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.

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.

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.

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.

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.

An anthropogenic habitat within a suboptimal colonized ecosystem provides improved conditions for a range-shifting species.

Many species are shifting their ranges in response to the changing climate. In cases where such shifts lead to the colonization of a new ecosystem, it is critical to establish how the shifting species itself is impacted by novel environmental and biological interactions. Anthropogenic habitats that are analogous to the historic habitat of a shifting species may play a crucial role in the ability of that species to expand or persist in suboptimal colonized ecosystems. We tested if the anthropogenic habitat of docks, a likely mangrove analog, provides improved conditions for the range-shifting mangrove tree crab Aratus pisonii within the colonized suboptimal salt marsh ecosystem. To test if docks provided an improved habitat, we compared the impact of the salt marsh and dock habitats on ecological and life history traits that influence the ability of this species to persist and expand into the salt marsh and compared these back to baselines in the historic mangrove ecosystem. Specifically, we examined behavior, physiology, foraging, and the thermal conditions of A. pisonii in each habitat. We found that docks provide a more favorable thermal and foraging habitat than the surrounding salt marsh, while their ability to provide conditions which improved behavior and physiology was mixed. Our study shows that anthropogenic habitats can act as analogs to historic ecosystems and enhance the habitat quality for range-shifting species in colonized suboptimal ecosystems. If the patterns that we document are general across systems, then anthropogenic habitats may play an important facilitative role in the range shifts of species with continued climate change.

Indirect effects of ecosystem engineering combine with consumer behaviour to determine the spatial distribution of herbivory.

Ecosystem engineers alter environments by creating, modifying or destroying habitats. The indirect impacts of ecosystem engineering on trophic interactions should depend on the combination of the spatial distribution of engineered structures and the foraging behaviour of consumers that use these structures as refuges. In this study, we assessed the indirect effects of ecosystem engineering by a wood-boring beetle in a neotropical mangrove forest system. We identified herbivory patterns in a dwarf mangrove forest on the archipelago of Twin Cays, Belize. Past wood-boring activity impacted more than one-third of trees through the creation of tree holes that are now used, presumably as predation or thermal refuge, by the herbivorous mangrove tree crab Aratus pisonii. The presence of these refuges had a significant impact on plant-animal interactions; herbivory was more than fivefold higher on trees influenced by tree holes relative to those that were completely isolated from these refuges. Additionally, herbivory decreased exponentially with increasing distance from tree holes. We use individual-based simulation modelling to demonstrate that the creation of these herbivory patterns depends on a combination of the use of engineered tree holes for refuge by tree crabs, and the use of two behaviour patterns in this species-site fidelity to a "home tree," and more frequent foraging near their home tree. We demonstrate that understanding the spatial distribution of herbivory in this system depends on combining both the use of ecosystem engineering structures with individual behavioural patterns of herbivores.