Early life sensory ability—ventilatory responses of thornback ray embryos (Raja clavata) to predator-type electric fields

Predator avoidance is fundamental for survival and it can be particularly challenging for prey animals if physical movement away from a predatory threat is restricted. Many sharks and rays begin life within an egg capsule that is attached to the sea bed. The vulnerability of this sedentary life stage is exacerbated in skates (Rajidae) as the compulsory ventilatory activity of embryos makes them conspicuous to potential predators. Embryos can reduce this risk by mediating ventilatory activity if they detect the presence of a predator using an acute electrosense. To determine how early in embryonic life predator elicited behavioral responses can occur, the reactions of three different age groups (1/3 developed, 2/3 developed, and near hatching) of embryonic thornback rays Raja clavata were tested using predator-type electric field stimuli. Egg capsules were exposed to continuous or intermittent stimuli in order to assess varying predator-type encounter scenarios on the ventilatory behavior of different developmental stages. All embryos reacted with a “freeze response” following initial electric field (E-field) exposure, ceasing ventilatory behavior in response to predator presence, demonstrating electroreceptive functionality for the first time at the earliest possible stage in ontogeny. This ability coincided with the onset of egg ventilatory behavior and may represent an effective means to enhance survival. A continuous application of stimuli over time revealed that embryos can adapt their behavior and resume normal activity, whereas when presented intermittently, the E-field resulted in a significant reduction in overall ventilatory activity across all ages. Recovery from stimuli was significantly quicker in older embryos, potentially indicative of the trade-off between avoiding predation and adequate respiration. © 2015 Wiley Periodicals, Inc. Develop Neurobiol 76: 721–729, 201

Intraguild processes drive space‐use patterns in a large‐bodied marine predator community

ACKNOWLEDGEMENTS We dedicate this paper to the memory of Samuel (‘Doc’) Gruber who passed away before the completion of this manuscript. This work was supported by the Bimini Biological Field Station Foundation staff and volunteers, and funded by Save Our Seas Foundation, Swiss Shark Foundation (Hai Stiftung) and Guy Harvey Ocean Foundation. We are grateful for the unwavering support provided by Bimini Scuba Center. We thank Volker Grimm, A. Bradley Duthie and an anonymous reviewer for their constructive feedback on earlier versions of the manuscript. This is publication # 1708 from the Institute of Environment at Florida International University.Peer reviewe

Bridging disciplines to advance elasmobranch conservation: applications of physiological ecology

A strength of physiological ecology is its incorporation of aspects of both species\u27 ecology and physiology; this holistic approach is needed to address current and future anthropogenic stressors affecting elasmobranch fishes that range from overexploitation to the effects of climate change. For example, physiology is one of several key determinants of an organism\u27s ecological niche (along with evolutionary constraints and ecological interactions). The fundamental role of physiology in niche determination led to the development of the field of physiological ecology. This approach considers physiological mechanisms in the context of the environment to understand mechanistic variations that beget ecological trends. Physiological ecology, as an integrative discipline, has recently experienced a resurgence with respect to conservation applications, largely in conjunction with technological advances that extended physiological work from the lab into the natural world. This is of critical importance for species such as elasmobranchs (sharks, skates and rays), which are an especially understudied and threatened group of vertebrates. In 2017, at the American Elasmobranch Society meeting in Austin, Texas, the symposium entitled \u27Applications of Physiological Ecology in Elasmobranch Research\u27 provided a platform for researchers to showcase work in which ecological questions were examined through a physiological lens. Here, we highlight the research presented at this symposium, which emphasized the strength of linking physiological tools with ecological questions. We also demonstrate the applicability of using physiological ecology research as a method to approach conservation issues, and advocate for a more available framework whereby results are more easily accessible for their implementation into management practices

Development of a novel environmental DNA (eDNA) tool for monitoring Vulnerable Freckled Guitarfish, Pseudobatos lentiginosus, in the Western Central Atlantic

Rhino-rays are the most threatened group of elasmobranchs, having experienced widespread declines due to mortalities in fisheries and habitat degradation. Within the Western Central Atlantic, there are two extant species of Rhino-rays, the Critically Endangered Smalltooth Sawfish, Pristis pectinata, and the Vulnerable Freckled Guitarfish, Pseudobatos lentiginosus. Although there is research committed to P. pectinata in this region, less is known about the distribution status of P. lentiginosus. Over the past 50 years, P. lentiginosus have undergone a presumed range contraction in U.S. waters; once found from North Carolina to Texas, and historically common in the north central Gulf of Mexico, they are now only abundant in Florida. Their occurrence in the north-central Gulf of Mexico remains uncertain, and they have not been sighted in the Mississippi Sound in 15 years. Therefore, a highly sensitive, species-specific Droplet Digital™ PCR environmental DNA (eDNA) assay was designed to detect the presence of this species, targeting a 174 base pair portion of the mitochondrial 16S rRNA gene. The assay detects DNA from only P. lentiginosus, and not from other co-occurring closely related species. This tool can be used in future eDNA surveys across the northern Gulf of Mexico and Western Central Atlantic to inform the current distribution of this threatened species and implement conservation action

Morphology and distribution of taste papillae and oral denticles in the developing oropharyngeal cavity of the bamboo shark, Chiloscyllium punctatum.

Gustation in sharks is not well understood, especially within species that ingest food items using suction. This study examines the morphological and immunohistochemical characterisation of taste papillae and oral denticles in the oropharynx of the brown-banded bamboo shark Chiloscyllium punctatum and compares their distribution during development. Taste papillae of the brown-banded bamboo shark Chiloscyllium punctatum are located throughout the oropharyngeal region and are most concentrated on the oral valves (2,125-3,483 per cm(2) in embryos; 89-111 per cm(2) in mature adults) close to the tooth territories. Papillae appearance is comparable at all stages of development, with the exception of the embryos (unhatched specimens), where no microvilli are present. Oral valve papillae are comparable in structure to Type I taste buds of teleost fishes, whereas those of the rest of the oropharyngeal region are comparable to Type II. Both types of papillae show immunofluorescence for a number of markers of taste buds, including β-Catenin and Sox2. Taste papillae densities are highest in embryos with 420-941 per cm(2) compared to 8-29 per cm(2) in mature adults. The total number of papillae remains around 1,900 for all stages of development. However, the papillae increase in diameter from 72±1 µm in embryos to 310±7 µm in mature individuals. Microvilli protrude in multiple patches at the apical tip of the papilla covering ∼0.5% of the papillar surface area. We further document the relationship between taste papillae and the closely associated oral denticles within the shark orophayngeal cavity. Oral denticles first break through the epithelium in the antero-central region of the dorsal oral cavity, shortly after the emergence of teeth, around time of hatching. Denticles are located throughout the oropharyngeal epithelium of both immature and mature stages, with the highest concentrations in the antero-dorsal oral cavity and the central regions of the pharynx. These denticle-rich areas of the mouth and pharynx are therefore thought to protect the epithelium, and importantly the taste papillae, from abrasion since they correlate with regions where potential food items are processed or masticated for consumption. Taste papillae and denticles are more dense in anterior oropharyngeal regions in close association with the oral jaws and teeth, and in the juvenile/hatchling shark taste units are functional, and innervated, allowing the shark to seek out food in utero, at birth or on emergence from the egg case

Environmental associations of cownose ray (Rhinoptera bonasus) seasonal presence along the U.S. Atlantic Coast

Identifying the mechanistic drivers of migration can be crucial in shaping conservation and management policies. The cownose ray (Rhinoptera bonasus) is a relatively poorly understood elasmobranch species that occurs along the U.S. Atlantic coast and undergoes large-scale seasonal migrations. To better understand the drivers and timing of cownose ray seasonal migration in order to inform potential management measures, we analyzed telemetry detections of 51 mature cownose rays (38 female, 13 male) tagged with acoustic transmitters in the Maryland and Virginia portions of Chesapeake Bay. Detections within their summer habitat in Chesapeake Bay and winter habitat in the vicinity of Cape Canaveral, Florida, were matched with publicly available sea surface temperature (SST) data recorded by data buoys near the areas of tag detections and with local photoperiod and day of year. These variables were used in boosted regression tree models of ray presence (all rays combined, females only, and males only) in each seasonal habitat. Models were developed for presence during the entire summer and winter season, and for the time periods of arrival and departure from both summer and winter habitats. Seasonal presence in both summer and winter habitats was associated with distinct temperature, photoperiod, and date ranges, with temperature as the most influential variable in seasonal models. In models of arrival and departure periods, southward migration (departure from Chesapeake Bay and arrival off Cape Canaveral) was strongly associated with SST for all rays and arrival in the Chesapeake Bay region after northward migration was most strongly associated with day of year. The most influential variable during the period of northward departure from Cape Canaveral differed between males (day of year) and females (SST). This suggests that mature female northward migration may be driven by temperature while male northward migration may be driven by endogenous cues. These findings provide detailed information on the timing of cownose ray arrival at, presence in, and departure from seasonal habitats and provide potential justification for including the species in cross-taxa comparative studies on migratory behavior

Breadth of the Wild: Global Patterns in Elasmobranch Dietary Niche Breadth

A widely recognized pattern in ecology is the latitudinal diversity gradient: increasing biodiversity with decreasing latitude. The latitude niche-breadth hypothesis states that the stable climate of the tropics allows for increased specialization (smaller niche), promoting greater biodiversity in the available niche space. The highly dynamic climate of the poles drives the evolution of generalists (larger niche), limiting biodiversity. While the fundamental question of “what drives species richness?” on land remains debated, it is even less understood in the marine environment. Elasmobranchs (sharks, skates, and rays) are a data-rich, globally distributed group that occupy an array of functional roles, inhabiting coastal to open ocean habitats from the poles to the tropics. In this thesis, I use a global-scale stomach contents dataset to calculate standardized Levin’s niche breadth for 237 populations of 85 elasmobranch species in order to examine spatial patterns in niche breadth. I find that niche breadth varies widely across all functional, taxonomic, and regional groups, highlighting the diversity and potential resiliency of this clade. Niche breadth of elasmobranchs does not follow a latitudinal gradient. Instead, niche varies with depth, with niche breadth generally increasing with increasing depth. This depth gradient is strongest in bottom-dwelling elasmobranchs with smaller range sizes and weakest in wide-ranging pelagic elasmobranchs. This pattern suggests that for species with limited mobility, specialization may mediate coexistence in highly biodiverse areas with elevated competition. Why this pattern applies in a depth, but not latitudinal, gradient remains unclear

The interaction between resource species and electromagnetic fields associated with electricity production by offshore wind farms

As offshore wind energy production increases, the number of subsea cables will proliferate along with associated electromagnetic field (EMF) emissions. Understanding how EMF interactions (a potential pressure) affect resource species (receptor) requires an improved knowledge base to aid management decisions. Within the framework of a potential effect on a receptor, we review key aspects of assessing EMF exposure. From the vantage point of the receptor species, we consider how their perception of EMF varies through time as a consequence of species’ sensory biology, life history theory, and movement ecology. We review known effects of EMFs on species and consider EMF interactions with benthic, bentho-pelagic, and migratory species, focusing on functional roles of electro- and magneto-reception at different life stages. We must move our understanding from individual effects to population-level impacts. The present knowledge base has been drawn from a diverse range of laboratory and field approaches, which can be better integrated to address gaps and reach the desired knowledge base. Improving models of future scenarios depends on taking a more systematic and consistent approach to measuring and modeling alternating current and direct current EMFs and accounting for cable properties and local environmental characteristics. We make recommendations to help decipher receptor species’ responses. Acquiring such knowledge will enable us to translate EMFs, and their effects and encounter rates, into impact assessments for resource species to inform appropriate management.Publisher PDFPeer reviewe

Perception & Use of Magnetic Field Information in Navigation Behaviors in Elasmobranch Fishes.

Ph.D. Thesis. University of Hawaiʻi at Mānoa 2018