Mark C. Belk

Bergmann's Rule in Ectotherms: A Test Using Freshwater Fishes

Understanding patterns of variation in body size within and among species is a central question in evolutionary ecology (Schlichting and Pigliucci 1998). The most well known pattern of variation in body size is Bergmann’s rule (Bergmann 1847; Mayr 1956). The intraspecific version of Bergmann’s rule holds that within endothermic species, body size increases with increasing latitude (or decreasing temperature; Blackburn et al. 1999; Ashton et al. 2000). In general, mammals conform to this rule (Ashton et al. 2000). Ray (1960) proposed that ectothermic organisms also follow Bergmann’s rule, on the basis of primarily one line of argument. Specifically, ectotherms reared at relatively lower temperatures typically mature later at larger sizes when compared with conspecifics reared at higher temperatures (Atkinson 1994; Sibly and Atkinson 1994). Ray (1960) reasoned that the negative slope of the reaction norm between size at maturity and rearing temperature combined with generally lower temperatures at higher latitudes would produce a cline of increasing body size with increasing latitude. Ray (1960) summarized field data from previous studies to add generality to his claim of ectotherms following Bergmann’s rule. In regard to fishes, he states that “the rule is obeyed by a great number of fishes as shown by numerous reports in the literature” (Ray 1960, p. 93), but he provides no citations related to variation in body size across latitude. All his citations regarding fish apply to meristic counts

Cost of Reproduction, Resource Quality, and Terminal Investment in a Burying Beetle

We evaluate the cost‐of‐reproduction hypothesis in the burying beetle Nicrophorus orbicollis and examine how the importance of this trade‐off changes as females age (i.e., the terminal‐investment hypothesis). These beetles breed on small vertebrate carcasses, which serve as a food resource for them and their offspring. Consistent with the cost‐of‐reproduction hypothesis, females manipulated to overproduce offspring suffered a reduction in fecundity and life span when compared to controls, although all reproducing females had reduced life spans compared to nonbreeding females. Older females produced larger broods and allocated less of the carcass to their own body mass and a greater proportion to offspring than did younger females. Resource allocation to offspring increased with age. Females given larger carcasses invested more in current reproduction and less in future reproduction than did females given smaller carcasses. Our results provide unconfounded support for both the cost‐of‐reproduction hypothesis (i.e., current reproduction constrains future reproductive output) and the terminal‐investment hypothesis (i.e., the importance of the trade‐off between current and future reproduction declines with age such that allocation to current reproduction should increase as females age).

Risk assessment in western mosquitofish (Gambusia affinis): do multiple cues have additive effects?

Abstract. The threat-sensitivity hypothesis predicts that prey individuals will increase antipredator behaviors as apparent predator risk increases. An implicit assumption of the threat-sensitivity hypothesis is that predator risk is additive. In other words, all characteristics of a predator that indicate risk should contribute in an additive way to determine the degree of risk-sensitive behavior. We tested this assumption in the laboratory by presenting live predators (green sunfish, Lepomis cyanellus) to groups of western mosquitofish (Gambusia affinis). We examined effects of predator diet, hunger level, and size on predator avoidance and inspection behavior of mosquitofish. Both predator diet and predator hunger level were significant and additive determinants of distance maintained from a predator, resulting in a graded response to combinations of these predator cues. In contrast, whereas predator diet was the most important determinant of general avoidance distances, predator hunger level was more important in determining mosquitofish vertical distribution and inspection behavior. Thus, the relationship between predator cue and the antipredator behavior that it elicits is dependent on which cues and behaviors are examined. Our data suggest that during risky behaviors, such as predator inspection, mosquitofish rely mainly on visual cues (behavior differences between hungry and satiated predators), whereas general avoidance behavior is determined by additive responses from visual and chemical cues.

Neglected Taxonomy of Rare Desert Fishes: Congruent Evidence for Two Species of Leatherside Chub

Conservation biologists rely heavily on taxonomy to set the scope for biological monitoring and recovery planning of rare or threatened species. Yet, taxonomic boundaries are seldom evaluated as falsifiable hypotheses that can be statistically tested. Here, we examine species boundaries in leatherside chub (Teleostei, Cyprinidae), an imperiled desert fish native to the Bonneville Basin and upper Snake River drainages of western North America. Recent molecular data hint that this fish could be composed of two distinct taxa that are geographically separated into northern and southern species. To formally test this hypothesis, we evaluated leatherside chub using several different categories of species concepts, including criteria dependent on phylogenetic, morphological, and ecological data. We found that leatherside chub is composed of two reciprocally monophyletic clades (candidate species) characterized by numerous fixed genetic differences for both mitochondrial and nuclear DNA markers; mtDNA sequence divergence between the two clades approached 8%. The candidate species also showed significant differences in cranial shape, revealed by morphometric analysis. Finally, controlled growth and foraging experiments using representative populations from each clade show that candidate species appear to be locally adapted to the thermal environments where they now occur. Combined, these three lines of evidence support the hypothesis that leatherside chub is composed of two species. Moreover, all lines of evidence place these two species within the genusLepidomeda, a group consisting of three additional species of endangered spinedace fishes, and one extinct species, all native to the Colorado River system. Hence, we elevate the two clades of leatherside chub to distinct species status (Lepidomeda copeiin the north andL. aliciaein the south), and argue that each warrants independent conservation and recovery action.

Empirical tests for ecological exchangeability

The concept of ecological exchangeability, together with genetic exchangeability, is central to both the Cohesion Species Concept as well as to some definitions of Evolutionarily Significant Units. While there are well-established criteria for measuring genetic exchangeability, the concept of ecological exchangeability has generated considerable confusion. We describe a procedure that uses the complementary strengths, while recognising the limitations, of both molecular genetic data and ecological experiments to determine the ecological exchangeability of local populations within a species. This is the first synthesis of a combined approach (experiments and genetics) and the first explicit discussion of testing ecological exchangeability. Although it would be ideal to find functional genes that interact to influence quantitative traits resulting in ecological differences (e.g. growth, size, fecundity), we suggest that our current knowledge of functional markers is too limited for most species to use them to differentiate adaptively different local populations. Thus, we argue that ecological experiments using whole organisms combined with neutral markers that indicate evolutionary divergence, provide the strongest case for detecting adaptive differences among local populations. Both genetic divergence and ecological experiments provide the best information for infering ecological exchangeability. This procedure can be used to decide which local populations should be preserved to maintain intraspecific variation and to determine which populations would enhance captive-breeding programs, augment endangered local populations and could best be used to re-introduce native species into historically occupied areas.

Predator-induced delayed maturity in bluegill sunfish (Lepomis macrochirus): variation among populations

Abstract Previous studies suggested that differences in age at maturity among populations of bluegill sunfish (Lepomis macrochirus) were not genetically based, but rather were a phenotypic response to the presence of predators. I conducted two experiments to determine if the presence of largemouth bass affected age at maturity in bluegill sunfish. Bluegills from three populations were tested to see if the response to the threat of predation varied among source populations. Juvenile bluegills were maintained in the presence of predators or in controls with no contact with predators. Refuge use and growth were monitored during the experiments and reproductive activity was evaluated when bluegills reached age 1. Bluegills from one population exhibited delayed maturity in the presence of predators. Individuals from the other two populations showed no significant differences between predator and control treatments. The population that responded to the presence of predators had a history of high predation levels over the past 30–40 years. The other populations had a history of low levels of predation. This study suggests that presence of predators can induce phenotypic shifts in age at maturity of bluegills, but that the magnitude of response varies among populations in a manner consistent with historical patterns of coexistence.

Ontogeny and sex alter the effect of predation on body shape in a livebearing fish: sexual dimorphism, parallelism, and costs of reproduction

Predation can cause morphological divergence among populations, while ontogeny and sex often determine much of morphological diversity among individuals. We used geometric morphometrics to characterize body shape in the livebearing fish Brachyrhaphis rhabdophora to test for interactions between these three major shape-determining factors. We assessed shape variation between juveniles and adults of both sexes, and among adults for populations from high- and low-predation areas. Shape differed significantly between predation regimes for all juveniles regardless of sex. As males grew and matured into adults, ontogenetic shape trajectories were parallel, thus maintaining shape differences in adult males between predation environments. However, shape of adult females between predation environments followed a different pattern. As females grew and matured, ontogenetic shape trajectories converged so that shape differences were less pronounced between mature females in predator and nonpredator environments. Convergence in female body shape may indicate a trade-off between optimal shape for predator evasion versus shape required for the livebearing mode of reproduction.

Ground-truthing the impact of invasive species: spatio-temporal overlap between native least chub and introduced western mosquitofish

Western mosquitofish (Gambusia affinis) are one of the most destructive introduced species in the American West. The negative impact of introduced species on native taxa depends on their spatio-temporal overlap, which will determine the availability of refugia for native species. Experiments on the mechanisms underlying the interactions between introduced and native species rarely address habitat use, overlap, and refugia because individuals are confined to enclosures. In a previous study we used cages, microcosms, and aquaria to show that mosquitofish could prey on and out-compete native least chub (Iotichthys phlegethontis). In this study, we examined the spatio-temporal overlap between mosquitofish and least chub under natural conditions. We found periods of overlap and partitioning in the seasonal and diel habitat use of these species. Both species used shallow habitats during the day and night throughout the spring when least chub were spawning. Predation by adult mosquitofish on young least chub during the spring likely explains the reduction in least chub recruitment in the presence of mosquitofish. During the summer least chub avoided mosquitofish by exclusively using cooler habitats, or by occupying deeper, cooler habitats during the day when mosquitofish were active, and shallower, warmer habitats at night when mosquitofish were inactive. A shift to cooler habitats in the presence of mosquitofish may result in decreased growth and fecundity of least chub. However, we suggest that a reduction of warm shallow habitat may have a disproportionately greater negative impact on mosquitofish than species native to temperate regions, such as least chub. Habitat manipulations that reduce or eliminate warm habitats may ameliorate the harmful effects of mosquitofish and promote the long-term persistence of native taxa.

Morphological divergence driven by predation environment within and between species of Brachyrhaphis fishes.

Natural selection often results in profound differences in body shape among populations from divergent selective environments. Predation is a well-studied driver of divergence, with predators having a strong effect on the evolution of prey body shape, especially for traits related to escape behavior. Comparative studies, both at the population level and between species, show that the presence or absence of predators can alter prey morphology. Although this pattern is well documented in various species or population pairs, few studies have tested for similar patterns of body shape evolution at multiple stages of divergence within a taxonomic group. Here, we examine morphological divergence associated with predation environment in the livebearing fish genus Brachyrhaphis. We compare differences in body shape between populations of B. rhabdophora from different predation environments to differences in body shape between B. roseni and B. terrabensis (sister species) from predator and predator free habitats, respectively. We found that in each lineage, shape differed between predation environments, consistent with the hypothesis that locomotor function is optimized for either steady swimming (predator free) or escape behavior (predator). Although differences in body shape were greatest between B. roseni and B. terrabensis, we found that much of the total morphological diversification between these species had already been achieved within B. rhabdophora (29% in females and 47% in males). Interestingly, at both levels of divergence we found that early in ontogenetic development, females differed in shape between predation environments; however, as females matured, their body shapes converged on a similar phenotype, likely due to the constraints of pregnancy. Finally, we found that body shape varies with body size in a similar way, regardless of predation environment, in each lineage. Our findings are important because they provide evidence that the same source of selection can drive similar phenotypic divergence independently at multiple divergence levels.

Effects of Predation on Life-History Evolution in Utah Chub (Gila atraria)

We compared eight populations of Utah chub (Gila atraria), isolated since the late Pleistocene, to evaluate the relationship between predation by cutthroat trout (Oncorhynchus clarki) and chub life histories. Utah chub populations that have historically coexisted with cutthroat trout show higher juvenile growth rates, delayed age at maturity, larger size at maturity, and lower female reproductive effort than isolated populations with no predators. These results are consistent with life-history models of size-selective predation, in which juvenile mortality is high relative to adult mortality. We evaluated temperature differences, resource availability, and phylogenetic history as alternatives to the predation hypothesis. We conclude that lifehistory divergence among Utah chub populations is best explained by differences in predator-mediated mortality. This study is the first to evaluate effects of predation on life-history evolution in a long-lived prey species.