Fathoming sea turtles: monitoring strategy evaluation to improve conservation status assessments.

Population monitoring must be accurate and reliable to correctly classify population status. For sea turtles, nesting beach surveys are often the only population-level surveys that are accessible. However, process and observation errors, compounded by delayed maturity, obscure the relationship between trends on the nesting beach and the population. We present a simulation-based tool, monitoring strategy evaluation (MoSE), to test the relationships between monitoring data and assessment accuracy, using green sea turtles, Chelonia mydas, as a case study. To explore this first application of MoSE, we apply different treatments of population impacts to virtual true populations, and sample the nests or nesters, with observation error, to test if the observation data can be used to diagnose population status accurately. Based on the observed data, we examine population trend and compare it to the known values from the operating model. We ran a series of scenarios including harvest impacts, cyclical breeding probability, and sampling biases, to see how these factors impact accuracy in estimating population trend. We explored the necessary duration of monitoring for accurate trend estimation and the probability of a false trend diagnosis. Our results suggest that disturbance type and severity can have important and persistent effects on the accuracy of population assessments drawn from monitoring nesting beaches. The underlying population phase, age classes disturbed, and impact severity influenced the accuracy of estimating population trend. At least 10 yr of monitoring data is necessary to estimate population trend accurately, and >20 yr if juvenile age classes were disturbed and the population is recovering. In general, there is a greater probability of making a false positive trend diagnosis than a false negative, but this depends on impact type and severity, population phase, and sampling duration. Improving detection rates to 90% does little to lower probability of a false trend diagnosis with shorter monitoring spans. Altogether, monitoring strategies for specific populations may be tailored based on the impact history, population phase, and environmental drivers. The MoSE is an important framework for analysis through simulation that can comprehensively test population assessments for accuracy and inform policy recommendations regarding the best monitoring strategies.

The role of maternal age and context-dependent maternal effects in the offspring provisioning of a long-lived marine teleost.

Despite evidence of maternal age effects in a number of teleost species, there have been challenges to the assertion that maternal age intrinsically influences offspring quality. From an evolutionary perspective, maternal age effects result in young females paradoxically investing in less fit offspring despite a greater potential fitness benefit that might be gained by allocating this energy to individual somatic growth. Although a narrow range of conditions could lead to a maternal fitness benefit via the production of lower quality offspring, evolutionary theorists suggest these conditions are seldom met and that the reported maternal age effects are more likely products of the environmental context. Our goal was to determine if maternal effects operated on offspring provisioning in a long-lived rockfish (genus Sebastes), and to evaluate any such effects as an intrinsic function of maternal age or a context-dependent effect of the offspring release environment. We found that offspring provisioning is a function of both maternal age and the timing of offspring release; older females exhibit increased provisioning over younger females throughout the spawning season despite a decrease in provisioning across all maternal ages as the season progresses. These findings suggest a role for both maternal age effects and a potential context-dependent maternal effect in population productivity, carrying important implications when modelling population persistence and resilience.

Growth dynamics of juvenile loggerhead sea turtles undergoing an ontogenetic habitat shift.

Ontogenetic niche theory predicts that individuals may undergo one or more changes in habitat or diet throughout their lifetime to maintain optimal growth rates, or to optimize trade-offs between mortality risk and growth. We combine skeletochronological and stable nitrogen isotope (δ15N) analyses of sea turtle humeri (n = 61) to characterize the growth dynamics of juvenile loggerhead sea turtles (Caretta caretta) during an oceanic-to-neritic ontogenetic shift. The primary objective of this study was to determine how ontogenetic niche theory extends to sea turtles, and to individuals with different patterns of resource use (discrete shifters, n = 23; facultative shifters n = 14; non-shifters, n = 24). Mean growth rates peaked at the start of the ontogenetic shift (based on change in δ15N values), but returned to pre-shift levels within 2 years. Turtles generally only experienced 1 year of relatively high growth, but the timing of peak growth relative to the start of an ontogenetic shift varied among individuals (before, n = 14; during, n = 12; after, n = 8). Furthermore, no reduction in growth preceded the transition, as is predicted by ontogenetic niche theory. Annual growth rates were similar between non-transitioning turtles resident in oceanic and neritic habitats and turtles displaying alternative patterns of resource use. These results suggest that factors other than maximization of size-specific growth may more strongly influence the timing of ontogenetic shifts in loggerhead sea turtles, and that alternative patterns of resource use may have limited influence on somatic growth and age at maturation in this species.

Patterns and Variation in Benthic Biodiversity in a Large Marine Ecosystem.

While there is a persistent inverse relationship between latitude and species diversity across many taxa and ecosystems, deviations from this norm offer an opportunity to understand the conditions that contribute to large-scale diversity patterns. Marine systems, in particular, provide such an opportunity, as marine diversity does not always follow a strict latitudinal gradient, perhaps because several hypothesized drivers of the latitudinal diversity gradient are uncorrelated in marine systems. We used a large scale public monitoring dataset collected over an eight year period to examine benthic marine faunal biodiversity patterns for the continental shelf (55-183 m depth) and slope habitats (184-1280 m depth) off the US West Coast (47°20'N-32°40'N). We specifically asked whether marine biodiversity followed a strict latitudinal gradient, and if these latitudinal patterns varied across depth, in different benthic substrates, and over ecological time scales. Further, we subdivided our study area into three smaller regions to test whether coast-wide patterns of biodiversity held at regional scales, where local oceanographic processes tend to influence community structure and function. Overall, we found complex patterns of biodiversity on both the coast-wide and regional scales that differed by taxonomic group. Importantly, marine biodiversity was not always highest at low latitudes. We found that latitude, depth, substrate, and year were all important descriptors of fish and invertebrate diversity. Invertebrate richness and taxonomic diversity were highest at high latitudes and in deeper waters. Fish richness also increased with latitude, but exhibited a hump-shaped relationship with depth, increasing with depth up to the continental shelf break, ~200 m depth, and then decreasing in deeper waters. We found relationships between fish taxonomic and functional diversity and latitude, depth, substrate, and time at the regional scale, but not at the coast-wide scale, suggesting that coast-wide patterns can obscure important correlates at smaller scales. Our study provides insight into complex diversity patterns of the deep water soft substrate benthic ecosystems off the US West Coast.

Evaluating Temporal Consistency in Marine Biodiversity Hotspots.

With the ongoing crisis of biodiversity loss and limited resources for conservation, the concept of biodiversity hotspots has been useful in determining conservation priority areas. However, there has been limited research into how temporal variability in biodiversity may influence conservation area prioritization. To address this information gap, we present an approach to evaluate the temporal consistency of biodiversity hotspots in large marine ecosystems. Using a large scale, public monitoring dataset collected over an eight year period off the US Pacific Coast, we developed a methodological approach for avoiding biases associated with hotspot delineation. We aggregated benthic fish species data from research trawls and calculated mean hotspot thresholds for fish species richness and Shannon's diversity indices over the eight year dataset. We used a spatial frequency distribution method to assign hotspot designations to the grid cells annually. We found no areas containing consistently high biodiversity through the entire study period based on the mean thresholds, and no grid cell was designated as a hotspot for greater than 50% of the time-series. To test if our approach was sensitive to sampling effort and the geographic extent of the survey, we followed a similar routine for the northern region of the survey area. Our finding of low consistency in benthic fish biodiversity hotspots over time was upheld, regardless of biodiversity metric used, whether thresholds were calculated per year or across all years, or the spatial extent for which we calculated thresholds and identified hotspots. Our results suggest that static measures of benthic fish biodiversity off the US West Coast are insufficient for identification of hotspots and that long-term data are required to appropriately identify patterns of high temporal variability in biodiversity for these highly mobile taxa. Given that ecological communities are responding to a changing climate and other environmental perturbations, our work highlights the need for scientists and conservation managers to consider both spatial and temporal dynamics when designating biodiversity hotspots.

Elemental markers in elasmobranchs: effects of environmental history and growth on vertebral chemistry.

Differences in the chemical composition of calcified skeletal structures (e.g. shells, otoliths) have proven useful for reconstructing the environmental history of many marine species. However, the extent to which ambient environmental conditions can be inferred from the elemental signatures within the vertebrae of elasmobranchs (sharks, skates, rays) has not been evaluated. To assess the relationship between water and vertebral elemental composition, we conducted two laboratory studies using round stingrays, Urobatis halleri, as a model species. First, we examined the effects of temperature (16°, 18°, 24°C) on vertebral elemental incorporation (Li/Ca, Mg/Ca, Mn/Ca, Zn/Ca, Sr/Ca, Ba/Ca). Second, we tested the relationship between water and subsequent vertebral elemental composition by manipulating dissolved barium concentrations (1x, 3x, 6x). We also evaluated the influence of natural variation in growth rate on elemental incorporation for both experiments. Finally, we examined the accuracy of classifying individuals to known environmental histories (temperature and barium treatments) using vertebral elemental composition. Temperature had strong, negative effects on the uptake of magnesium (DMg) and barium (DBa) and positively influenced manganese (DMn) incorporation. Temperature-dependent responses were not observed for lithium and strontium. Vertebral Ba/Ca was positively correlated with ambient Ba/Ca. Partition coefficients (DBa) revealed increased discrimination of barium in response to increased dissolved barium concentrations. There were no significant relationships between elemental incorporation and somatic growth or vertebral precipitation rates for any elements except Zn. Relationships between somatic growth rate and DZn were, however, inconsistent and inconclusive. Variation in the vertebral elemental signatures of U. halleri reliably distinguished individual rays from each treatment based on temperature (85%) and Ba exposure (96%) history. These results support the assumption that vertebral elemental composition reflects the environmental conditions during deposition and validates the use of vertebral elemental signatures as natural markers in an elasmobranch. Vertebral elemental analysis is a promising tool for the study of elasmobranch population structure, movement, and habitat use.

The relationship between maternal phenotype and offspring quality: do older mothers really produce the best offspring?

Maternal effects are increasingly recognized as important drivers of population dynamics and determinants of evolutionary trajectories. Recently, there has been a proliferation of studies finding or citing a positive relationship between maternal size/age and offspring size or offspring quality. The relationship between maternal phenotype and offspring size is intriguing in that it is unclear why young mothers should produce offspring of inferior quality or fitness. Here we evaluate the underlying evolutionary pressures that may lead to a maternal size/age-offspring size correlation and consider the likelihood that such a correlation results in a positive relationship between the age or size of mothers and the fitness of their offspring. We find that, while there are a number of reasons why selection may favor the production of larger offspring by larger mothers, this change in size is more likely due to associated changes in the maternal phenotype that affect the offspring size-performance relationship. We did not find evidence that the offspring of older females should have intrinsically higher fitness. When we explored this issue theoretically, the only instance in which smaller mothers produce suboptimal offspring sizes is when a (largely unsupported) constraint on maximum offspring size is introduced into the model. It is clear that larger offspring fare better than smaller offspring when reared in the same environment, but this misses a critical point: different environments elicit selection for different optimal sizes of young. We suggest that caution should be exercised when interpreting the outcome of offspring-size experiments when offspring from different mothers are reared in a common environment, because this approach may remove the source of selection (e.g., reproducing in different context) that induced a shift in offspring size in the first place. It has been suggested that fish stocks should be managed to preserve these older age classes because larger mothers produce offspring with a greater chance of survival and subsequent recruitment. Overall, we suggest that, while there are clear and compelling reasons for preserving older females in exploited populations, there is little theoretical justification or evidence that older mothers produce offspring with higher per capita fitness than do younger mothers.

Application of diffusion approximation for risk assessments of sea turtle populations.

Population viability analysis (PVA) to forecast extinction risk is a commonly used tool in decision- and policy-making processes of governments and conservation organizations. A drawback to PVA is the high degree of uncertainty in these forecasts due to both population stochasticity and parameter estimation uncertainty. With sparse or noisy data, extinction probabilities frequently have 95% confidence intervals ranging from 0 to 1. To make stochastic simulation results more interpretable, we present a new metric, susceptibility to quasi-extinction (SQE), to assess whether or not a population is at risk of declining to a prespecified level (quasi-extinction). Following standard methods for diffusion approximation of extinction risk, we use a parametric bootstrap to determine the 95% CI for the probability of quasi-extinction. SQE is the proportion of this parametric bootstrap that indicates a high (defined as > or = 0.90) probability of quasi-extinction, resulting in a point estimate that integrates both parameter uncertainty and stochasticity in extinction forecasting. We demonstrate the application of the metric with sea turtle nest census data, which have a high degree of year-to-year variance and represent only a small fraction of the total population. Using population simulations, we found that for these types of data a critical SQE value of 0.40 corresponds to populations that have a true risk of quasi-extinction. The metric has an accuracy of > 80%, which can be increased further by lowering the 0.40 threshold and trading off Type I error (considering a population to be "not at risk" when it actually is) and Type II error (considering a population to be "at risk" when it actually is not), giving managers a flexible and quantitative tool for assessments of population status.

Models to compare management options for a protogynous fish.

Populations of gag (Mycteroperca microlepis), a hermaphroditic grouper, have experienced a dramatic shift in sex ratio over the past 25 years due to a decline in older age classes. The highly female-skewed sex ratio can be predicted as a consequence of increased fishing mortality that truncates the age distribution, and raises some concern about the overall fitness of the population. Management efforts may need to be directed toward maintenance of sex ratio as well as stock size, with evaluations of recruitment based on sex ratio or male stock size in addition to the traditional female-based stock-recruitment relationship. We used two stochastic, age-structured models to heuristically compare the effects of reducing fishing mortality on different life history stages and the relative impact of reductions in fertilization rates that may occur with highly skewed sex ratios. Our response variables included population size, sex ratio, lost egg fertility, and female spawning stock biomass. Population growth rates were highest for scenarios that reduced mortality for female gag (nearshore closure), while improved sex ratios were obtained most quickly with spawning reserves. The effect of reduced fertility through sex ratio bias was generally low but depended on the management scenario employed. Our results demonstrate the utility of evaluation of fishery management scenarios through model analysis and simulation, the synergistic interaction of life history and response to changes in mortality rates, and the importance of defining management goals.

Carryover aquatic effects on survival of metamorphic frogs during pond emigration.

In organisms with complex life cycles, physiological stressors during early life stages may have fitness-level impacts that are delayed into later stages or habitats. We tested the hypothesis that body size and date of metamorphosis, which are highly responsive to aquatic stressors, influence post-metamorphic survival and movement patterns in the terrestrial phase of an ephemeral pond-breeding frog by examining these traits in two populations of northern red-legged frogs (Rana aurora aurora). To increase variation of body size at metamorphosis, we manipulated food availability for 314 of 1045 uniquely marked tadpoles and estimated the probability that frogs survived and emigrated using concentric rings of drift fencing surrounding ponds and Bayesian capture-recapture modeling. The odds of surviving and emigrating from the ponds to the innermost drift fences, approximately 12 m, increased by factors of 2.20 (95% credibility intervals 1.39-4.23) and 2.54 (0.94-4.91) with each millimeter increase in snout-vent length and decreased by factors of 0.91 (0.85-0.96) and 0.89 (0.80-1.00) with each day's delay in metamorphosis for the two ponds. The odds of surviving and moving to the next ring of fencing, 12 m to approximately 40 m from the ponds, increased by a factor of 1.20 (0.45-4.06) with each millimeter increase in size. Our results demonstrated that body size and timing of metamorphosis relate strongly to the performance of newly metamorphosed frogs during their initial transition into terrestrial habitat. Carryover effects of aquatic stressors that reduce size and delay metamorphosis may have population-level impacts that are not expressed until terrestrial stages. Since changes in both aquatic and terrestrial systems are implicated in many amphibian declines, quantifying both immediate and delayed effects of stressors on demographic rates is critical to sound management.