Andrew M. Lohrer

Bioturbators enhance ecosystem function through complex biogeochemical interactions

Predicting the consequences of species loss is critically important, given present threats to biological diversity such as habitat destruction, overharvesting and climate change. Several empirical studies have reported decreased ecosystem performance (for example, primary productivity) coincident with decreased biodiversity, although the relative influence of biotic effects and confounding abiotic factors has been vigorously debated. Whereas several investigations focused on single trophic levels (for example, grassland plants), studies of whole systems have revealed multiple layers of feedbacks, hidden drivers and emergent properties, making the consequences of species loss more difficult to predict. Here we report functionally important organisms and considerable biocomplexity in a sedimentary seafloor habitat, one of Earths most widespread ecosystems. Experimental field measurements demonstrate how the abundance of spatangoid urchins—infaunal (in seafloor sediment) grazers / deposit feeders—is positively related to primary production, as their activities change nutrient fluxes and improve conditions for production by microphytobenthos (sedimentatry microbes and unicellular algae). Declines of spatangoid urchins after trawling are well documented, and our research linking these bioturbators to important benthic–pelagic fluxes highlights potential ramifications for productivity in coastal oceans.

Muddy waters: elevating sediment input to coastal and estuarine habitats

Changes in land use and the development of coastal regions around the world have markedly increased rates of sediment input into estuarine and coastal habitats. Field studies looking at the consequences of terrestrial sediment deposition, water-borne sediment, and long-term changes in habitats indicate that increasing rates of sediment loading adversely affect the biodiversity and ecological value of estuarine and coastal ecosystems. Managing this threat requires means with which to convey the magnitude of the problem, forecast long-term trends, and assess the risks associated with changes in land use. Here we focus on approaches for assessing the risks of changes in land use, which include combining biological effect studies with catchment and hydrodynamic modeling, using statistical models that forecast the distribution and abundance of species relative to changes in habitat type, and using sensitive species that play important ecological roles as indicators of change.

Forecasting the limits of resilience: integrating empirical research with theory

Despite the increasing evidence of drastic and profound changes in many ecosystems, often referred to as regime shifts, we have little ability to understand the processes that provide insurance against such change (resilience). Modelling studies have suggested that increased variance may foreshadow a regime shift, but this requires long-term data and knowledge of the functional links between key processes. Field-based research and ground-truthing is an essential part of the heuristic that marries theoretical and empirical research, but experimental studies of resilience are lagging behind theory, management and policy requirements. Empirically, ecological resilience must be understood in terms of community dynamics and the potential for small shifts in environmental forcing to break the feedbacks that support resilience. Here, we integrate recent theory and empirical data to identify ways we might define and understand potential thresholds in the resilience of nature, and thus the potential for regime shifts, by focusing on the roles of strong and weak interactions, linkages in meta-communities, and positive feedbacks between these and environmental drivers. The challenge to theoretical and field ecologists is to make the shift from hindsight to a more predictive science that is able to assist in the implementation of ecosystem-based management.

INTERACTIONS AMONG ALIENS: APPARENT REPLACEMENT OF ONE EXOTIC SPECIES BY ANOTHER

Although many studies have documented the impact of invasive species on indigenous flora and fauna, few have rigorously examined interactions among invaders and the potential for one exotic species to replace another. European green crabs (Carcinus maenas), once common in rocky intertidal habitats of southern New England, have recently declined in abundance coincident with the invasion of the Asian shore crab (Hemigrapsus sanguineus). Over a four-year period in the late 1990s we documented a significant (40- 90%) decline in green crab abundance and a sharp (10-fold) increase in H. sanguineus at three sites in southern New England. Small, newly recruited green crabs had a significant risk of predation when paired with larger H. sanguineus in the laboratory, and recruitment of 0-yr C. maenas was reduced by H. sanguineus as well as by larger conspecifics in field- deployed cages (via predation and cannibalism, respectively). In contrast, recruitment of 0-yr H. sanguineus was not affected by larger individuals of either crab species during the same experiments. The differential susceptibility of C. maenas and H. sanguineus recruits to predation and cannibalism likely contributed to the observed decrease in C. maenas abundance and the almost exponential increase in H. sanguineus abundance during the period of study, While the Asian shore crab is primarily restricted to rocky intertidal habitats, C. maenas is found intertidally, subtidally, and in a range of substrate types in New England. Thus, the apparent replacement of C. maenas by H. sanguineus in rocky intertidal habitats of southern New England may not ameliorate the economic and ecological impacts attributed to green crab populations in other habitats of this region. For example, field experiments indicate that predation pressure on a native bivalve species (Mytilus edulis) has not nec- essarily decreased with the declines of C. maenas. While H. sanguineus has weaker per capita effects than C. maenas, its densities greatly exceed those of C. maenas at present and its population-level effects are likely comparable to the past effects of C. maenas. The Carcinus-Hemigrapsus interactions documented here are relevant in other parts of the world where green crabs and grapsid crabs interact, particularly on the west coast of North America where C. maenas has recently invaded and co-occurs with two native Hemigrapsus species.

THE EFFECTS OF HABITAT LOSS, FRAGMENTATION, AND COMMUNITY HOMOGENIZATION ON RESILIENCE IN ESTUARIES

When changes in the frequency and extent of disturbance outstrip the recovery potential of resident communities, the selective removal of species contributes to habitat loss and fragmentation across landscapes. The degree to which habitat change is likely to influence community resilience will depend on metacommunity structure and connectivity. Thus ecological connectivity is central to understanding the potential for cumulative effects to impact upon diversity. The importance of these issues to coastal marine communities, where the prevailing concept of open communities composed of highly dispersive species is being challenged, indicates that these systems may be more sensitive to cumulative impacts than previously thought. We conducted a disturbance-recovery experiment across gradients of community type and environmental conditions to assess the roles of ecological connectivity and regional variations in community structure on the recovery of species richness, total abundance, and community composition in Mahurangi Harbour, New Zealand. After 394 days, significant differences in recovery between sites were apparent. Statistical models explaining a high proportion of the variability (R2 > 0.92) suggested that community recovery rates were controlled by a combination of physical and ecological features operating across spatial scales, affecting successional processes. The dynamic and complex interplay of ecological and environmental processes we observed driving patch recovery across the estuarine landscape are integral to recovery from disturbances in heterogeneous environments. This link between succession/recovery, disturbance, and heterogeneity confirms the utility of disturbance-recovery experiments as assays for cumulative change due to fragmentation and habitat change in estuaries.

Structural complexity and vertical zonation of intertidal crabs, with focus on habitat requirements of the invasive asian shore crab, Hemigrapsus sanguineus (de Haan)

The strengths of biological processes (e.g., larval settlement, competition, predation, distribution of food resources) and physical factors (e.g., desiccation, freezing, salinity fluctuations) can be correlated with tidal height and may contribute to the vertical zonation of many rocky intertidal organisms. Habitat structural complexity has also been shown to influence the density and diversity of marine organisms and could contribute to vertical zonation where the level of complexity varies significantly with tidal height. To test the hypothesis that vertical zonation of brachyuran crabs was related to structural complexity, shelter was experimentally manipulated at 2 heights at a rocky intertidal site in Tanabe Bay, Japan. The densities of four brachyuran species, varying in size and life history type, were compared before and after the manipulation. Removal of shelter negatively affected all species, regardless of tidal height. Doubling shelter positively affected Hemigrapsus sanguineus de Haan and Leptodius exaratus Milne Edwards, especially at the tidal heights where they were initially more abundant. Two smaller, more opportunistic species, Gaetice depressus de Haan and Acmaeopleura parvula Stimpson, did not react positively to shelter increases and each showed unique responses to the experimental manipulations. Differences in the amount of structural complexity in the upper and lower intertidal may be responsible for conflicting literature reports of the vertical distribution of Hemigrapsus sanguineus. Information gathered about the habitat requirements of this invasive grapsid crab will be useful for monitoring its impact and spread along the eastern coast of the United States.

Scale-dependent benthic recolonization dynamics: life stage-based dispersal and demographic consequences

Soft-sediment recruitment dynamics are dependent upon two sources of colonists; larvae transported from the water column and post-settlement movement of juvenile and/or adult life-stages across the seabed. Differences in the relative dispersal ability of the different life-stages into disturbed patches of habitat should vary predictably with the spatial scale of the disturbance. Smaller patches with a greater edge:surface area ratio should be more influenced by the post-settlement colonist pool than larger patches possessing a smaller edge:surface area ratio. A life stage-based recolonization model, using a Polydora cornuta life table, has been developed to describe how differences in the immigration rates of larvae, juveniles and adults can influence within-patch recovery times. Model results indicate that immigration of adult stages into disturbed patches has the least influence on patch recovery time. In contrast, post-settlement juvenile stages generally has a pronounced effect on patch population dynamics. Experimental evidence of scale-dependent migration of different life-stages to disturbed patches is also presented for the spionid polychaete Boccardia syrtis. Future research on scale-dependent recolonization dynamics in soft-sediment habitats should focus on acquisition of within-patch demographic data in order to more fully understand the importance of post-settlement life-stage movement in regulating population and community dynamics.

Context-specific bioturbation mediates changes to ecosystem functioning

Species are often grouped according to their biological or functional traits to better understand their contribution to ecosystem functioning. However, it is becoming clear that a single species can perform different roles in different habitats. Austrohelice crassa, a burrow-building mud crab shifts its primary bioturbational role to that of a vertical mixer in non-cohesive sediments as frequent burrow collapse greatly enhances sediment reworking. We conducted in situ crab density manipulations in two sediment environments (a non-cohesive sand and a cohesive muddy-sand) to examine if the context-specific functional roles were linked to changes in solute fluxes across the sediment–water interface. Across both habitats, we show that A. crassa regulated nutrient cycling, creating strong density driven effects on solute exchanges. Increasing crab density increased sediment O2 demand and the flux of NH4+ from the sediment, indicating much of the response was physiologically driven. Clear interactions between A. crassa and microphytobenthos were also detected in both habitats. Despite lowering microphyte standing stock through deposit feeding, A. crassa increased benthic primary production per unit of chlorophyll a. Our experiment also revealed important context-specific differences, most notably for NH4+ fluxes, which were higher where burrows and their associated microbial communities were most stable (muddy-sand). This study highlights the need to integrate interactions between organism behavior and habitat type into functional group studies to broaden conceptual frameworks and avoid oversimplification of highly complex organism–sediment interactions.

A latent threat to biodiversity: consequences of small-scale heterogeneity loss

The threat of homogenisation to biodiversity is generally considered to occur at broad scales or in response to high-intensity impacts. Therefore, most biodiversity studies estimate local average or total species richness rather than local heterogeneity. Here we consider the potential for relative shifts between these different aspects of biodiversity at small spatial scales to be an early warning signal for biodiversity loss. In response to chronic, very low-level pollution, we observed a disjunctive response with gamma diversity (total species richness) and beta diversity (heterogeneity) decreasing while alpha diversity (average species richness) was still increasing. Homogenisation may, therefore, affect biodiversity through thresholds that alter the relationship between the average species richness and its heterogeneity, leading to the potential for regime shifts. Our stressor also had a strong negative effect on rare species, meaning that the purported importance of rare species as “insurance” in the face of environmental change may be overstated.

When small changes matter: the role of cross-scale interactions between habitat and ecological connectivity in recovery.

Interaction between the diversity of local communities and the degree of connectivity between them has the potential to influence local recovery rates and thus profoundly affect community dynamics in the face of the cumulative impacts that occur across regions. Although such complex interactions have been modeled, field experiments in natural ecosystems to investigate the importance of interactions between local and regional processes are rare, especially so in coastal marine seafloor habitats subjected to many types of disturbance. We conducted a defaunation experiment at eight subtidal sites, incorporating manipulation of habitat structure, to test the relative importance of local habitat features and colonist supply in influencing macrobenthic community recovery rate. Our sites varied in community composition, habitat characteristics, and hydrodynamic conditions, and we conducted the experiment in two phases, exposing defaunated plots to colonists during periods of either high or low larval colonist supply. In both phases of the experiment, five months after disturbance, we were able to develop models that explained a large proportion of variation in community recovery rate between sites. Our results emphasize that the connectivity to the regional species pool influences recovery rate, and although local habitat effects were important, the strength of these effects was affected by broader-scale site characteristics and connectivity. Empirical evidence that cross-scale interactions are important in disturbance-recovery dynamics emphasizes the complex dynamics underlying seafloor community responses to cumulative disturbance.