Ecotoxicology of Declining Amphibian Populations

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1 Ecotoxicology of Declining Amphibian Populations

2 Some Questions What does the term declining amphibians mean? decrease in number of individuals in an area decrease in number of sites occupied by breeding amphibians How can we tell if there is a decline in amphibian populations? anecdotal reports long term field studies metadata analysis

3 More Questions Where are amphibian populations declining? North America Europe Australia Central and South America (declines in eastern Europe, Asia, and Africa suggested) How many amphibian species are threatened? more than 500 species worldwide listed as in decline in US 1/3 of known amphibian species thought to be in trouble most severe problems in western mountains also in Midwest and Southeast What are the possible causes of amphibian declines?

4 Defining Declines Many anurans (frogs and toads) exist as metapopulations population Study Year D. Green et al.

5 AmphibianPopulation Declines Amphibian population trends from 1950 to 1997 using 936 populations. Houlahan et al., Nature 404:752

6 Amphibian Population Declines Amphibian population trends from 1960 to 1997 for North America and Western Europe. Houlahan et al., Nature 404:752

7 Possible Causes for Amphibian Declines habitat destruction* disease** climate change exotic predators or competitors increased solar UV radiation contaminants synergistic effects * known cause ** extremely high probability

8 Diseases Chytridiomhycosis Ranaviral diseases (e.g. iridoviruses) Malformations

9 Chytrid Infection Histological section of severely infected digital skin of a wild frog, Litoria caerulea, from Queensland, Australia Berger, Lee et al. (1998) Proc. Natl. Acad. Sci. USA 95, Copyright 1998 by the National Academy of Sciences

10 Chytridiomycosis Fungal disease ubiquitous fungi infects plants, algae, protists, inverts. first described in amphibians 1998 Australia and Panama disease is considered emerging effects catastrophic: speed, death rate Attacks keratinized structures tadpoles = mouthparts adults = skin Amphibian susceptibility increases with cool, dry conditions

11 Global Temperature Change Global average temperatures (difference from normals, C), using air measurements at land stations and sea surface temperatures measured by ships and buoys. (From the Hadley Centre, U.K.)

12 Golden Toad Golden Toad Michael Fogden/Bruce Coleman, Inc

13 Climate Change and Chytridiomycosis Monteverde Cloud Forest Preserve, Costa Rica home of the Golden Toad as temperatures climb, cloud layer ascends normal limit of high moisture content leaving the golden toad s habitat drier more susceptibility to chytrid fungal infection

14 Amphibian Malformations

15 Acute Malformation Outbreaks Potential malformation agents: UV radiation Retinoid mimics Ribeiroia sp. Trematode parasites (Ribeiroia sp.) present currently/historically presence correlated with severity cause malformations in native frogs in lab parasites not present in all cases

16 Malformed Frogs Species N Malf Prev. (%) Rana pipiens Hyla spp R. clamitans R. sylvatica Bufo americanus R. septentrionalis Pseudacris crucifer Pseudacris triseriata R. catsbeiana unknown Total %

17 Historical Malformation Rates Analysis of museum specimens (D. Hoppe, 2000) early 1960 s collection overlapping geographical area 2166 Rana pipiens 0.3% malformation prevalence Other records agree with % malformation prevalence. Current prevalence of % represents a 5 to 6 fold increase over historic Midwestern prevalence.

18 Parasites and Amphibian Malformations Ecotoxicological Queries: why are malformations showing up in new areas? why are they showing up now? is the parasite increasing it s range? are the frogs more susceptible to parasitic infection? are there anthropogenic influences involved?

19 Increased UV B Radiation UV radiation reaching Earth s surface increasing greater effect in high latitudes greater effect at high altitudes Known UV effects on amphibians include: physiological problems, e.g. edema malformation decreased reproductive success immune suppression Possible mitigating factors rapid attenuation (especially with DOC) behavioral adaptation physiological adaptation (e.g. photolyase)

20 UV B Effects on Reproduction?

21 tadpoles

22 Effect of UV B on Hatching Success Field experiment results. a, Effects of water depth and exposure to UV B radiation on mean hatching success (+/ s.e.m.) for B. boreas. Open column, ultraviolet blocking filter; filled column, ultraviolet transmitting filter. b, Measurements of UV B flux (µw cm 2) at different depths Kiessecker et al., Nature 410:681

23 A Chemical Cause? Frogs may have been exposed to an Endocrine Disruptor natural or man made chemicals may mimic endogenous molecules exposure to exogenous endocrines can disrupt development

24 How Do Endocrines Work? Endocrine producing tissue e.g. gonad thyroid bloodstream Physiological effects e.g. growth blood pressure ovulation developmental control Endocrine sensitive tissue e.g. uterus gut

25 Atrazine corn 48.0 million acres USGS 1997

26 Atrazine Effects Presence of atrazine and metabolites: atrazine, DIA, DEA, and DAC at sites 1 8 (A) and frequency (%) of gonadal abnormalities in males collected from the wild (B). Atrazine contaminant levels for each site are also indicated in (B). Atrazine was not detected at site 1. Hayes et al., Environmental Health Perspectives

27 Atrazine Effects Frequency (percent) of gonadal abnormalities in males treated with atrazine in the laboratory. Hayes et al., Environmental Health Perspectives

28 Gonadal Development in R. pipiens male female Hayes et al., Environmental Health Perspectives

29 Gonadal Misdevelopment, R. pipiens Gonad of a male R. pipiens from site 8 (Clinton, Iowa). (A) Left testis fixed in Bouin's solution. The white arrow shows the area where the transverse cross section was taken; bar = 0.1 mm. (B) Transverse cross section taken from the area indicated by the white arrow in (A). Well developed testicular lobules with spermatids, and three lobules that contain both spermatids and a single large oocyte each; bar = 250 µm. Hayes et al., Environmental Health Perspectives

30 Gonadal Misdevelopment, R. pipiens Gonads of a R. pipiens hermaphrodite from Carbon County, Wyoming, undergoing what appears to be complete sex reversal. (A) Gonads (fixed in Bouin's solution) are becoming convoluted similar to an ovary. White arrows show the areas where the transverse cross sections were taken; bar = 0.1 mm. (B) Anterior and (C) posterior transverse cross sections reveal that the gonads contain numerous oocytes; bar = 250 µm. The animal has developed an ovarian cavity and lost its lobular structure. Hayes et al., Environmental Health Perspectives

31 Stressor Effects on Amphibians Stressors Biological Effects Global Climate Change { temperature precipitation UV B radiation accelerated development immune dysfunction species diversity (?) { habitat Agricultural Practices restructuring pesticides nutrients physiological stress immune dysfunction disease susceptibility developmental anomalies

32 Amphibian Stressors exotics new parasites pesticides UV emerging diseases pharmaceuticals acidification development / habitat fragmentation temperature eutrophication desiccation novel predators

33 Response to Multiple Stressors normal stress level Tolerance/ Resilience Total Stress / Multiple Stressors

34 Response to Multiple Stressors Tolerance/ Resilience normal stress level Multiple Stressors / Total Stress

35 Stress Pyramid Individuals death extinction Populations reproductive failure immune system stress increased disease elevated stress hormones population collapse local extinctions reproductive failure periodic loss of breeding class genetic bottlenecks Stress normal stressors limited food parasites disease competition periodic restrictions on fertility and fecundity Tolerance

36 Conclusions Amphibian declines are most likely real Some known causes habitat destruction diseases Likely that multiple stressors contribute to overall declines likely that many stressors are anthropogenic Deciphering causes of declines is likely to be difficult

37 Are Frogs Canaries in the Coal Mine? African reed frogs

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