Dov F. Sax

THE INVASION PARADOX: RECONCILING PATTERN AND PROCESS IN SPECIES INVASIONS

The invasion paradox describes the co-occurrence of independent lines of support for both a negative and a positive relationship between native biodiversity and the invasions of exotic species. The paradox leaves the implications of native-exotic species richness relationships open to debate: Are rich native communities more or less susceptible to invasion by exotic species? We reviewed the considerable observational, experimental, and theoretical evidence describing the paradox and sought generalizations concerning where and why the paradox occurs, its implications for community ecology and assembly processes, and its relevance for restoration, management, and policy associated with species invasions. The crux of the paradox concerns positive associations between native and exotic species richness at broad spatial scales, and negative associations at fine scales, especially in experiments in which diversity was directly manipulated. We identified eight processes that can generate either negative or positive native-exotic richness relationships, but none can generate both. As all eight processes have been shown to be important in some systems, a simple general theory of the paradox, and thus of the relationship between diversity and invasibility, is probably unrealistic. Nonetheless, we outline several key issues that help resolve the paradox, discuss the difficult juxtaposition of experimental and observational data (which often ask subtly different questions), and identify important themes for additional study. We conclude that natively rich ecosystems are likely to be hotspots for exotic species, but that reduction of local species richness can further accelerate the invasion of these and other vulnerable habitats.

Species diversity: from global decreases to local increases

Current patterns of global change can strongly affect biodiversity at global, regional and local scales. At global scales, habitat destruction and the introduction of exotic species are contributing to declines in species diversity. At regional and local scales, evidence for declines in diversity is mixed, and recent work suggests that diversity might commonly be increasing. In spite of these trends, considerable research continues to consider explicitly the effects of declines in diversity on processes that operate at regional and local scales (such as ecosystem functioning), without explicitly considering the converse set of questions, namely the effects of increases in diversity. Here, we examine evidence that indicates how species diversity is changing across spatial scales and argue that global decreases in diversity are commonly contrasted by increases in diversity at regional and local scales.

Species invasions and extinction: The future of native biodiversity on islands

Predation by exotic species has caused the extinction of many native animal species on islands, whereas competition from exotic plants has caused few native plant extinctions. Exotic plant addition to islands is highly nonrandom, with an almost perfect 1 to 1 match between the number of naturalized and native plant species on oceanic islands. Here, we evaluate several alternative implications of these findings. Does the consistency of increase in plant richness across islands imply that a saturation point in species richness has been reached? If not, should we expect total plant richness to continue to increase as new species are added? Finally, is the rarity of native plant extinctions to date a misleading measure of the impact of past invasions, one that hides an extinction debt that will be paid in the future? By analyzing historical records, we show that the number of naturalized plant species has increased linearly over time on many individual islands. Further, the mean ratio of naturalized to native plant species across islands has changed steadily for nearly two centuries. These patterns suggest that many more species will become naturalized on islands in the future. We also discuss how dynamics of invasion bear upon alternative saturation scenarios and the implications these scenarios have for the future retention or extinction of native plant species. Finally, we identify invasion-motivated research gaps (propagule pressure, time-lags to extinction, abundance shifts, and loss of area) that can aid in forecasting extinction and in developing a more comprehensive theory of species extinctions.

Species Invasions Exceed Extinctions on Islands Worldwide: A Comparative Study of Plants and Birds

Species richness is decreasing at a global scale. At subglobal scales, that is, within any defined area less extensive than the globe, species richness will increase when the number of nonnative species becoming naturalized is greater than the number of native species becoming extinct. Determining whether this has occurred is usually difficult because detailed records of species extinctions and naturalizations are rare; these records often exist, however, for oceanic islands. Here we show that species richness on oceanic islands has remained relatively unchanged for land birds, with the number of naturalizations being roughly equal to the number of extinctions, and has increased dramatically for vascular plants, with the number of naturalizations greatly exceeding the number of extinctions. In fact, for plants, the net number of species on islands has approximately doubled. We show further that these patterns are robust to differences in the history of human occupation of these islands and to the possibility of undocumented species extinctions. These results suggest that species richness may be increasing at subglobal scales for many groups and that future research should address what consequences this may have on ecological processes.

Balancing biodiversity in a changing environment: extinction debt, immigration credit and species turnover

Here, we outline a conceptual framework for biodiversity dynamics following environmental change. The model incorporates lags in extinction and immigration, which lead to extinction debt and immigration credit, respectively. Collectively, these concepts enable a balanced consideration of changes in biodiversity following climate change, habitat fragmentation and other forcing events. They also reveal transient phenomena, such as biodiversity surpluses and deficits, which have important ramifications for biological conservation and the preservation of ecosystem services. Predicting such transient dynamics poses a serious conservation challenge in a time of rapid environmental change.

The potential conservation value of non-native species.

Non-native species can cause the loss of biological diversity (i.e., genetic, species, and ecosystem diversity) and threaten the well-being of humans when they become invasive. In some cases, however, they can also provide conservation benefits. We examined the ways in which non-native species currently contribute to conservation objectives. These include, for example, providing habitat or food resources to rare species, serving as functional substitutes for extinct taxa, and providing desirable ecosystem functions. We speculate that non-native species might contribute to achieving conservation goals in the future because they may be more likely than native species to persist and provide ecosystem services in areas where climate and land use are changing rapidly and because they may evolve into new and endemic taxa. The management of non-native species and their potential integration into conservation plans depends on how conservation goals are set in the future. A fraction of non-native species will continue to cause biological and economic damage, and substantial uncertainty surrounds the potential future effects of all non-native species. Nevertheless, we predict the proportion of non-native species that are viewed as benign or even desirable will slowly increase over time as their potential contributions to society and to achieving conservation objectives become well recognized and realized.

Multidimensional evaluation of managed relocation

Managed relocation (MR) has rapidly emerged as a potential intervention strategy in the toolbox of biodiversity management under climate change. Previous authors have suggested that MR (also referred to as assisted colonization, assisted migration, or assisted translocation) could be a last-alternative option after interrogating a linear decision tree. We argue that numerous interacting and value-laden considerations demand a more inclusive strategy for evaluating MR. The pace of modern climate change demands decision making with imperfect information, and tools that elucidate this uncertainty and integrate scientific information and social values are urgently needed. We present a heuristic tool that incorporates both ecological and social criteria in a multidimensional decision-making framework. For visualization purposes, we collapse these criteria into 4 classes that can be depicted in graphical 2-D space. This framework offers a pragmatic approach for summarizing key dimensions of MR: capturing uncertainty in the evaluation criteria, creating transparency in the evaluation process, and recognizing the inherent tradeoffs that different stakeholders bring to evaluation of MR and its alternatives.

Managed Relocation: Integrating the Scientific, Regulatory, and Ethical Challenges

Managed relocation is defined as the movement of species, populations, or genotypes to places outside the areas of their historical distributions to maintain biological diversity or ecosystem functioning with changing climate. It has been claimed that a major extinction event is under way and that climate change is increasing its severity. Projections indicating that climate change may drive substantial losses of biodiversity have compelled some scientists to suggest that traditional management strategies are insufficient. The managed relocation of species is a controversial management response to climate change. The published literature has emphasized biological concerns over difficult ethical, legal, and policy issues. Furthermore, ongoing managed relocation actions lack scientific and societal engagement. Our interdisciplinary team considered ethics, law, policy, ecology, and natural resources management in order to identify the key issues of managed relocation relevant for developing sound policies that support decisions for resource management. We recommend that government agencies develop and adopt best practices for managed relocation.

Globalization of human infectious disease.

Globalization has facilitated the spread of numerous infectious agents to all corners of the planet. Analysis of the Global Infectious Disease and Epidemiology Network (GIDEON) database quantitatively illustrates that the globalization of human infectious agents depends significantly on the range of hosts used. Infectious agents specific to humans are broadly and uniformly distributed, whereas zoonotic infectious agents are far more localized in their geographical distribution. Moreover, these patterns vary depending on transmission mode and infectious agent taxonomy. This dichotomy is unlikely to persist if certain aspects of globalization (for example, exotic species introductions) continue unabated. This raises a serious concern for public health and leaves nations with the task of determining the infectious agents that have the greatest potential to establish within their borders. At the advent of a century characterized by an apparent increase in emerging infectious diseases, these results have critical implications for public-health policy and future research pathways of infectious disease ecology.

Managed relocation: a nuanced evaluation is needed.

Managed relocation (aka ‘assisted colonization’ and ‘assisted migration’ [1,2]) aims to save species from the effects of climate change by purposefully transporting them to areas where they have not previously occurred, but where they are expected to survive as temperatures increase. In a recent Opinion article in TREE [3], Ricciardi and Simberloff suggest that ‘assisted colonization is tantamount to ecological roulette and should probably be rejected as a sound conservation strategy by the precautionary principle.’ We disagree for three primary reasons.