Fertilization limitation of Diadema antillarum on coral reefs in the Florida Keys.

Mass mortality of the sea urchin Diadema antillarum due to disease outbreaks in 1983 and 1991 decimated populations in the Florida Keys, and they have yet to recover. Here, we use a coupled advection-diffusion and fertilization-kinetics model to test the hypothesis that these populations are fertilization limited. We found that fertilization success was ≥ 96% prior to the first disease outbreak, decreased substantially following recurrent disease to 3%, and has since remained low. By investigating the combined effects of physical factors (population spatial extent and current velocity) and sea urchin behavior (aggregation) on density-dependent fertilization success, we show that fertilization success at a given density increases with increasing population spatial extent and decreasing current velocity, and is greater under simulated aggregation behavior of D. antillarum. However, at present population densities, the increase in fertilization success due to aggregation is < 1%, even under the most favorable physical conditions. These results indicate that populations are severely fertilization limited, and that Allee effects at low population density will continue to limit recovery. Our results can serve as a practical guide to managers in the development of coral reef restoration strategies, including the design of a D. antillarum restocking program to obtain reproductively viable populations.

Modeling effects of climate change and phase shifts on detrital production of a kelp bed.

The exchange of energy and nutrients between ecosystems (i.e., resource subsidies) plays a central role in ecological dynamics over a range of spatial and temporal scales. Little attention has been paid to the role of anthropogenic impacts on natural systems in altering the magnitude, timing, and quality of resource subsidies. Kelp ecosystems are highly productive on a local scale and export over 80% of kelp primary production as detritus, subsidizing consumers across broad spatial scales. Here, we generate a model of detrital production from a kelp bed in Nova Scotia to hindcast trends in detrital production based on temperature and wave height recorded in the study region from 1976 to 2009, and to project changes in detrital production that may result from future climate change. Historical and projected increases in temperature and wave height led to higher rates of detrital production through increased blade breakage and kelp dislodgment from the substratum, but this reduced kelp biomass and led to a decline in detrital production in the long-term. We also used the model to demonstrate that the phase shift from a highly productive kelp bed to a low-productivity barrens, driven by the grazing activity of sea urchins, reduces kelp detrital production by several orders of magnitude, an effect that would be exacerbated by projected increases in temperature and wave action. These results indicate that climate-mediated changes in ecological dynamics operating on local scales may alter the magnitude of resource subsidies to adjacent ecosystems, affecting ecological dynamics on regional scales.

Validating the identity of Paramoeba invadens, the causative agent of recurrent mass mortality of sea urchins in Nova Scotia, Canada.

Green sea urchins Strongylocentrotus droebachiensis along the coast of Nova Scotia, Canada, suffer mass mortalities from infection by the pathogenic amoeba Paramoeba invadens Jones, 1985. It has been speculated that P. invadens could be a form of Neoparamoeba pemaquidensis, a species associated with disease in S. droebachiensis and lobsters in the northeast USA. During a disease outbreak in fall 2011, we isolated amoebae from moribund urchins collected from 4 locations along ~200 km of coastline. In laboratory infection trials, we found that timing and rate of morbidity corresponded to that of similar experiments conducted in the early 1980s, when P. invadens was first identified. All isolates had a similar size and morphology to the original description, including an absence of microscales. Sequences of nuclear SSU rDNA show that disease was caused by one 'species' of amoeba across the range sampled. Phylogenetic analyses prove that P. invadens is not conspecific with N. pemaquidensis, but is a distinct species most closely related to N. branchiphila, a suspected pathogen of sea urchins Diadema aff. antillarum in the Canary Islands, Spain. Morphology and closest phylogenetic affinities suggest that P. invadens would be assignable to the genus Neoparamoeba; however, nuclear SSU rDNA trees show that Neoparamoeba and Paramoeba are phylogenetically inseparable. Therefore, we treat Neoparamoeba as a junior synonym of Paramoeba, with P. invadens retaining that name, and N. pemaquidensis and N. aestuarina reverting to their original names (P. pemaquidensis and P. aestuarina), and with new combinations for N. branchiphila Dykova et al., 2005, and N. perurans Young et al., 2007, namely P. branchiphila comb. nov. and P. perurans comb. nov.

FORMATION AND PROPAGATION OF FEEDING FRONTS IN BENTHIC MARINE INVERTEBRATES: A MODELING APPROACH.

Feeding fronts are a striking pattern of spatial distribution observed in both marine and terrestrial ecological systems. These fronts not only determine the abundance and distribution of prey populations, but on a broader scale they may also affect the structure and dynamics of entire communities. Several mechanisms leading to the formation of feeding fronts have been proposed, and chemotaxis has been suggested as an important component. Here we develop two mathematical models that show front formation can occur with simple kinesis (and without chemotaxis) in two marine invertebrates with different feeding habits: a microphagous sea star (Oreaster reticulatus) that feeds on sediments and an herbivorous sea urchin (Strongylocentrotus droebachiensis) that grazes kelp beds. We utilize a large body of detailed empirical information on movement pattern, foraging behavior, and front dynamics for each species to develop, parameterize, and evaluate our models. We found that our model predictions for the rate of advance of a front and its relationship to the density of consumers at the front were in close agreement with independently collected, empirical observations in both systems. This work shows that simple local interactions between mobile consumers and a stationary resource can result in large-scale heterogeneous patterns of abundance of both species.

Importance of spatial population characteristics on the fertilization rates of sea urchins.

We show that inclusion of population characteristics in coupled advection-diffusion and fertilization-kinetics models results in higher fertilization rates than those previously reported in theoretical studies. We incorporate parameters related to both individuals and populations by running simulations over a large spatial scale and incorporating sperm contribution from multiple males. We compare predictions for three subpopulations of the sea urchin Strongylocentrotus droebachiensis (those occupying kelp beds, barrens, and grazing fronts) to observations from small-scale experiments, and estimate effects of population size and current velocity in each subpopulation. Model outputs suggest that fertilization rates are low in kelp beds, intermediate in barrens, and high in grazing fronts. In all populations, increasing current velocity has a negative effect on the relationship between fertilization rate and downstream distance of gametes after release, but no effect on the relationship between fertilization rate and elapsed time since gamete release. Our model output was most sensitive to changes in the number of spawning males and the sperm release rate, suggesting that spawning synchrony and high gonadic index could greatly increase the fertilization success in sea urchins.

Relating dispersal and range expansion of California sea otters.

Linking dispersal and range expansion of invasive species has long challenged theoretical and quantitative ecologists. Subtle differences in dispersal can yield large differences in geographic spread, with speeds ranging from constant to rapidly increasing. We developed a stage-structured integrodifference equation (IDE) model of the California sea otter range expansion that occurred between 1914 and 1986. The non-spatial model, a linear matrix population model, was coupled to a suite of candidate dispersal kernels to form stage-structured IDEs. Demographic and dispersal parameters were estimated independent of range expansion data. Using a single dispersal parameter, alpha, we examined how well these stage-structured IDEs related small scale demographic and dispersal processes with geographic population expansion. The parameter alpha was estimated by fitting the kernels to dispersal data and by fitting the IDE model to range expansion data. For all kernels, the alpha estimate from range expansion data fell within the 95% confidence intervals of the alpha estimate from dispersal data. The IDE models with exponentially bounded kernels predicted invasion velocities that were captured within the 95% confidence bounds on the observed northbound invasion velocity. However, the exponentially bounded kernels yielded range expansions that were in poor qualitative agreement with range expansion data. An IDE model with fat (exponentially unbounded) tails and accelerating spatial spread yielded the best qualitative match. This model explained 94% and 97% of the variation in northbound and southbound range expansions when fit to range expansion data. These otters may have been fat-tailed accelerating invaders or they may have followed a piece-wise linear spread first over kelp forests and then over sandy habitats. Further, habitat-specific dispersal data could resolve these explanations.