Howard H. Whiteman

Evolutionary ecology of facultative paedomorphosis in newts and salamanders.

Facultative paedomorphosis is an environmentally induced polymorphism that results in the coexistence of mature, gilled, and fully aquatic paedomorphic adults and transformed, terrestrial, metamorphic adults in the same population. This polymorphism has been of interest to scientists for decades because it occurs in a large number of caudate amphibian taxa as well as in a large diversity of habitats. Numerous experimental and observational studies have been conducted to explain the proximate and ultimate factors affecting these heterochronic variants in natural populations. The production of each alternative phenotype is based on a genotype × environment interaction and research suggests that differences in the environment can produce paedomorphs through several ontogenetic pathways. No single advantage accounts for the maintenance of this polymorphism. Rather, the interplay of different costs and benefits explains the success of the polyphenism across variable environments. Facultative paedomorphosis allows individuals to cope with habitat variation, to take advantage of environmental heterogeneity in the presence of open niches, and to increase their fitness. This process is expected to constitute a first step towards speciation events, and is also an example of biodiversity at the intraspecific level. The facultative paedomorphosis system is thus ripe for future studies encompassing ecology, evolution, behaviour, endocrinology, physiology, and conservation biology. Few other systems have been broad enough to provide varied research opportunities on topics as diverse as phenotypic plasticity, speciation, mating behaviour, and hormonal regulation of morphology. Further research on facultative paedomorphosis will provide needed insight into these and other important questions facing biologists.

Foraging trade-offs along a predator-permanence gradient in subalpine wetlands

We conducted a series of field and laboratory experiments to determine the direct and indirect effects of a top predator, the tiger salamander (Ambystoma tigrinum nebulosum), on larvae of two species of limnephilid caddisflies (Limnephilus externus and Asynarchus nigriculus) in subalpine wetlands in central Colorado. Asynarchus larvae pre- dominate in temporary wetlands and are aggressive intraguild predators on Limnephilus larvae, which only predominate in permanent basins with salamanders. We first conducted a field experiment in mesocosms (cattle tanks) to quantify the predatory effects of different life stages of salamanders on the two caddisfly species. Two life stages of the salamanders (larvae and paedomorphs) preferentially preyed on Asynarchus relative to Limnephilus. Subsequent laboratory experiments revealed that high Asynarchus activity rates and rela- tively ineffective antipredatory behaviors led to higher salamander detection and attack rates compared to Limnephilus. In a second field experiment (full factorial for presence and absence of each of the three species), we found that salamander predation on Asynarchus had an indirect positive effect on Limnephilus: survival was higher in the presence of salamanders + Asynarchus than with just Asynarchus. In the laboratory we compared the predatory effects of salamanders with and without their mouths sewn shut and found the observed indirect positive effect on Limnephilus survival to be mainly the result of reduced numbers of Asynarchus rather than salamander-induced changes in Asynarchus behavior. We argue that indirect effects of predator-predator interactions on shared prey will be mainly density-mediated and not trait-mediated when one of the predators (in this case, Asynarchus) is under strong selection for rapid growth and therefore does not modify foraging behaviors in response to the other predator. The reciprocal dominance of Lim- nephilus and Asynarchus in habitats with and without salamanders probably reflects a trade- off between competitive superiority and vulnerability to predation. The high activity levels and aggressiveness that enable Asynarchus to complete development in temporary habitats result in strong asymmetric competition (via intraguild predation) with Limnephilus. In permanent habitats these same behaviors increase Asynarchus vulnerability to salamander predation, which indirectly benefits Limnephilus. This and previous work implicate sala- manders as keystone predators that exert a major influence on the composition of benthic and planktonic assemblages in subalpine wetlands.

Differential effects of mate competition and mate choice on eastern tiger salamanders

Male tiger salamanders, Ambystoma tigrinum tigrinumare slightly larger in body size and have considerably higher and longer tails than females. To determine how these dimorphic traits affected reproductive performance and success, we conducted breeding trials using 12 males and six females per trial and monitored male-female and male-male interactions. Larger males had an advantage in most aspects of mate competition investigated. Males with higher tails had no advantage in either mate competition or mate choice. Males with longer tails also had no advantage in mate competition but were preferred as mates by females. Larger males interrupted courting males more often than smaller males did. The form of male-male interference was conditional on body size and not on either tail dimension. If the intruder was larger than the courting male, it would shove the female away from the courting male and initiate courtship; if the intruder was smaller, it adopted a female mimicry tactic in which it positioned itself between the courting male and female and performed female behaviours to the courting male while simultaneously courting the female. Our trials indicated that the two components of sexual selection may influence the evolution of different male morphological traits in tiger salamanders. Mate competition may favour increased male body length; mate choice may select for greater male tail length.

Growth and foraging consequences of facultative paedomorphosis in the tiger salamander,Ambystoma tigrinum nebulosum

SummaryFacultative paedomorphosis in salamanders occurs when larvae respond to varying environmental conditions by either metamorphosing into terrestrial metamorphic adults or retaining their larval morphology to become sexually mature paedomorphic adults. Several hypotheses have been proposed for the evolutionary maintenance of this environmentally induced dimorphism, but few data are available to assess them adequately. We studied a montane population of the tiger salamander,Ambystoma tigrinum nebulosum, and measured the adult growth rate and body condition across three growing seasons to assess the relative costs and benefits of each morph. Metamorphic adults grew more than paedomorphic adults in terms of snout—vent length across years and in weight within years. Dietary analyses and foraging experiments revealed some of the proximate factors that may underlie these differential growth patterns. Across all prey, metamorphs had significantly higher biomass and calories per stomach sample than paedomorphs. Metamorphic diets primarily consisted of the fairy shrimpBranchinecta coloradensis, whereas paedomorphic diets contained a variety of benthic and terrestrial invertebrates. Foraging experiments revealed that both morphs are more successful at capturing fairy shrimp relative to other prey types and both show high electivity toward this prey. However, fairy shrimp occurred only in non-permanent ponds and thus are inaccessible to paedomorphs, which can survive only in permanent ponds. Paedomorphs also experience higher levels of intraspecific competition with large larvae in permanent ponds than metamorphs do in non-permanent ponds. Thus, metamorphs obtain a growth advantage over paedomorphs by foraging in non-permanent ponds that contain fairy shrimp and have reduced intraspecific competition. These results suggest that paedomorphs should have decreased fitness relative to metamorphs, primarily because metamorphs can move into the best habitats for growth. The net fitness effect of morph-specific differences in dispersal depend on whether there are trade-offs with other life history traits. Nonetheless, because the relative benefit of metamorph dispersal will change with environmental conditions in permanent ponds and the surrounding habitat, the relative fitness payoff to each morph should track changes in the environment. Thus, facultative paedomorphosis may be maintained in part by variable, environmentally-specific fitness payoffs to each morph.

Consumptive and nonconsumptive effects of cannibalism in fluctuating age‐structured populations

Theory and empirical studies suggest that cannibalism in age-structured populations can regulate recruitment depending on the intensity of intraspecific competition between cannibals and victims and the nature of the cannibalism window, i.e., which size classes interact as cannibals and victims. Here we report on a series of experiments that quantify that window for age-structured populations of salamander larvae and paedomorphic adults. We determined body size limits on cannibalism in microcosms and then the consumptive and nonconsumptive (injuries, foraging and activity, diet, growth) effects on victims in mesocosms with seminatural levels of habitat complexity and alternative prey. We found that cannibalism by the largest size classes (paedomorphs and > or = age 3+ yr larvae) occurs mainly on young-of-the-year (YOY) victims. Surviving YOY and other small larvae had increased injuries, reduced activity levels, and reduced growth rates in the presence of cannibals. Data on YOY survival in an experiment in which we manipulated the density of paedomorphs combined with historical data on the number of cannibals in natural populations indicate that dominant cohorts of paedomorphs can cause observed recruitment failures. Dietary data indicate that ontogenetic shifts in diet should preclude strong intraspecific competition between YOY and cannibals in this species. Thus our results are consistent with previous empirical and theoretical work that suggests that recruitment regulation by cannibalism is most likely when YOY are vulnerable to cannibalism but have low dietary overlap with cannibals. Understanding the role of cannibalism in regulating recruitment in salamander populations is timely, given the widespread occurrences of amphibian decline. Previous studies have focused on extrinsic (including anthropogenic) factors that affect amphibian population dynamics, whereas the data presented here combined with long-term field observations suggest the potential for intrinsically driven population cycles.

SEXUAL SELECTION IN AMERICAN TOADS: A TEST OF A GOOD-GENES HYPOTHESIS

Adaptive mate choice in species lacking male resource control and/or paternal care might be maintained by selection because preferred males sire genetically superior offspring. For such a process to occur, some male phenotypic trait(s) must both reliably indicate male genetic quality and influence the pattern of mate choice by females. In American toads, Bufo americanus, male body length has been documented to influence female mating patterns: females usually mate with males that are larger than average. However, the relationship between male size and male genetic quality is unknown. We conducted a controlled breeding experiment using 48 sires and 19 dams to determine if larger males sire offspring with superior larval performance characteristics (greater survival to metamorphosis, larger mass at metamorphosis, and earlier metamorphosis). We also aged each sire to test the hypothesis that older males are, on average, genetically superior to younger males. We crossed each female with three sires representing three body size categories (mean and 1 SD ± mean snout‐ischium length). Hatchlings (500 from each cross) were reared to metamorphosis in seminatural ponds in the field. Metamorph weight (log transformed) and age at metamorphosis showed significant heritability and were genetically correlated with each other. Hence, sires differed in genetic quality. However, none of the three measures of offspring performance was correlated with sire body size or age. Thus, we obtained no support for the prediction that sire body size or age is related to genetic quality.

Fluctuation in a rocky mountain population of salamanders : anthropogenic acidification or natural variation?

We monitored the demographics of the salamander Ambystoma tigrinum nebulosum as part of a community-wide study on the effects of acidification in sub-alpine (elevation 3600 m) ponds in central Colorado. A decline in A. t. nebulosum at this site from 1982 to 1988 has been hypothesized to result from embryonic mortality during a pulse of acidity that accompanies snowmelt in spring. Since 1988 we have monitored salamander population size, reproduction, and recruitment, and compared survival and individual growth rates among ponds which differ five-fold in acid-neutralizing capacity (ANC)

Larval growth in polyphenic salamanders: making the best of a bad lot

Polyphenisms are excellent models for studying phenotypic variation, yet few studies have focused on natural populations. Facultative paedomorphosis is a polyphenism in which salamanders either metamorphose or retain their larval morphology and eventually become paedomorphic. Paedomorphosis can result from selection for capitalizing on favorable aquatic habitats (paedomorph advantage), but could also be a default strategy under poor aquatic conditions (best of a bad lot). We tested these alternatives by quantifying how the developmental environment influences the ontogeny of wild Arizona tiger salamanders (Ambystoma tigrinum nebulosum). Most paedomorphs in our study population arose from slow-growing larvae that developed under high density and size-structured conditions (best of a bad lot), although a few faster-growing larvae also became paedomorphic (paedomorph advantage). Males were more likely to become paedomorphs than females and did so under a greater range of body sizes than females, signifying a critical role for gender in this polyphenism. Our results emphasize that the same phenotype can be adaptive under different environmental and genetic contexts and that studies of phenotypic variation should consider multiple mechanisms of morph production.

Accuracy Assessment of Skeletochronology in the Arizona Tiger Salamander (Ambystoma Tigrinum Nebulosum)

Abstract Skeletochronology is the most commonly used tool for evaluating the age of amphibians and reptiles. However, the accuracy of skeletochronology is questionable because few studies have utilized individuals of known age to calibrate their results. In this study, the accuracy of skeletochronology was assessed using individual Arizona Tiger Salamanders (Ambystoma tigrinum nebulosum) that were of known ages that varied from 2–15 years. Cross-sections of salamander toes were analyzed to compare the number of LAG (lines of arrested growth) to the actual age of known cohorts. Our results suggest that skeletochronology was an inaccurate tool for estimating age in this population of A. tigrinum nebulosum because it grossly underestimated age. The high intensity of endosteal resorption coupled with rapprochement of the most peripheral LAG may have produced these results. Our research indicates that skeletochronological studies that do not use individuals of known age for calibration may underestimate age.

MAINTENANCE OF POLYMORPHISM PROMOTED BY SEX-SPECIFIC FITNESS PAYOFFS

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