Life-history trade-offs influence disease in changing climates: strategies of an amphibian pathogen

Life-history trade-offs allow many animals to maintain reproductive fitness across a range of climatic conditions. When used by parasites and pathogens, these strategies may influence patterns of disease in changing climates. The chytrid fungus, Batrachochytrium dendrobatidis, is linked to global declines of amphibian populations. Short-term growth in culture is maximal at 17 degrees-25 degrees C. This has been used in an argument that global warming, which increases the time that amphibians spend at these temperatures in cloud-covered montane environments, has led to extinctions. Here we show that the amphibian chytrid responds to decreasing temperatures with trade-offs that increase fecundity as maturation rate slows and increase infectivity as growth decreases. At 17 degrees-25 degrees C, infectious zoospores encyst (settle and develop a cell wall) and develop into the zoospore-producing stage (zoosporangium) faster, while at 7 degrees-10 degrees C, greater numbers of zoospores are produced per zoosporangium; these remain infectious for a longer period of time. We modeled the population growth of B. dendrobatidis through time at various temperatures using delayed differential equations and observational data for four parameters: developmental rate of thalli, fecundity, rate of zoospore encystment, and rate of zoospore survival. From the models, it is clear that life-history trade-offs allow B. dendrobatidis to maintain a relatively high long-term growth rate at low temperatures, so that it maintains high fitness across a range of temperatures. When a seven-day cold shock is simulated, the outcome is intermediate between the two constant temperature regimes, and in culture, a sudden drop in temperature induces zoospore release. These trade-offs can be ecologically important for a variety of organisms with complex life histories, including pathogenic microorganisms. The effect of temperature on amphibian mortality will depend on the interaction between fungal growth and host immune function and will be modified by host ecology, behavior, and life history. These results demonstrate that B. dendrobatidis populations can grow at high rates across a broad range of environmental temperatures and help to explain why it is so successful in cold montane environments.     

TOWARDS CHARACTERIZING AND PLANNING FOR DROUGHT IN VERMONT‐PART I: A CLIMATOLOGICAL PERSPECTWE1

ABSTRACT: In the Green Mountain state of Vermont, droughts of one form or another and of varying intensities, seventies, and areal extent are not uncommon occurrences. The 1990s were marked by at least three drought events of which the 1998 to 1999 was the most recent. In spite of this recurrence, ongoing drought monitoring and mitigative planning efforts are not as advanced as they could be and no official drought plan exists for the state. This article is the first of two in this volume. It summarizes the cascade of drought types that impacted the state during the 1998 to 1999 episode. From a number of precipitation statistics and drought indices, fine spatial scales (county or better) were found to best capture the character of drought impacts, while the weekly time step is recommended as the temporal unit around which to base planning and monitoring efforts. The companion article outlines a possible framework for drought planning efforts and highlights key constituencies to be included in the process.     

Sex differences in the repeatability of boldness over metamorphosis

Consistent individual differences in boldness have been identified in many species and can have important effects on fitness. In most animals, juveniles face different costs and benefits of risk-taking behavior than do adults. Furthermore, profound changes in hormones, morphology and environment often occur when juveniles become adults. Therefore, the boldness of individuals might change with ontogeny. In field crickets, adult males call to attract sexually receptive females, and male calling increases predation risk. We measured the repeatability of boldness (latency to emerge from a safe refuge) in both male and female crickets. Each cricket was tested once as a small nymph and once as an adult. We found that boldness was repeatable across metamorphosis in females, but not in males. Males became less bold with maturation, a result that we predicted because of the risk associated with calling for mates. We also found that in general, nymphs were bolder than adults and that individuals spent more time immobile in response to a predator cue when they were nymphs, versus when they were adults.     

Do rewardless orchids show a positive relationship between phenotypic diversity and reproductive success?

Among rewardless orchids, pollinator sampling behavior has been suggested to drive a positive relationship between population phenotypic variability and absolute reproductive success, and hence population fitness. We tested this hypothesis by constructing experimental arrays using the rewardless orchid Dactylorhiza sambucina, which is dimorphic for corolla color. We found no evidence that polymorphic arrays had higher mean reproductive success than monomorphic arrays for pollinia removal, pollen deposition, or fruit set. For pollinia removal, monomorphic yellow arrays had significantly greater reproductive success, and monomorphic red the least. A tendency for yellow arrays to have higher pollen deposition was also found. We argue that differential population fitness was most likely to reflect differential numbers of pollinators attracted to arrays, through preferential long-distance attraction to arrays with yellow inflorescences. Correlative studies of absolute reproductive success in 52 populations of D. sambucina supported our experimental results. To our knowledge this is the first study to suggest that attraction of a greater number of pollinators to rewardless orchids may be of greater functional importance to population fitness, and thus ecology and conservation, than are the behavioral sequences of individual pollinators.     

Prey density and the behavioral flexibility of a marine predator: the common murre (Uria aalge)

Flexible time budgets allow individual animals to buffer the effects of variable food availability by allocating more time to foraging when food density decreases. This trait should be especially important for marine predators that forage on patchy and ephemeral food resources. We examined flexible time allocation by a long-lived marine predator, the Common Murre (Uria aalge), using data collected in a five-year study at three colonies in Alaska (USA) with contrasting environmental conditions. Annual hydroacoustic surveys revealed an order-of-magnitude variation in food density among the 15 colony-years of study. We used data on parental time budgets and local prey density to test predictions from two hypotheses: Hypothesis A, the colony attendance of seabirds varies nonlinearly with food density; and Hypothesis B, flexible time allocation of parent murres buffers chicks against variable food availability. Hypothesis A was supported; colony attendance by murres was positively correlated with food over a limited range of poor-to-moderate food densities, but independent of food over a broader range of higher densities. This is the first empirical evidence for a nonlinear response of a marine predator's time budget to changes in prey density. Predictions from Hypothesis B were largely supported: (1) chick-feeding rates were fairly constant over a wide range of densities and only dropped below 3.5 meals per day at the low end of prey density, and (2) there was a nonlinear relationship between chick-feeding rates and time spent at the colony, with chick-feeding rates only declining after time at the colony by the nonbrooding parent was reduced to a minimum. The ability of parents to adjust their foraging time by more than 2 h/d explains why they were able to maintain chick-feeding rates of more than 3.5 meals/d across a 10-fold range in local food density.     

Invasive species impacts on ecosystem structure and function: A comparison of the Bay of Quinte, Canada, and Oneida Lake, USA, before and after zebra mussel invasion

As invasion rates of exotic species increase, an ecosystem level understanding of their impacts is imperative for predicting future spread and consequences. We have previously shown that network analyses are powerful tools for understanding the effects of exotic species perturbation on ecosystems. We now use the network analysis approach to compare how the same perturbation affects another ecosystem of similar trophic status. We compared food web characteristics of the Bay of Quinte, Lake Ontario (Canada), to previous research on Oneida Lake, New York (USA) before and after zebra mussel (Dreissena polymorpha) invasion. We used ecological network analysis (ENA) to rigorously quantify ecosystem function through an analysis of direct and indirect food web transfers. We used a social network analysis method, cohesion analysis (CA), to assess ecosystem structure by organizing food web members into subgroups of strongly interacting predators and prey. Together, ENA and CA allowed us to understand how food web structure and function respond simultaneously to perturbation. In general, zebra mussel effects on the Bay of Quinte, when compared to Oneida Lake, were similar in direction, but greater in magnitude. Both systems underwent functional changes involving focused flow through a small number of taxa and increased use of benthic sources of production; additionally, both systems structurally changed with subgroup membership changing considerably (33% in Oneida Lake) or being disrupted entirely (in the Bay of Quinte). However, the response of total ecosystem activity (as measured by carbon flow) differed between both systems, with increasing activity in the Bay of Quinte, and decreasing activity in Oneida Lake. Thus, these analyses revealed parallel effects of zebra mussel invasion in ecosystems of similar trophic status, yet they also suggested that important differences may exist. As exotic species continue to disrupt the structure and function of our native ecosystems, food web network analyses will be useful for understanding their far-reaching effects.     

Adaptations in a hierarchical food web of southeastern Lake Michigan

Two issues in ecological network theory are: (1) how to construct an ecological network model and (2) how do entire networks (as opposed to individual species) adapt to changing conditions? We present a novel method for constructing an ecological network model for the food web of southeastern Lake Michigan (USA) and we identify changes in key system properties that are large relative to their uncertainty as this ecological network adapts from one time point to a second time point in response to multiple perturbations. To construct our food web for southeastern Lake Michigan, we followed the list of seven recommendations outlined in Cohen et al. [Cohen, J.E., et al., 1993. Improving food webs. Ecology 74, 252–258] for improving food webs. We explored two inter-related extensions of hierarchical system theory with our food web; the first one was that subsystems react to perturbations independently in the short-term and the second one was that a system's properties change at a slower rate than its subsystems’ properties. We used Shannon's equations to provide quantitative versions of the basic food web properties: number of prey, number of predators, number of feeding links, and connectance (or density). We then compared these properties between the two time-periods by developing distributions of each property for each time period that took uncertainty about the property into account. We compared these distributions, and concluded that non-overlapping distributions indicated changes in these properties that were large relative to their uncertainty. Two subsystems were identified within our food web system structure (p < 0.001). One subsystem had more non-overlapping distributions in food web properties between Time 1 and Time 2 than the other subsystem. The overall system had all overlapping distributions in food web properties between Time 1 and Time 2. These results supported both extensions of hierarchical systems theory. Interestingly, the subsystem with more non-overlapping distributions in food web properties was the subsystem that contained primarily benthic taxa, contrary to expectations that the identified major perturbations (lower phosphorous inputs and invasive species) would more greatly affect the subsystem containing primarily pelagic taxa. Future food-web research should employ rigorous statistical analysis and incorporate uncertainty in food web properties for a better understanding of how ecological networks adapt.     

Trophic specialisation of metazoan meiofauna at the Håkon Mosby Mud Volcano: fatty acid biomarker isotope evidence

We report the results of a detailed investigation on the trophoecology of two dominant meiofaunal species at the Håkon Mosby Mud Volcano (HMMV), a deep-sea cold methane-venting seep. Analyses of fatty acids (FAs) and their stable carbon isotopes were used to determine the importance of chemosynthetic nutritional pathways for the dominant copepod species (morphologically very similar to Tisbe wilsoni) inhabiting the volcano’s centre and the abundant nematode Halomonhystera disjuncta from the surrounding microbial mats. The strong dominance of bacterial biomarkers (16:1ω7c, 18:1ω7c and 16:1ω8c) coupled with their individual light carbon isotopes signatures (δ¹³C ranging from ?52 to ?81‰) and the lack of symbiotic relationships with prokaryotes (as revealed by molecular analyses and fluorescent in situ hybridisation) indicated that chemosynthetically derived carbon constitutes the main diet of both species. However, the copepod showed a stronger reliance on the utilisation of methanotrophic bacteria and contained polyunsaturated FAs of bacterial origin (20:5ω3 and 22:6ω3 with isotope signatures δ¹³C < ?80‰). Instead, the FA profiles of H. disjuncta suggested that sulphide-oxidising bacteria constituted the main diet of this nematode. Therefore, HMMV can be regarded as a persistent deep-sea cold seep, allowing a chemosynthesis-based trophic specialisation by the dominant meiofaunal species inhabiting its sediments. The present investigation, through the determination of the fatty acid profiles, provides the first evidence for trophic specialisation of meiofauna associated with sub-habitats within a cold seep.