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Diversity and distributional patterns of legumes in northeastern Mexico.

Next to grasses, legumes are one of the most important groups of plants, because of their use as food (e.g., Glycine, Phaseolus, Vicia, Pisum, Cicer), forage (e.g., Trifolium, Melilotus, Medicago; Isely, 1981), as fuel (e.g., Prosopis, Acacia, Havardia, Ebenopsis), as charcoal (e.g., Prosopis, Ebenopsis), and in the chemical industry (Acacia, Coronilla, Indigofera; Doyle and Luckow, 2003). In contrast, many legumes can be noxious plants, e.g., Astragalus, Calia, Sophora, and Lupinus, which produce serious economic loss, particularly in the cattle industry because of their toxicity (Lynn, 1983; Lynn and Shupe, 1984). In addition, some thorny shrubs and forbs such as species of Acacia (Elias, 1974; Estrada and Marroquin, 1991), Prosopis (Burkart, 1976), Senna (Irwin and Barneby, 1982), and Mimosa (Barneby, 1991) are aggressive weeds, which are able to colonize bush fallows, burned sites, and overgrazed pastures.

Legumes are cosmopolitan in distribution, living in nearly all existing ecosystems, often as dominant members of plant communities, such as in scrublands in arid and semi-arid areas of the world. In Mexico, Leguminosae occurs in all plant communities and is the second most diverse family, with 139 genera and 1,850 species (Sousa and Delgado, 1993; Sousa et al., 2004). Northern Mexico hosts 121 genera (Estrada and Martiinez, 2003) and ca. 550 species of legumes. A large proportion of these belong to the subfamily Papilionoideae. Genera such as Astragalus, Dalea, and Desmodium, as well as members of the other two subfamilies, such as Acacia, Mimosa, and Senna contribute to the great number of species. Several Mimosoideae, especially species of Acacia and Prosopis, play a dominant ecological role due to their abundance, canopy cover, and density in the region (Estrada and Marroquiin, 1991; Jurena and Van Auken, 1998; Estrada et al., 2004, 2005; Seigler et al., 2007). The aim of this study was to elucidate diversity of legumes and their association with plant communities in northeastern Mexico.

Materials and Methods--The study area (Fig. 1) is between 23[degrees]01' and 28[degrees]58'N and 98[degrees]01' and 101[degrees]04'W, and most of this (70-75%) harbors different scrub communities, while the rest is covered mainly by oak and coniferous forests. The northeastern region of Mexico, as here defined, includes the westernmost parts of Tamaulipas and Nuevo Leon, and the eastern edge of Coahuila. The region is characterized by low and high plains, low hills, and high mountains, at elevations of 150-3,650 m, comprising three main and contrasting physiographic provinces (Great Plains of North America, Gulf of Mexico Coastal Plains, and Sierra Madre Oriental; Arriaga et al., 2000; Comision Nacional para el Conocimiento y Uso de la Biodiversidad, 2000).

[FIGURE 1 OMITTED]

Geologically, the region is composed of sedimentary rocks of marine origin; products of chemical and clastic Mesozoic deposits. Nearly all outcrops of the Gulf Coastal Plains and the Great Plains of North America, at 150-560 m elevation were derived from Upper Cretaceous deposits. These outcrops are mainly lutites, sands, conglomerates, and limestone. Low hills in the central portion were formed by regozols, which includes associations of rendzines and xerosols. Intermountain valleys and low plains were composed mainly by clayish dark black or dark gray, pelic vertisols, and reddish and clayish cromic vertisols, whereas calcic xerosols prevail in the high plains. Higher-elevation plains and intermountain valleys (1,400-1,950 m) bordering the mountains in the south-central region formed flattened plateaus, with xerosols and gypsic yermosol soils (Secretariia de Programacion y Presupuesto, 1986).

Climate in northern and southern low plains is semidry and it is dry in the high plains; however, semi-calid, subhumid climates occur in the central low plains and temperate-subhumid climates characterize the mountains (Garcia, 1973; Secretariia de Programacion y Presupuesto, 1986). Annual precipitation in low and high plains is 400-600 mm (Garcia, 1973), where mean annual temperature is >22[degrees]C. In contrast, cooler temperatures, 12-18[degrees]C, and 600-800 mm of annual rainfall, have been recorded in the mountains. McDonald (1993) described climatic conditions of two of the highest peaks carrying subalpine and alpine vegetation (Cerro Potosi and Pena Nevada); mean annual temperatures were -3 to 18[degrees]C and precipitation was >100 mm/year, occurring mostly during summer.

Fossil evidence suggests that climate of the region probably was more tropical and humid in the past and, therefore, probably supported a more mesophytic flora. For example, fossils from La Popa, Nuevo Leoin (Calvillo-Canadel and Cevallos-Ferris, 2005), in the east-entral portion of the study area, suggest the occurrence of Inga, a legume tree restricted to more mesic environments.

Existing vegetational associations in northeastern Mexico are highly heterogeneous, and 12 main plant communities have been recognized: tamaulipan thornscrub, piedmont scrub, rosetophyllous scrubland, xeric scrubland, chaparral, halophytic communities, oak forest, oak-pine forest, xeric-conifer forest (forests of Pinus cembroides), mesic-conifer forest, mainly with Pinus teocote and P. pseudostrobus, the cool-conifer forest, characterized by P. hartwegii, P. strobiformis, Abies vejari, and Pseudotsuga menziesi, and the subalpine and alpine-meadow vegetation (Muller, 1939; Rojas-Mendoza, 1965; Rzedowski, 1978; Secretaria de Programacion y Presupuesto, 1981 b).

At low elevations (150-300 m), the landscape is dominated by dry Tamaulipan thornscrub, with vegetation composed of shrubs from low (1-2.5 m) to medium (2.5-4 m) height that are armed with thorns and spines (Acacia, Havardia, Prosopis, and Ebenopsis (Muller, 1939; Secretariia de Programacion y Presupuesto, 1981 a). Immediately above or adjacent to it, a belt of piedmont scrub is present (Rzedowski, 1978; Secretariia de Programacion y Presupuesto, 1981 b; Estrada, 1998). Although broadly similar to Tamaulipan thornscrub, this community differs in height of shrubs (3-5 m), armature (predominance of unarmed shrubby species), and diversity. The most common woody genera in the piedmont scrub are Zanthoxyllum and Helietta (Rutaceae), and species of Forestiera and Fraxinus (Oleaceae; Gonzalez-Medrano, 1972). Rosetophyllous scrublands are mainly on rocky mountain slopes and on the Mexican High Plateau (750-1,900 m), and are characterized by genera such as Agave, Dasylirion, Hespheraloe, Yucca (Agavaceae), and Nolina (Nolinaceae). Xeric scrublands dominate high-elevation plains (1,400-1,750 m), and their most conspicuous element is Larrea tridentata (Zygophyllaceae), mainly associated with Acacia, Flourensia, Parthenium (Asteraceae), Rhus (Anacardiaceae), Koeberlinia (Koeberliniaceae), Forestiera (Oleaceae), and Schaefferia (Celastraceae). The chaparral community is discontinuous and fragmented in northern Mexico and, being prone to fire, occupies mostly dry areas, slopes of low mountains (1,400 m), and burned areas of the highest peaks (2,700-3,000 m). Diverse types of forests occur in the mountains of northeastern Mexico; oak forests (Quercus), oak-pine forests, and conifer forests with different associations of genera such as Pinus, Pseudotsuga, Abies, Taxus, Cupressus, and Juniperus. Oak forests predominate at 900-1,900 m elevation; whereas conifer forests occur at 1,600-1,900 m (xeric and mesic conifer forests) and 3,450 m (cool conifer forest) elevations. Mixed oak-pine forests occupy elevations of 1,250-2,100 m. Halophytic communities are fairly common on the high plains and intermountain valleys of the west-central and southern portions of the region, mainly at 1,550-1,850 m elevation. Indicative of these is the occurrence of Mexican prairie dogs (Cynomys mexicanus; Villarreal and Grant, 1998; Scott et al., 2004), with plants 15-40 cm tall dominated by perennial grasses such as Muhlenbergia, Scleropogon, and Buchloe. Summits of the highest peaks sheltered small patches of alpine-meadow vegetation, which, in the case of Cerro Potosii, is characterized by populations of the dwarf, endemic conifer, Pinus culminicola (Andresen and Beaman, 1961).

During 8 years (2001-2008), collections of legumes (native and non-native) were made in the 12 communities. In these 12 communities, 224 sites were sampled (Fig. 1). At each site, geographic coordinates, elevation, type of soil, orientation of slope, and occurrence of species were recorded. All species of legumes were collected as well, and observations of their habitat and phenology were recorded. A matrix listing presence-absence data of each species for each plant community was assembled. All botanical specimens were identified and deposited in the CFNL (Faculad de Ciencias Forestales, Universidad Autonoma de Nuevo Leon, Nuevo Leoin, Meixico); duplicates were sent to herbaria at ANSM (Universidad Autonoma Agraria Antonio Narro, Saltillo, Mexico), BRIT (Botanical Research Institue of Texas), MEXU (Universidad Nacional Autonoma de Meixico, Meixico, Distrito Federal), and TEX (Plant Resource Center, University of Texas at Austin). In addition, collections of legumes in herbaria at ANSM, MEXU, UNL, and TEX were consulted to include those species not collected during our field work.

The Sorensen index (ISs = 2W/(A + B) * 100) was used (Muller-Dumbois and Ellenberg, 1974) to determine degree of similarity among plant communities. Similarity and dissimilarity matrices were constructed for legumes present in the 12 plant communities (cultivated legumes were excluded from the analysis). Indices were analyzed using cluster analysis by means of hierarchic-polythetic-agglomerative classification (Gauch, 1982; Manly, 1992) and the minimum-variance method (Ward, 1963) using Statistical Analysis System (SAS Institute, Inc., 1985). To estimate distortion with respect to the original distance matrix, a resulting dendrogram was evaluated by cophenetic correlation coefficients (Sneath and Sokal, 1973).

Results--Diversity--We recorded 79 genera, 259 species, and 45 infraspecific taxa of legumes in the study region. Subfamily Papilionoideae had the largest number of genera and species, followed by Mimosoideae and Caesalpinioideae (Table 1). Genera with the largest number of wild species were Dalea (28 species), Desmodium (16), Astragalus (13), Senna (13), Acacia (11, excluding two species currently included in Acaciella; Rico Arce and Bachman, 2006), Phaseolus (10), Crotalaria (9), and Lupinus (8); 24 genera had [greater than or equal to]3 species. Of the 17 species of cultivated legumes, most were Caesalpinioideae; they were recorded and included in this study but not analyzed statistically. Endemic to the area were 21 species, most were in three genera, Lupinus (5 species), Astragalus (4), and Dalea (4).

In oak-pine forests, we recorded 125 species of legumes, whereas oak forests, Tamaulipan thornscrub, and mesic conifer forests harbored 111, 94, and 92 species, respectively. These four plant communities had the greatest diversity of legumes. In contrast, alpine meadow (10 species), halophytic communities (33), rosetophyllous scrubland (39), and xeric conifer forest (36) had fewer species. Only Papilionoideae was present in all communities. Most species of this subfamily occurred in oak-pine forests, oak forests, and alpine meadows. However, most species of mimosoids and caesalpinioids inhabited the Tamaulipan thornscrub and piedmont scrub communities, whereas only a few were in the cool temperate forest (8 species) and halophytic grasslands (7). In addition, and excluding cultivated legumes, herbaceous (123 species) and non-thorny shrubs (55) were the most common biological forms of legumes in the area, whereas thorny shrubs (29 species) and trees (8) were less common (Fig. 2).

Endemism--In the study area, 21 species of legumes were endemic. Most occurred at elevations > 1,450 m, inhabiting all plant communities of the high plains and mountains. Some occurred in three contiguous plant communities; thus, showing preferences to specific climates, soils, and topography. Only one species, Desmanthus pringlei was in the low plains (Tamaulipan thornscrub and piedmont scrub) besides being present in oak-pine forest, <1,400 m elevation. Nine endemic species inhabited oak-pine forests, five were in oak forests, four were in halophytic communities, cool conifer forests, and mesic conifer forests, three were in xeric conifer forests and alpine meadows, two were on xeric scrubland, and one was in rosetophyllous scrubland. Of the endemic legumes, 14 species were herbaceous, 5 were shrubs, and 1 was a tree. Most endemic species were in three genera: Lupinus (5 species), all in oak, oak-pine, or conifer forests; Dalea (4), in rosetophyllous scrubland, xeric pine forest, and halophytic communities; and Astragalus (4), restricted to oak-pine forests and alpine meadows.

The four species endemic to alpine meadows were Lupinus (2), Astragalus (1), and Trifolium (1). All five shrubby endemic legumes (Dalea capitata var. lupinocalyx, D. gypsophila, D. radicans, D. uniflora, and Sophora juanhintoniana) were in semi-arid climates, occupying the rosetophyllous and xeric scrublands, halophytic grasslands, and xeric conifer forests.

Similarities Among Communities--The heterogeneous physiography of the study region, from low plains to high peaks (250-3,650 m elevation), dramatically influenced vegetational composition and environmental climatic conditions. Contrasting changes of vegetation and patterns of diversity are evident at different elevations. Analogous to other plants, legumes respond to fluctuations in these abiotic factors, showing particular distribution patterns within specific areas. Some are restricted to particular sites, such as calcareous soils (e.g., Dalea, Astragalus, and Hoffmannseggia) or high elevations in a temperate climate (Astragalus, Lupinus, and Vicia), or low elevations (Diphysa microphylla, Ebenopsis ebano, and Acacia) and dry climates (Acacia).

[FIGURE 3 OMITTED]

In our study, three assemblages of plant communities were recognized based on diversity of legumes. The dendrogram of plant communities (Fig. 3) showed a correlation of r = 0.83, with a cophenetic correlation coefficient of r = 0.81.

Group I (Fig. 3) had two subgroups, including tropical and subtropical scrublands and warm-cold temperate woodlands. Subgroup IA was characterized by tropical and subtropical scrublands including 1) Tamaulipan thornscrub and 2) piedmont scrub. Both communities were adjacent to each other, occupying semi-calid and semi-dry climates at low elevations (150-750 m). This subgroup has a high predominance of shrubby and thorny mimosoids, and herbaceous caesalpinioids and papilonoids. All 4 species of Prosopis, 12 species of Acacia,7 of Mimosa, and several species of Dalea and Senna were distributed mainly in these lowlands. Taxa restricted to subgroup 1A were Acaciella angustissima var. leucothrix, Acacia schaffneri var. bravoensis, Acacia schaffneri var. schaffneri, Acacia greggii, Astragalus emoryanus var. emoryanus, Caesalpinia caudata, Caesalpinia mexicana, Dalea laniceps, Desmanthus pringlei, D. glandulosus, Ebenopsis ebano, Galactia wrightii, Lespedeza repens, Neptunia pubescens var. microcarpa, Pomaria wootonii, Prosopis reptans var. cinerascens, and Rhynchosia difformis.

Subgroup IB (Fig. 3) included four communities: oak forest, oak-pine forest, mesic conifer forest, and cool conifer forest. All were along mountain ranges of the Sierra Madre Oriental in the most humid and coldest areas, such as high mountains peaks, cliffs, and gullies. Communities of this subgroup harbored the richest diversity, mainly concentrated in oak forests (111 species), oak-pine forests (125), and mesic conifer forests (92). Most species in this subgroup were Papilionoideae, leading in diversity with 47 genera and 145 species. Desmodium (13 species), Dalea (12), Phaseolus (9), Crotalaria (8), Lupinus (6), Vicia (6), Astragalus (5), and Rhynchosia (4) were prominent in these communities. Moreover, genera such as Amicia, Amphicarpaea, Canavalia, Clitoria, Lathyrus, Lotus, Lupinus, Myrospermum, and Orbexilum were restricted to these communities. The 9 genera and 25 species of Mimosoideae were distributed in these high elevations and cool climates, dominated by Acacia (9 species), Mimosa (4), and Desmanthus (3). Only one species of Caesalpinioideae, Gleditsia triacanthos, was restricted to these communities that were associated with oak-pine forests (particularly Quercus greggii-Pinus cemborides-Juniperus deppeana forests) in the northern portion of the study region (Sierra de Lampazos, Nuevo Leon; Estrada et al., 2002). Compared to subgroup IA, subgroup IB had fewer genera (19) and species (41) of papilionoids. However, both subgroups shared the same diversity of herbaceous genera; Lupinus (5 species), Phaseolus (3), Vicia (4), Desmodium (4), Dalea (3), Trifolium (3), Medicago (2), Lathyrus (2), and Cologania (2).

Group II (Fig. 3) included species of the Mexican High Plateau and those inhabiting arid zones of the Sierra Madre Oriental at 1,400-1,900 m elevation. These regions were occupied mainly by woody and scrubland communities, including chaparral, xeric conifer forests, rosetophyllous scrublands, xeric scrublands, and halophytic grasslands. Based on similarities in composition of the leguminous flora, Group II encompasses three subgroups: subgroup IIC, species of chaparral and xeric conifer forests; subgroup IID, species occurring in rosetophyllous and xerophytic scrublands; and subgroup IIE, species distributed in most of the fragmented halophytic communities, mainly dominated by grasses. Although members of all three subfamilies occurred in subgroup IIE, diversity of legumes was lower than in other plant communities. The most diverse genera were Dalea (14 species), Acacia (5), Mimosa (4), Bauhinia (4), Astragalus (4), and Desmanthus (3), and just one climber, Cologania angustifolia, occurred in these communities. Rosetophyllous and xeric scrublands embraced the most distinctive communities in the highland plains in northeastern Mexico; they represent most species of mimosoids and almost one-half of the caesalpinioids occurring in all other communities. In contrast with group I and its subgroups, fewer genera of papilionoids (14) occurred in these communities. However, Dalea (11 species) and Astragalus (5) had the greatest diversity.

Halophytic communities clearly were distinct from the other two subgroups (IIC and IID). These occurred as patches on plains or intermountain valleys, and were confined to deep, white, non-rocky, chalky soils, at elevations of 1,550-1,850 m. With the exception of subalpine and alpine meadows, these halophytic grassland communities had the lowest diversity of legumes. Only species of Dalea and Sophora were restricted to these gypsum-soil communities.

Group III (Fig. 3) of alpine and subalpine vegetation included legumes that occurred in all three alpine meadows: Cerro El Potosii, Cerro El Viejo, and Cerro Pefia Nevada, representing the highest peaks in northeastern Mexico (3,500-3,750 m). These alpine meadows were characterized by low temperatures and dwarf forms of plants. All legumes were in the Papilionoideae, represented by six genera: Astragalus (2 species), Lathyrus (2), Lupinus (2), Vicia (2), Cologania (1), and Trifolium (1; T. schneideri was reported by McDonald, 1993). All were species restricted to northeastern Mexico, and three were endemics (Lupinus cacuminis, L. texensis, and Trifolium schenideri) to these alpine meadows.

Discussion--Discontinuities in topography, soils, variable climatic regions, and different elevational gradients have influenced structure and composition of vegetation in northeastern Mexico (Rojas-Mendoza, 1965; Rzedowski, 1978). Plants such as legumes are distributed along these geographic and climatic variations (Estrada and Marroquiin, 1991). Our results demonstrate that most species of cesalpinioids and mimosoids are distributed in areas with warm-humid climates on plains or low mountains, associated with scrublands of varying heights. In contrast, most papilionoids occurred in temperate climates, associated mainly with montane forests.

Analysis of similarity of legumes present in plant communities in our study area demonstrated low-to-medium levels of similarity among communities. The S0rensen index generally was 20-30% when comparing Groups I-III, but reached 35 and 40%, respectively, when comparing among subgroups of Groups I and II. Group I was comprised of eastern tropical and subtropical scrublands that clearly were connected to vegetation in lowlands near the Gulf of Mexico (seasonally dry tropical forests), and to a lesser extent, this group was associated with temperate forests. According to Lavin et al. (2004) and Lavin (2006), these scrublands are related to seasonally dry tropic forests, and often conceal sister species whose recent common ancestry traces back in time at least several million years. All coniferous forests, except for xeric coniferous forest, assembled together in Group I. Group I was the most speciose and contained nine endemics, sharing three more with the alpine group. Group II occupied a more central and western distribution with a floristic composition perhaps more related to vegetation of the Mexican Central Plateau, the Chihuahuan Desert communities, and the Great Plains. Within Group II, two large subgroups were identified. One linked species comprising chaparral and xeric pine forest, other species that grow in more arid environments such as in rosetophyllous and xeric scrublands, and the second subgroup brought together species occurring in the semi-isolated halophytic communities. Halophytic communities, although clustered with assemblages of Group II, shared endemic species with mesic and cool forests grouped in subgroup IB. Group III was composed of subalpine and alpine vegetation made up of frost-tolerant species, and some narrow endemics. Of the 10 species of legumes present in this group, three are narrow endemics. McDonald (1993) considered that these isolated patches in northeastern Mexican were more related to alpine meadows of the southern Rocky Mountains than to those in southern Mexico.

Overall, the study area contains 259 species of legumes, of which 18 are endemic to northeastern Mexico, and 3 are narrow endemics. Such a level of endemism (8.1%) is surprisingly high if we compare it to the estimate of 6.2% by Sousa et al. (2004) for endemic legumes in the state of Oaxaca. This unexpected level of endemism and groupings of assemblages raise concerns about their origins and relationships; further investigation integrating more variable floristic elements is needed. However, given the anthropogenic changes that impact most of these communities, the question to address is how many of these communities and their members will survive such disturbance in the future.

We thank Consejo Nacional de Ciencia y Tecnologiia (grant 34033-V) and Programa de Apoyo a la Investigacion Cientifica y Tecnologica (Universidad Autonoma de Nuevo Leoi n). We thank M. Sousa Sainchez and L. Torres-Colin at Universidad Nacional Autonoma de Mexico (MEXU) for her curatorial work and taxonomic assistance with Lonchocarpus and Desmodium, respectively. We are also grateful to C. Yen Mendez, M. A. Gonzalez Botello, G. Cavazos G., J. Luna Zuniga, and M. Barba Platas by their participation in fieldwork. L. Rico Arce and M. Lavin generously provided relevant bibliography. We thank J. K. Bush, J. Sprent, and one anonymous reviewer for their comments and review of the manuscript.

Submitted 20 February 2009. Accepted 14 October 2009.

Associate Editor was Janis K. Bush.

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Eduardo Estrada C., * Alfonso Delgado-Salinas, J. Angel Villarreal Q., Laura Scott M., Cesar Cantu A., and Jaime Garcia P.

Facultad de Ciencias Forestales, Universidad Autonoma de Nuevo Leon, Km 145 Carretera National 85, Apartado Postal 41, C.P. 67700 Linares, Nuevo Leon, Mexico (EEC, LSM, CCA, JGP)

Universidad National Autonoma de Mexico, Instituto de Biologia, Apartado Postal 70-233, Delegation Coyoacan, C.P. 04510, Mexico, Distrito Federal, Mexico (ADS)

Departamento de Botanica, Universidad Autonoma Agraria Antonio Narro, Saltillo, Coahuila, C.P. 25315, Mexico (JAY)

* Correspondent: aeduardoestradac@prodigy.net.mx
Table 1--Wild genera, species, and endemic species, and their
percentages for three subfamilies of legumes in northeastern Mexico.

                   Number                   Number
                     of      Percentage       of
Subfamily          genera     of genera     species

Caesalpinioideae     13         16.5          39
Mimosoideae          14         17.7          45
Papilionoideae       52         65.8          175
Total                79          100          259

                                   Number      Percentage
                   Percentage    of endemic    of endemic
Subfamily          of species      species       species

Caesalpinioideae       15             1            4.8
Mimosoideae           17.5            1            4.8
Papilionoideae        67.5           19           90.4
Total                  100           21            100

FIG. 2--Total number of species representing the
five main biological forms of legumes in northeastern
Mexico. Number of species within each biological form
is shown above each bar.

Herbaceous          123
Non-thorny shrubs    55
Climbers             43
Thorny shrubs        29
Trees                 8
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Author:Estrada C., Eduardo; Delgado-Salinas, Alfonso; Villarreal Q., J. Angel; Scott M., Laura; Cantu A., C
Publication:Southwestern Naturalist
Article Type:Report
Geographic Code:1MEX
Date:Sep 1, 2010
Words:4736
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