Paul D. Cowley

Aquatic animal telemetry: A panoramic window into the underwater world

A brave new world with a wider view Researchers have long attempted to follow animals as they move through their environment. Until relatively recently, however, such efforts were limited to short distances and times in species large enough to carry large batteries and transmitters. New technologies have opened up new frontiers in animal tracking remote data collection. Hussey et al. review the unique directions such efforts have taken for marine systems, while Kays et al. review recent advances for terrestrial species. We have entered a new era of animal ecology, where animals act as both subjects and samplers of their environments. Science, this issue 10.1126/science.1255642, 10.1126/science.aaa2478 BACKGROUND Global aquatic environments are changing profoundly as a result of human actions; consequently, so too are the ways in which organisms are distributing themselves through space and time. Our ability to predict organism and community responses to these alterations will be dependent on knowledge of animal movements, interactions, and how the physiological and environmental processes underlying them shape species distributions. These patterns and processes ultimately structure aquatic ecosystems and provide the wealth of ecosystem services upon which humans depend. Until recently, the vast size, opacity, and dynamic nature of the aquatic realm have impeded our efforts to understand these ecosystems. With rapid technological advancement over the past several decades, a suite of electronic tracking devices (e.g., acoustic and satellite transmitters) that can remotely monitor animals in these challenging environments are now available. Aquatic telemetry technology is rapidly accelerating our ability to observe animal behavior and distribution and, as a consequence, is fundamentally altering our understanding of the structure and function of global aquatic ecosystems. These advances provide the toolbox to define how future global aquatic management practices must evolve. ADVANCES Aquatic telemetry has emerged through technological advances in miniaturization, battery engineering, and software and hardware development, allowing the monitoring of organisms whose habitats range from the poles to the tropics and the photic zone to the abyssal depths. This is enabling the characterization of the horizontal and vertical movements of individuals, populations, and entire communities over scales of meters to tens of thousands of kilometers and over time frames of hours to years and even over the entire lifetimes of individuals. Electronic tags can now be equipped with sensors that measure ambient physical parameters (depth, temperature, conductivity, fluorescence), providing simultaneous monitoring of animals’ environments. By linking telemetry with biologgers (e.g., jaw-motion sensors), it is possible to monitor individual feeding events. In addition, other devices on instrumented animals can communicate with one another, providing insights into predator-prey interactions and social behavior. Coupling telemetry with minute nonlethal biopsy allows understanding of how trophic dynamics, population connectivity, and gene-level basis for organismal health and condition relate to movement. These advances are revolutionizing the scope and scales of questions that can be addressed on the causes and consequences of animal distribution and movement. OUTLOOK Aquatic animal telemetry has advanced rapidly, yet new challenges present themselves in coordination of monitoring across large-spatial scales (ocean basins), data sharing, and data assimilation. The continued advancement of aquatic telemetry lies in establishing and maintaining accessible and cost-effective infrastructure and in promoting multidisciplinary tagging approaches to maximize cost benefits. A united global network and centralized database will provide the mechanism for global telemetry data and will promote a transparent environment for data sharing that will, in turn, increase global communication, scope for collaboration, intellectual advancement, and funding opportunities. An overarching global network will realize the potential of telemetry, which is essential for advancing scientific knowledge and effectively managing globally shared aquatic resources and their ecosystems in the face of mounting human pressures and environmental change. Aquatic telemetry in action. A southern rock lobster (Jasus edwardsii) (A) and a lemon shark (Negaprion brevirostris) (D) fitted with acoustic tags are detected and logged by moored receivers (D) or mobile receivers attached to opportunistic platforms or carried by large animals (C). A juvenile green turtle (Chelonia mydas) (B) fitted with a satellite tag is monitored in real time via orbiting satellites. A grey seal (Halichoerus grypus) “bioprobe” (C), fitted with intercommunicating acoustic and satellite transmitters, transmits and receives data on animal interactions and ocean conditions. The distribution and interactions of aquatic organisms across space and time structure our marine, freshwater, and estuarine ecosystems. Over the past decade, technological advances in telemetry have transformed our ability to observe aquatic animal behavior and movement. These advances are now providing unprecedented ecological insights by connecting animal movements with measures of their physiology and environment. These developments are revolutionizing the scope and scale of questions that can be asked about the causes and consequences of movement and are redefining how we view and manage individuals, populations, and entire ecosystems. The next advance in aquatic telemetry will be the development of a global collaborative effort to facilitate infrastructure and data sharing and management over scales not previously possible.

The Influence of Selected Environmental Variables on Fish Assemblage Structure in a Range of Southeast African Estuaries

This study compared the ichthyofaunal assemblages in 10 Eastern Cape Province, South Africa, estuaries to identify whether there were any structural variations between the assemblages and to determine the environmental and physical factors linked to these variations. Species belonging to both the marine migrant and estuarine resident groups, by consistent representation within each estuary grouping, were responsible for the separation of fish assemblage structures between the different types of systems. The data further revealed that fish assemblages in the three main types of estuaries investigated were distinct, linked primarily to estuary mouth status and estuary size.

A multidisciplinary study of a small, temporarily open/closed South African estuary, with particular emphasis on the influence of mouth state on the ecology of the system

In 2005/2006 a multidisciplinary research programme that included studies on the hydrodynamics, sediment dynamics, macronutrients, microalgae, macrophytes, zoobenthos, hyperbenthos, zooplankton, ichthyoplankton, fish and birds of the temporarily open/closed East Kleinemonde Estuary was conducted. Particular attention was given to the responses of the different ecosystem components to the opening and closing of the estuary mouth and how this is driven by both riverine and marine events. Using a complementary dataset of daily estuary mouth conditions spanning a 14-year period, five distinct phases of the estuary were identified, including closed (average = 90% of the days), outflow (<1%), tidal (9%) and semi-closed (<1%). The open-mouth phase is critical for the movements of a number of estuary-associated fish (e.g. Rhabdosargus holubi) and invertebrates (e.g. Scylla serrata) between the estuary and sea. The timing of this open phase has a direct influence on the ability of certain estuaryassociated fish (e.g. Lithognathus lithognathus) and invertebrates (e.g. Palaemon peringueyi) to successfully recruit into the system, with a spring opening (October/November) being regarded as optimal for most species. The type of mouth-breaching event and outflow phase is also important in terms of the subsequent salinity regime once the berm barrier forms. A deep mouth breaching following a large river flood tends to result in major tidal inputs of marine water prior to mouth closure and therefore higher salinities (15–25). Conversely, a shallow mouth breaching with reduced tidal exchange during the open phase often leads to a much lower salinity regime at the time of mouth closure (5–15). The biota, especially the submerged macrophytes, respond very differently to the above two scenarios, with Ruppia cirrhosa benefiting from the former and Potamogeton pectinatus from the latter. River flooding and the associated outflow of large volumes of water through the estuary can result in major declines in zooplankton, zoobenthos, hyperbenthos and fish populations during this phase. However, this resetting of the estuary is necessary because certain marine invertebrate and fish species are dependent on the opening of the estuary mouth in order to facilitate recruitment of larvae and post-larvae into the system from the sea. Slight increases in the numbers of certain piscivorous and resident wading bird species were recorded when the estuary mouth opened, possibly linked to increased feeding opportunities during that phase.

A preliminary investigation of the feeding ecology of skates (Batoidea: Rajidae) off the west coast of southern Africa

The diets of 14 species of skates (Rajiformes: Rajidae) collected along the coast of South-Western Africa between Walvis Bay and Cape Agulhas over a depth range of 50–1 016 m were analysed. Two distinct communities of skates could be recognized on the basis of depth zonation, the boundary between these communities being at approximately 380 m water depth. These two skate communities have similar species components: the so-called biscuit skate community (the shallow one) has two crustacean specialists (Cruriraja parcomaculata, Raja wallacei), one fish specialist (R. alba) and two generalists (R. pullopunctata, R. cf. clavata); the so-named grey skate community has two crustacean specialists (Raja caudaspinosa, R. confundens) and two generalists (Bathyraja smithii, R. leopardus). The grey skate community appears to be a more complex and dynamic assemblage with higher diversity (at least 13 species) than the biscuit skate community (five species). In both communities the most common prey items were crustacea...

Distribution of offshore demersal cartilaginous fish (Class Chondrichthyes) off the west coast of southern Africa, with notes on their systematics

The geographic and the bathymetric distribution of offshore demersal cartilaginous fish off the west coast of southern Africa are reviewed. The results were collected during 12 cruises of F.R.S. Africana between 1986 and 1990. The area covered was between Walvis Bay (23°S, 14°E) and the Agulhas Bank west of Cape Agulhas (36°S, 20°E) over a depth range of 33–1 016 m. In all, 55 species of cartilaginous fish were collected, including 32 sharks, 17 rays and six chimaeras, on 869 stations and representing 3 092 station records. Computer-generated maps and station lists are presented for the species in the sample, and the distribution records, including records from the literature, are reviewed and discussed for these species and 12 more demersal species not collected during the survey. The survey revealed many range extensions for described species. West Coast demersal cartilaginous fish show zonation by depth and latitude, and groups of species with similar depth and latitudinal distributions were apparent. ...

A preliminary investigation of the feeding ecology of squaloid sharks off the west coast of southern Africa

The diets of 15 species of squaloid sharks caught between Walvis Bay and Cape Agulhas over a depth range of 50–1 016 m are analysed. The most common prey items were fish and cephalopods. Hake Merluccius spp. were common in the diets of Centrophorus squamosus, Squalus acanthias, and S. cf. mitsukurii. Myctophids were extensively preyed on by Centroscyllium fabricii, Deania calcea, D. profundorum, Etmopterus cf. brachyurus, E. compagnoi, S. acanthias and S. megalops, among others. The most common cephalopods in shark stomachs were Histioteuthis miranda, Lycoteuthis ?diadema, Octopus vulgaris and Todarodes angolensis. Crustaceans were uncommon prey of most species, except for Centroscyllium fabricii and Etmopterus cf. granulosus. Centroscymnus coelolepis was the only squaloid with cetacean remains in the stomach. That species appears to parasitize its cetacean victims.

Fish communities in temporarily open/closed estuaries from the warm- and cool-temperate regions of South Africa: A review

The majority of estuaries along the coastline of southern Africa are termed temporarily open/closed estuaries (TOCEs) and are closed off from the sea for varying periods by a sandbar which forms at the mouth. It is therefore important to understand the processes occurring within TOCEs and their importance to fishes in order to make sound management recommendations. Estuaries along the coast of South Africa and their associated fish assemblages are biogeographically distinct and occur in either a subtropical, warm-temperate or cool-temperate zone. There are 125 TOCEs found within the cool-temperate and warm-temperate zones. Most fish species found in TOCEs are the juveniles of marine taxa that breed at sea. Permanently open estuaries generally have a higher diversity of species than TOCEs, but TOCEs still provide important nursery areas for many marine species and numerically often have a higher proportion of estuarine resident species. Important taxa in terms of abundance and biomass in warm-temperate TOCEs include the sparids Rhabdosargus holubi and Lithognathus lithognathus, several mugilid species, estuarine residents (particularly Gilchristella aestuaria and Atherina breviceps) and the freshwater cichlid Oreochromis mossambicus. The diversity of fishes in cool-temperate TOCEs is low when compared with warm-temperate systems and Liza richardsonii tends to dominate catches by number and mass in most systems. Several species recorded in TOCEs show clear longitudinal distribution trends. For example Atherina breviceps is generally more abundant in the lower reaches of estuaries. Mouth state, particularly the frequency, timing and duration of mouth opening plays a key role in determining species richness, composition, diversity and abundance in TOCEs. Mouth state is directly linked to freshwater input. Reduced river inflow leads to prolonged mouth closure and shorter open phases, which inhibits immigration and emigration of marine fish species between estuaries and the sea. Understanding of the effects of various processes occurring within these systems, particularly variation in freshwater input, on the biota of these important systems facilitates the development of informed management recommendations.

Diet, feeding behaviour and habitat utilisation of the blue stingray Dasyatis chrysonota (Smith, 1828) in South African waters

Analysis of stomach contents for Dasyatis chrysonota revealed that diet varied with size and habitat. The diet of all size classes in the surf zone was comprised primarily of Callianassa spp., Donax spp. and unidentified polychaete species. The medium and large size classes fed primarily on Donax spp., whereas the very large size class fed mainly on Callianassa spp. Polychaetes were of secondary importance as prey for the medium size class. The diet of D. chrysonota in the nearshore zone consisted mainly of Balanoglossus capensis and Callianassa spp. Balanoglossus capensis decreased from an index of relative importance (IRI) of 75.3% for the medium size class to 59.9% for the very large size class, whereas Callianassa spp. increased from 22.8% to 39.4% between the medium and the very large size classes. The offshore zone was the only area in which small size class D. chrysonota were caught. The diet of these small D. chrysonota was primarily polychaetes and amphipods. Polychaetes increased in importance in the medium size class, but declined in each successively larger size class. Conversely, Pterygosquilla armata capensis became the single most important prey item for the very large size class, comprising an IRI of 50.9%. The behaviour pattern used by D. chrysonota to locate and extract prey is described.

Estuarine habitat use by juvenile dusky kob Argyrosomus japonicus (Sciaenidae), with implications for management

The spatial and temporal area-use patterns of estuarine-dependent juvenile dusky kob Argyrosomus japonicus in the Great Fish Estuary, South Africa, were examined using acoustic telemetry. In all, 29 individuals (307–400 mm total length) were surgically equipped with individually coded transmitters and monitored for a period of up to 195 days using an array of 11 moored data-logging acoustic receivers. Tagged dusky kob spent most time in the estuary (84%), compared with neighbouring marine (13%) and riverine (4%) environments. Tagged fish made extensive use of the estuary from the mouth to between 6.4 km and 10.3 km upstream, and spent approximately equal proportions of time at each of the seven receivers located between 0.5 km and 6.5 km from the mouth. A total of 18 fish undertook sea trips of a mean duration of 3.5 days, whereas three individuals made riverine excursions (mean duration = 7.3 days). A total of 12 (41%) tagged fish was captured in the estuary prior to, during or after the monitoring period. These findings highlight the importance of estuaries as critical nursery areas, and that the use of these habitats by dusky kob should be better reflected in the management arrangements for this fishery species.

Crossing Invisible Boundaries: the Effectiveness of the Langebaan Lagoon Marine Protected Area as a Harvest Refuge for a Migratory Fish Species in South Africa

The application of no-take areas in fisheries remains controversial. Critics argue that many targeted species are too mobile to benefit from area protection and that no-take areas are only appropriate for resident species. The degree of protection does not depend on the size of the no-take area but rather on the time fish reside inside its boundaries during key life-history events (i.e., spawning) and during periods of peak fishing activity. We evaluated the potential of a small no-take marine protected area (MPA) inside a coastal embayment as a harvest refuge for a mobile, possibly migratory, long-lived fish species. We used acoustic telemetry to track movements of 30 transmitter-tagged white stumpnose (Rhabdosargus globiceps) across and on both sides of the boundary of a small (34 km(2)) no-take area over a full year. Being landlocked on 3 sides, the location of the MPA inside the lagoon made it practical to detect all boundary crossings and to calculate the time individual fish used the MPA. We detected frequent movements across the boundary, with strong seasonal and individual variations. There were significant differences in MPA use patterns between fish from different release areas. The time spent in the MPA by individual fish during summer (mean 50%; max 98%) was out of proportion with the size of that area (4% of total habitat). Summer coincided with peak recreational fishing activity and with the spawning season of this species. The small MPA provided a refuge for a part of the spawning stock of white stumpnose. Our findings suggest that if strategically placed, a small no-take area can be effective in protecting mobile species and that models of spillover from no-take areas should account for seasonal and individual variation in area use and the spatiotemporal distribution of fish and fishers.