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.

An experimental test of stationary lay-up periods and simulated transit on biofouling accumulation and transfer on ships.

Biofouling accumulation on ships' submerged surfaces typically occurs during stationary periods that render surfaces more susceptible to colonization than when underway. As a result, stationary periods longer than typical port residence times (hours to days), often referred to as lay-ups, can have deleterious effects on hull maintenance strategies, which aim to minimize biofouling impacts on ship operations and the likelihood of invasive species transfers. This experimental study tested the effects of different lay-up durations on the magnitude of biofouling, before and after exposure to flow, using fouling panels with three coating treatments (antifouling, foul-release, and controls), at two sites, and a portable field flume to simulate voyage sheer forces. Control panels subjected to extended stationary durations (28-, 45- and 60-days) had significantly higher biofouling cover and there was a 13- to 25-fold difference in biofouling accumulation between 10-days and 28-days of static immersion. Prior to flume exposure, the antifouling coating prevented biofouling accumulation almost entirely at one site and kept it below 20% at the other. Foul-release coatings also proved effective, especially after flume exposure, which reduced biofouling at one site from >52% to <6% cover (on average). The experimental approach was beneficial for co-locating panel deployments and flume processing using a consistent (standardized) flow regime on large panels across sites of differing conditions and biofouling assemblages. While lay-ups of commercial vessels are relatively common, inevitable, and unavoidable, it is important to develop a better understanding of the magnitude of their effects on biofouling of ships' submerged surfaces and to develop workable post-lay-up approaches to manage and respond to elevated biofouling accumulation that may result.

Spatial and temporal dynamics of Antarctic shallow soft-bottom benthic communities: ecological drivers under climate change.

BACKGROUND: Marine soft sediments are some of the most widespread habitats in the ocean, playing a vital role in global carbon cycling, but are amongst the least studied with regard to species composition and ecosystem functioning. This is particularly true of the Polar Regions, which are currently undergoing rapid climate change, the impacts of which are poorly understood. Compared to other latitudes, Polar sediment habitats also experience additional environmental drivers of strong seasonality and intense disturbance from iceberg scouring, which are major structural forces for hard substratum communities. This study compared sediment assemblages from two coves, near Rothera Point, Antarctic Peninsula, 67°S in order to understand the principal drivers of community structure, for the first time, evaluating composition across all size classes from mega- to micro-fauna. RESULTS: Morpho-taxonomy identified 77 macrofaunal species with densities of 464-16,084 individuals m-2. eDNA metabarcoding of microfauna, in summer only, identified a higher diversity, 189 metazoan amplicon sequence variants (ASVs) using the 18S ribosomal RNA and 249 metazoan ASVs using the mitochondrial COI gene. Both techniques recorded a greater taxonomic diversity in South Cove than Hangar Cove, with differences in communities between the coves, although the main taxonomic drivers varied between techniques. Morphotaxonomy identified the main differences between coves as the mollusc, Altenaeum charcoti, the cnidarian Edwardsia sp. and the polychaetes from the family cirratulidae. Metabarcoding identified greater numbers of species of nematodes, crustaceans and Platyhelminthes in South Cove, but more bivalve species in Hangar Cove. There were no detectable differences in community composition, measured through morphotaxonomy, between seasons, years or due to iceberg disturbance. CONCLUSIONS: This study found that unlike hard substratum communities the diversity of Antarctic soft sediment communities is correlated with the same factors as other latitudes. Diversity was significantly correlated with grain size and organic content, not iceberg scour. The increase in glacial sediment input as glaciers melt, may therefore be more important than increased iceberg disturbance.

Geographic variation in marine invasions among large estuaries: effects of ships and time.

Coastal regions exhibit strong geographic patterns of nonnative species richness. Most invasions in marine ecosystems are known from bays and estuaries, where ship-mediated transfers (on hulls or in ballasted materials) have been a dominant vector of species introductions. Conspicuous spatial differences in nonnative species richness exist among bays, but the quantitative relationship between invasion magnitude and shipping activity across sites is largely unexplored. Using data on marine invasions (for invertebrates and algae) and commercial shipping across 16 large bays in the United States, we estimated (1) geographic variation in nonnative species richness attributed to ships, controlling for effects of salinity and other vectors, (2) changes through time in geographic variation of these ship-mediated invasions, and (3) effects of commercial ship traffic and ballast water discharge magnitude on nonnative species richness. For all nonnative species together (regardless of vector, salinity, or time period), species richness differed among U.S. coasts, being significantly greater for Pacific Coast bays than Atlantic or Gulf Coast bays. This difference also existed when considering only species attributed to shipping (or ballast water), controlling for time and salinity. Variation in nonnative species richness among Pacific Coast bays was strongly affected by these same criteria. San Francisco Bay, California, had over 200 documented nonnative species, more than twice that reported for other bays, but many species were associated with other (non-shipping) vectors or the extensive low-salinity habitats (unavailable in some bays). When considering only ship- or ballast-mediated introductions in high-salinity waters, the rate of newly detected invasions in San Francisco Bay has converged increasingly through time on that for other Pacific Coast bays, appearing no different since 1982. Considering all 16 bays together, there was no relationship between either (1) number of ship arrivals (from foreign ports) and number of introductions attributed to ships since 1982 or (2) volume of foreign ballast water discharge and number of species attributed to ballast water since 1982. These shipping measures are likely poor proxies for propagule supply, although they are sometimes used as such, highlighting a fundamental gap in data needed to evaluate invasion dynamics and management strategies.

Predator control of marine communities increases with temperature across 115 degrees of latitude.

Early naturalists suggested that predation intensity increases toward the tropics, affecting fundamental ecological and evolutionary processes by latitude, but empirical support is still limited. Several studies have measured consumption rates across latitude at large scales, with variable results. Moreover, how predation affects prey community composition at such geographic scales remains unknown. Using standardized experiments that spanned 115° of latitude, at 36 nearshore sites along both coasts of the Americas, we found that marine predators have both higher consumption rates and consistently stronger impacts on biomass and species composition of marine invertebrate communities in warmer tropical waters, likely owing to fish predators. Our results provide robust support for a temperature-dependent gradient in interaction strength and have potential implications for how marine ecosystems will respond to ocean warming.

1 °C warming increases spatial competition frequency and complexity in Antarctic marine macrofauna.

Environmental conditions of the Southern Ocean around Antarctica have varied little for >5 million years but are now changing. Here, we investigated how warming affects competition for space. Little considered in the polar regions, this is a critical component of biodiversity response. Change in competition in response to environment forcing might be detectable earlier than individual species presence/absence or performance measures (e.g. growth). Examination of fauna on artificial substrata in Antarctica's shallows at ambient or warmed temperature found that, mid-century predicted 1°C warming (throughout the year or just summer-only), increased the probability of individuals encountering spatial competition, as well as density and complexity of such interactions. 2°C, late century predicted warming, increased variance in the probability and density of competition, but overall, competition did not significantly differ from ambient (control) levels. In summary only 1°C warming increased probability, density and complexity of spatial competition, which seems to be summer-only driven.

Lack of long-term acclimation in Antarctic encrusting species suggests vulnerability to warming.

Marine encrusting communities play vital roles in benthic ecosystems and have major economic implications with regards to biofouling. However, their ability to persist under projected warming scenarios remains poorly understood and is difficult to study under realistic conditions. Here, using heated settlement panel technologies, we show that after 18 months Antarctic encrusting communities do not acclimate to either +1 °C or +2 °C above ambient temperatures. There is significant up-regulation of the cellular stress response in warmed animals, their upper lethal temperatures decline with increasing ambient temperature and population genetic analyses show little evidence of differential survival of genotypes with treatment. By contrast, biofilm bacterial communities show no significant differences in community structure with temperature. Thus, metazoan and bacterial responses differ dramatically, suggesting that ecosystem responses to future climate change are likely to be far more complex than previously anticipated.

Mitochondrial DNA reveals multiple Northern Hemisphere introductions of Caprella mutica (Crustacea, Amphipoda).

Caprella mutica (Crustacea, Amphipoda) has been widely introduced to non-native regions in the last 40 years. Its native habitat is sub-boreal northeast Asia, but in the Northern Hemisphere, it is now found on both coasts of North America, and North Atlantic coastlines of Europe. Direct sequencing of mitochondrial DNA (cytochrome c oxidase subunit I gene) was used to compare genetic variation in native and non-native populations of C. mutica. These data were used to investigate the invasion history of C. mutica and to test potential source populations in Japan. High diversity (31 haplotypes from 49 individuals), but no phylogeographical structure, was identified in four populations in the putative native range. In contrast, non-native populations showed reduced genetic diversity (7 haplotypes from 249 individuals) and informative phylogeographical structure. Grouping of C. mutica populations into native, east Pacific, and Atlantic groups explained the most among-region variation (59%). This indicates independent introduction pathways for C. mutica to the Pacific and Atlantic coasts of North America. Two dominant haplotypes were identified in eastern and western Atlantic coastal populations, indicating several dispersal routes within the Atlantic. The analysis indicated that several introductions from multiple sources were likely to be responsible for the observed global distribution of C. mutica, but the pathways were least well defined among the Atlantic populations. The four sampled populations of C. mutica in Japan could not be identified as the direct source of the non-native populations examined in this study. The high diversity within the Japan populations indicates that the native range needs to be assessed at a far greater scale, both within and among populations, to accurately assess the source of the global spread of C. mutica.

Environmental tolerance of Caprella mutica: implications for its distribution as a marine non-native species.

Physiological tolerances limit the distribution of marine species, with geographical ranges being set by environmental factors, such as temperature and salinity, which affect the rates of vital processes and survival of marine ectotherms. The physiological tolerances of the non-native marine amphipod Caprella mutica were investigated in laboratory experiments. Adult C. mutica were collected from a fish farm on the west coast of Scotland and exposed to a range of temperatures and salinities for 48 h. C. mutica were tolerant of a broad range of temperature and salinity conditions, with 100% mortality at 30 degrees C (48 h LT50, 28.3+/-0.4 degrees C), and salinities lower than 16 (48 h LC50, 18.7+/-0.2). Although lethargic at low temperatures (2 degrees C), no mortality was observed, and the species is known to survive at temperatures as low as -1.8 degrees C. The upper LC(50) was greater than the highest salinity tested (40), thus it is unlikely that salinity will limit the distribution of C. mutica in open coastal waters. However, the species will be excluded from brackish water environments such as the heads of sea lochs or estuaries. The physiological tolerances of C. mutica are beyond the physical conditions experienced in its native or introduced range and are thus unlikely to be the primary factors limiting its present distribution and future spread.

Warming by 1°C Drives Species and Assemblage Level Responses in Antarctica's Marine Shallows.

Forecasting assemblage-level responses to climate change remains one of the greatest challenges in global ecology [1, 2]. Data from the marine realm are limited because they largely come from experiments using limited numbers of species [3], mesocosms whose interior conditions are unnatural [4], and long-term correlation studies based on historical collections [5]. We describe the first ever experiment to warm benthic assemblages to ecologically relevant levels in situ. Heated settlement panels were used to create three test conditions: ambient and 1°C and 2°C above ambient (predicted in the next 50 and 100 years, respectively [6]). We observed massive impacts on a marine assemblage, with near doubling of growth rates of Antarctic seabed life. Growth increases far exceed those expected from biological temperature relationships established more than 100 years ago by Arrhenius. These increases in growth resulted in a single "r-strategist" pioneer species (the bryozoan Fenestrulina rugula) dominating seabed spatial cover and drove a reduction in overall diversity and evenness. In contrast, a 2°C rise produced divergent responses across species growth, resulting in higher variability in the assemblage. These data extend our ability to expand, integrate, and apply our knowledge of the impact of temperature on biological processes to predict organism, species, and ecosystem level ecological responses to regional warming.

Response to van der Meer.

In our recent Current Biology paper [1], we describe an ocean warming experiment in which we manipulated the temperature of panels set on the seafloor to provide a realistic and relevant indication of how benthic communities may change under future ocean warming. We describe increases in growth associated with warming by 1°C, with growth rates up to doubled in some species. The definition of Q10 is a measure of the temperature sensitivity of an enzymatic reaction rate or a physiological process due to an increase by 10°C; doubling of growth rates with a 1°C change gives Q10s around 1,000. In his correspondence, Jaap van der Meer [2] questions our methods and provides alternative analyses which lead him to conclude that our observed increases in growth rate were in fact much lower and in accordance with previous studies from temperate zones. We provide justification for our use of absolute growth rate, justification for not using instantaneous growth rate (or a measure of growth in proportion to previous growth) and encourage the on-going discussion of how to measure and compare growth rates.

The Panama Canal and the transoceanic dispersal of marine invertebrates: evaluation of the introduced amphipod Paracaprella pusilla Mayer, 1890 in the Pacific Ocean.

Although the Panama Canal is one of the major corridors for shipping and potential dispersal of marine invaders in the tropics, little is known about the effect that the Canal has had on the distribution of marine biota. In this study, we (a) document the existence of established populations of the Western Atlantic caprellid amphipod Paracaprella pusilla, Mayer, 1890 for the first time at the Pacific entrance to the Canal, (b) review its distribution in the Pacific Ocean, and (c) evaluate possible mechanisms of introduction. The confirmed distribution of P. pusilla in the Pacific Ocean is limited to Australia, Hawaii, and Panama, despite earlier published reports from Chile and China. Laboratory experiments demonstrated intolerance of P. pusilla to freshwater, causing 100% mortality, and suggest invasion of the Pacific coast of Panama occurred through the Canal via ships' ballast water or by secondary spread via ships (ballast water or hull fouling) from another Pacific region.

Promoting invasive species control and eradication in the sea: options for managing the tunicate invader Didemnum vexillum in Sitka, Alaska.

Bioinvasions are a significant force of change--and economic and ecological threat--in marine ecosystems. The threat now encroaches on Alaska, which has had relatively few invasions compared to other global regions, prompting need to develop new incursion response tools. We appraised five 'eco-friendly' immersion treatment options (dilute acetic acid, dilute bleach, freshwater, brine and hypoxia) at either minute- or hour-scale exposures to kill the invasive tunicate Didemnum vexillum. Data revealed 100% treatment efficacy after two minutes in acetic acid, ten minutes in bleach, four hours in freshwater and over four hours in brine solution. We also demonstrated the importance of monitoring D. vexillum recovery for at least three weeks, since seemingly destroyed colonies rebounded during this timeframe. Combined, these findings provide insights towards a bay-scale eradication and post-border management plan applicable to the recent D. vexillum incursion in Whiting Harbor, Alaska and other shallow, inshore invasion sites.