(Translations may not be accurate.)


Originally posted 23 March 2004

Researchers are finding that multiple factors of decline are working synergistically to adversely affect amphibian populations. Combinations of multiple factors, such as, habitat destruction and introduced species, or climate change, UV-B and disease have a larger negative effect on amphibians than any single factor acting alone does. In fact, factors that may have little to no effect on amphibian populations may have large negative impacts when combined with other stressors. For example, pathogens may only have marginal effects on the demography of a healthy population, but the same pathogens can cause catastrophic declines in populations in the presence of sublethal concentrations of pesticides or UV-B radiation. Here we briefly summarize the findings of a few studies that have found synergisms between two or more factors of decline.

Synergisms involving climate change, UV-B, pesticides and disease

Disease has been implicated as a factor in the decline of amphibian populations worldwide, and it has been suggested that other factors of decline are working synergistically with disease (Blaustein et al. 1994, Laurance et al. 1996, Berger et al. 1998, Daszak 2000, Keisecker et al. 2001). It is uncertain if these infectious diseases are new agents that recently have been spread to the amphibian's geographic range (Laurance et al. 1996, Lips 1999), or old agents that previously co-existed with the amphibian but the pathogenicity of the agent recently increased or amphibian immune function recently decreased (Carey 1993). Here, we detail two examples in which it appears that one or more agents of decline, climate change, UV-B or pesticides, decreased amphibian immune function.

Climate Change, UV-B and disease: the case of the Western Toad

One excellent example of how multiple factors are working synergistically was discovered in The Pacific Northwest by Kiesecker, Blaustein and Belden (2002a). They noticed an increased mortality of Western toad (Bufo boreas) eggs in high elevation lakes in the Cascade Mountains by a parasitic fungus (Saprolignia ferix) during drought years. During years with low precipitation, embryos develop in extremely shallow water and are exposed to higher levels of UV-B radiation. In normal years (i.e. non-drought years), the physical properties of water protect embryos from high exposure to harmful UV-B radiation. During dry years, when amphibian embryos are exposed to increased amounts of UV-B radiation they are more susceptible to infection by Saprolignia ferix (Kiesecker et al. 2001a). Precipitation, and thus water depth/UV-B exposure, is strongly linked to El Niño or the Southern Oscillation cycles. Elevated sea-surface temperatures in this region since the mid-1970s have affected the climate over much of the world; for example, increasing the frequency and intensity of El Niño years. Thus, large-scale changes in climatic patterns could be a precursor for pathogen-mediated amphibian declines in several areas of the world.

normal Bufo boreas eggs and eggs infected with the parasitic fungus Saprolignia
Figure 1. Western toad eggs uninfected (left) and infected with Saprolignia ferix (right). Photos by Joseph Kiesecker

Exposure of leopard frogs (Rana pipiens) to a pesticide mixture affects life history characteristics of the lungworm Rhabdias ranae

Gendron et al. (2003) studied the infection dynamics of a common ranid frog parasite, the lungworm Rhabdias ranae, in adult leopard frogs (Rana pipiens) exposed to a mix of agricultural pesticides. They found that the migration of Rhabdias ranae was significantly accelerated in hosts exposed to the highest concentrations of pesticides, leading to the establishment of twice as many adult worms in the lungs of frogs 21 days post-infection. Furthermore, lungworms matured and reproduced earlier in frogs exposed to pesticides compared to frogs that were not exposed to pesticides. This plus other supporting evidence suggests that certain components of the frogís immune response were significantly suppressed after exposure to the pesticide mixture.

Leopard frog and the life cycle of Rhabdias ranae
Figure 2. Rana pipiens
photo © 2001 Joyce Gross (left). Life cycle of Rhabdias ranae (Rhabditidae) from Gendron et al. (2003) (right). The cycle includes a parasitic phase inside the frog and a free-living phase in the soil from which infective larvae arise. When in contact with a frog, infective larvae penetrate the skin (1) and migrate to the lungs (2) where they establish and become hermaphroditic adults (3). They then produce eggs which pass up the trachea, enter the gut (4) and hatch into larvae in the large intestine before they are released in feces (5). In the soil, these larvae molt into male and female adults that then mate (6). Ovoviviparous larvae that escape from degenerating females are infective (7).

Chemical contaminants alter predator prey dynamics

Amphibian populations are often embedded in agricultural landscapes. As such, amphibians in many areas around the world are exposed to pesticides, herbicides, and fertilizers, which are used liberally in these environments. The consequences of chemical contamination on amphibians can be subtle. Contaminants at sublethal levels can affect growth and development leading to developmental and behavioral abnormalities. These abnormalities may, in turn, increase susceptibility to predation and decrease reproductive success.

Effects of sublethal concentrations of carbaryl on Gray treefrog (Hyla versicolor) tadpoles

Our knowledge of pesticide effects on amphibians is largely limited to short-term (4-d) toxicity tests conducted under highly artificial conditions to determine lethal concentrations (LC50; see Contaminants for more details). Recently, several studies have examined the effects of sublethal pesticide doses and longer exposure times on amphibians.

Reylea and Mills (2001), exposed gray treefrog (Hyla versicolor) tadpoles to the pesticide carbaryl for 10ñ16 days (slightly longer than the usual 4 day LC50 toxicity tests) and used low pesticide concentrations (3-4% of the LC50 4-d concentration) and found that 10-60% of the tadpoles died. They then examined the response of tadpoles to low pesticide concentrations in the presence of predatory cues. When predator cues were present, they found that the pesticide became 2ñ4 times more lethal, killing 60-98% of tadpoles.

Bridges (1999), also exposed gray treefrog tadpoles to sublethal concentrations of carbaryl and found that the responses of exposed tadpoles were non-adaptive; they spent less time in refugia compared to tadpoles not exposed to carbaryl when predators were present, and more time in refugia when predators were absent. Thus, tadpoles increased their risk of predation by not increasing their time spent in refugia when predators were present, lowering overall survival.

In natural environments tadpoles are continuously exposed to predators and subjected to multiple environmental stressors. To survive, tadpoles must be able to effectively detect predators, hiding to escape predation in their presence and actively foraging in their absence. The results of Reylea and Mills (2001) and Bridges (1999), suggest that this is not the case for gray treefrog tadpoles exposed to sublethal carbaryl concentrations.

Introduced species and habitat modification

For invasive species and habitat destruction, invaders are more likely to integrate into communities and extirpate native species in permanently altered habitats than in pristine environments (Herbold and Moyle 1986, Moyle 1996). The American bullfrog (Rana catesbeiana) has been accidentally and intentionally introduced throughout the world (see introduced species). Invasive bullfrogs are more likely to become established in and extirpate native amphibians in man-made and heavily disturbed environments. Kiesecker et al. (2001b) found that competition between bullfrog and red-legged frog (Rana aurora) tadpoles was exacerbated in an artificial enclosure experiment when resources were clumped together (Kiesecker et al. 2001b). Kiesecker et al. (2001b) suggested that the clumping of resources in the enclosure experiment represented the effects of anthropogenic habitat modifications on the distribution of resources in a pond. When aquatic habitat is converted from shallow, ephemeral wetlands to deep permanent ponds, the lack of water level fluctuations results in the clumping of emergent vegetation in a narrow band around the ponds perimeter, in turn, resulting in clumped rather than dispersed resources (Kiesecker et al. 2001b).

Anthropogenic habitat modifications and the introduction of predatory fish are thought to be facilitating the spread of bullfrogs throughout western North America (Jennings and Hayes 1985, Adams 1999, Kiesecker et al. 2001b). Adams, Pearl and Bury (2003) found that invasion of bullfrogs is facilitated by the presence of co-evolved non-native fish. Non-native fish increase bullfrog tadpole survival by reducing predatory macroinvertebrate densities. Adams et al. (2003) found that in the absence of fish, native dragonfly nymphs caused zero survival of bullfrog tadpoles in a replicated field experiment unless a non-native sunfish was present to reduce dragonfly density. This pattern was also evident in pond surveys where the best predictors of bullfrog abundance were the presence of non-native fish and bathymetry (Adams et al. 2003). Such positive interactions among non-native species have the potential to disrupt ecosystems by amplifying invasions, and exacerbating the effect of exotic predators on native amphibians.

American Bullfrog tadpole and a foodweb diagram of bluegill fish, dragonfly nymphs, and tadpoles
Figure 3. Rana catesbeiana tadpole, photo © 2003 Pierre Fidenci (left). A food web diagram (© Rebecca Doubledee 2003) illustrating the interactions between bluegill, dragonfly nymphs (Aeshnids) and bullfrog tadpoles (right). Arrow width represents the strength of each interaction and the dashed arrows represent indirect effects.

Literature cited

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Adams, M. J., C. A. Pearl, and R. B. Bury. 2003. Indirect facilitation of an anuran invasion by non-native fishes. Ecology Letters 6:343-351.

Allran, J. W., and W. H. Karasov. 2000. Effects of atrazine and nitrate on northern leopard frog (Rana pipiens) larvae exposed in the laboratory from posthatch through metamorphosis. Environmental Toxicology & Chemistry [print] 19:2850-2855.

Berger, L., R. Speare, P. Daszak, D. E. Green, A. A. Cunningham, C. L. Goggin, R. Slocombe, M. A. Ragan, A. D. Hyatt, K. R. McDonald, H. B. Hines, K. R. Lips, G. Marantelli, and H. Parkes. 1998. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proceedings of the National Academy of Sciences of the United States of America 95:9031-9036.

Blaustein, A. R., D. G. Hokit, R. K. O'Hara, and R. A. Holt. 1994. Pathogenic fungus contributes to amphibian losses in the Pacific Northwest. Biological Conservation 67:251-254.

Bridges, C. M. 1999. Effects of a pesticide on tadpole activity and predator avoidance behavior. Journal of Herpetology 33:303-306.

Bridges, C. M. 1999b. Predator-prey interactions between two amphibian species: Effects of insecticide exposure. Aquatic Ecology 33:205-211.

Carey, C. 1993. Hypothesis concerning the causes of the disappearance of boreal toads from the mountains of Colorado. Conservation Biology 7:355-362.

Daszak, P., A. A. Cunningham, and A. D. Hyatt. 2000. Emerging infectious diseases of wildlife-Threats to biodiversity and human health. Science 287:443-449.

Gendron, A. D., D. J. Marcogliese, S. Barbeau, M. S. Christin, P. Brousseau, S. Ruby, D. Cyr, and M. Fournier. 2003. Exposure of leopard frogs to a pesticide mixture affects life history characteristics of the lungworm Rhabdias ranae. Oecologia 135:469-476.

Herbold, B., and P. B. Moyle. 1986. Introduced Species and Vacant Niches. American Naturalist 128:751-760.

Jennings, M. R., and M. P. Hayes. 1985. Pre-1900 overharvest of California [USA] red-legged frogs (Rana aurora draytonii): The inducement for bullfrog (Rana catesbeiana) introduction. Herpetologica 41:94-103.

Kiesecker, J. M., A. R. Blaustein, and L. K. Belden. 2001a. Complex causes of amphibian population declines. Nature V410:681-684.

Kiesecker, J. M., A. R. Blaustein, and C. L. Miller. 2001b. Potential mechanisms underlying the displacement of native red- legged frogs by introduced bullfrogs. Ecology 82:1964-1970.

Moyle, P. B. 1996. Effects of invading species on freshwater and estuarine ecosystems. Pages 86-92 in Proceedings of the Norway/UN Conference on Alien Species. Norwegian Institute for Nature Research (NINA), Trondheim, Norway.

Relyea, R. A., and N. Mills. 2001. Predator-induced stress makes the pesticide carbaryl more deadly to gray treefrog tadpoles (Hyla versicolor). Proceedings of the National Academy of Sciences of the United States of America (Allran and Karasov) 98:2491-2496.