The contribution of policy,law, management,research, and advocacy failings to the recent extinctions of three Australian vertebrate species

Extinctions typically have ecological drivers, such as habitat loss. However, extinction events are also influenced by policy and management settings that may be antithetical to biodiversity conservation, inadequate to prevent extinction, insufficiently resourced, or poorly implemented. Three endemic Australian vertebrate species—the Christmas Island pipistrelle (Pipistrellus murrayi), Bramble Cay melomys (Melomys rubicola), and Christmas Island forest skink (Emoia nativitatis)—became extinct from 2009 to 2014. All 3 extinctions were predictable and probably preventable. We sought to identify the policy, management, research, and other shortcomings that contributed to their extinctions or failed to prevent them. These included a lack within national environmental legislation and policy of explicit commitment to the prevention of avoidable extinctions, lack of explicit accountability, inadequate resources for conservation (particularly for species not considered charismatic or not of high taxonomic distinctiveness), inadequate biosecurity, a slow and inadequate process for listing species as threatened, recovery planning that failed to consider the need for emergency response, inability of researchers to identify major threatening factors, lack of public engagement and involvement in conservation decisions, and limited advocacy. From these 3 cases, we recommend: environmental policy explicitly seeks to prevent extinction of any species and provides a clear chain of accountability and an explicit requirement for public inquiry following any extinction; implementation of a timely and comprehensive process for listing species as threatened and for recovery planning; reservation alone not be assumed sufficient to maintain species; enhancement of biosecurity measures; allocation of sufficient resources to undertake actions necessary to prevent extinction; monitoring be considered a pivotal component of the conservation response; research provides timely identification of factors responsible for decline and of the risk of extinction; effective dissemination of research results; advocacy by an informed public for the recovery of threatened species; and public involvement in governance of the recovery process. These recommendations should be applicable broadly to reduce the likelihood and incidence of extinctions.     

Global reforestation and biodiversity conservation

The loss of forest is a leading cause of species extinction, and reforestation is 1 of 2 established interventions for reversing this loss. However, the role of reforestation for biodiversity conservation remains debated, and lacking is an assessment of the potential contribution that reforestation could make to biodiversity conservation globally. We conducted a spatial analysis of overlap between 1,550 forest-obligate threatened species’ ranges and land that could be reforested after accounting for socioeconomic and ecological constraints. Reforestation on at least 43% (∼369 million ha) of reforestable area was predicted to potentially benefit threatened vertebrates. This is approximately 15% of the total area where threatened vertebrates occur. The greatest opportunities for conserving threatened vertebrate species are in the tropics, particularly Brazil and Indonesia. Although reforestation is not a substitute for forest conservation, and most of the area containing threatened vertebrates remains forested, our results highlight the need for global conservation strategies to recognize the potentially significant contribution that reforestation could make to biodiversity conservation. If implemented, reforestation of ∼369 million ha would also contribute substantially to climate-change mitigation, offering a way to achieve multiple sustainability commitments at once. Countries must now work to overcome key barriers (e.g., unclear revenue streams, high transaction costs) to investment in reforestation.     

Level of environmental threat posed by horticultural trade in Cactaceae

Ornamental horticulture has been identified as an important threat to plant biodiversity and is a major pathway for plant invasions worldwide. In this context, the family Cactaceae is particularly challenging because it is considered the fifth most threatened large taxonomic group in the world; several species are among the most widespread and damaging invasive species; and Cactaceae is one of the most popular horticultural plant groups. Based on the Convention on International Trade in Endangered Species of Wild Flora and Fauna and the 11 largest online auction sites selling cacti, we documented the international cactus trade. To provide an in‐depth look at the dynamics of the industry, we surveyed the businesses involved in the cactus trade in South Africa (a hotspot of cactus trade and invasions). We purchased seeds of every available species and used DNA barcoding to identify species to the genus level. Although <20% of this trade involved threatened species and <3% involved known invasive species, many species were identified by a common name. However, only 0.02% of the globally traded cacti were collected from wild populations. Despite a large commercial network, all South African imports (of which 15% and 1.5% were of species listed as threatened and invasive, respectively) came from the same source. With DNA barcoding, we identified 24% of the species to genus level. Based on our results, we believe that if trade restrictions are placed on the small proportion of cacti that are invasive and there is no major increase in harvesting of native populations, then the commercial trade in cactus poses a negligible environmental threat. However, there are currently no effective methods for easily identifying which cacti are traded, and both the illicit harvesting of cacti from the wild and the informal trade in invasive taxa pose on‐going conservation challenges.     

Conservation Prioritization Using GAP Data

Data collected by the Gap Analysis Program in the state of Idaho (U.S.A.) are used to prioritize the selection of locations for conservation action and research. Set coverage and integer programming algorithms provide a sequence of localities that maximize the number of species or vegetation classes represented at each step. Richness maps of vegetation cover class diversity, terrestrial vertebrate species diversity ("hot spot analysis"), endangered, threatened, and candidate species diversity, and unprotected vertebrate species diversity ("gap analysis"), when prioritized, show a rapid accumulation of species as more localities are chosen for terrestrial vertebrates and unprotected vertebrates. Gap analysis identifies four target areas ("gaps") that include 79 of the 83 vertebrate species not currently protected. Accumulation of vegetation cover classes and endangered, threatened, and candidate species is much slower. Sweep analysis is used to determine how well prioritizing on one component of diversity accumulates other components. Endangered, threatened, and candidate species do not sweep total vertebrates as well as unprotected vertebrates do, but are better than vegetation classes. Total vertebrates sweep endangered, threatened, and candidate species better than unprotected vertebrates do, which in turn are better than vegetation classes. We emphasize that prioritization must be part of conservation efforts at multiple scales and that prioritization points out important localities where more detailed work mast be undertaken.     

Vascular plant extinction in the continental United States and Canada

Extinction rates are expected to increase during the Anthropocene. Current extinction rates of plants and many animals remain unknown. We quantified extinctions among the vascular flora of the continental United States and Canada since European settlement. We compiled data on apparently extinct species by querying plant conservation databases, searching the literature, and vetting the resulting list with botanical experts. Because taxonomic opinion varies widely, we developed an index of taxonomic uncertainty (ITU). The ITU ranges from A to F, with A indicating unanimous taxonomic recognition and F indicating taxonomic recognition by only a single author. The ITU allowed us to rigorously evaluate extinction rates. Our data suggest that 51 species and 14 infraspecific taxa, representing 33 families and 49 genera of vascular plants, have become extinct in our study area since European settlement. Seven of these taxa exist in cultivation but are extinct in the wild. Most extinctions occurred in the west, but this outcome may reflect the timing of botanical exploration relative to settlement. Sixty-four percent of extinct plants were single-site endemics, and many occurred outside recognized biodiversity hotspots. Given the paucity of plant surveys in many areas, particularly prior to European settlement, the actual extinction rate of vascular plants is undoubtedly much higher than indicated here.     

A global ecological signal of extinction risk in terrestrial vertebrates

To determine the distribution and causes of extinction threat across functional groups of terrestrial vertebrates, we assembled an ecological trait data set for 18,016 species of terrestrial vertebrates and utilized phylogenetic comparative methods to test which categories of habitat association, mode of locomotion, and feeding mode best predicted extinction risk. We also examined the individual categories of the International Union for Conservation of Nature Red List extinction drivers (e.g., agriculture and logging) threatening each species and determined the greatest threats for each of the four terrestrial vertebrate groups. We then quantified the sum of extinction drivers threatening each species to provide a multistressor perspective on threat. Cave dwelling amphibians (p < 0.01), arboreal quadrupedal mammals (all of which are primates) (p < 0.01), aerial and scavenging birds (p < 0.01), and pedal (i.e., walking) squamates (p < 0.01) were all disproportionately threatened with extinction in comparison with the other assessed ecological traits. Across all threatened vertebrate species in the study, the most common risk factors were agriculture, threatening 4491 species, followed by logging, threatening 3187 species, and then invasive species and disease, threatening 2053 species. Species at higher risk of extinction were simultaneously at risk from a greater number of threat types. If left unabated, the disproportionate loss of species with certain functional traits and increasing anthropogenic pressures are likely to disrupt ecosystem functions globally. A shift in focus from species- to trait-centric conservation practices will allow for protection of at-risk functional diversity from regional to global scales.     

When all life counts in conservation

Conservation science involves the collection and analysis of data. These scientific practices emerge from values that shape who and what is counted. Currently, conservation data are filtered through a value system that considers native life the only appropriate subject of conservation concern. We examined how trends in species richness, distribution, and threats change when all wildlife count by adding so-called non-native and feral populations to the International Union for Conservation of Nature Red List and local species richness assessments. We focused on vertebrate populations with founding members taken into and out of Australia by humans (i.e., migrants). We identified 87 immigrant and 47 emigrant vertebrate species. Formal conservation accounts underestimated global ranges by an average of 30% for immigrants and 7% for emigrants; immigrations surpassed extinctions in Australia by 52 species; migrants were disproportionately threatened (33% of immigrants and 29% of emigrants were threatened or decreasing in their native ranges); and incorporating migrant populations into risk assessments reduced global threat statuses for 15 of 18 species. Australian policies defined most immigrants as pests (76%), and conservation was the most commonly stated motivation for targeting these species in killing programs (37% of immigrants). Inclusive biodiversity data open space for dialogue on the ethical and empirical assumptions underlying conservation science.     

Not Knowing, Not Recording, Not Listing: Numerous Unnoticed Mollusk Extinctions

Abstract:  Mollusks are the group most affected by extinction according to the 2007 International Union for Conservation of Nature (IUCN) Red List, despite the group having not been evaluated since 2000 and the quality of information for invertebrates being far lower than for vertebrates. Altogether 302 species and 11 subspecies are listed as extinct on the IUCN Red List. We reevaluated mollusk species listed as extinct through bibliographic research and consultation with experts. We found that the number of known mollusk extinctions is almost double that of the IUCN Red List. Marine habitats seem to have experienced few extinctions, which suggests that marine species may be less extinction prone than terrestrial and freshwater species. Some geographic and ecologic biases appeared. For instance, the majority of extinctions in freshwater occurred in the United States. More than 70% of known mollusk extinctions took place on oceanic islands, and a one-third of these extinctions may have been caused precipitously by introduction of the predatory snail Euglandina rosea. We suggest that assessment of the conservation status of invertebrate species is neglected in the IUCN Red List and not managed in the same way as for vertebrate species .     

The Role of Behavior in Recent Avian Extinctions and Endangerments

Abstract: Understanding patterns of differential extinction and predicting the relative risks of extinction among extant species are among the most important problems in conservation biology. Although recent studies reveal that behavior can be a critical component in many species' extinctions or endangerments, current approaches to the problem of predicting extinction patterns largely ignore behavior. I reviewed how behavior can affect population persistence and then used recent avian extinctions and endangerments to illustrate behaviors relevant to extinction risk. Behaviors that affect population persistence can be grouped as aggregation, interspecific responses, dispersal, habitat selection, intraspecific behavior, and maladaptive behavior. Behavior that can affect extinction risk is not limited to birds; for example, in many taxonomic groups (vertebrate and invertebrate) there is evidence of socially facilitated reproduction in colonial species, Allee effects on reproductive success and survival, behavioral regulation of population size, and conspecific attraction to breeding sites. Incorporating specific behaviors into models predicting extinction probabilities and patterns should improve their predictions.     

Reliability of social media data in monitoring the global pet trade in ants

The global pet trade is a major risk to biodiversity and humans and has become increasingly globalized, diversified, digitalized, and extremely difficult to control. With billions of internet users posting online daily, social media could be a powerful surveillance tool. But it is unknown how reliably social media can track the global pet trade. We tested whether Instagram data predicted the geographic distribution of pet stores and the taxonomic composition of traded species in the emerging pet trade in ants (Hymenoptera, Formicidae). We visited 138 online stores selling ants as pets worldwide and recorded the species traded. We scraped ∼38,000 Instagram posts from ∼6300 users referencing ants as pets and analyzed comments on post and geolocation (available for ∼1800 users). We tested whether the number of Instagram users predicted the number of ant sellers per country and whether the species referenced as pets on Instagram matched the species offered in online stores, with a particular focus on invasive species. The location of Instagram users referencing ants as pets predicted the location of ant sellers across the globe (R² = 0.87). Instagram data detected 439 of the 631 ant species traded in online stores (70%), including 59 of the 68 invasive species traded (87%). The number of Instagram users referencing a species was a good predictor of the number of sellers offering the species (R² = 0.77). Overall, Instagram data provided affordable and reliable data for monitoring the emerging pet trade in ants. Easier access to these data would facilitate monitoring of the global pet trade and help implement relevant regulations in a timely manner.     

E‐commerce trade in invasive plants

Biological invasions are a major concern in conservation, especially because global transport of species is still increasing rapidly. Conservationists hope to anticipate and thus prevent future invasions by identifying and regulating potentially invasive species through species risk assessments and international trade regulations. Among many introduction pathways of non‐native species, horticulture is a particularly important driver of plant invasions. In recent decades, the horticultural industry expanded globally and changed structurally through the emergence of new distribution channels, including internet trade (e‐commerce). Using an automated search algorithm, we surveyed, on a daily basis, e‐commerce trade on 10 major online auction sites (including eBay) of approximately three‐fifths of the world's spermatophyte flora. Many recognized invasive plant species (>500 species) (i.e., species associated with ecological or socio‐economic problems) were traded daily worldwide on the internet. A markedly higher proportion of invasive than non‐invasive species were available online. Typically, for a particular plant family, 30–80% of recognized invasive species were detected on an auction site, but only a few percentages of all species in the plant family were detected on a site. Families that were more traded had a higher proportion of invasive species than families that were less traded. For woody species, there was a significant positive relationship between the number of regions where a species was sold and the number of regions where it was invasive. Our results indicate that biosecurity is not effectively regulating online plant trade. In the future, automated monitoring of e‐commerce may help prevent the spread of invasive species, provide information on emerging trade connectivity across national borders, and be used in horizon scanning exercises for early detection of new species and their geographic source areas in international trade.     

Synergies and trade‐offs in achieving global biodiversity targets

After their failure to achieve a significant reduction in the global rate of biodiversity loss by 2010, world governments adopted 20 new ambitious Aichi biodiversity targets to be met by 2020. Efforts to achieve one particular target can contribute to achieving others, but different targets may sometimes require conflicting solutions. Consequently, lack of strategic thinking might result, once again, in a failure to achieve global commitments to biodiversity conservation. We illustrate this dilemma by focusing on Aichi Target 11. This target requires an expansion of terrestrial protected area coverage, which could also contribute to reducing the loss of natural habitats (Target 5), reducing human‐induced species decline and extinction (Target 12), and maintaining global carbon stocks (Target 15). We considered the potential impact of expanding protected areas to mitigate global deforestation and the consequences for the distribution of suitable habitat for >10,000 species of forest vertebrates (amphibians, birds, and mammals). We first identified places where deforestation might have the highest impact on remaining forests and then identified places where deforestation might have the highest impact on forest vertebrates (considering aggregate suitable habitat for species). Expanding protected areas toward locations with the highest deforestation rates (Target 5) or the highest potential loss of aggregate species’ suitable habitat (Target 12) resulted in partially different protected area network configurations (overlapping with each other by about 73%). Moreover, the latter approach contributed to safeguarding about 30% more global carbon stocks than the former. Further investigation of synergies and trade‐offs between targets would shed light on these and other complex interactions, such as the interaction between reducing overexploitation of natural resources (Targets 6, 7), controlling invasive alien species (Target 9), and preventing extinctions of native species (Target 12). Synergies between targets must be identified and secured soon and trade‐offs must be minimized before the options for co‐benefits are reduced by human pressures.     

Mapping Hotspots of Threatened Species Traded in Bushmeat Markets in the Cross–Sanaga Rivers Region

Bushmeat markets exist in many countries in West and Central Africa, and data on species sold can be used to detect patterns of wildlife trade in a region. We surveyed 89 markets within the Cross–Sanaga rivers region, West Africa. In each market, we counted the number of carcasses of each taxon sold. During a 6‐month period (7594 market days), 44 mammal species were traded. Thirteen species were on the International Union for Conservation of Nature (IUCN) Red List or protected under national legislation, and at least 1 threatened species was traded in 88 of the 89 markets. We used these data to identify market groups that traded similar species assemblages. Using cluster analyses, we detected 8 market groups that were also geographically distinct. Market groups differed in the diversity of species, evenness of species, and dominant, prevalent, and characteristic species traded. We mapped the distribution of number of threatened species traded across the study region. Most threatened species were sold in markets nearest 2 national parks, Korup National Park in Cameroon and Cross River in Nigeria. To assess whether the threatened‐species trade hotspots coincided with the known ranges of these species, we mapped the overlap of all threatened species traded. Markets selling more threatened species overlapped with those regions that had higher numbers of these. Our study can provide wildlife managers in the region with better tools to discern zones within which to focus policing efforts and reduce threats to species that are threatened by the bushmeat trade. Mapeo de Sitios Críticos para Especies Amenazadas Comercializadas en Mercados de Vida Silvestre en la Región de los Ríos Cross‐Sanaga     

Effects of Native and Non‐Native Vertebrate Mutualists on Plants

Abstract: Extinctions can leave species without mutualist partners and thus potentially reduce their fitness. In cases where non‐native species function as mutualists, mutualism disruption associated with species’ extinction may be mitigated. To assess the effectiveness of mutualist species with different origins, we conducted a meta‐analysis in which we compared the effectiveness of pollination and seed‐dispersal functions of native and non‐native vertebrates. We used data from 40 studies in which a total of 34 non‐native vertebrate mutualists in 20 geographic locations were examined. For each plant species, opportunistic non‐native vertebrate pollinators were generally less effective mutualists than native pollinators. When native mutualists had been extirpated, however, plant seed set and seedling performance appeared elevated in the presence of non‐native mutualists, although non‐native mutualists had a negative overall effect on seed germination. These results suggest native mutualists may not be easily replaced. In some systems researchers propose taxon substitution or the deliberate introduction of non‐native vertebrate mutualists to reestablish mutualist functions such as pollination and seed dispersal and to rescue native species from extinction. Our results also suggest that in places where all native mutualists are extinct, careful taxon substitution may benefit native plants at some life stages.     

Critique of the Evolutionarily Significant Unit as a Definition for "Distinct Population Segments" under the U.S. Endangered Species Act

The U.S. Endangered Species Act grants protection to species, subspecies, and "distinct population segments" of vertebrate species. Historically, Congress included distinct population segments into endangered species legislation to enable the U.S. Fish and Wildlife Service to implement a flexible and pragmatic approach in listing populations of vertebrate species. Recently, the U.S. Fish and Wildlife Service and the National Marine Fisheries Service have proposed a policy that would narrowly define distinct population segments as evolutionarily significant units based on morphological and genetic distinctiveness between populations. Historically, the power to list species or populations as distinct population segments has been used to tailor management practices to unique circumstances; grant varied levels of protection in different parts of a species' range; protect species from extinction in significant portions of their ranges as well as to protect populations that are unique evolutionary entities. A strict redefinition of distinct population segments as evolutionarily significant units will compromise management efforts because the role of demographic and behavioral data will be reduced. Furthermore, strictly cultural, economic, or geographic justifications for listing populations as threatened or endangered will be greatly curtailed.     

Intact Faunal Assemblages in the Modern Era

Abstract: In light of limited conservation funding, global conservation initiatives are increasingly focused on regions of the planet that have been identified as valuable on the basis of their species diversity, the vulnerability of resident species to extinction, or the perceived pristine nature of their ecosystems. Regions that have been resilient to high rates of extinction have not yet been systematically considered in conservation efforts. We used published range maps for 392 vertebrate species to compare historical and current species ranges. We used the results of the comparison to identify regions of the globe in which no known vertebrate species has been extirpated in the past 200 years. In 17 regions, no detectable vertebrate extinctions occurred in the past 200 years. In 6 other regions, reintroductions of species restored the full historic complement of vertebrate species. The effects of humans on a landscape, as measured by the human‐footprint index, although useful, was not a singularly good predictor of faunal intactness because more than 20% of intact land area was in heavily affected areas (50% of Earth's land area), and several regions where humans have had very little effect did not have intact faunas. Only 22% of intact land area was within protected‐area networks. High‐latitude areas were particularly underrepresented; they made up 3 of the 4 least‐protected areas in our analyses. Our results indicate that although protected areas are in some cases associated with the prevention of extinctions, there are many regions in which human activity coexists with intact vertebrate assemblages. In addition, our new approach for assessing the value of global regions for conservation identifies several regions that are not represented in other prioritization metrics.     

Two Hundred Years of Local Avian Extinctions in Eastern Amazonia

Local, regional, and global extinctions caused by habitat loss, degradation, and fragmentation have been widely reported for the tropics. The patterns and drivers of this loss of species are now increasingly well known in Amazonia, but there remains a significant gap in understanding of long‐term trends in species persistence and extinction in anthropogenic landscapes. Such a historical perspective is critical for understanding the status and trends of extant biodiversity as well as for identifying priorities to halt further losses. Using extensive historical data sets of specimen records and results of contemporary surveys, we searched for evidence of local extinctions of a terra firma rainforest avifauna over 200 years in a 2500 km² eastern Amazonian region around the Brazilian city of Belém. This region has the longest history of ornithological fieldwork in the entire Amazon basin and lies in the highly threatened Belém Centre of Endemism. We also compared our historically inferred extinction events with extensive data on species occurrences in a sample of catchments in a nearby municipality (Paragominas) that encompass a gradient of past forest loss. We found evidence for the possible extinction of 47 species (14% of the regional species pool) that were unreported from 1980 to 2013 (80% last recorded between 1900 and 1980). Seventeen species appear on the International Union for Conservation of Nature Red List, and many of these are large‐bodied. The species lost from the region immediately around Belém are similar to those which are currently restricted to well‐forested catchments in Paragominas. Although we anticipate the future rediscovery or recolonization of some species inferred to be extinct by our calculations, we also expect that there are likely to be additional local extinctions, not reported here, given the ongoing loss and degradation of remaining areas of native vegetation across eastern Amazonia. Doscientos Años de Extinciones Locales de Aves en la Amazonia Oriental     

Invasion versus Isolation: Trade-Offs in Managing Native Salmonids with Barriers to Upstream Movement

Abstract: Conservation biologists often face the trade‐off that increasing connectivity in fragmented landscapes to reduce extinction risk of native species can foster invasion by non‐native species that enter via the corridors created, which can then increase extinction risk. This dilemma is acute for stream fishes, especially native salmonids, because their populations are frequently relegated to fragments of headwater habitat threatened by invasion from downstream by 3 cosmopolitan non‐native salmonids. Managers often block these upstream invasions with movement barriers, but isolation of native salmonids in small headwater streams can increase the threat of local extinction. We propose a conceptual framework to address this worldwide problem that focuses on 4 main questions. First, are populations of conservation value present (considering evolutionary legacies, ecological functions, and socioeconomic benefits as distinct values)? Second, are populations vulnerable to invasion and displacement by non‐native salmonids? Third, would these populations be threatened with local extinction if isolated with barriers? And, fourth, how should management be prioritized among multiple populations? We also developed a conceptual model of the joint trade‐off of invasion and isolation threats that considers the opportunities for managers to make strategic decisions. We illustrated use of this framework in an analysis of the invasion‐isolation trade‐off for native cutthroat trout (Oncorhynchus clarkii) in 2 contrasting basins in western North America where invasion and isolation are either present and strong or farther away and apparently weak. These cases demonstrate that decisions to install or remove barriers to conserve native salmonids are often complex and depend on conservation values, environmental context (which influences the threat of invasion and isolation), and additional socioeconomic factors. Explicit analysis with tools such as those we propose can help managers make sound decisions in such complex circumstances.     

Evidence for the Role of Infectious Disease in Species Extinction and Endangerment

Abstract:  Infectious disease is listed among the top five causes of global species extinctions. However, the majority of available data supporting this contention is largely anecdotal. We used the IUCN Red List of Threatened and Endangered Species and literature indexed in the ISI Web of Science to assess the role of infectious disease in global species loss. Infectious disease was listed as a contributing factor in <4% of species extinctions known to have occurred since 1500 (833 plants and animals) and as contributing to a species' status as critically endangered in <8% of cases (2852 critically endangered plants and animals). Although infectious diseases appear to play a minor role in global species loss, our findings underscore two important limitations in the available evidence: uncertainty surrounding the threats to species survival and a temporal bias in the data. Several initiatives could help overcome these obstacles, including rigorous scientific tests to determine which infectious diseases present a significant threat at the species level, recognition of the limitations associated with the lack of baseline data for the role of infectious disease in species extinctions, combining data with theory to discern the circumstances under which infectious disease is most likely to serve as an agent of extinction, and improving surveillance programs for the detection of infectious disease. An evidence-based understanding of the role of infectious disease in species extinction and endangerment will help prioritize conservation initiatives and protect global biodiversity.