• Defensive secretions1. Widespread, naturally occurring compounds.

• Can serve other functions microbes and fungi

• Defensive when secreted in large quantities

2. Evolved for defense toxic

• Origin• Synthesized within the animal (Smith et al. 2002)

• Derived from chemicals of other organisms (Daly et al. 1994)

Anaxyrus sp.










Anaxyrus sp.

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Anaxyrus sp.

Oophaga pumilioHyla chrysoscelis

Adult Defense: Aposematic Coloring

• Coloration to warn or deter predators

• Only beneficial when predator can see colors

• Dendrobatidae• Color brightness

correlates to toxicity (Summers and Clough

2001)

Adult Defense: Mimicry

• Predators learn to avoid the aposematic patterns

• Batesian mimicry: edible species benefit by evolving pseudoaposematic colors

• Pseudotriton ruber & Notophthalmus viridescens

• readily eaten before exposure to red efts (Brodie & Howard 1972)

• less palatable than Desmognathus species (Brandon et al. 1979)

• produce toxins Mullerian

• Mullerian mimicry: toxic species share a common warning coloration

Pseudotriton ruberNotophalmus viridescens

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Future Directions

• Impact on populations• demographic impact of predation

• impact of specific predators

• invasive predators

• Genetics

• Relationships between toxicity and predators

• Caecilians and salamanders


Summary

• Subject to vast array of predators

• Predation is greatest on egg and larval stages

• Most predators are generalists

• Protection against predators is varied

• Predation lessened by:

• reduce the change of detection

• reduce the changes of being consumed once detected

• chemical, phenological, behavioral, physiological, morphological

Ensatina eschscholtzii


• Azizi, E., and T. Landberg. 2002. Effects of metamorphosis on the aquatic escape response of the two-lined salamander (Eurycea bislineata)." Journal of Experimental Biology. 205: 841-849.

• Brandon, Ronald A., George M. Labanick, and James E. Huheey. "Relative palatability, defensive behavior, and mimetic relationships of red salamanders (Pseudotriton ruber), mud salamanders

(Pseudotriton montanus), and red efts (Notophthalmus viridescens). Herpetologica 1979: 289-303.

• Brodie, E. D., and R. R. Howard. Behavioral mimicry in the defensive displays of the Urodele amphibians Nophthalmus viridescens and Pseudotriton ruber. BioScience 22: 666-667.

• Caldwell, J. P. 1982. Disruptive selection: a tail color polymorphism in Acris tadpoles in response to differential predation. Canadian Journal of Zoology, 60, 2818-2827.

• Chivers, D. P. and R. S. Mirza. 2001 Journal of Chemical Ecology. 27, 45-51.

• Chivers. D. P., J. M. Kiesecker, A. Marco, E. L. Wildy and A. R. Blaustein. 1999. Shift in life history as a response to predation in western toads (Bufo boreas). Journal of Chemical Ecology. 25, 2455-2463.

• Daly, J. W., S. L. Secunda, H. M. Garraffo, T. F. Spande, A. Wisnieski, and J. F. Cover. 1994. An uptake system for dietary alkaloids in poison frogs (Dendrobatidae). Toxicon, 32(6), 657-663.

• Heinen, Joel T., and George Hammond. 1997. Antipredator behaviors of newly metamorphosed green frogs (Rana clamitans) and leopard frogs (R. pipiens) in encounters with eastern garter snakes

(Thamnophis s. sirtalis). American Midland Naturalist. 1997: 136-144.

• Hews, D. K. "Alarm response in larval western toads, Bufo boreas: release of larval chemicals by a natural predator and its effect on predator capture efficiency." Animal Behaviour 36:125-133.

• Hews, D. K., and A. R. Blaustein. "An investigation of the alarm response in Bufo boreas and Rana cascadae tadpoles. Behavioral and Neural Biology 43.: 47-57.

• Hopey, M. E., and J. W. Petranka. 1994. Restriction of wood frogs to fish-free habitats: how important is adult choice? Copeia, 1994, 1023-1025.

• Fogleman, J. C., P. S. Corn, and D. A. Pettus. The genetic basis of a dorsal color polymorphism in Rana pipiens. The Journal of heredity 71: 439-440.

• Gallie, J. A., Ronald L. M., and S. A. Wissinger. Experience has no effect on the development of chemosensory recognition of predators by tadpoles of the American toad, Bufo americanus." Herpetologica

2001: 376-383.

• García-París, M., and S. M. Deban. 1995. A novel antipredator mechanism in salamanders: rolling escape in Hydromantes platycephalus. Journal of herpetology 29: 149-151.

• Harkey, G. A., and R. D. Semlitsch. Effects of temperature on growth, development, and color polymorphism in the ornate chorus frog Pseudacris ornata. Copeia, 1988: 1001-1007.

• Howard, R. D. 1978. The influence of male‐defended oviposition sites on early embryo mortality in bullfrogs. Ecology, 59, 789-798.

• Kiesecker, J. M., and A. R. Blaustein. "Population differences in responses of red‐legged frogs (Rana aurora) to introduced bullfrogs." Ecology 78.6: 1752-1760.

• Kuchta, S. R. Experimental support for aposematic coloration in the salamander Ensatina eschscholtzii xanthoptica: implications for mimicry of Pacific newts. Copeia. 2005: 265-271.

• LaFiandra, E. M., and K. J. Babbitt, K.J. Oecologia 2004 138: 350.

• Lefcourt, H., 1996. Adaptive, chemically mediated fright response in tadpoles of the southern leopard frog, Rana utricularia. Copeia 1996:455-59.

• Lefcourt H.,1998. Chemically mediated fright response in southern toad (bufo terrestris) tadpoles. Copeia 1998:445-50.

• Marvin, G. A., and V. H. Hutchison. Avoidance response by adult newts (Cynops pyrrhogaster and Notophthalmus viridescens) to chemical alarm cues. Behaviour 132.1 1995: 95-105.

References

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• Mathis, A. 2003. Use of chemical cues in detection of conspecific predators and prey by newts, Notophthalmus viridescens. Chemoecology, 13, 193-197.

• Petranka, J. W., M. E. Hopey, B. T. Jennings, S. D. Baird, and S. J. Boone. 1994. Breeding habitat segregation of wood frogs and American toads: the rol e of interspecific tadpole predation and adult choice.

Copeia, 691-697.

• Porter, K. R. 1972. Herpetology. Saunders Limited.

• Richards, S. J., and C. M. Bull. Size-limited predation on tadpoles of three Australian frogs. Copeia 1990: 1041-1046.

• Smith, B. P., M. J. Tyler, T, Kaneko, H. M. Garraffo, T. F. Spande, and J. W. Daly. 2002. Evidence for biosynthesis of pseudophrynamine alkaloids by an Australian myobatrachid frog (Pseudophryne) and for

sequestration of dietary pumiliotoxins. Journal of natural products, 65, 439-447.

• Stegen, James C., C. M. Gienger, and Lixing Sun. 2004. The control of color change in the Pacific tree frog, Hyla regilla. Canadian journal of zoology 82: 889-896.

• Storfer, A., J. Cross, V. Rush, and J. Caruso. 1999. Adaptive coloration and gene flow as a constraint to local adaptation in the streamside salamander, Ambystoma barbouri. Evolution, 889-898.

• Summers, K. and M. E. Clough. The evolution of coloration and toxicity in the poison frog family (Dendrobatidae). Proceedings of the National Academy of Sciences 98: 6227-6232.

• Taylor, H., and J. P. Ludlam. 2013. The role of size preference in prey selection of Amphiuma means. Bios. 84: 8-13.

• Travis, J. Variation in growth and survival of Hyla gratiosa larvae in experimental enclosures. Copeia 1983: 232-237.

• Travis, J., and J. C. Trexler. "Investigations on the control of the color polymorphism in Pseudacris ornata." Herpetologica. 1984: 252-257.

• Tyler, M. J. 1976. Frogs. Sydney, Australia: Collins.

• Van Buskirk, J., and S. A. McCollum. 1999. Plasticity and selection explain variation in tadpole phenotype between ponds with different predator composition. Oikos, 31-39.

• Vaz-Silva, W., and J. G. Frota. 2004. Bufo marinus (Marine Toad) defensive behavior. Herpetological Review. 35: 371.

• Wake, D. B., and I. G. Dresner. 1967. Functional morphology and evolution of tail autotomy in salamanders. Journal of Morphology 122: 265-305.

• Walters, B. 1975. Studies of interspecific predation within an amphibian community. Journal of Herpetology, 267-279.

• Warkentin, K. M. Adaptive plasticity in hatching age: a response to predation risk trade-offs. Proceedings of the National Academy of Sciences 92. 8: 3507-3510.

• Warkentin, K. M. Wasp predation and wasp-induced hatching of red-eyed treefrog eggs. Animal Behaviour 60. 4: 503-510.

• Warkentin, K. M., C. R. Currie, and S. A. Rehner. Egg‐killing fungus induces early hatching of red‐eyed treefrog eggs. Ecology 82. 10: 2860-2869.

• Wente, W. H., and J. B. Phillips. 2005 Seasonal color change in a population of pacific treefrogs (Pseudacris regilla). Journal of Herpetology 39: 161-165.

• Whiteman, H. H., and S. A. Wissinger. 1991. Differences in the antipredator behavior of three plethodontid salamanders to snake attack. Journal of herpetology. 25: 352-355.

• Weber, Ernst. Distress calls of Bufo calamita and B. viridis (Amphibia: Anura). Copeia 1978 : 354-356.

• Wildy, E. L., D. P. Chivers, Kiesecker, J. M., and A. R. Blaustein. 1998. Cannibalism enhances growth in larval long-toed salamanders (Ambystoma macrodactylum). Journal of Herpetology 32:286-289.

• Woody, D. R., and A. Mathis. 1998. Acquired recognition of chemical stimuli from an unfamiliar predator: associative learning by adult newts, Notophthalmus viridescens. Copeia 1998: 1027-1031.

References

Photo Credits


• Anna Spyrka

• Amber Hart

• Audobaun Society

• Barbara Magnuson

• Brandon Ballengee

• Brian Gratwicke

• Christina Rollo

• David Huth

• Douglas Mills

• Dwight Kuhn

• Gary Nafis

• Greg Pecold

• Harikrishnan S.

• Jacob Loyacano

• Jason Gibson

• Johnathan Mays

• John Whit

• John White

• Jones Fish Hatcher

• Kristiina Hurme

• Larry Kimball

• Mike Benard

• Montgomery Co. Dept. of Environmental Protection

• Nancy Tray

• Natalle McNear

• Nathan Shepard

• Oliver Kratz

• Peter May

• Ricky Relya

• Robert Clontz Photography

• Rod Williams

• Ryan Photographic

• The Amphibain Foundation

• Warren Photographic

• Werther Pereira Ramalho

Questions?

Katie Harris240 EPS [email protected]

Documents

PowerPoint Presentationfwf.ag.utk.edu/mgray/wfs493/Lectures/Harris.pdf•light intensity and temperature thermoregulation (Stegen et al. 2004) seasonal shifts Acris crepitans Adult