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Species As Units of Analysis in Ecology and Biogeography: Time to Take the Blinders Off

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Species As Units of Analysis in Ecology and Biogeography: Time to Take the Blinders Off Global Ecology and Biogeography (1999) 8, 433±441 ECOLOGICAL SOUNDING Species as units of analysis in ecology and biogeography: time to take the blinders off BRETT R. RIDDLE and DAVID J. HAFNER∗ Department of Biological Sciences, University of Nevada Las Vegas, 4505 Maryland Pk., Las Vegas, NV 89154±4004 U.S.A. E-mail: [email protected] ∗New Mexico Museum of Natural History, 1801 Mountain Road NW, Albuquerque, NM 87104 U.S.A. E-mail: [email protected] ABSTRACT when evidence clearly indicates that a formally recognized species either fails to convey important Species and their geographical distributions, evolutionary and geographical information (i.e. tabulated either from regional faunal and ¯oral includes multiple geographically distinct evolu- monographs or directly from natural history tionary lineages) or fails to delineate a natural collections, often are used as the basic units of entity (i.e. does not represent a monophyletic set of analysis by ecologists and biogeographers. It has been argued that in order for species to be populations). We demonstrate the limitations of operationally useful units for evolutionary and current species as evolutionary, geographical, and ecological studies, they need to be recognizable and conservation units within the ecologically well- identi®able as distinct entities. A growing body studied North American desert rodent assemblage. of molecular phylogeographic studies demonstrates We suggest that biotic surveys should be designed that currently recognized species often are unreliable to allow the efficient assembly and dissemination of in their approximation of fundamental evolutionary molecular phylogeographic data from ecologically and geographical units, leading, for example, to and biogeographically representative systems. proposed usage of molecular-based evolutionarily signi®cant units in lieu of species in conservation biology. We argue that ecologists and bio- Key words. Biogeography, conservation biology, geographers should likewise employ evolutionarily ecology, evolutionarily signi®cant units, macro- signi®cant units as basic units of analysis ecology, mammals, phylogeography, rodents. INTRODUCTION as`. .thestudyoftheprinciplesandprocessesgoverning the geographical distributions of genealogical lineages, Species are widely used as fundamental units of analysis including those at the intraspeci®c level' (Avise, 1994, in several areas of ecology and biogeography (Brown, p. 233). Conservation biologists have proposed calling 1995; Brown et al., 1996; Blackburn & Gaston, 1998). A such lineages evolutionarily signi®cant units (ESUs). pragmatic reason for doing so is that species historically While some controversy exists over the best recognition have attained a role as primary entities in palaeontology, criteria for delineating evolutionarily signi®cant units macroevolution, and conservation biology, thus (ESUs) (e.g. Moritz et al., 1995; Waples, 1995), Moritz providing a common currency between disciplines and colleagues have de®ned the phylogeographically (Brown, 1995). However, a rapidly increasing number based ESU as consisting of `. historically isolated sets of biogeographers have begun to utilize a different of populations for which a stringent and qualitative currency: the geographically discreet evolutionary criterion is reciprocal monophyly for mitochondrial lineages revealed through analysis of molecular data, DNA (mtDNA) combined with signi®cant divergence usually mitochondrial DNA (mtDNA) in animals. This in frequencies of nuclear alleles' (Moritz et al., 1995 discipline has been called phylogeography, and de®ned p. 249). 1999 Blackwell Science Ltd. http://www.blackwell-science.com/geb 433 434 B. R. Riddle & D. J. Hafner Our intention is to address three related issues, units of biological organization, and that the stemming from the remarkable growth in individuals and populations recognized as being phylogeographic surveys of geographical population conspeci®c be more closely related to each other than structure over recent years (Avise, 1998). First, we ask to other recognized species. The species of terrestrial whether recent ®ndings in phylogeography seriously vertebrates and many other well-studied groups meet challenge several assumptions underlying the use of these criteria.' Thus, terrestrial vertebrate species are currently recognized species as units of analysis in considered to represent appropriate units for ecology and biogeography. Second, we brie¯y address evolutionary, palaeontological, and ecological studies the kinds of questions that most likely could be (Brown, 1995; Blackburn & Gaston, 1998). This would compromised by using species as primary units if they be an acceptable perspective if, as is commonly believed, either subsume signi®cant phylogenetic and the most contentious issue regarding species- geographical structure, or are not natural entities. designations revolves around the particular species Third, we offer suggestions for efficient implementation concept being employed (e.g. biological, phylogenetic, of biotic surveys that would develop representative or congruence species concepts; reviewed in Avise, phylogeographic information for use by ecologists and 1994). A more insidious problem in using species as biogeographers. We recognize that a variety of units of analysis would arise if the kinds of characters questions in ecology and biogeography will not be and criteria historically used by systematists frequently affected appreciably by the issues we raise here (e.g. result in either overly coarse or inaccurate depictions tabulation of species within local community of taxonomic species as evolutionary lineages. Below, assemblages for purposes of investigating local patterns we contrast information content of species vs. ESUs and processes). Instead, we draw attention to areas of in a system that has been an ecological workhorse: the inquiry where distinct advantages should accrue from guild of North American desert rodents. using phylogeographically based ESUs. Speci®cally, we recommend that ecologists and biogeographers make North American desert rodents use of the most appropriate and informative phylogeographic information currently available by North American desert rodents make up one of the incorporating ESUs into species-level analysis. most intensively studied guilds of terrestrial vertebrates in the world and have been used as a paradigmatic system for testing hypotheses about ecological SPECIES AS UNITS OF ANALYSIS organization at population, community, and landscape scales (summarized by Reichman, 1991; Brown & As used in ecological and many biogeographic analyses, Harney, 1993). In a seminal study of community species and their geographical distributions are most composition, Brown & Kurzius (1987) compiled a large, often extracted either from available monographs (e.g. geographically representative data set on desert rodent Hall, 1981) or directly from natural history collections. species distribution and coexistence in 202 local We would not expect most practitioners in need of communities across four desert regions in North an operational unit for ecological and biogeographic America (Great Basin, Mojave, Sonoran, analysis to have insight into the reliability of species Chihuahuan). Their study produced the core data set tabulated in this way. Rather, they must rely on the used in a series of recent papers in which the North taxonomies generated by systematists. Ecologists American desert rodent guild has been contrasted with understand that recognition and delineation of species patterns of community assembly and organization in are not without error (Brown, 1995; FAUNMAP physically similar biomes across the globe (e.g. Morton working group, 1996). Nevertheless, in well-studied et al., 1994; Kelt et al., 1996). It has become customary groups (e.g. terrestrial vertebrates), currently in these studies to combine local assemblage presence/ recognized species are assumed to represent a absence data from large geographical areas into a single sufficiently accurate and robust depiction of natural regional species pool for subsequent intercontinental phylogenetic and geographical entities that subsequent comparisons. For example, Kelt et al., (1996) concluded revisions will result only in small changes in species- that the four major deserts in North America share a level taxonomy. As Brown, (1995, p. 27) states, `All that sufficiently large number of species to justify lumping is really necessary . is that species be operationally all data into a single North American desert region for identi®able, that they represent relatively comparable comparison with regional deserts on different 1999 Blackwell Science Ltd, Global Ecology and Biogeography, 8, 433±441 Species vs. ESUs in ecology and biogeography 435 continents. Implicit in this procedure are several in the pocket mice (Chaetodipus and Perognathus) and assumptions: (1) that individuals have been properly white-footed mice (Peromyscus). Often, ®eld identi®ed (`operationally identi®able'; criterion 1 of identi®cation in areas of sympatry is only an Brown, 1995; (2) that a species represents the same approximation, and reliable identi®cation must await evolutionary entity (ESU) in each desert region where detailed analysis of cranial and dental anatomy, bacular it occurs (criterion 2); and (3) that all populations of morphology, chromosomal complement, or molecular a species are more closely related to each other than sequence data. to populations within a different
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