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Phenology and pollination of Manilkara zapota in forest and homegardens
Forest Ecology and Management 248 (2007) 136–142 www.elsevier.com/locate/foreco
Phenology and pollination of Manilkara zapota in forest and homegardens Luis Salinas-Peba, Victor Parra-Tabla * Departamento de Ecologı´a Tropical, Campus de Ciencias Biolo´gicas y Agropecuarias, Universidad Auto´noma de Yucata´n, Km. 15.5, Carretera Me´rida-Xmatkuil, 4-116 Itzimna´, Yucata´n 97000, Mexico Received 19 February 2007; received in revised form 23 April 2007; accepted 25 April 2007
Abstract Knowledge on reproductive phenology and pollination biology are basic elements that should be considered in the management and exploitation of plant species that offer non-timber products. The tropical tree Manilkara zapota is a species from which non-timber products have been obtained for centuries by Mayan communities in Mexico. Nevertheless, there are no quantitative reports on its reproductive biology and the factors that limit fruit production. The present study describes the reproductive phenology, breeding system and pollination of this species in two contrasting environments: medium-height, subdeciduous forest, and homegardens (‘‘solares’’) in a Mayan community in the state of Yucatan. Significant differences were found between environments both in the temporal distribution of flower and mature fruit production, as well as in the proportion of mature fruits. Homegarden trees showed the greatest fruit production, although flower production did not differ between environments. Mature fruits were of better quality (i.e., greater fresh weight) in homegardens. Hand pollination experiments showed that M. zapota is self-compatible, and that there is pollinator limitation for fruit production in trees that grow in homegardens. We propose that water and soil nutrients are the main factors limiting M. zapota fruit production in forests, while in homegardens the main factor appears to be pollinator availability. # 2007 Elsevier B.V. All rights reserved. Keywords: Homegardens; Manilkara zapota; Mexico; Non-timber products; Plant breeding system; Reproductive phenology; Tropical tree; Yucata´n
1. Introduction For centuries rural Mayan communities of the Yucatan Peninsula have depended on the exploitation of natural resources from tropical forests and on the implementation of productive systems called ‘‘solares’’ (i.e., homegardens) in order to satisfy their basic subsistence needs. Some of these resources include the use of non-timber products such as leaves, fruits, resins, etc., which are used for direct consumption, medicine, and utensil and craft elaboration (Ros-Tonen, 2000; La Torre-Cuadros and Islebe, 2003). During the last decade, the use of non-timber products has been proposed as key conservation strategy in tropical forests, as well as an approach to improve life quality in rural communities (Michael and Ruiz, 2001; Paumgarten, 2005). Nevertheless, information on the reproductive biology for many tropical tree species is usually scarce, and this limits the development and implementation of management strategies for these species (Ashton and Bawa,
* Corresponding author. Tel.: +52 999 942 32 06; fax: +52 999 942 32 06. E-mail address: [email protected] (V. Parra-Tabla). 0378-1127/$ – see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2007.04.046
1990; Bawa et al., 1990; Kress and Beach, 1994). Specifically, for tropical tree species used for fruit production, there are no detailed descriptions on the reproductive phenology patterns, breeding systems, factors limiting productivity, as well as knowledge on how these factors are modified in managed systems (Bawa and Hadley, 1991). Homegradens are production systems found throughout the tropics, in which selection of plant species takes place for consumption and medicine production purposes (La TorreCuadros and Islebe, 2003). Homegardens can be considered environments in which plant resources are less limited compared to the original environments in which the species naturally occur (e.g., forests). The reason for this is that plants in homegardens are subject to selective pruning, irrigation, as well as fertilization from animal and plant wastes, which are recycled, in situ (Nair, 1992; Benjamin et al., 2001). In contrast, the same species in tropical forests can exhibit lower growth and reproductive rates due to reduced water availability, nutrients and light (Borchert, 1994). For hundreds of years the tropical tree Manilkara zapota has represented an important species for many rural communities in southeast Mexico because its fruits are highly valued for human
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consumption, and the latex is used for gum production (La Torre-Cuadros and Islebe, 2003). In the eastern portion of the state of Yucatan, M. zapota is a common species found in homegardens of Mayan communities. Nevertheless, despite traditional management practices, there is limited knowledge on its breeding system, factors limiting fruit production, as well as variation in reproductive phenology and output across contrasting environments (e.g., homegardens versus forests). Given the previous, the present study addresses the following: (1) describe the reproductive phenology of M. zapota, (2) determine its reproductive system (i.e., is it self-compatible?), and (3) determine if there is pollinator limitation in fruit production, and evaluate if this constraining factor varies across contrasting environments (i.e., homegardens and forest). 2. Materials and methods 2.1. Study species M. zapota is a tropical tree that reaches 10–20 m in height, and is distributed from central Mexico to the Yucatan Peninsula and Central America. It is a co-dominant species in high evergreen forests and medium-height subdeciduous forests (Pennington, 1991; Cairns et al., 2003; Cruz-Rodrı´guez and Lo´pez-Mata, 2004). Several non-timber products are obtained from this species, such as latex, which is used for gum production. Fruits collected in homegardens are commonly sold by local families, and leaves have medicinal properties (La Torre-Cuadros and Islebe, 2003). It produces solitary flowers clumped at the end of stems; sepals are brownish–greenish in color, and the corolla is white and 10 mm in length. The flower has six stamens (ca. 3 mm in length) inserted in the corolla tube. The style is larger than the corolla, and the stigma is small and simple (<5 mm). Flowers present protoginy (i.e., stigma maturation occurs first). Fruits are oval, from 4 to 10 cm in diameter, and have a fleshy brown-colored pulp with five seeds (Pennington, 1991). M. zapota can produce flowers and fruits throughout the whole year, although there is a considerable decrease during the dry season (December–May). It is during the rainy season (June–October) when the study species’ reproductive display is greatest (Mizrahi et al., 2001); this study focuses on the latter season. Based on studies done in India (Sambamurty and Ramalingham, 1954; Reddi, 1989) species from the genus Thrips act as pollinators of M. zapota, while bees appear to be inefficient pollinators. In our study region, bee species of Euglosa and Trigona (e.g., Trigona nigra), as well as members of Lepidoptera and Coleoptera are the most common floral visitors and potential pollinators (L. Salinas, pers. observ.). M. zapota trees are introduced to homegardens from seed or cuttings and in some cases are previously present before homegarden establishment. 2.2. Study area Field work was conducted in the eastern portion of the state of Yucatan, in a village named ‘‘Poop’’ (208210 24.8900 N,
Fig. 1. Area and study site.
888180 05.1800 W; Fig. 1). Mean annual temperature is 25.6 8C, and mean annual precipitation 1229.4 mm, with a monthly average of 34.7 mm. The vegetation type is subdeciduous medium-height forest (Flores and Espejel, 1994), which has been exploited by local villagers for agricultural purposes, resulting in several patches of successional vegetation spanning from 15 to 35 years of age (Mizrahi et al., 2001). Homegardens, along with forest patches, represent areas that provide an important source of food and medicines for local people (La Torre-Cuadros and Islebe, 2003). In addition, homegardens also represent a source of income to villagers as several vegetable species are grown in them such as: raddish (Raphanus sativus), pumpkin (Cucurbita sp.), pepper (Capsicum sp.) and tomato (Lycopersicun esculentum), as well as some fruit trees such as plum (Spondias purpurea), white ‘‘nance’’ (Byrsonima bucidaefolia), and ‘‘ramon’’ (Brosimum alicastrum), among others (Mizrahi et al., 2001). Some of the most common management activities practiced in homegardens include: raising of animals for self-consumption (i.e., birds and pigs), tree pruning, elimination of non-desired herbaceous plants, cleaning and burning of plant material, and irrigation (HerreraCastro, 1994). These activities create an environment of low plant competition for nutrients, light and water (Benjamin et al., 2001). 2.3. Reproductive phenology of M. zapota In order to describe and quantify the reproductive phenology of M. zapota, we selected 30 adult trees, 15 in homegardens, and 15 in a portion of subdeciduous forest located 500 m from ‘‘Poop’’. Trees in homegardens were selected from 12 different backyards randomly selected within the village, and were already present before the establishment of the homegardens by local villagers. In order to avoid tree size differences between environments, we used trees that had similar dbh (diameter at breast height, cm; homegarden: 25.2 8.4; forest: 24.01 9.6;
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t28 = 0.35, P = 0.7) and crown cover, m2 (homegarden: 16.54 5.1; forest: 19.26 5.8; t28 = 1.36, P = 0.18). In order to collect fruits, we established four 1 m2 nets beneath the canopy of each study tree in early June of 2004, and these were visited weekly from mid-June until the end of October (period of greatest flower production; Mizrahi et al., 2001). During these visits we counted flowers, aborted fruits and mature fruits, from which we estimated the proportion of mature fruits (no. of mature fruits/no. of flowers). Flower number was obtained from the total count of reproductive structures (flower buds + aborted flowers + aborted fruits + mature fruits). We measured fresh weight of mature fruits based on a random sample of 10 different homegarden (n = 92) and 12 forest (n = 107) trees. In order to compare possible differences in the temporal distribution of flower, aborted fruit and mature fruit number between environments we used a Mann–Whitney u-test (Zar, 1996). To evaluate differences between environments (homegarden versus forest) in the number of flowers, mature fruits and aborted fruits, fruit weight and the proportion of mature fruits we used t-tests (Zar, 1996). 2.4. Breeding system To understand the pollination system in M. zapota, as well as reproductive success differences across environments, we conducted an artificial pollination experiment with two levels: self-pollination using pollen from the same flower (i.e., autogamy), and cross-pollination using pollen from flowers of other trees in the same environment (forest patch or homegarden). Each pollination treatment was applied to three inflorescences per tree, and 10 study trees were used per environment. After treatment application, inflorescences were isolated with bags to avoid additional pollination events from an unknown source. Inflorescences were monitored until fruit formation and maturation. To evaluate environment and treatment effects on the proportion of mature fruits produced (no. of fruits/no. of flowers) we used a two-way ANOVA (environment, pollination treatment), and each tree was considered a block. Mature fruit data was arcsin transformed to achieve normality (Zar, 1996).
influenced by other post-pollination events, which limit fruit filling (e.g., bottom-up effects) and thus confound results pertaining pollinator limitation (Herrera, 2002). We assumed that if the proportion of initiated fruits was lower for the natural pollination treatment, then there is pollinator limitation (Bawa and Webb, 1984). All analyses were performed with SYSTAT, ver. 10.0 (SYSTAT, 2000). Data on initiated fruits was arcsin transformed to achieve normality (Zar, 1996). 3. Results 3.1. Reproductive phenology of M. zapota For both homegarden and forest trees flowering starts at the end of the dry season (June), and flowering peaks during August and September (Fig. 2A). In homegardens we observed two flowering peaks, one at the start of June, and the other at the start of September (Fig. 2A). On the other hand, forest trees started flowering in mid June, and peaked during August (Fig. 2A). We observed significant differences between environments in the temporal distribution of flower number (x2 = 55.47, P < 0.001). However, the average number of flowers produced per tree did not differ between environments (homegardens: 404.06 570.20; forest: 307.7 520.92; t = 0.93, P = 0.35).
2.5. Pollinator limitation To determine the presence pollinator limitation, as well as differences among environments, we used 10 trees from each environment and marked four inflorescences per tree, two of which were randomly assigned to one of the following pollination treatment levels: natural (open) and hand (artificial) pollination. For hand pollination, we used pollen from at least three different trees from the same environment; once pollinated, flowers were excluded from pollinators using plastic bags. For the natural pollination treatment, inflorescences were marked but not bagged. We used a two-way ANOVA to test for environment and pollination treatment effects on the proportion of initiated fruits (no. of initiated fruits/no. of flowers). We used proportion of initiated fruits as response variable because the proportion of mature fruits can be
Fig. 2. Average (2S.E.) number of flowers and mature fruits produced by Manilkara zapota in (A) homegardens and (B) forest, in the locality of Poop, Yucata´n, Mexico. Note scale differences between environments.
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Table 1 Analysis of variance results for Manilkara zapota pollinator limitation experiment for proportion of initiated fruits, using environment (forest vs. homegardens), pollination treatment (natural vs. artificial pollination), and tree as main effects
Fig. 3. Production of mature fruits (mean 1S.D.) in M. zapota for pollination treatments (self-pollination, and cross-pollination) in two environments (forest and homegardens) in Poop, Yucata´n, Mexico.
The temporal distribution of mature fruit number differed between environments (x2 = 113.73, P < 0.001). Mature fruit production in homegardens started by late June, and peaked in early September, after which it decreased considerably (Fig. 2B). In contrast, fruit production in the forest was markedly lower compared to that in homegardens and exhibited two peaks, one in July and the other in September (Fig. 2B). The average number of mature fruits was significantly greater for homegarden trees (23.73 23.93) compared to forest trees (2.06 3.50) (t = 4.62, P < 0.05). Likewise, mature fruit set (no. of mature fruits/no. of flowers) was greater in homegardens (0.10 0.07) compared to the forest (0.03 0.06) (t = 3.4, P < 0.001). Fresh weight (g) of mature fruits was also greater in homegardens (74.77 36.66) compared to forest (58.76 20.82) (t = 4.44, P < 0.01).
Source
SS
df
MS
F
P
Environment Treatment Environment treatment Block (tree) Error
0.58 0.12 0.08 0.06 0.46
1 1 1 9 27
0.58 0.12 0.08 0.007 0.017
33.5 7.2 4.7 0.4
<0.01 0.02 0.04 0.92
3.3. Effect of pollinator limitation Significant environment, treatment and environment by treatment effects were observed for the proportion of initiated fruits (Table 1). The proportion of initiated fruits was significantly greater in the forest (P < 0.05; Tukey test; Fig. 4), and the artificial pollination experiment showed that M. zapota is pollinator-limited as the proportion of initiated fruits was significantly lower for open-pollinated flowers (P < 0.05; Tukey test). However, the significant interaction shows that pollinator limitation depends on the environment (Table 1, Fig. 4): the proportion of initiated fruits in forest trees was the same between pollination treatments (P > 0.05, Tukey test), however, in homegardens, hand-pollinated flowers had a lower proportion of initiated fruits compared to open-pollinated flowers (P < 0.05; Tukey test, Fig. 4). 4. Discussion 4.1. Reproductive phenology of M. zapota
3.2. Breeding system No significant differences were observed due to environment, pollination treatment, and block effects, or their interaction on the proportion of mature fruits (F 2.3, P > 0.1 in all cases). The artificial pollination experiment defined M. zapota as a self-compatible species, because flowers subject to self-pollination produced an equal proportion of mature fruits compared to cross-pollinated flowers (Fig. 3).
Fig. 4. Interaction between environment and treatment effects for the proportion of initiated fruits (mean 2S.D.) in M. zapota, in two environments (forest and homegardens) in Poop, Yucatan, Mexico.
The reproductive phenology of M. zapota coincided with flowering and fruiting periods reported for other tree species in tropical dry forests (e.g., Bullock and Solis-Magallanes, 1990; Bullock, 1995). However, widely distributed tropical tree species such as M. zapota have shown variation in their reproductive phenology patterns which can be explained by seasonality in precipitation and water availability (Borchert et al., 2004). The comparison between trees in homegardens and forests revealed important qualitative and quantitative differences among environments. Flowering started several days earlier and peaked twice in homegardens, and although trees in this environment produced on average the same number of flowers than those in forests, total (absolute) fruit production, and the probability of a flower converting into a mature fruit was markedly higher in homegardens. Likewise, fruit fresh weight was also greater in homegardens compared to forest. Mature fruit output and reproductive phenology differences between environments could be due to greater nutrient and water availability in homegardens. Plants in homegardens are subject to active use and management, which involves yearlong irrigation, as well as constant deposition of fertilizing material from animals (Ferna´ndez and Nair, 1986; Benjamin et al., 2001). In addition, it has been shown that the tradition of continually burning dry foliage in homegardens accelerates
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nutrient cycling in the soil (Benjamin et al., 2001; Xuluc-Tolosa et al., 2003). In contrast, nutrient availability and renewal in seasonally dry tropical forests depends only on dry foliage deposition, and water availability is restricted to the rainy season (Bullock, 1995). Water availability in homegardens is virtually constant throughout the year because not only do trees obtain this resource during the rainy season, but also from periodic irrigation, personal hygiene activities, and cleaning of utensils and clothes (Herrera-Castro, 1994). Thus, greater water availability in homegardens not only allows trees to make a greater use of this resource, but also makes nutrients more available to plants (Holbrook et al., 1995). Tree species from seasonally dry tropical forests have shown shorter flowering and fruiting seasons, as well as multiple cycles within a given year (Bullock, 1995; Kudo and Suzuki, 2004), and artificial irrigation and abnormal rains during the dry season can extend or induce earlier flowering seasons (e.g., Domı´nguez and Dirzo, 1995; Tissue and Wright, 1995; Parra-Tabla and Bullock, 1998). For M. zapota, we observed earlier flowering for homegarden trees, as well as two flowering peaks (June–July, and September), which is to some extent evidence of a certain degree of plasticity in reproductive phenology patterns in response to variation in water availability (Borchert et al., 2004). Thus, water ‘‘surplus’’ in homegardens compared to forests, and its subsequent effects on nutrient cycling dynamics, might explain differences in reproductive phenology dynamics, as well as fruit production between environments. Nevertheless, experiments with artificial fertilization and irrigation are necessary to confirm this hypothesis (Parra-Tabla and Bullock, 1998). 4.2. Breeding system in M. zapota Artificial pollination experiments showed that M. zapota is self-compatible. It has been suggested that self-compatibility is common in tropical tree species because individuals are commonly isolated (i.e., low population densities) (Bullock, 1995; Cascante et al., 2002). Thus, self-compatibility assures reproductive success under low conspecific and pollinator availability (Kalisz and Vogler, 2003). Generally, plant species with large flower displays (e.g., tropical trees) exhibit high geitonogamy levels because pollinators tend to focus on one individual and visit as many flowers as they can within the same tree in order to minimize foraging costs. This might be another cause that could explain self-compatibility in this species for which large floral displays and high rates of geitonogamy have been observed (L. Salinas, pers. observ.). Several pollination studies with M. zapota in India have suggested Thrips spp. as possible pollinators (Reddi, 1989), as bees have shown not to be efficient pollinators (Sambamurty and Ramalingham, 1954). Nevertheless, preliminary observations in this study suggest that native bee species of Trigona can act as efficient pollen vectors due to their abundance and commonly observed pollen loads subsequent to flower visitation (L. Salinas, pers. observ.). Likewise, we also observed Thysanoptera inside flowers, which suggests that
members of this group can also act as pollinators. Two aspects of M. zapota pollination biology in Yucata´n are still pending: (a) differentiate effective pollinators from floral visitors which do not pollinate and (b) consequences of the breeding system on genetic variation of natural versus homegarden populations. 4.3. Pollinator limitation in M. zapota We observed pollinator limitation for initiated fruits in M. zapota only in homegardens, which suggests lower activity and/ or abundance of pollinators in this environment. Results showed that manually pollinated flowers in homegardens had almost twice the probability of initiating fruits than naturally pollinated flowers. A possible reason for this difference could be the management given to plants in homegardens, because undesired herbs are constantly removed, and tree pruning as well as burning of plant material represent activities that can cause a reduction in the abundance of pollinators. In addition, pollinator limitation in homegardens could be also due to tree isolation. Several studies have shown that pollinators prefer sites with high availability of floral resources (e.g, Bawa et al., 1985). In contrast, pollinators can obtain greater floral rewards in the forest because distance between trees is shorter and other species they depend on are also flowering and thus maintain pollinator populations (Franceschinelli and Bawa, 2000). At the landscape level, homegardens can be considered fragments in which the distribution of species is not continuous. In this way, it has been shown that tropical trees are vulnerable to fragmentation (Cascante et al., 2002; Fuchs et al., 2003), and there is evidence that plant species located in agricultural areas exhibit reductions in their fruit production (e.g., Parra-Tabla et al., 2000). It has been commonly reported that tropical trees are pollinator-limited in natural systems (Bawa and Webb, 1984; Bullock et al., 1989), in this study we found that M. zapota trees in the forest are apparently not pollinator-limited, as artificial pollination did not increase the proportion of initiated fruits compared to naturally pollinated flowers. This might indicate that fragmentation effects on pollinator limitation of M. zapota trees in forests at the study area are of lower magnitude than those experienced by homegarden trees. However, further fragmentation events in surrounding forests, might lead to similar levels of pollinator limitation between environments. Together, the results suggest that constraints to fruit production in M. zapota are due to different reasons in each environment. Homegarden management by local people increases water and nutrient availability, results in a greater fruit production and individual fruit mass. In contrast, reduced mature fruit production in the forest might be due to lower nutrient availability, although greater pollinator abundance allows for a higher proportion of initiated fruits. This pattern indicates that although homegarden trees show a lower proportion of initiated fruits, they are able to assure maturation of a greater proportion of those fruits (>3 times), resulting in a greater absolute fruit production compared to M. zapota trees found in forests (7 times greater).
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5. Conclusion The sustainable use of non-timber products in forests or managed systems such as homegardens, depends on knowledge about basic aspects of the plant’s reproductive biology. Our study indicates that, in order to increase fruit production of M. zapota in homegardens for self-consumption and commercialization, more attention should be paid to pollinator conservation. In contrast, if the goal is fruit extraction from trees in forests, and given lower fruit production in this environment, it will be important to conserve a proportion of the fruits in each tree unharvested in order to assure the maintenance of natural populations. Acknowledgements We thank Luis Abdala, Salvador Flores, Aliza Mizrahi, Rocı´o Ruenes, Carmen Salazar, Fabia´n Vargas and two anonymous reviewers for their valuable comments. Special thanks to Luis Abdala for his Spanish to English translation help. References Ashton, P., Bawa, K., 1990. Reproductive biology and tree improvement programs commentary. In: Bawa, K.S., Hadley, (Eds.), Reproductive Ecology of Tropical Forest Plants. Man and the Biosphere Series, vol. 7. UNESCO. Bawa, K.S., Hadley, M., 1991. Reproductive ecology of tropical forest plants. Man and the Biosphere Series, vol. 7. UNESCO. Bawa, K., Webb, C.J., 1984. Flower, fruit and seed abortion in tropical forest trees: implications for the evolution of paternal and maternal reproductive patterns. Am. J. Bot. 71, 736–751. Bawa, K., Bullock, S., Perry, D.R., Coville, R.E., Grayum, M.H., 1985. Reproductive biology of tropical lowland rain forest trees. II. Pollination systems. Am. J. Bot. 72, 331–345. Bawa, K., Ashton, P., Salleh Mohd, N., 1990. Reproductive ecology of tropical forest plants: management issues. In: Bawa, K.S., Hadley, (Eds.), Reproductive Ecology of Tropical Forest Plants. Man and the Biosphere Series, vol. 7. UNESCO. Benjamin, T.J., Montan˜ez, P.I., Jime´nez, J.J.M., Gillespie, A.R., 2001. Carbon, water and nutrient flux in Maya homegardens in the Yucatan Peninsula of Me´xico. Agroforest. Syst. 53, 103–111. Borchert, R., 1994. Soil and stem water storage determine phenology and distribution of tropical dry forest trees. Ecology 75, 1437–1449. Borchert, R., Meyer, S., Felger, R., Porter-Bolland, L., 2004. Environmental control of flowering periodicity in Costa Rican and Mexican tropical dry forests. Global Ecol. Biogeogr. 13, 409–425. Bullock, S.H., 1995. Plant reproduction in neotropical dry forests. In: Bullock, S.H., Mooney, H.A., Medina, E. (Eds.), Seasonally Dry Tropical Forests. Cambridge University Press, Cambridge U.S.A, pp. 203– 277. Bullock, S.H., Solis-Magallanes, 1990. Phenology of canopy trees of a tropical deciduous forest in Mexico. Biotropica 22, 22–35. Bullock, S., Martı´nez del Rı´o, C., Ayala, R., 1989. Bee visitation rates to trees of Prockia crucis differing in flower number. Oecologia 78, 389– 393. Cairns, M.A., Olmsted, I., Granados, J., Argaez, J., 2003. Composition and aboveground tree biomass of a dry semi-evergreen forest on Mexico’s Yucatan Peninsula. Forest Ecol. Manage. 186, 125–132. Cascante, A., Quesada, M., Lobo, J., Fuchs, E., 2002. Effects of dry tropical forest fragmentation on the reproductive success and genetic structure of the tree Samanea saman. Conserv. Biol. 16, 137–147.
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Phenology and pollination of Manilkara zapota in forest and homegardens Luis Salinas-Peba, Victor Parra-Tabla * Departamento de Ecologı´a Tropical, Campus de Ciencias Biolo´gicas y Agropecuarias, Universidad Auto´noma de Yucata´n, Km. 15.5, Carretera Me´rida-Xmatkuil, 4-116 Itzimna´, Yucata´n 97000, Mexico Received 19 February 2007; received in revised form 23 April 2007; accepted 25 April 2007
Abstract Knowledge on reproductive phenology and pollination biology are basic elements that should be considered in the management and exploitation of plant species that offer non-timber products. The tropical tree Manilkara zapota is a species from which non-timber products have been obtained for centuries by Mayan communities in Mexico. Nevertheless, there are no quantitative reports on its reproductive biology and the factors that limit fruit production. The present study describes the reproductive phenology, breeding system and pollination of this species in two contrasting environments: medium-height, subdeciduous forest, and homegardens (‘‘solares’’) in a Mayan community in the state of Yucatan. Significant differences were found between environments both in the temporal distribution of flower and mature fruit production, as well as in the proportion of mature fruits. Homegarden trees showed the greatest fruit production, although flower production did not differ between environments. Mature fruits were of better quality (i.e., greater fresh weight) in homegardens. Hand pollination experiments showed that M. zapota is self-compatible, and that there is pollinator limitation for fruit production in trees that grow in homegardens. We propose that water and soil nutrients are the main factors limiting M. zapota fruit production in forests, while in homegardens the main factor appears to be pollinator availability. # 2007 Elsevier B.V. All rights reserved. Keywords: Homegardens; Manilkara zapota; Mexico; Non-timber products; Plant breeding system; Reproductive phenology; Tropical tree; Yucata´n
1. Introduction For centuries rural Mayan communities of the Yucatan Peninsula have depended on the exploitation of natural resources from tropical forests and on the implementation of productive systems called ‘‘solares’’ (i.e., homegardens) in order to satisfy their basic subsistence needs. Some of these resources include the use of non-timber products such as leaves, fruits, resins, etc., which are used for direct consumption, medicine, and utensil and craft elaboration (Ros-Tonen, 2000; La Torre-Cuadros and Islebe, 2003). During the last decade, the use of non-timber products has been proposed as key conservation strategy in tropical forests, as well as an approach to improve life quality in rural communities (Michael and Ruiz, 2001; Paumgarten, 2005). Nevertheless, information on the reproductive biology for many tropical tree species is usually scarce, and this limits the development and implementation of management strategies for these species (Ashton and Bawa,
* Corresponding author. Tel.: +52 999 942 32 06; fax: +52 999 942 32 06. E-mail address: [email protected] (V. Parra-Tabla). 0378-1127/$ – see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2007.04.046
1990; Bawa et al., 1990; Kress and Beach, 1994). Specifically, for tropical tree species used for fruit production, there are no detailed descriptions on the reproductive phenology patterns, breeding systems, factors limiting productivity, as well as knowledge on how these factors are modified in managed systems (Bawa and Hadley, 1991). Homegradens are production systems found throughout the tropics, in which selection of plant species takes place for consumption and medicine production purposes (La TorreCuadros and Islebe, 2003). Homegardens can be considered environments in which plant resources are less limited compared to the original environments in which the species naturally occur (e.g., forests). The reason for this is that plants in homegardens are subject to selective pruning, irrigation, as well as fertilization from animal and plant wastes, which are recycled, in situ (Nair, 1992; Benjamin et al., 2001). In contrast, the same species in tropical forests can exhibit lower growth and reproductive rates due to reduced water availability, nutrients and light (Borchert, 1994). For hundreds of years the tropical tree Manilkara zapota has represented an important species for many rural communities in southeast Mexico because its fruits are highly valued for human
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consumption, and the latex is used for gum production (La Torre-Cuadros and Islebe, 2003). In the eastern portion of the state of Yucatan, M. zapota is a common species found in homegardens of Mayan communities. Nevertheless, despite traditional management practices, there is limited knowledge on its breeding system, factors limiting fruit production, as well as variation in reproductive phenology and output across contrasting environments (e.g., homegardens versus forests). Given the previous, the present study addresses the following: (1) describe the reproductive phenology of M. zapota, (2) determine its reproductive system (i.e., is it self-compatible?), and (3) determine if there is pollinator limitation in fruit production, and evaluate if this constraining factor varies across contrasting environments (i.e., homegardens and forest). 2. Materials and methods 2.1. Study species M. zapota is a tropical tree that reaches 10–20 m in height, and is distributed from central Mexico to the Yucatan Peninsula and Central America. It is a co-dominant species in high evergreen forests and medium-height subdeciduous forests (Pennington, 1991; Cairns et al., 2003; Cruz-Rodrı´guez and Lo´pez-Mata, 2004). Several non-timber products are obtained from this species, such as latex, which is used for gum production. Fruits collected in homegardens are commonly sold by local families, and leaves have medicinal properties (La Torre-Cuadros and Islebe, 2003). It produces solitary flowers clumped at the end of stems; sepals are brownish–greenish in color, and the corolla is white and 10 mm in length. The flower has six stamens (ca. 3 mm in length) inserted in the corolla tube. The style is larger than the corolla, and the stigma is small and simple (<5 mm). Flowers present protoginy (i.e., stigma maturation occurs first). Fruits are oval, from 4 to 10 cm in diameter, and have a fleshy brown-colored pulp with five seeds (Pennington, 1991). M. zapota can produce flowers and fruits throughout the whole year, although there is a considerable decrease during the dry season (December–May). It is during the rainy season (June–October) when the study species’ reproductive display is greatest (Mizrahi et al., 2001); this study focuses on the latter season. Based on studies done in India (Sambamurty and Ramalingham, 1954; Reddi, 1989) species from the genus Thrips act as pollinators of M. zapota, while bees appear to be inefficient pollinators. In our study region, bee species of Euglosa and Trigona (e.g., Trigona nigra), as well as members of Lepidoptera and Coleoptera are the most common floral visitors and potential pollinators (L. Salinas, pers. observ.). M. zapota trees are introduced to homegardens from seed or cuttings and in some cases are previously present before homegarden establishment. 2.2. Study area Field work was conducted in the eastern portion of the state of Yucatan, in a village named ‘‘Poop’’ (208210 24.8900 N,
Fig. 1. Area and study site.
888180 05.1800 W; Fig. 1). Mean annual temperature is 25.6 8C, and mean annual precipitation 1229.4 mm, with a monthly average of 34.7 mm. The vegetation type is subdeciduous medium-height forest (Flores and Espejel, 1994), which has been exploited by local villagers for agricultural purposes, resulting in several patches of successional vegetation spanning from 15 to 35 years of age (Mizrahi et al., 2001). Homegardens, along with forest patches, represent areas that provide an important source of food and medicines for local people (La Torre-Cuadros and Islebe, 2003). In addition, homegardens also represent a source of income to villagers as several vegetable species are grown in them such as: raddish (Raphanus sativus), pumpkin (Cucurbita sp.), pepper (Capsicum sp.) and tomato (Lycopersicun esculentum), as well as some fruit trees such as plum (Spondias purpurea), white ‘‘nance’’ (Byrsonima bucidaefolia), and ‘‘ramon’’ (Brosimum alicastrum), among others (Mizrahi et al., 2001). Some of the most common management activities practiced in homegardens include: raising of animals for self-consumption (i.e., birds and pigs), tree pruning, elimination of non-desired herbaceous plants, cleaning and burning of plant material, and irrigation (HerreraCastro, 1994). These activities create an environment of low plant competition for nutrients, light and water (Benjamin et al., 2001). 2.3. Reproductive phenology of M. zapota In order to describe and quantify the reproductive phenology of M. zapota, we selected 30 adult trees, 15 in homegardens, and 15 in a portion of subdeciduous forest located 500 m from ‘‘Poop’’. Trees in homegardens were selected from 12 different backyards randomly selected within the village, and were already present before the establishment of the homegardens by local villagers. In order to avoid tree size differences between environments, we used trees that had similar dbh (diameter at breast height, cm; homegarden: 25.2 8.4; forest: 24.01 9.6;
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t28 = 0.35, P = 0.7) and crown cover, m2 (homegarden: 16.54 5.1; forest: 19.26 5.8; t28 = 1.36, P = 0.18). In order to collect fruits, we established four 1 m2 nets beneath the canopy of each study tree in early June of 2004, and these were visited weekly from mid-June until the end of October (period of greatest flower production; Mizrahi et al., 2001). During these visits we counted flowers, aborted fruits and mature fruits, from which we estimated the proportion of mature fruits (no. of mature fruits/no. of flowers). Flower number was obtained from the total count of reproductive structures (flower buds + aborted flowers + aborted fruits + mature fruits). We measured fresh weight of mature fruits based on a random sample of 10 different homegarden (n = 92) and 12 forest (n = 107) trees. In order to compare possible differences in the temporal distribution of flower, aborted fruit and mature fruit number between environments we used a Mann–Whitney u-test (Zar, 1996). To evaluate differences between environments (homegarden versus forest) in the number of flowers, mature fruits and aborted fruits, fruit weight and the proportion of mature fruits we used t-tests (Zar, 1996). 2.4. Breeding system To understand the pollination system in M. zapota, as well as reproductive success differences across environments, we conducted an artificial pollination experiment with two levels: self-pollination using pollen from the same flower (i.e., autogamy), and cross-pollination using pollen from flowers of other trees in the same environment (forest patch or homegarden). Each pollination treatment was applied to three inflorescences per tree, and 10 study trees were used per environment. After treatment application, inflorescences were isolated with bags to avoid additional pollination events from an unknown source. Inflorescences were monitored until fruit formation and maturation. To evaluate environment and treatment effects on the proportion of mature fruits produced (no. of fruits/no. of flowers) we used a two-way ANOVA (environment, pollination treatment), and each tree was considered a block. Mature fruit data was arcsin transformed to achieve normality (Zar, 1996).
influenced by other post-pollination events, which limit fruit filling (e.g., bottom-up effects) and thus confound results pertaining pollinator limitation (Herrera, 2002). We assumed that if the proportion of initiated fruits was lower for the natural pollination treatment, then there is pollinator limitation (Bawa and Webb, 1984). All analyses were performed with SYSTAT, ver. 10.0 (SYSTAT, 2000). Data on initiated fruits was arcsin transformed to achieve normality (Zar, 1996). 3. Results 3.1. Reproductive phenology of M. zapota For both homegarden and forest trees flowering starts at the end of the dry season (June), and flowering peaks during August and September (Fig. 2A). In homegardens we observed two flowering peaks, one at the start of June, and the other at the start of September (Fig. 2A). On the other hand, forest trees started flowering in mid June, and peaked during August (Fig. 2A). We observed significant differences between environments in the temporal distribution of flower number (x2 = 55.47, P < 0.001). However, the average number of flowers produced per tree did not differ between environments (homegardens: 404.06 570.20; forest: 307.7 520.92; t = 0.93, P = 0.35).
2.5. Pollinator limitation To determine the presence pollinator limitation, as well as differences among environments, we used 10 trees from each environment and marked four inflorescences per tree, two of which were randomly assigned to one of the following pollination treatment levels: natural (open) and hand (artificial) pollination. For hand pollination, we used pollen from at least three different trees from the same environment; once pollinated, flowers were excluded from pollinators using plastic bags. For the natural pollination treatment, inflorescences were marked but not bagged. We used a two-way ANOVA to test for environment and pollination treatment effects on the proportion of initiated fruits (no. of initiated fruits/no. of flowers). We used proportion of initiated fruits as response variable because the proportion of mature fruits can be
Fig. 2. Average (2S.E.) number of flowers and mature fruits produced by Manilkara zapota in (A) homegardens and (B) forest, in the locality of Poop, Yucata´n, Mexico. Note scale differences between environments.
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Table 1 Analysis of variance results for Manilkara zapota pollinator limitation experiment for proportion of initiated fruits, using environment (forest vs. homegardens), pollination treatment (natural vs. artificial pollination), and tree as main effects
Fig. 3. Production of mature fruits (mean 1S.D.) in M. zapota for pollination treatments (self-pollination, and cross-pollination) in two environments (forest and homegardens) in Poop, Yucata´n, Mexico.
The temporal distribution of mature fruit number differed between environments (x2 = 113.73, P < 0.001). Mature fruit production in homegardens started by late June, and peaked in early September, after which it decreased considerably (Fig. 2B). In contrast, fruit production in the forest was markedly lower compared to that in homegardens and exhibited two peaks, one in July and the other in September (Fig. 2B). The average number of mature fruits was significantly greater for homegarden trees (23.73 23.93) compared to forest trees (2.06 3.50) (t = 4.62, P < 0.05). Likewise, mature fruit set (no. of mature fruits/no. of flowers) was greater in homegardens (0.10 0.07) compared to the forest (0.03 0.06) (t = 3.4, P < 0.001). Fresh weight (g) of mature fruits was also greater in homegardens (74.77 36.66) compared to forest (58.76 20.82) (t = 4.44, P < 0.01).
Source
SS
df
MS
F
P
Environment Treatment Environment treatment Block (tree) Error
0.58 0.12 0.08 0.06 0.46
1 1 1 9 27
0.58 0.12 0.08 0.007 0.017
33.5 7.2 4.7 0.4
<0.01 0.02 0.04 0.92
3.3. Effect of pollinator limitation Significant environment, treatment and environment by treatment effects were observed for the proportion of initiated fruits (Table 1). The proportion of initiated fruits was significantly greater in the forest (P < 0.05; Tukey test; Fig. 4), and the artificial pollination experiment showed that M. zapota is pollinator-limited as the proportion of initiated fruits was significantly lower for open-pollinated flowers (P < 0.05; Tukey test). However, the significant interaction shows that pollinator limitation depends on the environment (Table 1, Fig. 4): the proportion of initiated fruits in forest trees was the same between pollination treatments (P > 0.05, Tukey test), however, in homegardens, hand-pollinated flowers had a lower proportion of initiated fruits compared to open-pollinated flowers (P < 0.05; Tukey test, Fig. 4). 4. Discussion 4.1. Reproductive phenology of M. zapota
3.2. Breeding system No significant differences were observed due to environment, pollination treatment, and block effects, or their interaction on the proportion of mature fruits (F 2.3, P > 0.1 in all cases). The artificial pollination experiment defined M. zapota as a self-compatible species, because flowers subject to self-pollination produced an equal proportion of mature fruits compared to cross-pollinated flowers (Fig. 3).
Fig. 4. Interaction between environment and treatment effects for the proportion of initiated fruits (mean 2S.D.) in M. zapota, in two environments (forest and homegardens) in Poop, Yucatan, Mexico.
The reproductive phenology of M. zapota coincided with flowering and fruiting periods reported for other tree species in tropical dry forests (e.g., Bullock and Solis-Magallanes, 1990; Bullock, 1995). However, widely distributed tropical tree species such as M. zapota have shown variation in their reproductive phenology patterns which can be explained by seasonality in precipitation and water availability (Borchert et al., 2004). The comparison between trees in homegardens and forests revealed important qualitative and quantitative differences among environments. Flowering started several days earlier and peaked twice in homegardens, and although trees in this environment produced on average the same number of flowers than those in forests, total (absolute) fruit production, and the probability of a flower converting into a mature fruit was markedly higher in homegardens. Likewise, fruit fresh weight was also greater in homegardens compared to forest. Mature fruit output and reproductive phenology differences between environments could be due to greater nutrient and water availability in homegardens. Plants in homegardens are subject to active use and management, which involves yearlong irrigation, as well as constant deposition of fertilizing material from animals (Ferna´ndez and Nair, 1986; Benjamin et al., 2001). In addition, it has been shown that the tradition of continually burning dry foliage in homegardens accelerates
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nutrient cycling in the soil (Benjamin et al., 2001; Xuluc-Tolosa et al., 2003). In contrast, nutrient availability and renewal in seasonally dry tropical forests depends only on dry foliage deposition, and water availability is restricted to the rainy season (Bullock, 1995). Water availability in homegardens is virtually constant throughout the year because not only do trees obtain this resource during the rainy season, but also from periodic irrigation, personal hygiene activities, and cleaning of utensils and clothes (Herrera-Castro, 1994). Thus, greater water availability in homegardens not only allows trees to make a greater use of this resource, but also makes nutrients more available to plants (Holbrook et al., 1995). Tree species from seasonally dry tropical forests have shown shorter flowering and fruiting seasons, as well as multiple cycles within a given year (Bullock, 1995; Kudo and Suzuki, 2004), and artificial irrigation and abnormal rains during the dry season can extend or induce earlier flowering seasons (e.g., Domı´nguez and Dirzo, 1995; Tissue and Wright, 1995; Parra-Tabla and Bullock, 1998). For M. zapota, we observed earlier flowering for homegarden trees, as well as two flowering peaks (June–July, and September), which is to some extent evidence of a certain degree of plasticity in reproductive phenology patterns in response to variation in water availability (Borchert et al., 2004). Thus, water ‘‘surplus’’ in homegardens compared to forests, and its subsequent effects on nutrient cycling dynamics, might explain differences in reproductive phenology dynamics, as well as fruit production between environments. Nevertheless, experiments with artificial fertilization and irrigation are necessary to confirm this hypothesis (Parra-Tabla and Bullock, 1998). 4.2. Breeding system in M. zapota Artificial pollination experiments showed that M. zapota is self-compatible. It has been suggested that self-compatibility is common in tropical tree species because individuals are commonly isolated (i.e., low population densities) (Bullock, 1995; Cascante et al., 2002). Thus, self-compatibility assures reproductive success under low conspecific and pollinator availability (Kalisz and Vogler, 2003). Generally, plant species with large flower displays (e.g., tropical trees) exhibit high geitonogamy levels because pollinators tend to focus on one individual and visit as many flowers as they can within the same tree in order to minimize foraging costs. This might be another cause that could explain self-compatibility in this species for which large floral displays and high rates of geitonogamy have been observed (L. Salinas, pers. observ.). Several pollination studies with M. zapota in India have suggested Thrips spp. as possible pollinators (Reddi, 1989), as bees have shown not to be efficient pollinators (Sambamurty and Ramalingham, 1954). Nevertheless, preliminary observations in this study suggest that native bee species of Trigona can act as efficient pollen vectors due to their abundance and commonly observed pollen loads subsequent to flower visitation (L. Salinas, pers. observ.). Likewise, we also observed Thysanoptera inside flowers, which suggests that
members of this group can also act as pollinators. Two aspects of M. zapota pollination biology in Yucata´n are still pending: (a) differentiate effective pollinators from floral visitors which do not pollinate and (b) consequences of the breeding system on genetic variation of natural versus homegarden populations. 4.3. Pollinator limitation in M. zapota We observed pollinator limitation for initiated fruits in M. zapota only in homegardens, which suggests lower activity and/ or abundance of pollinators in this environment. Results showed that manually pollinated flowers in homegardens had almost twice the probability of initiating fruits than naturally pollinated flowers. A possible reason for this difference could be the management given to plants in homegardens, because undesired herbs are constantly removed, and tree pruning as well as burning of plant material represent activities that can cause a reduction in the abundance of pollinators. In addition, pollinator limitation in homegardens could be also due to tree isolation. Several studies have shown that pollinators prefer sites with high availability of floral resources (e.g, Bawa et al., 1985). In contrast, pollinators can obtain greater floral rewards in the forest because distance between trees is shorter and other species they depend on are also flowering and thus maintain pollinator populations (Franceschinelli and Bawa, 2000). At the landscape level, homegardens can be considered fragments in which the distribution of species is not continuous. In this way, it has been shown that tropical trees are vulnerable to fragmentation (Cascante et al., 2002; Fuchs et al., 2003), and there is evidence that plant species located in agricultural areas exhibit reductions in their fruit production (e.g., Parra-Tabla et al., 2000). It has been commonly reported that tropical trees are pollinator-limited in natural systems (Bawa and Webb, 1984; Bullock et al., 1989), in this study we found that M. zapota trees in the forest are apparently not pollinator-limited, as artificial pollination did not increase the proportion of initiated fruits compared to naturally pollinated flowers. This might indicate that fragmentation effects on pollinator limitation of M. zapota trees in forests at the study area are of lower magnitude than those experienced by homegarden trees. However, further fragmentation events in surrounding forests, might lead to similar levels of pollinator limitation between environments. Together, the results suggest that constraints to fruit production in M. zapota are due to different reasons in each environment. Homegarden management by local people increases water and nutrient availability, results in a greater fruit production and individual fruit mass. In contrast, reduced mature fruit production in the forest might be due to lower nutrient availability, although greater pollinator abundance allows for a higher proportion of initiated fruits. This pattern indicates that although homegarden trees show a lower proportion of initiated fruits, they are able to assure maturation of a greater proportion of those fruits (>3 times), resulting in a greater absolute fruit production compared to M. zapota trees found in forests (7 times greater).
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