Juvenile Lemon Sharks Negaprion Brevirostris Research Articles

Predator abundance drives the association between exploratory personality and foraging habitat risk in a wild marine meso‐predator

Abstract In recent years, the incorporation of lower levels of organization to the understanding of population ecology, has led to an increase in interest for animal personality and individual foraging specialization. Despite these topics investigating comparable phenomena, that is, individual consistency in behaviour and in food resource use respectively, they have rarely been investigated together. Food resource use is thought to be at the interface between personality and life history. More explorative individuals in a population, for example, are thought to increase encounter rates with food resources and consequently have faster growth than less explorative conspecifics. Such hypotheses have so far only received partial support, and the link between personality and life history is increasingly speculated to be plastic and dependent on spatio‐temporal variation in ecological conditions. Intraspecific competition and/or predation risk, for example are known to influence foraging specialization. Here, we investigated the relationship between exploration personality of juvenile lemon sharks Negaprion brevirostris (measured in captivity) and foraging habitat use (high risk vs. low risk; measured via stable isotope analysis in the field) in relation to conspecific and predator abundance. We identified predator abundance as the main driver for the association between foraging habitat and exploration personality. When predators were less abundant, increased exploration was associated with foraging in riskier habitats. When predator abundance increased, an inverse relationship occurred, with less explorative individuals using more dangerous habitat. We conclude that the relationship between personality and resource use is plastic and context dependent, which could explain the inconclusive results of previous studies investigating links between personality and life history. A free Plain Language Summary can be found within the Supporting Information of this article.

Personality-driven life history trade-offs differ in two subpopulations of free-ranging predators.

Consistent individual differences in behaviour (i.e. personality) can be explained in an evolutionary context if they are favoured by life history trade-offs as conceptualized in the pace-of-life syndrome (POLS) hypothesis. Theory predicts that faster-growing individuals suffer higher mortality and that this trade-off is mediated through exploration/risk-taking personality, but empirical support for this remains limited and ambiguous. Equivocal support to the POLS hypothesis suggests that the link between life history and personality may only emerge under certain circumstances. Understanding personality-driven trade-offs would be facilitated by long-term studies in wild populations experiencing different ecological conditions. Here, we tested whether personality measured in semi-captivity was associated with a growth-mortality trade-off via risk-taking in the wild in two subpopulations of juvenile lemon sharks Negaprion brevirostris known to differ in their predator abundance. We expected stronger personality-driven trade-offs in the predator-rich environment as compared to the predator-poor environment. Sharks were captured yearly from 1995 onwards allowing us to obtain long-term data on growth and apparent survival in each subpopulation. We then used a novel open-field assay to test sharks for exploration personality yearly from 2012 to 2017. A subset of the tested sharks was monitored in the field using telemetry to document risk-taking behaviours. We tested (a) if fast explorers in captivity took more risks and grew faster in the wild and (b) if natural selection acted against more explorative, faster-growing sharks. In the subpopulation with fewer predators, more explorative sharks in captivity took more risks in the wild and grew faster. In turn, larger, fast-growing sharks had lower apparent survival. In the predator-rich subpopulation, despite finding selection on fast growth, we found no link between exploration personality and the growth-mortality trade-off. Our study demonstrates that the association between personality and life history is favoured in some ecological contexts but not in others. We identify predator and resource abundance as two main potential drivers of the personality-mediated trade-off and emphasize that future work on the POLS hypothesis would benefit from an approach integrating behaviour and life history across ecological conditions.

Treading water: respirometer choice may hamper comparative studies of energetics in fishes

Measuring the metabolic rate of animals is an essential part of understanding their ecology, behaviour and life history. Respirometry is the standard method of measuring metabolism in fish, but different respirometry methods and systems can result in disparate measurements of metabolic rate, a factor often difficult to quantify. Here we directly compare the results of two of the most common respirometry systems used in elasmobranch studies, a Steffensen-style flume respirometer and an annular static respirometer. Respirometry trials with juvenile lemon sharks Negaprion brevirostris were run in both systems under the same environmental conditions and using the same individuals. Relationships between metabolic rate, swimming speed, overall dynamic body acceleration (ODBA) and tail beat frequency (TBF) were compared between the two systems. The static respirometer elicited higher TBF and ODBA for a given swimming speed compared with the flume respirometer, although it produced relationships between kinematic parameters that were more similar to those observed in free-swimming animals. Metabolic rates and swimming speeds were higher for the flume respirometer. Therefore, although flume respirometers are necessary for many types of controlled laboratory studies, static respirometers may elicit lower stress and produce results that are more applicable to fish in wild systems.

The behaviour and recovery of juvenile lemon sharks Negaprion brevirostris in response to external accelerometer tag attachment.

Behavioural responses of lemon sharks Negaprion brevirostris to a fin-mounted tag package (CEFAS G6A tri-axial accelerometer with epoxied Sonotronics PT4 acoustic transmitter) were measured in a controlled captive environment (n = 10, total length, LT range 80-140 cm) and in free-ranging sharks upon release (n = 7, LT range 100-160 cm). No changes were detected in behaviour (i.e. swimming speed, tailbeat frequency, time spent resting and frequency of chafing) between control and tagged captive shark trials, suggesting that the tag package itself does not alter behaviour. In the free-ranging trials, an initial period of elevated swimming activity was found in all individuals (represented by overall dynamic body acceleration). Negaprion brevirostris, however, appeared to recover quickly, returning to a steady swimming state between 2 and 35 min after release. Post-release tracking found that all sharks swim immediately for the shoreline and remain within 100 m of shore for prolonged periods. Hence, although N. brevirostris are capable of quick adaptation to stressors and demonstrate rapid recovery in terms of activity, tracking data suggest that they may modify their spatial use patterns post release. This research is important in separating deviation in behaviour due to environmental stressors from artefacts caused by experimental techniques.

Diel temperature patterns of juvenile lemon sharks Negaprion brevirostris, in a shallow‐water nursery

The relatively complex pattern of temperature selection exhibited by juvenile lemon sharks Negaprion brevirostris in the North Sound differed markedly from many previously described responses of fish preferenda. Thermal data demonstrated that juvenile N. brevirostris did not attempt to behaviourally maintain a constant eccritic temperature. Rather, juveniles selected progressively warmer temperatures throughout the day until reaching the highest temperatures available, and then moved to cooler temperatures during late evening and early morning hours. It is possible that by exploiting habitat thermal heterogeneity juvenile N. brevirostris prolong activities such as feeding or digestion well into the cooler parts of the evening. The complex pattern of temperature occupation by juvenile N. brevirostris within the thermally heterogeneous North Sound nursery is probably linked to key daily activities such as prey capture, predator avoidance and digestive efficiency.

Deep danger: intra-specific predation risk influences habitat use and aggregation formation of juvenile lemon sharks Negaprion brevirostris

Non-consumptive or risk effects imposed by predators can influence prey behaviour over different spatio-temporal scales. Prey vulnerability to predation can also be dependent on abiotic conditions, such as tidal height. We conducted direct field observations of juvenile lemon sharks Negaprion brevirostris in a tidally influenced mangrove-inlet. We also used acoustic tracking to determine the movement patterns of juvenile lemon sharks and their predators (sub-adult lemon sharks) across the tidal cycle. Results showed that greater numbers of juvenile lemon sharks used the mangrove-inlet for longer time periods at deeper and warmer high tide depths. This coincided with an increased presence of potential predators (sub-adult lemon sharks) in the surrounding areas. Furthermore, in accordance with body-size dependent anti-predatory investment, smaller juvenile lemon sharks visited the mangrove inlet more often, spent longer there and left latest on average. Our acoustic tracking data also revealed a tidally-influenced pattern, with both juvenile and sub-adult lemon sharks detected at locations inshore over the high tide and offshore during the low tide. We concluded that the mangrove lake served as a 'refuge' for juvenile lemon sharks over the high tide, providing safe habitat when inshore areas become accessible to large predators, such as sub-adult lemon sharks. We suggest that these decisions are updated through ontogeny and also with daily fluctuations in abiotic factors, such as water depth. This study provides evidence for how intra-specific predatorprey interactions in a top predator species influence juvenile habitat selection, with potential implications for population structure and regulation.

Dietary metal and macro-nutrient intakes of juvenile lemon sharks determined from the nutritional composition of prey items

The trace element requirements of sharks are poorly understood and the dietary intake of metals from prey items in wild sharks has not been measured. In this study whole prey of nursery bound juvenile lemon sharks Negaprion brevirostris, from Bimini, Bahamas were analysed for car- cass total protein, lipids, carbohydrates, ash content, energy, and elemental composition. Metal analysis included 415 prey items from 18 species (fish: Atherinidae, Belonidae, Gerreidae, Haemuli- dae, Lutjanidae, Scaridae, Sphyraenidae; decapod crustaceans: Penaeidae, Portunidae). There were some seasonal and location effects (North Sound versus South Bimini shark nurseries), but overall prey metal concentrations were broadly similar to reports for temperate species. Yellow fin mojarra Gerres cinereus dominate the shark diet, in which electrolytes were similar (Na 10, K 10, Ca 65, and Mg 2 mg g -1 dry weight) but trace metals were higher (Cu 2.4, Zn 96, Fe 63, Mn 0.7 µg g -1 dry weight) than in other prey fish species at Bimini. Swimming crabs (Portunidae) were an important source of dietary Ca, Mg, Cu and Mn for lemon sharks. The calculated daily dietary metal intakes (mg d -1 ) for Cu (0.17), Fe (1.2) and Mn (0.01) of lemon sharks are below previously estimated requirements of other fish. Dietary salt intake (272 mg Na d -1 , 1% dietary salt) is similar to other fishes, but the Ca and Zn intakes are higher. Yellow fin mojarra contained 65% protein, 4% lipid, 23% ash. The average juvenile lemon shark (1.85 kg, 24.84 g daily ration) ate a very lean high protein diet (61.9% protein, 4.6% lipid, 24.9% ash, 8.6% carbohydrate), with a calculated energy intake of 397 kJ d -1 . Overall, the data suggests the gross macronutrient composition of the shark diet is adequate, but some of the trace metals may be limiting in the diet of wild juvenile lemon sharks at Bimini.

Chemical excretions of angled bonefish Albula vulpes and their potential use as predation cues by juvenile lemon sharks Negaprion brevirostris

Bonefish Albula vulpes (n = 7) exercised to exhaustion and air exposed for 1 min as part of a catch-and-release angling event were found to excrete both ammonia and urea, but cortisol and lactate were below detectable levels. Urea made up a greater proportion of total nitrogen excretion from these fish at all time points following an angling event. When captive juvenile lemon sharks Negaprion brevirostris (n = 12) were exposed to a 30 s pulse of these chemicals [ammonia (500 mM), cortisol (20 µg l(-1) ), lactate (6 mM) or urea (3 mM)], they showed a significant reduction in the frequency of resting behaviours when exposed to ammonia and urea than when exposed to control water. It appears that products excreted by A. vulpes, particularly ammonia and urea, may provide an olfactory cue for the post-release predation of A. vulpes by N. brevirostris during catch-and-release angling events.

Novel Acoustic Technology for Studying Free-Ranging Shark Social Behaviour by Recording Individuals' Interactions

Group behaviours are widespread among fish but comparatively little is known about the interactions between free-ranging individuals and how these might change across different spatio-temporal scales. This is largely due to the difficulty of observing wild fish groups directly underwater over long enough time periods to quantify group structure and individual associations. Here we describe the use of a novel technology, an animal-borne acoustic proximity receiver that records close-spatial associations between free-ranging fish by detection of acoustic signals emitted from transmitters on other individuals. Validation trials, held within enclosures in the natural environment, on juvenile lemon sharks Negaprion brevirostris fitted with external receivers and transmitters, showed receivers logged interactions between individuals regularly when sharks were within 4 m (∼4 body lengths) of each other, but rarely when at 10 m distance. A field trial lasting 17 days with 5 juvenile lemon sharks implanted with proximity receivers showed one receiver successfully recorded association data, demonstrating this shark associated with 9 other juvenile lemon sharks on 128 occasions. This study describes the use of acoustic underwater proximity receivers to quantify interactions among wild sharks, setting the scene for new advances in understanding the social behaviours of marine animals.

Prey selection and functional response of juvenile lemon sharks Negaprion brevirostris

Prey preference of juvenile lemon sharks Negaprion brevirostris was examined in experiments conducted in field-based pens where the fish were offered meals of live teleosts: grey snapper Lutjanus griseus and yellow fin majorra Gerres cinereus in ratios of L. griseus:G. cinereus varying from 10:0 to 2:8. Relative electivity indices for each treatment showed that N. brevirostris preyed on G. cinereus rather than L. griseus. They showed a prey preference relating to density of G. cinereus (type II functional response) but not to L. griseus.

Movement patterns of juvenile lemon sharks Negaprion brevirostris within Atol das Rocas, Brazil: a nursery characterized by tidal extremes

Movement patterns and habitat use of juvenile lemon sharks Negaprion brevirostris were monitored at Atol das Rocas, Brazil, an atypical nursery area for this species, characterized by extreme tides and a lack of seagrass flats and mangroves. Twenty-three sharks carrying transmitters were monitored using an array of bottom-fixed automated receivers during 3 trips over a total of 60 d. Transmitters were recorded on receivers over 13 000 times, and the majority of sharks were detected more than 100 times. Newborn sharks (60 to 80 cm total length, TL) showed restricted but repeated movements between small tide pools on reef flats at low tide and a small, shallow, nearby tidal creek at high tide. Larger sharks (up to 106 cm TL) sampled 6 and 20 mo after the study in March 2000 frequented the tidal creek and several other locations at high tide and a variety of larger pools at low tide, and in general exhibited more extensive movements within the atoll than did newborn sharks. Sharks approaching 2 yr of age were generally observed in specific pools or shallow water locations within the atoll during high and low tides, but also expanded their movements to include more of the atoll. Throughout the study, young lemon sharks appeared to concentrate movements within shal- low-water low-tide refuges and separate high tidal areas. Movement patterns of sharks in Atol das Rocas differ from those at other well-studied lemon shark nursery locations, where individuals con- tinuously occupy shallow flats and mangrove habitats. Nevertheless, lemon sharks in general restrict their movements to shallow-water habitats regardless of the specific nursery area occupied. This behavior is most likely related to predator avoidance. This study provides an example of the inter- action between the physical environment and the biology of animals—in this case, the influence of the physical characteristics of a nursery area and the behavioral ecology of young lemon sharks.

The scarecrow toadfish: habitat, abundance and size at maturity at Bimini, Bahamas

Six scarecrow toadfish Opsanus phobetron were found in the stomachs of five juvenile lemon sharks Negaprion brevirostris, and subsequent sampling yielded 29 O. phobetron specimens from mangroves (45% of toadfish), conch shells (28%), and seagrass beds (25%) around Bimini, Bahamas during the winter. The presence of large numbers of scarecrow toadfish including mature females, when the water temperature was >22° C, suggests that this is a successful breeding tropical population and not a glacial relict.

Effects of capture and transmitter attachments on the swimming speed of large juvenile lemon sharks in the wild

The swimming speed of seven large juvenile lemon sharks Negaprion brevirostris following attachment of an external speed‐sensing ultrasonic transmitter was significantly higher during the first 18 h after release compared to the average swimming speed obtained >48 h after release. The external speed‐sensing transmitter can be used to monitor the voluntary swimming speed of large fishes in the field, but data during the first 24 h period should be excluded from analysis of natural speeds, at least from species similar in behaviour to N. brevirostris.

Survival of Juvenile Lemon Sharks at Bimini, Bahamas, Estimated by Mark–Depletion Experiments

The survival rate of juvenile lemon sharks Negaprion brevirostris in North Sound, Bimini, Bahamas, was estimated by marking a cohort of small sharks (≤53 cm precaudal length) each spring from 1995 to 1999 and by estimating the number of survivors 1 year later by using a depletion method on the marked population. Annual survival rate estimates varied between 38% and 65%, which was somewhat higher than the 39% steady-state survival predicted from a life cycle (Leslie matrix) model. These are the first direct estimates of the survival rate of a juvenile elasmobranch, and the results support modeling efforts that have been used in determining limits to sustainable exploitation of elasmobranchs. Estimates of survival rates in the present study were negatively correlated with estimated initial abundance and are consistent with strong, density-dependent survival.