Translating Marine Animal Tracking Data into Conservation Policy and Management.

There have been efforts around the globe to track individuals of many marine species and assess their movements and distribution, with the putative goal of supporting their conservation and management. Determining whether, and how, tracking data have been successfully applied to address real-world conservation issues is, however, difficult. Here, we compile a broad range of case studies from diverse marine taxa to show how tracking data have helped inform conservation policy and management, including reductions in fisheries bycatch and vessel strikes, and the design and administration of marine protected areas and important habitats. Using these examples, we highlight pathways through which the past and future investment in collecting animal tracking data might be better used to achieve tangible conservation benefits.

The Role of Herbivory in Structuring Tropical Seagrass Ecosystem Service Delivery.

Seagrass meadows support key ecosystem services, via provision of food directly for herbivores, and indirectly to their predators. The importance of herbivores in seagrass meadows has been well-documented, but the links between food webs and ecosystem services in seagrass meadows have not previously been made explicit. Herbivores interact with ecosystem services - including carbon sequestration, cultural values, and coastal protection. Interactions can be positive or negative and depend on a range of factors including the herbivore identity and the grazing type and intensity. There can be unintended consequences from management actions based on a poor understanding of trade-offs that occur with complex seagrass-herbivore interactions. Tropical seagrass meadows support a diversity of grazers spanning the meso-, macro-, and megaherbivore scales. We present a conceptual model to describe how multiple ecosystem services are influenced by herbivore pressure in tropical seagrass meadows. Our model suggests that a balanced ecosystem, incorporating both seagrass and herbivore diversity, is likely to sustain the broadest range of ecosystem services. Our framework suggests the pathway to achieve desired ecosystem services outcomes requires knowledge on four key areas: (1) how size classes of herbivores interact to structure seagrass; (2) desired community and management values; (3) seagrass responses to top-down and bottom-up controls; (4) the pathway from intermediate to final ecosystem services and human benefits. We suggest research should be directed to these areas. Herbivory is a major structuring influence in tropical seagrass systems and needs to be considered for effective management of these critical habitats and their services.

Compensating for geographic variation in detection probability with water depth improves abundance estimates of coastal marine megafauna.

The probability of an aquatic animal being available for detection is typically <1. Accounting for covariates that reduce the probability of detection is important for obtaining robust estimates of the population abundance and determining its status and trends. The dugong (Dugong dugon) is a bottom-feeding marine mammal and a seagrass community specialist. We hypothesized that the probability of a dugong being available for detection is dependent on water depth and that dugongs spend more time underwater in deep-water seagrass habitats than in shallow-water seagrass habitats. We tested this hypothesis by quantifying the depth use of 28 wild dugongs fitted with GPS satellite transmitters and time-depth recorders (TDRs) at three sites with distinct seagrass depth distributions: 1) open waters supporting extensive seagrass meadows to 40 m deep (Torres Strait, 6 dugongs, 2015); 2) a protected bay (average water depth 6.8 m) with extensive shallow seagrass beds (Moreton Bay, 13 dugongs, 2011 and 2012); and 3) a mixture of lagoon, coral and seagrass habitats to 60 m deep (New Caledonia, 9 dugongs, 2013). The fitted instruments were used to measure the times the dugongs spent in the experimentally determined detection zones under various environmental conditions. The estimated probability of detection was applied to aerial survey data previously collected at each location. In general, dugongs were least available for detection in Torres Strait, and the population estimates increased 6-7 fold using depth-specific availability correction factors compared with earlier estimates that assumed homogeneous detection probability across water depth and location. Detection probabilities were higher in Moreton Bay and New Caledonia than Torres Strait because the water transparency in these two locations was much greater than in Torres Strait and the effect of correcting for depth-specific detection probability much less. The methodology has application to visual survey of coastal megafauna including surveys using Unmanned Aerial Vehicles.

A low-cost solution for documenting distribution and abundance of endangered marine fauna and impacts from fisheries.

Fisheries bycatch is a widespread and serious issue that leads to declines of many important and threatened marine species. However, documenting the distribution, abundance, population trends and threats to sparse populations of marine species is often beyond the capacity of developing countries because such work is complex, time consuming and often extremely expensive. We have developed a flexible tool to document spatial distribution and population trends for dugongs and other marine species in the form of an interview questionnaire supported by a structured data upload sheet and a comprehensive project manual. Recognising the effort invested in getting interviewers to remote locations, the questionnaire is comprehensive, but low cost. The questionnaire has already been deployed in 18 countries across the Indo-Pacific region. Project teams spent an average of USD 5,000 per country and obtained large data sets on dugong distribution, trends, catch and bycatch, and threat overlaps. Findings indicated that >50% of respondents had never seen dugongs and that 20% had seen a single dugong in their lifetimes despite living and fishing in areas of known or suspected dugong habitat, suggesting that dugongs occurred in low numbers. Only 3% of respondents had seen mother and calf pairs, indicative of low reproductive output. Dugong hunting was still common in several countries. Gillnets and hook and line were the most common fishing gears, with the greatest mortality caused by gillnets. The questionnaire has also been used to study manatees in the Caribbean, coastal cetaceans along the eastern Gulf of Thailand and western Peninsular Malaysia, and river dolphins in Peru. This questionnaire is a powerful tool for studying distribution and relative abundance for marine species and fishery pressures, and determining potential conservation hotspot areas. We provide the questionnaire and supporting documents for open-access use by the scientific and conservation communities.

Evidence for a postreproductive phase in female false killer whales Pseudorca crassidens.

BACKGROUND: A substantial period of life after reproduction ends, known as postreproductive lifespan (PRLS), is at odds with classical life history theory and its causes and mechanisms have puzzled evolutionary biologists for decades. Prolonged PRLS has been confirmed in only two non-human mammals, both odontocete cetaceans in the family Delphinidae. We investigate the evidence for PRLS in a third species, the false killer whale, Pseudorca crassidens, using a quantitative measure of PRLS and morphological evidence from reproductive tissues. RESULTS: We examined specimens from false killer whales from combined strandings (South Africa, 1981) and harvest (Japan 1979-80) and found morphological evidence of changes in the activity of the ovaries in relation to age. Ovulation had ceased in 50% of whales over 45 years, and all whales over 55 years old had ovaries classified as postreproductive. We also calculated a measure of PRLS, known as postreproductive representation (PrR) as an indication of the effect of inter-population demographic variability. PrR for the combined sample was 0.14, whereas the mean of the simulated distribution for PrR under the null hypothesis of no PRLS was 0.02. The 99th percentile of the simulated distribution was 0.08 and no simulated value exceeded 0.13. These results suggest that PrR was convincingly different from the measures simulated under the null hypothesis. CONCLUSIONS: We found morphological and statistical evidence for PRLS in South African and Japanese pods of false killer whales, suggesting that this species is the third non-human mammal in which this phenomenon has been demonstrated in wild populations. Nonetheless, our estimate for PrR in false killer whales (0.14) is lower than the single values available for the short-finned pilot whale (0.28) and the killer whale (0.22) and is more similar to working Asian elephants (0.13).

Spatial and Temporal Variation in the Effects of Climatic Variables on Dugong Calf Production.

Knowledge of the relationships between environmental forcing and demographic parameters is important for predicting responses from climatic changes and to manage populations effectively. We explore the relationships between the proportion of sea cows (Dugong dugon) classified as calves and four climatic drivers (rainfall anomaly, Southern Oscillation El Niño Index [SOI], NINO 3.4 sea surface temperature index, and number of tropical cyclones) at a range of spatially distinct locations in Queensland, Australia, a region with relatively high dugong density. Dugong and calf data were obtained from standardized aerial surveys conducted along the study region. A range of lagged versions of each of the focal climatic drivers (1 to 4 years) were included in a global model containing the proportion of calves in each population crossed with each of the lagged versions of the climatic drivers to explore relationships. The relative influence of each predictor was estimated via Gibbs variable selection. The relationships between the proportion of dependent calves and the climatic drivers varied spatially and temporally, with climatic drivers influencing calf counts at sub-regional scales. Thus we recommend that the assessment of and management response to indirect climatic threats on dugongs should also occur at sub-regional scales.

Key Questions in Marine Megafauna Movement Ecology.

It is a golden age for animal movement studies and so an opportune time to assess priorities for future work. We assembled 40 experts to identify key questions in this field, focussing on marine megafauna, which include a broad range of birds, mammals, reptiles, and fish. Research on these taxa has both underpinned many of the recent technical developments and led to fundamental discoveries in the field. We show that the questions have broad applicability to other taxa, including terrestrial animals, flying insects, and swimming invertebrates, and, as such, this exercise provides a useful roadmap for targeted deployments and data syntheses that should advance the field of movement ecology.

The User, not the Tool: Perceptions of Credibility and Relevance Affect the Uptake of Prioritisation.

Prioritisation methods have been used in conservation planning for over 20 years. The scientific literature focuses on the technical aspects of prioritisation, providing limited information on factors affecting the uptake of priorities. We focused on the Back on Track species prioritisation program in Queensland, Australia, used to prioritise species conservation efforts across Queensland from 2005. The program had low uptake by intended users. Our study aimed to identify the perceived limitations in the technical-scientific quality of this species-based prioritisation process and its outcomes in terms of credibility (scientific adequacy of the technical evidence) and relevance (of information to the needs of decision-makers). These criteria have been used to understand the uptake of scientific information in policy. We interviewed 73 key informants. Perceptions of credibility were affected by concerns related to the use of expert judgement (rather than empirical evidence) to assess species, impressions that key experts were not included in the planning process, and the lack of confidence in the information supporting prioritisation. We identified several trade-offs and synergies between the credibility and relevance of priorities to potential users. The relevance of the output plans was negatively affected by the lack of clarity about who were potential users and implementers of the priorities identified. We conclude with recommendations to enhance the credibility and relevance of such initiatives.

Discriminating between the vocalizations of Indo-Pacific humpback and Australian snubfin dolphins in Queensland, Australia.

Australian snubfin and Indo-Pacific humpback dolphins co-occur throughout most of their range in coastal waters of tropical Australia. Little is known of their ecology or acoustic repertoires. Vocalizations from humpback and snubfin dolphins were recorded in two locations along the Queensland coast during 2008 and 2010 to describe their vocalizations and evaluate the acoustic differences between these two species. Broad vocalization types were categorized qualitatively. Both species produced click trains burst pulses and whistles. Principal component analysis of the nine acoustic variables extracted from the whistles produced nine principal components that were input into discriminant function analyses to classify 96% of humpback dolphin whistles and about 78% of snubfin dolphin calls correctly. Results indicate clear acoustic differences between the vocal whistle repertoires of these two species. A stepwise routine identified two principal components as significantly distinguishable between whistles of each species: frequency parameters and frequency trend ratio. The capacity to identify these species using acoustic monitoring techniques has the potential to provide information on presence/absence, habitat use and relative abundance for each species.

Satellite tracking of sympatric marine megafauna can inform the biological basis for species co-management.

CONTEXT: Systematic conservation planning is increasingly used to identify priority areas for protection in marine systems. However, ecosystem-based approaches typically use density estimates as surrogates for animal presence and spatial modeling to identify areas for protection and may not take into account daily or seasonal movements of animals. Additionally, sympatric and inter-related species are often managed separately, which may not be cost-effective. This study aims to demonstrate an evidence-based method to inform the biological basis for co-management of two sympatric species, dugongs and green sea turtles. This approach can then be used in conservation planning to delineate areas to maximize species protection. METHODOLOGY/RESULTS: Fast-acquisition satellite telemetry was used to track eleven dugongs and ten green turtles at two geographically distinct foraging locations in Queensland, Australia to evaluate the inter- and intra-species spatial relationships and assess the efficacy of existing protection zones. Home-range analysis and bathymetric modeling were used to determine spatial use and compared with existing protection areas using GIS. Dugong and green turtle home-ranges significantly overlapped in both locations. However, both species used different core areas and differences existed between regions in depth zone use and home-range size, especially for dugongs. Both species used existing protection areas in Shoalwater Bay, but only a single tracked dugong used the existing protection area in Torres Strait. CONCLUSIONS/SIGNIFICANCE: Fast-acquisition satellite telemetry can provide evidence-based information on individual animal movements to delineate relationships between dugongs and green turtles in regions where they co-occur. This information can be used to increase the efficacy of conservation planning and complement more broadly based survey information. These species also use similar habitats, making complimentary co-management possible, but important differences exist between locations making it essential to customize management. This methodology could be applied on a broader scale to include other sympatric and inter-related species.

Positive interactions between irrawaddy dolphins and artisanal fishers in the Chilika Lagoon of eastern India are driven by ecology, socioeconomics, and culture.

In human-dominated landscapes, interactions and perceptions towards wildlife are influenced by multidimensional drivers. Understanding these drivers could prove useful for wildlife conservation. We surveyed the attitudes and perceptions of fishers towards threatened Irrawaddy dolphins (Orcaella brevirostris) at Chilika Lagoon India. To validate the drivers of fisher perceptions, we : (1) observed dolphin foraging behavior at stake nets, and (2) compared catch per unit effort (CPUE) and catch income of fishers from stake nets in the presence and absence of foraging dolphins. We found that fishers were mostly positive towards dolphins, believing that dolphins augmented their fish catch and using culture to express their perceptions. Foraging dolphins were observed spending half their time at stake nets and were associated with significantly higher catch income and CPUE of mullet (Liza sp.), a locally preferred food fish species. Wildlife conservation efforts should use the multidimensional drivers of human-wildlife interactions to involve local stakeholders in management.

Thermal biology of sea snakes and sea kraits.

Temperature probably had no direct effect on the evolution of sea kraits within their center of origin, a geologically stable thermal zone straddling the equator, but may have indirectly affected expansions and contractions in distributions beyond that zone through global fluctuations that caused alternation of higher and lower sea levels. The northern limit of the Laticauda colubrina complex seems to be the 20°C isotherm; in the south, the range does not reach that isotherm because there is no land (also a habitat requirement of sea kraits) within the zone of suitable temperature. The relationship of temperature to the pattern of geographic variation in morphology supports either the hypothesis of peripheral convergence or the developmental hypothesis but does not distinguish between them. Quadratic surfaces relating cumulative scores for coloration and morphological characters to global position showed a strong latitudinal component and an even stronger longitudinal one in which the direction of the latitudinal effect was reversed between east and west. A multivariate analysis revealed that while morphological characters vary significantly by location and climate when tested separately, when the influence of location on morphology is taken into account, no residual relationship between climate and morphology remains. Most marine snakes have mean upper temperature tolerances between 39°C and 40°C and operate at temperatures much nearer their upper thermal limits than their lower limits but still avoid deleterious extremes by diving from excessively hot water to deeper, cooler strata, and by surfacing when water is cold. At the surface in still water in sunlight, Pelamis can maintain its body temperature slightly above that of the water, but whether this is significant in nature is questionable. As temperature falls below 18-20°C, survival time is progressively reduced, accompanied by the successive occurrence of cessation of feeding, cessation of swimming, and failure to orient. Acclimation does not seem to be in this species' repertoire. In the water column, marine snakes track water temperature; on land, sea kraits can thermoregulate by basking, selecting favorable locations, and by kleptothermy. Laticauda colubrina adjusts its reproductive cycle geographically in ways that avoid breeding in the coldest months. Mean voluntary diving time is not temperature-dependent within the normal range of temperatures experienced by marine snakes in the field, but is reduced in water colder than 20°C. On land, much as while diving in the sea, sea kraits maintain long periods of apnea; intervals between breaths are inversely related to temperature.

Informing species conservation at multiple scales using data collected for marine mammal stock assessments.

BACKGROUND: Conservation planning and the design of marine protected areas (MPAs) requires spatially explicit information on the distribution of ecological features. Most species of marine mammals range over large areas and across multiple planning regions. The spatial distributions of marine mammals are difficult to predict using habitat modelling at ecological scales because of insufficient understanding of their habitat needs, however, relevant information may be available from surveys conducted to inform mandatory stock assessments. METHODOLOGY AND RESULTS: We use a 20-year time series of systematic aerial surveys of dugong (Dugong dugong) abundance to create spatially-explicit models of dugong distribution and relative density at the scale of the coastal waters of northeast Australia (∼136,000 km(2)). We interpolated the corrected data at the scale of 2 km * 2 km planning units using geostatistics. Planning units were classified as low, medium, high and very high dugong density on the basis of the relative density of dugongs estimated from the models and a frequency analysis. Torres Strait was identified as the most significant dugong habitat in northeast Australia and the most globally significant habitat known for any member of the Order Sirenia. The models are used by local, State and Federal agencies to inform management decisions related to the Indigenous harvest of dugongs, gill-net fisheries and Australia's National Representative System of Marine Protected Areas. CONCLUSION/SIGNIFICANCE: In this paper we demonstrate that spatially-explicit population models add value to data collected for stock assessments, provide a robust alternative to predictive habitat distribution models, and inform species conservation at multiple scales.

Adaptive management of the Great Barrier Reef: a globally significant demonstration of the benefits of networks of marine reserves.

The Great Barrier Reef (GBR) provides a globally significant demonstration of the effectiveness of large-scale networks of marine reserves in contributing to integrated, adaptive management. Comprehensive review of available evidence shows major, rapid benefits of no-take areas for targeted fish and sharks, in both reef and nonreef habitats, with potential benefits for fisheries as well as biodiversity conservation. Large, mobile species like sharks benefit less than smaller, site-attached fish. Critically, reserves also appear to benefit overall ecosystem health and resilience: outbreaks of coral-eating, crown-of-thorns starfish appear less frequent on no-take reefs, which consequently have higher abundance of coral, the very foundation of reef ecosystems. Effective marine reserves require regular review of compliance: fish abundances in no-entry zones suggest that even no-take zones may be significantly depleted due to poaching. Spatial analyses comparing zoning with seabed biodiversity or dugong distributions illustrate significant benefits from application of best-practice conservation principles in data-poor situations. Increases in the marine reserve network in 2004 affected fishers, but preliminary economic analysis suggests considerable net benefits, in terms of protecting environmental and tourism values. Relative to the revenue generated by reef tourism, current expenditure on protection is minor. Recent implementation of an Outlook Report provides regular, formal review of environmental condition and management and links to policy responses, key aspects of adaptive management. Given the major threat posed by climate change, the expanded network of marine reserves provides a critical and cost-effective contribution to enhancing the resilience of the Great Barrier Reef.

Optimizing allocation of management resources for wildlife.

Allocating money for species conservation on the basis of threatened species listings is not the most cost-effective way of promoting recovery or minimizing extinction rates. Using ecological and social factors in addition to threat categories, we designed a decision-support process to assist policy makers in their allocation of resources for the management of native wildlife and to clarify the considerations leading to a priority listing. Each species is scored on three criteria at the scale of the relevant jurisdiction: (1) threat category, (2) consequences of extinction, and (3) potential for successful recovery. This approach provides opportunity for independent input by policy makers and other stakeholders (who weight the relative importance of the criteria) and scientists (who score the species against the criteria). Thus the process explicitly separates societal values from the technical aspects of the decision-making process while acknowledging the legitimacy of both inputs. We applied our technique to two Australian case studies at different spatial scales: the frogs of Queensland (1,728,000 km(2); 116 species) and the mammals of the Wet Tropics bioregion (18,500 km(2); 96 species). We identified 7 frog and 10 mammal species as priorities for conservation. The frogs included 1 of the 9 species classified as endangered under Queensland legislation, 3 of the 10 species classified as vulnerable, 2 of the 22 species classified as rare, and 1 of the 75 species classified as least concern. The mammals identified included 3 of the 6 species classified as endangered, 1 of the 4 species classified as vulnerable, 5 of the 11 species classified as rare, and 1 of the 75 species classified as least concern. The methods we used to identify species were robust to comparisons across the two taxonomic groups. We concluded that (1) our process facilitates comparisons of data required to make transparent, cost-effective, and strategic management decisions across taxonomic groups and (2) the process should be used to short-list species for further discussion rather than for allocating resources per se.

Corneal avascularity is due to soluble VEGF receptor-1.

Corneal avascularity-the absence of blood vessels in the cornea-is required for optical clarity and optimal vision, and has led to the cornea being widely used for validating pro- and anti-angiogenic therapeutic strategies for many disorders. But the molecular underpinnings of the avascular phenotype have until now remained obscure and are all the more remarkable given the presence in the cornea of vascular endothelial growth factor (VEGF)-A, a potent stimulator of angiogenesis, and the proximity of the cornea to vascularized tissues. Here we show that the cornea expresses soluble VEGF receptor-1 (sVEGFR-1; also known as sflt-1) and that suppression of this endogenous VEGF-A trap by neutralizing antibodies, RNA interference or Cre-lox-mediated gene disruption abolishes corneal avascularity in mice. The spontaneously vascularized corneas of corn1 and Pax6+/- mice and Pax6+/- patients with aniridia are deficient in sflt-1, and recombinant sflt-1 administration restores corneal avascularity in corn1 and Pax6+/- mice. Manatees, the only known creatures uniformly to have vascularized corneas, do not express sflt-1, whereas the avascular corneas of dugongs, also members of the order Sirenia, elephants, the closest extant terrestrial phylogenetic relatives of manatees, and other marine mammals (dolphins and whales) contain sflt-1, indicating that it has a crucial, evolutionarily conserved role. The recognition that sflt-1 is essential for preserving the avascular ambit of the cornea can rationally guide its use as a platform for angiogenic modulators, supports its use in treating neovascular diseases, and might provide insight into the immunological privilege of the cornea.

Dugong grazing and turtle cropping: grazing optimization in tropical seagrass systems?

Grazing by dugongs and cropping by green turtles have the capacity to alter the subsequent nutritional quality of seagrass regrowth. We examined the effects of simulated light and intensive grazing by dugongs and cropping by turtles on eight nutritionally relevant measures of seagrass chemical composition over two regrowth periods (short-term, 1-4 months; long-term, 11-13 months) at two seagrass communities (a mixed species community with Zostera capricorni, Halophila ovalis, Halodule uninervis, Cymodocea rotundata and C. serrulate; and a monospecific bed of Halodule uninervis) in tropical Queensland, Australia. The concentrations of organic matter, total nitrogen, total water-soluble carbohydrates, total starch, neutral detergent fiber, acid detergent fiber, acid lignin, as well as the in vitro dry matter digestibility (IVDMD) were measured in the leaves and below-ground parts of each species using near-infrared reflectance spectroscopy (NIRS). Regrowth of preferred species such as H. ovalis and H. uninervis from simulated intensive dugong grazing after a year exhibited increased (by 35 and 25%, respectively, relative to controls) whole-plant N concentrations. Similarly, regrowth of H. ovalis from simulated turtle cropping showed an increase in the leaf N concentration of 30% after a year. However, these gains are tempered by reductions in starch concentrations and increases in fiber. In the short-term, the N concentrations increased while the fiber concentrations decreased. These data provide experimental support for a grazing optimization view of herbivory in the tropical seagrass system, but with feedback in a different manner. Furthermore, we suggest that in areas where grazing is the only major source of natural disturbance, it is likely that there are potential ecosystem level effects if and when numbers of dugongs and turtles are reduced.

Near-infrared reflectance spectroscopy is a rapid, cost-effective predictor of seagrass nutrients.

Near-infrared reflectance spectroscopy was used to analyze nutrient composition of tropical and subtropical seagrasses in Queensland, Australia, as part of a broader study of impacts of grazing by dugongs on seagrass. Seagrass samples of 10 species were collected, transported to the laboratory, and separated into leaf and root/rhizome fractions. They were dried, ground, and near-infrared spectra (400-2500 nm) were collected. We used partial least-squares regression to develop calibration equations relating spectral data to standard compositional analyses performed in the laboratory. These compositional analyses focused on attributes believed to be important determinants of nutritional quality of marine vertebrate herbivores (nitrogen, organic matter, neutral detergent fiber, acid detergent fiber, lignin, neutral starch, water-soluble carbohydrates, and in vitro dry matter digestibility). Calibration equations for each attribute were developed separately for (1) roots/rhizomes and (2) leaves, irrespective of plant species. An equation that combined both plant parts was equally robust. These studies demonstrated the utility of near-infrared spectroscopy in providing rapid and cost-effective analysis of marine plants, which, in turn, permits a rigorous statistical approach to be applied to studies of foraging by marine herbivores.