Ecologists increasingly recognize pathogens as playing significant roles in community dynamics, yet few experimental studies have documented patterns of disease impacts on natural systems. We studied the effects of a pathogenic fungus (Batrachochytrium dendrobatidis) on community interactions between two sympatric North American anurans: Fowler's toad, Bufo fowleri, and the gray treefrog, Hyla chrysoscelis. Recent studies have identified chytridiomycosis as an emerging infectious disease, whose widespread occurrence poses a significant risk for amphibian populations. We manipulated the presence of B. dendrobatidis in replicated experimental tanks and examined if exposure to this fungus during development could influence recruitment and competitive interactions between larval Bufo and Hyla. Tanks were followed throughout larval development, and we recorded survival, time to metamorphosis, and body mass at metamorphosis. We also tested the effects of competitive and pathogen-mediated stress on developmental stability by measuring fluctuating asymmetry (FA) of surviving metamorphs. B. dendrobatidis had no significant effect on larval survival, but the pathogen reduced metamorphic body mass and increased larval-period length. B. dendrobatidis had different effects on larval growth depending on the community structure; in the presence of the pathogen, both Bufo and Hyla metamorphosed at smaller body masses when reared together compared to when reared separately. Bufo also had strong negative effects on Hyla development, but only in the presence of B. dendrobatidis. FA of hind-limb length was significantly higher for metamorphs from pathogen tanks, but was not associated with density or competitive environment. Our results suggest that chytridiomycosis may impact Bufo and Hyla directly by reducing life-history performance and increasing developmental instability, and indirectly by inducing interspecific competitive effects in mixed-species environments.
The immune system is a necessary, but potentially costly, defense against infectious diseases. When nutrition is limited, immune activity may consume a significant amount of an organism's energy budget. Levels of dietary protein affect immune system function; high levels can enhance disease resistance. We exposed southern leopard frog [Lithobates sphenocephalus (=Rana sphenocephala)] tadpoles to high and low protein diets crossed with the presence or absence of the pathogenic amphibian chytrid fungus (Batrachochytrium dendrobatidis; Bd) and quantified: (1) tadpole resistance to Bd; (2) tadpole skin-swelling in response to phytohaemagglutinin (PHA) injection (a measure of the T cell-mediated response of the immune system); (3) bacterial killing ability (BKA) of tadpole blood (a measure of the complement-mediated cytotoxicity of the innate immune system); and (4) tadpole growth and development. Tadpoles raised on a low-protein diet were smaller and less developed than tadpoles on a high-protein diet. When controlled for developmental stage, tadpoles raised on a low-protein diet had reduced PHA and BKA responses relative to tadpoles on a high-protein diet, but these immune responses were independent of Bd exposure. High dietary protein significantly increased resistance to Bd. Our results support the general hypothesis that host condition can strongly affect disease resistance; in particular, fluctuations in dietary protein availability may change how diseases affect populations in the field.
Pathogen-induced modifications in host behavior, including alterations in foraging behavior or foraging efficiency, can compromise host fitness by reducing growth and development. Chytridiomycosis is an infectious disease of amphibians caused by the fungus Batrachochytrium dendrobatidis (Bd), and it has played an important role in the worldwide decline of amphibians. In larval anurans, Bd infections commonly result in reduced developmental rates, however, the mechanism(s) responsible are untested. We conducted laboratory experiments to test whether Bd infections reduced foraging performance of Grey Treefrog (Hyla chrysoscelis) and Fowler's Toad (Anaxyrus [= Bufo] fowleri) tadpoles. In the first experiment, we observed foraging behavior of Bd-infected and uninfected tadpoles to test for differences in foraging activity. In a second experiment, we tested for differences in the ingestion rates of tadpoles by examining the amount of food in their alimentary track after a 3-hour foraging period. We hypothesized that Bd-infected tadpoles would forage less often and less efficiently than uninfected tadpoles. As predicted, Bd-infected larvae forage less often and were less efficient at obtaining food than uninfected larvae. Our results show that Bd infections reduce foraging efficiency in Anaxyrus and Hyla tadpoles, and that Bd differentially affects foraging behavior in these species. Thus, our results provide a potential mechanism of decreased developmental rates of Bd-infected tadpoles.
Distinguishing whether pathogens are novel or endemic is critical for controlling emerging infectious diseases, an increasing threat to wildlife and human health. To test the endemic vs. novel pathogen hypothesis, we present a unique analysis of intraspecific host-pathogen phylogenetic concordance of tiger salamanders and an emerging Ranavirus throughout Western North America. There is significant non-concordance of host and virus gene trees, suggesting pathogen novelty. However, non-concordance has likely resulted from virus introductions by human movement of infected salamanders. When human-associated viral introductions are excluded, host and virus gene trees are identical, strongly supporting coevolution and endemism. A laboratory experiment showed an introduced virus strain is significantly more virulent than endemic strains, likely due to artificial selection for high virulence. Thus, our analysis of intraspecific phylogenetic concordance revealed that human introduction of viruses is the mechanism underlying tree non-concordance and possibly disease emergence via artificial selection.
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