Abyssal hydrothermal springs-Cryptic incubators for brooding octopus.

Does warmth from hydrothermal springs play a vital role in the biology and ecology of abyssal animals? Deep off central California, thousands of octopus (Muusoctopus robustus) migrate through cold dark waters to hydrothermal springs near an extinct volcano to mate, nest, and die, forming the largest known aggregation of octopus on Earth. Warmth from the springs plays a key role by raising metabolic rates, speeding embryonic development, and presumably increasing reproductive success; we show that brood times for females are ~1.8 years, far faster than expected for abyssal octopods. Using a high-resolution subsea mapping system, we created landscape-scale maps and image mosaics that reveal 6000 octopus in a 2.5-ha area. Because octopuses die after reproducing, hydrothermal springs indirectly provide a food supplement to the local energy budget. Although localized deep-sea heat sources may be essential to octopuses and other warm-tolerant species, most of these unique and often cryptic habitats remain undiscovered and unexplored.

Phenology in the deep sea: seasonal and tidal feeding rhythms in a keystone octocoral.

Biological rhythms are widely known in terrestrial and marine systems, where the behaviour or function of organisms may be tuned to environmental variation over periods from minutes to seasons or longer. Although well characterized in coastal environments, phenology remains poorly understood in the deep sea. Here we characterized intra-annual dynamics of feeding activity for the deep-sea octocoral Paragorgia arborea. Hourly changes in polyp activity were quantified using a time-lapse camera deployed for a year on Sur Ridge (1230 m depth; Northeast Pacific). The relationship between feeding and environmental variables, including surface primary production, temperature, acoustic backscatter, current speed and direction, was evaluated. Feeding activity was highly seasonal, with a dormancy period identified between January and early April, reflecting seasonal changes in food availability as suggested by primary production and acoustic backscatter data. Moreover, feeding varied with tides, which likely affected food delivery through cyclic oscillation in current speed and direction. This study provides the first evidence of behavioural rhythms in a coral species at depth greater than 1 km. Information on the feeding biology of this cosmopolitan deep-sea octocoral will contribute to a better understanding of how future environmental change may affect deep-sea coral communities and the ecosystem services they provide.

Historical comparisons of body size are sensitive to data availability and ecological context.

Historical comparisons of body size often lack pertinent details, including information on the sampling protocol and relevant ecological covariates that influence body size. Moreover, historical estimates of body size that rely on museum specimens may be biased towards larger size classes because of collector preferences, and thus size thresholds have been used to focus attention on maximum body size. We tested the consequences of sampling design, ecological covariates, and size thresholds on inferences of body-size change using field-contextualized historical records, rather than museum specimens. In 2014-2015, we revisited historical (1947-1963) size-frequency distributions of three gastropods (Tegula funebralis, Lottia digitalis/L. austrodigitalis, Littorina keenae) in the context of population density and tidal height. In general, gastropods declined in size. However, our inferences regarding body-size decline were tempered when the variation between sampling units was taken into consideration, resulting in greater uncertainty around the estimate of proportional change in body size. Gastropod size was correlated with population density and tidal height, and these relationships varied over time. Finally, the magnitude and direction of body-size change varied with the amount of data available for analysis, demonstrating that the use of size thresholds can lead to incomplete conclusions.

Assessment of food web recovery following restoration using resource niche metrics.

The primary goal of habitat restoration is to recover the ecological structure, function, and services of natural ecosystems lost due to disturbance. Post-restoration success typically focuses on the return of a desired habitat type, consumer species composition, or abundance relative to a reference site. However, how energy flow responds to habitat restoration has not been widely studied, and there is a need to develop a better understanding of how energy flows through a restored vs reference ecosystem following restoration. We tested recently developed niche metrics as a tool to assess the degree of recovery of ecosystem energy flow and evaluate the success of habitat restoration. Using published stable isotope values from six systems, one to three years post-restoration, we used Bayesian mixing models to quantify resource use by consumers to generate food web hypervolumes for restored and reference habitats in each ecosystem and to quantify similarity in resource use between restored and reference systems. Our analysis showed that there were differences in restoration success at each restoration project between the restored and reference food webs, but two general patterns emerged in the early stages following restoration. Restoration efforts that restore biogenic habitats display lower levels of recovery of food web function than those that only restore abiotic habitat structural. Restoration increases the variability in basal resource use of consumers in food webs that rely heavily on one basal resource, while in food webs that relied on multiple basal resources consumers decrease variability in basal resource use. Our results demonstrate that hypervolume analysis is a powerful tool that can be used to quantify energy flow, the recovery of food web function, and measure restoration success.

Microbial community networks associated with variations in community respiration rates during upwelling in nearshore Monterey Bay, California.

Respiration of organic material is a central process in the global carbon (C) cycle catalysed by diverse microbial communities. In the coastal ocean, upwelling can drive variation in both community respiration (CR) and the microbial community, but linkages between the two are not well-understood. We measured CR rates and analysed microbial dynamics via 16S rRNA gene sequencing, to assess whether CR correlated with upwelling irrespective of changes in the microbial community, or if the particular microbial community present was a factor in explaining variations in CR. CR varied significantly over time as a function of temperature, dissolved oxygen (DO) and chlorophyll-all of which are altered by upwelling-but also varied with a 'subnetwork' (i.e., a group of microbial taxa that covaried with one another) of the whole community. One subnetwork was associated with higher CR and warmer temperatures, while another was associated with lower CR and DO. Our results suggest that CR in the coastal ocean varies with both environmental variables, and a portion of the microbial community that is not directly correlated with upwelling intensity.

Assessing vertebrate biodiversity in a kelp forest ecosystem using environmental DNA.

Preserving biodiversity is a global challenge requiring data on species' distribution and abundance over large geographic and temporal scales. However, traditional methods to survey mobile species' distribution and abundance in marine environments are often inefficient, environmentally destructive, or resource-intensive. Metabarcoding of environmental DNA (eDNA) offers a new means to assess biodiversity and on much larger scales, but adoption of this approach for surveying whole animal communities in large, dynamic aquatic systems has been slowed by significant unknowns surrounding error rates of detection and relevant spatial resolution of eDNA surveys. Here, we report the results of a 2.5 km eDNA transect surveying the vertebrate fauna present along a gradation of diverse marine habitats associated with a kelp forest ecosystem. Using PCR primers that target the mitochondrial 12S rRNA gene of marine fishes and mammals, we generated eDNA sequence data and compared it to simultaneous visual dive surveys. We find spatial concordance between individual species' eDNA and visual survey trends, and that eDNA is able to distinguish vertebrate community assemblages from habitats separated by as little as ~60 m. eDNA reliably detected vertebrates with low false-negative error rates (1/12 taxa) when compared to the surveys, and revealed cryptic species known to occupy the habitats but overlooked by visual methods. This study also presents an explicit accounting of false negatives and positives in metabarcoding data, which illustrate the influence of gene marker selection, replication, contamination, biases impacting eDNA count data and ecology of target species on eDNA detection rates in an open ecosystem.

Stable isotope analysis of vertebrae reveals ontogenetic changes in habitat in an endothermic pelagic shark.

Ontogenetic changes in habitat are driven by shifting life-history requirements and play an important role in population dynamics. However, large portions of the life history of many pelagic species are still poorly understood or unknown. We used a novel combination of stable isotope analysis of vertebral annuli, Bayesian mixing models, isoscapes and electronic tag data to reconstruct ontogenetic patterns of habitat and resource use in a pelagic apex predator, the salmon shark (Lamna ditropis). Results identified the North Pacific Transition Zone as the major nursery area for salmon sharks and revealed an ontogenetic shift around the age of maturity from oceanic to increased use of neritic habitats. The nursery habitat may reflect trade-offs between prey availability, predation pressure and thermal constraints on juvenile endothermic sharks. The ontogenetic shift in habitat coincided with a reduction of isotopic niche, possibly reflecting specialization upon particular prey or habitats. Using tagging data to inform Bayesian isotopic mixing models revealed that adult sharks primarily use neritic habitats of Alaska yet receive a trophic subsidy from oceanic habitats. Integrating the multiple methods used here provides a powerful approach to retrospectively study the ecology and life history of migratory species throughout their ontogeny.

Ocean fronts drive marine fishery production and biogeochemical cycling.

Long-term changes in nutrient supply and primary production reportedly foreshadow substantial declines in global marine fishery production. These declines combined with current overfishing, habitat degradation, and pollution paint a grim picture for the future of marine fisheries and ecosystems. However, current models forecasting such declines do not account for the effects of ocean fronts as biogeochemical hotspots. Here we apply a fundamental technique from fluid dynamics to an ecosystem model to show how fronts increase total ecosystem biomass, explain fishery production, cause regime shifts, and contribute significantly to global biogeochemical budgets by channeling nutrients through alternate trophic pathways. We then illustrate how ocean fronts affect fishery abundance and yield, using long-term records of anchovy-sardine regimes and salmon abundances in the California Current. These results elucidate the fundamental importance of biophysical coupling as a driver of bottom-up vs. top-down regulation and high productivity in marine ecosystems.

Oceanographic and biological effects of shoaling of the oxygen minimum zone.

Long-term declines in oxygen concentrations are evident throughout much of the ocean interior and are particularly acute in midwater oxygen minimum zones (OMZs). These regions are defined by extremely low oxygen concentrations (<20-45 µmol kg(-1)), cover wide expanses of the ocean, and are associated with productive oceanic and coastal regions. OMZs have expanded over the past 50 years, and this expansion is predicted to continue as the climate warms worldwide. Shoaling of the upper boundaries of the OMZs accompanies OMZ expansion, and decreased oxygen at shallower depths can affect all marine organisms through multiple direct and indirect mechanisms. Effects include altered microbial processes that produce and consume key nutrients and gases, changes in predator-prey dynamics, and shifts in the abundance and accessibility of commercially fished species. Although many species will be negatively affected by these effects, others may expand their range or exploit new niches. OMZ shoaling is thus likely to have major and far-reaching consequences.

Tissue turnover rates and isotopic trophic discrimination factors in the endothermic teleost, pacific bluefin tuna (Thunnus orientalis).

Stable isotope analysis (SIA) of highly migratory marine pelagic animals can improve understanding of their migratory patterns and trophic ecology. However, accurate interpretation of isotopic analyses relies on knowledge of isotope turnover rates and tissue-diet isotope discrimination factors. Laboratory-derived turnover rates and discrimination factors have been difficult to obtain due to the challenges of maintaining these species in captivity. We conducted a study to determine tissue- (white muscle and liver) and isotope- (nitrogen and carbon) specific turnover rates and trophic discrimination factors (TDFs) using archived tissues from captive Pacific bluefin tuna (PBFT), Thunnus orientalis, 1-2914 days after a diet shift in captivity. Half-life values for (15)N turnover in white muscle and liver were 167 and 86 days, and for (13)C were 255 and 162 days, respectively. TDFs for white muscle and liver were 1.9 and 1.1‰ for δ(15)N and 1.8 and 1.2‰ for δ(13)C, respectively. Our results demonstrate that turnover of (15)N and (13)C in bluefin tuna tissues is well described by a single compartment first-order kinetics model. We report variability in turnover rates between tissue types and their isotope dynamics, and hypothesize that metabolic processes play a large role in turnover of nitrogen and carbon in PBFT white muscle and liver tissues. (15)N in white muscle tissue showed the most predictable change with diet over time, suggesting that white muscle δ(15)N data may provide the most reliable inferences for diet and migration studies using stable isotopes in wild fish. These results allow more accurate interpretation of field data and dramatically improve our ability to use stable isotope data from wild tunas to better understand their migration patterns and trophic ecology.

Stable isotope analysis challenges wasp-waist food web assumptions in an upwelling pelagic ecosystem.

Eastern boundary currents are often described as 'wasp-waist' ecosystems in which one or few mid-level forage species support a high diversity of larger predators that are highly susceptible to fluctuations in prey biomass. The assumption of wasp-waist control has not been empirically tested in all such ecosystems. This study used stable isotope analysis to test the hypothesis of wasp-waist control in the southern California Current large marine ecosystem (CCLME). We analyzed prey and predator tissue for δ¹³C and δ¹5N and used Bayesian mixing models to provide estimates of CCLME trophic dynamics from 2007-2010. Our results show high omnivory, planktivory by some predators, and a higher degree of trophic connectivity than that suggested by the wasp-waist model. Based on this study period, wasp-waist models oversimplify trophic dynamics within the CCLME and potentially other upwelling, pelagic ecosystems. Higher trophic connectivity in the CCLME likely increases ecosystem stability and resilience to perturbations.

Disentangling trophic interactions inside a Caribbean marine reserve.

Recent empirical studies have demonstrated that human activities such as fishing can strongly affect the natural capital and services provided by tropical seascapes. However, policies to mitigate anthropogenic impacts can also alter food web structure and interactions, regardless of whether the regulations are aimed at single or multiple species, with possible unexpected consequences for the ecosystems and their associated services. Complex community response to management interventions have been highlighted in the Caribbean, where, contrary to predictions from linear food chain models, a reduction in fishing intensity through the establishment of a marine reserve has led to greater biomass of herbivorous fish inside the reserve, despite an increased abundance of large predatory piscivores. This positive multi-trophic response, where both predators and prey benefit from protection, highlights the need to take an integrated approach that considers how numerous factors control species coexistence in both fished and unfished systems. In order to understand these complex relationships, we developed a general model to examine the trade-offs between fishing pressure and trophic control on reef fish communities, including an exploration of top-down and bottom-up effects. We then validated the general model predictions by parameterizing the model for a reef system in the Bahamas in order to tease apart the wide range of species responses to reserves in the Caribbean. Combining the development of general theory and site-specific models parameterized with field data reveals the underlying driving forces in these communities and enables us to make better predictions about possible population and community responses to different management schemes.