Shade-Coffee Plantations as Refuges for Tropical Wild Orchids in

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Abstract: In central Veracruz, Mexico, coffee plantations have replaced large areas of lower montane cloud forest. .... from pollinator visits, we covered flower buds before an- thesis. ..... culture, three orchid species are able to develop abun-.
Shade-Coffee Plantations as Refuges for Tropical Wild Orchids in Central Veracruz, Mexico ´ LISLIE SOLIS-MONTERO,∗ ‡ ALEJANDRO FLORES-PALACIOS,†§ AND ANDREA CRUZ-ANGON† ∗

Departamento de Qu´ımica y Biolog´ıa, Universidad de las Am´ericas—Puebla Sta. Catarina M´artir s/n, Cholula, Puebla, Mexico †Departamento de Ecolog´ıa Vegetal, Instituto de Ecolog´ıa A. C. Apartado Postal 63, Xalapa, 91000, Veracruz, Mexico

Abstract: In central Veracruz, Mexico, coffee plantations have replaced large areas of lower montane cloud forest. Shade-coffee plantations with high levels of structural diversity provide refuge for forest-dependent biota (e.g., birds and insects). Orchids typical of natural forest may also be found in the canopy of shade-coffee agroecosystems. It is not known, however, whether these are relicts from the original forest vegetation or if the plantations themselves provide the necessary conditions to support a self-sustained orchid population. We studied the population structure of the epiphytic orchids Jacquiniella teretifolia (Sw.) Britton & Willson, Scaphyglottis livida (Lindl.) Schltr., and Maxillaria densa Lindl. in a shade-coffee plantation (commercial polyculture) in central Veracruz. We also studied the previously undescribed reproductive biology of the latter two species. Our results show that the three orchid species had high population densities (>800 plants/ha). In our study site, 50% to 68% of the orchid plants of the target species were young individuals (less than five shoots). Reproductive structures were present in 80% of individuals larger than 30 shoots in the three species. M. densa is self-incompatible, and the fruit set obtained from cross pollination (42.7%) was higher than that obtained from natural pollination (18.2%), suggesting that this species could be pollinator limited. S. livida is autocompatible, not autogamous, and was not pollinator limited. Our results show that the coffee plantation had abundant orchid populations with log-normal size/age structures. Two of the target species, M. densa and S. livida, depend on pollinators to reproduce. It is clear that pollinators that allow orchids to set a high proportion of fruits persist in shade-coffee plantations. Coffee plantations may not replace the original conditions of a forest, but it is possible that these and other orchid species survive and reproduce in coffee plantations that provide appropriate microclimate conditions for the plants, including pollinators.

Key Words: pollinator limitation, population structure, reproductive biology, vascular epiphytes, vertical stratification Plantaciones Cafetaleras de Sombra como Refugio de Orqu´ıdeas Silvestres en Veracruz Central, M´exico

Resumen: En el centro de Veracruz, M´exico, las plantaciones de caf´e han reemplazado a extensas a´ reas de bosque nublado montano. Las plantaciones cafetaleras de sombra con altos niveles de diversidad estructural proporcionan refugio a biota dependiente de bosques (e. g., aves e insectos). En el dosel de agroecosistemas de caf´e de sombra tambi´en se pueden encontrar orqu´ıdeas t´ıpicas de bosques naturales. Sin embargo, no se conoce si son relictos de la vegetaci´ on del bosque original o si las plantaciones mismas proporcionan los recursos necesarios para soportar a una poblaci´ on de orqu´ıdeas auto sostenida. Estudiamos la estructura de la poblaci´ on de orqu´ıdeas epifitas Jacquiniella teretifolia (Sw.) Britton & Willson, Scaphyglottis livida (Lindl.) Schltr y Maxillaria densa Lindl en una plantaci´ on de caf´e de sombra (policultivo comercial) en el centro de Veracruz. Tambi´en estudiamos la biolog´ıa reproductiva, no descrita previamente, de las u ´ ltimas dos especies. Nuestros resultados muestran que las tres especies de orqu´ıdea tuvieron densidades poblacionales altas (>800

‡Current address: Herbario, ECOSUR, Carretera Panamericana y Perif´erico Sur s/n, C.P. 29290, Barrio de Mar´ıa Auxiliadora, San Crist´ obal de las Casas, Chiapas, Mexico, email [email protected] or [email protected] §Current address: CEAMISH Universidad Aut´ onoma del Estado de Morelos, Av. Universidad 1001, Cuernavaca, Morelos, 62000 Mexico. Paper submitted October 28, 2003; revised manuscript accepted August 1, 2004.

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plantas/ha). En nuestro sitio de estudio, entre 50% y 68% de las plantas de las especies estudiadas eran individuos j´ ovenes (menos de cinco rebrotes). En las tres especies hubo presencia de estructuras reproductivas en 80% de los individuos con m´ as de 30 rebrotes. M. densa es auto incompatible, y el conjunto de frutos obtenido por polinizaci´ on cruzada (42.7%) fue mayor que el obtenido por polinizaci´ on natural (18.2%), lo que sugiere que esta especie puede estar limitada por polinizadores. S. livida es autocompatible no autogama, y no fue limitada por polinizadores. Nuestros resultados muestran que la plantaci´ on de caf´e ten´ıa poblaciones de orqu´ıdeas abundantes con estructuras tama˜ no/edad log normales. Dos de las especies, M. densa y S. livida, dependen de polinizadores para su reproducci´ on. Es claro que los polinizadores que permiten una alta proporci´ on de frutos a las orqu´ıdeas persisten en las plantaciones. Puede que las plantaciones de caf´e no sustituyan las condiciones originales de un bosque, pero es posible que estas, y otras, especies de orqu´ıdeas sobrevivan y se reproduzcan en plantaciones de caf´e que proporcionen condiciones microclim´ aticas adecuadas, incluyendo polinizadores, para las plantas.

Palabras Clave: biolog´ıa reproductiva, epifitas vasculares, estratificaci´on vertical, estructura poblacional, limitaci´ on de polinizador

Introduction Lower montane cloud forest (LMCF) represents only 1% of the Mexican territory, but it contains high vascularplant diversity, especially of epiphytes (Aguirre-Le´ on 1992; Williams-Linera et al. 2002). The LMCF hosts more than half of the orchid species known to Mexico (IUCN/SSC [World Conservation Union/Species Survival Commission] Orchid Specialist Group 1996) and a high proportion of Bromeliaceae, Hymenophyllaceae, Lycopodiaceae, and Piperaceae epiphytes (Aguirre-Le´ on 1992; Rzedowski 1996; Espejo-Serna & L´ opez-Ferrari 1999). Yet more than 90% of the original LMCF has been lost, making this habitat one of the most endangered forest types in the country ( Williams-Linera et al. 2002). The principal causes of LMCF destruction have been deforestation and fragmentation for wood extraction and conversion to cattle pasture and agricultural fields, such as sugarcane and coffee plantations (Rzedowski 1978; Williams-Linera et al. 2002). Of all the agroecosystems that replace LMCF in this region, shade-coffee plantations retain some of the structural features of a pristine forest and thus have the greatest potential for conservation. In Mexico more than 90% of coffee is cultivated under some kind of shade (Santoyo 1995; Moguel & Toledo 1999). In the mountainous region of central Veracruz, commercial polyculture, for which the original forest trees are removed and shade trees are planted, is the most common canopy-management practice. Usually, nitrogenfixing, fast-growing legumes such as Inga spp. dominate the shade layer (Moguel & Toledo 1999). In commercial polycultural coffee farms, the canopy is more open than in LMCF because tree density is only about 11% of the tree density found in LMCF. Canopy trees are about half the height of those found in LMCF and tree species richness (2−6 species/0.1 ha) is lower than in LMCF (15–22 species/0.1 ha) (Solis-Montero 2002; Flores-Palacios 2003; A.C.-A., unpublished data). Even though commercial polycultures may not share a great number of tree species with LMCF, several authors

have reported up to 30 species of forest-specialist epiphytic orchids in this type of coffee plantation (WilliamsLinera et al. 1995; Sosa & Platas 1998; A.C.-A., unpublished data). We analyzed the abundance of the epiphytic orchids Jacquiniella teretifolia (Sw.) Britton & Willson, Maxillaria densa Lindl., and Scaphyglottis livida (Lindl.) Schltr., and their distributions, population structures, and reproductive systems under a commercial polyculture system. Our main objective was to assess the conservation potential of this system of coffee production for the three species.

Methods Study Area We worked in a 200-ha coffee plantation located in La Ordu˜ na (19◦ 29 LN, 90◦ 42 LW, 1200 m asl), Coatepec, Veracruz, Mexico. At the time of the study the plantation was about 30 years old (A.C.-A., unpublished data). Tree density is (mean ± 1 SD) 136.7 ± 15.3 trees/ha (dbh ≥ 10 cm), and tree height is 9.5 ± 2.7 m. Shade is dominated by trees of the genus Inga (Fabaceae), which can comprise up to 90% of the trees. In this plantation we recorded 11 epiphytic orchid species, but in order to get a large-enough sample size, we focused our sampling efforts on the three most abundant species: J. teretifolia, M. densa, and S. livida. These species were growing on 52%, 31%, and 77% of the shade-coffee trees, respectively (Solis-Montero 2002; A.C.-A., unpublished data). In addition, these species frequently inhabit the LMCF of the region (Hietz & Hietz-Seifert 1995; Winkler & Hietz 2001; Flores-Palacios 2003).

Data Collection During the winter of 2001–2002, we set up three 10 × 100 m plots. On each plot, we marked, identified, and Conservation Biology Volume 19, No. 3, June 2005

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Table 1. Orchid species frequency on the trees surveyed (n = 41), number of sampled trees where orchids were measured, and mean orchid plant density. Orchid species Jacquiniella teretifolia Maxillaria densa Scaphyglottis livida

Species frequency (%)

Number of sampled trees

Plant density (plants/ha)

95% CI

39 41 58

7 6 7

1004 1157 7560

853–1155 968–1347 6972–8148

measured all trees (dbh ≥ 10 cm). We used binoculars (8 × 23, 6.3◦ ) to check for the presence of the target species. To assess J. teretifolia, M. densa, and S. livida abundance and distribution, we randomly selected between 30–50% of the trees where we had seen orchids (Table 1). To sample orchids we climbed the tree with ladders, identified orchid plants, and measured the diameter of the branch or trunk upon which the plants were growing. We also counted the number of stems ( J. teretifolia) or pseudobulbs (M. densa and S. livida) and recorded the presence of reproductive structures in each plant. Hereafter, we refer to both stems and pseudobulbs as shoots. In the tree parts that were not accessible by ladder, we counted the number of tree branches and measured the orchid plants in a sample (≥10% of the total number of branches). We studied only the breeding system of M. densa and S. livida because a previous study conducted in the region established that J. teretifolia is an autogamous species (M. Winkler, personal communication). To isolate flowers from pollinator visits, we covered flower buds before anthesis. When the flowers opened, we randomly assigned each flower to one of three treatments. The first treatment was designed to test for autogamy, in which flowers were isolated from pollinators. With the second treatment we evaluated self-compatibility (self-pollination) by manually pollinating each flower with its own pollen. For the third treatment (cross-pollination), we cross-pollinated flowers with pollen from a different plant—usually from a different shade tree—and removed the plant’s pollinia to avoid self-pollination. After each treatment was applied, we enclosed the flowers again to ensure that other pollinators would not interfere with the treatments. To evaluate the background effect of pollinators, we marked flowers and left them exposed to all natural pollinators. When the flowering season was over, we counted the number of fruits produced by the flowers in each treatment and natural pollination, and we calculated the percentage of flowers that set fruits (fruit set). Data Analysis To describe the distribution of J. teretifolia, M. densa, and S. livida in their tree hosts, we grouped plants by diameter class (5-cm increments) of the branch or trunk (substrate) upon which they were located. Substrate-

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diameter classes are an indirect indicator of the epiphyte position in their tree hosts because these classes can be related to the Johansson’s zones ( Johansson 1974). Branches ≤5 cm in diameter are considered twigs ( Johansson’s zone VI); those >5 ≤ 15 cm in diameter, exterior branches (zone V); those >15 ≤ 25 cm in diameter, interior branches (zone IV); those >25 ≤ 35 cm in diameter, trunk and basal canopy (zones III and II); and those >35 cm, trunk base (zone I). We tested to see whether the different species deviated significantly from being homogeneously distributed across all substratediameter classes with a chi-square goodness-of-fit test (Zar 1996). To estimate the species density (plants per hectare) of the three orchid species, we followed the method suggested by Scheaffer and collaborators (1987) for a random sampling. This method assumes a Poisson distribution of the response variable (number of orchid plants per tree) and has been previously used in epiphyte surveys (Wolf & Konings 2001). Because orchid plants were not counted on all tree parts, we calculated the total number of plants per tree as the sum of the plants counted per tree plus the number of plants estimated on the upper inaccessible tree parts. It is expected that relatively young plant populations or long-lived plant species, such as orchids, will display a log-normal size and age distribution (Silvertown & LovettDoust 1993). To test for a log-normal size and age distribution in the orchid populations, we grouped plants into classes of five shoots each. We used the number of shoots because it is an estimator of an orchid’s age. Many orchid species produce only one shoot per year per growth axis, and flower development depends on plant size and the number of growth axes (Hern´andez-Apolinar 1992; Zotz 1998, 2000; Flores-Palacios & Garc´ıa-Franco 2003). Departure between observed and expected log-normal distribution was tested with a Kolmogorov-Smirnov goodness-offit test (Zar 1996). Additionally, we used a Spearman rank correlation test (Zar 1996) to determine whether size distribution was related to the proportion of reproductive plants. To test for differences in fruit set between treatments and natural pollination, we used a chi-square test for more than two proportions (Zar 1996). When one treatment differed, we performed a chi-square multiple-comparisons test for proportions (χ 2 Tukey-like test; Zar 1996).

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Results We found a total of 510 orchids in 41 host trees surveyed: 94 J. teretifolia, 114 M. densa, and 302 S. livida (Table 1). The three orchid species each occurred in more than 35% of the trees (Table 1). None of the species showed a homogeneous distribution on trees (χ 2 = 93 for J. teretifolia, χ 2 = 78 for M. densa, and χ 2 = 141 for S. livida; for all species df = 7, p < 0.00001). Jacquiniella teretifolia was significantly more abundant in the trunk and exterior branches (6–10 cm in diameter; Fig. 1a), M. densa was found more often on thicker branches, including the trunk (Fig. 1b), and S. livida was found on twigs and branches ≤10 cm in diameter (Fig. 1c). The mean number of plants per tree (± SE) was 25.1 ± 6.8, 24.8 ± 7.6, and 94.5 ± 26.8 for J. teretifolia, M. densa, and S. livida, respectively. All species had minimum population densities higher than 800 plants/ha (Table 1). The most abundant species was S. livida, followed by M. densa and J. teretifolia (Table 1). The three orchid species showed a log-normal size distribution (D max = 0.10 for J. teretifolia, D max = 0.22 for M. densa, and D max = 0.19 for S. livida; all df = 7, p > 0.05; Fig. 2). The percentage of plants with five or fewer shoots was 50.0%, 56.1%, and 67.5% for J. teretifolia, M. densa, and S. livida, respectively (Fig. 2). The number of plants with reproductive structures was correlated with plant size (all Spearman correlation coefficients, rs > 0.8, p < 0.05) (Fig. 3). For all three species, the probability of finding reproductive structures was more than 80% for individuals with 30 or more shoots. The fruit sets were significantly different among pollination treatments for S. livida (χ 2 = 50.5, df = 3, p < 0.0001) and M. densa (χ 2 = 76.9, df = 3, p < 0.001) (Table 2). M. densa was a self-incompatible species; when compared with natural pollination, cross-pollination resulted in the highest fruit set, suggesting that the species might be pollinator limited. Scaphyglottis livida was a self-compatible, nonautogamous species; natural pollination resulted in the highest fruit set when compared with other pollination treatments. This indicates that S. livida is not limited by pollinators.

Discussion

Figure 1. Distribution of three (a-c) orchid species on different substrate ( branch/trunk) sizes. Dashed lines indicate the number of plants expected in each branch or trunk size class under the hypothesis of homogeneous distribution. Values on the x-axis are the upper size limit for each class ( ∗ p < 0.05; ∗∗ p < 0.005; ∗∗∗ p < 0.0005; ns, no significant differences between observed and expected plant abundance).

Coffee Plantations as a Refuge for Forest Orchid Species Orchids can be negatively affected by habitat conversion (Sanford 1968; Turner et al. 1994; Bertin 2002), but not all habitat conversion will have the same effect on forest orchid species. Shade plantations are a converted habitat that might be expected to support populations of epiphytic orchids. The question is, are the existing populations self-sustaining or simply relicts left over from the natural habitat that preceded conversion? To assess the

status of orchid populations in shade-coffee populations, one must assess their standing crop abundance; infer their reproductive activity by analyzing the size structure of the population; establish whether pollinators are limiting to the species and if they are, whether the limiting pollinators are present in the plantation; and finally examine whether the habitat structure can support a diversity of species. Based on the following assessment, we conclude

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Figure 3. Relationship between the number of reproductive plants and plant size (number of shoots) of the orchids J. teretifolia, M. densa, and S. livida. Values on the x-axis are the upper size limit for each class.

Figure 2. Size distribution (number of shoots) of three (a-c) orchids. Dashed lines correspond to the expected log-normal size distribution. Size distributions of none of the species depart from log-normal expectations ( p > 0.05). Values on the x-axis are the upper size limit for each class.

that these orchid species are probably self-sustaining in coffee plantations, at least in the farm we studied. Orchid Abundance Population size is one the most important factors for the permanence and survival of species. Small populations can be negatively affected by inbreeding depression, genetic drift, demographic stochasticity, and natural disasters (Frankel & Soul´e 1981; Larson 1992; Hedrick

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1996; Newman & Pilson 1997). The orchid abundances on the coffee plantation we studied were in the range of those reported for epiphytes elsewhere. In a mature pine-oak forest, Wolf and Konings (2001) estimated a mean population density of between 33 and 39,718 rosettes/species growing on oaks. In a disturbed pine-oak forest, Hern´andez-Apolinar (1992) estimated mean population densities between 3,300 and 27,400 plants/ha for the epiphytic orchid Laelia speciosa (HBK) Schltr. In a mature LMCF near our study site, the epiphytic orchid Prostechea vitellina (Lindl.) W. E. Higgins has a mean population density of between 1716 and 2144 plants/ha (A. F.-P., unpublished data). We observed a minimum population density of more than 800 plants/ha in all three species. There was a relatively high abundance of the focal orchid species despite profound differences in both diversity and composition of canopy trees in the plantation versus comparable natural habitat (LMCF). Inga trees dominated the coffee plantation studied. By contrast, Inga occurred infrequently in any LMCF of the region. For example, in LMCF near the coffee plantation we studied, the importance value (sensu Mueller-Dombois & Ellemberg 1974) of Inga species was between 0% and 0.32%. Even though the canopy structure of our study site is much simpler than that of the local LMCF, our data show that epiphytic orchid species are abundant in this habitat and that coffee plantations may be acting as refuges for some epiphytic orchids. The coffee plantation we studied was only 30 years old, which suggests that some orchids can develop abundant populations in coffee plantations in a relatively short period of time. On other tropical plantations, epiphytic bromeliad biomass can increase by one order of magnitude in about 4 years (Merwin et al. 2003). Additionally, the proportion of trees with orchids we found in our

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Table 2. Fruit set (percent) of two orchid species on a coffee plantation in central Veracruz.∗ Treatment Species Maxillaria densa Scaphyglottis livida

autogamy (n)

self-pollination (n)

cross-pollination (n)

natural pollination (n)

0.0c (88) 0.0c (94)

1.1c (89) 15.9b (69)

42.7a (89) 17.4b (69)

18.2b (362) 35.5a (200)

∗ Numbers in parentheses are the number of flowers used per treatment. Different letters in a row indicate significant differences between percentages (χ 2 Tukey-like test).

study site was similar to that found in some primary forest of the region. For example, M. densa occurs in 22% of the LMCF trees and in 43% of the oak-forest trees (Hietz & Hietz-Seifert 1995); J. teretifolia is present on 3.2% to 49% of the LMCF trees (Flores-Palacios 2003) and in all trees in a LMCF (Hietz & Hietz-Seifert 1995); and S. livida occurs on 26% to 43% of oak-forest trees (Hietz & Hietz-Seifert 1995). The orchid frequency and abundance we observed suggests that the target orchids are as successful in the coffee plantation as they are in their native habitats.

metric distribution or disappear if the population size is small (