Bird diversity and conservation of Alto Balsas ( Southwestern Puebla ) , Mexico

Knowledge of the composition of the bird community in Alto Balsas (southwestern Puebla, Central Mexico) is needed for management programs aiming at protection and conservation of bird species and their habitats I studied sites with tropical deciduous forest. Data were obtained during 1666 hours of field work in 238 days from March 1998 to September 2000. Six permanent transect (3.5 km long and 100 m wide; 30 to 40 ha in each transect) were used to determine species richness in the study sites. The Shannon-Wiener diversity index was calculated for each site and Sorensen’s index was used to assess similarity between sites. One-way analysis of variance was used to test for differences between sites in species richness and diversity values. A total of 128 species were recorded, Tepexco (n = 75, H ́= 3.76) and Puente Márquez (n = 61, H ́= 3.62) were the sites that showed the greatest specific richness and diversity. However, species richness and diversity seasonally patterns were similar among sites (ANOVA p > 0.05), with highest diversity during the rainy season. Most species were resident; 42 were migrants. The avifauna was represented by 30 species associated with tropical deciduous forest and 12 from open habitats or heavily altered habitats. Insectivores were the best represented trophic category, followed by carnivores and omnivores. Rev. Biol. Trop. 55 (1): 287-300. Epub 2007 March. 31.

Dramatic reduction and fragmentation of forest cover in several parts of the world have prompted many to ask what the impacts of such changes are on animal abundance, species richness and community dynamics (Faaborg et al. 1995, McGarigal andMcComb 1995).Forest fragmentation in the Neotropical region has been considered an important force in the loss of biodiversity (Bierregaard and Lovejoy 1989).Decreases in the number of bird species and changing avifaunal composition have been documented by many works (Bierregaard 1990, Aleixo andVielliard 1995).The regulation of diversity and abundance in animal communities has intrigued ecologist for many years, but their study has evoked as much controversy as consensus (MacArthur and Wilson 1967).Many studies have assumed that the community is in equilibrium, and many of them sought to support some favored ecological process rather than weighing several to determine their relative importance (Wilson and Comet 1996).Monitoring temporal changes of avifauna can provide valuable information on factors influencing population dynamics, interactions, community structure, and conservation (Ornelas et al. 1993).Seasonal changes in abundance and number of species have been studied in several temperate avian communities (Anderson et al. 1981, Best 1981), but rarely in tropical regions (Karr 1981, Blake 1992, Blake and Loiselle 2000).
The Alto Balsas region is located in central Mexico (Tlaxcala, Puebla, Morelos and Guerrero states), south of the mountainous Trans-volcanic belt.It runs west to east over a vast portion of relatively flat terrain, and occurs mostly below 1000 m (except on isolated peaks; Guizar andSánchez 1991, WWF 2001).The Balsas River and its drainage basin delineate the regions eastern boundary, while the mountains of Sierra Madre del Sur mark the western boundary along the Pacific coast.The Balsas basin has been also termed the "Balsas Depression" (because it forms a valley descending down to 200 m) in the west.The northern side of the depression is a plateau (containing the highest elevations) that reaches 1000 m above sea level, with few, scattered peaks at 2000 m (WWF 2001).In terms of the fauna, the Balsas dry forest is considered as a zone with high fauna diversity (e.g., mammalian, papilionid butterflies, birds and herpetofauna; Challenger 1998, Escalante et al. 1998).

Study site:
The study was conducted in sites of Alto Balsas in the southwestern Puebla (18°39´N, 98°58´W) in Central Mexico (Fig. 1, Table 1).Altitudinal range is from 800 to 1500 m a. s. l. (Table 1).The climate is tropical subhumid, with a dry season (that can last up to eight months) in which most or all trees lose their leaves and mean annual temperature is 23 °C.The precipitation levels are always below 1200 mm/year (INEGI 1987, Guizar andSánchez 1991).The study area is characterized by the tropical deciduous forest associated with secondary forest, riparian vegetation (gallery forest), cattle pastures, agricultural fields and suburban zones.Some species common to tropical deciduous forest are Bursera morelensis, B. fagaroides, B. grandifolia, Ficus sp., Lysiloma sp., Ipomomoea sp., Pseudobombax palmeri, Ceiba parvifolia, Prosopis laevigata, Mimosa luisana and Erythryna sp.(Rzedowski 1978, INEGI 1987).Arid tropical scrub is also common element of this community, principally giant columnar cacti (Pachycereus weberi, P. dumortieri, Neobuxbaumia tetetzo and Stenocereus stellatus).The herbaceous stratum is poorly developed, but species such as Bouteloua curtipendula, B. rothrockii and Hilaria semplei can be found.The isolation of the Balsas dry forests from other forests of its kind has promoted the diversification of many taxa, resulting in a high number of endemic species.For this reason, this is one of the most studied and most appreciated regions in terms of its value for biological conservation (Escalante et al. 1998).
Data birds: Bird surveys were conducted between March 1998 and September 2000.I used a transect method (Emlen 1971) to conduct monthly censuses in each site: San Isidro, Jolalpan, Los Linderos, Santiago Mazatla, Santa María Xuchapa, Puente Marquez and Tepexco (Table 1).A total of 35 transect (five permanent transect for each site; 3.5 km long) were used to determine species richness in the study sites.I recorded each bird seen or heard within the survey area during each survey.A complete daily census along a transect consisted of five surveys: three in the morning (0700-1100) and two in the evening .Each transect was surveyed where the tropical deciduous forest was associated with others types of vegetation (secondary forest, cattle pastures, arid tropical scrub, agricultural fields and riparian vegetation) by determining differences on species composition between them.Scientific nomenclature order follows American Ornithologist's Union check-list (1998).
Seasonal variation was determined following criteria: winter visitor (non-breeding visitor present during the northern winter), summer resident (breeds in the region, but is present only for a period during the northern summer), transient (non-breeding visitors only present during spring and/or autumn migration), resident (breeds and resides within its range throughout the year) and occurrence (non-breeding, includes vagrant and winter records; Howell and Webb 1995).Relative abundance (sense, Stiles 1983, Arizmendi et al. 1990, Ramírez-Albores and Ramírez 2002): abundant (total of 40 or more individuals recorded daily), common (17 to 39 individuals recorded daily), scarce (11 to 16 individuals recorded), irregular (five to ten individuals The feeding category assigned to each species was determined according to the food most often eaten and literature data: insectivores, frugivores, nectarivores, carnivores, granivores, omnivores, granivore-insectivores (mixed diet with a higher proportion of seed), insectivore-frugivores (mixed diet with a higher proportion of insects), granivore-insectivore-frugivores (mixed diet), carnivore-insectivore-frugivores (mixed diet) and carnivore-insectivores(mixed diet with a higher proportion of small vertebrates).
Shannon-Wiener diversity index (H = -∑ p i ln p i ) was calculated for each site (Magurran 1988).Similarity between sites, using the Sorensen's index of similarity [IS =2j / (a + b)] where j is the number of species common to both sites, a is the number of species in site A, and b is the number of species in site B. It ranges from 0-1 with increasing similarity of the two sites (Magurran 1988).One-way analysis of variance (ANOVA) was used to test for differences between sites in species richness and diversity values.

RESULTS
A total of 128 species grouped into 34 families were recorded at the area during 1666 hours of field work during 238 days (Appendix 1).The Tyrannidae family shows the highest species richness in the study sites (17 species), followed by Icteridae (10 species) and Parulidae (8 species) (Appendix 1).
Overall species richness varied from 39 to 75, while overall diversity values ranged from 2.84 to 3.76 (Table 2).The fewest diversity were found in Santiago Mazatla (H´= 2.60) and the most in Tepexco (H´= 3.20) in the dry season.In the rainy season, the fewest diversity were found in Santiago Mazatla (H´= 2.89) and the most in Tepexco (H´= 3.19) and Jolalpan (H´= 3.31).However, species richness and the diversity values for the sites were seasonally similar (ANOVA, p>0.05); with highest diversity during the rainy season (Table 2).The similarity of species composition between sites indicates that there was a tendency for similar habitats to present similar species composition (Table 3).The highest similarity indexes were for Puente Marquez-Jolalpan (0.84) and the smallest similarity was for Tepexco-Santiago Mazatla (0.57).
Of the species recorded in this study, 86 species were residents, and the remaining of the In the habitat selection, 30 species were recorded in the tropical deciduous forest, 12 in open habitats or heavily altered habitats, eight aquatics, four in riparian vegetation and four aerial, of this group of species, only were recorded in these habitats (Appendix 1).The remaining species were detected in two or more habitats.Insectivores were representing by the greatest number of species, followed by carnivores and omnivores (Appendix 1).Granivores and nectarivores were representing by few species in all sites.Many birds occur in the rainy season (July-October), when insects and fruits are most abundant.

DISCUSSION
The 128 bird species recorded in this study represent about 26% of the species in Puebla (Rojas 1995, reported 481 species to Puebla) and 12% of the birds of Mexico (Arizmendi and Marquez-Valdelamar 2000).This study has shown that study sites in Alto Balsas supports a high diversity of birds.Factors that contribute to determining avian diversity and abundance can be sorted into two levels, which are not entirely independent (Brown and Maurer 1987).Furthermore, the area is influenced for two biotic provinces: Trans-volcanic belt and Balsas Depression that presents a topographic complexity, and this to help to capacity of movements of the birds (Escalante et al. 1998).
The avifauna in the area is a speciesrich as other similar tropical deciduous forest areas in Mexico (Chamela-Cuixmala in Jalisco; Arizmendi et al. 1990, Ornelas et al. 1993), owing to that many species are associated with the tropical deciduous forest corridor and have continuous distributions from northern Sonora, Mexico to Central America (Arizmendi et al. 1990, Ornelas et al. 1993).Twenty-nine species encountered in this study had not been recorded previously for the study region (Rojas 1995, Feria 1997, Ramírez-Albores 2000).Of these, three were new recorded for Puebla: Dendrocygna autumnalis, Egretta thula and Parabuteo unincinctus (Rojas 1995).
Seasonal changes in richness and total number of species may be due to resident species joining during the dry season only, the absence of summer visitors during the dry season, and seasonal variation in frequency with which some species associated (Maldonado-Coelho and Marini 2004).I expected higher bird diversity in more diverse sites but my results contradict this expectation.The winter distributions of most western North American Neotropical migratory land bird species are centered in western Mexico.Several studies have demonstrating that many birds carry out seasonal movements relationships with the rainy seasons, probably in function of the availability variation of food resources (Powell 1989, Levey and Stiles 1992, Ornelas et al. 1993), habitat structure and climatic conditions (Malizia 2001).Habitats occupied by many migrants in winter, the density and proportion of migrants in most habitats, the diversity of migrants and residents that co-occur in flocks, the extent of participation in flocks by local avifauna and the proportion of migratory species that participates are all unique ornithological features of western Mexico (Hutto 1984).Behavioral some migratory of the birds is owing to that follow the phenology of resources that they use (Ornelas and Arizmendi 1995).This pattern permitted the birds proposed the dependency different types of resources requires: capacity to colonize new habitats, mobility to the able to follow changes in resource abundance, knowledge of the changes in resource in the landscape and the spatial distribution of these resources (Ornelas and Arizmendi 1995).
Tropical forest avifauna typically are characterized by the presence of many rare species (Karr et al. 1990, Terborgh et al. 1990, Loiselle and Blake 1992) that will be affects to food resources, structure and complexity of habitat or to the spatial and temporal availability of resources, indicated that communities are very inequality.However, the number of abundant species is very low, but these species have a high ecological success, and determining the conditions of the entailed species a theirs; established a sui generis feature of the communities, this is that include few abundant species and many rare species (Krebs 1978).Species locally abundant on average tended to be more widespread than locally rare species.This is also a consistent trend among birds (Gaston 1996).However this apparent correlation may be influenced by the higher overall detectability of common species.
Rapid deforestation in the neotropics has undoubtedly had an impact on birds.The recent increase of second growth forest, cattle pastures and agriculture fields has resulted in an increase in the abundance of species dependent upon these habitats.Conservation efforts often are focused on regions or sites that support threatened, endemic, or rare species.Thus, knowledge of the distribution patterns of threatened species can be an important argument for protection of different areas (Wege and Long 1995).
This study showed that there is no marked difference in bird species diversity between dry and rainy seasons in the study sites in Alto Balsas.The pattern of distribution could also be due to local patchiness caused by the fragmentation of historically contiguous habitat due to agricultural development in the sites.Knowledge of the composition of the bird communities of the region and the specific or temporary uses which the different species make of the region allowed provide elements witch can be included or modified in a management program, and in this was the protection and conservation of the species and their habitat will be a success.

ACKNOWLEDGMENTS
I would like to thank Museo de Zoología (Facultad de Estudios Superiores Zaragoza, Universidad Nacional Autónoma de México).I sincerely thank Alfredo Bueno for comments and suggestions during the field work.I thank Guadalupe Ramírez, Eduardo Tepale, Ayerím Lopez and Alejandro Abundis for their assistance in data collection.
Check-list of bird species in the study sites of Alto Balsas (southwestern Puebla), Mexico * Endemic and cuasiendemic bird species in the study area (Navarro and Benitez 1993).
APPENDIX 1 (Continued) Check-list of bird species in the study sites of Alto Balsas (southwestern Puebla), Mexico

TABLE 1
Study sites in Alto Balsas (southwestern Puebla), Mexico

TABLE 2
Bird species richness and diversity values for study sites in Alto Balsas (southwestern Puebla), Mexico

TABLE 3
Matrix representing the similarity values between study sites in Alto Balsas (southwestern Puebla), Mexico Check-list of bird species in the study sites of Alto Balsas (southwestern Puebla), Mexico