What Is Conservation Taxonomy?

THE AUTHORS Eugene Shinn

retired from the US Geological Survey recently after 31 years. Before that he worked for Shell Oil and established the Fisher Island Field Station in Miami Beach, Florida. He was a co-discoverer of modern giant submarine stromatolites (considered the first life forms on earth) that are forming in tidal areas of the Exuma Cays. He moved to the Coastal and Marine Geology Centre in St Petersburg, Florida in 1989 to work on the effects of offshore drilling on ecosystems, but is most recognised for his research on the effects of African dust on coral reef ecosystems. He is presently a courtesy professor at the University of South Florida College of Marine Sciences. William Hayes is a biology professor at Loma Linda University, California. He and his students study the behavioral ecology and conservation of various birds and reptiles in The Bahamas, including seabirds and endangered iguanas. However, much of his work has focused on venomous animals, especially rattlesnakes. He co-edited the volume Iguanas: Biology and Conservation and is currently editing The Biology of Rattlesnakes. Dan Brumbaugh is senior conservation scientist at the American Museum of Natural History’s Center for Biodiversity and Conservation. He has developed and leads a number of projects focusing on the design and implementation of marine protected areas. Dr. Brumbaugh has worked throughout the greater Caribbean and is a member of the BNT’s governing council. Juerg Brunnschweiler is a member of the American Elasmobranch Society, Animal Behavior Society, American Society of Ichthyologists and Herpetologists and a Fellow of the Conservation Science Institute. Since 2003 he has been working on his PhD at the University of Zurich, Switzerland. The main research topic of the thesis aims at a better understanding of bull shark ecology and behavior. Josh Van Buskirk did his PhD at Duke University on the population dynamics of dragonflies and went on to four postdoctoral research positions studying such diverse topics as Lyme disease ecology, metapopulation modeling, and sea turtle life history evolution. Currently, he has been a lecturer in the Department of Zoology, University of Melbourne, since 2003.

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Bahamas Naturalist & Journal of Science February 2006

Alfred Brathwaite

was born in Grenada and studied medicine at the University of the West Indies and London University. He has since worked in many Caribbean countries including Grenada, The Bahamas, Dominica, Suriname and the British Virgin Islands, where he is now based. He has published works on cancer and AIDS. He is married to Bahamian Vivian nee Isaacs, and they have three children. Lee Kass is visiting professor at Cornell University. As a Fulbright Scholar (1995-96), she established the National Herbarium for The Bahamas. She conducts research on plant diversity and pollination biology, and has published histories of nineteenth and twentieth-century American botanists. The second edition of her illustrated field guide to plants of San Salvador island, Bahamas, was published last June. Ingeria Miller is an undergraduate student at Cornell University. She graduated from the College of The Bahamas, where she learned botany and assisted in research on the Kirtland’s Warbler. She currently holds a scholarship at Cornell and is a research collaborator on the Red Winged Blackbird in the Bahamas. Paul Bartels was educated in the USA and at the University of the West Indies. A long-time researcher in the Bahamas where he conducts courses on coral reef ecology in the Bahamas, he is currently professor of Environmental Studies and Biology, and Chair of the Division of Science and the Environment Aat Warren Wilson College. Anthony White is a retired U.S. naval officer who is active in birding and conservation. He is a part time resident of the Bahamas, and the author of “A Birder’s Guide to the Bahamas”. He is a member of the BNT’s governing council, and a director of the American Birding Association and the Ornithological Council. He is currently working with Aileen Bainton on a bibliography of Bahamian birds. Alan Bolten is a University of Florida biologist who studies sea turtles. He is an advisor to the Archie Carr Center for Sea Turtle Research and a member of the BNT’s governing council.

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THE URGENT NEED FOR CONSERVATION TAXONOMY IN THE BAHAMAS: New Bird Species as an Example William Hayes Department of Earth and Biological Sciences Loma Linda University, California Taxonomists have largely ignored biodiversity questions in the Bahamas, so many distinct species of flora and fauna remain to be described as full species. Some of these previously overlooked species are highly endangered, warranting high-priority conservation status because distinct species receive higher priority than subspecies or local races. Their discovery in an era when new species are rarely described can generate considerable publicity, igniting efforts to save them and the habitats they require and improving public and decision-maker attitudes toward the environment. Thus, conservation taxonomy—the study of organismal classification to clarify conservation priorities— should be pursued vigorously, before many unrecognized species become extinct. There are a number of overlooked species candidates among birds, a group that engenders considerable public interest and sympathy. Recognizing some or all of these candidate taxa as distinct and (in many cases) endangered species may increase up to fourfold the number of endemic bird species in The Bahamas and dramatically alter conservation priorities. As ‘flagship’ species, protected birds can help to save other flora and fauna that depend on the same threatened habitats.

What Is Conservation Taxonomy? Few people—including many scientists and conservationists—recognize the importance of taxonomy. Our understanding of taxonomic relationships has profound, often unappreciated implications for conservation priorities (e.g., McNeely, 2002; Dubois, 2003; Mace, 2004). Because of this, we must understand the basic concepts and goals of conservation taxonomy and why we must pursue this emerging discipline vigorously. Simply put, conservation taxonomy is the study of organismal classification with the primary aim of clarifying conservation priorities. Taxonomy involves judgments regarding the relationships between groups of organisms, deciding, for example, what groups are distinct enough to be recognized as species (the fundamental unit of classification and biodiversity). The distinction between species (uniquely diagnosable forms) and subspecies (local races showing slight 12


differentiation) is important, as biologists prioritize saving species rather than subspecies with the limited funds available for conservation (see further discussion below). This prioritization also aims to preserve historically important processes, biodiversity, and habitats (e.g., Moritz, 1994; Zink, 2004). To illustrate this strategy, consider two species of lizards on one island, both of which are declining and, therefore, are in danger of extirpation. Species A is unique to this island, with no close relatives elsewhere. Species B, however, has very closely related populations (subspecies, or local races) that are common on two other islands. If funds are limited such that only one species can be saved, how should we prioritize their use? Obviously, we would prioritize saving species A because the loss of species A would result in global extinction, whereas the loss of species B would result only in local extinction. Clearly, our Vol 1 Issue 1

prioritization would be based on well-defined taxonomic relationships, with the goal of preserving the most distinct taxonomic groups. I should point out that, apart from Hayes et al. (2004a) and Goebel (2005), I have not seen the phrases ‘conservation taxonomy’ or ‘conservation systematics’ explicitly stated in the literature. I have used these terms in anticipation that they will become widely adopted in the future, as has begun to happen with ‘conservation genetics’ (Frankham et al., 2002) and ‘conservation medicine’ (Aguirre et al., 2002).

Why is Conservation Taxonomy Important? Tragically, and largely because of human indifference, we are now witnessing some of the highest rates of extinctions the planet has ever seen. Unfortunately, extinctions are just a small part of the equation that describes what we are doing to our planet. Although the loss of one or a few species may seem trivial, they often have major ramifications for entire ecosystems. An important lesson we need to recognize is that the health of our societies tracks closely the health of our natural environments. As Jared Diamond (2004) points out in his recent book, Collapse: How Societies Choose to Fail or Succeed, history assures us that environmental neglect often leads to an eco-meltdown, precipitating the collapse of otherwise-robust societies. Rapid population growth in The Bahamas currently drives an unprecedented boom in development, and this is exacerbated by wealthy North Americans and Europeans who value the archipelago’s beauty and tropical climate. As lamented by Pericles Maillis, former president of the Bahamas National Trust, the absence of a conservation ethic, ignorance, indifference to conservation, and population explosion all represent challenges that must urgently be met in The Bahamas. The greatest needs, he points out, are for massive public and decision-maker education and intensified scientific research (Maillis, 1998). The outcome of conservation taxonomy can help to meet these needs. The history of endangered species protection—especially for ‘charismatic’ megafauna such as reptiles, birds, and mammals—renders clear the fact that carefully orchestrated ‘rescue’ programmes can profoundly change a society’s attitudes toward the environment (e.g., Czech and Krausman, 2001). Indeed, The Bahamas National Trust has capitalized on this notion by using the Bahama Parrot and West Indian Whistling Duck, two threatened species, to increase public sympathies toward the environment. Conservation taxonomy also aids us in prioritizing biodiversity and endangered species management.

Biodiversity preservation is a major goal of conservation and species represent the taxonomic level at which biodiversity is usually measured. To sustain biodiversity, threatened species are often singled out for intensive management, which can consume valuable resources. Consider the following example. Until recently, raccoons in The Bahamas were regarded as an endemic species and were afforded official conservation status of high concern. However, Helgen and Wilson (2003) found historical, biogeographic, genetic, and morphological evidence that all West Indian raccoon populations (including those in Barbados and Guadeloupe) derived from human-sponsored introductions from the eastern U.S. Thus, while considerable funds might have been channeled to the study and protection of this ecologically disruptive, invasive species (see Hayes et al., 2004b, for the devastating impact a single raccoon had on an endangered iguana population), we can now allocate those funds for other, more deserving, endangered species. Without conservation taxonomy, we might lose biodiversity without realizing it until after the fact!

How Does One Conduct Conservation Taxonomy? Taxonomy involves studying the relationships between groups of organisms and making decisions about how to classify them. The basic unit of taxonomy and biodiversity is a species. Unfortunately, the terms ‘species’ and ‘subspecies’ are exceptionally difficult to define and will always remain controversial (see Box 1). However, one can think of a species as a distinct group of organisms that is clearly different from any other group, and a subspecies as one of several groups within a species that shows only a small degree of differentiation. A number of criteria can be applied to help one decide whether a group is distinct enough to comprise a species, including diagnosability (the capacity to assign an individual to the correct group with 100% accuracy) and reciprocal monophyly (showing that all members of a group are the unique descendents of a common ancestor; Figure 1). Here, I use both of these criteria in the sections that follow; however, because of their technical nature, they are treated in more detail in Box 1. Not all taxonomists may be in agreement as to whether a particular group warrants species status, so the more criteria and alternative species definitions that can be satisfied for a group under consideration (a candidate species), the more likely a consensus will be reached. Taxonomists measure variation among individuals within and between groups to reach their conclusions. They can evaluate many different characters, including molecular, morphological, physiological, developmental, Bahamas Naturalist & Journal of Science February 2006

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behavioral, and ecological traits. The choice of what to measure depends largely on the investigator’s area of specialty. A molecular biologist, for example, would examine genetic variation, whereas a morphologist would consider morphological traits. Today, some argue that we should restrict study to genetic variation, but this view is unnecessarily restrictive. Taxonomy can be readily conducted by virtually anyone with skills at deciphering and measuring variation in any of its many forms. By definition, conservation taxonomy focuses investigation on groups that may need special consideration because of their threatened status. The outcome of taxonomic investigation—whether or not one or more groups warrant recognition as distinct species or subspecies—provides invaluable information for setting conservation priorities.

Conservation Taxonomy of Bahamian Birds Ornithology—the study of birds—offers several compelling examples of the need for conservation taxonomy in The Bahamas. Here, I will illustrate that this relatively wellunderstood group has been overlooked to the point where potentially numerous species remain to be recognized in The Bahamas. This startling conclusion demonstrates our

poor understanding of biodiversity in the archipelago and argues that considerable work remains to be done for all groups of flora and fauna. But why study birds? First, because of their elegance, beauty, and the emotional response they evoke, endangered birds are hailed by conservationists as ideal ‘flagship’ species for rallying high-profile efforts to save threatened habitats. Flagship species must satisfy two criteria (Caro et al., 2004): their charismatic appeal to the general public and their potential to save additional species through efforts to protect them. Second, we are losing our bird diversity very rapidly. Recent computer models suggest that up to 14% of the world’s 9,000 species of birds will become extinct by the end of the century (Sekercioglu et al., 2004). As a consequence of their greater vulnerability, up to 56% of oceanic island species are expected to become extinct unless conservation efforts are greatly intensified. These numbers are disturbing. More than 10% of the West Indies region’s birds are already considered globally threatened (IUCN Red List; see Birdlife International’s web site). Within the Bahamas, local population extinctions have been well documented, with many recent examples (see Table 1). Finally, when considering the history of environmental activism from various perspectives (e.g., basic research,

THE PROBLEM OF SPECIES DEFINITIONS Unfortunately, no single, universally-applicable species definition exists. The term ‘species’ remains ambiguous, with a vast spectrum of meanings. Although a number of species concepts exist (e.g., morphological, ecological, biological, evolutionary, phylogenetic), they all have met with mixed success (e.g., Johnson et al., 1999; Agapow et al., 2004; Wiens, 2004; Weckstein et al., 2001; Remsen, 2005). Each species definition adopts a different biological property acquired by diverging lineages over time, with some properties evolving sooner than others (de Queiroz, 2005; Watson, 2005). One principle inherent to most, if not all, species definitions is the requirement that species be diagnosable (de Queiroz, 1998, 2005; Watson, 2005). Operationally, we can insist that 100% of the individuals of a given sex or age class of one group must be distinguishable from 100% of the corresponding individuals of any other group, and vice versa (e.g., Helbig et al., 2002). The character(s) used for diagnosis can include molecular, morphological, physiological, ecological, and/or behavioral traits, so long as they are heritable (not environmentally determined), non-clinal, and non-polymorphisms. To give an example, if all adult males of one frog group possess a dark bar on the hind leg, and all adult males of an otherwise similar group lack the dark bar, then many taxonomists would agree that two distinct species exist. More would subscribe to this view if additional independent (non-correlated) traits were similarly diagnostic (e.g., Helbig et al., 2002).

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Although less problematic for island (allopatric) populations, this approach breaks down where hybrid zones result because intermediate individuals will exist, and these befuddle diagnosis. However, one can infer a reproductive barrier by examining the breadth of the hybrid zone relative to dispersal ability (e.g., Johnson et al., 1999; Helbig et al., 2002). A relatively narrow hybrid zone would suggest that gene mixing is constrained by biological differences between the two groups. For those who study molecular variation, reciprocal monophyly has recently emerged as a popular concept for defining species. As a tree-based approach, gene sequences (usually from mitochondrial DNA) from individual organisms are used by sophisticated computer algorithms to generate a tree that captures the history of diverging lineages (Figure 1). A monophyletic group (or clade) consists of individuals sharing a common ancestor. To be reciprocally monophyletic, each such clade must have a common ancestor not shared by members of the other group (Figure 1). Different species may also be inferred from relative genetic distance, which often corresponds to the branching patterns described above. For example, if individuals of one group differ from individuals of a second group by 5% or more in sequence variation, they would frequently be considered distinct species. However, the amount of variance deemed sufficient for species recognition varies from group to group (Ferguson, 2002), so comparison of relative distance to that between Vol 1 Issue 1

public awareness, legislation), the plights of numerous threatened and endangered bird species have arguably galvanized more conservation initiatives than perhaps all other animal forms combined—such is their appeal to humans. As an archipelago, The Bahamas provide an ideal context for both speciation and extinction events. Because the ocean creates an obvious barrier to dispersal, many island populations evolve in isolation and gradually acquire unique traits. This long-term process results in endemism: the formation of new species and subspecies that occur only on a single island or island group. Indeed, the entire West Indies region is a recognized biodiversity hotspot with exceptionally high rates of endemism (e.g., plants 58%; amphibians 87%; reptiles 84%; birds 26%; mammals 30%; see Birdlife International’s web site). Because taxonomic relationships can be complex and sometimes exceedingly difficult to interpret, some unique forms in the Bahamas have no doubt been overlooked. Unfortunately, because of limited geographic distribution and constrained dispersal, many endemic forms are highly vulnerable to habitat loss and invasive species. Because new vertebrate species are rarely described today, the ‘discovery’ of a new one often captures considerable attention. Historically, ornithologists have recognized three bird species (Bahama Swallow, Bahama Woodstar,

other closely related species will serve as a rough guide for decision-making. Subspecies are also difficult to define. They are generally considered to be geographically distinct, genetically differentiated population segments of a single species. Because of its arbitrary nature, some have urged that we abandon the subspecies concept altogether (e.g., Zink, 2004). How distinct, for example, should a population be to warrant subspecific status, especially when clinal character variation frequently occurs? Recently, Patten and Unitt (2002) argued for the concept’s utility, showing how a criterion of 75% (or, more conservatively, 95%) reciprocal discrimination could be applied statistically to delineate subspecies more objectively. This view has gained a recent measure of acceptance (e.g., Remson, 2005). Conservationists have sought to refine somewhat analogous but equally contentious terms for setting conservation priorities (reviewed by Crandall et al., 2000; Fraser and Bernatchez, 2001). An evolutionarily significant unit (ESU) receives highest priority, and is quasi-equivalent to a distinct species. It can be defined (though opinions vary) as a population worthy of separate management based on having ecological and genetic variation of adaptive significance and/or unique evolutionary history. A management unit (MU) receives lesser priority, and is considered frequently to be quasi-equivalent to a subspecies. So how should we deal with the ‘species’ problem? Obviously, the greater the divergence we can demonstrate

Bahama Yellowthroat) and a multitude of subspecies as being endemic to The Bahamas (see Table 2). Of these, the Bahama Swallow is considered threatened but none are regarded as endangered. More research using refined techniques (and species concepts) will reveal that some currently recognized subspecies are, in fact, distinct species—and some of these may be highly endangered, without effective protection of their habitats. In reviewing the list of birds endemic to The Bahamas (Table 2), several stand out as excellent candidates for study. If some of these could be shown to be distinct, endangered species, they might dramatically alter conservation priorities within the Bahamas. Again, I have chosen to emphasize both diagnosability and monophyly as alternative tools for delineating species. Cuban Parrot (Amazona leucocephala; Figure 2) – The five subspecies described occur in the Bahamas, Cuba and Isle of Pines (two subspecies in Cuba), Grand Cayman, and Cayman Brac. Formerly widespread in the Bahamas, only two populations remain. Recent estimates suggest approximately 2,600 remain on Abaco and roughly 5,000 on Great Inagua (Wiley et al., 2004; Stahala, 2005). However, recent fires and the 2004 hurricanes significantly damaged habitat on Abaco, where new surveys are urgently needed. Using mitochondrial cytochrome b sequence data, Ottens-

between candidate species (as reflected by number of divergent traits, relative genetic distance, and even the number of species definitions met), the more likely a consensus will be reached on taxonomic status. Thus, exploring species limits ideally involves studying multiple lines of evidence (often called ‘total evidence’) and applying several or more species definitions appropriate for the evidence. In doing so, however, we need to be aware that different species concepts may yield different numbers of recognized species and, consequently, different quantities of biodiversity. Analyses suggest, for example, that the phylogenetic species concept recognizes more species (48% more on average) than the non-phylogenetic concepts (Agapow et al., 2004; see also Zink, 2004). With this in mind, we need to be as objective as possible when undertaking conservation taxonomy, resisting pressure to create new taxa as a strategy to serve conservation goals (Hey et al., 2003; Isaac et al., 2004). Here, I have chosen to emphasize both diagnosability and monophyly as alternative—though not always complimentary—tools for delineating species. Operationally, both of these criteria are sample size-dependent. As sample size increases, individuals having intermediate characters or non-exclusive haplotypes (an individual’s DNA sequence that falls outside a cluster of other individuals) may be detected, resulting in rejection of diagnosis or monophyly, respectively. Thus, sample size and associated variance warrant careful consideration.


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Table 1. Some recent (or probable) bird extinctions and extirpations in the Bahamas, with approximate decade of event.

Decade

Species, subspecies, or population

Island(s)

Source

Pre-1900

Brace’s Emerald (Chlorostilbon bracei) – species

New Providence

Graves and Olson, 1987

Pre-1900

Giant Kingbird (Tyrannus cubensis)

Great Inagua

Cory, 1891

Cuban Parrot (Amazona leucocephala bahamensis) – population West Indian Woodpecker (Melanerpes superciliaris bahamensis) – subspecies Bahama Swallow (Tachycineta cyaneoviridis) – population Great Lizard-cuckoo (Saurothera merlini bahamensis) – population Bahama Yellowthroat (Geothlypis rostrata rostrata) – subspecies Greater Antillean Oriole (Icterus dominicensis bahamensis) – population

Crooked, Acklins Islands

Snyder et al., 2000; Wiley et al., 2004

Grand Bahama

Emlen, 1977; White, 1998

1940’s 1950’s 1990’s 1990’s 1990’s 1990’s

Wainright et al. (2004) showed that the Bahamas subspecies (A. l. bahamensis) formed a distinct lineage that was monophyletic with the ‘short’ data set (based on shorter DNA fragments to include material extracted from museum specimens). The Grand Cayman subspecies (A. l. caymanensis) was also monophyletic (with the ‘long’ data set from fresh tissue samples; no data were available for the Cayman Brac form). Thus, although the authors did not comment on species limits, both the Bahamas and Grand Cayman taxa could be viewed as phylogenetic species dis-

New Providence New Providence New Providence Abaco

White, 1998, personal communication A. W. White, personal communication A. W. White, personal communication White, 1998, personal communication

tinct from the Cuban forms. The two Bahamas populations were less resolved by the sequence data, but their genetic divergence of 0.9% and obvious behavioral, ecological, and plumage differences (Ottens-Wainright et al., 2004; R. S. Gnam, pers. comm.) suggest that each population could be similarly viewed as diagnosably distinct species. Nesting habits differ remarkably, with Abaco birds utilizing limestone solution holes and Inagua birds relying, like all other New World parrots, on tree holes. The vocalizations of these two populations

Figure 1. Contrasting phylogenetic reconstructions (trees) for deciphering historical relationships between two hypothetical species (A and B) and a closely-related outgroup (C). Reciprocal monophyly can be inferred from the tree on the left, in which case all haplotypes (unique DNA sequences) of four individuals from group A are clustered and share a common ancestor (node with asterisk beside it) exclusive of all individuals from group B, and vice versa. Monophyly does not exist in the tree to the right, in which case the haplotypes of individuals are intermixed and non-exclusive.

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Figure 2. Cuban Parrot (Amazona leucocephala). The two island populations in the Bahamas (Abaco and Inagua) may represent one or two distinct species. With as few as 2,600 individuals, the Abaco population is especially endangered. Photo: Mark L. Stafford.

may also differ (R. Gnam, pers. comm.). Unfortunately, we do not know how variable other Bahamas populations were prior to their disappearance, though museum specimens suggest that the extirpated Crooked-Acklins population more closely resembled the Abaco population in plumage characters (M. B. J. Reynolds and W. K. Hayes, unpubl. data). The species (including all five subspecies) has been classified as ‘near threatened’ (Birdlife International, 2004), but the Bahamas form, as a candidate species, should be considered at least ‘vulnerable’ if not ‘endangered’ (Snyder et al., 2000). If viewed as two distinct species, the Abaco population should be considered ‘endangered’ (if not ‘critically endangered’) and the Inagua population at least ‘vulnerable.’ With support from Parrots International and other sources, Caroline Stahala, formerly at North Carolina State University, is studying the ecology of the Abaco population, which suffers from heavy invasive-mammal predation (cats and raccoons). Gina Mori, at University of Maryland Eastern Shore, is also studying their habitat use. The Bahamas National Trust is considering translocating Abaco birds to establish one or more additional populations (Wiley et al., 2004), a strategy urgently needed along with effective predator control. Further taxonomic resolution of this group can be expected from analysis of plumage, morphometric, and vocal variation by Bryant Reynolds, a graduate student at Loma Linda University. West Indian Woodpecker (Melanerpes superciliaris; Figure 3) – Six subspecies are currently recognized from

the Bahamas, Cuba, Isle of Pines and Grand Cayman Island. Whereas the Abaco subspecies (M. s. blakei) remains fairly common, the Grand Bahama subspecies (M. s. bahamensis) is already extinct, and the San Salvador Island subspecies (M. s. nyeanus) is critically endangered (probably fewer than 300 individuals remaining; Miller, 1978; W. K. Hayes, unpubl. data). As my own study of morphometric and plumage characters nears completion (most but not all available North American specimens have been examined), the data suggest that both the Abaco and San Salvador forms may be distinct species. Among the males that I have examined, (1) there was no overlap in body size (for combined measures) between the three Bahamas forms and the much larger Cuban form (M. s. superciliaris); (2) the small eye patch of nyeanus showed no overlap in size relative to all other populations (others possess a large eye patch, but the Cayman form, M. s. caymanensis, lacks an eye patch altogether); and (3) nyeanus had dark nasal tufts in contrast to the pale tufts of blakei (bahamensis was variable in this trait). However, Cuban specimens from offshore cays may overlap in size with Bahamas birds (Arturo Kirkconnell, pers. comm.). Vocalization and molecular analyses, when completed, will further clarify the species limits of this group. Unfortunately, both the Abaco and San Salvador populations took a severe hit from the September 2004 hurricanes (Bracey, 2005; W. K. Hayes, unpubl. data) and pending, large-scale development seriously threatens the San Salvador population (Hayes, 2004). A Disney Conservation Program grant supported recent work by Hayes on the San Salvador population,

Figure 3. West Indian Woodpecker (Melanerpes superciliaris). The two remaining subspecies in the Bahamas (on Abaco and San Salvador) may represent one or two distinct species. The San Salvador population is critically endangered, with fewer than 300 individuals. Photo: William K. Hayes. Bahamas Naturalist & Journal of Science February 2006

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which included field surveys and a conservation education program for all school-aged children (see www. SaveSanSalvador.com). Obviously, more will need to be done to save this critically endangered population. As an amusing anecdote, Nye (1899) mistakenly declared the San Salvador form extinct in 1899. Elwood Bracey is also studying the Abaco population (Bracey, 2005). Brown-headed Nuthatch (Sitta pusilla; Figure 4) – The Brown-headed Nuthatch is widespread in the southeastern United States, but an isolated population occurs on Grand Bahama. Long regarded as a subspecies (S. p. insularis), the Grand Bahama form was neglected until my own recent studies showed that it was not only a full species (S. insularis) but was also highly endangered, in desperate need of protection (Hayes et al., 2004a). Compared to continental populations, this taxon sports a longer bill and shorter wings, but its highly distinctive vocalizations lead to complete diagnosis. Surveys by Smith and Smith (1994) suggested the population had suffered a recent decline (>90%), but detection was hampered because Bahamas birds frequently use a vocalization different from continental populations. Recent surveys in July and August 2004, sponsored by the Grand Bahama Power Company, suggested that hundreds—possibly fewer than 1,000—remained (Hayes et al., 2004a).

Figure 4. Brown-headed Nuthatch (Sitta pusilla). The Bahamas population, restricted to Grand Bahama’s pine forest, has been proposed as a distinct species. With fewer than 1,000 individuals, this bird is also endangered. Photo: Gary L. Slater.

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Surveys in January, February, and July 2005 (by W. K. Hayes and Zeko McKenzie) indicated that the hurricanes in 2004 reduced this population and those of all other pine forest species. Intensive field work in April 2005 (by Gary Slater) suggested that nesting was delayed or foregone by many individuals, as nests were located for only two of eight nuthatch pairs encountered. This endemic bird requires fire-maintained tracts of Caribbean Pine (Pinus caribaea) and faces myriad threats, particularly from development and potential logging. At present, none of its habitat is formally protected. Yellow-throated Warbler (Dendroica dominica; Figure 5) – The Yellow-throated Warbler is another widespread southeastern United States species with isolated populations on Grand Bahama and Abaco. According to David Lee, of The Tortoise Reserve in North Carolina (manuscript in preparation), The Bahamas form (D. d. flavescens) may be a distinct species. It can be readily diagnosed from North American birds by bill length (longer) and shape, plumage characters (extensive yellow below, different facial pattern, different molt sequence), and song (ascending rather than descending notes). Unpublished genetic work by Irby Lovette at Cornell University (pers. comm.), based on a small sample (N = 1 from the Bahamas and N = 2 from the continent), found that The Bahamas and North American populations differed by only 0.4%, which would not support a species split (but again, molecular data do not always correspond

Figure 5. Yellow-throated Warbler (Dendroica dominica). Although not presently threatened, the two island populations in the Bahamas (Abaco and Grand Bahama) have a limited distribution and may comprise a distinct species. Photo: J. Bruce Hallett, Jr. Vol 1 Issue 1

Table 2. Endemic bird species (bold font) and subspecies of the Bahamas (modified after White, 1998).

Common name

Scientific name

Present range (status) and comments

Green Heron Clapper Rail

Butorides virescens bahamensis Rallus longirostris coryi Amazona leucocephala bahamensis Saurothera merlini andria Saurothera m. bahamensis Chlorostilbon bracei Calliphlox evelynae evelynae Calliphlox evelynae lyrura

Throughout (common) Throughout (common) Abaco and Great Inagua (threatened); probably one or two distinct species Andros (common) New Providence (extirpated?) and Eleuthera (common) Formerly New Providence (extinct) Throughout except Inaguas (common) Great and Little Inagua (common) Abaco (common before 2004 hurricanes); possibly colonizing east end of Grand Bahama Grand Bahama (extirpated) San Salvador (endangered) New Providence and Andros (common) Grand Bahama and Abaco (common) Northern islands (common) Northern islands and Inaguas (common)

Cuban (Bahama) Parrot Great Lizard-Cuckoo Brace’s Emerald Bahama Woodstar

Melanerpes superciliaris blakei West Indian Woodpecker

Bahama Swallow

Melanerpes s. bahamensis Melanerpes s. nyeanus Picoides villosus maynardi Picoides villosus piger Contopus caribaeus bahamensis Myiarchus sagrae lucaysiensis Tyrannus caudifasciatus bahamensis Tachycineta cyaneoviridis

Brown-headed Nuthatch

Sitta pusilla insularis

Red-legged Thrush

Yellow Warbler

Turdus plumbeus plumbeus Vireo crassirostris crassirostris Vireo crassirostris stalagmium Dendroica petechia flaviceps

Yellow-throated Warbler

Dendroica dominica flavescens

Pine Warbler

Dendroica pinus achrustera Geothlypis rostrata rostrata Geothlypis r. exigua Geothlypis r. tanneri Geothlypis r. coryi Coereba flaveola bahamensis

Hairy Woodpecker Cuban Pewee La Sagra’s Flycatcher Loggerhead Kingbird

Thick-billed Vireo

Bahama Yellowthroat Bananaquit Western Spindalis (Stripeheaded Tanager)

Spindalis zena zena

Greater Antillean Bullfinch

Loxigilla violacea violacea

Spindalis zena townsendi

Red-winged Blackbird

Loxigilla violacea ofella Agelaius phoeniceus bryanti

Greater Antillean Oriole

Icterus dominicensis northropi

well with other data sets; see Box 2). Fortunately, this Bahamian endemic is neither threatened nor endangered, but like the nuthatch, it is dependent on the pine forest, which is clearly at risk from development and logging interests. Its limited distribution, on just two islands, makes it a species of special concern.

Northern islands (common) Northern islands (threatened) Grand Bahama (endangered); recently described as a distinct species Northern islands (common) Throughout except Turks and Caicos (common) Caicos Islands (common) Throughout (common) Grand Bahama and Abaco (common); probably a distinct species Northern islands (common) New Providence (endangered, possibly extirpated) Andros (common) Grand Bahama and Abaco (common) Eleuthera and Cat Island (common ) Throughout (common) Throughout except Grand Bahama, Abaco, San Salvador, and Rum Cay (common) Grand Bahama and Abaco (common) Throughout except San Salvador, Rum Cay, and Turks and Caicos (common) Middle and East Caicos (common) Northern islands (common) Abaco (extirpated) and Andros (endangered); probably a distinct species

Curiously, both this bird and the nuthatch have longer bills in the Bahamas compared to continental populations, suggesting that their bills have been subject to similar selective pressures (c.f . Ficken et al., 1968). At present, nobody is studying the Bahamas form. Bahamas Naturalist & Journal of Science February 2006

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Greater Antillean Oriole (Icterus dominicensis; Figure 6) – Four subspecies of I. dominicensis are currently recognized in the Caribbean, each on a different island group (Bahamas, Cuba, Hispaniola, Puerto Rico). The Bahamas form (I. dominicensis northropi), although genetically similar to the Cuban race (0.9% genetic distance; Omland et al., 1999), can be easily diagnosed by several plumage characters in adults (Omland and Lanyon, 2000; M. Price and W. K. Hayes, unpubl. data). Additional differences in adult morphology, juvenile plumage, and vocalizations prompted Garrido et al. (in press) to elevate each of the island groups to full species status. Thus, The Bahamas form should soon be recognized as a distinct species (I. northropi). Sadly, the population on Abaco disappeared in the early 1990s, for unknown reasons. More alarming, Shiny Cowbirds (Molothrus bonariensis), nest parasites that lay their eggs in the nests of other bird species, have recently immigrated to the Bahamas and now threaten the last remaining oriole population on Andros (Baltz, 1996). Shiny cowbirds parasitize up to 100% of nests in some oriole populations in Puerto Rico (Wiley, 1985; Perez-Rivera, 1986) and have driven several West Indies bird populations to near-extirpation (e.g., Wiley et al., 1991). A brief survey in 1997 suggested that fewer than 300 orioles remained on Andros (Baltz, 1997). Clearly, this bird is critically endangered. Intensive management (e.g., cowbird trapping near nest sites, translocation of new population to Abaco) seems required to prevent extinction of this elegant bird, and should commence immediately. Melissa Price, a graduate student at

Loma Linda University, is nearing completion of a study on plumage variation among the island populations. She also conducted population surveys on Andros in 2005 (her analyses remain unfinished). Other species candidates – The remaining bird forms listed in Table 2 also deserve investigation, though few other than those mentioned above are likely to become soon threatened. James Wiley (pers. comm.) is nearing completion of studies of the Red-legged Thrush (Turdus plumbeus) and Loggerhead Kingbird (Tyrannus caudifasciatus), and he suggests that The Bahamas populations may be distinct species. He is also studying the Cuban Pewee (Contopus caribeus). In their recent split of the West Indies genus, Spindalis (Stripe-headed Tanager), Garrido et al. (1997) included The Bahamas populations with the widespread species S. zena, occurring also on Cuba, Grand Cayman, and Cozumel Island. They also recognized two endemic subspecies in the Bahamas: S. z. townsendi on Grand Bahama and Abaco, and S. z. zena elsewhere in the Bahamas (Table 2). However, genetic work by Nedra Kline, who passed away before publishing her data, suggested that The Bahamas populations represented a distinct species (A. W. White, pers. comm.).Unfortunately, it may be of little use to examine the New Providence race of the Bahama Yellowthroat (Geothlypis r. rostrata), which may already be extinct (White, 1998). The Blue-gray Gnatcatcher (Polioptila caerula) could be added to the list, as some have considered The Bahamas population to be a distinct subspecies (see White, 1998). Curiously, the Blue-gray Gnatcatchers and Pine Warblers (Dendroica pinus achrustera) forage extensively on bark in the pine forests of Andros, but avoid doing so on Grand Bahama (Emlen, 1981). Gnatcatchers from these two islands may also differ in voice and plumage (Larry Manfredi, pers. comm.).

An Overlooked Avifauna

Figure 6. Greater Antillean Oriole (Icterus dominicensis). The only remaining population in the Bahamas, on Andros, has been proposed as a species split. As few as 300 individuals remain of this critically endangered bird. Photo: J. Bruce Hallett, Jr.

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It seems remarkable that, after decades of stasis in Bahamas bird taxonomy, up to 10 previously unrecognized species (and possibly more) may still be out there. This list of candidate species includes two parrots, two woodpeckers, a flycatcher, a nuthatch, a thrush, a warbler, a tanager, and an oriole. Compared to the Greater Antilles, The Bahamas seem to have relatively low endemism for bird species (Table 3). At present, only three are recognized as endemic: the Bahama Swallow, Bahama Woodstar, and Bahama Yellowthroat (Table 2). The candidate species described here could increase Vol 1 Issue 1

up to fourfold the number of Bahamas endemics, bringing it closer to the number of endemics supported by some of the larger West Indies islands and exceeding that of any single Lesser Antilles island (Table 3). How have these birds eluded us? The reality is that they haven’t. We’ve simply overlooked them. It’s not like these birds have been hiding from us behind impenetrable vegetation, as was the case with recently discovered Double-striped Thickknees (Burhinus bistriatus) breeding on Great Inagua in The Bahamas (A. W. White, pers. comm.). We’ve actually had the specimens out of sight but easily accessed in museum drawers for many decades!

An Unprotected Avifauna Would the outcome of conservation taxonomy create new conservation priorities? Table 4 summarizes the endangered and threatened bird taxa in The Bahamas and the extent to which their populations enjoy formal protection of their habitat. The level of threat varies considerably among taxa, but the candidates for new species will definitely emerge as the most threatened. At present, just two resident species are considered ‘vulnerable’ (West Indian Whistling Duck, Dendrocygna arborea, and Bahama Swallow), and none are regarded as ‘endangered’ or ‘critically endangered.’ However, if elevated to full species, the Abaco Parrot and Bahama Nuthatch would be recognized as ‘endangered’ at a minimum, and the San Salvador Woodpecker and Bahama Oriole would be ‘critically endangered.’ Clearly, priority for conservation would increase dramatically for these species and conservation authorities would need to grapple with options to better protect and save them. How well protected are the most threatened bird speTable 3. Number of endemic bird species for various West Indies islands and island groups (as gleaned from Raffaele et al., 1998); extinct taxa and populations are excluded, as are very recent and anticipated splits. These numbers differ slightly from those cited by Gnam (2004) and by other authors.

Bahamas Turks & Caicos Cuba Cayman Islands Jamaica Hispaniola Puerto Rico Virgin Islands Anguilla St. Martin St. Barthelemy Saba St. Eustacius

3 0 25 0 31 26 15 0 0 0 0 0 0

St. Christopher & Nevis Antigua & Barbuda Montserrat Guadeloupe Dominica Martinique St. Lucia Barbados St. Vincent & Grenadines Grenada Providencia San Andres

0 0 1 1 2 1 4 0 2 1 0 1

cies in The Bahamas? The government has laudably set aside 25 national parks comprising more than 2500 square kilometers. Fortunately, some of these protect substantial habitat for a few threatened species (Table 4), including the Audubon’s Shearwater (Puffinus lherminieri) in the Exuma Cays Land and Sea Park, and the Cuban Parrot in both the Abaco National Park (where about 64% of the parrots nest, but they disperse widely outside the breeding season; C. Stahala, pers. comm.) and the Inagua National Park. However, several of the new candidate species considered here are conspicuously lacking habitat protection (Table 4). The Bahama Oriole receives trivial benefit, whereas the Bahama Nuthatch and San Salvador Woodpecker receive none whatsoever. A number of seabird species are also included in Table 4 because of their dramatic declines in the West Indies region. As a group, seabirds are disproportionately threatened because of their high vulnerability to human disturbance (White and Lee, 2001). Although five of the nine seabird taxa listed are not endemic to the West Indies region, The Bahamas hosts major colonies that urgently need protection. Rather than offer recommendations on where to establish additional preserves, I’m simply pointing out the current lack of adequate taxonomic knowledge for setting conservation priorities. Clearly, some of the bird taxa most at risk have been tragically overlooked, are in dire threat of extinction, and lack formal protection of their habitat. Money should not necessarily be spent preferentially to save the most endangered species, because some highly ranked species require huge recovery efforts with a small chance of success (Possingham et al., 2002). Similarly, preserves should not be preferentially allocated to the most endangered species because other objectives, such as securing as many species as possible within socioeconomic constraints, might be more appropriate (Possingham et al., 2002). In other words, the concept of triage will need to be applied to the decision-making. To better identify and understand potential biodiversity ‘hotspots’ (local areas with exceptionally high biodiversity) in The Bahamas, several collaborators and I are presently analyzing various indices of biodiversity (species richness, endemism, threat) for each of the terrestrial vertebrate classes (amphibians, reptiles, birds, mammals) that live on the various island groups of The Bahamas. Because measures of biodiversity depend on taxonomic rankings, our analyses will consider independently both species and subspecies. We expect to find incongruence among these factors (the different indices, vertebrate classes, and taxonomic levels), much as hotspots differ among the different indices for birds at a global scale (Orme et al., 2005). Nevertheless, the exercise should be Bahamas Naturalist & Journal of Science February 2006

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highly informative for identifying local hotspots and their salient properties. Apart from the issue of habitat protection, further research is essential for each of these candidate taxa. We urgently need to (1) identify or confirm their taxonomic distinctivenes, (2) determine habitat preferences, current population size, and long-term population trends through detailed field surveys, (3) assess current or potential conservation threats, (4) learn more about the bird’s basic ecology and reproductive requirements, and (5) develop sound management plans that may include predator/host parasite control, captive breeding, and translocation to establish (or reestablish) new populations. Clearly, much work remains to be done!

Conservation Taxonomy of Additional Groups I have chosen to emphasize birds in this paper, but conservation taxonomy is certainly needed for other organisms. As examples, I’ll briefly mention just two groups. There are many dozens of morphologically differentiated reptile populations scattered throughout The Bahamas. Most of these are recognized at only the subspecific level, and we have virtually no data on their population (conservation) status. With rapid habitat destruction and increasing competition from invasive species (Lee, 2005), how many of these reptiles will disappear before we learn that they are distinct species? Recent work on tenebrionid beetles by Warren Steiner points out our even greater lack of knowledge about invertebrates. From San Salvador Island alone, he has recently described 10 species new to science, most of which were presumed to be endemic to the island (Steiner, in press). Of the 29 species he found on San Salvador, only four had been detected previously. Although the conservation status of these beetles remains in question, four of the beetle species were introduced exotics. Of course, the presence of exotics does not bode well for the endemic forms.

A Plea for Funding Progress on conservation taxonomy requires considerable time, effort, and expense. Those engaged in it are generally from foreign academic institutions (primarily in the U.S.) who struggle continually for funding. Often, these individuals are motivated by intellectual curiosity and a compelling desire to contribute to an understudied region, rather than to earn promotion and tenure. Without doubt, there are countless private individuals and corporations sympathetic to conservation issues and willing to contribute financially. As an example, the Grand Bahama Power Company recently supported my own work on the Brown-headed Nuthatches, which led to 22


its recognition as a distinct, endangered species (Hayes et al., 2004a). Given the uncertain future the nuthatches face, we can only hope that our new understanding has arrived in time to make a difference. Even more challenging will be the follow-up needs of conservation taxonomy when newly-recognized, highlyendangered species are described. Recovery programmes for endangered species can be very costly, as they often involve extensive in situ work. Some endangered species require perpetual management, as their habitats have been decimated to the point where they are now relegated to suboptimal habitats that can no longer support them without human intervention. Ideally, management decisions should be based on real science (Sutherland et al., 2004) and include detailed natural history study (Greene, 2005), adding to the costs. As good neighbors and stewards, we owe our feathered friends their continued existence. The continuing challenge will be to bring the researchers and potential sponsors together. What will it take to make this happen? Historically, researchers studying the archipelago’s flora and fauna have been largely on their own in finding sources of funding. No doubt, this explains much of the lack of attention to taxonomic relationships. (Tragically, some biologists have even repressed investigation by others, seeking exclusive recognition for their own expertise.) Perhaps the government and NGOs can take a more active role in soliciting funds from sources they have better access to. Obviously, the plight of endangered species can be used as an advantage in making appeals for contributions. The outcome of conservation taxonomy will likely net a plethora of high-priority endangered species. Many of these species will need costly rescue programmes if they are to persist. Do the people of The Bahamas, their government, and their NGOs have the willpower to take on such a commitment? I can only hope so. ACKNOWLEDGMENTS This manuscript benefited from discussions with Tony White, David Lee, Rosemarie Gnam, Floyd Hayes, Eric Carey, Carolyn Stahala, James Wiley, and Woody Bracey. I must also take this opportunity to single out Tony White, thanking him for encouraging me to study bird taxonomy and for his extensive knowledge of and willingness to share references on Bahamas birds. This work derives in part from studies supported by the Grand Bahama Power Company and the Disney Conservation Programme

REFERENCES Agapow, P. M., O. R. P. Bininda-Emonds, K. A. Crandall, J. L. Gittleman, G. M. Mace, J. C. Marshall, and A. Purvis. 2004. The impact of species concepts on biodiversity studies. Quart. Rev. Biol.79:161-179. Aguirre, A. A., R. S. Ostfeld, G. M. Tabor, C. House, and M. C. Pearl (Editors). 2002. Conservation Medicine: Ecological Health in Practice. Oxford University Press, Oxford. Baltz, M. E. 1996. The distribution and status of shiny cowbirds on North Andros Island. Bahamas J. Sci. 3(2):2-6. Baltz, M. E. 1997. Status of the black-cowled oriole (Icterus dominicensis northropi) in the Bahamas. Unpublished report to the Ministry of Fisheries and Agriculture, Department of Agriculture, Nassau, Bahamas.

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Table 4. Endangered and threatened birds of the Bahamas, with current taxonomic rank (including range where found), threat status (NT = near-threatened; VU = vulnerable; EN = endangered; CR = critically endangered), estimated West Indies population size, estimated Bahamas population size, source for threat and population assessments, and amount of protected habitat relative to the estimated population within the Bahamas (none; poor = less than 10%; fair = 10-50%; good = more than 50% of Bahamas population). Endemic species are shown in bold.

Audubon’s Shearwater

Taxonomic rank (range) Subspecies (West Indies)

White-tailed Tropicbird

Subspecies (West Indies)

Common name

Brown Booby Red-footed Booby Brown Pelican Double-crested Cormorant Magnificent Frigatebird West Indian Whistling Duck

Population (West Indies) Population (West Indies) Subspecies (West Indies) Subspecies (West Indies) Population (West Indies) Species (West Indies)

Estim. pairs West Indies

Estim. pairs Bahamas

Source

NT

3,000-5,000

2,000-3,000

White & Lee, 2001

NT

5,000

1,000

White & Lee, 2001

NT

5,000-8,000

200-1,500

NT

8,000-10,000

3

NT

1,500

50-100

NT