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Tropical Biology |
2Universidad de Costa Rica, Escuela de Biología, San Pedro, Costa Rica; 3Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México, Campus Morelia, Apartado Postal 27-3 (Xangari), Morelia, Michoacán, México 58089
Received for publication November 8, 2002. Accepted for publication February 4, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Bombacaceae • Costa Rica • Mexico • nectarivorous bats • Neotropics • phenology • plant reproduction • pollinator competition
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Borchert, 1994
; but see Wright and Cornejo, 1990
; Wright, 1991
), seasonal variations in rainfall (Opler et al., 1976
), changes in temperature (Ashton et al., 1988
; Williams-Linera, 1997
), photoperiod (Leopold, 1951
; Tallak Nilsen and Huller, 1981
; van Schaik, 1986
; Rivera et al., 2002
), irradiance (Wright and van Schaik, 1994
), and sporadic climatic events (Sakai et al., 1999
) have been mentioned as proximate causes triggering phenological events in tropical plants. In forests with a marked dry season, changes in water availability from shifts in precipitation regimes and soil moisture have been proposed as the essential proximate and ultimate causes affecting phenological patterns (Reich and Borchert, 1984
; Borchert, 1994
).
In contrast, biotic factors, such as competition for pollinators or pollinator attraction (Robertson, 1895
; Janzen, 1967
; Gentry, 1974
; Stiles, 1975
; Augspurger, 1981
; Appanah, 1985
; Murray et al., 1987
; Sakai et al., 1999
), competition for seed dispersers (Snow, 1965
), and avoidance of herbivory (Marquis, 1988
; Aide, 1993
; van Schaik et al., 1993
; Coley and Barone, 1996
) have been interpreted as ultimate causes responsible for phenological patterns in tropical species. Biotic factors have been suggested as affecting phenological synchronization between species within the same guild (Frankie et al., 1974
; Stiles 1977
).
Finally, some studies have suggested that plant phenology is principally constrained by phylogenetic membership or life form (Kochmer and Handel, 1986
; Wright and Calderón, 1995
). This hypothesis supports the idea that phylogenetic constraints are stronger than local selective pressure, thus members of the same taxa should have similar phenological patterns regardless of geographical location (Kochmer and Handel, 1986
).
Few studies have evaluated proximate and ultimate causes of phenological patterns of plants in different environments or geographic regions and most of these studies compared communities (Frankie et al., 1974
; van Schaik et al., 1993
; Murali and Sukumar, 1994
). Frankie et al. (1974)
reported that greatest leaf fall corresponded to the driest periods both in wet (La Selva) and dry forests (Comelco) in Costa Rica. This study concluded that synchronization in flowering during particular seasons depended on climatic conditions. Nonetheless, they suggest that biotic factors, such as competition for pollinators, also may have a subtle but important influence on flowering phenology. Another study comparing two tropical dry forest sites with different annual rainfall in southern India concluded that phenological patterns depend upon precipitation (Murali and Sukumar, 1994
). However, they recognized the importance of ultimate causes and suggested that in some species flowering phenology might be determined by competition for pollinators.
Comparative phenological studies of plants of the same taxa over different geographic locations that vary in climatic conditions or pollinator assemblages may help to establish the relative importance of different hypotheses to explain phenological patterns. These comparisons will determine if phenological variation is due to changes in climatic conditions between sites or are a response to biological factors such as competition for pollinators within sites. This study focuses on phenological patterns of tree species of the family Bombacaceae in three seasonal forests in Mexico and Costa Rica that vary in dry season duration and intensity. Our objectives include (1) determining intraspecific variation in phenology between sites in different geographic locations with different precipitation regimes, (2) comparing interspecific phenological patterns within sites during one year, and (3) documenting seasonal pollinator use of floral resources at one site in relation to the flowering phenology of these species.
If the intensity and duration of the dry season are the main factors affecting phenological patterns in the members of the family Bombacaceae, we expect to find significant differences in the onset of leaf flushing, flowering, and fruiting between sites within species. Conversely, if competition for pollinators is one of the most important factors in determining phenological events in the species studied, we expect to find a sequential pattern of peak flowering dates of each species within sites (i.e., staggered flowering). Furthermore, if competition for pollinators is affecting the phenological patterns of Bombacaceae, we expect that the species of pollinators will be using the same bombacaceous plants within sites and that they will sequentially concentrate on the different species of plants depending on their flowering pattern.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The predominant vegetation type in this area is tropical dry forest. Average annual rainfall is 707 mm with a dry season from November through June. The majority of the tree species are deciduous, abscising their leaves during the dry season and producing flowers (Bullock and Solís-Magallanes, 1990
). This site will be referred to hereafter as Chamela-Cuixmala.
The second site was located in the northern Pacific coast of Costa Rica in the province of Guanacaste (10°45' N, 85°30' W) within the Guanacaste Conservation Area. This protected area is considered tropical dry forest according to the life zone classification system proposed by Holdridge (1969)
. Average annual rainfall is 1440 mm, and the dry season extends from December through April (Maldonado et al., 1995
). Most of the tree species are deciduous and their flowering peak occurs during the dry season (Frankie et al., 1974
). This site will be referred to hereafter as Guanacaste.
The third site was located in the Osa Peninsula in the southern Pacific coast of Costa Rica (8°26' N, 83°30' W) within the Osa Conservation Area (ACOSA). This area is considered tropical moist forest according to Holdridge (1969)
, and average annual rainfall is 3000 mm in the lowlands and 4000 mm in the uplands, with a marked dry season from December to April (Hartshorn, 1983
). Most tree species are evergreen, and only a few drop their leaves during specific intervals of the dry season (December–March; Allen, 1956
). This site will be referred to hereafter as Osa.
Study species
We studied six species from the family Bombacaceae at the three study sites. All species studied possess hermaphroditic, chiropterophilic flowers that are principally visited by bats and sphingid moths (Alvárez and González-Quintero, 1970
; Heithaus et al., 1975
; Quiroz et al., 1983
; Eguiarte et al., 1987
; Haber and Frankie, 1989
; Stoner et al., 2002
, 2003
). All species are characterized by compound digitate leaves that abscise prior to flowering in the dry season and produce new leaves in the rainy season. With the exception of C. aesculifolia, all fruits mature during the dry season after flowering (Frankie et al., 1974
; Bullock, 1995
). Fruits are five-valved, woody, and dehiscent with abundant kapok fibers surrounding the seeds for wind dispersal (Cascante-Marín, 1997
; Avendaño-Reyes, 1998
).
Ceiba aesculifolia is a Neotropical species distributed from Mexico to northern Costa Rica (Avendaño-Reyes, 1998
). Trees may grow up to 20 m in height and have diameters of 20–50 cm. Ceiba aesculifolia has large (10–16 cm) flowers with five brown pubescent petals and five white filaments with yellow stamens. Styles are on average 15 cm long and surpass the stamens by 1–2 cm. Very little information exists on the reproductive biology of this species.
Ceiba grandiflora has only been reported from the states of Jalisco and Colima, Mexico, and thus appears to be an endemic tree species to the tropical dry forest in this region (Rose, 1895
; Lott, 1993
). This is a relatively short species (<12 m) with a diameter up to 60 cm. The actinomorphic flowers are cream-colored with petals approximately 9–12 cm long with five stamens with cream-colored filaments united at the base (Rose, 1895
).
Ceiba pentandra is distributed in the Neotropics from México to the Amazonian basin and in the paleotropics throughout western Africa (Hartshorn, 1983
). This species is a tall (>40 m) emergent deciduous tree that may reach diameters (dbh) of more than 200 cm. Flowers are small (3–3.5 cm) with five stamens around a protruding style with white to pink petals (Cascante-Marín, 1997
).
Pachira quinata is a Neotropical species distributed in dry forests from Honduras to northern South America (Alverson, 1994
). Trees may grow up to 35 m in height with diameters (dbh) over 100 cm. Flowers are medium-sized (5–10 cm) and protandrous, with multistaminate white filaments and a single central style (Quesada et al., 2001
; Fuchs et al., 2003
).
Pseudobombax ellipticum is found only in Mexico along the Gulf of Mexico from Tamaulipas and San Luis Potosí to the Yucatan Peninsula and on the Pacific side from Sinaloa to Chiapas. This species is relatively short (<12 m) with a diameter up to 60 cm. Flowers are multistaminate and actinomorphic, 13–15 cm long with light pink coloration on the base of the petals (Pennington and Sarukhán, 1998
).
Pseudobombax septenatum is distributed from Nicaragua to Brazil (Quesada et al., 1997
). Trees are usually tall (>30 m), and the trunk has green, vertical stripes separated by grayish bark. The trunk varies in diameter according to water storage. Flowers are large (15–20 cm) with a single central style. Light pink flowers are multi-staminate with denser stamens and thicker filaments than in other genera.
Phenology data
To determine the sequence of phenological events in trees of the family Bombacaceae across the three study sites, we recorded the phenology of marked individuals every 2 wk from September 2000 through August 2001 for all six species. Individuals were marked along access roads and permanent trails within all three sites. We used 55 individuals of Ceiba aesculifolia, 83 individuals of Ceiba grandiflora, 21 individuals of Ceiba pentandra, and 34 individuals of Pseudobombax ellipticum in Chamela-Cuixmala. In Costa Rica, we determined the phenology of 33 individuals of C. aesculifolia, 35 of C. pentandra, 98 of Pachira quinata, and 20 of Pseudobombax septenatum in Guanacaste. In Osa, phenological data was collected for 67 individuals of C. pentandra and 72 of Pseudobombax septenatum. In total, phenology data was collected for 518 trees across all three sites.
We determined the phenology of all species for each sampling date by scoring leaf, flower, and fruit production. Quantitative estimation of leaf production was not possible, but the dates of leaf flush and leaf fall (all leaves dropped) were recorded for all individuals sampled. An individual was considered to be fully leafed between the dates of flower flushing and leaf fall. We counted total flower and fruit production for each individual except for C. pentandra for which flower and fruit production were estimated based on the percentage of cover of the crown (Fournier, 1974
). Using flower counts, we estimated the number of individuals in the population that were blooming for each sampling date. An individual was considered to be blooming if flower production on any sampling date exceeded 10% of total flower production for that individual. Flowering period was divided into (1) beginning, <50% of the population blooming; (2) peak, 51–100% of the population blooming; and (3) end, <50% of the population blooming. We also estimated the number of individuals in the population that matured fruits for each sampling date.
Intraspecific comparisons in flowering phenology
To determine if the intensity and duration of the dry season affect the flowering phenology of bombacaceous species, we compared intraspecific flowering overlap between study sites in different geographic locations with different precipitation regimes. Flowering overlap was estimated by pairwise comparisons of flowering intensity between sites. Flowering intensity for each species was determined as the percentage of trees flowering at each sampling date. Flowering overlap was estimated for C. pentandra between all three sites and for C. aesculifolia between Chamela-Cuixmala and Guanacaste. Flowering overlap was also estimated for Pseudobombax septenatum between Guanacaste and Osa. An overlap index (Pianka, 1973
) was calculated for each species comparing flowering intensity between all pairwise combinations of sites. To determine if flowering overlap indexes differed statistically from random expectations (i.e., Pianka's index differed statistically form zero), a null model analysis was used to compare the mean overlap index with 1000 randomly simulated values (Kochmer and Handel, 1986
; Wright and Calderón, 1995
). Simulated values were generated by randomly sampling flowering intensities between dates for each species while maintaining the overall length of the flowering season constant. Flowering overlap was considered to occur when the observed index was larger than 95% of the 1000 simulated values. All calculations were performed using the EcoSim 7.0 computer program for null model analysis in community ecology (Gotelli and Entsminger, 2001
).
To study the variation in flowering and fruiting of C. pentandra, which has been described as having a supra-annual flowering cycle, we estimated the variation in reproduction by comparing the number of trees flowering over three years (1999, 2000, 2001) at the three study sites (except for Osa in 1999). Logistic regressions (Stokes et al., 2000
) were used to determine the effect of site and year on flowering and fruiting probability. Site and year were used as the independent variables, and the response variables were the number of trees in flower and the number of trees that matured fruits.
Interspecific comparisons in flowering phenology
To determine the importance of pollinator competition in bombacaceous trees, we compared interspecific flowering overlap between different species within each study site. Pianka's index (Pianka, 1973
; Pleasants, 1990
) was used to assess flowering overlap between all pairwise combinations of species co-occurring within each site. The level of significance of Pianka's index was determined by the same procedure and assumptions previously described for intraspecific comparisons.
Estimation of pollinator use of floral resources
To estimate the importance of bombacaceous species in the diet of frugivorous and nectarivorous bats in Chamela-Cuixmala, mist-net sampling was conducted every 2 wk during the flowering of bombacaceous plants (November 2000 through June 2001). One 12-m and one 9-m mist net were placed in natural corridors in areas near bombacaceous species in flower and were opened for 4 h beginning at dusk. We collected pollen samples from the bodies and faces of all frugivorous and nectarivorous species captured using the glycerine-fucsin gelatin technique of Beattie (1971)
. For individuals that had no pollen on their bodies, fecal samples were collected. Each fecal sample was mixed with 2.5 mL of 70% alcohol and slides were made with this material. Pollen was identified using pollen keys (Lozano-García and Martínez-Hernández, 1990
; Roubick and Moreno, 1991
) and our own reference collection, developed during the study from flowers in the region that previously had been described as bat-pollinated or flowers that appeared to have bat-syndrome characteristics. All species of pollen were identified for each gelatin and fecal sample, and the most common was considered the principal pollen for that sample. In all cases, the most common pollen accounted for more than 80% of the pollen grains in the sample.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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In addition to studying intraspecific phenological patterns of trees of the family Bombacaceae at the three sites during 1 yr, we compared the flowering frequency and fruit production of individuals of C. pentandra at the three sites for three consecutive years (1999–2001). Ceiba pentandra had a supra-annual blooming frequency. The percentage of individuals that flowered and matured fruits of C. pentandra varied depending on the site and the year (Table 2). The greatest reproductive success was observed in 1999 at Chamela-Cuixmala when approximately 100% of the individuals matured fruits. The lowest reproductive success was recorded in Guanacaste in 2000, when only 21% of the studied individuals matured fruits, and in Osa in 2001, when only 21% matured fruits. A logistic regression analysis (Stokes et al., 2000
) shows that C. pentandra differed in flowering frequency at the three sites over the years. During the three years studied, individual trees at Chamela-Cuixmala tended to flower more frequently than trees in Guanacaste (odds ratio of the probability of flowering = 8.4, 95% confidence interval [CI]: 3.26–21.73) and Osa (odds ratio = 7.87, 95% CI: 3.10–20.00). However, there are no differences in the flowering frequency between Guanacaste and Osa (odds ratio = 1.06, 95% CI: 0.55–2.06). The probability of flowering in C. pentandra was greater in 1999 in Guanacaste and Chamela-Cuixmala compared to 2000 (odds ratio = 7.14, 95% CI: 2.32–25.00) and 2001 (odds ratio = 9.41, 95% CI: 3.14–25.22).
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Similar to the pattern observed in Chamela-Cuixmala and in Guanacaste, in Osa C. pentandra flowered from December through February with a peak in January (Fig. 3a). Pseudobombax septenatum flowered from December through May with a peak in March (Fig. 3b). Flowering of P. septenatum overlapped with the flowering distribution of C. pentandra (Pianka's index 0.791, P < 0.05) at this site.
Seasonal pollinator use of floral resources
In Chamela-Cuixmala, pollen of bombacaceous species was not found on any of the frugivourous species sampled: Artibeus intermedius (N = 84), A. jamaicensis (N = 416), A. lituratus (N = 30), A. phaeotis (N = 40), A. toltecus (N = 3), and Centurio senex (N = 9). Leptonycteris curasoae was the most important pollinator of bombacaceous trees at Chamela-Cuixmala, and Glossophaga soricina was the second most important (Table 4). Bombacaceous species were the principal pollen found in samples from L. curasoae during 8 mo of the year, comprising 13% of the samples in November, 44% in December, 79% in January, more than 90% from February to April, and 25% in June. Although L. curasoae consumed pollen from up to three species of bombacaceous trees during 1 mo, one species generally made up the majority of the samples. In November and December 100% of the bombacaceous samples were Ceiba grandiflora, in January 75% were C. pentandra, in February 96% were Pseudobombax ellipticium, in March 91% were P. ellipticum, in April 100% were C. grandiflora, in May 99% were C. aesculifolia, and in June 92% were C. aesculifolia.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Wright and Calderón, 1995
). Finally, flowering between tree species within different sites had little overlap, with the exception of C. grandiflora in Chamela and P. septenatum in Guanacaste, suggesting that competition for pollinators is a strong selective force that influences the staggered flowering pattern within this family. This selective pressure may have caused divergence in flowering time between species of similar taxa, thus modifying historical constraints related to this trait.
Effect of intensity and dry season duration on phenology (intraspecific variation)
The intraspecific comparisons showed that the same species flowered at similar times between sites in spite of different rainfall regimes. Flowering of C. pentandra initiated in December in Chamela-Cuixmala and in Guanacaste. In Chamela-Cuixmala this was approximately 3 mo after the dry season began, while in Guanacaste this was only about 1 mo after the beginning of the dry season. Similarly, in Osa C. pentandra began flowering in December (immediately after the beginning of the dry season) even though average monthly rainfall contrasted considerably with Chamela-Cuixmala and Guanacaste (Table 1, Figs. 1–3). The flowering pattern of C. pentandra is supra-annual in tropical wet forests, where individual trees have flowering and fruiting cycles with several years between blooming (Frankie et al., 1974
; Newstrom et al., 1994
; Gribel et al., 1999
). This pattern is more common in Costa Rica, but it is not the case in Mexico, where trees flowered and set fruit almost every year (Table 2). In addition, there is annual variation in reproductive success between sites. However, regardless of the reproductive regularity of individuals, C. pentandra initiated flowering during a similar period of the year at the three sites.
Similarly, flowering began at the same time in Guanacaste and Osa for P. septenatum (i.e., December). Peak flowering of C. aesculifolia occurred in May at Chamela and in Guanacaste, and it was the last species of Bombacaceae to flower at both sites (i.e., end of the dry season). Several phenological studies have concluded that changes in water availability from shifts in precipitation regimes and soil moisture are the essential proximate causes affecting phenological patterns (Opler et al., 1976
; Reich and Borchert, 1984
; Borchert, 1994
). However, few of these studies have compared the same species in contrasting environments. Our data suggest that the flowering period of bombacaceous species is not determined by precipitation. Moreover, levels of soil moisture between these sites vary greatly. In Osa, the most superficial levels of soil remain saturated during the wet season and the first months of the dry season (December and January), and the water deficit is 0 or very small during this period (Gómez and Herrera, 1985
). In contrast, in the dry forest of Guanacaste there is a significant level of water deficit in the beginning of the dry season (Gómez and Herrera, 1985
), and in the case of Chamela-Cuixmala soil water content is completely dry from January through June (Galicia et al., 1999
). Because bombacaceous species have the ability to store water in their trunks (Wangaard et al., 1954
; Borchert, 1994
), intensity and duration of the dry season and soil water content do not appear to restrict flowering to a particular period during the dry season.
Interspecific variation
The interspecific comparisons within sites showed a pattern of sequential flowering with the exception of C. grandiflora in Chamela-Cuixmala and P. septenatum in Guanacaste (Figs. 1–3). In the case of C. grandiflora, the extended flowering period can be explained by a relatively low number of flowers produced each day (Quesada et al., 2003
), thereby distributing the reproductive effort over a longer period of time and producing an overlap with other species. Pseudobombax septenatum also demonstrated an extended flowering period with fewer flowers produced at the beginning and the end of the flowering period; however, unlike C. grandiflora, a massive flowering occurred in the middle of the dry season. Although P. septenatum overlapped with C. pentandra at the beginning and with P. quinatum at the end, the massive peak of flowering occurred between the peaks of these other two species (Fig. 2).
Several evolutionary hypotheses have been proposed to explain staggered flowering of plants. One of the first ideas to be suggested was that plants with the same pollinators will avoid competition through staggered flowering and thus will increase their reproductive success by attracting more pollinators (Robertson, 1895
). This hypothesis has been supported by empirical evidence that establishes a relationship between the staggered flowering patterns of plants with their hummingbird pollinators (Stiles, 1975
; Feinsinger, 1978
). Another hypothesis states that staggered flowering avoids the transfer of interspecific pollen that may cause pollen loss, reduction of receptive stigma surfaces, and overall lower reproductive success (Thomson et al., 1981
). These hypotheses are not mutually exclusive, and both may partially explain the staggered flowering observed in bombacaceous species. Therefore, competition for pollinators and avoidance of interspecific pollen deposition are important ultimate factors that will selectively favor staggered flowering of species within the same family having the same pollinators.
Another factor that may affect phenological patterns in the bombacaceous species studied is timing of seed dispersal. Most of the species matured fruits shortly after flowering and dispersed their seeds during the dry season both in Costa Rica and Mexico, occurring at the best time for wind dispersal (i.e., dry and windy). The only exception is C. aesculifolia, which flowered at the end of the dry season both in Guanacaste and Chamela and dehisced mature fruits during the following dry season (Fig. 2). This is the only Neotropical bombacaceous species with a fruiting pattern that belongs to a previously described group of "dry season fruiters" (Frankie et al., 1974
). This pattern suggests that seed dispersal may be an important ultimate factor that constrains the flowering period of these bombacaceous trees.
The species in the family Bombacaceae used in our study have been classified within the functional group of deciduous trees with low-density wood and high-stem water storage (Borchert, 1994
). According to this classification, water deficits trigger leaf shedding followed by flowering for prolonged periods. Our results are not consistent with this hypothesis. Although all species of trees of the family Bombacaceae shed leaves at the beginning of the dry season, flowering and fruiting patterns are staggered throughout the dry season in the dry forests of Mexico and Costa Rica. Therefore, the loss of leaves is likely to be correlated with the relative high minimum leaf water potential and low-density wood of these species (Holbrook et al., 1995
), but it is not directly involved in triggering the sequence of flowering or fruiting. Inter- and intraspecific variation in flowering and fruiting is consistent for most tree species at both sites. Wright and Cornejo (1990)
showed that even when soil water potential is maintained at field capacity during the dry season, the timing of leaf fall of deciduous trees of low-density wood and high-density wood is not affected.
Seasonal pollinator use of floral resources
Our data suggest that competition for pollinators is, perhaps, one of the most important ultimate factors affecting the phenological patterns observed in the family Bombacaceae in the Neotropics. In Chamela-Cuixmala, trees of the family Bombacaceae were a main resource for the nectar-specialist Leptonycteris curasoae during 8 mo, and this bat generally concentrated on one bombacaceous species each month. The more generalist nectarivore, Glossophaga soricina, utilized bombacaceous species during 6 mo and also concentrated on one bombacaceous species each month. The sequential use of bombacaceous species by bats coincided with the flowering phenology of these species. These data support the idea that flowering phenology is staggered to avoid competition for pollinators as has been suggested by various authors (Janzen, 1967
; Stiles, 1975
; Feinsinger, 1978
). It is especially important for bombacaceous species to avoid competition for pollinators since they have been described principally as self-incompatible (Hamrick and Murawski, 1990
; Gribell et al., 1999
; Quesada et al., 2001
, 2003) and therefore are completely dependent upon pollinators to achieve fruit set. Furthermore, greater pollinator attraction during peak flowering in species with synchronous blooming (i.e., Ceiba pentandra, C. aesculifolia, Pachira quinata, and Pseudobombax septenatum) favors higher levels of outcrossing (Stephenson, 1982
; Quesada et al., 2003
).
In conclusion, our study suggests that phenological patterns of the Bombacaceae family in Neotropical dry forests are mainly constrained by adaptive selective pressures associated with competition for pollinators and phylogenetic membership. Abiotic factors related to precipitation and soil water content appear to be regulating leaf flush and abscission of leaves, but the principal causes of flowering are related to ultimate factors associated with competition for pollinators. This study is the first that evaluates the phenological pattern of species and genera of the same family at different latitudes in a similar life zone. Future studies should evaluate other taxonomically related groups found in similar habitats but different regions to further test the conclusions of our study.
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FOOTNOTES |
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4 Author for reprint requests (mquesada{at}oikos.unam.mx
)
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