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AOBPreview originally published online on August 19, 2004
Annals of Botany 2004 94(4):545-551; doi:10.1093/aob/mch171
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Annals of Botany 94/4, © Annals of Botany Company 2004; all rights reserved

Diversity and Genetic Structure of the Mexican Endemic Epiphyte Tillandsia achyrostachys E. Morr. ex Baker var. achyrostachys (Bromeliaceae)

JORGE GONZÁLEZ-ASTORGA1,*, ANDREA CRUZ-ANGÓN1,{dagger}, ALEJANDRO FLORES-PALACIOS2 and ANDREW P. VOVIDES1

1 Laboratorio de Genética de Poblaciones, Departamento de Biología Evolutiva, Instituto de Ecología, A. C. Km 2·5 Antigua Carretera a Coatepec, Xalapa 91070, Veracruz, México and 2 CEAMISH-UAEM, Av. Universidad 1001, Col. Chamilpa, Cuernavaca, Morelos, México

* For correspondence. E-mail astorga{at}ecologia.edu.mx

Received: 9 April 2004    Returned for revision: 15 June 2004    Accepted: 18 June 2004    Published electronically: 19 August 2004


   ABSTRACT
TOP
 FOOTNOTES
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 

• Background and Aims The monoecious, bird-pollinated epiphytic Tillandsia achyrostachys E. Morr. ex Baker var. achyrostachys is an endemic bromeliad of the tropical dry forests of Mexico with clonal growth. In the Sierra de Huautla Natural Reserve this species shows a host preference for Bursera copallifera (Sessé & Moc ex. DC) Bullock. As a result of deforestation in the study area, B. copallifera has become a rare tree species in the remaining forest patches. This human-induced disturbance has directly affected the population densities of T. achyrostachys. In this study the genetic consequences of habitat fragmentation were assessed by comparing the genetic diversity, gene flow and genetic differentiation in six populations of T. achyrostachys in the Sierra de Huautla Natural Reserve, Mexico.

• Methods Allozyme electrophoresis of sixteen loci (eleven polymorphic and five monomorphic) were used. The data were analysed with standard statistical approximations for obtaining diversity, genetic structure and gene flow.

• Key Results Genetic diversity and allelic richness were: HE = 0·21 ± 0·02, A = 1·86 ± 0·08, respectively. F-statistics revealed a deficiency of heterozygous plants in all populations (Fit = 0·65 ± 0·02 and Fis = 0·43 ± 0·06). Significant genetic differentiation between populations was detected (Fst = 0·39 ± 0·07). Average gene flow between pairs of populations was relatively low and had high variation (Nm = 0·46 ± 0·21), which denotes a pattern of isolation by distance. The genetic structure of populations of T. achyrostachys suggests that habitat fragmentation has reduced allelic richness and genetic diversity, and increased significant genetic differentiation (by approx. 40 %) between populations.

• Conclusions The F-statistic values (>0) and the level of gene flow found suggest that habitat fragmentation has broken up the former population structure. In this context, it is proposed that the host trees of T. achyrostachys should be considered as a conservation priority, since they represent the limiting factor to bromeliad population growth and connectivity.

Key words: Allozymic electrophoresis, bromeliad, conservation genetics, genetic structure, gene flow, habitat fragmentation, tropical dry forest, Sierra de Huautla Natural Reserve Mexico


   INTRODUCTION
TOP
 FOOTNOTES
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 
Genetic population analysis of tropical plant species has the potential to address a range of evolutionary and ecological questions. It allows the measurement of variation within and between species (Hamrick, 1994Go; Alvarez-Bullya et al., 1996Go; Hamrick and Godt, 1996aGo, bGo), the determination of phylogenetic relationships among species (Gitzendanner and Soltis, 2000Go; Cole, 2003Go), and the distribution of genetic variation in widespread populations (Loveless and Hamrick, 1984Go). The genetic structure of plant populations reflects the interactions of different processes, including the long-term evolutionary and short-term ecological history of the species, such as the effects of habitat fragmentation, shifts in distribution and population isolation. In addition, several factors may influence the genetic structure of plant populations. Among these, the more important are the breeding systems (Lande and Schemske, 1985Go) and seed dispersal mechanisms (Hamrick et al., 1995Go; Hamrick and Godt, 1996bGo), as well as the action of natural selection (Endler, 1986Go) and inbreeding at the microhabitat level (Lande and Shannon, 1996Go).

Reduction in population size due to habitat fragmentation may produce a loss of allelic richness or gene diversity (Lande, 1999Go). This can occur through population bottlenecks at the time of the disturbance and genetic drift afterwards (Barrett and Kohn, 1991Go; Ellstrand and Elam, 1993Go). Thus, the study of the genetic consequences of habitat fragmentation in plant populations has implications for species conservation (Young et al., 1996Go; González-Astorga and Núñez-Farfán, 2001Go; González-Astorga and Castillo-Campos, 2004Go).

Although 10 % of the world's vascular flora is epiphytic (Kress, 1986Go), population genetic data for epiphytes are very scarce. Only a few epiphyte ferns (Ranker, 1992Go; Hooper and Haufler, 1997Go), orchids (Ackerman and Ward, 1999Go; Tremblay and Ackerman, 2001Go) and bromeliads (Soltis et al., 1987Go, Izquierdo, 1995Go) have been studied genetically. Epiphytes represent an ideal model to study population genetic structure and genetics of speciation, because of their colonization habit, their patchy ecological and geographical distribution patterns, as well as their specific pollination strategies (Ackerman, 1986Go; Ackerman and Ward, 1999Go; Benzing, 2000Go). In epiphytes with host-specificity, the action of genetic drift and founder events could determine their genetic structure (Tremblay and Ackerman, 2001Go). In fact, at a biogeographical level, the patchy distribution of epiphytes has been suggested to be a force that induces isolation between populations and promotes fast species evolution. However, this will depend on how low are the levels of gene flow, and whether the population was founded by few individuals with low effective population size (Gentry and Dodson, 1987Go; Tremblay and Ackerman, 2001Go).

In this study, the impact was assessed of recent habitat fragmentation on diversity and genetic structure of an epiphyte plant species, Tillandsia achyrostachys var. achyrostachys, in the tropical dry forest of central Mexico. In the study area, T. achyrostachys shows a clear host preference, indicated by its greater abundance on a rare tree species (Martínez, 1999Go). Allozyme loci were used to examine the population genetics of T. achyrostachys. The objectives were: (1) to evaluate the genetic diversity in a fragmented landscape; (2) to determine the amount and distribution of genetic diversity within and among the six populations; (3) to estimate the gene flow between populations, and (4) to evaluate the conservation status of the species, given the actual disturbance conditions.


   METHODS
TOP
 FOOTNOTES
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 
Study site
The study was carried out at the Sierra de Huautla Natural Reserve, during 1998–99. The site is located in the State of Morelos (18°29–18°32'N, 99°05'–99°08'W) in central Mexico (Fig. 1). The original vegetation is tropical dry forest (sensu Rzedowski, 1978Go), which is now highly fragmented as a result of recent human activities (Trejo and Dirzo, 2000Go). The Reserve has 114 forest fragments, which comprise 31·5 % of the total area (Dorado et al., in press). Tropical dry forest physiognomy is produced by marked seasonal changes. Most plants lose their leaves for periods of 6–7 months during the dry season (September–March). The climate is warm sub-humid (the driest of the sub-humid climates according to García, 1988Go). The precipitation/temperature ratio is less than 43·2, and less than 5 % of the rainfall occurs in winter. Mean annual temperature and precipitation for the study site are 24·5 °C and 1039 mm, respectively (García, 1988Go).



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  		FIG. 1. Geographical distribution of Tillandsia achyrostachys in the Sierra de Huautla Natural Reserve, Morelos, Mexico. The numbers show the geographical position of each population evaluated.

 
Target species
Tillandsia achyrostachys var. achyrostachys (T. achyrostachys hereafter) is a Mexican endemic epiphyte (Smith and Downs, 1977Go), with flowers borne in a glabrous, shell-pink inflorescence, up to 10 cm long. The actinomorphic flowers are citron-coloured, 42 mm long, and only one flower at a time per inflorescence is produced. The breeding system is unknown; however, the flower anatomy suggests an outcrossing, bird-mediated mating system. The exerted pistil is longer than exerted stamens and the flowers appear to be suited for hummingbird pollination, which are the most common bromeliad pollinators (Gardner, 1986Go; Sazima et al., 1995Go, 1996Go; Cruz-Angón, pers. obs.).

In the study area, T. achyrostachys can be found in up to 16 different host tree species, but it shows a clear host preference (sensu Cornelissen and ter Steege, 1989Go) for Bursera copallifera ({chi}2 = 1141·33, P < 0·0001; Martínez, 1999Go). The T. achyrostachys individuals occur on 35·1 % of B. copallifera trees, which is a very rare species in the tropical dry forest of the Sierra de Huautla Natural Reserve. Bursera copallifera trees have a mean density (± SD) of 2 ± 4 trees ha–1, while total forest tree density is 110 ± 81 trees ha–1.

Sample collection
Tissue sampling was done in the only six populations of Tillandsia achyrostachys where the plant could be found in the Sierra de Huautla Natural Reserve, Morelos, Mexico. Distances ranging from 2·6 to 25·4 km separate populations. Fully expanded young leaves were collected from reproductive individuals in each population. To prevent the effect of sampling clonal growth, only one T. achyrostachys plant was sampled per individual host as recommended by Ranker (1992)Go.

Electrophoretic procedure
To determinate the diversity and genetic structure of T. achyrostachys populations, allozyme variation was analysed using horizontal starch gel electrophoresis (12 % w/v) (Müller-Strack, 1998Go). Multilocus genotypes of 15–22 individuals from each population were obtained and allozymic variation was scored in 16 loci for each individual plant. The polymorphic loci were: malate-dehydrogenase (E.C. 1.1.1.37, loci Mdh1 and Mdh2), phosphoglucoisomerase (E.C. 5.3.1.9, locus Pgi), phosphoglucomutase (E.C. 5.2.2, locus Pgm), esterase (E.C. 3.1.1, loci Est1 and Est1), alcohol-dehydrogenase (E.C. 1.1.1.1. locus Adh), aminopeptidase (E.C. 3.4.11.1, loci Amp1 and Amp2), and glucose-6-phosphate-dehydrogenase (E.C. 1.1.1.49, loci G-6-pdh1 and G-6-pdh 2). The monomorphic loci were: isocitrate-dehydrogenase (E.C. 1.1.1.41, locus Idh), diaphorase (E.C. 1.6.99.-, loci Dia1 and Dia2), leucine aminopeptidase (E.C. 3.4.11.1, locus Lap) and peroxidase anodic (E.C. 1.11.1.7, locus Apx). The enzymes were extracted from the young leaves using extraction buffer according to Wendel and Weeden (1989Go; i.e. Tris–HCl pH 7.5, sucrose, PVP-40, mercaptoethanol, ascorbic acid, diethyldithiocarbamate, bovine serum albumin, sodium metabisulphite and sodium tetraborate) and the resulting solution was absorbed onto filter paper wicks and stored at –70 °C until analyses. The buffers (gel and electrode) used were histidine to pH 5.7 and citric acid (Soltis et al., 1983Go, 1987Go). Electrophoresis was carried out at 4 °C over 8 h (constant current of 60 mA at 250 V).

Statistical methods
The data matrix of individual genotypes was analyzed using the TFPGA 1.3 program (Miller, 1997Go). Genotypic frequencies of each population were obtained and used to calculate observed mean heterozygosity (HO) and allelic frequencies. The observed allelic frequencies for each population were used to estimate the mean number of alleles per locus (A), the average proportion of polymorphic loci (P), and expected mean heterozygosity (HE), based on Hardy–Weinberg expectations (Hartl and Clark, 1997Go). Significance of estimators was obtained by Monte Carlo methods (Weir, 1990Go; Guo and Thompson, 1992Go).

To quantify levels of allelic variation within and among populations (population subdivision), F-statistics were calculated (Wright, 1965Go, 1978Go). To determine whether Fis and Fit estimations for each locus were significantly different from zero, Chi-square statistics [{chi}2 = F(2N)(k – 1)] were obtained, with k(k – 1)/2 degrees of freedom, where N is the sample size, and k the number of alleles (Weir, 1990Go). To determine the significance of the Fst statistic per locus, the Chi-square statistic was used: {chi}2 = (2N)Fst(k – 1), with (k – 1)(s – 1) degrees of freedom, where s is the number of populations sampled (Workman and Niswander, 1970Go). The F-statistic confidence intervals (at 95 %) were obtained by bootstrapping over loci for the multilocus estimate, and jackknifing over populations for the single-locus estimates (Weir and Cockerham, 1984Go; Weir, 1990Go). The average gene flow among populations (Nm) was estimated from Fst values, as Fst = 1/(4Nma + 1), where a = [n/(n – 1)]2 and n is the number of populations (Crow and Aoki, 1984Go). Nm is interpreted as the number of migrants per generation between two given populations and can be correlated with geographical distances (Slatkin, 1993Go, 1994Go). The significance of this relationship was evaluated through a Mantel's test (1967)Go, because no other statistical methods can be used since Nm estimates are not independent (Smouse et al., 1986Go; Sokal and Rohlf, 1995Go).


   RESULTS
TOP
 FOOTNOTES
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 
Genetic diversity
Allelic frequencies for the sixteen loci (Mdh, Est, Amp, G-6-pdh and Dia, with two loci each; Pgi, Pgm, Adh, Idh, Lap and Apx with one locus each) scored for each individual plants are given in Table 1. The test for Hardy–Weinberg equilibrium of the entire data set indicated significant differences between a number of individuals for each observed and expected genotype (for polymorphic loci), as determined by a {chi}2 test with one degree of freedom and a = 0·0001 (Table 1).


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  		TABLE 1. Allelic frequencies of 16 loci for six populations of bromeliad epiphyte Tillandsia achyrostachys, in the Sierra de Huautla Natural Reserve, Morelos, Mexico

 
Mean number of alleles per locus was 1·86 ± 0·08. Percentage of polymorphic loci per population varied from 50 % (population 2) to 62·5 % (populations 1, 3, 4 and 6), with an overall mean of 59·4 % ± 5·2 %. Observed mean heterozygosity was 0·127 ± 0·04 (range 0·088–0·176). Similarly, expected mean heterozygosity was 0·210 ± 0·02 (range 0·195–0·218) (Table 2).


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  		TABLE 2. Levels of genetic variation of six populations of Tillandsia achyrostachys in the Sierra de Huautla Natural Reserve, Morelos, Mexico. A, mean number of alleles per locus; P, percentage of polymorphic loci; Ni, average sample size; HO and HE are the observed and expected mean heterozygosity, respectively

 
Genetic structure
The Wright's F-statistics, Fit and Fis, were positive and significantly different from zero for all polymorphic loci (P < 0·05) in all populations, indicating inbreeding (Table 3). In addition, all loci showed estimates that were positive and significantly different from zero Fst (P < 0·05). The means of the global Fit and local Fis inbreeding were 0·651 ± 0·021 and 0·433 ± 0·058, respectively, which suggests that genetic drift and inbreeding have been the dominant differentiating processes. The magnitude of genetic differentiation among populations indicated that on average approx. 40 % of T. achyrostachys genetic variation was due to differences between populations (Table 3).


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  		TABLE 3. Wright's F-statistics in six populations of Tillandsia achyrostachys, in the Sierra de Huautla Natural Reserve, Morelos, Mexico

 
Gene flow
An average of 0·46 ± 0·21 migrant individuals per generation between pairs of populations was obtained (Table 4). The lowest estimate was obtained between populations 3 and 6 (Nm = 0·22) separated by approx. 25·4 km, and the highest was found between populations 1 and 3 (Nm = 0·94) separated by approx. 2·6 km. Correlations between Nm estimates and the geographical distance matrices between population pairs indicated that genetic differentiation has occurred as expected under an isolation-by-distance model, as demonstrated using the Mantel's test (r = –0·74; P = 0·009). Moreover, the relationship between gene flow and geographical distances between pairs of populations was negative and statistically significant (ß = –0·472; P = 0·002; R2 = 52·8 %) (Fig. 2).


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  		TABLE 4. Number of individual migrants per generation (Nm; above diagonal) and geographical distance (km; below diagonal) between pairs of populations of Tillandsia achyrostachys. The Mantel test indicated a significant relationship between Nm and geographical distances (r = –0·74; P = 0·009)

 


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  		FIG. 2. Linear regression between individual migrants per generation (Nm) and Euclidian distances (d) among pairs of populations (both transformed to natural logarithms), for six populations of Tillandsia achyrostachys. (log(Nm) = 0·315 – 0·472 logd; P = 0·002, R2 = 52·8 %).

 


   DISCUSSION
TOP
 FOOTNOTES
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
ACKNOWLEDGEMENTS
 LITERATURE CITED
 
Genetic diversity
Tillandsia achyrostachys exhibits moderate diversity and genetic variability even though it has a restricted distribution in Mexican tropical dry forests. This is probably a consequence of habitat fragmentation. The results presented here suggest that the effect of inbreeding and genetic drift on genetic structure in T. achyrostachys might be counteracted by the influence of clonal growth. This growth helps to maintain T. achyrostachys genets and the genetic variability at both local and regional levels, as suggested for the saxicolous bromeliad Pitcairnia geykesii (Sarthou et al., 2001Go) and the terrestrial bromeliad Chevaliera (=Aechmea) magdalenae (Murawski and Hamrick, 1990Go). The percentage of polymorphic loci in T. achyrostachys was similar (59·4 %) to other values reported for several plant species of similar geographic range and mixed-animal breeding systems (52·9 % and 40 %, respectively; Hamrick and Godt 1996aGo). Mean expected heterozygosity within populations for T. achyrostachys was higher (0·21) than that reported for other plant species with similar distribution (0·15; Hamrick, 1994Go).

On the other hand, the results indicated higher levels of variability in T. achyrostachys when compared with those previously reported for three other bromeliad species, the epiphytes Tillandsia ionantha and T. recurvata (Soltis et al., 1987Go) and the terrestrial Chevaliera magdalenae (Murawski and Hamrick, 1990Go). However, we found similar results to those reported for the saxicolous bromeliad Pitcairnia geyskesii (Sarthou et al., 2001Go) and the terrestrial bromeliad Ursulaea (=Aechmea) tuitensis (Izquierdo and Piñero, 2000Go). The species studied by Soltis et al. (1987)Go, Murawski and Hamrick (1990)Go and Izquierdo and Piñero (2000)Go had smaller population sizes than T. achyrostachys. Thus, the moderate genetic diversity and variability exhibited by T. achyrostachys is similar to those found in other bromeliad species.

Genetic structure and gene flow
The populations of T. achyrostachys show homogeneity in Fst values for all the analysed loci (Fst = 0·391 ± 0·068), which may indicate that genetic drift and inbreeding are responsible for the deficiency of heterozygous individuals both at the population and sub-population level. Our results show that the percentage of variation among T. achyrostachys populations is larger than that reported for the outcrossing epiphytic bromeliad T. ionantha (0·043; Soltis et al., 1987Go), and also for the self-incompatible orchid Tolumnia variegata (0·060; Ackerman and Ward, 1999Go), and the outcrossing ferns Adenophorus tamarisinus (0·024), A. tripinatifidus (0·122), Grammitis hookeri (0·161), G. tenella (0·070; Ranker, 1992Go), Pleopeltis astrolepis (0·021), P. complanata (0·039), P. crassinervata (0·035), P. polylepis var. polylepis (0·069), and P. wiesbaurii (0·032; Hooper and Haufler, 1997Go) where sporophyte or seedling establishment is independent of host availability.

On the other hand, the Fst values found in the autogamous bromeliads T. recurvata (0·906; Soltis et al., 1987Go) and Podaechmea (=Aechmea) mexicana (0·56; Izquierdo, 1995Go) were greater than the Fst value of T. achyrostachys populations. This pattern is expected since autogamy promotes reproductive isolation, even in sympatric congeneric bromeliad species (Wendt et al., 2002Go). The Fst values we report for T. achyrostachys are similar to those reported for other three autogamous and terrestrial bromeliad species, Chevaliera (=Aechmea) magdelaneae (0·356; Murawski and Hamrick, 1990Go), Pitcairnia geyskesii (0·320; Sarthou et al., 2001Go) and Podaechmea (=Aechmea) lueddemanina (0·31, Izquierdo, 1995Go). Whilst in these three species autogamy and inefficient seed dispersal by birds could explain the population genetic structure, in the case of Tillandsia achyrostachys it is probably caused by outcrossing and long distance seed dispersal by wind, and so the Fst value should be correlated with host abundance (see below).

On average, gene flow was low between population pairs in T. achyrostachys (Nm = 0·46 ± 0·21). This is consistent with the high genetic differentiation between populations and is evidence for a high host-dependence in the study area. Our results differ from those reported for epiphyte ferns (Ranker, 1992Go; Hooper and Haufler, 1997Go) and for 213 plant species with wind-dispersed seeds (Hamrick and Godt, 1996aGo). The species in the latter study were mostly annual and short-lived perennials, with no host-dependency (micro-habitat dependency) reported. However, epiphyte species depend upon host availability to develop populations. Thus, in order to increase the chances of exploiting hosts, we would expect epiphytes to develop both abundant and highly viable seeds (Callaway et al., 2002Go); otherwise, the population will depend on the abundance of an adequate host, as is the case for T. achyrostachys in the Sierra de Huautla Natural Reserve. Moreover, if tree hosts become scarce and distant from each other (as occurs with fragmentation), then isolation by distance should be expected, because populations would be founded by local seed-pools, not by regional ones. In accordance with this, Nm was negatively correlated to geographic distance. A similar pattern of isolation by distance has been found for the saxicolous/epiphyte Podaechmea mexicana (Izquierdo, 1995Go), and the epiphyte orchid Tolumnia variegata (Ackerman and Ward, 1999Go). Whilst the maximum distance between pairs of populations was 25 km for T. achyrostachys, the maximum distance for T. variegata was 1800 km (Ackerman and Ward, 1999Go), and 1748 km for P. mexicana (Izquierdo, 1995Go). Thus the populations of T. achyrostachys have the smallest geographical degree of isolation by distance reported for an epiphyte species (cf. Izquierdo, 1995Go; Ackerman and Ward, 1999Go).

Conservation implications
Habitat fragmentation reduces the sizes of a species' populations, increases isolation and modifies the abiotic environment (Rathcke and Jules, 1993Go). As a direct outcome of this, genetic variation is reduced and interpopulation genetic divergence increases due to increased random genetic drift, elevated inbreeding and reduced gene flow (Young et al., 1996Go; Lande, 1999Go; González-Astorga and Núñez-Farfán, 2001Go; González-Astorga and Castillo-Campos, 2004Go).

In our study site, more than 60 % of the original forest area has been clear-cut (Trejo and Hernandez, 1996Go; Trejo and Dirzo, 2000Go; Dorado et al., in press) and the removal of trees associated with fragmentation reduces the colonization possibilities for any phorophyte-dependent species, thus affecting its population numbers. This phenomenon is more pronounced in T. achyrostachys because of its host preference. To date, all available information indicates that habitat fragmentation may also affect plant pollinators' abundance and diversity (Rathcke and Jules, 1993Go; Allen-Wardel et al., 1998Go; Kearns et al., 1998Go; Packer and Owen, 2001Go). Further research would clearly be desirable to assess the ecological consequences (e.g. effects on pollinator guild) of the decline in the population of T. achyrostachys at the study site.


   ACKNOWLEDGEMENTS
TOP
 FOOTNOTES
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGEMENTS
LITERATURE CITED
 
This study was supported by two grants: FOMES-UAEM-1998, and CONACyT-SEMARNAT 2002-C01-0183. The authors would like to thank Daniel Piñero, Pat Heslop-Harrison, Tania Chew, Miriam Ferrer and two anonymous reviewers for their comments for improving the manuscript, Genoveva Arteaga and Jesús Vargas for technical assistance in the laboratory and Amparo Lima and José Antonio García, who provided relentless assistance in the field. We also thank Eva Martínez for providing the picture used in the snapshot for this article.


   FOOTNOTES
TOP
 FOOTNOTES
ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 
{dagger} Present address: Smithsonian Migratory Bird Center, National Zoological Park Washington, DC 20008, USA. Back


   LITERATURE CITED
TOP
 FOOTNOTES
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 

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