Taxonomic Considerations in Listing Subspecies Under the U.S. Endangered Species Act

Abstract:  The U.S. Endangered Species Act (ESA) allows listing of subspecies and other groupings below the rank of species. This provides the U.S. Fish and Wildlife Service and the National Marine Fisheries Service with a means to target the most critical unit in need of conservation. Although roughly one-quarter of listed taxa are subspecies, these management agencies are hindered by uncertainties about taxonomic standards during listing or delisting activities. In a review of taxonomic publications and societies, we found few subspecies lists and none that stated standardized criteria for determining subspecific taxa. Lack of criteria is attributed to a centuries-old debate over species and subspecies concepts. Nevertheless, the critical need to resolve this debate for ESA listings led us to propose that minimal biological criteria to define disjunct subspecies (legally or taxonomically) should include the discreteness and significance criteria of distinct population segments (as defined under the ESA). Our subspecies criteria are in stark contrast to that proposed by supporters of the phylogenetic species concept and provide a clear distinction between species and subspecies. Efforts to eliminate or reduce ambiguity associated with subspecies-level classifications will assist with ESA listing decisions. Thus, we urge professional taxonomic societies to publish and periodically update peer-reviewed species and subspecies lists. This effort must be paralleled throughout the world for efficient taxonomic conservation to take place.     

Species Richness, Endemism, and the Choice of Areas for Conservation

Although large reserve networks will be integral components in successful biodiversity conservation, implementation of such systems is hindered by the confusion over the relative importance of endemism and species richness. There is evidence (  Prendergast et al. 1993) that regions with high richness for a taxon tend to be different from those with high endemism. I tested this finding using distribution and richness data for 368 species from Mammalia, Lasioglossum, Plusiinae, and Papilionidae. The study area, subdivided into 336 quadrats, was the continuous area of North America north of Mexico. I also tested the hypothesis that the study taxa exhibit similar diversity patterns in North America. I found that endemism and richness patterns within taxa were generally similar. Therefore, the controversy over the relative importance of endemism and species richness may not be necessary if an individual taxon were the target of conservation efforts. I also found, however, that richness and endemism patterns were not generally similar between taxa. Therefore, centering nature reserves around areas that are important for mammal diversity (the umbrella species concept) may lead to large gaps in the overall protection of biodiversity because the diversity and endemism of other taxa tend to be concentrated elsewhere. I investigated this further by selecting four regions in North America that might form the basis of a hypothetical reserve system for Carnivora. I analyzed the distribution of the invertebrate taxa relative to these regions and found that this preliminary carnivore reserve system did not provide significantly different protection for these invertebrates than randomly selected quadrats. I conclude that the use of Carnivora as an umbrella taxon is an unreliable method for invertebrate conservation.     

Evaluating Completeness of Species Lists for Conservation and Macroecology: a Case Study of Mexican Land Birds

Abstract: Studies of species diversity, macroecology, and conservation are usually based on lists of species, but lists found in the scientific literature vary in completeness. The use of such data sets can produce misleading results, making it necessary to test species lists for completeness before undertaking an analysis. Species-richness estimators are useful for judging the completeness of species lists but have limitations. To add rigor to studies based on species lists, we propose that species lists should test for " omnipresent" taxa—species, genera, and families that occur throughout the region concerned—and for a minimum number of species and families. As a case study, we compared species assemblages in diverse habitats in Mexico and found that seven families and two genera of land birds are omnipresent in mainland Mexico (excluding treeless areas) and that the most depauperate assemblage known contains 35 species from 21 families. We concluded that a list of land birds from Mexico that lacks any of these omnipresent taxa or that contains fewer than 35 species or 21 families is incomplete. Similar analyses can be done for other taxa and other parts of the world. Tests for omnipresent taxa and for a minimum number of species and families can be used in combination with other existing criteria, such as species-richness functions, to better evaluate the completeness of species lists. Realistic results may be produced in macroecological and conservation studies only if they are based on reasonably complete species lists.     

Conservation Status as a Biodiversity Trend Indicator: Recommendations from a Decade of Listing Species at Risk in British Columbia

Abstract:  Species conservation status is commonly used as a broad-scale indicator of the state of biological diversity. To learn about its value for tracking trends, we examined provincial lists of terrestrial vertebrate species and subspecies at risk in British Columbia, Canada, for 1992 and 2002 to see whether changes in these lists reflected changes in the status of the taxa they represent. Examination of the case histories of individual species and subspecies showed that 65% of additions and deletions to the British Columbia Red List were the result of improvement in knowledge of species status, changes in assessment procedures, and refinements in taxonomy rather than actual changes in a species' status. Comparison to an alternate set of rank scores provided by NatureServe for taxa that appeared on both 1992 and 2002 British Columbia Red Lists revealed changes in status that were not reflected by movement from the list. Estimates of historical conservation status for species on the 1992 British Columbia Red List demonstrated ambiguity around the natural baseline with regard to tracking changes in list composition over time. We discourage the continued use of indicators based solely on conservation status as a means of tracking biodiversity. Instead we recommend advancing strategic indicators around species at risk based on long-term monitoring data, deliberate and explicitly stated baselines, and consistent methods of conservation ranking.     

Impacts of phylogenetic nomenclature on the efficacy of the U.S. Endangered Species Act

Cataloging biodiversity is critical to conservation efforts because accurate taxonomy is often a precondition for protection under laws designed for species conservation, such as the U.S. Endangered Species Act (ESA). Traditional nomenclatural codes governing the taxonomic process have recently come under scrutiny because taxon names are more closely linked to hierarchical ranks than to the taxa themselves. A new approach to naming biological groups, called phylogenetic nomenclature (PN), explicitly names taxa by defining their names in terms of ancestry and descent. PN has the potential to increase nomenclatural stability and decrease confusion induced by the rank‐based codes. But proponents of PN have struggled with whether species and infraspecific taxa should be governed by the same rules as other taxa or should have special rules. Some proponents advocate the wholesale abandonment of rank labels (including species); this could have consequences for the implementation of taxon‐based conservation legislation. I examined the principles of PN as embodied in the PhyloCode (an alternative to traditional rank‐based nomenclature that names biological groups based on the results of phylogenetic analyses and does not associate taxa with ranks) and assessed how this novel approach to naming taxa might affect the implementation of species‐based legislation by providing a case study of the ESA. The latest version of the PhyloCode relies on the traditional rank‐based codes to name species and infraspecific taxa; thus, little will change regarding the main targets of the ESA because they will retain rank labels. For this reason, and because knowledge of evolutionary relationships is of greater importance than nomenclatural procedures for initial protection of endangered taxa under the ESA, I conclude that PN under the PhyloCode will have little impact on implementation of the ESA. Impactos de la Nomenclatura Filogenética sobre la Eficiencia del Acta Estadunidense para las Especies en Peligro     

The Potential Conservation Value of Non‐Native Species

Abstract: 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.     

Impacts of tropical forest disturbance on species vital rates

Tropical forests are experiencing enormous threats from deforestation and habitat degradation. Much knowledge of the impacts of these land-use changes on tropical species comes from studies examining patterns of richness and abundance. Demographic vital rates (survival, reproduction, and movement) can also be affected by land-use change in a way that increases species vulnerability to extirpation, but in many cases these impacts may not be manifested in short-term changes in abundance or species richness. We conducted a literature review to assess current knowledge and research effort concerning how land-use change affects species vital rates in tropical forest vertebrates. We found a general paucity of empirical research on demography across taxa and regions, with some biases toward mammals and birds and land-use transitions, including fragmentation and agriculture. There is also considerable between-species variation in demographic responses to land-use change, which could reflect trait-based differences in species sensitivity, complex context dependencies (e.g., between-region variation), or inconsistency in methods used in studies. Efforts to improve understanding of anthropogenic impacts on species demography are underway, but there is a need for increased research effort to fill knowledge gaps in understudied tropical regions and taxa. The lack of information on demographic impacts of anthropogenic disturbance makes it difficult to draw definite conclusions about the magnitude of threats to tropical ecosystems under anthropogenic pressures. Thus, determining conservation priorities and improving conservation effectiveness remains a challenge.     

Biodiversity and Conservation of Plants in Brazil

Abstract:  With more than 56,000 species (excluding fungi), Brazil has one of the richest floras in the world—nearly 19% of the world flora. Our knowledge of the diversity and status of nonvascular plants in Brazil is still fragmentary, although localized studies on algae have revealed loss of species resulting from environmental pollution. Emphasis on local floral surveys, rather than wider taxonomic studies, has obscured estimates of national totals for most taxonomic groups. Knowledge of angiosperms, especially monocotyledons (of which 45% of the species are endemic), is more complete than most. For this group figures are more reliable, with some distribution patterns, endemism levels, and centers of diversity identified. Much, however, still awaits discovery. Coordinated efforts to catalog Brazil's flora are in progress and include projects such as the conservation priority-setting workshops of the Brazilian Ministry of the Environment, which have identified key conservation areas in the major biomes; development of threatened species lists for plants; and the assembly of type data on species of northeastern Brazil through the Darwin Initiative—all of which greatly assist in increasing our knowledge. These initiatives also underline the urgent need to expand the numbers and geographic spread of projects on plant systematics and taxonomy in Brazil, a measure that demands adequate provision of funding and training programs for plant specialists. Finally, Brazil's environmental agency (IBAMA) could play a proactive role in opening protected areas under its jurisdiction, thereby facilitating botanical research by university departments and research institutes.     

Building on IUCN Regional Red Lists to Produce Lists of Species of Conservation Priority: a Model with Irish Bees

Abstract:  A World Conservation Union (IUCN) regional red list is an objective assessment of regional extinction risk and is not the same as a list of conservation priority species. Recent research reveals the widespread, but incorrect, assumption that IUCN Red List categories represent a hierarchical list of priorities for conservation action. We developed a simple eight-step priority-setting process and applied it to the conservation of bees in Ireland. Our model is based on the national red list but also considers the global significance of the national population; the conservation status at global, continental, and regional levels; key biological, economic, and societal factors; and is compatible with existing conservation agreements and legislation. Throughout Ireland, almost one-third of the bee fauna is threatened (30 of 100 species), but our methodology resulted in a reduced list of only 17 priority species. We did not use the priority species list to broadly categorize species to the conservation action required; instead, we indicated the individual action required for all threatened, near-threatened, and data-deficient species on the national red list based on the IUCN's conservation-actions template file. Priority species lists will strongly influence prioritization of conservation actions at national levels, but action should not be exclusive to listed species. In addition, all species on this list will not necessarily require immediate action. Our method is transparent, reproducible, and readily applicable to other taxa and regions.     

Variation in resource consumption across a gradient of increasing intra- and interspecific richness

Based on the premise that ecosystems with more species will function at more efficient rates, declining biodiversity is expected to alter important ecosystem functions, goods, and services across the globe. However, applicability of this general hypothesis to genetic or clonal richness in assemblages composed of few species is understudied. This illustrates the need to expand the focus of biodiversity-ecosystem-function experiments across all levels of biological diversity (including genetic). To explore this generality, we manipulated intraspecific (clonal) and interspecific (species) richness of a primary consumer, Daphnia, and measured assemblage feeding rate and total resource consumption. Our results showed that greater clonal richness had no effect on Daphnia feeding, and greater species richness decreased feeding-related effects of Daphnia. This suggests that multiclonal Daphnia assemblages may be no more efficient at consuming resources than monocultures, and that monocultures of Daphnia may consume resources more efficiently than more species-rich assemblages. The inhibitory effect of increasing richness observed in this study resulted from chemical and mechanical interference among some of the Daphnia taxa. This suggests that consumer-mediated ecosystem functions could be reduced when assemblages include taxa equipped with adaptations for interference competition.     

Modern Insect Extinctions, the Neglected Majority

Abstract:  Most extinctions estimated to have occurred in the historical past, or predicted to occur in the future, are of insects. Despite this, the study of insect extinctions has been neglected. Only 70 modern insect extinctions have been documented, although thousands are estimated to have occurred. By focusing on some of the 70 documented extinctions as case studies, I considered ways in which insect extinctions may differ from those of other taxa. These case studies suggested that two types of extinction might be common for insects but rare for other taxa: extinction of narrow habitat specialists and coextinctions of affiliates with the extinctions of their hosts. Importantly, both of these forms of extinction are often ignored by conservation programs focused on vertebrates and plants. Anecdotal evidence and recent simulations suggest that many insect extinctions may have already occurred because of loss of narrow habitat specialists from restricted habitats and the loss of hosts. If we are serious about insect conservation, we need to spend more time and money documenting such extinctions. To neglect such extinctions is to ignore the majority of species that are or were in need of conservation.     

On how much biodiversity is covered in Europe by national protected areas and by the Natura 2000 network: insights from terrestrial vertebrates

The European Union has made extensive biodiversity conservation efforts with the Habitats and Birds Directives and with the establishment of the Natura 2000 network of protected areas, one of the largest networks of conservation areas worldwide. We performed a gap analysis of the entire Natura 2000 system plus national protected areas and all terrestrial vertebrates (freshwater fish excluded). We also evaluated the level of connectivity of both systems, providing therefore a first estimate of the functionality of the Natura 2000 system as an effective network of protected areas. Together national protected areas and the Natura 2000 network covered more than one‐third of the European Union. National protected areas did not offer protection to 13 total gap species (i.e., species not covered by any protected area) or to almost 300 partial gap species (i.e., species whose representation target is not met). Together the Natura 2000 network and national protected areas left 1 total gap species and 121 partial gap species unprotected. The terrestrial vertebrates listed in the Habitats and Birds Directives were relatively well covered (especially birds), and overall connectivity was improved considerably by Natura 2000 sites that act as stepping stones between national protected areas. Overall, we found that the Natura 2000 network represents at continental level an important network of protected areas that acts as a good complement to existing national protected areas. However, a number of problems remain that are mainly linked to the criteria used to list the species in the Habitats and Birds Directives. The European Commission initiated in 2014 a process aimed at assessing the importance of the Birds and Habitats Directives for biodiversity conservation. Our results contribute to this assessment and suggest the system is largely effective for terrestrial vertebrates but would benefit from further updating of the species lists and field management.     

Patterns of animal diversity in different forms of tree cover in agricultural landscapes.

As tropical regions are converted to agriculture, conservation of biodiversity will depend not only on the maintenance of protected forest areas, but also on the scope for conservation within the agricultural matrix in which they are embedded. Tree cover typically retained in agricultural landscapes in the neotropics may provide resources and habitats for animals, but little is known about the extent to which it contributes to conservation of animal species. Here, we explore the animal diversity associated with different forms of tree cover for birds, bats, butterflies, and dung beetles in a pastoral landscape in Nicaragua. We measured species richness and abundance of these four animal taxa in riparian and secondary forest, forest fallows, live fences, and pastures with high and low tree cover. We recorded over 20,000 individuals of 189 species including 14 endangered bird species. Mean abundance and species richness of birds and bats, but not dung beetles or butterflies, were significantly different among forms of tree cover. Species richness of bats and birds was positively correlated with tree species richness. While the greatest numbers of bird species were associated with riparian and secondary forest, forest fallows, and pastures with >15% tree cover, the greatest numbers of bat species were found in live fences and riparian forest. Species assemblages of all animal taxa were different among tree cover types, so that maintaining a diversity of forms of tree cover led to conservation of more animal species in the landscape as a whole. Overall, the findings indicate that retaining tree cover within agricultural landscapes can help conserve animal diversity, but that conservation efforts need to target forms of tree cover that conserve the taxa that are of interest locally. Preventing the degradation of remaining forest fragments is a priority, but encouraging farmers to maintain tree cover in pastures and along boundaries may also make an important contribution to animal conservation.     

Contribution of the Natura 2000 Network to Biodiversity Conservation in Italy

Abstract:  The Natura 2000 network is the most important conservation effort being implemented in Europe. Nevertheless, no comprehensive and systematic region—or nationwide evaluation of the effectiveness of the network has been conducted. We used habitat suitability models and extent of occurrence of 468 species of vertebrates to evaluate the contribution of the Natura 2000 network to biodiversity conservation in Italy. We also estimated the population size of 101 species inside the Natura 2000 network to assess its capacity to maintain or improve the population status of listed species. In general the Italian Natura 2000 did not seem to integrate existing protected areas well. The Natura 2000 network increased from 11% to 20% the area devoted to conservation in Italy and the coverage provided to areas with high biodiversity. Nevertheless, some areas with high numbers of species were devoid of conservation areas, and more than 50% of the highly irreplaceable areas were not considered in the system. Moreover, the Natura 2000 network cannot maintain 44–80% (depending on the taxa considered) of the species in a "favorable conservation status" under World Conservation Union Red List criteria. The Natura 2000 network is probably stronger than the results of our analyses suggest. The system is based on a site-specific expert-based strategy and is driven by direct and detailed knowledge of local diversity. Nevertheless, if Natura 2000 is taken to represent the final point of all the EU conservation policies, it will inevitably fail. Its role in conservation could be enhanced by integrating the Natura 2000 system into a more general strategy that considers natural processes and the ecological and evolutionary mechanisms underlying these processes.     

An Evaluation of Threatened Species Categorization Systems Used on the American Continent

Abstract:  Endangered species lists are important tools in conservation. It is essential that these lists be prepared using categorization systems that objectively assess species extinction risk. To determine which threatened species categorization system is the most appropriate and the virtues and limitations of systems used on the American continent, we evaluated 25 categorization systems from 20 countries. These systems included examples of international lists, most national systems used on the American continent, and some systems independently proposed by academics. We based our assessment on 15 characteristics that categorization systems should have, in terms of categories, criteria, and other relevant issues, in order to evaluate species conservation status objectively. Of all evaluated systems, the current World Conservation Union system is the most suitable for assessing species extinction risk. Most categorization systems, but particularly national systems, have serious deficiencies and need to be improved substantially. We recommend governments use three types of lists: (1) threatened species lists constructed following a sound categorization system, (2) lists of species of conservation priority, and (3) lists that serve as normative tools (e.g., Convention on International Trade in Endangered Species of Wild Fauna and Flora). Additionally, the information used to categorize species should be explicit and available to the public. To make the most of threatened species lists in conservation, it is imperative that all countries use the same categorization system.     

Terrestrial Reserve Networks Do Not Adequately Represent Aquatic Ecosystems

Abstract: Protected areas are a cornerstone of conservation and have been designed largely around terrestrial features. Freshwater species and ecosystems are highly imperiled, but the effectiveness of existing protected areas in representing freshwater features is poorly known. Using the inland waters of Michigan as a test case, we quantified the coverage of four key freshwater features (wetlands, riparian zones, groundwater recharge, rare species) within conservation lands and compared these with representation of terrestrial features. Wetlands were included within protected areas more often than expected by chance, but riparian zones were underrepresented across all (GAP 1–3) protected lands, particularly for headwater streams and large rivers. Nevertheless, within strictly protected lands (GAP 1–2), riparian zones were highly represented because of the contribution of the national Wild and Scenic Rivers Program. Representation of areas of groundwater recharge was generally proportional to area of the reserve network within watersheds, although a recharge hotspot associated with some of Michigan's most valued rivers is almost entirely unprotected. Species representation in protected areas differed significantly among obligate aquatic, wetland, and terrestrial species, with representation generally highest for terrestrial species and lowest for aquatic species. Our results illustrate the need to further evaluate and address the representation of freshwater features within protected areas and the value of broadening gap analysis and other protected‐areas assessments to include key ecosystem processes that are requisite to long‐term conservation of species and ecosystems. We conclude that terrestrially oriented protected‐area networks provide a weak safety net for aquatic features, which means complementary planning and management for both freshwater and terrestrial conservation targets is needed.     

Alternate Species Concepts as Bases for Determining Priority Conservation Areas

Abstract: Analysis of geographic concentrations of endemic taxa is often used to determine priorities for conservation action; nevertheless, assumptions inherent in the taxonomic authority list used as the basis for analysis are not always considered. We analyzed foci of avian endemism in Mexico under two alternate species concepts. Under the biological species concept, 101 bird species are endemic to Mexico and are concentrated in the mountains of the western and southern portions of the country. Under the phylogenetic species concept, however, total endemic species rises to 249, which are concentrated in the mountains and lowlands of western Mexico. Twenty-four narrow endemic biological species are concentrated on offshore islands, but 97 narrow endemic phylogenetic species show a concentration in the Transvolcanic Belt of the mainland and on several offshore islands. Our study demonstrates that conservation priorities based on concentrations of endemic taxa depend critically on the particular taxonomic authority employed and that biodiversity evaluations need to be developed in collaboration or consultation with practicing systematic specialists.     

Invertebrate Morphospecies as Surrogates for Species: A Case Study

Environmental monitoring and conservation evaluation in terrestrial habitats may be enhanced by the use of invertebrate inventories, but taxonomic and logistic constraints frequently encountered during conventional taxonomic treatment have greatly restricted their use. To overcome this problem we suggest that nonspecialists may be used to classify invertebrates to morphospecies without compromising scientific accuracy. To test this proposition, large pitfall and litter samples of ants, beetles, and spiders from four forest types were sorted to morphospecies by a nonspecialist and to species by specialists. These data were used to generate morphospecies and species inventories and to estimate richness (α diversity) and turnover (β diversity), information frequently used in the above activities. Our results show that the estimates of richness of ants and spiders varied little between morphospecies and species inventories. Differences between estimates of beetle richness were largely influenced by errors of identification in two families, Curculionidae and Staphylinidae. But morphospecies and species inventories yielded identical ranking of forest type using richness. Turnover was assessed by sample ordination, which revealed similar clusters regardless of the type of inventory. Analysis of similarities of assemblages of ants and beetles showed significant differences between all forest types. Spider assemblages showed a lower level of discrimination. The assessment of turnover was consistent among inventories but different between the major taxa. Our findings suggest that morphospecies may be used as surrogates for species in some environmental monitoring and conservation, in particular when decisions are guided by estimates of richness and the assessment of turnover.     

A strategy for the next decade to address data deficiency in neglected biodiversity

Measuring progress toward international biodiversity targets requires robust information on the conservation status of species, which the International Union for Conservation of Nature (IUCN) Red List of Threatened Species provides. However, data and capacity are lacking for most hyperdiverse groups, such as invertebrates, plants, and fungi, particularly in megadiverse or high-endemism regions. Conservation policies and biodiversity strategies aimed at halting biodiversity loss by 2020 need to be adapted to tackle these information shortfalls after 2020. We devised an 8-point strategy to close existing data gaps by reviving explorative field research on the distribution, abundance, and ecology of species; linking taxonomic research more closely with conservation; improving global biodiversity databases by making the submission of spatially explicit data mandatory for scientific publications; developing a global spatial database on threats to biodiversity to facilitate IUCN Red List assessments; automating preassessments by integrating distribution data and spatial threat data; building capacity in taxonomy, ecology, and biodiversity monitoring in countries with high species richness or endemism; creating species monitoring programs for lesser-known taxa; and developing sufficient funding mechanisms to reduce reliance on voluntary efforts. Implementing these strategies in the post-2020 biodiversity framework will help to overcome the lack of capacity and data regarding the conservation status of biodiversity. This will require a collaborative effort among scientists, policy makers, and conservation practitioners.