Two’s company, three’s a crowd: fine-scale habitat partitioning by depth among sympatric species of marine mesopredator

A sympatric assemblage of morphologically similar predators is expected to exhibit fine-scale habitat segregation, or resource partitioning, to reduce the effects of direct competition. This principle has been well studied for predators in terrestrial ecosystems. In the marine environment, the fine-scale spatial segregation of sympatric species of large predators is poorly understood because detailed movement and behavioural data are often not available across multiple species within the same timeframe. The ways in which co-occurring congeneric predators separate spatially is even less well understood. Medium-sized species of skates (genus Raja) co-occur in temperate habitats of the north-east Atlantic Ocean, share similar morphologies and have distributional ranges that overlap significantly in the western English Channel ecosystem. In the present study, detailed depth time series retrieved from 89 electronic data storage tags attached to 4 species of skate were analysed to determine preferred depth ranges. The 4 species were found to segregate spatially into 2 groups, with one group having a significantly shallower core annual depth range than the other. To our knowledge, fine-scale segregation by depth has not been observed previously. Interestingly, the members of each species group appeared complementary, each group comprising species with different dietary preferences and with a larger and smaller body size. An understanding of how core depth ranges differ and how these species utilise vertical habitat could potentially enable geographic ranges around the coast to be predicted, with important implications for how these species interact with fisheries and Marine Protected Areas

A method for long-term electronic tagging and tracking of juvenile and adult European common cuttlefish Sepia officinalis

The physiology and behaviour of captive cuttlefish have been well studied over recent decades and yet very few parallel studies have investigated the movements and behaviour of free-ranging animals. One reason for this gap is that methods for longer term tracking are not well developed for the majority of species, especially those of smaller size. In this study we describe a methodology for the long-term attachment of electronic tags to free-ranging cuttlefish of a broad size range. Five common cuttlefish Sepia officinalis (122–240 mm mantle length) were fitted with temperature and depth-logging archival tags attached to the internal cuttlebone of the living animal (tag weight was < 1.8% of body weight). Tagged animals recovered rapidly from sedative and surgical procedures and resumed feeding within 24 h of tag attachment. Laboratory-kept cuttlefish maintained in a 2-m deep aquarium exhibited diel vertical movements, spending daylight hours close to the bottom and ascending into the water column at night, a behaviour which is consistent with normal diel vertical migration seen in other marine organisms such as zooplankton and fish. That regular feeding and expected patterns of depth use were observed indicates that tag attachment did not impede normal behaviours. Furthermore, tags remained attached to laboratory cuttlefish for up to 5 months, from first tagging through to natural mortality, and with the tag remaining attached to the cuttlebone post mortem. We also found that cuttlebones with attached tags remained buoyant at the water's surface post mortem, offering the unique opportunity to recover archival tags from cuttlebones washed ashore. The capacity for long-term attachment to juvenile cuttlefish and recovery following natural mortality identifies the potential of this method for recording near ‘lifetime’ behaviour and movements of cuttlefish in their natural environment

Data from: Year-round sexual harassment as a behavioral mediator of vertebrate population dynamics

Within-species sexual segregation is a widespread phenomenon among vertebrates but its causes remain a topic of much debate. Female avoidance of male coercive mating attempts has the potential to influence the social structure of animal populations, yet it has been largely overlooked as a driver of sexual separation. Indeed, its potential role in long-term structuring of natural populations has not been studied. Here we use a comparative approach to examine the suitability of multiple hypotheses forwarded to account for sexual segregation (i.e. activity budget; predation risk; thermal niche - fecundity; and social factors) as drivers underlying sex-specific habitat use in a monomorphic model vertebrate, the small spotted catshark, Scyliorhinus canicula. Using this hypothesis-driven approach we show that year-round sexual habitat segregation in S. canicula can be accounted for directly by female avoidance of male sexual harassment. Long-term electronic tracking reveals sperm-storing female catsharks form daytime refuging aggregations in shallow water caves (~3.2 m water depth), and undertake nocturnal foraging excursions into deeper water (~25 m) most nights. In contrast, males occupy deeper, cooler habitat (~18 m) by day, and exploit a range of depths nocturnally (1 - 23 m). Males frequent the locations of shallow water female refuges, apparently intercepting females for mating when they emerge from, and return to, refuges on foraging excursions. Females partly compensate for higher metabolic costs incurred when refuging in warmer habitat by remaining inactive; however, egg production rates decline in the warmest months, but despite this, refuging behavior is not abandoned. Thermal choice experiments confirm individual females are willing to &#39;pay&#39; in energy terms to avoid aggressive males and unsolicited male mating attempts. Long-term evasion of sexual harassment influences both the social structure and fecundity of the study population with females trading-off potential injury and unsolicited matings with longer term fitness. This identifies sexual harassment as a persistent cost to females that can mediate vertebrate population dynamics.,11-2052 dataMS Excel spreadsheet containing data obtained under natural (field) and controlled (laboratory) conditions. Individual S. canicula were electronically tracked in the natural environment, whilst in the laboratory the movements of individuals were tracked using video tracking techniques. Observations made under both natural and controlled conditions are also included. See manuscript materials and methods for further details.,</span

Movements and behaviour of European common cuttlefish Sepia officinalis in English Channel inshore waters first results from acoustic telemetry /

The increasing importance of the European common cuttlefish Sepia officinalis as a commercial fishery resource raises concerns that our limited understanding of its behaviour and movements in natural habitats may impede future management for this species. Whilst information regarding the fine-scale movements and behaviour of small marine species such as cuttlefish can be difficult to obtain, the increasing miniaturisation of electronic tags, combined with novel attachment techniques, has now enabled tracking of this cephalopod. In this study we describe the first use of electronic tags attached to adult and sub-adult S. officinalis to monitor their movements and behaviour within natural environments. Eight adults (170–205 mm dorsal mantle length [DML]) were fitted with continuous acoustic transmitters and ten sub-adults (132–180 mm DML) were fitted with coded acoustic transmitters. All transmitters were attached to the internal cuttlebone of the living animal. Tagged animals recovered rapidly from anaesthesia and surgical procedures and were found to retain tags for periods of up to 11 weeks in this short-term study. Six of the eight adult cuttlefish released into a radio–acoustic positioning (VRAP) array left the area rapidly (≤ 45 min) whilst two remained for multiple days (≤ 9 days). Short-term site fidelity at a local level was observed in only two adults, whilst larger scale movements along the coastline (≤ 35 km) occurred in three adults, indicating that a complex range of spatial behaviour patterns could occur among spawning adults. Similar patterns were observed in the space use of sub-adults monitored using a passive acoustic-receiver array on the seabed. Three sub-adults were detected within the study area over an extended period of time (≥ 73 days), whilst the remaining sub-adults left the study area rapidly and without return. The capacity to monitor the movements of both adult and sub-adult cuttlefish in their natural environment will facilitate identification and understanding of ontogenic changes in behaviours and migratory patterns of wild populations. Our results highlight the potential of electronic tagging methods as tools to aid conservation and management of this important commercial fishery species in the future

Hunt warm, rest cool: bioenergetic strategy underlying diel\ud vertical migration of a benthic shark

Diel vertical migration (DVM) is a widespread phenomenon among marine and freshwater organisms and many studies with various taxa have sought to understand its adaptive significance. Among crustacean zooplankton and juveniles of some fish species DVM is accepted widely as an antipredator behaviour, but little is known about its adaptive value for relatively large-bodied, adult predatory fish such as sharks. Moreover, the majority of studies have focused on pelagic forms, which raises the question of whether DVM occurs in bottom-living predators.\ud \ud To investigate DVM in benthic predatory fish in the marine environment and to determine why it might occur we tracked movements of adult male dogfish (Scyliorhinus canicula) by short- and long-term acoustic and archival telemetry. Movement studies were complemented with measurements of prey abundance and availability and thermal habitat within home ranges. A thermal choice experiment and energy budget modelling was used to investigate trade-offs between foraging and thermal habitat selection.\ud \ud Male dogfish undertook normal DVM (nocturnal ascent) within relatively small home ranges (∼100 × 100 m) comprising along-bottom movements up submarine slopes from deeper, colder waters occupied during the day into warmer, shallow prey-rich areas above the thermocline at night. Few daytime vertical movements occurred. Levels of activity were higher during the night above the thermocline compared to below it during the day indicating they foraged in warm water and rested in colder depths.\ud \ud A thermal choice experiment using environmentally realistic temperatures supported the field observation that dogfish positively avoided warmer water even when it was associated with greater food availability. Males in laboratory aquaria moved into warm water from a cooler refuge only to obtain food, and after food consumption they preferred to rest and digest in cooler water.\ud \ud Modelling of energy budgets under different realistic thermal-choice scenarios indicated dogfish adopting a 'hunt warm − rest cool' strategy could lower daily energy costs by just over 4%. Our results provide the first clear evidence that are consistent with the hypothesis that a benthic marine-fish predator utilizes DVM as an energy conservation strategy that increases bioenergetic efficiency

Scaling laws of marine predator search behaviour

Many free- ranging predators have to make foraging decisions with little, if any, knowledge of present resource distribution and availability(1). The optimal search strategy they should use to maximize encounter rates with prey in heterogeneous natural environments remains a largely unresolved issue in ecology(1-3). Levy walks(4) are specialized random walks giving rise to fractal movement trajectories that may represent an optimal solution for searching complex landscapes(5). However, the adaptive significance of this putative strategy in response to natural prey distributions remains untested(6,7). Here we analyse over a million movement displacements recorded from animal- attached electronic tags to show that diverse marine predators - sharks, bony fishes, sea turtles and penguins - exhibit Levy- walk- like behaviour close to a theoretical optimum(2). Prey density distributions also display Levy- like fractal patterns, suggesting response movements by predators to prey distributions. Simulations show that predators have higher encounter rates when adopting Levy- type foraging in natural- like prey fields compared with purely random landscapes. This is consistent with the hypothesis that observed search patterns are adapted to observed statistical patterns of the landscape. This may explain why Levy- like behaviour seems to be widespread among diverse organisms(3), from microbes(8) to humans(9), as a `rule' that evolved in response to patchy resource distributions.</p

Molecular markers reveal spatially segregated cryptic species in a critically endangered fish, the common skate (Dipturus batis)

Many sharks and skates are particularly vulnerable to overfishing because of their large size, slow growth, late maturity and low fecundity. In Europe dramatic population declines have taken place in common skate (Dipturus batis L.), one of the largest demersal fish in regional shelf seas, leading to extirpations from substantial parts of its former range. Here we report the discovery of cryptic species in common skate collected from the northeast Atlantic continental shelf. Data from nuclear microsatellite markers indicated two clearly distinct clades and phylogenetic analysis of mitochondrial DNA sequences demonstrated monophyly of each one of them. Capture locations showed evidence of strong spatial segregation, with one taxon occurring mainly in waters off the southern British Isles and around Rockall, while the other was restricted to more northerly shelf waters. These apparently cryptic species showed overlapping substrate and depth preferences, but distributional limits were closely related to temperature gradients, potentially indicating thermal limits to their distributions. This discovery of hidden diversity within a large, critically endangered marine vertebrate demonstrates how marine biodiversity can be underestimated, even in such a relatively well-studied and heavily exploited region

Environmental context explains Lévy and Brownian movement patterns of marine predators

An optimal search theory, the so-called Lévy-flight foraging hypothesis, predicts that predators should adopt search strategies known as Lévy flights where prey is sparse and distributed unpredictably, but that Brownian movement is sufficiently efficient for locating abundant prey. Empirical studies have generated controversy because the accuracy of statistical methods that have been used to identify Lévy behaviour has recently been questioned. Consequently, whether foragers exhibit Lévy flights in the wild remains unclear. Crucially, moreover, it has not been tested whether observed movement patterns across natural landscapes having different expected resource distributions conform to the theory’s central predictions. Here we use maximum-likelihood methods to test for Lévy patterns in relation to environmental gradients in the largest animal movement data set assembled for this purpose. Strong support was found for Lévy search patterns across 14 species of open-ocean predatory fish (sharks, tuna, billfish and ocean sunfish), with some individuals switching between Lévy and Brownian movement as they traversed different habitat types. We tested the spatial occurrence of these two principal patterns and found Lévy behaviour to be associated with less productive waters (sparser prey) and Brownian movements to be associated with productive shelf or convergence-front habitats (abundant prey). These results are consistent with the Lévy-flight foraging hypothesis1, supporting the contention that organism search strategies naturally evolved in such a way that they exploit optimal Lévy patterns.<br/

Scaling laws of marine predator search behaviour

Many free-ranging predators have to make foraging decisions with little, if any, knowledge of present resource distribution and availability1. The optimal search strategy they should use to maximize encounter rates with prey in heterogeneous natural environments remains a largely unresolved issue in ecology1, 2, 3. Lévy walks4 are specialized random walks giving rise to fractal movement trajectories that may represent an optimal solution for searching complex landscapes5. However, the adaptive significance of this putative strategy in response to natural prey distributions remains untested6, 7. Here we analyse over a million movement displacements recorded from animal-attached electronic tags to show that diverse marine predators—sharks, bony fishes, sea turtles and penguins—exhibit Lévy-walk-like behaviour close to a theoretical optimum2. Prey density distributions also display Lévy-like fractal patterns, suggesting response movements by predators to prey distributions. Simulations show that predators have higher encounter rates when adopting Lévy-type foraging in natural-like prey fields compared with purely random landscapes. This is consistent with the hypothesis that observed search patterns are adapted to observed statistical patterns of the landscape. This may explain why Lévy-like behaviour seems to be widespread among diverse organisms3, from microbes8 to humans9, as a 'rule' that evolved in response to patchy resource distributions.<br/