Analysis of the conservation status of taxa in an area or country allows to link extinction risk with morphological, ecological and/or environmental variables. Studies focused on vertebrates have reported that several variables (e.g., body size) are positively associated with risk of extinction, ecological traits, phylogenetic and genetic features, and habitat degradation (Murray & Hose, 2005; Anderson et al., 2011). The loss of biodiversity of amphibians and reptiles has become an important global trend (Gibbons et al., 2000; IUCN, 2010). In this context, Corey & Waite (2008) suggest that threats to amphibians are concentrated in South and Central America, the Caribbean, and Australia. In addition, it has been suggested that some herpetozoan clades are especially prone to extinction by virtue of shared evolutionary histories (Lips et al., 2003; Case et al., 1998).

Body size among animals is directly related to physiological, morphological, ecological and evolutionary characteristics, as well as extinction risk. The relationship between body size and extinction risk recently has been a topic of interest to researchers because both variables are related to direct human influences (Fig. 4). As the body size of mammals increases so does the risk of extinction. However, similar studies of herpetozoa have not been conducted (Cardillo, 2003), nor have links between distribution, habitat conditions, and biological characteristics, such as body size. From our results, central Chile has a marked species concentration (Fig. 3). Biodiversity hotspots are biogeographic regions that are significant reservoirs of biodiversity and are threatened with destruction. Therefore, Chilean herpetozoa in this area are likely at increased extinction risk (Tribsch, 2004). Although the validity of this trend has been previously supported for herpetozoa, it has not yet been associated with other variables, such as body size, conservation status and extinction risk, as seen below.

Fig. 4. Synergic effect of some variables involved in extinction risk among the amphibians and reptiles of Chile.

Interestingly, the distribution of herpetofauna are in direct relationship with its environment dependence, which would explain the presence of these proposed herpetofaunal hotspots coinciding with areas of higher winter rainfall in the Chilean-Valdivian forests (Chile Central), the hotspot proposed by Myers et al. (2000), and other in northern Chile. Both areas have the highest herpetofaunal species richness, but also more human intervention and fewer national

Analysis of the conservation status of taxa in an area or country allows to link extinction risk with morphological, ecological and/or environmental variables. Studies focused on vertebrates have reported that several variables (e.g., body size) are positively associated with risk of extinction, ecological traits, phylogenetic and genetic features, and habitat degradation (Murray & Hose, 2005; Anderson et al., 2011). The loss of biodiversity of amphibians and reptiles has become an important global trend (Gibbons et al., 2000; IUCN, 2010). In this context, Corey & Waite (2008) suggest that threats to amphibians are concentrated in South and Central America, the Caribbean, and Australia. In addition, it has been suggested that some herpetozoan clades are especially prone to extinction by virtue of

Body size among animals is directly related to physiological, morphological, ecological and evolutionary characteristics, as well as extinction risk. The relationship between body size and extinction risk recently has been a topic of interest to researchers because both variables are related to direct human influences (Fig. 4). As the body size of mammals increases so does the risk of extinction. However, similar studies of herpetozoa have not been conducted (Cardillo, 2003), nor have links between distribution, habitat conditions, and biological characteristics, such as body size. From our results, central Chile has a marked species concentration (Fig. 3). Biodiversity hotspots are biogeographic regions that are significant reservoirs of biodiversity and are threatened with destruction. Therefore, Chilean herpetozoa in this area are likely at increased extinction risk (Tribsch, 2004). Although the validity of this trend has been previously supported for herpetozoa, it has not yet been associated with other variables, such

Fig. 4. Synergic effect of some variables involved in extinction risk among the amphibians

parks that protect these species (Vidal et al., 2009).

**4. Correlation between biological variables**

shared evolutionary histories (Lips et al., 2003; Case et al., 1998).

as body size, conservation status and extinction risk, as seen below.

and reptiles of Chile.

To evaluate extinction risk it is necessary to relate a species conservation status to variables realted to extinction. While Chilean herpetozoa are categorized at the species level as to conservation status, many taxa are categorized as Data Deficient (DD; IUCN, 2010). Here we consider species at risk of extinction, those species categorized as Critically Endangered (CE), Endangered (E) and Vulnerable (V), following categorizations for amphibians and reptiles as proposed by IUCN (2010), and Nuñez et al. (1997), respectively. In accordance to this are considered at risk only those species found within the categories mentioned above (EC, E, and V). By grouping them and observe their latitudinal distribution in which we can detect that Central Chile is an area with numerous species with elevated extinction risk. Of particular concern are reptiles in the north-central area from 25 ° to 44 ° S latitude, and amphibians in the south from 34 ° to 44 ° S latitude. This concentration of threatened and endangered species coincides with proposed biodiversity hotspot for herpetofauna in Chile (Fig. 3).

The scarcity of information on Chilean amphibians and reptiles prevents analysis of associative patterns: however, body size appears to be related of extinction risk for both classes (Meiri, 2008). In reptiles the risk of extinction increases with its frequency in quadrants, while in the case of amphibians restricted distribution is related to extinction risk (Fig. 5). These patterns appear related to human impacts on both classes because reptiles are

Fig. 5. Map of Chile showing herpetozoa taxa in relation to their extinction risk for each degree of latitude.

Biogeography of Chilean Herpetofauna: Biodiversity Hotspot and Extinction Risk 147

Body size also may be correlated with other life-history or ecological traits that influence vulnerability, such as reproductive output, mobility, energy requirements or population density. Cardillo (2003) considered the additive impacts of environmental change on extinction risk. For example, the collapse of Pleistocene megafauna was exacerbated by

Fig. 6. Relationship between number of quadrants, snout-vent length (SVL) and extinction

Behavioural, morphological, and physiological characteristics appear to make some species more susceptible than others to extinction. In general, large-sized species with restricted distributions and habitat specialization tend to be at greater risk of anthropogenic extinction than are others within their respective taxa (Sodhi et al., 2009). Our data support the findings of Cardillo (2003), who found that body size, distribution and ecological specialization increase

Many studies suggest that larger bodied species are more susceptible to extinction than are smaller species (Cardillo & Bromham, 2001), while Murray & Hose (2005) reported no relationship. Our results show weak effect of body size on extinction risk in herpetozoans, although we note that snout–vent length was a predictor in the extinction risk (Figs. 5 and 6)

the risk of anthropogenic extinction, especially in situations with rapid habitat loss.

risk for Amphibians and Reptiles from Chile.

**5. Critical body size for conservation**

environmental change, including deforestation (Sodhi et al., 2008).

generally easier to observe and enjoy have greater interest on the part of man, whether due to aversive fear and beliefs, beauty (by virtue of colour, morphology, or as pets.) Furthermore, among amphibians the risk increases as frequency decreases, relating biological patterns and habitat dependence. It is intuitively obvious that the risk of extinction is greater for populations consisting of a few individuals than for those having many, but it also may be greater for populations undergoing greater flux than those with low temporal variability (Pimm et al., 1988).

Recent studies indicate that modern extinctions and declines of species have been phylogenetically selective (Cardillo, 2003). Thus, the habitat loss together the intrinsic traits some species make them particularly extinction-prone (Figure 4). Also, smaller-bodied species seem to be less vulnerable to decline and extinction than larger species (Gaston & Blackburn, 1995; Cardillo & Bromham, 2001). Furthermore, there may be tradeoffs between different traits; for example, smaller species may have an advantage in higher reproductive output and higher population densities, but larger species may have an advantage in greater mobility and energetic efficiency (Bielby, 2008; Sodhi et al., 2008). Nonetheless, larger vertebrates have a higher risk of extinction, and the explanation appears to be an inverse relationship between population size versus body size (Cardillo & Bromhman, 2001). In addition, the bigger the species the more vulnerable it may be to human persecution and hunting, while smaller species are generally more vulnerable to habitat loss due to anthropic activity (Cardillo, 2003; Sodhi et al., 2008). Similarly it has been established that smaller size confers greater protection.

We tested these extinction risk concepts using our Chilean herpetofaunal data. Among Chilean amphibians, the most important factor in risk is distribution (Figure 6, r Spearman = -0.52; P<0.001). For this class, size does not affect risk as much as habitat dependence; therefore, it appears that species with more limited ranges have the greatest risk of extinction. In contrast, body size among reptiles exacerbate extinction risk (Figure 6, r Spearman = 0.29; P<0.05), with many explanatory reasons. Thus, it is possible that body size directly determines a species' vulnerability: smaller species may, for instance, be less likely targets for human hunters, or less common prey items for invasive predators (Cardillo & Bromham, 2001). For example, *Calyptocephalella gayi* (Chilean Big frog) is the largest amphibian species in the country and is consumed due to their body size and good flavor of the meat. The species is broadly used for human consumption and an increase in the level of wild harvest has occurred since approximately 2000. The United States has been a significant commercial importer of wild-caught specimens of this species. From 2003 to 2007, 10,861 wild specimens were exported to the United States and were all traded for commercial purposes (Defenders of Wildlife, 2008). In the case of reptiles, *Callopistes maculatus* (Iguana Chilena) is the largest terrestrial reptile species and is negatively affected by traffic and trade (Auliya, 2003). According to Fitzgerald & Ortiz (1994), *C. maculatus* is "in danger" throughout its range due to habitat destruction, and in recent years by increasing harvest to meet international demand. During the years 1981-1991 this species sustained significant population loss from harvest, with the export of at least 2,400 live specimens (JNCC, 1993), which were sold as pets or used for the removal of skin (Díaz-Páez et al., 2008). Both of these large bodied species remain vulnerable to extinction due to harvest pressure.

generally easier to observe and enjoy have greater interest on the part of man, whether due to aversive fear and beliefs, beauty (by virtue of colour, morphology, or as pets.) Furthermore, among amphibians the risk increases as frequency decreases, relating biological patterns and habitat dependence. It is intuitively obvious that the risk of extinction is greater for populations consisting of a few individuals than for those having many, but it also may be greater for populations undergoing greater flux than those with

Recent studies indicate that modern extinctions and declines of species have been phylogenetically selective (Cardillo, 2003). Thus, the habitat loss together the intrinsic traits some species make them particularly extinction-prone (Figure 4). Also, smaller-bodied species seem to be less vulnerable to decline and extinction than larger species (Gaston & Blackburn, 1995; Cardillo & Bromham, 2001). Furthermore, there may be tradeoffs between different traits; for example, smaller species may have an advantage in higher reproductive output and higher population densities, but larger species may have an advantage in greater mobility and energetic efficiency (Bielby, 2008; Sodhi et al., 2008). Nonetheless, larger vertebrates have a higher risk of extinction, and the explanation appears to be an inverse relationship between population size versus body size (Cardillo & Bromhman, 2001). In addition, the bigger the species the more vulnerable it may be to human persecution and hunting, while smaller species are generally more vulnerable to habitat loss due to anthropic activity (Cardillo, 2003; Sodhi et al., 2008). Similarly it has been established that smaller size

We tested these extinction risk concepts using our Chilean herpetofaunal data. Among Chilean amphibians, the most important factor in risk is distribution (Figure 6, r Spearman = -0.52; P<0.001). For this class, size does not affect risk as much as habitat dependence; therefore, it appears that species with more limited ranges have the greatest risk of extinction. In contrast, body size among reptiles exacerbate extinction risk (Figure 6, r Spearman = 0.29; P<0.05), with many explanatory reasons. Thus, it is possible that body size directly determines a species' vulnerability: smaller species may, for instance, be less likely targets for human hunters, or less common prey items for invasive predators (Cardillo & Bromham, 2001). For example, *Calyptocephalella gayi* (Chilean Big frog) is the largest amphibian species in the country and is consumed due to their body size and good flavor of the meat. The species is broadly used for human consumption and an increase in the level of wild harvest has occurred since approximately 2000. The United States has been a significant commercial importer of wild-caught specimens of this species. From 2003 to 2007, 10,861 wild specimens were exported to the United States and were all traded for commercial purposes (Defenders of Wildlife, 2008). In the case of reptiles, *Callopistes maculatus* (Iguana Chilena) is the largest terrestrial reptile species and is negatively affected by traffic and trade (Auliya, 2003). According to Fitzgerald & Ortiz (1994), *C. maculatus* is "in danger" throughout its range due to habitat destruction, and in recent years by increasing harvest to meet international demand. During the years 1981-1991 this species sustained significant population loss from harvest, with the export of at least 2,400 live specimens (JNCC, 1993), which were sold as pets or used for the removal of skin (Díaz-Páez et al., 2008). Both of these large bodied species remain vulnerable to extinction due to harvest

low temporal variability (Pimm et al., 1988).

confers greater protection.

pressure.

Body size also may be correlated with other life-history or ecological traits that influence vulnerability, such as reproductive output, mobility, energy requirements or population density. Cardillo (2003) considered the additive impacts of environmental change on extinction risk. For example, the collapse of Pleistocene megafauna was exacerbated by environmental change, including deforestation (Sodhi et al., 2008).

Fig. 6. Relationship between number of quadrants, snout-vent length (SVL) and extinction risk for Amphibians and Reptiles from Chile.

Behavioural, morphological, and physiological characteristics appear to make some species more susceptible than others to extinction. In general, large-sized species with restricted distributions and habitat specialization tend to be at greater risk of anthropogenic extinction than are others within their respective taxa (Sodhi et al., 2009). Our data support the findings of Cardillo (2003), who found that body size, distribution and ecological specialization increase the risk of anthropogenic extinction, especially in situations with rapid habitat loss.

#### **5. Critical body size for conservation**

Many studies suggest that larger bodied species are more susceptible to extinction than are smaller species (Cardillo & Bromham, 2001), while Murray & Hose (2005) reported no relationship. Our results show weak effect of body size on extinction risk in herpetozoans, although we note that snout–vent length was a predictor in the extinction risk (Figs. 5 and 6)

Biogeography of Chilean Herpetofauna: Biodiversity Hotspot and Extinction Risk 149

isolation (Armesto et al., 1995). This history of isolation has contributed to the uniqueness of Chilean herpetofaunal assemblage, with many endemic taxa (Arroyo et al., 1999; (Veloso et al., 1995). In Chile, amphibians and reptiles have the highest level of endemism of any

Different evolutionary processes are involved in anthropogenic extinction risk among the Chilean herpetofauna. Smaller species may have lower energy requirements and larger population sizes, making them more resilient to human disturbances. The higher reproductive potential of smaller species may reduce population recovery time following disturbance (Gaston & Blackburn, 1995). In contrast, larger species have lower reproductive rates and higher net energetic demands, requiring larger home ranges. We report a positive association between body size and extinction risk among reptiles. Larger species are affected more by harvest (Cardillo & Bromhan, 2001) and by habitat alteration, including the introduction of non-native species, as is happening in Chile today. Overall, we conclude that life-history traits influence extinction risk, with smaller-bodied amphibians affected by environmental changes, and larger bodied reptiles affected by harvest and habitat loss.

The authors were financed by CONICYT 79090026 and DIUC Project 210.412.045-1sp. We thank to Chilean Herpetological Network (RECH) for encouraging this work. We also thank the Department of Basic Sciences at the Universidad del Bío-Bío, and the Department of Basic Sciences at the Universidad de Concepcion for partial financial support of this study.

Anderson SC, RG Farmer, F Ferretti, AM Houde & JA Hutchings (2011). Correlates of

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**7. Acknowledgment**

**8. References**

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based on IUCN status. There appear to be critical body size ranges in both classes: amphibians with small body sizes have a higher threat status, while increased body size in reptiles increases extinction risk. Similar analyses of Regional patterns from Australia and Central America corroborate our findings (Hero et al., 2005; Lips et al., 2003).

Fig. 7. Body sizes frequency distribution of Chilean herpetofauna, with status conservation according to IUCN (2010) for amphibians and Nuñez et al. (1997) for reptiles.

We used a combination of morphological and distribution data to elucidate extinction risk in Chile, finding that body size influenced extinction risk in opposite ways for the two classes (Fig. 7). Differences between our results and those of other analogous studies likely reflect different biogeographic realms (e.g., Australia Hero et al. 2005, Murray & Hose 2005, Williams & Hero 1998; or Central America Lips et al., 2003). Additionally, the biological traits underlying increased extinction risk/decline can and often do vary according to the particular threat involved, the environment of the location of study, and the species involved (Owens & Bennett, 2000). Our analyses explore the generalities that exist despite these differences, but will miss some of the specific regional correlates.

#### **6. Conclusions**

We present the first dynamic synthesis of the biogeographic variables affecting Chilean herpetozoa. Inadequate basic information has impeded or delayed studies in the Andean realm. Biogeographical knowledge plays a fundamental role in conservation because the relationship between geographic distribution and extinction risk can reveal new conservation issues and strategies. The herpetofauna of Chile has a lower richness relative to tropical and subtropical South America (Duellman, 1979) due to its prolonged geographical isolation (Armesto et al., 1995). This history of isolation has contributed to the uniqueness of Chilean herpetofaunal assemblage, with many endemic taxa (Arroyo et al., 1999; (Veloso et al., 1995). In Chile, amphibians and reptiles have the highest level of endemism of any vertebrate class, and endemism is focused in the hotspot in central Chile.

Different evolutionary processes are involved in anthropogenic extinction risk among the Chilean herpetofauna. Smaller species may have lower energy requirements and larger population sizes, making them more resilient to human disturbances. The higher reproductive potential of smaller species may reduce population recovery time following disturbance (Gaston & Blackburn, 1995). In contrast, larger species have lower reproductive rates and higher net energetic demands, requiring larger home ranges. We report a positive association between body size and extinction risk among reptiles. Larger species are affected more by harvest (Cardillo & Bromhan, 2001) and by habitat alteration, including the introduction of non-native species, as is happening in Chile today. Overall, we conclude that life-history traits influence extinction risk, with smaller-bodied amphibians affected by environmental changes, and larger bodied reptiles affected by harvest and habitat loss.

#### **7. Acknowledgment**

148 Global Advances in Biogeography

based on IUCN status. There appear to be critical body size ranges in both classes: amphibians with small body sizes have a higher threat status, while increased body size in reptiles increases extinction risk. Similar analyses of Regional patterns from Australia and

Fig. 7. Body sizes frequency distribution of Chilean herpetofauna, with status conservation

We used a combination of morphological and distribution data to elucidate extinction risk in Chile, finding that body size influenced extinction risk in opposite ways for the two classes (Fig. 7). Differences between our results and those of other analogous studies likely reflect different biogeographic realms (e.g., Australia Hero et al. 2005, Murray & Hose 2005, Williams & Hero 1998; or Central America Lips et al., 2003). Additionally, the biological traits underlying increased extinction risk/decline can and often do vary according to the particular threat involved, the environment of the location of study, and the species involved (Owens & Bennett, 2000). Our analyses explore the generalities that exist despite

We present the first dynamic synthesis of the biogeographic variables affecting Chilean herpetozoa. Inadequate basic information has impeded or delayed studies in the Andean realm. Biogeographical knowledge plays a fundamental role in conservation because the relationship between geographic distribution and extinction risk can reveal new conservation issues and strategies. The herpetofauna of Chile has a lower richness relative to tropical and subtropical South America (Duellman, 1979) due to its prolonged geographical

according to IUCN (2010) for amphibians and Nuñez et al. (1997) for reptiles.

these differences, but will miss some of the specific regional correlates.

**6. Conclusions**

Central America corroborate our findings (Hero et al., 2005; Lips et al., 2003).

The authors were financed by CONICYT 79090026 and DIUC Project 210.412.045-1sp. We thank to Chilean Herpetological Network (RECH) for encouraging this work. We also thank the Department of Basic Sciences at the Universidad del Bío-Bío, and the Department of Basic Sciences at the Universidad de Concepcion for partial financial support of this study.

#### **8. References**

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**9**

*México*

**Contributions**

**of Cladistic Biogeography**

 **to the Mexican Transition Zone**

Isolda Luna-Vega1,\* and Raúl Contreras-Medina2

*1Laboratorio de Biogeografía y Sistemática, Departamento de Biología Evolutiva, Facultad de Ciencias, Universidad Nacional Autónoma de México (UNAM), 2Escuela de Ciencias, Universidad Autónoma "Benito Juárez" de Oaxaca (UABJO),*

The Mexican Transition Zone (MTZ) was defined by Halffter (1987) as the complex area where Neotropical and Nearctic biotic elements overlap, including the southern United States, Mexico and adjacent areas of Central America. The biota of this area has received the attention of several naturalists since the mid 19th century (e.g. Sclater, 1858) due to its placement between the Nearctic and Neotropical regions and its "hybrid" character (Morrone, 2005 and references therein), associated with high biotic diversity and a high degree of endemism of plant and animal taxa. This area also has received attention in conservation and biodiversity plans at a worldwide level, because its central portion, the Mesoamerican hotspot, was considered one of the main biodiversity hotspots recognized in the world (Flores-Villela & Gerez, 1994; Luna-Vega and Contreras-Medina, 2010;

Recently, authors have proposed hypotheses to explain disjunct biotic patterns observed in the MTZ from different approaches and methodologies, such as panbiogeography (Álvarez & Morrone, 2004; Contreras-Medina & Eliosa-León, 2001; Escalante et al., 2004; Morrone & Márquez, 2001; Morrone & Gutiérrez, 2005), parsimony analysis of endemicity (Aguilar-Aguilar et al., 2003; Espinosa et al., 2000; Luna-Vega et al., 2001; Morrone et al., 1999; Morrone & Escalante, 2002), and cladistic biogeography (Contreras-Medina et al., 2007; Espinosa et al., 2006; Flores-Villela & Goyenechea, 2001; Liebherr, 1991; Marshall & Liebherr, 2000; Rosen, 1978). The latest studies based on cladistic biogeography approaches represent

Our goal here is to compare and discuss the different contributions made to the biogeography of the Mexican Transition Zone by applying different cladistic biogeographical methods. It is also to contrast the different areas of endemism proposed in these studies with the objective of obtaining consensus on areas of endemism to be

**1. Introduction**

Mittermeier et al., 1998; Myers et al., 2000).

the basis of this chapter.

considered in future research.

Corresponding Author

 \*

### **Contributions of Cladistic Biogeography to the Mexican Transition Zone**

Isolda Luna-Vega1,\* and Raúl Contreras-Medina2 *1Laboratorio de Biogeografía y Sistemática, Departamento de Biología Evolutiva, Facultad de Ciencias, Universidad Nacional Autónoma de México (UNAM), 2Escuela de Ciencias, Universidad Autónoma "Benito Juárez" de Oaxaca (UABJO), México*

#### **1. Introduction**

The Mexican Transition Zone (MTZ) was defined by Halffter (1987) as the complex area where Neotropical and Nearctic biotic elements overlap, including the southern United States, Mexico and adjacent areas of Central America. The biota of this area has received the attention of several naturalists since the mid 19th century (e.g. Sclater, 1858) due to its placement between the Nearctic and Neotropical regions and its "hybrid" character (Morrone, 2005 and references therein), associated with high biotic diversity and a high degree of endemism of plant and animal taxa. This area also has received attention in conservation and biodiversity plans at a worldwide level, because its central portion, the Mesoamerican hotspot, was considered one of the main biodiversity hotspots recognized in the world (Flores-Villela & Gerez, 1994; Luna-Vega and Contreras-Medina, 2010; Mittermeier et al., 1998; Myers et al., 2000).

Recently, authors have proposed hypotheses to explain disjunct biotic patterns observed in the MTZ from different approaches and methodologies, such as panbiogeography (Álvarez & Morrone, 2004; Contreras-Medina & Eliosa-León, 2001; Escalante et al., 2004; Morrone & Márquez, 2001; Morrone & Gutiérrez, 2005), parsimony analysis of endemicity (Aguilar-Aguilar et al., 2003; Espinosa et al., 2000; Luna-Vega et al., 2001; Morrone et al., 1999; Morrone & Escalante, 2002), and cladistic biogeography (Contreras-Medina et al., 2007; Espinosa et al., 2006; Flores-Villela & Goyenechea, 2001; Liebherr, 1991; Marshall & Liebherr, 2000; Rosen, 1978). The latest studies based on cladistic biogeography approaches represent the basis of this chapter.

Our goal here is to compare and discuss the different contributions made to the biogeography of the Mexican Transition Zone by applying different cladistic biogeographical methods. It is also to contrast the different areas of endemism proposed in these studies with the objective of obtaining consensus on areas of endemism to be considered in future research.

<sup>\*</sup> Corresponding Author

Contributions of Cladistic Biogeography to the Mexican Transition Zone 159

obtained, these are represented in a component or a three-item matrix and analyzed with a parsimony algorithm (Crisci et al., 2000). A parsimony analysis of these paralogy-free subtrees (PAPS) may thus be used to generate a more robust hypothesis, because geographic paralogy has been removed. Another frequent method that has been cited in biogeographic literature is component analysis (Nelson & Platnick, 1981), but unfortunately this method

Fig. 1. The 19 biogeographic provinces of Mexico according to Arriaga et al. (1997). Abbreviations are: APN = Altiplano Norte, APS = Altiplano Sur, BAL = Depresión del Balsas, BC = Baja California, CLF = California, CAB = Del Cabo, CHI = Los Altos de Chiapas, GM = Golfo de México, NUS = Soconusco, OAX = Oaxaca, PAC = Costa del Pacífico, PTN = Petén, SME = Sierra Madre Oriental, SMO = Sierra Madre Occidental, SMS = Sierra Madre del Sur, SON = Sonorense, TAM = Tamaulipeca, VOL = Eje Volcánico,

YUC = Yucatán. The provinces of Central America from Morrone (2001) are:

Panamá, and TAL = Sierra de Talamanca.

CHI= Los Altos de Chiapas, ECA= Eastern Central America, WIP= Western Isthmus of

has not been applied to the biota of the MTZ.

#### **2. Cladistic biogeography: Basis and methods**

Cladistic biogeography is an approach to historical biogeography that searches for patterns of relationships among areas of endemism based on the phylogenetic relationships of the taxa inhabiting them (Crisci et al., 2000; Humphries & Parenti, 1999; Morrone & Crisci, 1995). This approach emerged as a combination of principles of phylogenetic systematics of Willi Hennig (1966) and the biogeographic ideas formulated by Léon Croizat (1958, 1964) represented in his book Panbiogeography (Contreras-Medina, 2006; Craw, 1988; Crisci et al., 2000; Espinosa & Llorente, 1993; Flores-Villela & Goyenechea, 2001). Cladistic biogeography is based on a close relationship among systematics and biogeography, considering that taxonomic cladograms converted into area cladograms can elucidate the fragmentation sequence of studied areas. With this procedure, it is possible to propose hypotheses on historical relationships among areas of endemism (Contreras-Medina, 2006; Morrone, 1997). Cladistic biogeographic analysis essentially looks for congruent patterns among area cladograms of different taxa (Humphries & Parenti, 1999; Page & Lydeard, 1994) showed in a general area cladogram, which represents the final result of this kind of analysis (Contreras-Medina, 2006; Morrone, 1997). Interpretation of cladistic biogeographical results usually focuses on vicariance rather than on dispersal events, because vicariance affects different groups of organisms simultaneously (Morrone & Crisci, 1995; Nelson & Platnick, 1981).

The construction of area cladograms is simple when each taxon is endemic to a single area and each area has only one taxon (Morrone, 1997). Incongruence can occur between two or more area cladograms due to three main reasons, known as redundant distributions, widespread taxa and missing areas (Morrone et al., 1996). Redundant distributions occur when an area appears more than once in an area cladogram, because two or more terminal taxa are distributed in this area; widespread taxa occur when any of the terminal taxa inhabits two or more of the areas analyzed; missing areas occur when there is not a terminal taxon distributed in one of the areas analyzed, therefore this area is not represented in the area cladograms (Morrone, 2009). One or more of the methods that have been proposed in cladistic biogeography are then applied to these area cladograms, and the final result is a general area cladogram (Morrone, 1997).

The first method developed in cladistic biogeography was the reduced consensus cladogram proposed by Rosen (1978), which was only used by him. Another method proposed was the Brooks parsimony analysis or BPA (Brooks, 1990; Kluge, 1988), which has been extensively used in studies developed in the MTZ (Contreras-Medina et al., 2007; Espinosa et al., 2006; Marshall & Liebherr, 2000). BPA has been criticized by some authors as a suboptimal method, because it uses both dispersal and vicariance explanations to fit taxa and areas to the same tree (e.g. Siddall & Perkins, 2003); however, other authors (e.g. Brooks et al., 2001; Van Veller & Brooks, 2001) have defended it as a valid method. Nelson & Ladiges (1996) noted that when nodes and areas are associated in order to be included in a data matrix, geographic paralogy may result because of duplication or overlap in the distribution of taxa related by paralogous nodes. To this end, another method was proposed, known as paralogy-free subtrees (Nelson & Ladiges, 1995). This method consists in the reduction of complex cladograms to paralogy-free-subtrees, that means that geographic data are associated only with the informative nodes, and areas duplicated or redundant in the descendants of each node do not exist (Morrone, 2009). Once that paralogy-free-subtrees are

Cladistic biogeography is an approach to historical biogeography that searches for patterns of relationships among areas of endemism based on the phylogenetic relationships of the taxa inhabiting them (Crisci et al., 2000; Humphries & Parenti, 1999; Morrone & Crisci, 1995). This approach emerged as a combination of principles of phylogenetic systematics of Willi Hennig (1966) and the biogeographic ideas formulated by Léon Croizat (1958, 1964) represented in his book Panbiogeography (Contreras-Medina, 2006; Craw, 1988; Crisci et al., 2000; Espinosa & Llorente, 1993; Flores-Villela & Goyenechea, 2001). Cladistic biogeography is based on a close relationship among systematics and biogeography, considering that taxonomic cladograms converted into area cladograms can elucidate the fragmentation sequence of studied areas. With this procedure, it is possible to propose hypotheses on historical relationships among areas of endemism (Contreras-Medina, 2006; Morrone, 1997). Cladistic biogeographic analysis essentially looks for congruent patterns among area cladograms of different taxa (Humphries & Parenti, 1999; Page & Lydeard, 1994) showed in a general area cladogram, which represents the final result of this kind of analysis (Contreras-Medina, 2006; Morrone, 1997). Interpretation of cladistic biogeographical results usually focuses on vicariance rather than on dispersal events, because vicariance affects different groups of organisms simultaneously (Morrone & Crisci, 1995; Nelson & Platnick,

The construction of area cladograms is simple when each taxon is endemic to a single area and each area has only one taxon (Morrone, 1997). Incongruence can occur between two or more area cladograms due to three main reasons, known as redundant distributions, widespread taxa and missing areas (Morrone et al., 1996). Redundant distributions occur when an area appears more than once in an area cladogram, because two or more terminal taxa are distributed in this area; widespread taxa occur when any of the terminal taxa inhabits two or more of the areas analyzed; missing areas occur when there is not a terminal taxon distributed in one of the areas analyzed, therefore this area is not represented in the area cladograms (Morrone, 2009). One or more of the methods that have been proposed in cladistic biogeography are then applied to these area cladograms, and the final result is a

The first method developed in cladistic biogeography was the reduced consensus cladogram proposed by Rosen (1978), which was only used by him. Another method proposed was the Brooks parsimony analysis or BPA (Brooks, 1990; Kluge, 1988), which has been extensively used in studies developed in the MTZ (Contreras-Medina et al., 2007; Espinosa et al., 2006; Marshall & Liebherr, 2000). BPA has been criticized by some authors as a suboptimal method, because it uses both dispersal and vicariance explanations to fit taxa and areas to the same tree (e.g. Siddall & Perkins, 2003); however, other authors (e.g. Brooks et al., 2001; Van Veller & Brooks, 2001) have defended it as a valid method. Nelson & Ladiges (1996) noted that when nodes and areas are associated in order to be included in a data matrix, geographic paralogy may result because of duplication or overlap in the distribution of taxa related by paralogous nodes. To this end, another method was proposed, known as paralogy-free subtrees (Nelson & Ladiges, 1995). This method consists in the reduction of complex cladograms to paralogy-free-subtrees, that means that geographic data are associated only with the informative nodes, and areas duplicated or redundant in the descendants of each node do not exist (Morrone, 2009). Once that paralogy-free-subtrees are

**2. Cladistic biogeography: Basis and methods**

1981).

general area cladogram (Morrone, 1997).

obtained, these are represented in a component or a three-item matrix and analyzed with a parsimony algorithm (Crisci et al., 2000). A parsimony analysis of these paralogy-free subtrees (PAPS) may thus be used to generate a more robust hypothesis, because geographic paralogy has been removed. Another frequent method that has been cited in biogeographic literature is component analysis (Nelson & Platnick, 1981), but unfortunately this method has not been applied to the biota of the MTZ.

Fig. 1. The 19 biogeographic provinces of Mexico according to Arriaga et al. (1997). Abbreviations are: APN = Altiplano Norte, APS = Altiplano Sur, BAL = Depresión del Balsas, BC = Baja California, CLF = California, CAB = Del Cabo, CHI = Los Altos de Chiapas, GM = Golfo de México, NUS = Soconusco, OAX = Oaxaca, PAC = Costa del Pacífico, PTN = Petén, SME = Sierra Madre Oriental, SMO = Sierra Madre Occidental, SMS = Sierra Madre del Sur, SON = Sonorense, TAM = Tamaulipeca, VOL = Eje Volcánico, YUC = Yucatán. The provinces of Central America from Morrone (2001) are: CHI= Los Altos de Chiapas, ECA= Eastern Central America, WIP= Western Isthmus of Panamá, and TAL = Sierra de Talamanca.

Contributions of Cladistic Biogeography to the Mexican Transition Zone 161

Flores-Villela & Goyenechea (2001)

Sierra Madre Occidental

Chihuahuan Desert

Chihuahuan Desert

Semiarid lands of Tamaulipas

Sierra Madre Oriental

Transvolcanic Axis of Central

Mexico

Tehuantepec Sierra Madre del Sur

Cuicatlán Valley

Coahuayana and Tehuantepec

NUS Soconusco

Armería-

GM Costa del Golfo de

Depression

Transvolcanic Axis of Central

Pacific lowlands of Mexico plus

Mexico

Balsas Depression Contreras-Medina et al. (2007)

del Noroeste

Sierra Madre Occidental

Altiplano

Altiplano

Planicie Costera del Noreste

Sierra Madre Oriental

Serranías Meridionales

Balsas Basin

Serranías Meridionales

Tehuacán-Cuicatlán Valley

México

Costa Pacífica

Espinosa et al.

CLF Californian BC Baja California CAB El Cabo Baja California SON Sonoran Desert Sonora Sonoran Desert Planicie Costera

(2006)

Biogeographic provinces

Marshall & Liebherr (2000)

Occidental plus Central Plateau

Occidental plus Central Plateau

Occidental plus Central Plateau

Occidental plus Central Plateau

Transvolcánica

BAL W and E Balsas Balsas

SMO Sierra Madre

APN Sierra Madre

APS Sierra Madre

TAM Sierra Madre

SME Sierra Madre

SMS Sierra Madre

VOL Sierra

Oriental

del Sur

OAX Tehuacán-

PAC Tuito, Papagayo,

#### **3. Areas of endemism in the Mexican Transition Zone**

Areas of endemism are defined by the overlapped distributions of endemic taxa (Contreras-Medina, 2006; Morrone, 1994). These kinds of areas represent the basic units in cladistic biogeography (Contreras-Medina et al., 2001); for this reason, the recognition and delimitation of areas of endemism represent a prerequisite to carry out cladistic biogeographic studies (Morrone, 1997).

Some proposals on regionalization of the Mexican Transition Zone have been suggested based on different criteria. One of the most supported schemes was that proposed by the Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO) (National Commission for the Knowledge and Use of Biodiversity, Mexico), which represents the effort of a set of several specialists on geology, vascular plants, reptiles and mammals working together to provide different proposals on regionalization of the Mexican territory with different points of view. Nineteen Mexican biogeographic provinces were recognized through this workshop (Arriaga et al., 1997). An important regionalization proposal for Central America also was made by Morrone (2001). This scheme was also followed in this study, and was also used to compare the areas of endemism found in the different revised studies on cladistic biogeography of the Mexican Transition Zone.

In the study of Espinosa et al. (2006), the parsimony analysis of endemicity (PAE) method (Rosen, 1988) was used in order to generate the 23 areas of endemism that were used later in the cladistic biogeography section of this paper. The areas of endemism were obtained by merging those areas supported by endemic (synapomorphic) species from PAE following the proposed provinces of Morrone (1994).

In many cases, the Mexican mountain ranges coincide with the areas of endemism (Fig. 2), so their recognition and delimitation represent necessary tools in future cladistic biogeographic studies. The origin and development of these mountain chains have strongly

Fig. 2. The main Mexican mountain chains.

Areas of endemism are defined by the overlapped distributions of endemic taxa (Contreras-Medina, 2006; Morrone, 1994). These kinds of areas represent the basic units in cladistic biogeography (Contreras-Medina et al., 2001); for this reason, the recognition and delimitation of areas of endemism represent a prerequisite to carry out cladistic

Some proposals on regionalization of the Mexican Transition Zone have been suggested based on different criteria. One of the most supported schemes was that proposed by the Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO) (National Commission for the Knowledge and Use of Biodiversity, Mexico), which represents the effort of a set of several specialists on geology, vascular plants, reptiles and mammals working together to provide different proposals on regionalization of the Mexican territory with different points of view. Nineteen Mexican biogeographic provinces were recognized through this workshop (Arriaga et al., 1997). An important regionalization proposal for Central America also was made by Morrone (2001). This scheme was also followed in this study, and was also used to compare the areas of endemism found in the different revised

In the study of Espinosa et al. (2006), the parsimony analysis of endemicity (PAE) method (Rosen, 1988) was used in order to generate the 23 areas of endemism that were used later in the cladistic biogeography section of this paper. The areas of endemism were obtained by merging those areas supported by endemic (synapomorphic) species from PAE following

In many cases, the Mexican mountain ranges coincide with the areas of endemism (Fig. 2), so their recognition and delimitation represent necessary tools in future cladistic biogeographic studies. The origin and development of these mountain chains have strongly

**3. Areas of endemism in the Mexican Transition Zone**

studies on cladistic biogeography of the Mexican Transition Zone.

biogeographic studies (Morrone, 1997).

the proposed provinces of Morrone (1994).

Fig. 2. The main Mexican mountain chains.

Contributions of Cladistic Biogeography to the Mexican Transition Zone 163

including small parts of the MTZ - these areas were mainly in Chiapas, eastern Central

Rosen (1978) was the first to apply a cladistic biogeography approach to the MTZ. In his biogeographic research, the author included the phylogenies of two fresh water fish of the genera *Heterandria* and *Xiphophorus*. Rosen (1978) recognized three coincidences of historical relationships, indicating the existence of a common ancestral distributional area that had been fragmented twice and that currently constitutes the basins of the Bravo River (in northern Mexico), the Pánuco River (in northeastern Mexico), and the Grijalva River (on the

Another pioneering cladistic biogeographic study in the MTZ is that of Liebherr (1991). This author analyzed the history the mountain biota based on the phylogenies of two Coleoptera genera (*Elliptoleus* and *Calathus*). The complexity of the geologic history of southern Mexico is noted in the general area cladogram obtained, showing an ancient primary fragmentation that separated extra-tropical from tropical biota. Liebherr (1991) obtained a first clade that was divided in two subgroups, the first formed by the Sierra Madre Oriental and the second by the Sierra Madre Occidental and part of the Mexican Plateau. The tropical clade included the southern portions of the Sierra Madre Occidental, Sierra Madre Oriental and other Mexican

Marshall & Liebherr (2000) published a cladistic biogeography study applying BPA and Assumption 0 methods based on 33 taxa (beetles, reptiles, fish and one plant genus) and using nine areas of endemism; they obtained four general area cladograms, one with BPA and three with Assumption 0. The congruence among these cladograms is shown in the relationships among the Arizona Mountains plus the Sierra Madre Occidental in one clade, and the Sierra Madre del Sur plus the Trans-Mexican Volcanic Belt related with the Chiapan-Guatemalan Highlands in another clade. Unfortunately, their approach included methodological confusion regarding the Assumption 0: the missing taxa option (or missing areas) in the matrix is treated by them as '0', indicating the lack of information regarding a taxon's occurrence. However, the Assumption 0 approach considers missing areas to be uninformative, as well as the other two assumptions (1 and 2) in a component analysis method (Morrone, 1998), so missing areas are located in all possible positions in the resolved area cladograms. Assumption 0 in BPA implies that areas inhabited by a widespread taxon

Flores-Villela & Goyenechea (2001) used 10 animal taxa in their biogeographical study (beetles, lizards, snakes and frogs) distributed in 13 areas of endemism; the method of reconciled trees implementing assumptions 0, 1, and 2 was applied in this study. The authors obtained six general area cladograms, but they did not achieve a consistent pattern of relationships among these cladograms. They concluded that each cladogram could only explain portions of the geographic history of the taxa studied, and that the results obtained

Espinosa et al. (2006) generated hypotheses on the historical biogeography of tropical Mexico using the flowering plant genus *Bursera*. This study was based on the geographic distribution of 104 species in this genus analyzed with the BPA method. The consensus

mountain chains such the Sierra Madre del Sur and the Trans-Mexican Volcanic Belt.

**4. Cladistic biogeography studies in the Mexican Transition Zone**

America, Petén, and Golfo de México.

border between Mexico and Guatemala).

are considered as sister areas (Morrone, 1997).

were due to the geological complexity of the area under study.

NOTES: When the same name of an area of endemism appears in two or more cells, it means that this area in this particular study is very large and includes two or more biogeographic provinces. Empty cells mean that the biogeographic province was not included or considered in our study.

Table 1. Comparison among the areas of endemism of the Mexican Transition Zone used in some of the studies cited in this chapter, in relation to the biogeographic provinces of Arriaga et al. (1997) and Morrone (2001).

influenced the geographic distribution of the biota of the MTZ. The geological evolution of Mexico and Central America during the Cretaceous and Cenozoic has had a significant influence on the processes controlling the composition of their biota (Cevallos-Ferriz & González-Torres, 2005). The primary geological events shaping Mexico and Central America during these time intervals include the following: (1) the development of large magmatic provinces (Sierra Madre Occidental, Trans-Mexican Volcanic Belt, and Sierra Madre del Sur); (2) the fragmentation and displacement of continental segments including the opening of the Gulf of California (the separation of the Baja California Peninsula from the mainland) and the displacement of the Chortis Block to northern Central America; (3) the marine regression that outlined the current shape of Mexico; and (4) the formation and rise of an eastern orogenic belt known as the Sierra Madre Oriental (Cevallos-Ferriz & González-Torres, 2005; Ortega-Gutiérrez et al., 1994).

In Table 1 (above), two additional studies merit comment. Liebherr (1991) did not name areas of endemism, but designated them by letters, making it difficult to compare his areas with those of other authors. Rosen (1978) identified very small areas of endemism, only

Flores-Villela & Goyenechea (2001)

Highlands of Chiapas

Eastern Central American Atlantic lowlands

Western Central American Pacific

Talamanca ridge

lowlands

NOTES: When the same name of an area of endemism appears in two or more cells, it means that this area in this particular study is very large and includes two or more biogeographic provinces. Empty

Table 1. Comparison among the areas of endemism of the Mexican Transition Zone used in some of the studies cited in this chapter, in relation to the biogeographic provinces of

influenced the geographic distribution of the biota of the MTZ. The geological evolution of Mexico and Central America during the Cretaceous and Cenozoic has had a significant influence on the processes controlling the composition of their biota (Cevallos-Ferriz & González-Torres, 2005). The primary geological events shaping Mexico and Central America during these time intervals include the following: (1) the development of large magmatic provinces (Sierra Madre Occidental, Trans-Mexican Volcanic Belt, and Sierra Madre del Sur); (2) the fragmentation and displacement of continental segments including the opening of the Gulf of California (the separation of the Baja California Peninsula from the mainland) and the displacement of the Chortis Block to northern Central America; (3) the marine regression that outlined the current shape of Mexico; and (4) the formation and rise of an eastern orogenic belt known as the Sierra Madre Oriental (Cevallos-Ferriz & González-

In Table 1 (above), two additional studies merit comment. Liebherr (1991) did not name areas of endemism, but designated them by letters, making it difficult to compare his areas with those of other authors. Rosen (1978) identified very small areas of endemism, only

cells mean that the biogeographic province was not included or considered in our study.

Contreras-Medina et al. (2007)

Yucatán Península

Yucatán Península

Serranías Transístmicas

Eastern Central America

Costa Pacífica

Espinosa et al.

(2006)

Biogeographic provinces

YUC Chiapan

PTN Chiapan

CHI Chiapan

ECA Chiapan

WIP Talamancan

TAL Talamancan

Marshall & Liebherr (2000)

Guatemalan Highlands

Guatemalan Highlands

Guatemalan Highlands

Guatemalan Highlands

Cordillera

Cordillera

Arriaga et al. (1997) and Morrone (2001).

Torres, 2005; Ortega-Gutiérrez et al., 1994).

including small parts of the MTZ - these areas were mainly in Chiapas, eastern Central America, Petén, and Golfo de México.

#### **4. Cladistic biogeography studies in the Mexican Transition Zone**

Rosen (1978) was the first to apply a cladistic biogeography approach to the MTZ. In his biogeographic research, the author included the phylogenies of two fresh water fish of the genera *Heterandria* and *Xiphophorus*. Rosen (1978) recognized three coincidences of historical relationships, indicating the existence of a common ancestral distributional area that had been fragmented twice and that currently constitutes the basins of the Bravo River (in northern Mexico), the Pánuco River (in northeastern Mexico), and the Grijalva River (on the border between Mexico and Guatemala).

Another pioneering cladistic biogeographic study in the MTZ is that of Liebherr (1991). This author analyzed the history the mountain biota based on the phylogenies of two Coleoptera genera (*Elliptoleus* and *Calathus*). The complexity of the geologic history of southern Mexico is noted in the general area cladogram obtained, showing an ancient primary fragmentation that separated extra-tropical from tropical biota. Liebherr (1991) obtained a first clade that was divided in two subgroups, the first formed by the Sierra Madre Oriental and the second by the Sierra Madre Occidental and part of the Mexican Plateau. The tropical clade included the southern portions of the Sierra Madre Occidental, Sierra Madre Oriental and other Mexican mountain chains such the Sierra Madre del Sur and the Trans-Mexican Volcanic Belt.

Marshall & Liebherr (2000) published a cladistic biogeography study applying BPA and Assumption 0 methods based on 33 taxa (beetles, reptiles, fish and one plant genus) and using nine areas of endemism; they obtained four general area cladograms, one with BPA and three with Assumption 0. The congruence among these cladograms is shown in the relationships among the Arizona Mountains plus the Sierra Madre Occidental in one clade, and the Sierra Madre del Sur plus the Trans-Mexican Volcanic Belt related with the Chiapan-Guatemalan Highlands in another clade. Unfortunately, their approach included methodological confusion regarding the Assumption 0: the missing taxa option (or missing areas) in the matrix is treated by them as '0', indicating the lack of information regarding a taxon's occurrence. However, the Assumption 0 approach considers missing areas to be uninformative, as well as the other two assumptions (1 and 2) in a component analysis method (Morrone, 1998), so missing areas are located in all possible positions in the resolved area cladograms. Assumption 0 in BPA implies that areas inhabited by a widespread taxon are considered as sister areas (Morrone, 1997).

Flores-Villela & Goyenechea (2001) used 10 animal taxa in their biogeographical study (beetles, lizards, snakes and frogs) distributed in 13 areas of endemism; the method of reconciled trees implementing assumptions 0, 1, and 2 was applied in this study. The authors obtained six general area cladograms, but they did not achieve a consistent pattern of relationships among these cladograms. They concluded that each cladogram could only explain portions of the geographic history of the taxa studied, and that the results obtained were due to the geological complexity of the area under study.

Espinosa et al. (2006) generated hypotheses on the historical biogeography of tropical Mexico using the flowering plant genus *Bursera*. This study was based on the geographic distribution of 104 species in this genus analyzed with the BPA method. The consensus

Contributions of Cladistic Biogeography to the Mexican Transition Zone 165

may be the result of more than one vicariance pattern and/or to the reticulate biogeographic

A much needed analysis in the near future is consensus on the unification of areas of endemism in the MTZ. This will greatly strengthen cladistic biogeography interpretation, as well as the generation of new morphological and molecular phylogenies of the biota of the MTZ. Both activities represent a challenge, but it is the only way to advance in the comprehension of the complicated historical biogeography of this region. As Flores-Villela & Goyenechea (2001) noted in the title of their paper, we are still "seeking the lost pattern of

Dragana Manestar invited us to present this contribution. David Espinosa and Othón Alcántara assisted us with the figures and with useful comments on the manuscript. Lawrence E. Stevens made useful suggestions to this chapter. Finantial support was given

Álvarez, E. & Morrone, J.J. (2004). Propuesta de áreas para la conservación de aves de México,

Aguilar-Aguilar, R.; Contreras-Medina, R. & Salgado-Maldonado, G. (2003). Parsimony

Arriaga, L.; Aguilar, C.; Espinosa, D. & Jiménez, R. (eds). (1997). Regionalización ecológica y

Brooks, D.R.; Van Veller, M.G.P. & McLennan, D.A. (2001). How to do BPA, really. *Journal of*

Cevallos-Ferriz, S.R.S. & González-Torres, E. A. (2005). Geological setting and

Contreras-Medina, R. (2006). Los métodos de análisis biogeográfico y su aplicación a la

Contreras-Medina, R. & Eliosa-León, H. (2001). Una visión panbiogeográfica preliminar de

Autónoma de México-CONABIO, México, D. F. ISBN 968-36-9463-2

Conocimiento y Uso de la Biodiversidad (CONABIO), November 1997. Brooks, D.R. (1990). Parsimony analysis in historical biogeography and coevolution:

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history in areas of endemism (Morrone, 2009).

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**6. Acknowledgments**

by DGAPA-PAPIIT IN221711.

0305-0270

0039-7989

4020-3882-8

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**7. References**

general area cladogram obtained was formed by two main clades: the first included different areas of the Greater Antilles, and the second 12 Mexican areas of endemism. In this second clade all the areas located on the Pacific slope are included in one group, and the basal branch of this clade is constituted by the unique area located on the Gulf of Mexico slope. This general area cladogram shows the proposed historical relationships among tropical areas of Mexico.

The study of Contreras-Medina et al. (2007) was based on 81 gymnosperm species of the genera *Ceratozamia*, *Dioon* and *Pinus*, applying BPA and paralogy-free subtrees methods. In the case of the Mexican provinces, the unique relationship of both general area cladograms was the Mexican Plateau plus the Sierra Madre Oriental related with the Sierra Madre Occidental; the lowland provinces were mostly related, as in the study of Espinosa et al. (2006) with *Bursera*. Contreras-Medina and collaborators considered that both peninsulas of Mexico (Baja California and Yucatán) had a different history in relation to the continental portion of the country.

#### **5. Conclusions**

The MTZ represents a challenge for cladistic biogeography, due (in part) to its location at the boundaries between the Nearctic and Neotropical biogeographic regions, allowing the mixture of different biotic elements (Escalante et al., 2007), as suggested by previous studies from panbiogeographic approach (Contreras-Medina & Eliosa-León, 2001; Escalante et al. 2004; Morrone & Márquez, 2001). Also from a tectonic perspective, this region has formed through the convergence of three tectonic plates (North American, Cocos, and Caribbean), contributing to its geological complexity (Ortega et al., 1994).

After discussing the differences derived from applying different methods to carry out cladistic biogeographic analyses, Morrone & Carpenter (1994) concluded that when the data are "clean" (including few widespread taxa, redundant distributions, and missing areas), the results obtained using different methods are consistent. Some MTZ vicariance patterns, particularly those influenced by widespread taxa, redundant distributions and missing areas, appear to be ambiguous or the result of biogeographic noise. It remains difficult to select appropriate cladistic biogeographic methods because all have advantages and disadvantages, and all of them have been criticized (Morrone, 2009). One suggestion is to apply several methods and compare their differences and similarities (i.e., Contreras-Medina et al., 2007).

In addition, differences among the size and number of areas of endemism used in the different studies carried out in the MTZ make the search for congruent patterns of area relationships difficult. Unfortunately, it is not possible to make generalizations and comparisons among some clades obtained from the different studies commented upon here because, for example, some of the areas included in a clade of one study were not included in another, or in some studies wider units of analysis (areas of endemism) were used than those used in other studies. In some cases, different studies can be complementary, as occurred in the case of Marshall and Liebherr (2000) and Espinosa et al. (2006): the former was based mainly on mountainous taxa, whereas the latter was based mainly on lowland taxa. Notwithstanding, incongruent patterns should not be taken as signs of dispersal; they may be the result of more than one vicariance pattern and/or to the reticulate biogeographic history in areas of endemism (Morrone, 2009).

A much needed analysis in the near future is consensus on the unification of areas of endemism in the MTZ. This will greatly strengthen cladistic biogeography interpretation, as well as the generation of new morphological and molecular phylogenies of the biota of the MTZ. Both activities represent a challenge, but it is the only way to advance in the comprehension of the complicated historical biogeography of this region. As Flores-Villela & Goyenechea (2001) noted in the title of their paper, we are still "seeking the lost pattern of the biota inhabiting the Mexican Transition Zone."

#### **6. Acknowledgments**

Dragana Manestar invited us to present this contribution. David Espinosa and Othón Alcántara assisted us with the figures and with useful comments on the manuscript. Lawrence E. Stevens made useful suggestions to this chapter. Finantial support was given by DGAPA-PAPIIT IN221711.

#### **7. References**

164 Global Advances in Biogeography

general area cladogram obtained was formed by two main clades: the first included different areas of the Greater Antilles, and the second 12 Mexican areas of endemism. In this second clade all the areas located on the Pacific slope are included in one group, and the basal branch of this clade is constituted by the unique area located on the Gulf of Mexico slope. This general area cladogram shows the proposed historical relationships among

The study of Contreras-Medina et al. (2007) was based on 81 gymnosperm species of the genera *Ceratozamia*, *Dioon* and *Pinus*, applying BPA and paralogy-free subtrees methods. In the case of the Mexican provinces, the unique relationship of both general area cladograms was the Mexican Plateau plus the Sierra Madre Oriental related with the Sierra Madre Occidental; the lowland provinces were mostly related, as in the study of Espinosa et al. (2006) with *Bursera*. Contreras-Medina and collaborators considered that both peninsulas of Mexico (Baja California and Yucatán) had a different history in relation to the continental

The MTZ represents a challenge for cladistic biogeography, due (in part) to its location at the boundaries between the Nearctic and Neotropical biogeographic regions, allowing the mixture of different biotic elements (Escalante et al., 2007), as suggested by previous studies from panbiogeographic approach (Contreras-Medina & Eliosa-León, 2001; Escalante et al. 2004; Morrone & Márquez, 2001). Also from a tectonic perspective, this region has formed through the convergence of three tectonic plates (North American, Cocos, and Caribbean),

After discussing the differences derived from applying different methods to carry out cladistic biogeographic analyses, Morrone & Carpenter (1994) concluded that when the data are "clean" (including few widespread taxa, redundant distributions, and missing areas), the results obtained using different methods are consistent. Some MTZ vicariance patterns, particularly those influenced by widespread taxa, redundant distributions and missing areas, appear to be ambiguous or the result of biogeographic noise. It remains difficult to select appropriate cladistic biogeographic methods because all have advantages and disadvantages, and all of them have been criticized (Morrone, 2009). One suggestion is to apply several methods and compare their differences and similarities (i.e., Contreras-

In addition, differences among the size and number of areas of endemism used in the different studies carried out in the MTZ make the search for congruent patterns of area relationships difficult. Unfortunately, it is not possible to make generalizations and comparisons among some clades obtained from the different studies commented upon here because, for example, some of the areas included in a clade of one study were not included in another, or in some studies wider units of analysis (areas of endemism) were used than those used in other studies. In some cases, different studies can be complementary, as occurred in the case of Marshall and Liebherr (2000) and Espinosa et al. (2006): the former was based mainly on mountainous taxa, whereas the latter was based mainly on lowland taxa. Notwithstanding, incongruent patterns should not be taken as signs of dispersal; they

contributing to its geological complexity (Ortega et al., 1994).

tropical areas of Mexico.

portion of the country.

**5. Conclusions**

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**10**

*USA*

Lawrence E. Stevens

**The Biogeographic Significance of a Large,**

Mountains and uplifted areas occupy more than 10% of the Earth's surface, and their associated drainages rather commonly develop as constrained, canyon-bound channels. Therefore, large deep canyons (LDCs) are relatively frequently encountered, persistent landforms, occurring either as steeply dipping, V-shaped canyons that emerge from fold, fault-block, volcanic, and dome mountains, or occurring as drainages incised into uplifted plateaus. The latter type include the world's deepest canyons, including: the 3.35 km-deep Cotahuasi Canyon of the Rio Cotahuasi, a tributary of the Rio Ocona in southwestern Peru; the 2.44 km-deep Hells Canyon of the Snake River in Idaho; the >2.1 km-deep Barranca de Cobre in Chihuahua, Mexico; and the world-renowned 2.48 km-deep Grand Canyon in northern Arizona. LDCs also occur in submarine environments at the mouths of large rivers: the Nile and the Rhône Rivers have large submarine canyons at their mouths created during repeated Pliocene desiccation of the Mediterranean basin; the Indus and Ganges Rivers form lengthy submarine deltaic canyons; the Hudson River in northeastern North America has a substantial submarine canyon; and large canyons form in other tectonically active submarine areas. Whether terrestrial or subaqueous, LDCs support or generate strong ecological gradients, and periodically or perennially provide cascading deliveries of flow, sediments, nutrients, and biota to lower elevations (e.g., Gurnell and Petts 1995; Butman et al. 2006; Canals et al. 2009), processes that may influence the distribution and evolution of

Although both terrestrial and submarine LDCs are conspicuous landforms, their regional biogeographic significance has received remarkably little scientific attention, particularly in relation to that devoted to other major landforms, such as islands, lakes, and mountain ranges (Lomolino et al. 2010). Obviously functioning as barriers throughout human history and to many biota, terrestrial LDCs form complex habitat mosaics that also function as downstream and upstream corridors through higher elevation terrain, and LDCs contain an array of refugial habitats (Fig. 1; Stevens and Polhemus 2008). Consequently, LDCs may differentially facilitate or restrict gene flow, with ecological and evolutionary impacts on regional populations and assemblages across spatial and temporal scales, and in ways different from those of other conspicuous landforms. LDCs also are preferred sites for dam

**1. Introduction**

life around them.

**the Colorado River, Southwestern USA**

*Biology Department, Museum of Northern Arizona, Flagstaff, Arizona,*

**Deep Canyon: Grand Canyon of**

plant, insect, and bird taxa. *Southwestern Naturalist* Vol. 44, pp. 508—515, ISSN 0038-4909

### **The Biogeographic Significance of a Large, Deep Canyon: Grand Canyon of the Colorado River, Southwestern USA**

Lawrence E. Stevens *Biology Department, Museum of Northern Arizona, Flagstaff, Arizona, USA*

#### **1. Introduction**

168 Global Advances in Biogeography

Morrone, J.J. & Carpenter, J.M. (1994). In search of a method for cladistic biogeography: An

Myers, N.; Mittermeier, R.A.; Mittermeier, C.G.; da Fonseca, G.A.B. & Kent, J. (2000).

Nelson, G. & Ladiges, P.Y. (1995). TAX: MSDOS computer programs for systematics.

Nelson, G. & Ladiges, P.Y. (1996). Paralogy in cladistic biogeography and analysis of

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Ortega-Gutiérrez, F.; Sedlock, R. L. & Speed, R. C. (1994). Phanerozoic tectonic evolution of

Page, R.D.M. & Lydeard, C. (1994). Towards a cladistic biogeography of the Caribbean.

Rosen, D.E. (1978). Vicariant patterns and historical explanation in biogeography. *Systematic*

Sclater, P.L. (1858). On the geographical distribution of the Class Aves. *Journal of the Linnean*

Siddall, M.E. & Perkins, S.L. (2003). Brook parsimony analysis: a valiant failure. *Cladistics*

Van Veller, M. G. P. & Brooks, D.R. (2001). When simplicity is not parsimonious: a priori

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plant, insect, and bird taxa. *Southwestern Naturalist* Vol. 44, pp. 508—515, ISSN

empirical comparison of component analysis, Brooks parsimony analysis, and three-area statements. *Cladistics*, Vol. 10, No. 2, (June 1994), pp. 99—153, ISSN 1096-

Biodiversity hotspots for conservation priorities. *Nature* Vol. 403, pp. 853—858,

paralogy-free subtrees. *American Museum Novitates* Vol. 3167, pp. 1—58, ISSN 0003-

Mexico. In: *Phanerozoic evolution of North American continent-ocean transitions*, R.C. Speed (Ed.), pp. 265—306, The Geological Society of America, Boulder, Colorado. Mountains and uplifted areas occupy more than 10% of the Earth's surface, and their associated drainages rather commonly develop as constrained, canyon-bound channels. Therefore, large deep canyons (LDCs) are relatively frequently encountered, persistent landforms, occurring either as steeply dipping, V-shaped canyons that emerge from fold, fault-block, volcanic, and dome mountains, or occurring as drainages incised into uplifted plateaus. The latter type include the world's deepest canyons, including: the 3.35 km-deep Cotahuasi Canyon of the Rio Cotahuasi, a tributary of the Rio Ocona in southwestern Peru; the 2.44 km-deep Hells Canyon of the Snake River in Idaho; the >2.1 km-deep Barranca de Cobre in Chihuahua, Mexico; and the world-renowned 2.48 km-deep Grand Canyon in northern Arizona. LDCs also occur in submarine environments at the mouths of large rivers: the Nile and the Rhône Rivers have large submarine canyons at their mouths created during repeated Pliocene desiccation of the Mediterranean basin; the Indus and Ganges Rivers form lengthy submarine deltaic canyons; the Hudson River in northeastern North America has a substantial submarine canyon; and large canyons form in other tectonically active submarine areas. Whether terrestrial or subaqueous, LDCs support or generate strong ecological gradients, and periodically or perennially provide cascading deliveries of flow, sediments, nutrients, and biota to lower elevations (e.g., Gurnell and Petts 1995; Butman et al. 2006; Canals et al. 2009), processes that may influence the distribution and evolution of life around them.

Although both terrestrial and submarine LDCs are conspicuous landforms, their regional biogeographic significance has received remarkably little scientific attention, particularly in relation to that devoted to other major landforms, such as islands, lakes, and mountain ranges (Lomolino et al. 2010). Obviously functioning as barriers throughout human history and to many biota, terrestrial LDCs form complex habitat mosaics that also function as downstream and upstream corridors through higher elevation terrain, and LDCs contain an array of refugial habitats (Fig. 1; Stevens and Polhemus 2008). Consequently, LDCs may differentially facilitate or restrict gene flow, with ecological and evolutionary impacts on regional populations and assemblages across spatial and temporal scales, and in ways different from those of other conspicuous landforms. LDCs also are preferred sites for dam

The Biogeographic Significance

of a Large, Deep Canyon: Grand Canyon of the Colorado River, Southwestern USA 171

Fig. 2. Grand Canyon and the 144,000 km2 Grand Canyon ecoregion (dashed line) on the

dominated by intermountain Great Basin grasslands and pinyon-juniper woodlands. Upper elevation plateaus are occupied by cordilleran Rocky Mountain ponderosa pine (*Pinus ponderosa*) and mixed conifer forests, with large meadows, and highest elevations above 3600 m support 5 km2 of Rocky Mountain alpine tundra habitat (Table 1). The GCE is strongly dominated by upland shrublands, woodlands, and ponderosa pine forests, which collectively occupy 95% of the land area, while deserts below 1000 m and montane to alpine

The GCE is dominated by the large, deep canyons of the Colorado River and its many tributaries, and contains more than 75 ecosystems and habitats (Stevens and Nabhan 2002). Locations along the Colorado River are designated by distance from Lees Ferry, Arizona, and on the left (L) or right (R) side of the river looking downstream. Large tributaries include: the Paria River (Rkm 1.5R), the Little Colorado River (LCR; Rkm 98L), the Virgin River, Kanab Creek (Rkm 232R), Havasu/Cataract Canyon (253L), Diamond Creek/Peach Springs Wash (383L), and Grand Wash (479R; Figs. 2, 3). Hoover and Glen Canyon Dams on the Colorado River create the nation's two largest reservoirs, Lake Mead and Lake Powell, respectively, which overlap into the GCE. Not within GC, the Black, White, Eagle, and other tributaries of the upper Gila River form the southeastern drainage boundary of the GCE. Tonto Creek, a central Gila River tributary, drains the region west of the upper Gila River

southern Colorado Plateau, southwestern U.S.A.

habitats above 2800 m each occupy only about 2.5% of the land area.

construction, and many LDCs and their associated assemblages have been altered by flow regulation throughout the world. Here I describe the biogeographical characteristics and significance of the world's most famous terrestrial LDC, Grand Canyon (GC) of the Colorado River in the American Southwest within its drainage basin, the Grand Canyon ecoregion (GCE). I compare LDC characteristics with those of other major landforms, and describe conservation issues.

Fig. 1. Schematic diagram of the biogeographic functions of large, deep canyons.

#### **2. Study area**

The GCE includes 144,000 km2 of the southern Colorado Plateau in northern Arizona, southern Utah, and western New Mexico (Fig. 2). This is a topographically complex region, ranging in elevation from 350 m AMSL on eastern Lake Mead to 3,850 m on the San Francisco Mountains near Flagstaff, Arizona, and with the highest point on the North Rim of GC at approximately 2,830 m. The climate of the GCE is continental and arid, with low elevation desert summertime high temperatures >45oC, and high elevation mountain winter low temperatures < -55oC. Precipitation is bimodal, with wintertime snowfall and rain, and mid-late summer monsoonal rains (Sellers et al. 1985). More than 90 percent of the GCE is managed by federal agencies or Indian Tribes, including: 12 National Park units, particularly including Grand Canyon National Park; 6 National Forest units; the Bureau of Land Management; and 8 Native America tribes. State lands include small tracts of state fish and wildlife management units, and private lands are few.

A major geologic province boundary divides Arizona in half, with the Basin and Range geologic province to the south and west, and the Colorado Plateau division of the Rocky Mountain geologic province to the north and east (Fig. 2). The boundary runs diagonally NW-SE through central Arizona, creating a lengthy escarpment known as the Mogollon Rim. This geologic province boundary forms a biogeographic ecotone between the Mexicanneotropical Madrean floristic region and the boreal Rocky Mountain floristic region, referred to as the Lowe-Davis line (Lomolino et al. 2010). Drainages that breach this geologic province boundary (e.g., the Virgin and Verde Rivers) are richer in species of aquatic invertebrates than are those that do not bridge the boundary (e.g., the Escalante River, the Little Colorado River, the Paria River, Kanab Creek, and Havasu Creek; Stevens and Polhemus 2008, Stevens and Bailowitz 2009).

The GCE lies at the intersection of 4 biomes, including the Madrean, Mohavean/Sonoran, intermountain, and cordilleran biomes. Low desert habitats to the south are occupied by Madrean, Sonoran, and Mohavean desert shrub vegetation, while middle elevations are

construction, and many LDCs and their associated assemblages have been altered by flow regulation throughout the world. Here I describe the biogeographical characteristics and significance of the world's most famous terrestrial LDC, Grand Canyon (GC) of the Colorado River in the American Southwest within its drainage basin, the Grand Canyon ecoregion (GCE). I compare LDC characteristics with those of other major landforms, and

Fig. 1. Schematic diagram of the biogeographic functions of large, deep canyons.

and wildlife management units, and private lands are few.

Polhemus 2008, Stevens and Bailowitz 2009).

The GCE includes 144,000 km2 of the southern Colorado Plateau in northern Arizona, southern Utah, and western New Mexico (Fig. 2). This is a topographically complex region, ranging in elevation from 350 m AMSL on eastern Lake Mead to 3,850 m on the San Francisco Mountains near Flagstaff, Arizona, and with the highest point on the North Rim of GC at approximately 2,830 m. The climate of the GCE is continental and arid, with low elevation desert summertime high temperatures >45oC, and high elevation mountain winter low temperatures < -55oC. Precipitation is bimodal, with wintertime snowfall and rain, and mid-late summer monsoonal rains (Sellers et al. 1985). More than 90 percent of the GCE is managed by federal agencies or Indian Tribes, including: 12 National Park units, particularly including Grand Canyon National Park; 6 National Forest units; the Bureau of Land Management; and 8 Native America tribes. State lands include small tracts of state fish

A major geologic province boundary divides Arizona in half, with the Basin and Range geologic province to the south and west, and the Colorado Plateau division of the Rocky Mountain geologic province to the north and east (Fig. 2). The boundary runs diagonally NW-SE through central Arizona, creating a lengthy escarpment known as the Mogollon Rim. This geologic province boundary forms a biogeographic ecotone between the Mexicanneotropical Madrean floristic region and the boreal Rocky Mountain floristic region, referred to as the Lowe-Davis line (Lomolino et al. 2010). Drainages that breach this geologic province boundary (e.g., the Virgin and Verde Rivers) are richer in species of aquatic invertebrates than are those that do not bridge the boundary (e.g., the Escalante River, the Little Colorado River, the Paria River, Kanab Creek, and Havasu Creek; Stevens and

The GCE lies at the intersection of 4 biomes, including the Madrean, Mohavean/Sonoran, intermountain, and cordilleran biomes. Low desert habitats to the south are occupied by Madrean, Sonoran, and Mohavean desert shrub vegetation, while middle elevations are

describe conservation issues.

**2. Study area**

Fig. 2. Grand Canyon and the 144,000 km2 Grand Canyon ecoregion (dashed line) on the southern Colorado Plateau, southwestern U.S.A.

dominated by intermountain Great Basin grasslands and pinyon-juniper woodlands. Upper elevation plateaus are occupied by cordilleran Rocky Mountain ponderosa pine (*Pinus ponderosa*) and mixed conifer forests, with large meadows, and highest elevations above 3600 m support 5 km2 of Rocky Mountain alpine tundra habitat (Table 1). The GCE is strongly dominated by upland shrublands, woodlands, and ponderosa pine forests, which collectively occupy 95% of the land area, while deserts below 1000 m and montane to alpine habitats above 2800 m each occupy only about 2.5% of the land area.

The GCE is dominated by the large, deep canyons of the Colorado River and its many tributaries, and contains more than 75 ecosystems and habitats (Stevens and Nabhan 2002). Locations along the Colorado River are designated by distance from Lees Ferry, Arizona, and on the left (L) or right (R) side of the river looking downstream. Large tributaries include: the Paria River (Rkm 1.5R), the Little Colorado River (LCR; Rkm 98L), the Virgin River, Kanab Creek (Rkm 232R), Havasu/Cataract Canyon (253L), Diamond Creek/Peach Springs Wash (383L), and Grand Wash (479R; Figs. 2, 3). Hoover and Glen Canyon Dams on the Colorado River create the nation's two largest reservoirs, Lake Mead and Lake Powell, respectively, which overlap into the GCE. Not within GC, the Black, White, Eagle, and other tributaries of the upper Gila River form the southeastern drainage boundary of the GCE. Tonto Creek, a central Gila River tributary, drains the region west of the upper Gila River

The Biogeographic Significance

**3. Ecological gradients**

**3.1 Overview**

gradients in the GCE.

**3.2 Gravity**

of a Large, Deep Canyon: Grand Canyon of the Colorado River, Southwestern USA 173

Fig. 3. Grand Canyon rim and major tributaries map, showing the eastern and western basins divided by the Muav Gorge, and distances along river from Lees Ferry (Rkm 0). Map

LDCs create complex spatially and temporally intercorrelated environmental gradients, and ecological processes that often are stratified across elevation, strongly affecting the composition and structure of biotic assemblages. The major gradients in LDCs include: gravity, geology, regional climate, elevation, and aspect. Collectively, these affect, generate, or permit the solar radiation budget, micro- to synoptic climate, moisture availability, dip angle, pedogenesis, and natural disturbance regimes, all of which affect the development of canyon biotic assemblages over time. Here I briefly review the roles of these major physical

Gravity plays a profound role in species dispersal and ranges in LDCs. Passively dispersing taxa, including plants, non-flying invertebrates and vertebrates, and even some bird species more readily disperse and colonize downslope. Although the inner canyon corridor within 100 m of the river makes up less than 3 percent of the overall land area in the GC, that zone supports more than 760 plant species, more than 40% of the entire GC flora (Stevens and Ayers 2002, Busco et al. 2011). Downslope dispersal accounts for the in-canyon occurrence of many

redrawn from Billingsley and Hampton (1999), and prepared by J. D. Ledbetter.

Table 1. Merriam life zones and vegetation zonation across elevation in the GCE

basin. The Verde River basin breaches the geologic province boundary, draining the central southern portion of the GCE. The Virgin River drains southwestern Utah and northwestern Arizona, also breaching the geologic province boundary. In addition, the GCE supports thousands of caves and springs (Stevens and Meretsky 2008), and thousands of km of escarpment edges.

Embedded wholly within the southwestern Colorado Plateau, GC is naturally separated into an eastern basin, which receives the flows of the Paria and LCR drainages, and a more open western basin that connects western Grand Canyon to the Mojave and Sonoran deserts to the west and south (Fig. 3; Billingsley and Hampton 1999, Stevens and Huber 2004). The two GC basins are separated by the steep, narrow 35 km-long Muav Gorge, which creates a formidable cliff-dominated barrier to upstream and downstream dispersal of numerous southwestern plant, invertebrate, and vertebrate taxa (Miller et al. 1982; Phillips et al. 1987; Schmidt and Graf 1990; Stevens and Polhemus 2008).

Fig. 3. Grand Canyon rim and major tributaries map, showing the eastern and western basins divided by the Muav Gorge, and distances along river from Lees Ferry (Rkm 0). Map redrawn from Billingsley and Hampton (1999), and prepared by J. D. Ledbetter.

### **3.  Merriam life zones and vegetation zonation across elevation in the GCE

3600-3850 Alpine Tundra shrubs, graminoides At elevations above GC in

basin. The Verde River basin breaches the geologic province boundary, draining the central southern portion of the GCE. The Virgin River drains southwestern Utah and northwestern Arizona, also breaching the geologic province boundary. In addition, the GCE supports thousands of caves and springs (Stevens and Meretsky 2008), and thousands of km of

Embedded wholly within the southwestern Colorado Plateau, GC is naturally separated into an eastern basin, which receives the flows of the Paria and LCR drainages, and a more open western basin that connects western Grand Canyon to the Mojave and Sonoran deserts to the west and south (Fig. 3; Billingsley and Hampton 1999, Stevens and Huber 2004). The two GC basins are separated by the steep, narrow 35 km-long Muav Gorge, which creates a formidable cliff-dominated barrier to upstream and downstream dispersal of numerous southwestern plant, invertebrate, and vertebrate taxa (Miller et al. 1982; Phillips et al. 1987;

riparian vegetation

3000-3600 Hudsonian Spruce-fir forest; springs riparian vegetation

vegetation

Schmidt and Graf 1990; Stevens and Polhemus 2008).

Pinyon pine (*Pinus* spp.), *Juniperus* spp.; Great Basin shrublands; grasslands; stream and springs riparian vegetation

**Zone Characteristic Flora Comments**

GC floor and lower slopes

GC middle-upper slopes

Both GC rims

GC North Rim

Mtns

Mtns

At elevations above GC in the White and San Francisco

At elevations above GC in the White and San Francisco

the San Francisco Mtns

**Elevation Range (m)**

<1500 Lower

1100-2300 Upper

1600-2800 Transition

2500-3300 Canadian

3400-3700 Subalpine

escarpment edges.

**Vegetation**

Sonoran

Sonoran

LDCs create complex spatially and temporally intercorrelated environmental gradients, and ecological processes that often are stratified across elevation, strongly affecting the composition and structure of biotic assemblages. The major gradients in LDCs include: gravity, geology, regional climate, elevation, and aspect. Collectively, these affect, generate, or permit the solar radiation budget, micro- to synoptic climate, moisture availability, dip angle, pedogenesis, and natural disturbance regimes, all of which affect the development of canyon biotic assemblages over time. Here I briefly review the roles of these major physical gradients in the GCE.

#### **3.2 Gravity**

Gravity plays a profound role in species dispersal and ranges in LDCs. Passively dispersing taxa, including plants, non-flying invertebrates and vertebrates, and even some bird species more readily disperse and colonize downslope. Although the inner canyon corridor within 100 m of the river makes up less than 3 percent of the overall land area in the GC, that zone supports more than 760 plant species, more than 40% of the entire GC flora (Stevens and Ayers 2002, Busco et al. 2011). Downslope dispersal accounts for the in-canyon occurrence of many

The Biogeographic Significance

1997a,b; Stevens et al. 2009).

**3.4 Elevation**

and biome development (Olson et al. 2001).

of a Large, Deep Canyon: Grand Canyon of the Colorado River, Southwestern USA 175

Fluvial geomorphology has been thoroughly studied in GC (e.g., Howard and Dolan 1981; Schmidt and Graf 1990; Topping et al. 2005). Rapids form at the confluence of tributary canyons when rare debris flows deliver large boulders into the Colorado River, damming the mainstream (Webb et al. 1987). Rapids create recirculation zones (eddies) that, on descending flows, deposit fine sediments in characteristic locations both upstream and downstream of the debris fans. Thus, unlike alluvial rivers, the location of sandbars in the geomorphically constrained Colorado River are fixed within 13 geomorphic reaches (Table 2). More than 550 debris fan complexes generate a distinctive suite of fluvial microhabitats, each with discrete grain sizes, soils, stage elevation relationships, inundation frequencies, and stage-zoned riparian vegetation (Turner and Karpiscak 1980; Schmidt and Graf 1990; Melis et al. 1997). Analyses of flow regulation influences at a large suite of debris fan complexes revealed that flow regulation allowed extensive development of fluvial marshes, enhancing riverine plant species richness (Stevens et al. 1995; Waring et al. in press). Clearwater releases and flood control also greatly increased aquatic productivity within the river which, coupled with riparian vegetation expansion, has led to increased waterbird biodiversity, and peregrine falcon (*Falco peregrinus anatum*) population increases and the potential for formation of novel post-dam trophic cascades (Brown et al. 1992; Stevens et al.

Thus, flow regulation reduced flooding disturbance and increased productivity of this naturally flood-prone river ecosystem, changing the river ecosystem energetics from allochthonous to autochthonous sources (Carothers and Brown 1991), and increasing riverine species richness and trophic complexity, in accord with the predictions of both Connell's (1978) intermediate disturbance concept and Huston's (1979) dynamic equilibrium model (Stevens and Ayers 2002). But also of scientific and stewardship interest, flow regulation differentially influenced geomorphological influences on subaqueous versus subaerial biota, colonization, and production. Flow regulation has swamped geomorphic influences on biological organization in the aquatic domain of the river, reducing differences in benthic standing stock or species among various aquatic microhabitats (Stevens et al. 1997b). In contrast, flow regulation has enhanced variation in biotic development on the various geomorphic microhabitats in debris fans in the riparian domain (Stevens et al. 1995, 1997a). Differential responses of the river ecosystem to flow regulation on the aquatic versus the riparian domains vastly complicate environmental management of focal species and habitats, creating challenging administrative tradeoffs (Stevens et al. 2001; Lovich and Melis 2007).

Elevation strongly affects local climate, productivity, species composition, and microsite ecology. Following the model of Von Humboldt and Bonpland (1805, Jackson 2009), C.H. Merriam was the first American naturalist to quantify the influences of elevation on biotic zonation across an Arizona transect from the floor of Grand Canyon to the top of the San Francisco Peaks and out into the Painted Desert (Merriam and Steineger 1890). Merriam attributed the discrete zonation of trees across elevation primarily to temperature and latitude; however, Holdridge (1947) and others subsequently recognized the importance of seasonal and total precipitation, evapotranspiration, and other factors controlling vegetation

rim-dwelling species of grasses, forbs, shrubs (e.g., *Fallugia paradoxa, Parreyella filifolia*), and trees. These upper elevation "waif" or "Gilligan" species may reach the canyon-floor desert, far from their normal habitats and, while able to become established, they may not be able to reproduce or form permanent colonies. Such species are particularly likely to occur in aspect refugia: boreal colonists often occur in the desert on north-facing slopes. Numeorus insects (e.g, *Prionus heros*, various scarabaeids, *Pandora* moths), wild turkey (*Meleagris gallopavo*), and other rim fauna also readily disperse downslope, and have been regularly detected along the river (Brown et al. 1987; LaRue et al. 2001; Stevens unpublished data).

#### **3.3 Geology and geomorphology**

Geologic context, parent rock, structure, and tectonic history play dominant roles governing the development, functioning, and characteristics of LDC ecosystems. Geology and geologic processes control: 1) elevation, a primary determinant of local climate; 2) aspect, in turn influencing solar radiation budget, microclimate, productivity, pedogenesis, habitat availability, and species distributions; 3) geomorphology, including width-depth relationships of the canyon stream channel; and 4) rock color, which may differentially affect heat loading. The subject of microtopographic ecological gradient impacts on assemblages is generally poorly studied, but topographic differences of less than 10 m can affect local microclimate and species distributions, particularly near water sources where surface heating affects humidity.

Although much debated, drainage evolution of the Colorado River in the American Southwest has occurred over the past 40 million yr through conclusion of the Laramide orogeny and the onset of Basin and Range orogenic uplift and stream capture (Hunt 1956; Dickinson 2002; review in Blakey and Ranney 2008). On-going debate over development of the Colorado River basin is divided between advocacy for an old canyon (Oligocene-Miocene origination) as opposed to a young canyon (late Miocene-Pleistocene origination), and top-down drainage integration versus integration of variably independent sub-basins. Basin and Range crustal extension caused the uplift of the Sierra Nevada Range and numerous other north-trending ranges, which block the on-shore movement of moist Pacific airflow. This geologic deformation and development of the regional rain-shadow over the past 15 million ys changed the GCE from a low-lying, mesic, savannah-dominated landscape to its present-day uplifted, arid character. Also of great biogeographic impact was the tectonic/volcanic connection between South and North America 2.7 million years ago (Wallace 1876; Webb 2006). The ensuing land bridge permitted movement of biota between continents, resulting in the Great American Biotic Interchange, resulting in the movement and extinction of numerous species. The interchange is largely responsible for the contemporary co-occurrence of 150 genera of plants and animals in South America and the American Southwest. Following integration of the Colorado River, western Grand Canyon was dammed by numerous lava flows over the past 750,000 yr, forming large Pleistocene lakes and perhaps large outburst floods (Hamblin 1994; Crow et al. 2008). Biogeographic analyses of aquatic nepomorph Hemiptera (Stevens and Polhemus 2008) demonstrate significant upstream attenuation in species richness, suggesting that such flooding reversed or retarded upriver colonization in Pleistocene time. Interestingly, the ranges of aquatic Heteroptera taxa in that study also reveal the "biological shadow" of an earlier Paleogene east- and north-flowing Nevada river system into western Grand Canyon, a river unrelated to the present-day Colorado River.

Fluvial geomorphology has been thoroughly studied in GC (e.g., Howard and Dolan 1981; Schmidt and Graf 1990; Topping et al. 2005). Rapids form at the confluence of tributary canyons when rare debris flows deliver large boulders into the Colorado River, damming the mainstream (Webb et al. 1987). Rapids create recirculation zones (eddies) that, on descending flows, deposit fine sediments in characteristic locations both upstream and downstream of the debris fans. Thus, unlike alluvial rivers, the location of sandbars in the geomorphically constrained Colorado River are fixed within 13 geomorphic reaches (Table 2). More than 550 debris fan complexes generate a distinctive suite of fluvial microhabitats, each with discrete grain sizes, soils, stage elevation relationships, inundation frequencies, and stage-zoned riparian vegetation (Turner and Karpiscak 1980; Schmidt and Graf 1990; Melis et al. 1997). Analyses of flow regulation influences at a large suite of debris fan complexes revealed that flow regulation allowed extensive development of fluvial marshes, enhancing riverine plant species richness (Stevens et al. 1995; Waring et al. in press). Clearwater releases and flood control also greatly increased aquatic productivity within the river which, coupled with riparian vegetation expansion, has led to increased waterbird biodiversity, and peregrine falcon (*Falco peregrinus anatum*) population increases and the potential for formation of novel post-dam trophic cascades (Brown et al. 1992; Stevens et al. 1997a,b; Stevens et al. 2009).

Thus, flow regulation reduced flooding disturbance and increased productivity of this naturally flood-prone river ecosystem, changing the river ecosystem energetics from allochthonous to autochthonous sources (Carothers and Brown 1991), and increasing riverine species richness and trophic complexity, in accord with the predictions of both Connell's (1978) intermediate disturbance concept and Huston's (1979) dynamic equilibrium model (Stevens and Ayers 2002). But also of scientific and stewardship interest, flow regulation differentially influenced geomorphological influences on subaqueous versus subaerial biota, colonization, and production. Flow regulation has swamped geomorphic influences on biological organization in the aquatic domain of the river, reducing differences in benthic standing stock or species among various aquatic microhabitats (Stevens et al. 1997b). In contrast, flow regulation has enhanced variation in biotic development on the various geomorphic microhabitats in debris fans in the riparian domain (Stevens et al. 1995, 1997a). Differential responses of the river ecosystem to flow regulation on the aquatic versus the riparian domains vastly complicate environmental management of focal species and habitats, creating challenging administrative tradeoffs (Stevens et al. 2001; Lovich and Melis 2007).

#### **3.4 Elevation**

174 Global Advances in Biogeography

rim-dwelling species of grasses, forbs, shrubs (e.g., *Fallugia paradoxa, Parreyella filifolia*), and trees. These upper elevation "waif" or "Gilligan" species may reach the canyon-floor desert, far from their normal habitats and, while able to become established, they may not be able to reproduce or form permanent colonies. Such species are particularly likely to occur in aspect refugia: boreal colonists often occur in the desert on north-facing slopes. Numeorus insects (e.g, *Prionus heros*, various scarabaeids, *Pandora* moths), wild turkey (*Meleagris gallopavo*), and other rim fauna also readily disperse downslope, and have been regularly detected along the