Long-term stability in the circumpolar foraging range of a Southern Ocean predator between the eras of whaling and rapid climate change.

Assessing environmental changes in Southern Ocean ecosystems is difficult due to its remoteness and data sparsity. Monitoring marine predators that respond rapidly to environmental variation may enable us to track anthropogenic effects on ecosystems. Yet, many long-term datasets of marine predators are incomplete because they are spatially constrained and/or track ecosystems already modified by industrial fishing and whaling in the latter half of the 20th century. Here, we assess the contemporary offshore distribution of a wide-ranging marine predator, the southern right whale (SRW, Eubalaena australis), that forages on copepods and krill from ~30°S to the Antarctic ice edge (>60°S). We analyzed carbon and nitrogen isotope values of 1,002 skin samples from six genetically distinct SRW populations using a customized assignment approach that accounts for temporal and spatial variation in the Southern Ocean phytoplankton isoscape. Over the past three decades, SRWs increased their use of mid-latitude foraging grounds in the south Atlantic and southwest (SW) Indian oceans in the late austral summer and autumn and slightly increased their use of high-latitude (>60°S) foraging grounds in the SW Pacific, coincident with observed changes in prey distribution and abundance on a circumpolar scale. Comparing foraging assignments with whaling records since the 18th century showed remarkable stability in use of mid-latitude foraging areas. We attribute this consistency across four centuries to the physical stability of ocean fronts and resulting productivity in mid-latitude ecosystems of the Southern Ocean compared with polar regions that may be more influenced by recent climate change.

Ice-inhabiting species of Bdelloidea Rotifera reveal a pre-Quaternary ancestry in the Arctic cryosphere.

Historical climate data indicate that the Earth has passed through multiple geological periods with much warmer-than-present climates, including epochs of the Miocene (23-5.3 mya BP) with temperatures 3-4°C above present, and more recent interglacial stages of the Quaternary, for example, Marine Isotope Stage 11c (approx. 425-395 ka BP) and Middle Holocene thermal maximum (7.5-4.2 ka BP), during which continental glaciers may have melted entirely. Such warm periods would have severe consequences for ice-obligate fauna in terms of their distribution, biodiversity and population structure. To determine the impacts of these climatic events in the Nordic cryosphere, we surveyed ice habitats throughout mainland Norway and Svalbard ranging from maritime glaciers to continental ice patches (i.e. non-flowing, inland ice subjected to deep freezing overwinter), finding particularly widespread populations of ice-inhabiting bdelloid rotifers. Combined mitochondrial and nuclear DNA sequencing identified approx. 16 undescribed, species-level rotifer lineages that revealed an ancestry predating the Quaternary (> 2.58 mya). These rotifers also displayed robust freeze/thaw tolerance in laboratory experiments. Collectively, these data suggest that extensive ice refugia, comparable with stable ice patches across the contemporary Norwegian landscape, persisted in the cryosphere over geological time, and may have facilitated the long-term survival of ice-obligate Metazoa before and throughout the Quaternary.

Ancient RNA from Late Pleistocene permafrost and historical canids shows tissue-specific transcriptome survival.

While sequencing ancient DNA (aDNA) from archaeological material is now commonplace, very few attempts to sequence ancient transcriptomes have been made, even from typically stable deposition environments such as permafrost. This is presumably due to assumptions that RNA completely degrades relatively quickly, particularly when dealing with autolytic, nuclease-rich mammalian tissues. However, given the recent successes in sequencing ancient RNA (aRNA) from various sources including plants and animals, we suspect that these assumptions may be incorrect or exaggerated. To challenge the underlying dogma, we generated shotgun RNA data from sources that might normally be dismissed for such study. Here, we present aRNA data generated from two historical wolf skins, and permafrost-preserved liver tissue of a 14,300-year-old Pleistocene canid. Not only is the latter the oldest RNA ever to be sequenced, but it also shows evidence of biologically relevant tissue specificity and close similarity to equivalent data derived from modern-day control tissue. Other hallmarks of RNA sequencing (RNA-seq) data such as exon-exon junction presence and high endogenous ribosomal RNA (rRNA) content confirms our data's authenticity. By performing independent technical library replicates using two high-throughput sequencing platforms, we show not only that aRNA can survive for extended periods in mammalian tissues but also that it has potential for tissue identification. aRNA also has possible further potential, such as identifying in vivo genome activity and adaptation, when sequenced using this technology.

Stranded dolphin stomach contents represent the free-ranging population's diet.

Diet is a fundamental aspect of animal ecology. Cetacean prey species are generally identified by examining stomach contents of stranded individuals. Critical uncertainty in these studies is whether samples from stranded animals are representative of the diet of free-ranging animals. Over two summers, we collected faecal and gastric samples from healthy free-ranging individuals of an extensively studied bottlenose dolphin population. These samples were analysed by molecular prey detection and these data compared with stomach contents data derived from stranded dolphins from the same population collected over 22 years. There was a remarkable consistency in the prey species composition and relative amounts between the two datasets. The conclusions of past stomach contents studies regarding dolphin habitat associations, prey selection and proposed foraging mechanisms are supported by molecular data from live animals and the combined dataset. This is the first explicit test of the validity of stomach contents analysis for accurate population-scale diet determination of an inshore cetacean.

A regionally coherent ecological fingerprint of climate change, evidenced from natural history collections.

Climate change has dramatic impacts on ecological systems, affecting a range of ecological factors including phenology, species abundance, diversity, and distribution. The breadth of climate change impacts on ecological systems leads to the occurrence of fingerprints of climate change. However, climate fingerprints are usually identified across broad geographical scales and are potentially influenced by publication biases. In this study, we used natural history collections spanning over 250 years, to quantify a range of ecological responses to climate change, including phenology, abundance, diversity, and distributions, across a range of taxa, including vertebrates, invertebrates, plants, and fungi, within a single region, Central Norway. We tested the hypotheses that ecological responses to climate change are apparent and coherent at a regional scale, that longer time series show stronger trends over time and in relation to temperature, and that ecological responses change in trajectory at the same time as shifts in temperature. We identified a clear regional coherence in climate signal, with decreasing abundances of limnic zooplankton (on average by 7691 individuals m-3 °C-1) and boreal forest breeding birds (on average by 1.94 territories km-2 °C-1), and earlier plant flowering phenology (on average 2 days °C-1) for every degree of temperature increase. In contrast, regional-scale species distributions and species diversity were largely stable. Surprisingly, the effect size of ecological response did not increase with study duration, and shifts in responses did not occur at the same time as shifts in temperature. This may be as the long-term studies include both periods of warming and temperature stability, and that ecological responses lag behind warming. Our findings demonstrate a regional climate fingerprint across a long timescale. We contend that natural history collections provide a unique window on a broad spectrum of ecological responses at timescales beyond most ecological monitoring programs. Natural history collections are thus an essential source for long-term ecological research.

Macroalgal browsing on a heavily degraded, urbanized equatorial reef system.

The removal of macroalgal biomass is critical to the health of coral reef ecosystems. Previous studies on relatively intact reefs with diverse and abundant fish communities have quantified rapid removal of macroalgae by herbivorous fishes, yet how these findings relate to degraded reef systems where fish diversity and abundance are markedly lower and algal biomass substantially higher, is unclear. We surveyed roving herbivorous fish communities and quantified their capacity to remove the dominant macroalga Sargassum ilicifolium on seven reefs in Singapore; a heavily degraded urbanized reef system. The diversity and abundance of herbivorous fishes was extremely low, with eight species and a mean abundance ~1.1 individuals 60 m-2 recorded across reefs. Consumption of S. ilicifolium varied with distance from Singapore's main port with consumption being 3- to 17-fold higher on reefs furthest from the port (Pulau Satumu: 4.18 g h-1; Kusu Island: 2.38 g h-1) than reefs closer to the port (0.35-0.78 g h-1). Video observations revealed a single species, Siganus virgatus, was almost solely responsible for removing S. ilicifolium biomass, accounting for 83% of the mass-standardized bites. Despite low herbivore diversity and intense urbanization, macroalgal removal by fishes on some Singaporean reefs was directly comparable to rates reported for other inshore Indo-Pacific reefs.

Prickly business: abundance of sea urchins on breakwaters and coral reefs in Dubai.

Echinometra mathaei is a common echinoid on tropical reefs and where abundant plays an important role in the control of algal communities. Despite high prevalence of E. mathaei on southern Persian/Arabian Gulf reefs, their abundance and distribution is poorly known. Spatial and temporal patterns in population abundance were examined at 12 sites between breakwater and natural reef habitats in Dubai (UAE) every 3 months from 2008 to 2010. Within the breakwater habitat, densities were greatest at shallow wave-exposed sites, and reduced with both decreasing wave-exposure and increasing depth. Interestingly, E. mathaei were significantly more abundant on exposed breakwaters than natural reef sites, presumably due to differences in habitat structure and benthic cover. Population abundances differed seasonally, with peak abundances during summer (July-September) and lower abundances in winter (December-February). Seasonal fluctuations are likely the result of peak annual recruitment pulses coupled with increased fish predation from summer to winter.

The environmental impact of sewage and wastewater outfalls in Antarctica: An example from Davis station, East Antarctica.

We present a comprehensive scientific assessment of the environmental impacts of an Antarctic wastewater ocean outfall, at Davis station in East Antarctica. We assessed the effectiveness of current wastewater treatment and disposal requirements under the Protocol on Environmental Protection to the Antarctic Treaty. Macerated wastewater has been discharged from an outfall at Davis since the failure of the secondary treatment plant in 2005. Water, sediment and wildlife were tested for presence of human enteric bacteria and antibiotic resistance mechanisms. Epibiotic and sediment macrofaunal communities were tested for differences between sites near the outfall and controls. Local fish were examined for evidence of histopathological abnormalities. Sediments, fish and gastropods were tested for uptake of sewage as measured by stable isotopes of N and C. Escherichia coli carrying antibiotic resistance determinants were found in water, sediments and wildlife (the filter feeding bivalve Laternula eliptica). Fish (Trematomus bernacchii) within close proximity to the outfall had significantly more severe and greater occurrences of histopathological abnormalities than at controls, consistent with exposure to sewage. There was significant enrichment of 15N in T. bernacchii and the predatory gastropod Neobuccinum eatoni around the outfall, providing evidence of uptake of sewage. There were significant differences between epibiotic and sediment macrofaunal communities at control and outfall sites (<1.5 km), when sites were separated into groups of similar habitat types. Benthic community composition was also strongly related to habitat and environmental drivers such as sea ice. The combined evidence indicated that the discharge of wastewater from the Davis outfall is causing environmental impacts. These findings suggest that conditions in Antarctic coastal locations, such as Davis, are unlikely to be conducive to initial dilution and rapid dispersal of wastewater as required under the Protocol on Environmental Protection to the Antarctic Treaty. Current minimum requirements for wastewater treatment and disposal in Antarctica are insufficient to ameliorate these risks and are likely to lead to accumulation of contaminants and introduction of non-native microbes and associated genetic elements. This new understanding suggests that modernised approaches to the treatment and disposal of wastewater are required in Antarctica. The most effective solution is advanced levels of wastewater treatment, which are now possible, feasible and a high priority for installation. As a direct outcome of the study, a new advanced treatment system is being installed at Davis, effectively avoiding environmental risks.

Dispersal and dilution of wastewater from an ocean outfall at Davis Station, Antarctica, and resulting environmental contamination.

The Antarctic Treaty permits the discharge of wastewater into Antarctic marine waters providing that conditions exist for initial dilution and rapid dispersal. We investigated the dilution and dispersal of macerated wastewater around Australia's Davis Station in East Antarctica and examined sediments for evidence of contaminants. Methods used to examine hydrodynamic conditions included current meters, dye release experiments and measurement of sewage-associated microbial markers and surfactants in the water column. We measured marine sediments for metals, nutrients, PBDEs, hydrocarbons and faecal sterols. We propose that if there is adequate dilution and dispersal there would be no significant difference in contaminant concentrations in sediments around the outfall compared to distant control sites. Currents were strongly correlated with prevailing wind conditions. Modelling indicated that diffusivity of wastewater had the greatest effect on dilution factors and that neither discharge rates nor local currents had as much effect. During summer conditions of open water, wastewater is likely to be constrained in a narrow plume close to the coast. Concentrations of sewage bacteria were high around the outfall and detected up to 1.5 km away, along with dye. There were significant differences in sediment concentrations of metals, PBDEs, hydrocarbons, nutrients and faecal sterols between sites within 2 km of the outfall and control sites. We conclude that dilution and dispersal conditions at the Davis outfall are insufficient to prevent the accumulation of contaminants in local sediments and that microbial hazards posed by wastewater are an environmental risk to local wildlife.

Coral settlement on a highly disturbed equatorial reef system.

Processes occurring early in the life stages of corals can greatly influence the demography of coral populations, and successful settlement of coral larvae that leads to recruitment is a critical life history stage for coral reef ecosystems. Although corals in Singapore persist in one the world's most anthropogenically impacted reef systems, our understanding of the role of coral settlement in the persistence of coral communities in Singapore remains limited. Spatial and temporal patterns of coral settlement were examined at 7 sites in the southern islands of Singapore, using settlement tiles deployed and collected every 3 months from 2011 to 2013. Settlement occurred year round, but varied significantly across time and space. Annual coral settlement was low (~54.72 spat m(-2) yr(-1)) relative to other equatorial regions, but there was evidence of temporal variation in settlement rates. Peak settlement occurred between March-May and September-November, coinciding with annual coral spawning periods (March-April and October), while the lowest settlement occurred from December-February during the northeast monsoon. A period of high settlement was also observed between June and August in the first year (2011/12), possibly due to some species spawning outside predicted spawning periods, larvae settling from other locations or extended larval settlement competency periods. Settlement rates varied significantly among sites, but spatial variation was relatively consistent between years, suggesting the strong effects of local coral assemblages or environmental conditions. Pocilloporidae were the most abundant coral spat (83.6%), while Poritidae comprised only 6% of the spat, and Acroporidae <1%. Other, unidentifiable families represented 10% of the coral spat. These results indicate that current settlement patterns are reinforcing the local adult assemblage structure ('others'; i.e. sediment-tolerant coral taxa) in Singapore, but that the replenishment capacity of Singapore's reefs appears relatively constrained, which could lead to less resilient reefs.

Telomeres as age markers in vertebrate molecular ecology.

Chronological age is a fundamental and yet elusive variable in studies of many wild animals. Telomeres are nucleoprotein structures on the ends of chromosomes that change size throughout the life of many animals and because of this property have been advocated as a means to estimate age. In this review, we assess the existing and potential application of using telomeres for age estimation. We argue that there are conceptual and statistical inconsistencies in previous studies and that the basis for telomere change over time is not well understood and affected by several intrinsic and extrinsic process unrelated to chronological time. Furthermore, these processes are likely to vary spatially and temporally for animal populations. We conclude that the current data suggest telomeres should not be used for age estimation. If telomere-based age estimation is to be used, more work in understanding variability in key processes affecting telomere dynamics and rigorous substantiation via blind testing is needed.

DNA-based diet analysis for any predator.

BACKGROUND: Prey DNA from diet samples can be used as a dietary marker; yet current methods for prey detection require a priori diet knowledge and/or are designed ad hoc, limiting their scope. I present a general approach to detect diverse prey in the feces or gut contents of predators. METHODOLOGY/PRINCIPAL FINDINGS: In the example outlined, I take advantage of the restriction site for the endonuclease Pac I which is present in 16S mtDNA of most Odontoceti mammals, but absent from most other relevant non-mammalian chordates and invertebrates. Thus in DNA extracted from feces of these mammalian predators Pac I will cleave and exclude predator DNA from a small region targeted by novel universal primers, while most prey DNA remain intact allowing prey selective PCR. The method was optimized using scat samples from captive bottlenose dolphins (Tursiops truncatus) fed a diet of 6-10 prey species from three phlya. Up to five prey from two phyla were detected in a single scat and all but one minor prey item (2% of the overall diet) were detected across all samples. The same method was applied to scat samples from free-ranging bottlenose dolphins; up to seven prey taxa were detected in a single scat and 13 prey taxa from eight teleost families were identified in total. CONCLUSIONS/SIGNIFICANCE: Data and further examples are provided to facilitate rapid transfer of this approach to any predator. This methodology should prove useful to zoologists using DNA-based diet techniques in a wide variety of study systems.