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      Vertical Movements and Patterns in Diving Behavior of Whale Sharks as Revealed by Pop-Up Satellite Tags in the Eastern Gulf of Mexico

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          Abstract

          The whale shark ( Rhincodon typus) is a wide-ranging, filter-feeding species typically observed at or near the surface. This shark’s sub-surface habits and behaviors have only begun to be revealed in recent years through the use of archival and satellite tagging technology. We attached pop-up satellite archival transmitting tags to 35 whale sharks in the southeastern Gulf of Mexico off the Yucatan Peninsula from 2003–2012 and three tags to whale sharks in the northeastern Gulf off Florida in 2010, to examine these sharks’ long-term movement patterns and gain insight into the underlying factors influencing their vertical habitat selection. Archived data were received from 31 tags deployed on sharks of both sexes with total lengths of 5.5–9 m. Nine of these tags were physically recovered facilitating a detailed long-term view into the sharks’ vertical movements. Whale sharks feeding inshore on fish eggs off the northeast Yucatan Peninsula demonstrated reverse diel vertical migration, with extended periods of surface swimming beginning at sunrise followed by an abrupt change in the mid-afternoon to regular vertical oscillations, a pattern that continued overnight. When in oceanic waters, sharks spent about 95% of their time within epipelagic depths (<200 m) but regularly undertook very deep (“extreme”) dives (>500 m) that largely occurred during daytime or twilight hours (max. depth recorded 1,928 m), had V-shaped depth-time profiles, and comprised more rapid descents (0.68 m sec -1) than ascents (0.50 m sec -1). Nearly half of these extreme dives had descent profiles with brief but conspicuous changes in vertical direction at a mean depth of 475 m. We hypothesize these stutter steps represent foraging events within the deep scattering layer, however, the extreme dives may have additional functions. Overall, our results demonstrate complex and dynamic patterns of habitat utilization for R. typus that appear to be in response to changing biotic and abiotic conditions influencing the distribution and abundance of their prey.

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          Feeding anatomy, filter-feeding rate, and diet of whale sharks Rhincodon typus during surface ram filter feeding off the Yucatan Peninsula, Mexico.

          The feeding anatomy, behavior and diet of the whale shark Rhincodon typus were studied off Cabo Catoche, Yucatan Peninsula, Mexico. The filtering apparatus is composed of 20 unique filtering pads that completely occlude the pharyngeal cavity. A reticulated mesh lies on the proximal surface of the pads, with openings averaging 1.2mm in diameter. Superficial to this, a series of primary and secondary cartilaginous vanes support the pads and direct the water across the primary gill filaments. During surface ram filter feeding, sharks swam at an average velocity of 1.1m/s with 85% of the open mouth below the water's surface. Sharks on average spent approximately 7.5h/day feeding at the surface on dense plankton dominated by sergestids, calanoid copepods, chaetognaths and fish larvae. Based on calculated flow speed and underwater mouth area, it was estimated that a whale shark of 443 cm total length (TL) filters 326 m(3)/h, and a 622 cm TL shark 614 m(3)/h. With an average plankton biomass of 4.5 g/m(3) at the feeding site, the two sizes of sharks on average would ingest 1467 and 2763 g of plankton per hour, and their daily ration would be approximately 14,931 and 28,121 kJ, respectively. These values are consistent with independently derived feeding rations of captive, growing whale sharks in an aquarium. A feeding mechanism utilizing cross-flow filtration of plankton is described, allowing the sharks to ingest plankton that is smaller than the mesh while reducing clogging of the filtering apparatus. Copyright © 2010 Elsevier GmbH. All rights reserved.
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            Extreme diving behaviour in devil rays links surface waters and the deep ocean

            Many marine predators dive regularly to forage on pelagic fish and squid populations in the deep ocean. Often concentrated in deep scattering layers (DSLs), these prey populations represent a significant, albeit largely unquantified, fraction of the earth’s aquatic biomass1. Large fish and mammals typically target prey within DSLs either by making repetitive feeding dives to mesopelagic depths of 400–800 m, or by following the same patterns of diel vertical migrations as those undertaken by many mesopelagic organisms2 3. Sperm whales (Physeter macrocephalis), for instance, regularly dive to mesopelagic depths where they are hypothesized to consume a biomass of squid equivalent to global marine landings on an annual basis4. Yet, very few species have been observed diving consistently beyond the mesopelagic into the bathypelagic zone, presumably because of physiological or energetic constraints that limit an animal’s ability to forage efficiently in environments characterized by high pressures, low temperatures and low levels of dissolved oxygen that are typically found at depths below 1,000 m. These constraints may prevent at least some ocean predators from accessing significant food resources in open oceans where maximum prey biomass can be located 1,000–2,500 m deep5. Deep-diving behaviour in marine fishes is often associated with physiological thermoregulatory capabilities that allow for the generation and retention of heat in critical tissues. Indeed, the convergent evolution of cranial endothermy in lamnid sharks and scombroid fishes suggests that the maintenance of brain activity and visual acuity in deep, cold waters has conveyed significant selective advantages to these groups over time6. While most endothermic fishes are apex predators, cranial endothermy has also been identified in several species of myliobatoid rays. For instance, several species of devil rays in the family Mobulidae possess well-developed retia mirabilia around the cranial cavity7. The presence of a heat-exchange system in these species was perplexing as mobulids were thought to be surface-dwelling filter feeders inhabiting warm temperate to tropical epipelagic waters. The authors concluded that the cranial rete cooled rather than warmed the brain as these rays were known to bask at the surface in tropical waters. More recent examinations8 9 concluded that the retia in Mobula tarapacana and Manta birostris likely did act to warm the brain, although it was not clear what benefit the counter-current system provided for species that apparently did not encounter cold water. The difficulty assigning a function to retia mirabilia found in M. tarapacana highlights a lack of basic ecological information for pelagic mobulid rays. While members of the genus Mobula occur throughout tropical and warm-temperate oceans, we know little about horizontal or vertical movement patterns for any species. Two recent studies deployed satellite tags on Mobula japonica in the eastern north Pacific10 and Mobula mobular in the Mediterranean Sea11. Tag data in both instances revealed relatively small horizontal and vertical movements in waters where temperatures were largely constrained between 20 and 30 °C. Neither study, therefore, provided information that might explain the presence of a counter-current heat exchange system in the genus. Here we report horizontal and vertical movements of M. tarapacana in the central North Atlantic Ocean. The results confirm that this species of devil ray is capable of traversing large distances through the oligotrophic open ocean. The data also document remarkable diving behaviour with maximum depths attained in excess of 1,800 m. This behaviour provides a plausible evolutionary explanation for the morphological specializations that allow M. tarapacana and potentially other large pelagic rays to tolerate cold water, and highlights potential ecological connections between surface waters and meso- and bathypelagic communities in the open ocean. Results Horizontal and vertical movements Chilean devil rays moved considerable distances through oligotrophic temperate, subtropical and tropical waters of the central North Atlantic Ocean. All four rays tagged in 2011 moved due south, with straight-line distances between tag deployments at Princess Alice seamount and tag pop-up locations ranging from 2,500 to 3,800 km, and average minimum swimming speeds (straight-line distance between tag deployment and pop-up locations divided by deployment duration) ranging from 24 to 44 km d−1 (Fig. 1a). Rays tagged in 2012 moved straight-line distances ranging from 57 to 3,182 km from the tagging location, with average minimum swimming velocities ranging between 4 and 49 km d−1 (Fig. 1). Depth and temperature profiles collected in 2011 and 2012 revealed behaviours that differ significantly from the findings of earlier Mobula studies. Daily depth and temperature data showed that individuals tagged in 2011 dove to maximum depths ranging from 1,736 to 1,896 m with corresponding minimum water temperatures between 3.6 and 4.4 °C (Fig. 2). Moreover, tagged individuals were regularly travelling to bathypelagic depths, with one individual diving below 800 m on one-third of the 80 days after tag deployment, and below 1,400 m on six consecutive days during this period (Fig. 2a). We observed similar deep-diving behaviour in nine rays tagged in 2012, with daily maximum depths and minimum temperatures between 416 and 1,848 m, and 4.2 and 12.8 °C, respectively. The only individuals (n=3) that did not dive below 800 m had premature tag releases after less than 25 days of deployment (Table 1). Overall, tagged rays spent an average of 4.9% of their time at mesopelagic depths (range 0–15.3%), and 0.5% of their time at bathypelagic depths (range 0–3.8%). Dive profiles We identified a total of 49 dive profiles with maximum depths of at least 800 m, beyond the vertical extent of oxygen minimum layers in the tropical and subtropical North Atlantic12. These dives generally followed one of two distinct patterns (Fig. 3). The most common profile involved descent to the maximum depth followed by a slower, stepwise return to the surface with a total dive time of 60 to 90 min (Fig. 4). Tagged rays generally only made one such dive during a 24-h period, although on two occasions an individual produced two deep dives with surface intervals of 800 m) with all other times when the rays were not exhibiting deep-dive behaviour (Fig. 6). During daylight hours, when basking at the surface would presumably result in elevated body temperatures, devil rays spent consistently more time between 0 and 2 m for up to 1 h before and 1 h after a deep dive (59% and 73% of the time, respectively) than during non-diving intervals when they were at the surface 21% of the time. However, during nighttime hours this pattern changed markedly and we found little difference in patterns of surface residency before (21.4%) or after (27%) a deep dive compared with all other times (29.6%) when the rays were not diving beyond 800 m. Discussion Satellite archival tagging results from the central North Atlantic revealed that M. tarapacana is a truly oceanic species capable of traversing long distances through oligotrophic tropical and subtropical waters. All tagged rays remained in oceanic environments throughout the deployments, and it is clear that M. tarapacana is capable of rapid, long-distance migrations throughout the Atlantic Ocean. Our results are in contrast with data from PSAT deployments on Mobula japonica in the eastern Pacific10 and Mobula mobular in the Mediterranean Sea11. Horizontal movements by devil rays in both these studies were much more limited than those we observed. Most of the rays tagged in our study also frequently dived to depths of at least 1,500 m and were consistently encountering ambient water temperatures 800 m that both initiated and terminated at depths <50 m. We only used dives with full descent and ascent profiles when calculating summary dive statistics. Ethics statement This study was performed according to national Portuguese laws for the use of vertebrates in research, and the work and tagging protocol approved by the Azorean Directorate of Sea Affairs of the Azores Autonomous region (DRAM/SRRN ref. 24/2010). Author contributions S.R.T., P.A. and J.F. devised the study, conducted the research and drafted the paper. G.B.S., M.L.B. and R.S.S. provided funding for the research, and contributed to the experimental design and manuscript preparation. C.D.B. and S.R.T. analysed the data and C.D.B. produced the figures. Additional information How to cite this article: Thorrold, S. R. et al. Extreme diving behaviour in devil rays links surface waters and the deep ocean. Nat. Commun. 5:4274 doi: 10.1038/ncomms5274 (2014).
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              An Unprecedented Aggregation of Whale Sharks, Rhincodon typus, in Mexican Coastal Waters of the Caribbean Sea

              Whale sharks, Rhincodon typus, are often perceived as solitary behemoths that live and feed in the open ocean. To the contrary, evidence is accumulating that they are gregarious and form seasonal aggregations in some coastal waters. One such aggregation occurs annually north of Cabo Catoche, off Isla Holbox on the Yucatán Peninsula of Mexico. Here we report a second, much denser aggregation of whale sharks (dubbed “the Afuera”) that occurs east of the tip of the Yucatán Peninsula in the Caribbean Sea. The 2009 Afuera event comprised the largest aggregation of whale sharks ever reported, with up to 420 whale sharks observed in a single aerial survey, all gathered in an elliptical patch of ocean approximately 18 km2. Plankton studies indicated that the sharks were feeding on dense homogenous patches of fish eggs, which DNA barcoding analysis identified as belonging to little tunny, Euthynnus alletteratus. This contrasts with the annual Cabo Catoche aggregation nearby, where prey consists mostly of copepods and sergestid shrimp. Increased sightings at the Afuera coincide with decreased sightings at Cabo Catoche, and both groups have the same sex ratio, implying that the same animals are likely involved in both aggregations; tagging data support this idea. With two whale shark aggregation areas, high coastal productivity and a previously-unknown scombrid spawning ground, the northeastern Yucatán marine region is a critical habitat that deserves more concerted conservation efforts.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                18 November 2015
                2015
                : 10
                : 11
                : e0142156
                Affiliations
                [1 ]Center for Shark Research, Mote Marine Laboratory, Sarasota, Florida, United States of America
                [2 ]Ch'ooj Ajauil AC, Cancún, Quintana Roo, México
                [3 ]Proyecto Dominó, Comisión Nacional de Áreas Naturales Protegidas, Cancún, Quintana Roo, México
                Griffith University, AUSTRALIA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: JPT RdlPV JGC REH. Performed the experiments: JPT RdlPV JGC REH. Analyzed the data: JPT. Contributed reagents/materials/analysis tools: JPT RdlPV JGC REH. Wrote the paper: JPT REH.

                Article
                PONE-D-15-32426
                10.1371/journal.pone.0142156
                4651344
                26580405
                3a8eb719-824f-4271-b106-7d46ba3f6da6
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 23 July 2015
                : 18 October 2015
                Page count
                Figures: 11, Tables: 2, Pages: 25
                Funding
                This research was supported by funding from Georgia Aquarium ( www.georgiaaquarium.org), Christopher Reynolds Foundation ( www.creynolds.org), National Geographic Society ( www.ngs.org), Mote Marine Laboratory ( www.mote.org) and an anonymous private foundation. The Natural Protected Areas National Commission of Mexico (SEMARNAT/CONANP) provided personnel, biological station facilities, boats, fuel and conventional tags during the early stages of the work (2003-2009). Those stages also were supported in part by a Mexico Small Grants Program funded by the UNDP/Global Environment Facility, as provided by the Mexican NGO SER de Quintana Roo A.C. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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