Spatial separation without territoriality in shark communities

Spatial separation within predator communities can arise via territoriality but also from competitive interactions among and within species. However, linking competitive interactions to predator distribution patterns is difficult and theoretical models predict different habitat selection patterns dependent on habitat quality and how competition manifests itself. While models generally consider competitors to be either equal in ability, or for one phenotype to have a fixed advantage over the other, few studies consider that an animal may only have a competitive advantage in specific habitats. We used  10 years of telemetry data, habitat surveys and behavioral experiments, to show spatial partitioning between and within two species of reef shark (grey reef Carcharhinus amblyrhinchos and blacktip reef sharks C. melanopterus) at an unfished Pacific atoll. Within a species, sharks remained within small ‘sub‐habitats’ with very few movements of individuals between sub‐habitats, which previous models have suggested could be caused by intra‐specific competition. Blacktip reef sharks were more broadly distributed across habitat types but a greater proportion used lagoon and backreef habitats, while grey reef sharks preferred forereef habitats. Grey reef sharks at a nearby atoll where blacktip reef sharks are absent, were distributed more broadly between habitat types than when both species were present. A series of individual‐based models predict that habitat separation would only arise if there are competitive interactions between species that are habitat‐specific, with grey reefs having a competitive advantage on the forereefs and blacktips in the lagoons and backreef. We provide compelling evidence that competition helps drive distribution patterns and spatial separation of a marine predator community, and highlight that competitive advantages may not be constant but rather dependent on habitats.     

Acoustic accelerometry reveals diel activity patterns in premigratory Port Jackson sharks

Distinguishing the factors that influence activity within a species advances understanding of their behavior and ecology. Continuous observation in the marine environment is not feasible but biotelemetry devices provide an opportunity for detailed analysis of movements and activity patterns. This study investigated the detail that calibration of accelerometers measuring root mean square (RMS) acceleration with video footage can add to understanding the activity patterns of male and female Port Jackson sharks (Heterodontus portusjacksoni) in a captive environment. Linear regression was used to relate RMS acceleration output to time‐matched behavior captured on video to quantify diel activity patterns. To validate captive data, diel patterns from captive sharks were compared with diel movement data from free‐ranging sharks using passive acoustic tracking. The RMS acceleration data showed captive sharks exhibited nocturnal diel patterns peaking during the late evening before midnight and decreasing before sunrise. Correlation analysis revealed that captive animals displayed similar activity patterns to free‐ranging sharks. The timing of wild shark departures for migration in the late breeding season corresponded with elevated diel activity at night within the captive individuals, suggesting a form of migratory restlessness in captivity. By directly relating RMS acceleration output to activity level, we show that sex, time of day, and sex‐specific seasonal behavior all influenced activity levels. This study contributes to a growing body of evidence that RMS acceleration data are a promising method to determine activity patterns of cryptic marine animals and can provide more detailed information when validated in captivity.     

Trophic ecology of reef sharks determined using stable isotopes and telemetry

Establishing the ecological role of predators within an ecosystem is central to understanding community dynamics and is useful in designing effective management and conservation strategies. We analysed differences in the trophic ecology of four species of reef sharks (Carcharhinus melanopterus, Carcharhinus amblyrhynchos, Triaenodon obesus and Negaprion acutidens) at Ningaloo Reef, Western Australia, by analysing tissue stable isotopes (δ¹⁵N and δ¹³C). We also monitored animals using acoustic telemetry to determine long-term residency patterns in a bay at the southern end of the reef, Coral Bay. Overall, mean δ¹³C was similar among species, ranging between −10.9 and −11.8‰, suggesting a food-web dependency on coastal producers. Classification and regression tree analysis identified an effect of species on δ¹⁵N that separated C. amblyrhynchos and C. melanopterus from N. acutidens and T. obesus. For C. amblyrhynchos and C. melanopterus, animals were also divided by size classes, with smaller sharks having lower average δ¹⁵N than larger animals; this suggests that δ¹⁵N increases with size for these two species. Juvenile C. melanopterus, juvenile N. acutidens and adult T. obesus had trophic levels of 3.7, for juvenile C. amblyrhynchos and adult C. melanopterus it was 4, and adult C. amblyrhynchos had a value of 4.3. Trophic-level estimates for C. melanopterus and C. amblyrhynchos corroborate previous conclusions based on diet studies. We found no evidence for a difference in isotopic composition between resident and non-resident sharks. The lack of variation in isotopic composition was consistent with high mean residency of these species recorded using acoustic telemetry, which was 79% (±0.09 SE) of days monitored for T. obesus, followed by N. acutidens (57 ± 19.55%), C. amblyrhynchos (54 ± 13%) and C. melanopterus (33 ± 8.28%). High δ¹³C composition in reef sharks and long-term residency behaviour suggest that coastal marine reserves might provide effective conservation refuges for some species.     

Spatial and temporal analysis of juvenile blacktip reef shark (Carcharhinus melanopterus) demographies identifies critical habitats

Reef shark species have undergone sharp declines in recent decades, as they inhabit coastal areas, making them an easy target in fisheries (i.e., sharks are exploited globally for their fins, meat, and liver oil) and exposing them to other threats (e.g., being part of by-catch, pollution, and climate change). Reef sharks play a critical role in coral reef ecosystems, where they control populations of smaller predators and herbivorous fishes either directly via predation or indirectly via behavior, thus protecting biodiversity and preventing potential overgrazing of corals. The urgent need to conserve reef shark populations necessitates a multifaceted approach to policy at local, federal, and global levels. However, monitoring programmes to evaluate the efficiency of such policies are lacking due to the difficulty in repeatedly sampling free-ranging, wild shark populations. Over nine consecutive years, we monitored juveniles of the blacktip reef shark (Carcharhinus melanopterus) population around Moorea, French Polynesia, and within the largest shark sanctuary globally, to date. We investigated the roles of spatial (i.e., sampling sites) and temporal variables (i.e., sampling year, season, and month), water temperature, and interspecific competition on shark density across 10 coastal nursery areas. Juvenile C. melanopterus density was found to be stable over 9 years, which may highlight the effectiveness of local and likely federal policies. Two of the 10 nursery areas exhibited higher juvenile shark densities over time, which may have been related to changes in female reproductive behavior or changes in habitat type and resources. Water temperatures did not affect juvenile shark density over time as extreme temperatures proven lethal (i.e., 33°C) in juvenile C. melanopterus might have been tempered by daily variation. The proven efficiency of time-series datasets for reef sharks to identify critical habitats (having the highest juvenile shark densities over time) should be extended to other populations to significantly contribute to the conservation of reef shark species.     

Exclusive predation of sea turtle hatchlings by juvenile blacktip reef sharks Carcharhinus melanopterus at a turtle nesting site in Malaysia

This study reports the discovery of the exclusive predation of sea turtle hatchlings by several juvenile blacktip reef sharks (Carcharhinus melanopterus) in Chagar Hutang bay on Redang Island, Malaysia, in the South China Sea. Three dead specimens of C. melanopterus were retrieved from ghost nets, and the entire digestive tracts of these sharks solely contained the partially digested bodies of sea turtle hatchlings, with no evidence of the remains of any other prey. Thus, juvenile C. melanopterus may opportunistically feed primarily on turtle hatchlings during times when hatchling abundance is high.     

Risks and advantages of using surface laser photogrammetry on free‐ranging marine organisms: a case study on white sharks Carcharodon carcharias

This study employed a non‐lethal measurement tool, which combined an existing photo‐identification technique with a surface, parallel laser photogrammetry technique, to accurately estimate the size of free‐ranging white sharks Carcharodon carcharias. Findings confirmed the hypothesis that surface laser photogrammetry is more accurate than crew‐based estimations that utilized a shark cage of known size as a reference tool. Furthermore, field implementation also revealed that the photographer's angle of reference and the shark's body curvature could greatly influence technique accuracy, exposing two limitations. The findings showed minor inconsistencies with previous studies that examined pre‐caudal to total length ratios of dead specimens. This study suggests that surface laser photogrammetry can successfully increase length estimation accuracy and illustrates the potential utility of this technique for growth and stock assessments on free‐ranging marine organisms, which will lead to an improvement of the adaptive management of the species.     

Blacktip reef sharks,Carcharhinus melanopterus,have high genetic structure and varying demographic histories in their Indo‐Pacific range

For free‐swimming marine species like sharks, only population genetics and demographic history analyses can be used to assess population health/status as baseline population numbers are usually unknown. We investigated the population genetics of blacktip reef sharks, Carcharhinus melanopterus; one of the most abundant reef‐associated sharks and the apex predator of many shallow water reefs of the Indian and Pacific Oceans. Our sampling includes 4 widely separated locations in the Indo‐Pacific and 11 islands in French Polynesia with different levels of coastal development. Four‐teen microsatellite loci were analysed for samples from all locations and two mitochondrial DNA fragments, the control region and cytochrome b, were examined for 10 locations. For microsatellites, genetic diversity is higher for the locations in the large open systems of the Red Sea and Australia than for the fragmented habitat of the smaller islands of French Polynesia. Strong significant structure was found for distant locations with F_ST values as high as ~0.3, and a smaller but still significant structure is found within French Polynesia. Both mitochondrial genes show only a few mutations across the sequences with a dominant shared haplotype in French Polynesia and New Caledonia suggesting a common lineage different to that of East Australia. Demographic history analyses indicate population expansions in the Red Sea and Australia that may coincide with sea level changes after climatic events. Expansions and flat signals are indicated for French Polynesia as well as a significant recent bottleneck for Moorea, the most human‐impacted lagoon of the locations in French Polynesia.     

The use of an unoccupied aerial vehicle to survey shark species over sand and rocky-reef habitats in a marine protected area

Cabo Pulmo National Park was established in 1995 and has since seen a large increase in fish biomass. An unoccupied aerial vehicle (UAV) was used to survey shallow coastal habitat in which lemon sharks (Negaprion brevirostris), bull sharks (Carcharhinus leucas) and Pacific nurse sharks (Ginglymostoma unami) were recorded. Sharks were more common in the afternoon, potentially using warmer shallow areas to behaviourally thermoregulate. This study highlights UAV surveying to be a viable tool for species identification, a limitation of previous terrestrial surveys conducted in the area.     

Markov models and network analysis reveal sex‐specific differences in the space‐use of a coastal apex predator

Understanding the links between external variables such as habitat and interactions with conspecifics and animal space‐use is fundamental to developing effective management measures. In the marine realm, automated acoustic tracking has become a widely used method for monitoring the movement of free‐ranging animals, yet researchers generally lack robust methods for analysing the resulting spatial‐usage data. In this study, acoustic tracking data from male and female broadnose sevengill sharks Notorynchus cepedianus, collected in a system of coastal embayments in southeast Tasmania were analyzed to examine sex‐specific differences in the sharks’ coastal space‐use and test novel methods for the analysis of acoustic telemetry data. Sex‐specific space‐use of the broadnose sevengill shark from acoustic telemetry data was analysed in two ways: The recently proposed spatial network analysis of between‐receiver movements was employed to identify sex‐specific space‐use patterns. To include the full breadth of temporal information held in the data, movements between receivers were furthermore considered as transitions between states of a Markov chain, with the resulting transition probability matrix allowing the ranking of the relative importance of different parts of the study area. Both spatial network and Markov chain analysis revealed sex‐specific preferences of different sites within the study area. The identification of priority areas differed for the methods, due to the fact that in contrast to network analysis, our Markov chain approach preserves the chronological sequence of detections and accounts for both residency periods and movements. In addition to adding to our knowledge of the ecology of a globally distributed apex predator, this study presents a promising new step towards condensing the vast amounts of information collected with acoustic tracking technology into straightforward results which are directly applicable to the management and conservation of any species that meet the assumptions of our model.     

Size frequency,dispersal distances and variable growth rates of young sharks in a multi-species aggregation

During a mark–recapture survey from November 2014 until April 2017, 333 neonatal and juvenile blacktip reef sharks Carcharhinus melanopterus and 302 neonatal and juvenile sicklefin lemon sharks Negaprion acutidens were tagged and measured at the uninhabited and isolated St. Joseph Atoll (Republic of Seychelles). Both species demonstrated seasonal reproductive synchronicity and relatively large sizes at birth. Despite the extended times at liberty > 2.5 years, the majority of recaptures were found in close proximity to the initial tagging location (< 500 m). Annual growth rates of C. melanopterus (n = 24) and N. acutidens (n = 62) ranged from 6.6 to 31.7 cm year⁻¹ (mean ± SE; 16.2 ± 1.2 cm year⁻¹) and 0.2 to 32.2 cm year⁻¹ (11.8 ± 1 cm year⁻¹), respectively and are to date the most variable ever recorded in wild juvenile sharks. High abundances of both species coupled with long-term and repeated recaptures are indicative of a habitat where juveniles can reside for their first years of life. However, large variability in annual growth rates in both species may suggest high intra and interspecific competition induced by a possibly resource limited, isolated habitat.     

Metabolic rates and the energetic cost of external tag attachment in juvenile blacktip sharks Carcharhinus limbatus

This study reports on the metabolic rate of the blacktip shark Carcharhinus limbatus and the energetic costs of external tag attachment. Metabolic rates, swimming speed and tail‐beat (B_T) frequency were measured in a static respirometer with untagged animals and animals equipped with a small data logger. Tagged sharks showed significantly higher routine oxygen consumption and lower swimming speeds than untagged animals, indicating that tagging significantly affected the swimming efficiency and energetic requirements in these small sharks, and that these effects must be accounted for when interpreting telemetry data from free‐ranging individuals.     

Intraspecific variation in vertical habitat use by tiger sharks (Galeocerdo cuvier) in the western North Atlantic

Tiger sharks (Galeocerdo cuvier) are a wide ranging, potentially keystone predator species that display a variety of horizontal movement patterns, making use of coastal and pelagic waters. Far less, however, is known about their vertical movements and use of the water column. We used pop‐up satellite archival tags with two data sampling rates (high rate and standard rate tags) to investigate the vertical habitat use and diving behavior of tiger sharks tagged on the Puerto Rico–Virgin Islands platform and off Bermuda between 2008 and 2009. Useable data were received from nine of 14 sharks tagged, tracked over a total of 529 days. Sharks spent the majority of their time making yo‐yo dives within the upper 50 m of the water column and considerable time within the upper 5 m of the water column. As a result, sharks typically occupied a narrow daily temperature range (~2°C). Dives to greater than 200 m were common, and all sharks made dives to at least 250 m, with one shark reaching a depth of 828 m. Despite some similarities among individuals, a great deal of intraspecific variability in vertical habit use was observed. Four distinct depth distributions that were not related to tagging location, horizontal movements, sex, or size were detected. In addition, similar depth distributions did not necessitate similar dive patterns among sharks. Recognition of intraspecific variability in habitat use of top predators can be crucial for effective management of these species and for understanding their influence on ecosystem dynamics.     

Shark bite wounds of the valvular intestine: The cause of an acute mortality syndrome of captive blacktip reef sharks,Carcharhinus melanopterus

During 1987–1990 nine cases of mortality in captive blacktip reef sharks (Carcharhinus melanopterus) were attributed to bite wounds to the valvular intestine. Necropsies revealed lacerations, amputation of the scroll valve folds, or complete severance of the valvular intestine. Wounding resulting from attack by tankmates occurred during episodes of intestinal eversion, an apparently regular event of unclear physiological function in sharks with a scroll valve intestine. This paper adds intestinal biting as a putative cause of mortality in captive shark species having a scroll valve intestine.     

The Role of Early Learning in Determining Shoaling Preferences Based on Visual Cues in the Zebrafish, Danio rerio

Social preferences for specific colour patterns learned in early development, termed imprinting, may influence social and mating decisions. Imprinting has been demonstrated in both birds and fish and has been proposed to play a role in speciation. We raised wild‐type zebrafish, Danio rerio, either with individuals of the same colour pattern, an alternative colour pattern (leopard), or a closely related, unpatterned species, D. albolineatus. We also cross‐reared individual ‘leopard’D. rerio and D. albolineatus with wild‐type D. rerio. We tested the prediction that Danio would prefer to shoal with fish of the colour pattern with which they had been raised, irrespective of their own appearance. Rearing condition affected shoaling preferences between D. rerio and D. albolineatus, with individuals of both colour patterns preferring to associate with shoals of the colour pattern with which they had been raised. The more subtle distinction between the wild‐type and ‘leopard’D. rerio colour patterns did not elicit a shoaling preference. Thus, zebrafish exhibit shoaling preferences based on visual cues, the effect being stronger when patterns are more distinct. There is a strong learned component to these preferences, although the extent to which they may influence mating decisions is unclear.     

Comparative squamation of the lateral line canal pores in sharks

The current study collected the first quantitative data on lateral line pore squamation patterns in sharks and assessed whether divergent squamation patterns are similar to experimental models that cause reduction in boundary layer turbulence. In addition, the hypothesis that divergent orientation angles are exclusively found in fast‐swimming shark species was tested. The posterior lateral line and supraorbital lateral line pore squamation of the fast‐swimming pelagic shortfin mako shark Isurus oxyrinchus and the slow‐swimming epi‐benthic spiny dogfish shark Squalus acanthias was examined. Pore scale morphology and pore coverage were qualitatively analysed and compared. In addition, pore squamation orientation patterns were quantified for four regions along the posterior lateral line and compared for both species. Isurus oxyrinchus possessed consistent pore scale coverage among sampled regions and had a divergent squamation pattern with multiple scale rows directed dorsally and ventrally away from the anterior margin of the pore with an average divergent angle of 13° for the first row of scales. Squalus acanthias possessed variable amounts of scale coverage among the sampled regions and had a divergent squamation pattern with multiple scale rows directed ventrally away from the anterior margin of the pore with an average angle of 19° for the first row of scales. Overall, the squamation pattern measured in I. oxyrinchus fell within the parameters used in the fluid flow analysis, which suggests that this pattern may reduce boundary layer turbulence and affect lateral line sensitivity. The exclusively ventral oriented scale pattern seen in S. acanthias possessed a high degree of divergence but the pattern did not match that of the fluid flow models. Given current knowledge, it is unclear how this would affect boundary layer flow. By studying the relationship between squamation patterns and the lateral line, new insights are provided into sensory biology that warrant future investigation due to the implications for the ecology, morphology and sensory evolution of sharks.     

Spatial, seasonal and diel distribution patterns of two species of mojarras (Pisces: Gerreidae) in a Mexican tropical coastal lagoon

Spatial, seasonal and diel distribution patterns were analysed over a 2‐year period for Diapterus auratus and Eucinostomus melanopterus in Pueblo Viejo lagoon, a tropical coastal lagoon in Veracruz, Mexico. A total of 216 samples were collected with 329 individuals of D. auratus and 170 of E. melanopterus. Diapterus auratus individuals were captured throughout a wider range of environmental conditions, and consequently its spatial niche breadth was significantly greater (P < 0.001) than that of E. melanopterus. In general, more individuals were captured at localities with submerged vegetation (Ruppia maritima), with 70% for D. auratus and 87.2% for E. melanopterus, although only the latter species showed significant spatial differences. A spatial segregation influenced by distance from the lagoon inlet and salinity was observed between the species. It is considered that this segregation may allow resource partitioning and minimize interspecific competition. A relatively low niche overlap (4.9%) was observed for the two species. Seasonal capture peaks of D. auratus were related to rainfall and the productivity pattern in the lagoon system. Seasonal fluctuations in monthly mean number of D. auratus were correlated with preceding variations in local rainfall (r = 0.86, P < 0.02). Moreover, seasonal capture peaks of D. auratus coincided with ecosystem primary production peaks. Although E. melanopterus exhibited no significant seasonal differences, its maximum numbers also coincided with an ecosystem primary production peak and recruitment patterns. In 24‐h cycle analysis, both species were captured mainly around mid‐day, with minor peaks at dawn and/or at dusk. Generally, few individuals were collected during hours of darkness. It was proposed that diel abundance variation of gerreids might be related to both light penetration in the water column and feeding activity. Food availability within Pueblo Viejo lagoon appears to be an important factor influencing fish abundance.     

Experimental Validation of Sex Differences in Spatial Behavior Patterns of Free‐Ranging Snakes: Implications for Social Interactions

Social interactions often play a significant role in determining patterns of spatial use. Although snakes are generally thought of as asocial, recent spatial dispersion studies suggest that the spatial ecology of snakes may be more strongly influenced by social interactions than previously thought. We investigated the spatial behavior patterns of a western cottonmouth (Agkistrodon piscivorus) population in east Texas by uniquely combining radio‐telemetry studies on free‐ranging snakes with experimental arena trials with captive individuals from the same population. Observations from the radio‐telemetry study on free‐ranging A. piscivorus indicated that females were more gregarious than males. In the follow‐up study, spatial dispersion data from captive snakes maintained in experimental field arenas yielded similar results to spatial behavior patterns of free‐ranging individuals. When compared to random experimental controls, these data suggest that observed spatial behavior patterns are related to mechanisms associated with both active avoidance among males and conspecific attraction among females. In addition to uniquely combining both free‐ranging and captive observations, this is the first snake study to demonstrate sex differences with both of these divergent (attraction and avoidance) spatial patterns within a single population. Thus, similar to other vertebrate groups, a growing body of literature suggests that social interactions in snakes should be strongly considered in interpretations of spatial ecology and behavior.     

Trophic niche and habitat shifts of sympatric Gerreidae

The diet and mouth growth rates of three Gerreidae species (Eugerres brasilianus, Eucinostomus melanopterus and Diapterus rhombeus) were assessed at different ontogenetic phases (juveniles, sub‐adults and adults) in order to detect allometric growth, and whether they are related to habitat and seasonal changes in the Goiana Estuary, north‐east Brazil. The importance of each prey for each ontogenetic phase was described using the index of relative importance. The three species showed seasonal ontogenetic shifts in diet and allometric growth of mouth morphology. They also had an exclusively zoobenthic diet, comprising mainly Polychaeta, Copepoda, Ostracoda, Gastropoda and Bivalvia. Mouth development showed a possible influence on diet changes for E. melanopterus. Significant interactions (P < 0·01) were detected among seasons, areas and ontogenetic phases for the most important prey for E. brasilianus and E. melanopterus. Diet overlaps are evidence of intra and interspecific competition among gerreids for specific prey. A conceptual model of the competition and seasonal diet shifts among ontogenetic phases of gerreids is given. The sediment ingested due to the feeding mechanisms of Gerreidae species could also partially explain the ingestion of synthetic items observed for all ontogenetic phases, which indicates one of a myriad effects of human activities (e.g. artisanal fishery) in this estuary.     

Morphological scaling of body form in four shark species differing in ecology and life history

Body form can change across ontogeny, and can influence how animals of different sizes move and feed. Scaling data on live apex predatory sharks are rare and, therefore, we examined patterns of scaling in ontogenetic series of four sympatric shark species exhibiting a range of sizes, ecologies and life histories (tiger, bull, blacktip, and nurse shark). We evaluated 13 linear morphological variables and two areas (caudal and dorsal) that could influence both animal condition and locomotor performance. These measurements included dimensions of the dorsal, pectoral, and caudal fins, as well as several dimensions of body circumference, and of the head. For all four species, the body axis (eye‐to‐eye, lateral span, frontal span, proximal span) scaled close to isometry (expected slope of 1.0). The two largest sharks (tiger and bull sharks) also showed significant negative allometry for elements of the caudal fin. We found significant negative allometry in the lengths of the upper lobe of the caudal fin (caudal fin 1) and the overall height of the caudal fin (caudal fin 2) in tiger and bull sharks, with slopes ranging from about 0.60 to 0.73. Further, tiger sharks showed negative allometry in caudal fin area. These results suggest that in terms of overall body dimensions, small sharks are roughly geometrically similar to large sharks, at least within the species we examined. However, juvenile tiger (and to a lesser extent bull sharks) are notable in having proportionately larger caudal fins compared to adult sharks. As the caudal fin contributes to generating thrust during forward locomotion, this scaling implies differences among adult and juvenile sharks in locomotor ability. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 114 , 126–135.     

Cookie‐cutter shark Isistius spp. predation upon different tuna species from the south‐western Atlantic Ocean

The predation of cookie‐cutter sharks Isistius spp. upon the early life stages of yellowfin tuna Thunnus albacares, skipjack tuna Katsuwonus pelamis and little tunny Euthynnus alletteratus are described. New evidence suggesting a connection between commercial fishing and predation by Isistius sp. is presented, with these sharks biting tunas hooked in surface waters during daylight. The healing patterns of the wounds made by the sharks are described in detail and, although such damage is known to negatively influence market price elsewhere, it is not the case on the south‐east Brazilian coast.