S26.2: Species concepts and setting conservation priorities: A Mexican case study

With recognition of the global biodiversity crisis in the 1980s (Wilson 1988), many efforts were initiated to prioritise areas for conservation action on the basis of total species richness or richness of endemic species. For example, the International Council for Bird Preservation (ICBP 1992) plotted distributions of 2609 bird species with geographic ranges restricted to areas of less than 50000 km², and used patterns of coincidence of those distributions to identify 221 ‘endemic bird areas.’ Those areas, as well as priority areas identified by other projects, have served as guides in planning conservation action in numerous regions (e.g., Escalante-Pliego et al. 1993; Bojórquez-Tapia et al. 1995; Price et al. 1995).

Many such analyses, especially those related to birds, simply cite an authority for species names used as units of analysis (e.g., ICBP 1992; Collar et al. 1992; Bojórquez-Tapia et al. 1995). This approach - analysis of geographic patterns assuming a particular taxonomic authority list to be representative - leads investigators to focus attention on species' distributions without concern for geographic variation, systematic problems, or species limits. We question the validity of this approach for prioritising areas for conservation. So, we analysed conservation priorities under two alternative species concepts, and found that conservation priorities in biodiversity analyses depend critically on the taxonomic viewpoint of authority lists. This paper represents a further development of ideas developed in Peterson and Navarro (in press).

We assembled a data base of 128 avian taxa occurring in Mexico that are presently considered single biological species in a widely-used authority list (AOU 1983). Each taxon includes multiple units recognisable as phylogenetic or evolutionary species (Zink & McKitrick 1995). Sources included systematic studies by us and our colleagues and students (e.g., Benítez-Díaz 1993; Escalante-Pliego & Peterson 1992; Navarro-Sigüenza et al. 1992; Peterson 1992; Peterson et al. 1992; Peterson 1993); inspection of specimens in scientific collections (Peterson et al. 1998); review of the scientific literature (Rodríguez-Yáñez et al. 1994); and a recent guide to the birds of the region (Howell & Webb 1995). This list of phylogenetic species, contrasted with the biological species list (AOU 1983), formed the basis of the results reported herein and is presently under consideration for publication (Navarro-Sigüenza & Peterson submitted).

Assessment of conservation priorities based on alternative taxonomies followed approaches used in our previous studies (Escalante-Pliego et al. 1993) to permit detailed comparisons. A regionalisation based on Mexican biotic provinces divided the country into 35 units, of which five were peripheral islands and 30 were mainland areas. Endemism was defined at the level of all of Mexico (‘Mexican endemics’), and at the level of single regions (‘narrow endemics’). For the purpose of visualisation, we emphasised areas ranking in the top 10 and 20% as priority areas.

Under the biological species concept, Mexico holds 101 endemic species (AOU 1983; Escalante-Pliego et al. 1993). Many biological species, however, actually consist of multiple units that are diagnosable and presumably monophyletic, and can be recognised as phylogenetic species (Zink & McKitrick 1995). For example, among Mexican populations of the biological species Emerald Toucanet Aulacorhynchus prasinus are an eastern form A. prasinus with a yellow base of the bill, and an allopatric, southwest - Mexican endemic form A. wagleri that has a black base of the bill. Similarly, among the Mexican populations of the biological species Scrub Jay Aphelocoma coerulescens are three diagnosable subunits treatable as phylogenetic species: Baja California A. californica; Chihuahuan Desert and mountains of northern Mexico A. woodhouseii; and central and southern Mexico A. sumichrasti, endemic; (Peterson 1992). Among the most complex taxa currently considered a single biological species are the bobwhites Colinus virginianus, with recognisable forms in Sonora C. ridgwayi; central Veracruz C. pectoralis; the Mexican tableland and Balsas Basin C. graysoni; the Pacific coast from Guerrero to Chiapas C. coyolcos; southern Veracruz and the interior valley of Chiapas C. godmani; as well as true C. virginianus in northeastern Mexico. Considering phylogenetic species taxa across Mexico, endemism levels rose to about 249 species.

Switching to a taxonomy made up of phylogenetic species, which are more finely divided geographically than biological species (Zink & McKitrick 1995), might seem unlikely to change the overall geographic picture of endemism, simply providing increased detail (Amadon & Short 1992). Previously, we analysed geographic patterns of diversity and endemism of birds in 35 regions of Mexico based on a biological species list (Escalante-Pliego et al. 1993), pointing out a contrast between concentrations of species richness and concentrations of endemic species (Escalante-Pliego et al. 1993, Peterson et al. 1993, Peterson & Salazar in press). Species richness was concentrated in the eastern tropical lowlands, whereas endemism was concentrated at middle-to-high elevations in the mountains of western and central Mexico (Table 1, Fig. 1a). Regions especially rich in Mexican endemic species were the middle portion of the Sierra Madre Occidental, the Transvolcanic Belt, the southern Sierra Madre Oriental, and the Sierra Madre del Sur (Table 1). Narrow endemic species were sparsely distributed (Fig. 1c: ten regions held single narrow endemics, five held two narrow endemic species, and one [Islas Revillagigedos] held four).

The shift to phylogenetic species, however, changed the picture of avian endemism in Mexico considerably (Fig. 1b, Table 1). Besides the middle Sierra Madre Occidental and the Transvolcanic Belt, the Pacific coastal lowlands of western and southern Mexico were recognised as a previously under-appreciated focus of avian endemism (Table 1), and the southern Sierra Madre Oriental and the Nudo de Zempoaltepec were less important. Hence, changing the species concept had profound effects on conclusions regarding the distribution of endemism.

Focusing on species perhaps most vulnerable to extinction - narrow endemics - the picture changed drastically. In addition to the Islas Revillagigedos (four biological species), which were the sole focus in the biological species analysis, Isla Cozumel (nine species), the Islas Tres Marías (eight species), and Isla Guadalupe (seven species) all entered as important concentrations (Table 1). More interestingly, two continental areas were emphasised that had been ignored in the biological species analysis - the Transvolcanic Belt (nine species) and the southern tip of the Baja Peninsula (7 species) - previously unrecognised foci of narrow endemism (Fig. 1d). Hence, the distribution of narrow endemism changed considerably depending on the species concept employed.

Different species concepts also affect biological inventories for regions at different levels. For three major states in southern Mexico, state bird lists are available. Known avian diversity in each was augmented significantly by transition to the phylogenetic species concept: by 17 species for Veracruz (Alcántara in prep.), 25 for Guerrero (Navarro 1998) and 37 for Oaxaca (Binford 1989). The differences in incremental increases probably result from the states being physiographically and biogeographically complex, involving severeal areas of endemism that are more easily detectable under the phylogenetic species concept.

Avian taxonomy is in need of considerable study and reassessment (Peterson & Stotz 1992). In case after case, taxa considered polytypic species upon further study have proven to comprise two or more valid species under the biological species concept (e.g., Escalante-Pliego & Peterson 1992; Peterson 1992; Benítez-Díaz 1993). The AOU has recognised numerous new forms in North America as a result of such investigations (AOU 1998). The field has been challenged further by the appearance of the phylogenetic and evolutionary species concepts, which bypass the ‘biological species’ criterion of reproductive isolation and look instead to criteria of monophyly and diagnosability (Zink & McKitrick 1995). Changes to authoritative taxonomic lists are generally made only following publication of detailed systematic studies (AOU 1983), inevitably producing long time lags and taxonomic imbalances as some groups are reworked and others are not. These imbalances, combined with the results of our study, suggest that high priority should be placed on development and refinement of fauna-wide, regional taxonomic revisions to make broad comparisons and conclusions feasible.

Species-based biological inventories developed by non-systematists can encounter serious biases by ignoring independent evolutionary units, thus underestimating patterns of species richness and endemism that are present in certain regions. A common example is when one of the species units is a permanent resident and other is migrant (e.g. Dendroica [petechia] aestiva versus D. [petechia] petechia and D. [petechia] erithachorides), or in regions where more than one species units occur.

We have demonstrated that conservation priorities based on biodiversity considerations are sensitive to taxonomic viewpoint. General tendencies can be recognised in the shifts observed—biological species show faunas richest in endemic species in central areas, with faunas increasingly rarefied at peripheral sites. Phylogenetic or evolutionary species, in contrast, are often present in small, isolated areas along the periphery of species complexes' distributions, making peripheral and particularly isolated areas more rich in endemic species. These tendencies likely lead to the differences documented in this paper.

If changing species concepts can modify our view of distribution and endemism, an expected result is that many of those previously unrecognised units will fall in one of several conservation status categories widely used both at international and national levels. As an example, several of the new forms will fulfil the threshold criteria (Wege & Long 1995) of very small range (e.g. several island forms), habitat fragmentation (cloud-forest restricted species in western Mexico, Sierra de los Tuxtlas, and the Transvolcanic Belt; Hernández-Baños et al. 1995), and especially the amount of species that are ‘data deficient.’ In Mexico, the endangered species list (NOM-Ecol-059 1994) follows those same criteria, and so many of the species recognised under the alternative concepts merit careful consideration for special conservation status. An evaluation of the conservation status of the each phylogenetic species in Mexico will be published elsewhere (Navarro & Peterson in prep.).

Although efficiency of assessment is important in identifying conservation priorities, our study indicates that biodiversity studies for conservation purposes make serious, silent assumptions when taxonomic authority lists are used uncritically. We suggest that such studies would best be carried out from an informed perspective regarding the taxonomy and systematics of the groups under study. Conservation planning may provide fertile soil for collaboration between members of the conservation community and systematists interested in important applications of biodiversity data.

We thank R. Holt, L. Krishtalka, T.N. Taylor, and R.O. Prum for helpful comments on drafts of the manuscript, as well as Robert M. Zink for his extreme patience. For access to scientific specimens, we thank the curators and staff of the Field Museum, Chicago; Louisiana State University Museum of Natural Science; Natural History Museum, University of Kansas; Museo de Zoología, Facultad de Ciencias, Universidad Nacional Autónoma de México (UNAM); American Museum of Natural History; Museum of Comparative Zoology, Harvard University; U. S. National Museum of Natural History; and the British Museum of Natural History. This work was supported by grants from the National Science Foundation, the British Council and the Comisión Nacional para el Uso y Conocimiento de la Biodiversidad (CONABIO).

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Table 1. Summary of levels of endemism at the level of all Mexico (Mexican endemism) and of single geographic regions (narrow endemism), under the biological species concept (BSC; taken from Escalante-Pliego et al. 1993) and under the phylogenetic species concept (PSC).