- Email: [email protected]
Rodent communities in two natural and one cultivated “nopaleras” (Opuntia spp.) in north-eastern Jalisco, Mexico
ARTICLE IN PRESS Journal of Arid Environments
Journal of Arid Environments 67 (2006) 428–435 www.elsevier.com/locate/jnlabr/yjare
Rodent communities in two natural and one cultivated ‘‘nopaleras’’ (Opuntia spp.) in north-eastern Jalisco, Mexico M.E. Riojas-Lo´pez Departamento de Ecologı´a, Centro Universitario de Ciencias Biolo´gicas y Agropecuarias, Universidad de Guadalajara. Km. 15.5 carr. Nogales, C.P. 45100 Zapopan, Jalisco, Me´xico Received 19 October 2005; received in revised form 10 December 2005; accepted 24 February 2006 Available online 18 April 2006
Abstract In north-eastern Jalisco one of the most notorious original habitat features were xerophitic shrubs formed of different types of nopaleras (communities of flat-stemmed Opuntia cacti). Expansion of human activities have reduced these habitats but, conversely, perennial agroecosystems of domesticated varieties of native Opuntia spp. have been established. During 1997 I conducted a study to describe the rodent communities in two natural nopaleras, one arboreal and one arbustive, and one fruit-oriented cultivated nopalera. I recorded 14 rodent species at the three sites. There were no significant differences in total and seasonal abundances between sites, although some rodent species exhibited site-specific preferences and their abundances differed significantly between sites. Species richness ranged from 10 to 14. The arboreal nopalera had a significantly lower species richness than the arbustive and the cultivated nopaleras. The principal component analysis (PCA) clearly separated the arboreal nopalera from the other two based on the vegetative structure. Although agroecosystems have been considered as low diversity habitats, my results showed that fruit-oriented, cultivated nopaleras in north-eastern Jalisco create a habitat mosaic that is used by rodent species from different guilds. This suggests that these agroecosystems can contribute to the maintenance of local and regional rodent biodiversity in this severely fragmented region. r 2006 Elsevier Ltd. All rights reserved. Keywords: Fruit-oriented nopalera; Opuntia community; Llanos de Ojuelos; Rodent diversity
Tel: +52 33 37 77 11 56; fax: +52 33 37 77 11 59.
E-mail address: [email protected]. 0140-1963/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.jaridenv.2006.02.020
ARTICLE IN PRESS M.E. Riojas-Lo´pez / Journal of Arid Environments 67 (2006) 428–435
429
1. Introduction North-eastern Jalisco lies within the biogeografic subprovince ‘‘Llanos de OjuelosAguascalientes’’, which has a semi-arid climate. One of the most notorious orginal habitat features of this region were ‘‘nopaleras,’’ xerophytic shrubby communities composed mostly by flat-stemmed Opuntia cacti (individual Opuntia plants are known as ‘‘nopal’’ in singular and ‘‘nopales’’ in plural). The complex plant association of these nopaleras offered a variety of microhabitats that provided food and shelter for a considerable number of native vertebrates (Yeaton and Romero, 1986; Gonza´lez-Espinosa, 1999; Mellink and Riojas-Lo´pez, 2002; Riojas-Lo´pez and Mellink, 2005), especially small mammals and birds (Gonza´lez-Espinosa and Quintana-Ascencio, 1986). During the last several decades large areas of natural nopaleras have been reduced or fragmented through their conversion to dryland agriculture, their use as rangeland, and through human settlement (Challenger, 1998; PRODEFO, 1999), changes that probably had negative impacts on their native flora and fauna. However, re-establishment of natural nopaleras for conservation purposes does not seem viable. Conversely, over the last two decades there has been a widespread establishment of fruitoriented cultivated nopaleras, based on domesticated varieties of nopal. In north-eastern Jalisco, the surface of fruit-oriented cultivated nopaleras increased from 1900 ha in 1990 to 2600 ha in 2000 (F. Torres, com. pers.). These perennial farming systems, subject to only sporadic agricultural practices, play an important role for the inhabitants of the region providing both food and fodder (Granados and Castan˜eda, 1991). Although agricultural systems and related practices often have diminished biodiversity (Benton et al., 2003; Hietala-Koivu et al., 2004), some traditional rustic agricultural systems play an important role in biodiversity conservation, and provide suitable habitat for many species (Reichhardt et al., 1994; Gallina et al., 1996; Moguel and Toledo, 1999; Riojas-Lo´pez and Mellink, 2005). Due to the increase of fruit-oriented, cultivated nopaleras in north-eastern Jalisco it was important to assess how these man-made ecosystems contributed to the overall diversity in the region. The study of rodent communities may be especially useful to assess this contribution, as their communities respond rapidly to habitat changes, although they in turn can affect the structure and composition of vegetation (Brown and Heske, 1990; Chew and Whitford, 1992; Andersen and Kay, 1999). Cultivated nopaleras, being rustic, perennial systems, under low-impact agricultural management, can be hypothesized to be as diverse as natural ones. To begin to explore this issue, the purpose of this study was to describe and compare the composition and abundance of rodent communities in two natural nopaleras with different plant structure (arboreal and arbustive) and a cultivated one in north-eastern Jalisco, Mexico.
2. Materials and methods 2.1. Study sites The study sites were near the town of Ojuelos de Jalisco, Jalisco, Mexico (211330 –211000 N1011300 –1011560 W) in the Llanuras de Ojuelos-Aguascalientes (Fig. 1). This area has a semi-arid climate, with a mean annual precipitation of 400–500 mm, 90%
ARTICLE IN PRESS 430
M.E. Riojas-Lo´pez / Journal of Arid Environments 67 (2006) 428–435
22°15' Zacatecas
22°00'
San Luis Potosi
Aguascalientes Ojuelos de Jalisco
21°45'
Guanajuto 21°30'
102°15'
102°00'
101°45'
101°30'
101°15'
101°00'
Fig. 1. Geographical location of Ojuelos de Jalisco, Jalisco, where the rodent communities of three nopaleras were studied in 1997.
of which falls from June through September. The mean annual temperature is 16–18 1C, with a minimum in January (2 1C) and maximum in May (32 1C) (INEGI, 2003). The area is an extended high plateau (1800–2300 m.a.s.l.) of valleys intersected by smooth hills. Soils are mostly shallow, of a sandy-clay texture, derived from igneous rocks, and underlain by a silica hardpan. Soil pH varies from 5 to 7, and organic matter content from 0.8% to 1.8%. The native vegetation is composed mainly of isolated patches of shrubby nopaleras (O. robusta, O. joconostle and O. durangensis), woody perennial legumes (huizache, Acacia spp., and garabatillo, Mimosa sp.), and grasses (Bouteloua spp., Aristida spp., Muhlenbergia spp.). In some areas of the region, arboreal Opuntias (O. streptacantha, O. leuchotricha, O. hyptiacantha and O. chavena) dominate the landscape and together with huizache and garabatillo form dense thorny associations. Some 80% of the area is intensively grazed or under cultivation (PRODEFO, 1999). During 1997, I surveyed three nopaleras. The following vegetation description is based on the aereal plant cover in ten 3 10-m quadrats. One of the sites was an arboreal nopalera, ‘‘Matancillas’’, (211550 1900 N, 1011380 1300 W, 2160 m asl) of ca. 3 ha, surrounded by cultivated maize and bean fields. This community was dominated by arboreal species of opuntias (O. streptacantha, O. chavena and O. leucotricha). This site had a dense plant cover and a well-stratified vegetation. Herbs accounted for 35% of the total plant cover and the ground beneath the opuntias was mostly covered by litter (40% of the total ground). The second site, ‘‘La Campana’’ (211520 1200 N, 1011370 5100 W, 2210 m.a.s.l.) was an open, shrubby native nopalera of ca. 4 ha, with a few isolated clumps of arboreal nopales (O. streptacantha and O. leucotricha). The vegetation of this site was composed of short grasses with shrubby clumps of nopales composed by O. durangensis and O. robusta, legumes (Mimosa spp. and Dalea bicolor) and sangre de drago (Jatropha dioica), the herbaceous cover accounted for the 20% of the total
ARTICLE IN PRESS M.E. Riojas-Lo´pez / Journal of Arid Environments 67 (2006) 428–435
431
vegetal cover. The third site, ‘‘La Huerta’’ (211520 3200 N, 1011370 1600 W, 2290 m.a.s.l.), was a fruit-oriented, cultivated nopalera (O. megacantha var. c.v. naranjona), ca. 4 ha, planted in 1989 with plants spaced 3 m along rows that were 5 m apart. The herbaceous strata covered 30% of the ground, the shrubby strata was composed by the cultivated varieties of nopales. 2.2. Methods and data analysis I live-trapped rodents at the three described sites in February, April, July and November, 1997, except in February when La Huerta could not be sampled because of ongoing agricultural practices. Rodents were trapped using Sherman traps baited with oatmeal and vainilla extract in a 10 10 grid with lines and stations 8 m apart, for two consecutive nights, using one grid per site. All individuals captured were identified, marked numerically by toe clipping, and released at the site of capture. Species richness was considered as the number of species recorded at each study site on each sampling period. The sum of all different rodents captured in each visit was used as the best estimator of abundance. A two-way analysis of variance was used to compare rodent species richness and abundance between sampling sites and sampling periods. Tukey tests were perfomed when differences were found (Zar, 1999). These analyses were performed with ap0.05. Site and sampling periods were arranged through a principal component analysis (PCA) based on rodent abundances. 3. Results Fourteen different rodent species were recorded at the study sites. There were no significant differences in total and seasonal abundance of rodents per site or among sites. Some rodent species exhibited site-specific preferences and their abundances differed significantly between sites (Table 1). Reithrodontomys fulvenscens and Liomys irroratus Table 1 Mean and standart error of rodent species abundance at the natural and cultivated nopaleras (Opuntia spp.) in north-eastern Jalisco, Mexico, 1997 Species Liomys irrotatus Chaetodiphus nelsoni Perognathus flavus Dipodomys ordii Dipodomys phillipsi Chaetodipous hispidus Reithrodontomys megalotis Reithrodontomys fulvescens Peromyscus melanophrys Peromyscus difficilis Peromyscus gratus Peromyscus maniculatus Sigmodon fulviventer Sigmodon hispidus Species richness
Matancillas (n ¼ 4) a
22.574.73 4.570.57a 0.7570.47b 2.5071.50 0.00b 1.00 472.44b 46.25711.58a 1.00 6.2571.54 1.00b 0.00b 0.00b 0.00 6.7570.50a
La Campana (n ¼ 4) b
170.40 2.2570.75b 6.5071.70a 5.5072.06 10.7570.25a 0.00 972.67b 3.5070.64b 2.5070.64 8.7572.01 5.5072.06a 1.00b 0.00b 0.00 9.5070.50b
Values with different letter in the same row are statistically different (ap0:05).
La Huerta (n ¼ 3) b
0.6770.33 0.00b 1.6670.33b 3.3370.66 4.0070.57b 0.00 1872.00a 5.6672.18b 2.00 7.0072.08 3.00a 2.3370.33a 3.0070.88a 1.00 9.6670.66b
p 0.0047 0.0028 0.0343 0.2265 0.0001 — 0.0044 0.0144 0.0121 0.6040 0.0225 0.0003 0.0130 — 0.0034
ARTICLE IN PRESS 432
M.E. Riojas-Lo´pez / Journal of Arid Environments 67 (2006) 428–435
Fig. 2. Organization of three nopaleras and four sampling periods along the two first axis of a principal component analysis, based on the abundance of rodents in north-eastern Jalisco, Mexico, 1997.
were the most abundant species. In Matancillas they represented 80% of all individuals. At La Campana and La Huerta the abundance of individual species was more even than at Matancillas. Species richness varied from 10 to 14, and Matancillas had a lower species richness (pp0:0034) than La Campana and La Huerta. The first two axes of the PCA explained 43% and 35% of the total variation of the rodent community among sites. This analysis clearly separated Matancillas from La Campana and La Huerta (Fig. 2), which formed a single cluster, except for the November sampling period at La Campana which was intermediate.
4. Discussion and conclusions Although agroecosystems have been considered low diversity habitats, my results exhibited that this was not true in fruit-oriented cultivated nopaleras in north-eastern Jalisco. The rodent community species richness at the cultivated nopalera was comparable to that of the shrubby open nopalera at La Campana, and richer than the arboreal nopalera at Matancillas. The significant differences detected in abundances of individual rodent species were site-specific. Although Matancillas had the highest abundance, two species, L. irroratus and R. fulvescens, accounted of the 80% of its rodents. Both rodent species prefer grassy habitats with shrubs (Dowler and Genoways, 1978; Spencer and Cameron, 1982), which is concordant with my findings. Throughout the study I captured L. irroratus mostly beneath the arboreal nopales, where the ground was covered by a thick layer of litter, which seems to provied a suitable habitat for this species. R. fulvescens microsites had a better herbaceous cover than that for L. irroratus. The vegetation structure of Matancillas, defined by two strata (arboreal and herbaceous) made it a more homogenous habitat for rodents, which explains why the rodents captured at this nopalera were species that generally inhabit sites with dense plant cover and well stratificated vegetation. Overall, the organization of sites/period on the PCA graph is explained best by differences in the cover of herbs and litter, and was strongly related to the variation in abundance of rodent species that preferred dense cover and those that preferred more open habitats. The November sampling at both La Campana and Matancillas, separated from other periods at those sites reflected a heavy rain in October, whose effects were removed through agricultural practices at La Huerta.
ARTICLE IN PRESS M.E. Riojas-Lo´pez / Journal of Arid Environments 67 (2006) 428–435
433
According to site-specificity, the rodent communities in La Campana and in La Huerta could be divided in two groups: species that are found commonly in habitats of dense medium to tall herbaceous and shrubby cover, and those that preferred open spaces of short grassess intercepted with shrubby clumps. The first group included Reithrodontomys megalotis, Sigmodon fulviventer, S. hispidus, Peromyscus melanophrys and P. truei. The three former species are associated with grassy or grass-shrub habitats (Baker and Shump, 1978; Cameron and Spencer, 1981; Webster and Jones, 1982). P. melanophrys uses sites with dense growth of shrubs, whereas, in Mexico, P. gratus is found in a variety of habitats, including sites with dense growth of Opuntia cacti (Hoffmeister, 1981). In this study, all these rodent species were captured in traps located next to or beneath dense nopal clumps surrounded by abundant herbs. The second rodent group was composed by Dipodomys phillipsii, D. ordii and Perognathus flavus. These species are typically associated with short grassland with clumps of Opuntia cacti and other shrubby plants (Jones and Genoways, 1975; Bowers, 1982). The significantly higher species richness at La Campana and La Huerta, compared to Matancillas, was the result of a more spatially heterogeneous habitat, as habitat heterogeneity plays an important role in structuring rodent communities in desert systems (Rosenzweig and Winakur, 1969; Whitford, 1976; Heske et al., 1994; Mellink, 1995). Whereas La Campana had four vegetation layers (short and medium herbs, shrubs, and arboreal nopales) in La Huerta there were three layers (short and medium to tall herbs, and shrubby nopales), and in Matancillas, only two layers (short to medium herbs and arboreal nopales). Moreover, at La Campana, heavy grazing opened wide patches among the nopales but as cattle could not forage beneath the shrubby nopales, it left patches with dense herb cover interspread with the open spaces. On the other hand, the cultural practices at the nopal orchards consist of plowing between the rows, pruning of the Opuntia cacti pads and fertilizing with dry manure, every 3 or 4 years. These practices contribute to the maintenance of open spaces between the plants, but also allow the establishment of dense islands of herbs and low shrubs, which provide a variety of microsites, suitable for rodent species with different habitat requirements. This matrix of habitats within these sampling sites might have promoted the colonization by species with different requirements. Additionally, the feeding habits of the rodents themselves, especially of kangaroo rats, can influence the composition and structure of the plant communities in arid lands (Heske et al. 1993, 1994). The role of native rodents in the nopaleras of the region is unkonwn. In the Sonora Desert, small-scale indigenous agriculture increased plant diversity and formed a patchy habitat that favoured biodiversity (Nabhan et al., 1982; Mellink, 1985). Some other traditional agroecosystems such as shaded coffee agroforests play an important role in biodiversity conservation due to their structural complexity (Gallina et al., 1996; Moguel and Toledo, 1999). My results are concordant with the idea that, for rodents, environmental heterogeneity due to disturbance could be a key factor in promoting diversity (Mellink, 1985, 1991; Pardini, 2004). Although more research about other factors that determine the structure of rodent communities in cultivated nopaleras is necessary, current fruit-oriented, cultivated nopaleras in north-eastern Jalisco, create a habitat mosaic that is used by rodent species from different guilds through structurally diverse vegetal habitats and agricultural disturbance.
ARTICLE IN PRESS 434
M.E. Riojas-Lo´pez / Journal of Arid Environments 67 (2006) 428–435
The fruit-oriented cultivated nopaleras in north-eastern Jalisco, Mexico have three of the four conditions that define agroecosystems that might contribute to biodiversity conservation (Southwood and Way, 1970): (1) they are perennial farming systems that use domesticated varieties of native species; (2) the agricultural practices are sporadic; and (3) they seem to allow the establishment of a complex and diverse vegetation association of perennial and annual plants within the plots. These agricultural systems are an alternative habitat for some native species in this severely fragmented region and contribute to the maintenance of local and regional rodent biodiversity. They should not be overlooked as a mechanism to promote biological conservation, while allowing for economic activities to continue. Acknowledgements To Eric Mellink for statistical support and Mollie Harker for editorial assistance. To Adriana Gonza´lez-Dura´n who helped me during field work and to Rube´n Gonza´lez for allowed me to work in his property. To the Universidad de Guadalajara for financial support. References Andersen, M.C., Kay, F.R., 1999. Banner-tailed kangaroo rat burrow mounds and desert grassland habitats. Journal of Arid Environment 41, 147–160. Baker, R.H., Shump Jr., K.A., 1978. Sigmodon fulviventer. Mammalian Species 94, 1–4. Benton, T.G., Vickery, J.A., Wilson, J.D., 2003. Farmland biodiversity: is habitat heterogeneity the key? Trends in Ecology & Evolution 18, 82–188. Bowers, M., 1982. Foraging behavior of heteromyid rodents field evidence of resource partitioning. Journal of Mammalogy 63, 361–367. Brown, J.H., Heske, E.J., 1990. Temporal changes in a Chihuahuan Desert rodent community. Oikos 59, 290–302. Cameron, G.N., Spencer, S.R., 1981. Sigmondon hispidus. Mammalian Species 158, 1–9. Challenger, A., 1998. Utilizacio´n y Conservacio´n de los Ecosistemas Terrestres de Me´xico: Pasado, Presente y Futuro, Comisio´n Nacional para el Conocimiento y Uso de la Biodiversidad, Instituto de Biologı´ a, Universidad Nacional Auto´noma de Me´xico, Agrupacio´n Sierra Madre, S.C., Me´xico. Chew, R.M., Whitford, W.G., 1992. A long positive effect of kangaroo rats (Dipodomys spectabilis) on creosotebushes (Larrea tridentata). Journal of Arid Environment 22, 375–386. Dowler, R.C., Genoways, H.H., 1978. Liomys irroratus. Mammalian Species 82, 1–6. Gallina, S., Mandujano, S., Gonza´lez-Romero, A., 1996. Conservation of mammalian diversity in coffee plantations of Central Veracruz, Mexico. Agroforestry Systems 33, 13–27. Gonza´lez-Espinosa, M., 1999. Interacciones entre fenologı´ a, elementos bio´ticos y disturbio por pastoreo en las nopaleras del centro de Me´xico. In: Aguirre, R.J.R., Reyes, A.J.A. (Eds.), Memoria VIII Congreso Nacional y VI Internacional sobre Conocimiento y Aprovechamiento del Nopal. Editorial Universitaria Potosina, Universidad Auto´noma de San Luis Potosı´ , Me´xico, pp. 342–358. Gonza´lez-Espinosa, M., Quintana-Ascencio, P.F., 1986. Seed predation and dispersal in a dominant desert plant: Opuntia, ants, birds and mammals. In: Estrada, A., Fleming, T.H. (Eds.), Frugivores and Seed Dispersal. Dr. Junk Publishers, Dordrecht, pp. 273–283. Granados, S.D., Castan˜eda, P.A., 1991. El Nopal. Trillas, Me´xico. Heske, E.J., Brown, J.H., Mistry, S., 1994. Long-term experimental study of Chihuahuan Desert rodent community: 13 years of competition. Ecology 75, 438–445. Heske, E.J., Brown, J.H., Guo, Q., 1993. Effects of kangaroo rat exclusion on vegetation structure and plant species diversity in the Chihuahuan Desert. Oecologia 95, 520–524. Hietala-Koivu, R., Lankoski, J., Tarmi, S., 2004. Loss of biodiversity and its social cost in a agricultural landscape. Agriculture Ecosystems & Environment 103, 75–83. Hoffmeister, D.F., 1981. Peromyscus truei. Mammalian Species 161, 1–5.
ARTICLE IN PRESS M.E. Riojas-Lo´pez / Journal of Arid Environments 67 (2006) 428–435
435
Instituto Nacional de Estadı´ stica Geografı´ a e Informa´tica (INEGI), 2003. http://www.inegi.gob.mx/jalisco/ ojuelos.html Jones Jr., J.K., Genoways, H.H., 1975. Dipodomys phillipsii. Mammalian Species 51, 1–3. Mellink, E., 1985. Agricultural disturbance and rodents: three farming systems in the Sonoran Desert. Journal of Arid Environment 8, 207–222. Mellink, E., 1991. Rodent communities associated with three traditional agroecosystems in the San Luis Potosi Plateau, Mexico. Agriculture Ecosystems & Environment 33, 363–375. Mellink, E., 1995. Uso del ha´bitat, dina´mica poblacional y estacionalidad reproductiva de roedores en el Altiplano Potosino, Me´xico. Revista Mexicana de Mastozoologia 1, 1–8. Mellink, E., Riojas-Lo´pez, M.E., 2002. Consumption of platyopuntias by wild vertebrales. In: Nobel, P.S. (Ed.), Cacti: Biology and Uses. The University of California Press, California, pp. 109–123. Moguel, P., Toledo, V.M., 1999. Biodiversity conservation in traditional coffee systems of Mexico. Conservation Biology 13, 11–21. Nabhan, G.P., Rea, A.M., Reichardt, K.L., Mellink, E., Hutchinson, C.F., 1982. Papago influence on habitat and biotic diversity: Quitovac oasis ethnoecology. Journal of Ethnoecology 2, 124–143. Pardini, R., 2004. Effects of forest framentation on small mammals in an Atlantic Forest landscape. Biodiversity and Conservation 13, 2567–2586. Programa de Desarrollo Forestal de Jalisco (PRODEFO), 1999. Superficies de Recursos Forestales del Estado de Jalisco. Documento Te´cnico 21, Me´xico. Reichhardt, K.L., Mellink, E., Nabhan, G.P., Rea, A., 1994. Habitat heterogeneity and biodiversity associated with indigenous agriculture in Sonoran Desert. Etnoecolo´gica 2 (3), 21–34. Riojas-Lo´pez, M.E., Mellink, E., 2005. Potencial for biological conservation on man-modified habitats in northeastern Jalisco. Biodiversity and Conservation 14, 2251–2263. Rosenzweig, M.L., Winakur, J., 1969. Population ecology of desert rodent communities: habitat and environmental complexity. Ecology 50, 558–572. Spencer, S.R., Cameron, G.N., 1982. Reithrodontomys fulvescens. Mammalian Species 174, 1–7. Southwood, R.E., Way, M.J., 1970. Ecological background to pest management. In: Rabb, R.C., Guthrie, F.E. (Eds.), Concepts of Pest Management. North Carolina State University, Raleigh, NC, pp. 6–29. Webster, W.D., Jones Jr., J.K., 1982. Reithrodontomys megalotis. Mammalian Species 167, 1–5. Whitford, W., 1976. Temporal fluctuations in density and diversity of desert rodent populations. Journal of Mammalogy 57 (2), 351–369. Yeaton, R.I., Romero, M.A., 1986. Organization of vegetation mosaics in the Acacia schaffneri-Opuntia streptacantha association, southern Chihuahuan Desert, Mexico. Journal of Ecology 74, 211–217. Zar, J.H., 1999. Biostatistical Analysis, fourth ed. Prentice-Hall, Englewood Cliffs, NJ, USA.
Journal of Arid Environments 67 (2006) 428–435 www.elsevier.com/locate/jnlabr/yjare
Rodent communities in two natural and one cultivated ‘‘nopaleras’’ (Opuntia spp.) in north-eastern Jalisco, Mexico M.E. Riojas-Lo´pez Departamento de Ecologı´a, Centro Universitario de Ciencias Biolo´gicas y Agropecuarias, Universidad de Guadalajara. Km. 15.5 carr. Nogales, C.P. 45100 Zapopan, Jalisco, Me´xico Received 19 October 2005; received in revised form 10 December 2005; accepted 24 February 2006 Available online 18 April 2006
Abstract In north-eastern Jalisco one of the most notorious original habitat features were xerophitic shrubs formed of different types of nopaleras (communities of flat-stemmed Opuntia cacti). Expansion of human activities have reduced these habitats but, conversely, perennial agroecosystems of domesticated varieties of native Opuntia spp. have been established. During 1997 I conducted a study to describe the rodent communities in two natural nopaleras, one arboreal and one arbustive, and one fruit-oriented cultivated nopalera. I recorded 14 rodent species at the three sites. There were no significant differences in total and seasonal abundances between sites, although some rodent species exhibited site-specific preferences and their abundances differed significantly between sites. Species richness ranged from 10 to 14. The arboreal nopalera had a significantly lower species richness than the arbustive and the cultivated nopaleras. The principal component analysis (PCA) clearly separated the arboreal nopalera from the other two based on the vegetative structure. Although agroecosystems have been considered as low diversity habitats, my results showed that fruit-oriented, cultivated nopaleras in north-eastern Jalisco create a habitat mosaic that is used by rodent species from different guilds. This suggests that these agroecosystems can contribute to the maintenance of local and regional rodent biodiversity in this severely fragmented region. r 2006 Elsevier Ltd. All rights reserved. Keywords: Fruit-oriented nopalera; Opuntia community; Llanos de Ojuelos; Rodent diversity
Tel: +52 33 37 77 11 56; fax: +52 33 37 77 11 59.
E-mail address: [email protected]. 0140-1963/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.jaridenv.2006.02.020
ARTICLE IN PRESS M.E. Riojas-Lo´pez / Journal of Arid Environments 67 (2006) 428–435
429
1. Introduction North-eastern Jalisco lies within the biogeografic subprovince ‘‘Llanos de OjuelosAguascalientes’’, which has a semi-arid climate. One of the most notorious orginal habitat features of this region were ‘‘nopaleras,’’ xerophytic shrubby communities composed mostly by flat-stemmed Opuntia cacti (individual Opuntia plants are known as ‘‘nopal’’ in singular and ‘‘nopales’’ in plural). The complex plant association of these nopaleras offered a variety of microhabitats that provided food and shelter for a considerable number of native vertebrates (Yeaton and Romero, 1986; Gonza´lez-Espinosa, 1999; Mellink and Riojas-Lo´pez, 2002; Riojas-Lo´pez and Mellink, 2005), especially small mammals and birds (Gonza´lez-Espinosa and Quintana-Ascencio, 1986). During the last several decades large areas of natural nopaleras have been reduced or fragmented through their conversion to dryland agriculture, their use as rangeland, and through human settlement (Challenger, 1998; PRODEFO, 1999), changes that probably had negative impacts on their native flora and fauna. However, re-establishment of natural nopaleras for conservation purposes does not seem viable. Conversely, over the last two decades there has been a widespread establishment of fruitoriented cultivated nopaleras, based on domesticated varieties of nopal. In north-eastern Jalisco, the surface of fruit-oriented cultivated nopaleras increased from 1900 ha in 1990 to 2600 ha in 2000 (F. Torres, com. pers.). These perennial farming systems, subject to only sporadic agricultural practices, play an important role for the inhabitants of the region providing both food and fodder (Granados and Castan˜eda, 1991). Although agricultural systems and related practices often have diminished biodiversity (Benton et al., 2003; Hietala-Koivu et al., 2004), some traditional rustic agricultural systems play an important role in biodiversity conservation, and provide suitable habitat for many species (Reichhardt et al., 1994; Gallina et al., 1996; Moguel and Toledo, 1999; Riojas-Lo´pez and Mellink, 2005). Due to the increase of fruit-oriented, cultivated nopaleras in north-eastern Jalisco it was important to assess how these man-made ecosystems contributed to the overall diversity in the region. The study of rodent communities may be especially useful to assess this contribution, as their communities respond rapidly to habitat changes, although they in turn can affect the structure and composition of vegetation (Brown and Heske, 1990; Chew and Whitford, 1992; Andersen and Kay, 1999). Cultivated nopaleras, being rustic, perennial systems, under low-impact agricultural management, can be hypothesized to be as diverse as natural ones. To begin to explore this issue, the purpose of this study was to describe and compare the composition and abundance of rodent communities in two natural nopaleras with different plant structure (arboreal and arbustive) and a cultivated one in north-eastern Jalisco, Mexico.
2. Materials and methods 2.1. Study sites The study sites were near the town of Ojuelos de Jalisco, Jalisco, Mexico (211330 –211000 N1011300 –1011560 W) in the Llanuras de Ojuelos-Aguascalientes (Fig. 1). This area has a semi-arid climate, with a mean annual precipitation of 400–500 mm, 90%
ARTICLE IN PRESS 430
M.E. Riojas-Lo´pez / Journal of Arid Environments 67 (2006) 428–435
22°15' Zacatecas
22°00'
San Luis Potosi
Aguascalientes Ojuelos de Jalisco
21°45'
Guanajuto 21°30'
102°15'
102°00'
101°45'
101°30'
101°15'
101°00'
Fig. 1. Geographical location of Ojuelos de Jalisco, Jalisco, where the rodent communities of three nopaleras were studied in 1997.
of which falls from June through September. The mean annual temperature is 16–18 1C, with a minimum in January (2 1C) and maximum in May (32 1C) (INEGI, 2003). The area is an extended high plateau (1800–2300 m.a.s.l.) of valleys intersected by smooth hills. Soils are mostly shallow, of a sandy-clay texture, derived from igneous rocks, and underlain by a silica hardpan. Soil pH varies from 5 to 7, and organic matter content from 0.8% to 1.8%. The native vegetation is composed mainly of isolated patches of shrubby nopaleras (O. robusta, O. joconostle and O. durangensis), woody perennial legumes (huizache, Acacia spp., and garabatillo, Mimosa sp.), and grasses (Bouteloua spp., Aristida spp., Muhlenbergia spp.). In some areas of the region, arboreal Opuntias (O. streptacantha, O. leuchotricha, O. hyptiacantha and O. chavena) dominate the landscape and together with huizache and garabatillo form dense thorny associations. Some 80% of the area is intensively grazed or under cultivation (PRODEFO, 1999). During 1997, I surveyed three nopaleras. The following vegetation description is based on the aereal plant cover in ten 3 10-m quadrats. One of the sites was an arboreal nopalera, ‘‘Matancillas’’, (211550 1900 N, 1011380 1300 W, 2160 m asl) of ca. 3 ha, surrounded by cultivated maize and bean fields. This community was dominated by arboreal species of opuntias (O. streptacantha, O. chavena and O. leucotricha). This site had a dense plant cover and a well-stratified vegetation. Herbs accounted for 35% of the total plant cover and the ground beneath the opuntias was mostly covered by litter (40% of the total ground). The second site, ‘‘La Campana’’ (211520 1200 N, 1011370 5100 W, 2210 m.a.s.l.) was an open, shrubby native nopalera of ca. 4 ha, with a few isolated clumps of arboreal nopales (O. streptacantha and O. leucotricha). The vegetation of this site was composed of short grasses with shrubby clumps of nopales composed by O. durangensis and O. robusta, legumes (Mimosa spp. and Dalea bicolor) and sangre de drago (Jatropha dioica), the herbaceous cover accounted for the 20% of the total
ARTICLE IN PRESS M.E. Riojas-Lo´pez / Journal of Arid Environments 67 (2006) 428–435
431
vegetal cover. The third site, ‘‘La Huerta’’ (211520 3200 N, 1011370 1600 W, 2290 m.a.s.l.), was a fruit-oriented, cultivated nopalera (O. megacantha var. c.v. naranjona), ca. 4 ha, planted in 1989 with plants spaced 3 m along rows that were 5 m apart. The herbaceous strata covered 30% of the ground, the shrubby strata was composed by the cultivated varieties of nopales. 2.2. Methods and data analysis I live-trapped rodents at the three described sites in February, April, July and November, 1997, except in February when La Huerta could not be sampled because of ongoing agricultural practices. Rodents were trapped using Sherman traps baited with oatmeal and vainilla extract in a 10 10 grid with lines and stations 8 m apart, for two consecutive nights, using one grid per site. All individuals captured were identified, marked numerically by toe clipping, and released at the site of capture. Species richness was considered as the number of species recorded at each study site on each sampling period. The sum of all different rodents captured in each visit was used as the best estimator of abundance. A two-way analysis of variance was used to compare rodent species richness and abundance between sampling sites and sampling periods. Tukey tests were perfomed when differences were found (Zar, 1999). These analyses were performed with ap0.05. Site and sampling periods were arranged through a principal component analysis (PCA) based on rodent abundances. 3. Results Fourteen different rodent species were recorded at the study sites. There were no significant differences in total and seasonal abundance of rodents per site or among sites. Some rodent species exhibited site-specific preferences and their abundances differed significantly between sites (Table 1). Reithrodontomys fulvenscens and Liomys irroratus Table 1 Mean and standart error of rodent species abundance at the natural and cultivated nopaleras (Opuntia spp.) in north-eastern Jalisco, Mexico, 1997 Species Liomys irrotatus Chaetodiphus nelsoni Perognathus flavus Dipodomys ordii Dipodomys phillipsi Chaetodipous hispidus Reithrodontomys megalotis Reithrodontomys fulvescens Peromyscus melanophrys Peromyscus difficilis Peromyscus gratus Peromyscus maniculatus Sigmodon fulviventer Sigmodon hispidus Species richness
Matancillas (n ¼ 4) a
22.574.73 4.570.57a 0.7570.47b 2.5071.50 0.00b 1.00 472.44b 46.25711.58a 1.00 6.2571.54 1.00b 0.00b 0.00b 0.00 6.7570.50a
La Campana (n ¼ 4) b
170.40 2.2570.75b 6.5071.70a 5.5072.06 10.7570.25a 0.00 972.67b 3.5070.64b 2.5070.64 8.7572.01 5.5072.06a 1.00b 0.00b 0.00 9.5070.50b
Values with different letter in the same row are statistically different (ap0:05).
La Huerta (n ¼ 3) b
0.6770.33 0.00b 1.6670.33b 3.3370.66 4.0070.57b 0.00 1872.00a 5.6672.18b 2.00 7.0072.08 3.00a 2.3370.33a 3.0070.88a 1.00 9.6670.66b
p 0.0047 0.0028 0.0343 0.2265 0.0001 — 0.0044 0.0144 0.0121 0.6040 0.0225 0.0003 0.0130 — 0.0034
ARTICLE IN PRESS 432
M.E. Riojas-Lo´pez / Journal of Arid Environments 67 (2006) 428–435
Fig. 2. Organization of three nopaleras and four sampling periods along the two first axis of a principal component analysis, based on the abundance of rodents in north-eastern Jalisco, Mexico, 1997.
were the most abundant species. In Matancillas they represented 80% of all individuals. At La Campana and La Huerta the abundance of individual species was more even than at Matancillas. Species richness varied from 10 to 14, and Matancillas had a lower species richness (pp0:0034) than La Campana and La Huerta. The first two axes of the PCA explained 43% and 35% of the total variation of the rodent community among sites. This analysis clearly separated Matancillas from La Campana and La Huerta (Fig. 2), which formed a single cluster, except for the November sampling period at La Campana which was intermediate.
4. Discussion and conclusions Although agroecosystems have been considered low diversity habitats, my results exhibited that this was not true in fruit-oriented cultivated nopaleras in north-eastern Jalisco. The rodent community species richness at the cultivated nopalera was comparable to that of the shrubby open nopalera at La Campana, and richer than the arboreal nopalera at Matancillas. The significant differences detected in abundances of individual rodent species were site-specific. Although Matancillas had the highest abundance, two species, L. irroratus and R. fulvescens, accounted of the 80% of its rodents. Both rodent species prefer grassy habitats with shrubs (Dowler and Genoways, 1978; Spencer and Cameron, 1982), which is concordant with my findings. Throughout the study I captured L. irroratus mostly beneath the arboreal nopales, where the ground was covered by a thick layer of litter, which seems to provied a suitable habitat for this species. R. fulvescens microsites had a better herbaceous cover than that for L. irroratus. The vegetation structure of Matancillas, defined by two strata (arboreal and herbaceous) made it a more homogenous habitat for rodents, which explains why the rodents captured at this nopalera were species that generally inhabit sites with dense plant cover and well stratificated vegetation. Overall, the organization of sites/period on the PCA graph is explained best by differences in the cover of herbs and litter, and was strongly related to the variation in abundance of rodent species that preferred dense cover and those that preferred more open habitats. The November sampling at both La Campana and Matancillas, separated from other periods at those sites reflected a heavy rain in October, whose effects were removed through agricultural practices at La Huerta.
ARTICLE IN PRESS M.E. Riojas-Lo´pez / Journal of Arid Environments 67 (2006) 428–435
433
According to site-specificity, the rodent communities in La Campana and in La Huerta could be divided in two groups: species that are found commonly in habitats of dense medium to tall herbaceous and shrubby cover, and those that preferred open spaces of short grassess intercepted with shrubby clumps. The first group included Reithrodontomys megalotis, Sigmodon fulviventer, S. hispidus, Peromyscus melanophrys and P. truei. The three former species are associated with grassy or grass-shrub habitats (Baker and Shump, 1978; Cameron and Spencer, 1981; Webster and Jones, 1982). P. melanophrys uses sites with dense growth of shrubs, whereas, in Mexico, P. gratus is found in a variety of habitats, including sites with dense growth of Opuntia cacti (Hoffmeister, 1981). In this study, all these rodent species were captured in traps located next to or beneath dense nopal clumps surrounded by abundant herbs. The second rodent group was composed by Dipodomys phillipsii, D. ordii and Perognathus flavus. These species are typically associated with short grassland with clumps of Opuntia cacti and other shrubby plants (Jones and Genoways, 1975; Bowers, 1982). The significantly higher species richness at La Campana and La Huerta, compared to Matancillas, was the result of a more spatially heterogeneous habitat, as habitat heterogeneity plays an important role in structuring rodent communities in desert systems (Rosenzweig and Winakur, 1969; Whitford, 1976; Heske et al., 1994; Mellink, 1995). Whereas La Campana had four vegetation layers (short and medium herbs, shrubs, and arboreal nopales) in La Huerta there were three layers (short and medium to tall herbs, and shrubby nopales), and in Matancillas, only two layers (short to medium herbs and arboreal nopales). Moreover, at La Campana, heavy grazing opened wide patches among the nopales but as cattle could not forage beneath the shrubby nopales, it left patches with dense herb cover interspread with the open spaces. On the other hand, the cultural practices at the nopal orchards consist of plowing between the rows, pruning of the Opuntia cacti pads and fertilizing with dry manure, every 3 or 4 years. These practices contribute to the maintenance of open spaces between the plants, but also allow the establishment of dense islands of herbs and low shrubs, which provide a variety of microsites, suitable for rodent species with different habitat requirements. This matrix of habitats within these sampling sites might have promoted the colonization by species with different requirements. Additionally, the feeding habits of the rodents themselves, especially of kangaroo rats, can influence the composition and structure of the plant communities in arid lands (Heske et al. 1993, 1994). The role of native rodents in the nopaleras of the region is unkonwn. In the Sonora Desert, small-scale indigenous agriculture increased plant diversity and formed a patchy habitat that favoured biodiversity (Nabhan et al., 1982; Mellink, 1985). Some other traditional agroecosystems such as shaded coffee agroforests play an important role in biodiversity conservation due to their structural complexity (Gallina et al., 1996; Moguel and Toledo, 1999). My results are concordant with the idea that, for rodents, environmental heterogeneity due to disturbance could be a key factor in promoting diversity (Mellink, 1985, 1991; Pardini, 2004). Although more research about other factors that determine the structure of rodent communities in cultivated nopaleras is necessary, current fruit-oriented, cultivated nopaleras in north-eastern Jalisco, create a habitat mosaic that is used by rodent species from different guilds through structurally diverse vegetal habitats and agricultural disturbance.
ARTICLE IN PRESS 434
M.E. Riojas-Lo´pez / Journal of Arid Environments 67 (2006) 428–435
The fruit-oriented cultivated nopaleras in north-eastern Jalisco, Mexico have three of the four conditions that define agroecosystems that might contribute to biodiversity conservation (Southwood and Way, 1970): (1) they are perennial farming systems that use domesticated varieties of native species; (2) the agricultural practices are sporadic; and (3) they seem to allow the establishment of a complex and diverse vegetation association of perennial and annual plants within the plots. These agricultural systems are an alternative habitat for some native species in this severely fragmented region and contribute to the maintenance of local and regional rodent biodiversity. They should not be overlooked as a mechanism to promote biological conservation, while allowing for economic activities to continue. Acknowledgements To Eric Mellink for statistical support and Mollie Harker for editorial assistance. To Adriana Gonza´lez-Dura´n who helped me during field work and to Rube´n Gonza´lez for allowed me to work in his property. To the Universidad de Guadalajara for financial support. References Andersen, M.C., Kay, F.R., 1999. Banner-tailed kangaroo rat burrow mounds and desert grassland habitats. Journal of Arid Environment 41, 147–160. Baker, R.H., Shump Jr., K.A., 1978. Sigmodon fulviventer. Mammalian Species 94, 1–4. Benton, T.G., Vickery, J.A., Wilson, J.D., 2003. Farmland biodiversity: is habitat heterogeneity the key? Trends in Ecology & Evolution 18, 82–188. Bowers, M., 1982. Foraging behavior of heteromyid rodents field evidence of resource partitioning. Journal of Mammalogy 63, 361–367. Brown, J.H., Heske, E.J., 1990. Temporal changes in a Chihuahuan Desert rodent community. Oikos 59, 290–302. Cameron, G.N., Spencer, S.R., 1981. Sigmondon hispidus. Mammalian Species 158, 1–9. Challenger, A., 1998. Utilizacio´n y Conservacio´n de los Ecosistemas Terrestres de Me´xico: Pasado, Presente y Futuro, Comisio´n Nacional para el Conocimiento y Uso de la Biodiversidad, Instituto de Biologı´ a, Universidad Nacional Auto´noma de Me´xico, Agrupacio´n Sierra Madre, S.C., Me´xico. Chew, R.M., Whitford, W.G., 1992. A long positive effect of kangaroo rats (Dipodomys spectabilis) on creosotebushes (Larrea tridentata). Journal of Arid Environment 22, 375–386. Dowler, R.C., Genoways, H.H., 1978. Liomys irroratus. Mammalian Species 82, 1–6. Gallina, S., Mandujano, S., Gonza´lez-Romero, A., 1996. Conservation of mammalian diversity in coffee plantations of Central Veracruz, Mexico. Agroforestry Systems 33, 13–27. Gonza´lez-Espinosa, M., 1999. Interacciones entre fenologı´ a, elementos bio´ticos y disturbio por pastoreo en las nopaleras del centro de Me´xico. In: Aguirre, R.J.R., Reyes, A.J.A. (Eds.), Memoria VIII Congreso Nacional y VI Internacional sobre Conocimiento y Aprovechamiento del Nopal. Editorial Universitaria Potosina, Universidad Auto´noma de San Luis Potosı´ , Me´xico, pp. 342–358. Gonza´lez-Espinosa, M., Quintana-Ascencio, P.F., 1986. Seed predation and dispersal in a dominant desert plant: Opuntia, ants, birds and mammals. In: Estrada, A., Fleming, T.H. (Eds.), Frugivores and Seed Dispersal. Dr. Junk Publishers, Dordrecht, pp. 273–283. Granados, S.D., Castan˜eda, P.A., 1991. El Nopal. Trillas, Me´xico. Heske, E.J., Brown, J.H., Mistry, S., 1994. Long-term experimental study of Chihuahuan Desert rodent community: 13 years of competition. Ecology 75, 438–445. Heske, E.J., Brown, J.H., Guo, Q., 1993. Effects of kangaroo rat exclusion on vegetation structure and plant species diversity in the Chihuahuan Desert. Oecologia 95, 520–524. Hietala-Koivu, R., Lankoski, J., Tarmi, S., 2004. Loss of biodiversity and its social cost in a agricultural landscape. Agriculture Ecosystems & Environment 103, 75–83. Hoffmeister, D.F., 1981. Peromyscus truei. Mammalian Species 161, 1–5.
ARTICLE IN PRESS M.E. Riojas-Lo´pez / Journal of Arid Environments 67 (2006) 428–435
435
Instituto Nacional de Estadı´ stica Geografı´ a e Informa´tica (INEGI), 2003. http://www.inegi.gob.mx/jalisco/ ojuelos.html Jones Jr., J.K., Genoways, H.H., 1975. Dipodomys phillipsii. Mammalian Species 51, 1–3. Mellink, E., 1985. Agricultural disturbance and rodents: three farming systems in the Sonoran Desert. Journal of Arid Environment 8, 207–222. Mellink, E., 1991. Rodent communities associated with three traditional agroecosystems in the San Luis Potosi Plateau, Mexico. Agriculture Ecosystems & Environment 33, 363–375. Mellink, E., 1995. Uso del ha´bitat, dina´mica poblacional y estacionalidad reproductiva de roedores en el Altiplano Potosino, Me´xico. Revista Mexicana de Mastozoologia 1, 1–8. Mellink, E., Riojas-Lo´pez, M.E., 2002. Consumption of platyopuntias by wild vertebrales. In: Nobel, P.S. (Ed.), Cacti: Biology and Uses. The University of California Press, California, pp. 109–123. Moguel, P., Toledo, V.M., 1999. Biodiversity conservation in traditional coffee systems of Mexico. Conservation Biology 13, 11–21. Nabhan, G.P., Rea, A.M., Reichardt, K.L., Mellink, E., Hutchinson, C.F., 1982. Papago influence on habitat and biotic diversity: Quitovac oasis ethnoecology. Journal of Ethnoecology 2, 124–143. Pardini, R., 2004. Effects of forest framentation on small mammals in an Atlantic Forest landscape. Biodiversity and Conservation 13, 2567–2586. Programa de Desarrollo Forestal de Jalisco (PRODEFO), 1999. Superficies de Recursos Forestales del Estado de Jalisco. Documento Te´cnico 21, Me´xico. Reichhardt, K.L., Mellink, E., Nabhan, G.P., Rea, A., 1994. Habitat heterogeneity and biodiversity associated with indigenous agriculture in Sonoran Desert. Etnoecolo´gica 2 (3), 21–34. Riojas-Lo´pez, M.E., Mellink, E., 2005. Potencial for biological conservation on man-modified habitats in northeastern Jalisco. Biodiversity and Conservation 14, 2251–2263. Rosenzweig, M.L., Winakur, J., 1969. Population ecology of desert rodent communities: habitat and environmental complexity. Ecology 50, 558–572. Spencer, S.R., Cameron, G.N., 1982. Reithrodontomys fulvescens. Mammalian Species 174, 1–7. Southwood, R.E., Way, M.J., 1970. Ecological background to pest management. In: Rabb, R.C., Guthrie, F.E. (Eds.), Concepts of Pest Management. North Carolina State University, Raleigh, NC, pp. 6–29. Webster, W.D., Jones Jr., J.K., 1982. Reithrodontomys megalotis. Mammalian Species 167, 1–5. Whitford, W., 1976. Temporal fluctuations in density and diversity of desert rodent populations. Journal of Mammalogy 57 (2), 351–369. Yeaton, R.I., Romero, M.A., 1986. Organization of vegetation mosaics in the Acacia schaffneri-Opuntia streptacantha association, southern Chihuahuan Desert, Mexico. Journal of Ecology 74, 211–217. Zar, J.H., 1999. Biostatistical Analysis, fourth ed. Prentice-Hall, Englewood Cliffs, NJ, USA.