Integrating acoustic telemetry into mark-recapture models to improve the precision of apparent survival and abundance estimates

Capture-mark-recapture models are useful tools for estimating demographic parameters but often result in low precision when recapture rates are low. Low recapture rates are typical in many study systems including fishing-based studies. Incorporating auxiliary data into the models can improve precision and in some cases enable parameter estimation. Here, we present a novel application of acoustic telemetry for the estimation of apparent survival and abundance within capture-mark-recapture analysis using open population models. Our case study is based on simultaneously collecting longline fishing and acoustic telemetry data for a large mobile apex predator, the broadnose sevengill shark (Notorhynchus cepedianus), at a coastal site in Tasmania, Australia. Cormack-Jolly-Seber models showed that longline data alone had very low recapture rates while acoustic telemetry data for the same time period resulted in at least tenfold higher recapture rates. The apparent survival estimates were similar for the two datasets but the acoustic telemetry data showed much greater precision and enabled apparent survival parameter estimation for one dataset, which was inestimable using fishing data alone. Combined acoustic telemetry and longline data were incorporated into Jolly-Seber models using a Monte Carlo simulation approach. Abundance estimates were comparable to those with longline data only; however, the inclusion of acoustic telemetry data increased precision in the estimates. We conclude that acoustic telemetry is a useful tool for incorporating in capture-mark-recapture studies in the marine environment. Future studies should consider the application of acoustic telemetry within this framework when setting up the study design and sampling program.

Integrating network analysis, sensor tags, and observation to understand shark ecology and behavior

Group living in animals is a well-studied phenomenon, having been documented extensively in a wide range of terrestrial, freshwater, and marine species. Although social dynamics are complex across space and time, recent technological and analytical advances enable deeper understanding of their nature and ecological implications. While for some taxa, a great deal of information is known regarding the mechanistic underpinnings of these social processes, knowledge of these mechanisms in elasmobranchs is lacking. Here, we used an integrative and novel combination of direct observation, accelerometer biologgers, and recent advances in network analysis to better understand the mechanistic bases of individual-level differences in sociality (leadership, network attributes) and diel patterns of locomotor activity in a widespread marine predator, the lemon shark (Negaprion brevirostris). We found that dynamic models of interaction based on Markov chains can accurately predict juvenile lemon shark social behavior and that lemon sharks did not occupy consistent positions within their network. Lemon sharks did however preferentially associate with specific group members, by sex as well as by similarity or nonsimilarity for a number of behavioral (nonsimilarity: leadership) and locomotor traits (similarity: proportion of time swimming "fast," mean swim duration; nonsimilarity: proportion of swimming bursts/transitions between activity states). Our study provides some of the first information on the mechanistic bases of group living and personality in sharks and further, a potential experimental approach for studying fine-scale differences in behavior and locomotor patterns in difficult-to-study organisms.

Top Down Control in a Relatively Pristine Seagrass Ecosystem

The loss of large-bodied herbivores and/or top predators has been associated with large-scale changes in terrestrial, freshwater, and marine ecosystems around the world. Understanding the consequences of these declines has been hampered by a lack of studies in relatively pristine systems. To fill this gap, I investigated the dynamics of the relatively pristine seagrass ecosystem of Shark Bay, Australia. I began by examining the seagrass species distributions, stoichiometry, and patterns of nutrient limitation across the whole of Shark Bay. Large areas were N-limited, P-limited, or limited by factors other than nutrients. Phosphorus-limitation was centered in areas of restricted water exchange with the ocean. Nutrient content of seagrasses varied seasonally, but the strength of seasonal responses were species-specific. Using a cafeteria-style experiment, I found that fast-growing seagrass species, which had higher nutrient content experienced higher rates of herbivory than slow-growing species that are dominant in the bay but have low nutrient content. Although removal rates correlated well with nutrient content at a broad scale, within fast-growing species removal rates were not closely tied to N or P content. Using a combination of stable isotope analysis and animal borne video, I found that green turtles (Chelonia mydas) – one of the most abundant large-bodied herbivores in Shark Bay – appear to assimilate little energy from seagrasses at the population level. There was, however, evidence of individual specialization in turtle diets with some individuals foraging largely on seagrasses and others feeding primarily on macroalgae and gelatinous macroplankton. Finally, I used exclusion cages, to examine whether predation-sensitive habitat shifts by megagrazers (green turtles, dugongs) transmitted a behavior-mediated trophic cascade (BMTC) between sharks and seagrasses. In general, data were consistent with predictions of a behavior-mediated trophic cascade. Megaherbivore impacts on seagrasses were large only in the microhabitat where megaherbivores congregate to reduce predation risk. My study highlights the importance of large herbivores in structuring seagrass communities and, more generally, suggests that roving top predators likely are important in structuring communities - and possibly ecosystems - through non-consumptive pathways.

The Role of Teleost Grazers in a Relatively Pristine Seagrass Ecosystem

Trophic downgrading of ecosystems necessitates a functional understanding of trophic cascades. Identifying the presence of cascades, and the mechanisms through which they occur, is particularly important for seagrass meadows, which are among the most threatened ecosystems on Earth. Shark Bay, Western Australia provides a model system to investigate the potential importance of top-down effects in a relatively pristine seagrass ecosystem. The role of megagrazers in the Shark Bay system has been previously investigated, but the role of macrograzers (i.e., teleosts), and their importance relative to megagrazers, remains unknown. The objective of my dissertation was to elucidate the importance of teleost macrograzers in transmitting top-down effects in seagrass ecosystems. Seagrasses and macroalgae were the main food of the abundant teleost Pelates octolineatus, but stable isotopic values suggested that algae may contribute a larger portion of assimilated food than suggested by gut contents. Pelates octolineatus is at risk from numerous predators, with pied cormorants (Phalacrocorax varius) taking the majority of tethered P. octolineatus. Using a combination of fish trapping and unbaited underwater video surveillance, I found that the relative abundance of P. octolineatus was greater in interior areas of seagrass banks during the cold season, and that the mean length of P. octolineatus was greater in these areas compared to along edges of banks. Finally, I used seagrass transplants and exclosure experiments to determine the relative effect of megagrazers and macrograzers on the establishment and persistence of three species of seagrasses in interior microhabitats. Teleost grazing had the largest impact on seagrass species with the highest nutrient content, and these impacts were primarily observed during the warm season. My findings are consistent with predictions of a behaviorally-mediated trophic cascade initiated by tiger sharks (Galeocerdo cuvier) and transmitted through herbivorous fishes and their predators.

Conservation and management of exploited shark populations based on reproductive value

Several life history traits of sharks result in juveniles being particularly vulnerable to exploitation. However, population level impacts of harvests on juvenile sharks have not been well quantified. This paper examines a range of harvest strategies, including those targeting juveniles. Reproductive value and yield per recruit are used to compare the harvests, which are represented by Leslie matrix models with a harvest matrix. Two species are used as examples: the short-lived Rhizoprionodon taylori and the long-lived Squalus acanthias. Harvests that maintain a stationary population size cause reproductive values to change in opposing ways, but they remove equal fractions of the population's reproductive potential. A new theorem gives population growth as a function of the fraction of reproductive potential removed by a harvest, a relationship useful for comparing harvests on juveniles and adults. Stochastic projections indicate that the risk of depletion is associated with the fraction of reproductive potential removed annually, a measure which encompasses the information in both the selectivity and the rate of fishing mortality. These results indicate the value of focusing conservation efforts on preserving reproductive potential.

Effects of fishing methods on deep water shark species caught as by-catch off southern Portugal

Deep water sharks are commonly caught as by-catch of longlines targeting bony fishes and trawlers targeting crustaceans in deep water off the southern Portuguese coast. Due to low or no commercial value, these species are most of the times discarded at sea, with only the larger specimens of some species commercialized at very low prices. In this study we present size distributions, maturity distributions, and sex ratios of 2,138 specimens belonging to four different species, namely the lantern sharks Etmopterus pusillus and Etmopterus spinax and the catsharks Galeus melastomus and Galeus atlanticus, caught with these two gears. Trawls generally caught smaller-sized specimens, in a wider length range than longlines. Trawls caught mostly immature specimens of all species, namely 83.7% immature of E. pusillus, 84.3% of E. spinax, 89.5% of G. melastomus, and 95.5% of G. atlanticus, while longlines caught mostly immature E. pusillus (69.2%) and G. melastomus (78.6%) and mostly mature E. spinax (88.2%) and G. atlanticus (87.2%). Trawls tended to catch more males than females of all species except E. spinax, while longlines caught more females than males of E. spinax and G. melastomus and more males than females of the other two species. The main conclusion of this work is that trawls are catching smaller-sized and mostly immature specimens when compared to longlines, meaning that they are probably having a more detrimental effect on these shark populations. The data presented here have significant implications for the conservation of these shark populations since sizes, sexes, and the immature and mature components of the populations are being affected differently by these two fishing gears.

Feeding habits of the velvet belly lanternshark Etmopterus spinax (Chondrichthyes : Etmopteridae) off the Algarve, southern Portugal

Etmopterus spinax is one of the most abundant predators of the upper continental slope off the Algarve (southern Portugal), where it is captured in large quantities in deep-water fisheries. The feeding habits of E. spinax off the Algarve were investigated through the analysis of stomach contents of 376 individuals. Prey composition was described and maturity, sex and size related variations in the diet analysed. The overall diet of E. spinax suggested a fairly generalized benthopelagic foraging behaviour primarily tuned to pelagic macroplankton/microneckton, teleost fish and cephalopods. Sex and maturity related differences in the diet were not significant. Two main ontogenic diet shifts were observed at about 17 and 28 cm total length. Small and medium sized immature sharks had a diet dominated by eurybathic crustaceans, chiefly Meganyctiphanes norvegica and Pasiphaea sivado. Larger individuals consumed more teleosts and cephalopods, in part associated with scavenging as a new feeding strategy. With increasing shark size the diet diversified both in terms of resources exploited and prey size.

Life history of a wide-ranging deepwater lantern shark in the north-east Atlantic, Etmopterus spinax (Chondrichthyes: Etmopteridae), with implications for conservation

In this paper, the population biology of the velvet belly lanternshark Etmopterus spinax was studied and life-history coefficients determined. Age was estimated from sections of the second dorsal spine and validated by marginal increment analysis. Males attained a maximum age of 8 years while 11 year-old females were found. Several growth models were fitted and compared for both size-at-age and mass-at-age data, showing that even though this is a small-sized species, it has a relatively slow growth rate. This species matures late, specifically at 49.6 and 42.5% of the maximum observed ages for males and females, respectively. It has a low fecundity, with a mean ovarian fecundity of 9.94 oocytes and a mean uterine fecundity of 7.59 embryos per reproductive cycle. This species seems to have a long reproductive cycle, and even though no conclusive data were obtained, a 2-3 year cycle is possible. The estimated coefficients indicate that this species has a vulnerable life cycle, typical of deepwater squalid sharks. Given the high fishing pressures that it is suffering in the north-east Atlantic, this fish may already be facing severe declines or in risk of facing them in the near future. (C) 2008 The Authors Journal compilation (C) 2008 The Fisheries Society of the British Isles

Population parameters of the smooth lantern shark, Etmopterus pusillus, in southern Portugal (NE Atlantic)

Etmopterus pusillus is a deep water lantern shark with a widespread global distribution that is caught in large quantities in some areas, but is usually discarded due to the low commercial value. In this work, the population biology was studied and life history parameters determined for the first time in this species. Age was estimated from sections of the second dorsal spine and validated by marginal increment analysis. Males attained a maximum age of 13 years, while 17-year-old females were found. Several growth models were fitted and compared for both size and weight at age data, showing that even though this is a small sized species, it has a relatively slow growth rate. This species matures late and at a relatively large size: at 86.81% and 79.40% of the maximum observed sizes and at 58.02% and 54.40% of the maximum observed ages for males and females, respectively. It has a low fecundity, with a mean ovarian fecundity of 10.44 oocytes per reproductive cycle. The estimated parameters indicate that this species has a vulnerable life cycle, typical of deep water squalid sharks. Given the high fishing pressures that it is suffering in the NE Atlantic, the smooth lantern shark may be in danger of severe declines in the near future. (c) 2007 Elsevier B.V. All rights reserved.

Reduction of elasmobranch by-catch in the hake semipelagic near-bottom longline fishery in the Algarve (Southern Portugal)

Elasmobranch fish, particularly deep-sea sharks, are the most important component of the by-catch of the hake semipelagic near-bottom 'pedra-e-bola' longline fishery in the Algarve (South Portugal) and most of these fish are discarded. The effects of the removal of the lower hooks were evaluated, in terms of target and by-catch reductions, by quantifying the catches of each hook relative to the distance from the bottom. The analysis showed that most European hake (Merluccius merluccius), the target species of this fishery, were caught in the middle range of the hooks, with very few individuals caught near the bottom, whereas for sharks the situation was the opposite, with most hooked near the bottom. The removal of the lower three pairs of hooks would result in a small reduction in the catch of the target species, but a much more significant reduction in elasmobranch by-catch. In the specific case of the blackmouth catshark (Galeus melastomus), discard mortality would be further minimized due to the fact that the lower hooks capture significantly smaller animals that are always discarded compared with hooks that are more distant from the bottom.

Reproductive biology of the blackmouth catshark, Galeus melastomus (Chondrichthyes : Scyliorhinidae) off the south coast of Portugal

The reproductive biology of 1045 female (9.5-67 cm (total length(TL)) and 1007 male (9.4-64.3 cm TL) blackmouth catsharks, Galeus melastomus, was investigated. The sharks were caught off southern Portugal by bottom crustacean trawlers at depths from 209 to 754 m. The sex ratio was 1:1, and this species is sexually dimorphic with males approaching maturity at smaller size than females. Sexual segregation appears to be given for the stork within the study area. Sexual maturity was reached at a total length above 49 cm in males and above 56 cm in females. Mating and egg-deposition take place all year round, with two reproductive peaks of activity, in winter and summer. Egg capsules are, on average, 54 mm long and 21 mm wide, with a maximum of 63 x 25 mm encountered. Morphometric measurements of claspers, testes, ovaries, and oviducal glands were suitable for determining sexual maturity of blackmouth catshark.

Age and growth of the bigeye thresher shark, Alopias superciliosus, from the pelagic longline fisheries in the tropical northeastern Atlantic Ocean, determined by vertebral band counts

The bigeye thresher, Alopias supercilious, is commonly caught as bycatch in pelagic longline fisheries targeting swordfish. Little information is yet available on the biology of this species, however. As part of an ongoing study, observers sent aboard fishing vessels have been collecting set of information that includes samples of vertebrae, with the aim of investigating age and growth of A. supercilious. A total of 117 specimens were sampled between September 2008 and October 2009 in the tropical northeastern Atlantic, with specimens ranging from 101 to 242 cm fork length (FL) (176 to 407 cm total length). The A. supercilious vertebrae were generally difficult to read, mainly because they were poorly calcified, which is typical of Lamniformes sharks. Preliminary trials were carried out to determine the most efficient band enhancement technique for this species, in which crystal violet section staining was found to be the best methodology. Estimated ages in this sample ranged from 2 to 22 years for females and 1 to 17 years for males. A version of the von Bertalanffy growth model (VBGF) re-parameterised to estimate L(0), and a modified VBGF using a fixed L(0) were fitted to the data. The Akaike information criterion (AIC) was used to compare these models. The VBGF produced the best results, with the following parameters: L(inf) = 293 cm FL, k = 0.06 y(-1) and L(0) = 111 cm FL for females; L(inf) = 206 cm FL, k = 0.18 y(-1) and L(0) = 93 cm FL for males. The estimated growth coefficients confirm that A. supercilious is a slow-growing species, highlighting its vulnerability to fishing pressure. It is therefore urgent to carry out more biological research to inform fishery managers more adequately and address conservation issues.

Demography of a deep-sea lantern shark (Etmopterus spinax) caught in trawl fisheries of the northeastern Atlantic: Application of Leslie matrices with incorporated uncertainties

The deep-sea lantern shark Etmopterus spinax occurs in the northeast Atlantic on or near the bottoms of the outer continental shelves and slopes, and is regularly captured as bycatch in deep-water commercial fisheries. Given the lack of knowledge on the impacts of fisheries on this species, a demographic analysis using age-based Leslie matrices was carried out. Given the uncertainties in the mortality estimates and in the available life history parameters, several different scenarios, some incorporating stochasticity in the life history parameters (using Monte Carlo simulation), were analyzed. If only natural mortality were considered, even after introducing uncertainties in all parameters, the estimated population growth rate (A) suggested an increasing population. However, if fishing mortality from trawl fisheries is considered, the estimates of A either indicated increasing or declining populations. In these latter cases, the uncertainties in the species reproductive cycle seemed to be particularly relevant, as a 2-year reproductive cycle indicated a stable population, while a longer (3-year cycle) indicated a declining population. The estimated matrix elasticities were in general higher for the survivorship parameters of the younger age classes and tended to decrease for the older ages. This highlights the susceptibility of this deep-sea squaloid to increasing fishing mortality, emphasizing that even though this is a small-sized species, it shows population dynamics patterns more typical of the larger-sized and in general more vulnerable species. (C) 2014 Elsevier Ltd. All rights reserved.

Size at maturity and length-weight relationships of the blurred lantern shark Etmopterus bigelowi (Squaliformes: Etmopteridae) caught off southeastern Brazil

The blurred lantern shark Etmopterus bigelowi, a deep-water squaloid shark, is globally widespread in temperate and tropical waters, but there is little available information about its biology owing to its relative rarity of capture and taxonomic confusion with its sibling species Etmopterus pusillus. Specimens used in this study were collected from July to December 2004 as by-catch in the commercial deepwater trawl fishery targeting red shrimp Aristaeomorpha foliacea in the southwestern Atlantic. We examined 55 specimens (22 males and 33 females) ranging in total length (TL) from 31.5 to 73 cm and in total weight from 103 to 1600 g. Length-weight relationships were explored for each sex and significant differences were found in the slope coefficients of the male and female regressions. The size at maturity for each sex was evaluated fitting a logistic regression. Females matured at larger sizes than males, with estimated sizes at first maturity of 56.0 cm TL for females and 45.1 cm TL for males. The present study provides important preliminary information about E. bigelowi that can be incorporated in risk assessment and stock assessment models, essential for efficient management practices aimed at avoiding overexploitation of these vulnerable deep-sea sharks.

Age and growth of the smooth hammerhead shark, Sphyrna zygaena, in the Eastern Equatorial Atlantic Ocean, using vertebral sections

The smooth hammerhead shark Sphyrna zygaena (Sphyrnidae) is regularly caught as bycatch in pelagic longline fisheries, but is one of the least studied of all pelagic sharks. Recently, ICCAT (International Commission for the Conservation of Atlantic Tunas) issued recommendations underlining the need for more studies on the life history parameters of this and other pelagic shark species. To this end, the age and growth of S. zygaena were studied in the Eastern Equatorial Atlantic Ocean, in an area where growth parameters were not yet available for this species. Data from 139 specimens, caught between June and September 2009, ranging in size from 136 to 233 cm fork length (FL), were analysed. Preliminary trials were carried out to assess the most efficient growth band enhancement technique. These indicated that sectioning the vertebrae into 500 μm sections followed by staining with crystal violet produced the best results. Growth models were fitted using the traditional von Bertalanffy growth equation and a modification of this equation using a known size at birth. Growth models were compared using the Akaike information criterion (AIC). The von Bertalanffy growth equation seemed to be the most adequate model to describe growth in this species, with resulting growth parameters of L inf = 272 cm FL, k = 0.06 year for males and L inf = 285 cm FL, k = 0.07 year for females. In the first four years of life, S. zygaena grows 25 cm per year on average, but its growth slows down in later life. Future stock assessment models should incorporate these age and growth parameters for species management and conservation.