Using external morphology as a proxy for stomach size in Hemigrapsus sanguineus.

Stomach morphology can provide insights into an organism's diet. Gut size or length is typically inversely related to diet quality in most taxa, and has been used to assess diet quality in a variety of systems. However, it requires animal sacrifice and time-consuming dissections. Measures of external morphology associated with diet may be a simpler, more cost-effective solution. At the species level, external measures of the progastric region of the carapace in brachyuran crabs can predict stomach size and diet quality, with some suggestion that this approach may also work to examine individual diet preferences and specialization at the individual level; if so, the size of the progastric region could be used to predict trends in diet quality and consumption for individuals, which would streamline diet studies in crabs. Here, we tested whether external progastric region size predicts internal stomach size across latitude and time of year for individuals of the invasive Asian shore crab Hemigrapsus sanguineus. We found that the width of the progastric region increased at a faster rate with body size than stomach width. In addition, the width of the progastric region followed different trends across sites and over time compared to stomach width. Our results therefore suggest that the progastric region may not be used as a proxy for stomach size variation across individuals.

Shift from income breeding to capital breeding with latitude in the invasive Asian shore crab Hemigrapsus sanguineus.

Organisms vary in the timing of energy acquisition and use for reproduction. Thus, breeding strategies exist on a continuum, from capital breeding to income breeding. Capital breeders acquire and store energy for breeding before the start of the reproductive season, while income breeders finance reproduction using energy acquired during the reproductive season. Latitude and its associated environmental drivers are expected to heavily influence breeding strategy, potentially leading to latitudinal variation in breeding strategies within a single species. We examined the breeding strategy of the Asian shore crab Hemigrapsus sanguineus at five sites spanning nearly 10° of latitude across its invaded United States range. We hypothesized that the primary breeding strategy of this species would shift from income breeding to capital breeding as latitude increases. We found that though this species' breeding strategy is dominated by capital breeding throughout much of the range, income breeding increases in importance at lower latitudes. This latitudinal pattern is likely heavily influenced by the duration of the foraging and breeding seasons, which also vary with latitude. We also found that reproductive characteristics at the northern and southern edges of the invaded range were consistent with continued range expansion. We suggest that the reproductive flexibility of the Asian shore crab is a key facilitator of its continued invasion success. Our results highlight the influence of latitude on the breeding strategy of a species and emphasize the need for further research regarding the ecological importance and implications of flexibility in breeding strategies within species.

Past energy allocation overwhelms current energy stresses in determining energy allocation trade-offs.

Regeneration of lost appendages is a gradual process in many species, spreading energetic costs of regeneration through time. Energy allocated to the regeneration of lost appendages cannot be used for other purposes and, therefore, commonly elicits energetic trade-offs in biological processes. We used limb loss in the Asian shore crab Hemigrapsus sanguineus to compare the strength of energetic trade-offs resulting from historic limb losses that have been partially regenerated versus current injuries that have not yet been repaired. Consistent with previous studies, we show that limb loss and regeneration results in trade-offs that reduce reproduction, energy storage, and growth. As may be expected, we show that trade-offs in these metrics from historic limb losses far outweigh trade-offs from current limb losses, and correlate directly with the degree of historic limb loss that has been regenerated. As regenerating limbs get closer to their normal size, these historical injuries get harder to detect, despite the continued allocation of additional resources to limb development. Our results demonstrate the importance of and a method for identifying historic appendage losses and of quantifying the amount of regeneration that has already occurred, as opposed to assessing only current injury, to accurately assess the strength of energetic trade-offs in animals recovering from nonlethal injury.

Differences in growth within and across the reproductive forms of northern crayfish (Faxonius virilis).

Complex life histories are frequently associated with biological trade-offs, as the use of one trait can decrease the performance of a second trait due to the need to balance competing demands to maximize fitness. Here, we examine growth patterns in invasive adult male northern crayfish (Faxonius virilis) that are indicative of a potential trade-off between energy allocation for body size versus chelae size growth. Northern crayfish undergo cyclic dimorphism, a process characterized by seasonal morphological changes associated with reproductive status. We measured carapace length and chelae length before and after molting and compared these growth increments between the four morphological transitions of the northern crayfish. Consistent with our predictions, reproductive crayfish molting to the non-reproductive form and non-reproductive crayfish molting within the non-reproductive form experienced a larger carapace length growth increment. Reproductive crayfish molting within the reproductive form and non-reproductive crayfish molting to the reproductive form, on the other hand, experienced a larger growth increment in chelae length. The results of this study support that cyclic dimorphism evolved as a strategy for optimizing energy allocation for body and chelae size growth during discrete periods of reproduction in crayfish with complex life histories.

Predicting diet in brachyuran crabs using external morphology.

Morphological traits have often been used to predict diet and trophic position of species across many animal groups. Variation in gut size of closely related animals is known to be a good predictor of dietary habits. Species that are more herbivorous or that persist on low-quality diets often have larger stomachs than their carnivorous counterparts. This same pattern exists in crabs and in most species, individuals exhibit external markings on the dorsal side of their carapace that appear to align with the position and size of their gut. We hypothesized that these external markings could be used as an accurate estimate of the crab's cardiac stomach size, allowing an approximation of crab dietary strategies without the need to sacrifice and dissect individual animals. We used literature values for mean diet and standardized external gut size markings taken from crab photographs across 50 species to show that percent herbivory in the diet increases non-linearly across species of brachyuran crab with the external estimate of gut size. We also used data from dissections in four species to show that external gut markings were positively correlated with gut sizes, though the strength of this correlation differed across species. We conclude that when rough approximations of diet quality such as percent herbivory will suffice, measuring external carapace markings in crabs presents a quick, free, non-lethal alternative to dissections. Our results also provide important insights into tradeoffs that occur in crab morphology and have implications for crab evolution.

Latitudinal and temporal variation in injury and its impacts in the invasive Asian shore crab Hemigrapsus sanguineus.

Nonlethal injury is a pervasive stress on individual animals that can affect large portions of a population at any given time. Yet most studies examine snapshots of injury at a single place and time, making the implicit assumption that the impacts of nonlethal injury are constant. We sampled Asian shore crabs Hemigrapsus sanguineus throughout their invasive North American range and from the spring through fall of 2020. We then documented the prevalence of limb loss over this space and time. We further examined the impacts of limb loss and limb regeneration on food consumption, growth, reproduction, and energy storage. We show that injury differed substantially across sites and was most common towards the southern part of their invaded range on the East Coast of North America. Injury also varied idiosyncratically across sites and through time. It also had strong impacts on individuals via reduced growth and reproduction, despite increased food consumption in injured crabs. Given the high prevalence of nonlethal injury in this species, these negative impacts of injury on individual animals likely scale up to influence population level processes (e.g., population growth), and may be one factor acting against the widespread success of this invader.

Metabolic rates of the Asian shore crab Hemigrapsus sanguineus in air as a function of body size, location, and injury.

Rapid warming in the Gulf of Maine may influence the success or invasiveness of the Asian shore crab, Hemigrapsus sanguineus. To better predict the effects of climate change on this invasive species, it is necessary to measure its energy dynamics under a range of conditions. However, previous research has only focused on the metabolism of this intertidal species in water. We sampled adult crabs from three different sites and measured their metabolic rates in the air. We show that metabolic rate increases with body mass and the number of missing limbs, but decreases with the number of regenerating limbs, possibly reflecting the timing of energy allocation to limb regeneration. Importantly, metabolic rates measured here in the air are ~4× higher than metabolic rates previously measured for this species in water. Our results provide baseline measurements of aerial metabolic rates across body sizes, which may be affected by climate change. With a better understanding of respiration in H. sanguineus, we can make more informed predictions about the combined effects of climate change and invasive species on the northeast coasts of North America.

Morphometric correlations between dietary and reproductive traits of two brachyuran crabs, Hemigrapsus sanguineus and Aratus pisonii.

Many animals have flexible morphological traits that allow them to succeed in differing circumstances with differing diets available to them. For brachyuran crabs, claw height and gut size are diet-specific and largely reflect foraging strategies, while abdomen width reflects relative levels of fecundity. However, the link between claw size and diet has largely been documented only for primarily carnivorous crabs, while the link between diet and fecundity is strong in herbivorous crabs. We sought to determine the nature of the intraspecific relationship between claw size, dietary habits, and fecundity for two primarily herbivorous crab species, Hemigrapsus sanguineus and Aratus pisonii. Specifically, we examined whether claw size and/or abdomen width can be used as reliable measures of individual diet strategy. To test these hypotheses, we collected crabs and measured the dimensions of their claws, abdomens, and guts. By comparing these dimensions for each individual, we found that strongly predictive relationships do not exist between these traits for the primarily herbivorous species in our study. Thus, identifying external morphological features that can be used to assess diets of primarily herbivorous crabs remains elusive.

Polymorphism promotes edge utilization by marsh crabs.

Understanding how habitat edges affect ecological processes is crucial given widespread and increasing modifications to natural landscapes. Resource specialization is a key factor affecting among-species edge responses, but we know little about how intraspecific resource use variation mediates edge utilization. Here, we integrate stomach content analysis, geometric morphometrics and feeding experiments to explore the role of resource polymorphism in mediating marsh crab (Panopeus obesus) foraging within the marsh-oyster reef boundary. Stomachs of edge individuals contained a greater proportion of morphologically defended edge prey (bivalves) compared to core marsh individuals, and edge individuals possessed relatively tall and robust claw morphology for manipulating such prey. We further show experimentally that phenotypic changes of edge P. obesus are associated with enhanced feeding efficiency on small, but not large edge prey. Morphological and ecological traits of edge P. obesus overlapped with the edge-occurring congener, P. herbstii, suggesting some degree of functional convergence despite the potential for interspecific competition within edges. Though this polymorphism is likely plastic, the success of P. obesus along edges could subsidize predator production within marshes and alter top-down pressure across mosaic estuarine landscapes. More generally, our study reveals polymorphism as a driver of edge utilization, while yielding new insight into the processes that maintain or erode spatial niche differentiation within predator guilds.

Metabolic rates in the squareback marsh crab Armases cinereum.

Metabolic rate is a basic individual metric that extends beyond the individual to link the ecology of populations, communities, and ecosystems via its role as a central component of energy budgets. Metabolic rates are often measured indirectly by quantifying respiration under simplified, standard laboratory conditions. This approach limits the application of these measurements to a small range of conditions that commonly do not reflect natural field conditions. We measured metabolic rates of the squareback marsh crab Armases cinereum under field conditions. Previous work highlights that movement of individual A. cinereum, especially females, provides a potential spatial subsidy of energy, as individuals consume foods in salt marshes and then transfer the resulting energy to upland forest ecosystems. We show that metabolic rate increases with size for both males and females and that metabolic rates are influenced by temperature and by whether females are vitellogenic. The metabolic rates that we measured more closely approximate field metabolic rates than standard metabolic rates and demonstrate that individual crabs experience high energy expenditures, reducing the amount of energy that may be transferred as a subsidy between marsh and forest as a result of the daily movements of individual crabs. Our measurements are therefore also a key component for the construction of an energy budget for this species.

Evidence for use of both capital and income breeding strategies in the mangrove tree crab, Aratus pisonii.

Two common strategies organisms use to finance reproduction are capital breeding (using energy stored prior to reproduction) and income breeding (using energy gathered during the reproductive period). Understanding which of these two strategies a species uses can help in predicting its population dynamics and how it will respond to environmental change. Brachyuran crabs have historically been considered capital breeders as a group, but recent evidence has challenged this assumption. Here, we focus on the mangrove tree crab, Aratus pisonii, and examine its breeding strategy on the Atlantic Florida coast. We collected crabs during and after their breeding season (March-October) and dissected them to discern how energy was stored and utilized for reproduction. We found patterns of reproduction and energy storage that are consistent with both the use of stored energy (capital) and energy acquired (income) during the breeding season. We also found that energy acquisition and storage patterns that supported reproduction were influenced by unequal tidal patterns associated with the syzygy tide inequality cycle. Contrary to previous assumptions for crabs, we suggest that species of crab that produce multiple clutches of eggs during long breeding seasons (many tropical and subtropical species) may commonly use income breeding strategies.

Mechanisms of possible self-limitation in the invasive Asian shore crab Hemigrapsus sanguineus.

Population sizes of invasive species are commonly characterized by boom-bust dynamics, and self-limitation via resource depletion is posited as one factor leading to these boom-bust changes in population size. Yet, while this phenomenon is well-documented in plants, few studies have demonstrated that self-limitation is possible for invasive animal species, especially those that are mobile. Here we examined the invasive Asian shore crab Hemigrapsus sanguineus, a species that reached very high abundances throughout invaded regions of North America, but has recently declined in many of these same regions. We examined the relationship between diet, energy storage, reproduction, and growth in crabs collected from the New Hampshire coast. We show that energy storage and reproduction both increase with diet quality, while growth declines with diet quality. These results suggest that self-limitation may be a contributing factor to the recent declines of H. sanguineus at sites where this invader was once much more abundant. Further, these results suggest a diet-associated tradeoff in energy allocation to different vital rates, with a focus on reproduction when high quality resources are consumed, and a focus instead on growth when poor quality resources are consumed.

The effects of animal personality on the ideal free distribution.

The ideal free distribution (IFD) has been used to predict the distribution of foraging animals in a wide variety of systems. However, its predictions do not always match observed distributions of foraging animals. Instead, we often observe that there are more consumers than predicted in low-quality patches and fewer consumers than predicted in high-quality patches (i.e. undermatching). We examine the possibility that animal personality is one explanation for this undermatching. We first conducted a literature search to determine how commonly studies document the personality distribution of populations. Second, we created a simple individual-based model to conceptually demonstrate why knowing the distribution of personalities is important for studies of populations of foragers in context of the IFD. Third, we present a specific example where we calculate the added time to reach the IFD for a population of mud crabs that has a considerable number of individuals with relatively inactive personalities. We suggest that animal personality, particularly the prevalence of inactive personality types, may inhibit the ability of a population to track changes in habitat quality, therefore leading to undermatching of the IFD. This may weaken the IFD as a predictive model moving forward.

An artificial habitat increases the reproductive fitness of a range-shifting species within a newly colonized ecosystem.

When a range-shifting species colonizes an ecosystem it has not previously inhabited, it may experience suboptimal conditions that challenge its continued persistence and expansion. Some impacts may be partially mitigated by artificial habitat analogues: artificial habitats that more closely resemble a species' historic ecosystem than the surrounding habitat. If conditions provided by such habitats increase reproductive success, they could be vital to the expansion and persistence of range-shifting species. We investigated the reproduction of the mangrove tree crab Aratus pisonii in its historic mangrove habitat, the suboptimal colonized salt marsh ecosystem, and on docks within the marsh, an artificial mangrove analogue. Crabs were assessed for offspring production and quality, as well as measures of maternal investment and egg quality. Aratus pisonii found on docks produced more eggs, more eggs per unit energy investment, and higher quality larvae than conspecifics in the surrounding salt marsh. Yet, crabs in the mangrove produced the highest quality larvae. Egg lipids suggest these different reproductive outcomes result from disparities in the quality of diet-driven maternal investments, particularly key fatty acids. This study suggests habitat analogues may increase the reproductive fitness of range-shifting species allowing more rapid expansion into, and better persistence in, colonized ecosystems.

An artificial habitat facilitates a climate-mediated range expansion into a suboptimal novel ecosystem.

As the geographic ranges of tropical species and ecosystems continue to shift poleward with climate change, it is critical to prediction and management to identify factors that facilitate these expansions. This is especially true for range shifts that involve the decoupling of a shifting species from its historic ecosystem and the colonization of an ecosystem that it has not previously inhabited (i.e. is novel to the shifting species). In cases where the colonized ecosystem is suboptimal for the shifting species, stepping stone refuges may play a critical role in facilitating further expansion. Here we document the facilitation of the northward range expansion of the mangrove tree crab (Aratus pisonii) into the previously uninhabited salt marsh ecosystem by artificial boat docks. While the cold tolerance of crabs did not differ between habitats, they were found on docks 36 km and 22 km further north than elsewhere in the salt marsh after the winters of 2016-'17 and '17-'18, respectively. This extended range-edge appears to be a result of docks within the salt marsh acting as a stepping stone refuge by providing this historically tropical species with a relatively warm thermal refuge during the winter that mitigates seasonal population die-backs exhibited elsewhere at the range-edge. Further, population abundances were higher on docks at the range-edge than in the surrounding salt marsh. While artificial habitats often favor the expansion of non-indigenous species, our results demonstrate the facilitation of a native species' range shift into a suboptimal ecosystem which it has not previously inhabited. The potential for analogous and refuge habitats, artificial or otherwise, to increase the rate and success of range shifts could be critical to the fate of many current and future range shifting species.

Burrowing behavior and burrowing energetics of a bioindicator under human disturbance.

Bioindicator species are extensively used for rapid assessment of ecological changes. Their use commonly focuses on changes in population abundance and individual sizes in response to environmental change. These numerical and demographic shifts likely have behavioral and physiological mechanistic drivers that, if understood, could provide additional insights into the use of these species as bioindicators of habitat health.The Atlantic ghost crab, Ocypode quadrata, is a global bioindicator species of human disturbance on sandy shores. Individual size and population abundance of O. quadrata decline dramatically at sites with human disturbance, and the causes of this phenomenon remain unclear.Here, we test the hypothesis that individual and population-level changes at disturbed sites reflect changes in burrowing behavior and energetics. Specifically, we examine whether or not the burrowing behavior (e.g., burrow fidelity and longevity) of O. quadrata changes because of human disturbance. We also examine energy required for burrowing by O. quadrata across different levels of human disturbance.We show that O. quadrata have the highest burrow fidelity and longevity at sites with low level of human impact, and weakest burrow fidelity and longevity at pristine sites. O. quadrata reduce the burrowing energy allocation by manipulating the burrow dimension and increasing the burrow longevity even under low levels of human disturbance.Overall, this study shows that human disturbances not only change the behavior of organisms, but also shift energetic balance. Our results support the use of a bioenergetic approach to better understand how human disturbances influence natural populations, and the specific use of this approach with this bioindicator species.

Reproductive skipping as an optimal life history strategy in the southern elephant seal, Mirounga leonina.

Intermittent breeding by which organisms skip some current reproductive opportunities in order to enhance future reproductive success is a common life history trade-off among long-lived, iteroparous species. The southern elephant seal Mirounga leonina engages in intermediate breeding when body condition is low. While it is anticipated that this strategy may increase the lifetime reproductive output of this species, the conditions under which reproductive skipping are predicted to occur are not clear. Here I develop a dynamic state variable model based on published data that examines when southern elephant seals are predicted to optimally skip reproduction in order to maximize lifetime reproductive output as a function of current body mass, maternal age, and survivorship. I demonstrate that the optimal reproductive strategy for this species can include reproductive skipping, and that the conditions where this is optimal depend on patterns of mass-dependent adult female survival. I further show that intermittent breeding can increase lifetime reproductive output, and that the magnitude of this benefit increases with the ability of individual animals to replenish depleted body mass through foraging. Finally, I show that when the environment is variable and foraging is reduced in bad years, the benefit of adopting an optimal strategy that includes reproductive skipping increases asymptotically with the frequency of bad years. These results highlight the importance of characterizing the pattern of adult survival in this species, as well as the need to identify other factors that may influence the prevalence and benefits of reproductive skipping.

Ecological and evolutionary implications of allometric growth in stomach size of brachyuran crabs.

Individual characteristics often scale allometrically with organismal body size and the form of this scaling can be influenced by ecological and evolutionary factors. Examining the specific form of this scaling can therefore yield important insights into organismal ecology and evolution and the ability of organisms to respond to future environmental changes. We examine the intraspecific allometric scaling of stomach volume with body mass for 17 species of brachyuran crabs. We also examine how this scaling is influenced by dietary strategy, maximum body size, and activity level, all while controlling for phylogenetic relationships between the species. We show that the slope and intercept of the allometric scaling relationships vary across species and are influenced by all three ecological factors examined here, as well as by evolutionary relationships. These results highlight potential divergent strategies in stomach growth taken by different groups of crabs and highlight potential limitations that may be imposed on the ability of this group of organisms to respond to warming trends expected with climate change.

Personality interacts with habitat quality to govern individual mortality and dispersal patterns.

Individual phenotypic differences are increasingly recognized as key drivers of ecological processes. However, studies examining the relative importance of these differences in comparison with environmental factors or how individual phenotype interacts across different environmental contexts remain lacking. We performed two field experiments to assess the concurrent roles of personality differences and habitat quality in mediating individual mortality and dispersal. We quantified the predator avoidance response of mud crabs, Panopeus herbstii, collected from low- and high-quality oyster reefs and measured crab loss in a caging experiment. We simultaneously measured the distance crabs traveled as well as the stability of personalities across reef quality in a separate reciprocal transplant experiment. Habitat quality was the primary determinant of crab loss, although the distance crabs traveled was governed by personality which interacted with habitat quality to control the fate of crabs. Here, crabs on low-quality reefs rapidly emigrated, starting with the boldest individuals, and experienced modest levels of predation regardless of personality. In contrast, both bold and shy crabs would remain on high-quality reefs for months where bolder individuals experienced higher predation risk. These findings suggest that personalities could produce vastly different population dynamics across habitat quality and govern community responses to habitat degradation.

The timing of energy allocation to reproduction in an important group of marine consumers.

Organisms may energetically finance reproductive effort using energy stored prior to the reproductive period (termed capital breeders) or using energy acquired during the reproductive period (termed income breeders). The specific strategy used has implications for population dynamics as well as for the response to environmental variation. Crabs and other crustaceans have generally been assumed to be capital breeders. Here I demonstrate an experimental procedure used to determine whether crabs are capable of using an income breeding strategy. I then examine data from several published studies from a range of crab species across a broad phylogenetic spectrum that conducted similar experiments to look for evidence of income breeding strategy. I show that income breeding does occur in crabs, but that it appears to be taxon-specific. In particular, I show that income breeding occurs in two species from the family Portunidae, but fail to find evidence for income breeding in other taxa examined. This finding has a range of implications for this ecologically and economically important group of consumers, including implications for their response to human-induced environmental change, their response to fishing pressure, and best practices for aquaculture. The implications of breeding strategy in crabs likely depends on phylogeny (morphology) and ecology, both of which influence the space available for energy storage inside the carapace.