Stage-specific overcompensation, the hydra effect, and the failure to eradicate an invasive predator.

As biological invasions continue to increase globally, eradication programs have been undertaken at significant cost, often without consideration of relevant ecological theory. Theoretical fisheries models have shown that harvest can actually increase the equilibrium size of a population, and uncontrolled studies and anecdotal reports have documented population increases in response to invasive species removal (akin to fisheries harvest). Both findings may be driven by high levels of juvenile survival associated with low adult abundance, often referred to as overcompensation. Here we show that in a coastal marine ecosystem, an eradication program resulted in stage-specific overcompensation and a 30-fold, single-year increase in the population of an introduced predator. Data collected concurrently from four adjacent regional bays without eradication efforts showed no similar population increase, indicating a local and not a regional increase. Specifically, the eradication program had inadvertently reduced the control of recruitment by adults via cannibalism, thereby facilitating the population explosion. Mesocosm experiments confirmed that adult cannibalism of recruits was size-dependent and could control recruitment. Genomic data show substantial isolation of this population and implicate internal population dynamics for the increase, rather than recruitment from other locations. More broadly, this controlled experimental demonstration of stage-specific overcompensation in an aquatic system provides an important cautionary message for eradication efforts of species with limited connectivity and similar life histories.

Balanced polymorphism fuels rapid selection in an invasive crab despite high gene flow and low genetic diversity.

Adaptation across environmental gradients has been demonstrated in numerous systems with extensive dispersal, despite high gene flow and consequently low genetic structure. The speed and mechanisms by which such adaptation occurs remain poorly resolved, but are critical to understanding species spread and persistence in a changing world. Here, we investigate these mechanisms in the European green crab Carcinus maenas, a globally distributed invader. We focus on a northwestern Pacific population that spread across >12 degrees of latitude in 10 years from a single source, following its introduction <35 years ago. Using six locations spanning >1500 km, we examine genetic structure using 9376 single nucleotide polymorphisms (SNPs). We find high connectivity among five locations, with significant structure between these locations and an enclosed lagoon with limited connectivity to the coast. Among the five highly connected locations, the only structure observed was a cline driven by a handful of SNPs strongly associated with latitude and winter temperature. These SNPs are almost exclusively found in a large cluster of genes in strong linkage disequilibrium that was previously identified as a candidate for cold tolerance adaptation in this species. This region may represent a balanced polymorphism that evolved to promote rapid adaptation in variable environments despite high gene flow, and which now contributes to successful invasion and spread in a novel environment. This research suggests an answer to the paradox of genetically depauperate yet successful invaders: populations may be able to adapt via a few variants of large effect despite low overall diversity.

The role of functional diversity and facilitation in small-scale pollinator habitat.

People in urban and rural areas are planting habitat patches for pollinators in response to growing public awareness of the risks of pollinator declines; yet research rarely has been undertaken to inform the composition of such patches. Determining which key functional plant traits to prioritize and how plant-pollinator interaction dynamics operate in these small-scale, fragmented patches is critical to ensuring the efficacy of pollinator restoration efforts across landscapes. We established small-scale (2.5 m diameter) experimental patches and manipulated plant diversity and resource level (nectar) to determine the effects on pollinator abundance, pollinator diversity, and plant-pollinator facilitation-competition dynamics. Our results showed that in small-scale habitat, plant diversity and resource availability significantly affected the abundance and diversity of pollinating insects. Specifically, the treatments that contained high-resource plant species increased pollinator abundance and diversity the most. Plant diversity increased pollinator diversity and abundance only in the absence of high-resource plants. Pollination facilitation was observed in high-resource treatments, but varied among plant species. Competition for pollinators was observed in high-diversity treatments but did not affect seed set for high-resource plants in any of the treatments. Our results suggest that managers or landowners planting small-scale pollinator habitat should prioritize including species with high nectar production, and secondarily, a diverse mix of species if space and resources allow. The protocols we used to monitor pollinators can be used by community science observers with limited training, expanding the potential for assessment of future pollinator habitat restoration projects. Shared research identifying features critical to effective restoration will help conserve plant-pollinator mutualisms across landscapes.

Assessing accuracy in citizen science-based plant phenology monitoring.

In the USA, thousands of volunteers are engaged in tracking plant and animal phenology through a variety of citizen science programs for the purpose of amassing spatially and temporally comprehensive datasets useful to scientists and resource managers. The quality of these observations and their suitability for scientific analysis, however, remains largely unevaluated. We aimed to evaluate the accuracy of plant phenology observations collected by citizen scientist volunteers following protocols designed by the USA National Phenology Network (USA-NPN). Phenology observations made by volunteers receiving several hours of formal training were compared to those collected independently by a professional ecologist. Approximately 11,000 observations were recorded by 28 volunteers over the course of one field season. Volunteers consistently identified phenophases correctly (91% overall) for the 19 species observed. Volunteers demonstrated greatest overall accuracy identifying unfolded leaves, ripe fruits, and open flowers. Transitional accuracy decreased for some species/phenophase combinations (70% average), and accuracy varied significantly by phenophase and species (p < 0.0001). Volunteers who submitted fewer observations over the period of study did not exhibit a higher error rate than those who submitted more total observations. Overall, these results suggest that volunteers with limited training can provide reliable observations when following explicit, standardized protocols. Future studies should investigate different observation models (i.e., group/individual, online/in-person training) over subsequent seasons with multiple expert comparisons to further substantiate the ability of these monitoring programs to supply accurate broadscale datasets capable of answering pressing ecological questions about global change.

Integration of an invasive consumer into an estuarine food web: direct and indirect effects of the New Zealand mud snail.

Introduced species interact both directly and indirectly with native species. We examine interactions between the introduced New Zealand mud snail (Potamopyrgus antipodarum) and native estuarine invertebrates and predators through experiments and field studies. A widely held management concern is that when P. antipodarum, which has low nutritional value, becomes abundant, it replaces nutritious prey in fish diets. We tested two key components of this view: (1) that fish consume, but get little direct nutritional value from P. antipodarum; and (2) that P. antipodarum has an indirect negative effect on fish by reducing the energy derived from native prey. We also examined predation by the native signal crayfish, Pacifastacus leniusculus. Laboratory feeding trials showed that both crayfish and fish consume P. antipodarum, a direct effect. Crayfish consumed and successfully digested higher numbers of snails than did fish [Pacific staghorn sculpin (Leptocottus armatus), three spine stickleback (Gasterosteus aculeatus), and juvenile starry flounder (Platicthys stellatus)]. P. antipodarum occurred at low frequencies in the stomachs of wild-caught fish. More interesting were the indirect effects of this invader, which ran counter to predictions. P. antipodarum presence was associated with no change or an increase in the amount of energy derived from native prey by predators. The presence of P. antipodarum also led to increased consumption of and preference for the native amphipod Americorophium salmonis over the native isopod Gnorimosphaeroma insulare. This is an example of short-term, asymmetric, apparent competition, in which the presence of one prey species (snails) increases predation on another prey species (the amphipod).

Prozac in the water: Chronic fluoxetine exposure and predation risk interact to shape behaviors in an estuarine crab.

Predators exert considerable top-down pressure on ecosystems by directly consuming prey or indirectly influencing their foraging behaviors and habitat use. Prey is, therefore, forced to balance predation risk with resource reward. A growing list of anthropogenic stressors such as rising temperatures and ocean acidification has been shown to influence prey risk behaviors and subsequently alter important ecosystem processes. Yet, limited attention has been paid to the effects of chronic pharmaceutical exposure on risk behavior or as an ecological stressor, despite widespread detection and persistence of these contaminants in aquatic environments. In the laboratory, we simulated estuarine conditions of the shore crab, Hemigrapsus oregonensis, and investigated whether chronic exposure (60 days) to field-detected concentrations (0, 3, and 30 ng/L) of the antidepressant fluoxetine affected diurnal and nocturnal risk behaviors in the presence of a predator, Cancer productus. We found that exposure to fluoxetine influenced both diurnal and nocturnal prey risk behaviors by increasing foraging and locomotor activity in the presence of predators, particularly during the day when these crabs normally stay hidden. Crabs exposed to fluoxetine were also more aggressive, with a higher frequency of agonistic interactions and increased mortality due to conflicts with conspecifics. These results suggest that exposure to field-detected concentrations of fluoxetine may alter the trade-off between resource acquisition and predation risk among crabs in estuaries. This fills an important data gap, highlighting how intra- and interspecific behaviors are altered by exposure to field concentrations of pharmaceuticals; such data more explicitly identify potential ecological impacts of emerging contaminants on aquatic ecosystems and can aid water quality management.