Response to Comments on "Impacts of Biodiversity Loss on Ocean Ecosystem Services"

We show that globally declining fisheries catch trends cannot be explained by random processes and are consistent with declining stock abundance trends. Future projections are inherently uncertain but may provide a benchmark against which to assess the effectiveness of conservation measures. Marine reserves and fisheries closures are among those measures and can be equally effective in tropical and temperate areas—but must be combined with catch-, effort-, and gear restrictions to meet global conservation objectives.

Tropical Marginal Seas: Priority Regions for Managing Marine Biodiversity and Ecosystem Function

Tropical marginal seas (TMSs) are natural subregions of tropical oceans containing biodiverse ecosystems with conspicuous, valued, and vulnerable biodiversity assets. They are focal points for global marine conservation because they occur in regions where human populations are rapidly expanding. Our review of 11 TMSs focuses on three key ecosystems—coral reefs and emergent atolls, deep benthic systems, and pelagic biomes—and synthesizes, illustrates, and contrasts knowledge of biodiversity, ecosystem function, interaction between adjacent habitats, and anthropogenic pressures. TMSs vary in the extent that they have been subject to human influence—from the nearly pristine Coral Sea to the heavily exploited South China and Caribbean Seas—but we predict that they will all be similarly complex to manage because most span multiple national jurisdictions. We conclude that developing a structured process to identify ecologically and biologically significant areas that uses a set of globally agreed criteria is a tractable first step toward effective multinational and transboundary ecosystem management of TMSs.

Placing biodiversity in ecosystem models without getting lost in translation

A key challenge to progressing our understanding of biodiversity’s role in the sustenance of ecosystem function is the extrapolation of the results of two decades of dedicated empirical research to regional, global and future landscapes. Ecosystem models provide a platform for this progression, potentially offering a holistic view of ecosystems where, guided by the mechanistic understanding of processes and their connection to the environment and biota, large-scale questions can be investigated. While the benefits of depicting biodiversity in such models are widely recognized, its application is limited by difficulties in the transfer of knowledge from small process oriented ecology into macro-scale modelling. Here, we build on previous work, breaking down key challenges of that knowledge transfer into a tangible framework, highlighting successful strategies that both modelling and ecology communities have developed to better interact with one another. We use a benthic and a pelagic case-study to illustrate how aspects of the links between biodiversity and ecosystem process have been depicted in marine ecosystem models (ERSEM and MIRO), from data, to conceptualisation and model development. We hope that this framework may help future interactions between biodiversity researchers and model developers by highlighting concrete solutions to common problems, and in this way contribute to the advance of the mechanistic understanding of the role of biodiversity in marine (and terrestrial) ecosystems.

Marine biodiversity and ecosystem function relationships:the potential for practical monitoring applications

There is an increasing demand for environmental assessments of the marine environment to include ecosystem function. However, existing schemes are predominantly based on taxonomic (i.e. structural) measures of biodiversity. Biodiversity and Ecosystem Function (BEF) relationships are suggested to provide a mechanism for converting taxonomic information into surrogates of ecosystem function. This review assesses the evidence for marine BEF relationships and their potential to be used in practical monitoring applications (i.e. operationalized). Five key requirements were identified for the practical application of BEF relationships: (1) a complete understanding of strength, direction and prevalence of marine BEF relationships, (2) an understanding of which biological components are influential within specific BEF relationships, (3) the biodiversity of the selected biological components can be measured easily, (4) the ecological mechanisms that are the most important for generating marine BEF relationships, i.e. identity effects or complementarity, are known and (5) the proportion of the overall functional variance is explained by biodiversity, and hence BEF relationships, has been established. Numerous positive and some negative BEF relationships were found within the literature, although many reproduced poorly the natural species richness, trophic structures or multiple functions of real ecosystems (requirement 1). Null relationships were also reported. The consistency of the positive and negative relationships was often low that compromised the ability to generalize BEF relationships and confident application of BEF within marine monitoring. Equally, some biological components and functions have received little or no investigation. Expert judgement was used to attribute biological components using spatial extent, presence and functional rate criteria (requirement 2). This approach highlighted the main biological components contributing the most to specific ecosystem functions, and that many of the particularly influential components were found to have received the least amount of research attention. The need for biodiversity to be measureable (requirement 3) is possible for most biological components although difficult within the functionally important microbes. Identity effects underpinned most marine BEF relationships (requirement 4). As such, processes that translated structural biodiversity measures into functional diversity were found to generate better BEF relationships. The analysis of the contribution made by biodiversity, over abiotic influences, to the total expression of a particular ecosystem function was rarely measured or considered (requirement 5). Hence it is not possible to determine the overall importance of BEF relationships within the total ecosystem functioning observed. In the few studies where abiotic factors had been considered, it was clear that these modified BEF relationships and have their own direct influence on functional rate. Based on the five requirements, the information required for immediate ‘operationalization’ of BEF relationships within marine functional monitoring is lacking. However, the concept of BEF inclusion within practical monitoring applications, supported by ecological modelling, shows promise for providing surrogate indicators of functioning.

Horizon scanning for invasive alien species with the potential to threaten biodiversity in Great Britain

Invasive alien species (IAS) are considered one of the greatest threats to biodiversity, particularly through their interactions with other drivers of change. Horizon scanning, the systematic examination of future potential threats and opportunities, leading to prioritization of IAS threats is seen as an essential component of IAS management. Our aim was to consider IAS that were likely to impact on native biodiversity but were not yet established in the wild in Great Britain. To achieve this, we developed an approach which coupled consensus methods (which have previously been used for collaboratively identifying priorities in other contexts) with rapid risk assessment. The process involved two distinct phases: 1. Preliminary consultation with experts within five groups (plants, terrestrial invertebrates, freshwater invertebrates, vertebrates and marine species) to derive ranked lists of potential IAS. 2. Consensus-building across expert groups to compile and rank the entire list of potential IAS. Five hundred and ninety-one species not native to Great Britain were considered. Ninety-three of these species were agreed to constitute at least a medium risk (based on score and consensus) with respect to them arriving, establishing and posing a threat to native biodiversity. The quagga mussel, Dreissena rostriformis bugensis, received maximum scores for risk of arrival, establishment and impact; following discussions the unanimous consensus was to rank it in the top position. A further 29 species were considered to constitute a high risk and were grouped according to their ranked risk. The remaining 63 species were considered as medium risk, and included in an unranked long list. The information collated through this novel extension of the consensus method for horizon scanning provides evidence for underpinning and prioritizing management both for the species and, perhaps more importantly, their pathways of arrival. Although our study focused on Great Britain, we suggest that the methods adopted are applicable globally.

A review of climate change and the implementation of marine biodiversity legislation in the United Kingdom

1. Marine legislation, the key means by which the conservation of marine biodiversity is achieved, has been developing since the 1960s. In recent decades, an increasing focus on ‘holistic’ policy development is evident, compared with earlier ‘piecemeal’ sectoral approaches. Important marine legislative tools being used in the United Kingdom, and internationally, include the designation of marine protected areas and the Marine Strategy Framework Directive (MSFD) with its aim of meeting ‘Good Environmental Status’ (GES) for European seas by 2020. 2. There is growing evidence of climate change impacts on marine biodiversity, which may compromise the effectiveness of any legislation intended to promote sustainable marine resource management. 3. A review of key marine biodiversity legislation relevant to the UK shows climate change was not considered in the drafting of much early legislation. Despite the huge increase in knowledge of climate change impacts in recent decades, legislation is still limited in how it takes these impacts into account. There is scope, however, to account for climate change in implementing much of the legislation through (a) existing references to environmental variability; (b) review cycles; and (c) secondary legislation and complementary policy development. 4. For legislation relating to marine protected areas (e.g. the EC Habitats and Birds Directives), climate change has generally not been considered in the site-designation process, or for ongoing management, with the exception of the Marine (Scotland) Act. Given that changing environmental conditions (e.g. rising temperatures and ocean acidification) directly affect the habitats and species that sites are designated for, how this legislation is used to protect marine biodiversity in a changing climate requires further consideration. 5. Accounting for climate change impacts on marine biodiversity in the development and implementation of legislation is vital to enable timely, adaptive management responses. Marine modelling can play an important role in informing management decisions.

Relationships between biodiversity and the stability of marine ecosystems: comparisons at a European scale using meta-analysis.

The relationship between biodiversity and stability of marine benthic assemblages was investigated using existing data sets (n = 28) covering various spatial (m-km) and temporal (1973-2006) scales in different benthic habitats (emergent rock, rock pools and sedimentary habitats) through meta-analyses. Assemblage stability was estimated by measuring temporal variances of species richness, total abundance (density or % cover) and community species composition and abundance structure (using multivariate analyses). Positive relationships between temporal variability in species number and richness were generally observed at both quadrat (<1 m2) and site (100 m2) scales, while no relationships were observed by multivariate analyses. Positive relationships were also observed at the scale of site between temporal variability in species number and variability in community structure with evenness estimates. This implies that the relationship between species richness or evenness and species richness variability is slightly positive and depends on the scale of observation, suggesting that biodiversity per se is important for the stability of ecosystems. Changes within community assemblages in terms of structure are, however, generally independent of biodiversity, suggesting no effect of diversity, but the potential impact of individual species, and/or environmental factors. Except for sedimentary and rock pool habitats, no relationship was observed between temporal variation of the aggregated variable of total abundances and diversity at either scale. Overall our results emphasise that relationships depend on scale of measurements, type of habitats and the marine systems (North Atlantic and Mediterranean) considered.

Environmental tolerances of free-living coralline algae (maerl): implications for European marine conservation

Maerl is a general term used for loose-lying subtidal beds of nodular coralline red algae. Maerl beds support high associated invertebrate and algal biodiversity, and are subject to European and UK conservation legislation. Previous investigations have shown European maerl to be ecologically fragile due to growth rates of approximately I mm per year. However, these very slow growth rates have hampered attempts to determine the key ecological requirements and sensitivity characteristics of living maerl. In this study, photosynthetic capacity determined by pulse amplitude modulated (PAM) fluorometry was used as a diagnostic of stress caused by various environmental conditions. Maerl species were exposed to a range of temperatures, salinities and light levels and to burial, fragmentation, desiccation and heavy metal treatment. Maerl was not as susceptible as previously assumed to extremes of salinity, temperature and heavy metal pollution, but burial, especially in fine or anoxic sediments, was lethal or caused significant stress. These data indicate that the main anthropogenic hazard for live maerl and the rich communities that depend on them is smothering by fine sediment, such as that produced by trawling or maerl extraction, from sewage discharges or shellfish and fish farm waste, and sedimentation resulting from disruption to tidal flow. (C) 2004 Elsevier Ltd. All rights reserved.

Bio-folio: applying portfolio theory to biodiversity

Genes, species and ecosystems are often considered to be assets. The need to ensure a sufficient diversity of this asset is being increasingly recognised today. Asset managers in banks and insurance companies face a similar challenge. They are asked to manage the assets of their investors by constructing efficient portfolios. They deliberately make use of a phenomenon observed in the formation of portfolios: returns are additive, while risks diversify. This phenomenon and its implications are at the heart of portfolio theory. Portfolio theory, like few other economic theories, has dramatically transformed the practical work of banks and insurance companies. Before portfolio theory was developed about 50 years ago, asset managers were confronted with a situation similar to the situation the research on biodiversity faces today. While the need for diversification was generally accepted, a concept that linked risk and return on a portfolio level and showed the value of diversification was missing. Portfolio theory has closed this gap. This article first explains the fundamentals of portfolio theory and transfers it to biodiversity. A large part of this article is then dedicated to some of the implications portfolio theory has for the valuation and management of biodiversity. The last section introduces three development openings for further research.

4 ◦C and beyond: what did this mean for biodiversity in the past?

How do the predicted climatic changes (IPCC, 2007) for the next century compare in magnitude and rate to those that Earth has previously encountered? Are there comparable intervals of rapid rates of temperature change, sea-level rise and levels of atmospheric CO2 that can be used as analogues to assess possible biotic responses to future change? Or are we stepping into the great unknown? This perspective article focuses on intervals in time in the fossil record when atmospheric CO2 concentrations increased up to 1200 ppmv, temperatures in mid- to high-latitudes increased by greater than 4 ?C within 60 years, and sea levels rose by up to 3 m higher than present. For these intervals in time, case studies of past biotic responses are presented to demonstrate the scale and impact of the magnitude and rate of such climate changes on biodiversity. We argue that although the underlying mechanisms responsible for these past changes in climate were very different (i.e. natural processes rather than anthropogenic), the rates and magnitude of climate change are similar to those predicted for the future and therefore potentially relevant to understanding future biotic response. What emerges from these past records is evidence for rapid community turnover, migrations, development of novel ecosystems and thresholds from one stable ecosystem state to another, but there is very little evidence for broad-scale extinctions due to a warming world. Based on this evidence from the fossil record, we make four recommendations for future climate-change integrated conservation strategies.

Aligning conservation priorities across taxa in Madagascar with high-resolution planning tools

Globally, priority areas for biodiversity are relatively well known, yet few detailed plans exist to direct conservation action within them, despite urgent need. Madagascar, like other globally recognized biodiversity hot spots, has complex spatial patterns of endemism that differ among taxonomic groups, creating challenges for the selection of within-country priorities. We show, in an analysis of wide taxonomic and geographic breadth and high spatial resolution, that multitaxonomic rather than single-taxon approaches are critical for identifying areas likely to promote the persistence of most species. Our conservation prioritization, facilitated by newly available techniques, identifies optimal expansion sites for the Madagascar government's current goal of tripling the land area under protection. Our findings further suggest that high-resolution multitaxonomic approaches to prioritization may be necessary to ensure protection for biodiversity in other global hot spots.

Climate Change Adaptation for Conservation in Madagascar

Madagascar's imperilled biota are now experiencing the effects of a new threat—climate change (Raxworthy et al. 2008). With more than 90% endemism among plants, mammals, reptiles and amphibians, the stakes are high. The pristine landscapes that allowed this exceptional biodiversity to survive past climate changes are largely gone. Deforestation has claimed approximately 90% of the island's natural forest (Ingram & Dawson 2005; Harper et al. 2007) and what remains is highly fragmented, providing a poor template for large-scale species range shifts. The impacts of current and future climate change may therefore be much different than past impacts, with profound implications for biodiversity.
We review evidence of past response to climate change, models of future change and projected biological response, developing insights to formulate adaptation actions for reducing extinction in Madagascar's biota. We then explore the cost of implementing actions and examine new income opportunities developing through efforts to mitigate climate change.

Tentacular diversity in deep-sea deposit-feeding holothurians: implications for biodiversity in the deep sea

The tentacles of deep-sea holothurians show a wide range of morphological diversity. The present paper examines gross tentacle morphology in surface deposit feeding holothurians from a range of bathymetric depths. Species studied included the elasipods: Oneirophanta mutabilis, Psychropotes longicauda and Benthogone rosea and the aspidochirotids: Paroriza prouhoi, Pseudostichopus sp., Bathyplotes natans and Paroriza pallens. The sympatric abyssal species Oneirophanta mutabilis, Psychropotes longicauda and Pseudostichopus sp. show subtle differences in diet and the structure and filling patterns of the gut that suggest differences in feeding strategies which may represent one mechanism to overcome competition for food resources in an environment where nutrient resources are considered to be, at least periodically, limiting. Interspecific differences in tentacle functional morphology and digestive strategies, which reflects taxonomic diversity could be explained in terms of Sanders'; Stability–Time Hypothesis. Since different tentacle types will turn over sediments to different extents, their impact on sedimentary communities will be enormous so that high diversity in meiofaunal communities may be explained most simply by Dayton and Hessler's Biological Disturbance Hypothesis.

The conservation of bees: a global perspective

Bees are major pollinators of Angiosperms and therefore their apparent decline is of importance for humans and biodiversity. We synthesise results of 12 recent reviews to provide a global picture of the threats they face. Habitat loss is the major threat to bee diversity, whilst invasive species, emerging diseases, pesticide use, and climate change also have the potential to impact bee populations. We suggest that future conservation strategies need to prioritise (i) minimising habitat loss, (ii) making agricultural habitats bee-friendly, (iii) training scientists and the public in bee taxonomy and identification, (iv) basic autecological and population genetic studies to underpin conservation strategies, (v) assessing the value of DNA barcoding for bee conservation, (vi) determining the impact of invasive plants, animals, parasites and pathogens, and (vii) integrating this information to understand the potential impact of climate change on current bee diversity.