James P. Collins

Ecological Aspects of Amphibian Metamorphosis: Nonnormal distributions of competitive ability reflect selection for facultative metamorphosis

A synthetic theory of the ecology of amphibian metamorphosis is founded on the observation that the large variation in length of larval period and body size at metamorphosis typical of a particular species of amphibian cannot be directly explained by differences in dates of hatching or egg sizes. It is proposed that as development proceeds, variation in exponential growth coefficients causes a trend from a normal distribution to a skewed distribution of body sizes. The degree of skewing increases and the median of the distribution decreases with increasing initial densities of populations. The relative advantages of the largest members of a cohort may arise from a variety of mechanisms including the production of growth inhibitors, interference competition, and size-selective feeding behavior. These mechanisms result in a nonnormal distribution of competitive ability, a possible source of the density-dependent competition coefficient found in systems with many species (1). In our model the ranges of body sizes and dates of metamorphosis are determined by a minimum body size that must be obtained and a maximum body size that will not be exceeded at metamorphosis. Between these two size thresholds the endocrinological initiation of metamorphosis is expected to be related to the recent growth history of the individual larva. Species that exploit uncertain environments will have a wide range of possible sizes at metamorphosis. Species exploiting relatively certain environments will have a narrower range. The evolution of neoteny and direct development logically follow from the application of these ideas to the ecological context of the evolution of amphibian life histories. Species that live in constant aquatic habitats surrounded by hostile environments (desert ponds, caves, high-altitude lakes) may evolve permanent larvae genetically incapable of metamorphosis. Other populations may evolve a facultative metamorphosis such that populations are a mixture of neotenes and terrestrial adults. Direct development results from selection to escape the competition, predation, and environmental uncertainty characteristic of some aquatic habitats and is usually accompanied by parental care. The relation between our ecological model and the physiological mechanisms that initiate metamorphosis can only be suggested and it remains an open problem for developmental biologists.

Environmental Certainty, Trophic Level, and Resource Availability in Life History Evolution

Evolutionary theory has not yet determined the necessary and sufficient environmental factors that can be used to explain the observed diversity of life history patterns in plants and animals. Although recent theoretical treatments of the evolution of life history rely heavily on the concepts of r- and K-selection, we find this framework inadequate to explain life histories of many well-known organisms. Instead, using well-studied examples from the literature, we attempt to identify causal mechanisms in the evolution of their life histories. The density of the population in relation to resources, the trophic and successional position of the population, and predictability of mortality patterns all appear to be important determinants of adaptive strategies. Therefore, consideration of many environmental dimensions seems essential to provide complete understanding of the evolution of life histories.

Regulating gene drives

Regulatory gaps must be filled before gene drives could be used in the wild Genes in sexually reproducing organisms normally have, on average, a 50% chance of being inherited, but some genes have a higher chance of being inherited. These genes can increase in relative frequency in a population even if they reduce the odds that each organism will reproduce. Aided by technological advances, scientists are investigating how populations might be altered by adding, disrupting, or editing genes or suppressed by propagating traits that reduce reproductive capacity (1, 2). Potential beneficial uses of such “gene drives” include reprogramming mosquito genomes to eliminate malaria, reversing the development of pesticide and herbicide resistance, and locally eradicating invasive species. However, drives may present environmental and security challenges as well as benefits.

Intrapopulation Variation in the Body Size at Metamorphosis and Timing of Metamorphosis in the Bullfrog, Rana Catesbeiana

Variation in body size at metamorphosis and the time of metamorphosis were studied for 3 yr in a population of bullfrogs at the E. S. George Reserve, Michigan, USA. The size at metamorphosis and the week of metamorphosis were positively related through the 1972 activity season and the last half of the 1973 activity season. During the first half of 1973 and all of 1974 there was no significant relationship between size at metamorphosis and time of metamorphosis. The data suggest that the 1971 larval year class transformed during 1972 and 1973, the 1972 year class during 1973 and 1974 and the 1973 year class during 1974. Variation in length of the larval period and body size at metamorphosis varied with density of conspecifics and time of oviposition during spring and early summer. Data for the Michigan population of frogs are consistent with predictions derived from a model of amphibian metamorphosis proposed by Wilbur and Collins (1973). A review of the literature indicates that length of the larval period among populations of bullfrogs in the United States is negatively correlated with mean length of the frost-free period.

Move it or lose it? The ecological ethics of relocating species under climate change

Managed relocation (also known as assisted colonization, assisted migration) is one of the more controversial proposals to emerge in the ecological community in recent years. A conservation strategy involving the translocation of species to novel ecosystems in anticipation of range shifts forced by climate change, managed relocation (MR) has divided many ecologists and conservationists, mostly because of concerns about the potential invasion risk of the relocated species in their new environments. While this is indeed an important consideration in any evaluation of MR, moving species across the landscape in response to predicted climate shifts also raises a number of larger and important ethical and policy challenges that need to be addressed. These include evaluating the implications of a more aggressive approach to species conservation, assessing MR as a broader ecological policy and philosophy that departs from longstanding scientific and management goals focused on preserving ecological integrity, and considering MR within a more comprehensive ethical and policy response to climate change. Given the complexity and novelty of many of the issues at stake in the MR debate, a more dynamic and pragmatic approach to ethical analysis and debate is needed to help ecologists, conservationists, and environmental decision makers come to grips with MR and the emerging ethical challenges of ecological policy and management under global environmental change.

Evidence for emergence of an amphibian iridoviral disease because of human-enhanced spread

Our understanding of origins and spread of emerging infectious diseases has increased dramatically because of recent applications of phylogenetic theory. Iridoviruses are emerging pathogens that cause global amphibian epizootics, including tiger salamander (Ambystoma tigrinum) die‐offs throughout western North America. To explain phylogeographical relationships and potential causes for emergence of western North American salamander iridovirus strains, we sequenced major capsid protein and DNA methyltransferase genes, as well as two noncoding regions from 18 geographically widespread isolates. Phylogenetic analyses of sequence data from the capsid protein gene showed shallow genetic divergence (< 1%) among salamander iridovirus strains and monophyly relative to available fish, reptile, and other amphibian iridovirus strains from the genus Ranavirus, suggesting a single introduction and radiation. Analysis of capsid protein sequences also provided support for a closer relationship of tiger salamander virus strains to those isolated from sport fish (e.g. rainbow trout) than other amphibian isolates. Despite monophyly based on capsid protein sequences, there was low genetic divergence among all strains (< 1.1%) based on a supergene analysis of the capsid protein and the two noncoding regions. These analyses also showed polyphyly of strains from Arizona and Colorado, suggesting recent spread. Nested clade analyses indicated both range expansion and long‐distance colonization in clades containing virus strains isolated from bait salamanders and the Indiana University axolotl (Ambystoma mexicanum) colony. Human enhancement of viral movement is a mechanism consistent with these results. These findings suggest North American salamander ranaviruses cause emerging disease, as evidenced by apparent recent spread over a broad geographical area.

INTRASPECIFIC RESERVOIRS: COMPLEX LIFE HISTORY AND THE PERSISTENCE OF A LETHAL RANAVIRUS

Virulent parasites cannot persist in small host populations unless the parasite also has a reservoir host. We hypothesize that, in hosts with complex life histories, one stage may act as an intraspecific reservoir for another. In amphibians, for example, larvae often occur at high densities, but these densities are ephemeral and fixed in space, whereas metamorphs are long-lived and vagile but may be very sparse. Parasite persistence is unlikely in either stage alone, but transmission between stages could maintain virulent parasites in seasonally fluctuating amphibian populations. We examined this hypothesis with a lethal ranavirus, Ambystoma tigrinum virus (ATV), that causes recurrent epidemics in larval tiger salamander populations, but which has no reservoir host and degrades quickly in the environment. Although exposure to ATV is generally lethal, larvae and metamorphs maintained sublethal, transmissible infections for >5 mo. Field data corroborate the persistence of ATV between epidemics in sublethally infected metamorphs. Three-quarters of dispersing metamorphs during one epidemic were infected, and apparently healthy metamorphs returning to breed harbored ATV infections. Our results suggest that larval epidemics amplify virus prevalence and sublethally infected metamorphs (re)introduce the virus into uninfected larval populations. Intraspecific reservoirs may explain the persistence of parasites in and declines of small, isolated amphibian populations.

Site occupancy models in the analysis of environmental DNA presence/absence surveys : a case study of an emerging amphibian pathogen

Summary 1. The use of environmental DNA (eDNA) to detect species in aquatic environments such as ponds and streams is a powerful new technique with many benefits. However, species detection in eDNA-based surveys is likely to be imperfect, which can lead to underestimation of the distribution of a species. 2. Site occupancy models account for imperfect detection and can be used to estimate the proportion of sites where a species occurs from presence/absence survey data, making them ideal for the analysis of eDNA-based surveys. Imperfect detection can result from failure to detect the species during field work (e.g. by water samples) or during laboratory analysis (e.g. by PCR). 3. To demonstrate the utility of site occupancy models for eDNA surveys, we reanalysed a data set estimating the occurrence of the amphibian chytrid fungus Batrachochytrium dendrobatidis using eDNA. Our reanalysis showed that the previous estimation of species occurrence was low by 5–10%. Detection probability was best explained by an index of the number of hosts (frogs) in ponds. 4. Per-visit availability probability in water samples was estimated at 0� 45 (95% CRI 0� 32, 0� 58) and per-PCR detection probability at 0� 85 (95% CRI 0� 74, 0� 94), and six water samples from a pond were necessary for a cumulative detection probability >95%. A simulation study showed that when using site occupancy analysis, researchers need many fewer samples to reliably estimate presence and absence of species than without use of site occupancy modelling. 5. Our analyses demonstrate the benefits of site occupancy models as a simple and powerful tool to estimate detection and site occupancy (species prevalence) probabilities despite imperfect detection. As species detection from eDNA becomes more common, adoption of appropriate statistical methods, such as site occupancy models, will become crucial to ensure that reliable inferences are made from eDNA-based surveys.

Amphibian Commerce as a Likely Source of Pathogen Pollution

The commercial trade of wildlife occurs on a global scale. In addition to removing animals from their native populations, this trade may lead to the release and subsequent introduction of nonindigenous species and the pathogens they carry. Emerging infectious diseases, such as chytridiomycosis caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd), and ranaviral disease have spread with global trade in amphibians and are linked to amphibian declines and die-offs worldwide, which suggests that the commercial trade in amphibians may be a source of pathogen pollution. We screened tiger salamanders involved in the bait trade in the western United States for both ranaviruses and Bd with polymerase chain reaction and used oral reports from bait shops and ranavirus DNA sequences from infected bait salamanders to determine how these animals and their pathogens are moved geographically by commerce. In addition, we conducted 2 surveys of anglers to determine how often tiger salamanders are used as bait and how often they are released into fishing waters by anglers, and organized bait-shop surveys to determine whether tiger salamanders are released back into the wild after being housed in bait shops. Ranaviruses were detected in the tiger salamander bait trade in Arizona, Colorado, and New Mexico, and Bd was detected in Arizona bait shops. Ranaviruses were spread geographically through the bait trade. All tiger salamanders in the bait trade were collected from the wild, and in general they moved east to west and north to south, bringing with them their multiple ranavirus strains. Finally, 26-73% of anglers used tiger salamanders as fishing bait, 26-67% of anglers released tiger salamanders bought as bait into fishing waters, and 4% of bait shops released tiger salamanders back into the wild after they were housed in shops with infected animals. The tiger salamander bait trade in the western United States is a useful model for understanding the consequences of the unregulated anthropogenic movement of amphibians and their pathogens through trade.

Distribution, Habitats and Life History Variation in the Tiger Salamander, Ambystoma tigrinum, in East-Central and Southeast Arizona

Ninety-eight aquatic habitats in east-central and southeast Arizona were sampled for tiger salamanders during 1977-79. These collections indicate two taxa in the region: Ambystoma tigrinum nebulosum and A. t. mavortium. A. t. nebulosum is a native species and is commonly associated with natural and artificial aquatic habitats in montane conifer forests, interior chaparral and subalpine grasslands at elevations > 1,500 m. It was collected in both lotic and lentic habitats. A. t. mavortium is probably introduced, and was collected in artificial lentic habitats in Sonoran desertscrub and semi-desert grassland at elevations < 1,600 m. Both taxa occur in intermediate elevation plains grassland and conifer woodland habitats.