Characterization of highly informative cross-species microsatellite panels for the Australian dugong (Dugong dugon) and Florida manatee (Trichechus manatus latirostris) including five novel primers

The Australian dugong (Dugong dugon) and Florida manatee (Trichechus manatus latirostris) are threatened species of aquatic mammals in the order Sirenia. Sirenian conservation and management actions would benefit from a more complete understanding of genetic diversity and population structure. Generally, species-specific microsatellite markers are employed in conservation genetic studies; however, robust markers can be difficult and costly to isolate. To increase the number of available markers, dugong and manatee microsatellite primers were evaluated for cross-species amplification. Furthermore, one manatee and four dugong novel primers are reported. After polymerase chain reaction optimization, 23 (92%) manatee primers successfully amplified dugong DNA, of which 11 (48%) were polymorphic. Of the 32 dugong primers tested, 27 (84%) yielded product in the manatee, of which 17 (63%) were polymorphic. Dugong and manatee primers were compared and the most informative markers were selected to create robust and informative marker-panels for each species. These cross-species microsatellite marker-panels can be employed to assess other sirenian populations and can provide beneficial information for the protection and management of these unique mammals.     

海南省儒艮资源现状调查

为拟在海南省建立儒艮自然保护区提供科学依据,于2001 年11 月至2002 年10 月在海南省西部沿岸海域进行了为期一年的海洋环境综合调查和儒艮海上目视调查。此外还在海南省及广西壮族自治区、广东省进行了有关访问调查。调查结果表明,在广西沿岸合浦海域仍有儒艮存在。但在海南省西海域近岸未发现儒艮,且原有儒艮栖息地的海草均被破坏消失,认为目前建立海南儒艮自然保护区的条件尚不成熟。儒艮资源减少的主要原因是受人类活动加剧的影响,以及生态环境不断恶化,威胁着本种的生存。为此,亟待采取有效的管理措施和健全管理机制,加强对儒艮资源及其栖息地的保护。     

海南文昌椰林湾发现儒艮的尸体及死亡原因分析

<正>儒艮(Dugong dugon)隶属海牛目(Sirenia)儒艮科(Dugongidae)。广泛分布于印度洋、西太平洋热带及亚热带的大陆沿岸水域和岛屿间(周开亚等,2001),我国分布于广西、海南、广东和台湾省南部的沿岸海域,海南记录于东方北黎湾、儋州白马井洋浦港、澄迈东水港等地(王丕烈和孙建运,1986;周开亚等,2003;王丕烈等,2007)。     

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 km²). 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.     

Long-Term Occupancy Trends in a Data-Poor Dugong Population in the Andaman and Nicobar Archipelago

Prioritizing efforts for conserving rare and threatened species with limited past data and lacking population estimates is predicated on robust assessments of their occupancy rates. This is particularly challenging for elusive, long-lived and wide-ranging marine mammals. In this paper we estimate trends in long-term (over 50years) occupancy, persistence and extinction of a vulnerable and data-poor dugong (Dugong dugon) population across multiple seagrass meadows in the Andaman and Nicobar archipelago (India). For this we use hierarchical Bayesian dynamic occupancy models accounting for false negatives (detection probability<1), persistence and extinction, to two datasets: a) fragmentary long-term occurrence records from multiple sources (1959–2004, n = 40 locations), and b) systematic detection/non-detection data from current surveys (2010–2012, n = 57). Dugong occupancy across the archipelago declined by 60% (from 0.45 to 0.18) over the last 20 years and present distribution was largely restricted to sheltered bays and channels with seagrass meadows dominated by Halophila and Halodule sp. Dugongs were not found in patchy meadows with low seagrass cover. In general, seagrass habitat availability was not limiting for dugong occupancy, suggesting that anthropogenic factors such as entanglement in gillnets and direct hunting may have led to local extinction of dugongs from locations where extensive seagrass meadows still thrive. Effective management of these remnant dugong populations will require a multi-pronged approach, involving 1) protection of areas where dugongs still persist, 2) monitoring of seagrass habitats that dugongs could recolonize, 3) reducing gillnet use in areas used by dugongs, and 4) engaging with indigenous/settler communities to reduce impacts of hunting.     

Dugong habitat use in relation to seagrass nutrients,tides, and diel cycles

The dugong is the only herbivorous mammal that is strictly marine and a seagrass community specialist. The pasture available to the dugong varies with the tides because seagrass occurs in both intertidal and subtidal areas. We GPS-tracked seven dugongs within a 24 km², intensively used seagrass habitat in subtropical Australia in winter. We modeled resource selection within the habitat by comparing the dugongs’ use of space with the distribution of seagrass in an area defined using the combined space-use of the tracked animals. Selection by dugongs for seagrass quantity (biomass) and quality (nutrients) was analyzed within six time/tide combinations to examine the influences of tidal periodicity and the diel cycle on resource selection. Dugong habitat use was consistently centered over seagrass patches with high nitrogen concentrations, except during the day at low tides when the animals had fewer habitat choices and their space use was centered over high seagrass biomass. The association of dugongs with seagrass high in starch was positive during both day and night high tides when the animals could access the intertidal areas where seagrass biomass was generally low. Associations between dugongs and seagrass species were less definite, reflecting the potential for dugongs to exploit several species. Our model of dugong resource selection suggests that nitrogen is the primary limiting nutrient for dugong populations and also confirms the preference of dugongs for high-energy foods.     

Age and growth of grey triggerfish Balistes capriscus from trans-Atlantic populations

Anthropogenic factors that negatively impact reef fishes can include changes in life-history patterns of fisheries-targeted species. Understanding these impacts on growth and population age structure is essential in the management of exploited populations of fishes. This is the first study to directly compare age and growth for a major fisheries species between east and west populations of a transatlantic reef fish. The main goal of this study was to document age and growth in grey triggerfish Balistes capriscus from coastal waters of Ghana in the Gulf of Guinea (GOG) and compare those with the previous growth studies from that region and with the western Atlantic population. A secondary objective of this study was to evaluate the use of otoliths to age triggerfish and to provide a preliminary comparison with spine-derived age estimates. The results obtained from this study provided an updated understanding of the growth and age structure of the eastern B. capriscus population in GOG. The authors documented that shifts in population attributes occurred for B. capriscus after its major decline in abundance. The differences in physical and biotic characteristics of the East and West Atlantic regions and the differences in collection methods of samples make direct comparisons of growth parameters difficult. Nonetheless, overall differences in maximum sizes and ages were apparent; the western Atlantic population had a larger maximum size and older maximum age. The authors also documented that sagittal otoliths can be used to provide age estimates for triggerfish species, and otoliths as an ageing structure had better between-reader precision compared to dorsal spines.     

THE STATUS OF THE DUGONG (DUGONG DUGON MOLLER); KENYA, 1961

The scarcity of dugong (Dugong dugon Miiller) throughout their former range and lack of knowledge of the species' ecology justifies this record of the opinions of the fishermen in the Lamu district of Kenya, where the species is still plentiful. The area and the programme of questioning are described. The social life, reproduction, movements and predators of the dugong are recorded as reported by the fishermen. The present distribution is contrasted with the past. My observations on the food plants and their distribution are given, as well as the fishermen's estimation of the part each plays in the dugong's diet. The need for calm water over feeding grounds, afforded by depth of water or shelter from winds, seems to be a controlling factor in the distribution of dugong. Man appears to be the main predator.     

Improving population estimates by quantifying diving and surfacing patterns: A dugong example

Diving animals are available for detection from above the water when environmental conditions are favorable and the animals are near the surface. The number of animals that are unavailable for detection needs to be estimated to obtain unbiased population estimates. The current availability correction factors used in aerial surveys for the dugong (Dugong dugon) allow for variation in environmental conditions but use the average time dugongs spend near the surface (i.e., constant availability corrections). To improve availability estimates, we examined location and dive data from nine dugongs fitted with satellite telemetry units and time‐depth recorders (TDRs) in eastern Australia. The effects of water depth, tidal conditions, and habitat types on dugong surfacing time were examined using generalized linear mixed models (GLMMs). We found that availability for detection differed with water depth, and depth‐specific availability estimates were often lower than the constant estimates. The habitat effect was less influential, and there was no tidal effect. The number of dugongs estimated using depth‐specific availabilities were higher than those obtained using constant availabilities across water depth. Hence, information on water depth can refine availability estimates and subsequent abundance estimates from dugong aerial surveys. The methodology may be applicable to other aquatic wildlife.     

Effects of Tidal and Diel Cycles on Dugong Habitat Use

ABSTRACT Quantifying the factors influencing behaviors of aquatic mammalian grazers may enhance the generic understanding of grazer ecology. We investigated diel and tidal patterns in movements of the dugong (Dugong dugon) by Global Positioning System—tracking 12 animals in 5 inshore—intertidal and 3 offshore—subtidal habitats along the coast of Queensland, Australia. We examined effects of tide height and time of day on the dugong's distance from 1) the nearest coast, 2) water >3 m deep, 3) actual water depth (bathymetry + tide ht) experienced, and 4) distribution of the directions of movements. Both tidal and diel cycles influenced dugong movement. Tracked dugongs tended to be closer to shore at high tide than at low tide and closer to shore at night than during the day. Onshore movement was more prevalent on incoming tides and in the afternoon and evening. Offshore movement was more prevalent on outgoing tides and from midnight through the morning until midday. Tidal and diel variation in water depths used by the inshore—intertidal dugongs was small, but probably underestimated, hidden by a sampling bias in the telemetry equipment. Onshore movement at high tide allowed dugongs to exploit intertidal seagrass beds. Dugongs are closer to shore in afternoons and evenings than in mornings. This behavior may be related to the avoidance of predators or watercraft. Our findings can be used to predict spatial patterns of dugongs within areas of conservation management significance and to assess, avoid, and mitigate adverse effects of anthropogenic disturbance.     

Long‐term declines in an intertidal foundation species parallel shifts in community composition

The earth is in the midst of a biodiversity crisis, and projections indicate continuing and accelerating rates of global changes. Future alterations in communities and ecosystems may be precipitated by changes in the abundance of strongly interacting species, whose disappearance can lead to profound changes in abundance of other species, including an increase in extinction rate for some. Nearshore coastal communities are often dependent on the habitat and food resources provided by foundational plant (e.g., kelp) and animal (e.g., shellfish) species. We quantified changes in the abundance of the blue mussel (Mytilus edulis), a foundation species known to influence diversity and productivity of intertidal habitats, over the past 40 years in the Gulf of Maine, USA, one of the fastest warming regions in the global ocean. Using consistent survey methods, we compared contemporary population sizes to historical data from sites spanning >400 km. The results of these comparisons showed that blue mussels have declined in the Gulf of Maine by >60% (range: 29–100%) at the site level since the earliest benchmarks in the 1970s. At the same time as mussels declined, community composition shifted: at the four sites with historical community data, the sessile community became increasingly algal dominated. Contemporary (2013–2014) surveys across 20 sites showed that sessile species richness was positively correlated to mussel abundance in mid to high intertidal zones. These results suggest that declines in a critical foundation species may have already impacted the intertidal community. To inform future conservation efforts, we provide a database of historical and contemporary baselines of mussel population abundance and dynamics in the Gulf of Maine. Our results underscore the importance of anticipating not only changes in diversity but also changes in the abundance and identity of component species, as strong interactors like foundation species have the potential to drive cascading community shifts.     

Characterization of 26 new microsatellite loci in the dugong (Dugong dugon)

Twenty‐six microsatellite loci have been isolated from a dugong (Dugong dugon). The average heterozygosity was 0.52 with two to 10 alleles per locus surveyed from 50 individuals. The markers are suitable for genetic mark–recapture (P_ID = 5 × 10^?16) in dugongs and they could also be used to quantify physical tag loss, estimate relatedness, assign paternity, elucidate population structure and identify migrants. The loci also amplified in Florida manatees (22/26) and Asian elephants (6/26).     

The heart of the dugong (Dugong dugon) and the west indian manatee (Trichechus manatus) (Sirenia)

Thirty-eight dugong (Dugong dugon) hearts and 28 Florida manatee (Trichechus manatus) hearts were obtained from stranding programs in Australia and the United States. In addition to a double ventricular apex, a feature that has astonished scientists since the eighteenth century, the hearts of both animals have a double subvalvular conus and a dorsal left atrium. The heart lies in a vertical plane at right angles to that of the completely dorsal, symmetrical lungs. The dugong heart has a deeper interventricular cleft and a more conical left ventricle. The latter features may be part of a general morphological trend toward specialization for a more energetic aquatic existence. The presence of a bulbous ascending aorta in the manatee but not in the dugong is without explanation.     

Annual changes of urinary progesterone and estradiol-17beta of the Dugong (Dugong dugon) in captivity

Levels of urinary progesterone and estradiol-17 beta were measured twice a week in a female dugong, Dugong dugon, in captivity for two years from April 1996 to April 1998. The dugong showed 14 ovarian cycles during the period of study. Concentrations of progesterone ranged from 0.01 ng/mg creatinine (Cr) to 1.94 ng/mg Cr and the length of estrous cycle was 53.6+/-8.6 (mean+/-SEM) days based on intervals of urinary progesterone peak-to-peak measurements. Concentrations of urinary estradiol-17 beta ranged from 0.9pg/mgCr to 23.7pg/mgCr, and tended to peak just prior to elevations of progesterone during the first year of study. This is the first report demonstrates that the ovulatory cycle of the dugong is about 50 days. The present findings suggest that measurement of urinary progesterone is a useful method to detect ovarian cycle of the dugong in captivity.     

A NEW ABUNDANCE ESTIMATE FOR VAQUITAS: FIRST STEP FOR RECOVERY1

A line-transect survey specifically designed to estimate vaquita (Phocoena sinus) abundance over its entire range was carried out by three boats in the summer of 1997. There was a total of 125 sightings of vaquita groups, mainly due to the use of large 25 ± 150 binoculars, which were seven times more effective in detecting vaquitas than hand-held 7 ± binoculars. Results confirmed that the range of the vaquita is restricted to the northwestern corner of the Gulf of California, Mexico, but that the boundaries of the Upper Gulf of California and Colorado River Delta Biosphere Reserve do not correspond well with the distribution of vaquitas. The shallow water north of the town of San Felipe was found to have a higher density of animals than had been indicated by previous surveys. The total population size was estimated to be 567 animals, with a 95% confidence interval from 177 to 1,073. This estimate is an improvement over previous estimates, which had low numbers of sightings, relied on parameters taken from other species, and/or did not cover all areas where vaquitas could potentially be found. The 1997 estimate was more than twice the 1993 estimate, but there are several reasons why the numbers cannot be directly compared, and it should not be concluded the population is increasing. This first complete estimate of vaquita abundance can be a beginning for the recovery of this highly endangered species.     

Spatial Models of Northern Bobwhite Populations for Conservation Planning

Abstract: Since 1980, northern bobwhite (Colinus virginianus) range-wide populations declined 3.9% annually. Within the West Gulf Coastal Plain Bird Conservation Region in the south-central United States, populations of this quail species have declined 6.8% annually. These declines sparked calls for land use change and prompted implementation of various conservation practices. However, to effectively reverse these declines and restore northern bobwhite to their former population levels, habitat conservation and management efforts must target establishment and maintenance of sustainable populations. To provide guidance for conservation and restoration of habitat capable of supporting sustainable northern bobwhite populations in the West Gulf Coastal Plain, we modeled their spatial distribution using landscape characteristics derived from 1992 National Land Cover Data and bird detections, from 1990 to 1994, along 10-stop Breeding Bird Survey route segments. Four landscape metrics influenced detections of northern bobwhite: detections were greater in areas with more grassland and increased aggregation of agricultural lands, but detections were reduced in areas with increased density of land cover edge and grassland edge. Using these landscape metrics, we projected the abundance and spatial distribution of northern bobwhite populations across the entire West Gulf Coastal Plain. Predicted populations closely approximated abundance estimates from a different cadre of concurrently collected data but model predictions did not accurately reflect bobwhite detections along species-specific call-count routes in Arkansas and Louisiana. Using similar methods, we also projected northern bobwhite population distribution circa 1980 based on Land Use Land Cover data and bird survey data from 1976 to 1984. We compared our 1980 spatial projections with our spatial estimate of 1992 populations to identify areas of population change. Additionally, we used our projection of the spatial distribution and abundance of bobwhite to predict areas of population sustainability. Our projections of population change and sustainability provide guidance for targeting habitat conservation and rehabilitation efforts for restoration of northern bobwhite populations in the West Gulf Coastal Plain.     

Fine scale population structure of dugongs (Dugong dugon) implies low gene flow along the southern Queensland coastline

Populations of marine mammals can show the signature of phylogeographical breaks and restricted connectivity despite the apparent lack of physical boundaries in the marine environment and their high dispersal abilities. Dugongs (Dugong dugon) do not appear to undertake regular migrations but may show localised movement related to water temperature or seagrass availability. Previous mitochondrial DNA studies suggested that despite a strong phylogeographic break in the Torres Strait, there is local panmixia in Australian waters. In this study, we conducted a comprehensive study of the four major dugong populations in southern Queensland. We analysed genotypes of 1,293 dugongs based on 24 microsatellite loci from the four major dugong locations in the region (from south to north): Moreton Bay, Great Sandy Straits, Hervey Bay and Shoalwater Bay. Diversity levels were similar across locations (observed heterozygosity 0.48–0.52, allelic richness 4.3–4.5). There was low but significant population differentiation in southern Queensland (F_ST ranged from 0.005 to 0.040 and Jost’s D_EST ranged from 0.001 to 0.031 for microsatellite data). Bayesian clustering analysis implemented in STRUCTURE largely distinguished the southern Moreton Bay population from the three more northern populations. Twelve mitochondrial control region haplotypes identified from a subset of 182 samples confirmed significant population structuring (F_ST ranged from 0.16 to 0.28). These data suggested that the frequency and extent of dugong movements are insufficient to disrupt the long-term existence of at least two breeding populations in southern Queensland.     

Seagrass Herbivory Levels Sustain Site-Fidelity in a Remnant Dugong Population

Herds of dugong, a largely tropical marine megaherbivore, are known to undertake long-distance movements, sequentially overgrazing seagrass meadows in their path. Given their drastic declines in many regions, it is unclear whether at lower densities, their grazing is less intense, reducing their need to travel between meadows. We studied the effect of the feeding behaviour of a small dugong population in the Andaman and Nicobar archipelago, India to understand how small isolated populations graze seagrasses. In the seven years of our observation, all recorded dugongs travelled either solitarily or in pairs, and their use of seagrasses was limited to 8 meadows, some of which were persistently grazed. These meadows were relatively large, contiguous and dominated by short-lived seagrasses species. Dugongs consumed approximately 15% of meadow primary production, but there was a large variation (3–40% of total meadow production) in consumption patterns between meadows. The impact of herbivory was relatively high, with shoot densities c. 50% higher inside herbivore exclosures than in areas exposed to repeated grazing. Our results indicate that dugongs in the study area repeatedly graze the same meadows probably because the proportion of primary production consumed reduces shoot density to levels that are still above values that can trigger meadow abandonment. This ability of seagrasses to cope perhaps explains the long-term site fidelity shown by individual dugongs in these meadows. The fact that seagrass meadows in the archipelago are able to support dugong foraging requirements allows us to clearly identify locations where this remnant population persists, and where urgent management efforts can be directed.     

Distribution and abundance of the dugong in New Caledonia, southwest Pacific

New Caledonia is at the eastern limit of the dugong's range. In June 2003 standardized dugong aerial survey methodology was used to estimate the abundance and distribution of dugongs in the coastal waters of New Caledonia, resulting in a population estimate of 1,814 ± SE 332. This represents the largest concentration of dugongs in Melanesia and one of the largest populations in the world, outside Australia and the Arabian region. Calves comprised 7.2% of the population. The observed density of dugongs was highest in the center and southern part of the west coast of the island but not significantly different from the density on the north west and north east. In the central west region, sightings were associated with a pass in the barrier reef and up to a third of the on‐survey sightings were outside of the barrier reef. The dugong distribution we observed during June 2003 differs from the reported locations of historical hunts in several respects.     

Pleistocene sea level fluctuations and the phylogeography of the dugong in Australian waters

We investigated phylogeography, demography, and population connectivity of the dugong (Dugong dugon) in Australian waters using mitochondrial control region DNA sequences from 177 Australian dugongs and 11 from elsewhere. The dugong is widespread in shallow Indo‐West Pacific waters suitable for growth of its main food, seagrass. We hypothesized that the loss of habitat and creation of a land barrier (the Torres Strait landbridge) during low sea level stands associated with Pleistocene glacial cycles have left a persisting genetic signature in the dugong. The landbridge was most recently flooded about 7,000 yr ago. Individual dugongs are capable of traveling long distances, suggesting an alternative hypothesis that there might now be little genetic differentiation across the dugong's Australian range. We demonstrated that Australian dugongs fall into two distinct maternal lineages and exhibit a phylogeographic pattern reflecting Pleistocene sea‐level fluctuations. Within each lineage, genetic structure exists, albeit at large spatial scales. We suggest that these lineages diverged following the last emergence of the Torres Strait landbridge (ca. 115 kya) and remained geographically separated until after 7 kya when passage through Torres Strait again became possible for marine animals. Evidence for population growth in the widespread lineage, especially after the last glacial maximum, was detected.