Agroforestry Systems 33: 13-27, 1996. © 1996 Kluwer Academic Publishers. Printed in the Netherlands. Conservation of mammalian biodiversity in coffee plantations of Central Veracruz, Mexico S. GALLINA, S. MANDUJANO and A. GONZALEZ-ROMERO Instituto de Ecologia, Apartado Postal 63, 91000 Xalapa, Veracruz, Mexico Key words: arboreal strata, coffee shade trees, ecological diversity, mammalian community Abstract. The diversity and organization of the mammalian community is related to the vegetation structure of the coffee plantations in the area of Barranca Grande, in the State of Veracruz, Mexico. Four transects (each 200 m in length) were used to study the vegetation structure within the coffee plantation, and 178 nighUtraps, tracks registration and information from local people, were used in order to become familiar with the mammalian community. The sample period was from October 1989 to February 1991. The 24 mammals of medium-size species present in the area were classified using two measures of ecological diversity, locomo- tion and foraging in order to understand the guild organization. If the complexity of the plan- tation is reduced, the number of guilds occupied could suffer a loss of 45% and 43% in ecological richness and diversity, respectively, and 24% in the equitability of the mammalian fauna. We recommend the maintenance of a high diversity in the tree stratum (shade species), in this case, species such as Inga jinicuil, banana (Musa sapientum), Citrus spp., coyo avocado (Persea schiedeana), mango (Mangifera indica), species which could provide food resources and protection for the mammals. Resumen. En el frea de Barranca Grande, Estado de Veracruz, México, se estudié la relacién que tiene la estructura de la vegetacién de los cultivos de café con la diversidad de la comunidad de mamiferos medianos. Para ello, se establecieron 4 transectos fijos de 200 m de largo cada uno, en los que se tomaron los datos de los diferentes estratos. Para conocer la fauna de mamiferos, se hizo un muestreo con trampas Tomahawk (178 noches/trampas), registro de rastros asi como encuestas a la gente que vive en la zona, entre Octubre de 1989 y Febrero de 1991. Se registraron 24 especies de mamiferos medianos que fueron clasificados utilizando dos medidas de diversidad ecolégica, locomocién y forrajeo, para conocer la organizacién en gremios. Si se reduce la complejidad de los cafetales, puede existir una reduccién hasta del 45% en el niimero de gremios ocupados, 43% en la riqueza y en la diversidad ecolégica, y 24% en la equitatividad. Se recomienda mantener una alta diversidad en el estrato arboreo, en este caso especies como el jinicuil (Inga jinicuil), phitanos (Musa sapientum), citricos (Citrus spp.), pagua © aguacate (Persea schiedeana), mango (Mangifera indica), serian recomendables ya que proporcionan recursos alimenticios y proteccién a la mayoria de los mamiferos. Introduction Although the recent tendency in agricultural extension services in other countries is to recommend the cultivation of coffee without shade trees in order to gain the highest possible yields [Beer, [987], there are no studies on the effect of this practice on the local fauna. In Mexico, in the central region of the State of Veracruz, coffee plantations are the most important economic activity. There are 49,000 ha which produce 49% of the coffee in the State14 [Marchal and Palma, 1985]. However, there are few ecological studies in the region: one on birds [Aguilar Ortiz, 1982] and the rest on vegetation [Jimenez Avila, 1979; Jimenez Avila and Correa Peiia, 1980; Jimenez Avila and Gomez- Pompa, 1982; Jimenez Avila and Martinez Vara, 1979]. But due to the recent decline in the international price of coffee, there is a tendency to change these plantations to other crops such as sugar cane, and this change has had a negative effect on the mammalian fauna. With regard to mammalian communities, there are some studies concerning neotropical forests [August, 1983; Dubost, 1987; Fleming et al., 1987; Konecny, 1989; Lacher and Mares, 1986; Robinson and Redford, 1986a; Smythe, 1986; Sunquist et al., 1989; Terborgh, 1986; Wilkie and Finn, 1990; Wilson and Johns, 1982], but none on coffee crops. The main objective of this study was to gather information about the relationship between the vegetation structure of the coffee plantation and the organization of the mam- malian community, mainly those of medium size, in order to recommend some strategies for maintaining biodiversity and reducing the loss of species. Study area The area is located 40 km south of the city of Xalapa, Veracruz, Mexico, between 19° 19’ and 19° 20’ N and 97° 02’ and 97° 04’ W. The mean tem- perature is 19.4 °C, and the annual precipitation is 2082 mm. The elevation of the study sites varies between 920 and 1030 m. The original vegetation was the oak forest and tropical cloud forest, the latter found along creeks and ravines. Methods In November 1989, four fixed transects of 200 m length each, with ten sampling areas, were established in four coffee plantations which differ in the use of shade tree species. The arboreal density, basal area, cover and dominance were obtained by the point-centered method [Mueller-Dombois and Ellenberg, 1974]. Tree richness (N) was the number of species, tree diver- sity was obtained by the inverse of Simpson Index (N,) as: 1 Nee soap where ny PimN and evenness or equitability was calculated with the Pianka Index or modified15 Hill’s ratio (Z) [Ludwig and Reynolds, 1988; Mueller-Dombois and Ellenberg, 1974) as: x H= x, (pnp). Trees, coffee plants and other shrubs (density, height and cover) were sampled in each of the four transects using rectangles of 5 x 50 m (250 m’). This data was used to produce vegetation profiles in order to have a better image of the structure of the different plantations [Jimenez Avila, 1979; Matteucci and Colma, 1982]. The herb biomass was estimated in 40 sample areas of 1 m? each, distributed along the 200 m transects [Avery, 1975; Pechanec and Pickford, 1937]. In addition, diversity, richness and evenness were estimated for the herbaceous strata, using the same formulas. Principal Components Analysis (PCA) [Pla, 1986] was used to calculate which variables were determinant in coffee plantations, analyzing 15 vegeta- tional variables (using the mean value and the standard deviation, so a total of 23 variables were used, see Table 1). For each transect, only the eight variables of arboreal strata obtained in 200 m long, were used in the PCA to derive estimates of habitat complexity and patchiness [Ludwig and Reynolds, 1988]. The terms defined by August [1983] were used as follows: 1) ‘Com- plexity describes the development of vertical strata within the habitat. Complex habitats have many and well-developed vertical strata.’ 2) ‘Heterogeneity or patchiness represents horizontal variation in habitat physiognomy. For example, a small patch of tropical forest can be extremely complex but very homogeneous, whereas woodland savanna may be less complex but highly patchy. So potential niches are distributed vertically in complex habitats and both horizontally and vertically in patchy habitats.’ The index of habitat complexity was the mean of the factor scores from first component; the standard deviation of the mean factor score from first component was used as a measure of habitat heterogeneity or patchiness [August, 1983]. The information about the mammalian species was registered in January, February, April, May, July, and October 1990, and February 1991. A total of 178 night/Tomahawk traps were used to capture animals alive. Traps were baited with sausage, sardine or bananas. All individuals were marked, measured, and then released at the same site. Information from animal tracks and from the local people was also obtained.16 Table 1. Data of the 15 variables measured in the 4 transects in the coffee plantations of Barranca Grande, Veracruz. Mean (x), standard deviation (SD). Vegetational variables Transect 1 2 3 4 Absolute density (ind/dm?) 23 07 42 53 Arboreal distance (m) x 66 12.0 49 44 sD 24 26 2.0 2.0 Tree height (m) x 118 83 93 86 sp Sul 4s 18 37 Total basal area (m*/ha) 313 80 13.2 35.3 Mean basal area (cm*) x 1009 529 44 1206 sb 1246 658 310 2228 Cover (m?) x 49.3 205 18.3 40.0 sD 45.7 10.6 10.6 38.8 Arboreal richness x 2.4 16 22 2.4 sD 10 05 09 07 Arboreal diversity 37 14 23 48 Equitability 07 0.4 06 07 Coffee plants (ind/ha) 2120 1880 2840 2800 Shrub height (m) x 3. 20 23 41 sD 09 07 1.0 14 Shrub cover (m?) x 29 25 19 48 sD 15 22 14 44 Herb biomass (g/m?) x 110.6 292.6 70.1 70.6 sD 53.6 342.6 425 43.2 Herb diversity 32 58 15 45 Herb equitability 06 07 0.4 07 To estimate the relative animal abundance, a classification of rare, regular, and abundant was used, taking the following parameters into account: frequency of trapping, frequency of tracks found, and frequency of observa- tions or hunting by local people. Each mammalian species was also classified using its type of locomotion and foraging habits, for example, arboreal, scansorial, terrestrial or aquatic. The locomotor ecological measurement reflects the vertical habitat space17 utilized by the animals. The foraging diversity was divided into six cate- gories [Robinson and Redford, 1986b]: herbivore-grazer, frugivore-granivore, frugivore-omnivore, insectivore-omnivore, myrmecophage, and carnivore. The mammal classification was based on the information obtained from the main diets of the neotropical species [Eisenberg, 1989; Janzen, 1983; Smythe et al., 1986]. The categories are ranked such that species placed in categories high on the list have a generalist diet and/or feed on resources at low trophic levels, while species in categories low on the list have narrow diets and/or feed on resources at high trophic levels, making them more vulnerable species. These foraging categories show not only the food habits of the species, but also the amount of potentially available energy that is dependent on the availability of appropriate resources [Robinson and Redford, 1986b]. A measure of mammalian ecological diversity based on both foraging and locomotor diversity was derived [August, 1983; Eisenberg, 1989; Robinson and Redford, 1986a, b]. A matrix was made consisting of foraging types along the columns and locomotor types along the rows. The ecological diversity was calculated using the Shannon-Wiener Index: H’eco = -X(CJLE)n(C ZZ) where C,, is the total of each cell of the matrix and YD is the grand sum of the matrix. Ecological evenness, Pielou’s Index (J’), was the ecological diversity divided by the natural logarithm of the number of occupied cells [August, 1983}. To determine the effect of the habitat complexity and heterogeneity of the coffee plantations over the mammalian community, we took into account the number of occupied guilds, the ecological richness, diversity, and equitability. We obtained these values for all the coffee plantations with structures of differing complexity. Results Characteristics of arboreal strata Twenty species of trees were registered, the most common being: ‘jinicuil’ (Inga jinicuil Sch), ‘chalahuite’ (Inga spp.), ‘banana’ (Musa sapientum L.) and orange (Citrus sinensis Osb). Tree dominance varied according to the different management used in each plantation. ‘Jinicuil’ was dominant in transects | and 4, and ‘chalahuite’ in transects 2 and 3 (Table 1). The height of ‘Jinicuil’ was between 12 to 16 m, with a mean cover of 95 m’, while the ‘chalahuite’ had a height of between 7 and 8 m and a mean cover of 28 m’. Both the highest species richness (11 tree species) and diversity (5.04) were found in transect 4, and the least species richness (6 tree species) and diversity (1.37) in transect 2. The herb biomass and diversity were high inNUMBER SPECIES x 10 ANTM Fig. 1. Fructification period of all the plant species in coffee plantations at Barranca Grande, Veracruz, Mexico. transect 2 (F = 3.49, DG = 3,35, p < 0.03), a correlation existing between biomass and the distance of trees (r = 0.52, DG = 37, p < 0.001). In the study area it is possible to find fruits almost all year round, but between May and September we observed the fructification mode (Fig. 1). Complexity and heterogeneity of coffee plantations The PCA, using 23 variables, explained with the two principal components 84.1% of the variation (PCI = 54.9% and PCII = 29.3%), as well as out- standing arboreal richness, evenness and diversity, the variation in biomass in the PCI, and herbage evenness and the variation in tree height in the PCII (Fig. 2). Transects 1 and 4 were characterized by arboreal variables such as tree diversity and height; transect 3 by tree height variation, and transect 2 by herb biomass (here we registered a high biomass) and tree distance (also larger), as shown in Fig. 3. Analyzing each transect by the individual PCA, we concluded that the greatest complexity and heterogeneity was found in transect 4 and the lowest value in transect 3 (Table 2). In transect 4, tree species richness and the variation in tree height and cover were the determinant variables in habitat complexity and heterogeneity and explained the 79.5% of the total variation in the PCA. In transect 1, the PCA explained 72.2% of the variation, with tree height, basal area, and cover proving to be important. In transect 3, 63.2%19 we DAs T2 Vegetation variables DAx = Distance between arboreal strata (mean). DAs = Distance between arboreal strata (standard deviation). ARx = Arboreal richness strata (mean), ARs = Arboreal richness strata (standard deviation). AD = Arboreal diversity. EA = Arboreal equitativity. AHx = Arboreal height strata (mean). AHs = Arboreal height strata (standard deviation). BAt = Basal area total. BAx = Basal area (mean). BAs = Basal area (standard deviation). ACx = Cover arboreal (mean). ACs = Cover arboreal (standard deviation). ADe = Arboreal density. Cof = Coffee plants (number). SHx = Shrub height (mean). SHs = Shrub height (standard deviation). SCx = Shrub cover (mean). SCs = Shrub cover (standard deviation), HBx = Herb biomass (mean). HBs = Herb biomass (standard deviation). HD = Herb diversity. HE = Herb equitativity. Fig. 2. Principal components analysis considering 23 variables that explain 84.1% of the variation.20 TRANSECT -1! TRANSECT -3 TRANSECT -4 Fig. 3. Vegetation profiles of the four transects in coffee plantations at Barranca Grande, Veracruz, Mexico.21 usiy No} 6L'0 89°0 9e0 Ayaua8or019}1 100 oro 850 Aipxadwod +L WL ran eh LL8L'0 so9e'o sizs'0 £189°0 as Loo SLo0 109¢°0 sloeo ue, viz 6880 Lgr0- L6s°0 S70 ror'0- 88r'0 raro- ssouyory, ZL1'0 606'0- 690 zsi'0- zo0"0- 1oz0- orr'o- 889°0- Aussaaid orzo 1ze'0- £0r'0- sov'o 989°0 Isso Z1L0- 987'0- sseworg 6190 8PS'0- eso sso z9s'0 120 ve'0- 960 vequeoy rLz0 Ls80 zIvo €1L0 6400 810- 190°0- seoo sono) orzo 7260 390°0- £80 896'0- 862°0 0160 5 1819H £880 sevo- Lor‘o- +260 Izpo~ 1280 s90'0- x 181 7990 soeo 980 8ce'0 sivo £20 o01'0- wsiaary Mod IOd Mod Tod Hod Idd lod 1od rh eh aL iv aiqeue, “suonenueyd 993J09 ay) Jo AouaBoxaroy pue Arwxoiduioo oy) urejdxa weyp sioasues snoy ay Jo Yova 405 syusUodWIOD YId MUL °Z 71422 of the variation was explained, with tree height and arboreal distance being important. In transect 2, 62.9% was explained, with the highest value being the tree height. Mammals present at Barranca Grande There were 24 medium mammalian species registered in the coffee plantations (Table 3), but it is possible that the number could increase to 30 because there are species that the local people claim no longer exist in the area, such as, collared pecari (Pecari tajacu), white-tailed deer (Odocoileus virginianus), and brocked deer or temazate (Mazama americana). Others, such as, agouti (Dasyprocta punctata), grison (Galictis vittata), taira (Eira barbara), and ocelot (Leopardus pardalis), exist in other coffee plantations and could also be present, but we have had no the opportunity to register them. Some of the registered species found in the area are endangered: tamandua anteater (Jamandua mexicana), river otter (Lontra longicaudis), Mexican porcupine (Sphiggurus mexicanus), and the margay (Leopardus wiedii). Mammalian community organization The mammalian community found in the coffee plantations was structured as follows: 50% terrestrial, 25% scansorial, 21% arboreal, and 4% aquatic (Table 3). The six foraging categories, presented in Table 4, are herbivore-grazer (4.2%), frugivore-granivore (12.5%), frugivore-omnivore (37.5%), insecti- vore-omnivore (16.7%), mirmecophage (4.2%), and carnivore (25%). As noted, more than 50% of the species include fruits in their diet. Abundance The 29% (7) of the species registered were abundant in the study area, 38% (9) show an average presence, and 33% (8) were considered rare. It is known that the rare species are most likely to disappear. Our observations, coupled with those of the local people, indicate that the abundant species are Philander opossum, Didelphis marsupialis, D. virginiana, Dasypus novemcinctus, Nasua narica, Sciurus aureogaster, and Procyon lotor. Some of the rare species are: Sphiggurus mexicanus, Herpailurus yaguarondi, and Puma concolor. Relationships between coffee plantation complexity and the fauna If the habitat complexity is reduced, as in coffee plantations without arboreal strata, then we expected in Table 4, that certain guilds such as the arboreal and scansorial mammals will disappear, because they will not find their habitat needs. Also the frugivorous species which depend on fruits will suffer a reduction. Table 5 shows the results of this speculation: it compares the values