Plants with specialist relationships show higher rates of asexual reproduction from fragments Christine R. Isabella Department of Molecular and Cellular Biology, University of Puget Sound ABSTRACT Sexual reproduction increases genetic variation and allows offspring to be transported away from their parent plant . However , many plants in tropical forests are capable of reproducing from fragments, leading to a high density of clones in close proximity to the parent plant . Most plants require animals for pollen and seed transport, and in some cases plants have a specialist relationship with an animal , relying exclusively on them for successful reproduction. Other plants have generalist relationships with pollinators and dispersers with many animals able to complete reproductive tasks for the plant. This is the first study to examine the relationship between dispersal syndromes and the prevalence of asexual reproduction from fragments in natural habitats. I collected plants species with specialist pollinators ( Piper sp . ) , specialist dispersers ( Anturium obtusilobum ) , generalist pollinators and dispersers ( Inga marginata, Psychot ria spp ., Lonchocarpus oliganthus, and Chamaedorea sp . ) , and ballistic dispersal ( Aphelandra sp . ) . Each plantlet was identified as growing from a seed or a fragment and the percent of fragment regrowth was compared between species. Piper sp . and A. obtusil obum showed the highest rates of asexual reproduction, followed by Aphelandra sp . The species with generalist pollination and dispersal syndromes showed the lowest rates or asexual reproduction. This study shows specialist syndromes to utilize asexual repr oduction as a means of proliferation , presumably due to the ineff iciency of specialist syndromes . These results have important implications in understanding the vegetative properties of the understory. RESUMEN La reproducciÃ³n sexual aumenta la variabilidad genÃ©tica y permite a la descendencia transportarse lejos de la planta madre. Sin embargo, algunas plantas en los bosques tropicales son capaces de reproducirse con fragmentos, conllevando a una alta densidad de clones en la proximidad de la p lanta madre. La mayorÃa de las plantas requieren de animales para el transporte de polen y semillas, y en algunos casos las plantas tienen relaciones especializadas con un animal, dependiendo exclusivamente de ellos para una exitosa reproducciÃ³n. Otras p lantas tienen relaciones generalistas con polinizadores y dispersores con muchos animales capaces de completar las labores reproductivas para la planta. Este es el primer estudio que examina la relaciÃ³n entre los polinizadores y sÃndromes de dispersiÃ³n y la prevalencia de reproducciÃ³n asexual por medio de fragmentos en hÃ¡bitats naturales. ColectÃ© plantas de especies con polinizadores especializados ( Piper sp.), dispersores especializados ( Anturium obtusilobum ), polinizadores y dispersores generalistas ( In ga marginata , Psychotria spp., Lonchocarpus oliganthus , and Chamaedorea sp.), y dispersiÃ³n balÃstica ( Aphelandra sp.). Cada plÃ¡ntula fue identificada como creciendo de una semilla o fragmento y el porcentaje de crecimiento por fragmentos se comparo entre especies Piper sp. y A. obtusilobum mostraron las mayores tasas de reproducciÃ³n asexual, seguidos por Aphelandra sp. Las especies con polinizadores generalistas y sÃndromes de dispersiÃ³n mostraron las menores tasas de reproducciÃ³n asexual. Este estudio m uestra que los sÃndromes generalistas utilizan la reproducciÃ³n asexual como mÃ©todos de proliferaciÃ³n presumiblemente debido a la ineficiencia de los sÃndromes especialistas. Estos resultados tienen una importancia en el entendimiento de las propiedades ve getativas del dosel del bosque.
INTRODUCTION Sex is great , but sometimes you have to do it yourself . Outcrossing via sexual reproduction leads to increased genetic variation, which is essential for resilience and maintenance of populations ( Luck et al. 2003 ) . In tropical communities, this genetic variation is important for population level defense against the diverse range of herbivores and pathogens . In addition, seed dispersal maintains community diversity by moving reproductive material away fr om the parent plant (Wang & Smith 2002). Though seemingly paradoxical, many tropical species are also capable of asexual, vegetative reproduction (Kinsman 1990, Sagers 1993 ), which may reduce genetic variability within a population and lead to clumps of cl ones ( Sagers 1993, Bush 2000). The advantage s of sexual reproduction are able adaptations to promote out crossing (Sagers 1993). There is no doubt that plants and pollinators have 1983), with selection favoring plant traits that ensure reception of compatible pollen grains and dispersal of pollen to oth er conspecifics (Janzen 1977). Morphology, chemistry , a nd phenology of fruiting all have adaptations that promote th e correct anima ls to disperse plant s seeds (Janzen 1983a ) . Extreme cases of coevolution result in specialization between plants and pollinators or d ispersers. In the tropics, some plants produce high quality fruits to attract specialist frugivores , which should provide dispersal that increase s the probability of a dispersed seed surviving to reproductive age . Other plants produce a lot of small, lower quality fruits for more generalist dispersers (Wenny 2000). However, a study by Wenny (2000) found minor differen ces in survival of di spersed and non dispersed seeds . Thus, W enny failed to support the hypothesis that specialist dispersers are , in fact, high quality dispersers for the plant . In addition, d isruption of a specialist relationship could reduce the fitness of both plant and animal, and therefore, e xtreme specialization of both pollination and dispersal relationships may not be an ideal strategy (Feinsinger 1983, Janzen 1983a ). Lasso et al. (2009) propose d the hypothesis that asexual reproduction by resprouting of fragments may have evolved in environments with low opportunities for sexual reproduction. This could be a result of seed predation or low seed viability in general (Lasso et al. 2009). In t ropical forests , there is a strong presence of dens ity dependent predation and recruitment (Janzen 1983b, Harms et al. 2000), both of which reduce the sexual reproductive success of plants, and may promote conditions promoting regeneration by fragments (Kinsman 1990, Bush 2000) . Tropical moist and wet fore st communities have little variance in rainfall and temperature throughout the year, and asexual reproduction is likely to be a successful strategy u nder stable conditions (Sagers 1993) because there is less need for genetic variation . In addition, u nderst ory plant s are frequently broken by falli n g trees and plants, and the high moisture levels likely promote sprouting, grow th , and persistence of fragments resulting from disturbance (Kinsman 1990) . Asexual reproduction from fragments is poorly studied but has many implications for tropical biodiversity . If prevalent in the understory, fragment regrowth could be important for persistence of individuals (Kinsman 1993), but also has potential to reduce the genetic he terogeneity of tropical communiti es (Sagers 1993). In addition, species that have high instances of resprouting will have more clones in the population and increased self pollination (Lasso et al. 2009). Finally, resprouting could have important implications in gap dynamics in tropical forests (Kins man 1993, Dietze and Clark 2008, Lasso et al. 2009). Clearly, it is important to learn more about reproduction from fragmentation in order to better understand its role in maintaining both populations and diversity in tropical forests. T his study examines the
frequency of asexual reproduction via fragmentation in various plant species in the San Luis Valley of Puntarenas, Costa Rica that have different modes of pollination and dispersal . Based on the hypothesis by Lasso et al. (2009), and observations by Ja nzen (1 983b) and Feinsinger (1983) about the potential disadvantages of specialization , I expect to see a greater frequency of reproduction by fragmentation in plant species with specialist pollination or dispersal syndromes , as t his could be utilized as a method of persisting in the understory when sexual reproduction is inefficient. METHODS Study s ite This study took place in patches of intact pre montane moist forest in the San Luis Valley of Puntarenas, Costa Rica . San Luis is on the pacific slope between 700 and 1000 m of elevation and receives 1200 2200 m m of rainfall per year ( Haber 2000 a ). Fragmentation r ate To determine whether species differ ed in the level of asexual reproduction from fragments, plantlets sm aller than 15 cm tall were collected from natural populations . Plantlets were collected 2 m off the trail to avoid collection of fragments caused by trail use and maintenance. Each plantlet was determined to have been derived from a seed or an abscised pl ant fragment ( Fig. 1) and then replaced in the ground . Development from fragment s is distinguishable in many ways. One clue is that f ragments are easily dislodged from the soil in the first years of growth (Kinsman 1990) . When present, a twig at the stem root junction of the plantlet i ndicates growth from fragment. Finally, the presence of callous tissue at the stem root junction is an indicator of a fragment (Sage r s 1993). On the other hand, those plants with smooth root to stem transitions and with local ized root masses were considered seedlings. If derivation was questionable, that plantlet was replaced and not included in the data. After identification, plants were replaced in the understory. M ean percent fragmentation for each species was calculated as the number of plants derived from fragments over total number of plants collected and compared among species using a One way ANOVA . FIGURE 1. Examples of seedlings (A) and fragments (B, C). Seedlings have straight and smooth transitions from stem to root whereas fragments show callous masses (B) or twigs attached (C) at the root stem junction. A B C
Study Species This study fo cused on seven plant species with various life history strategies. Species were identified to species when possible, though many genera contain species that are difficult to differentiate at such a young age. The species studied were Piper sp. , Anthurium obtusilobum, Aphelandra sp . , Inga marginata, Psychotria spp ., Loncho carpus oliganthus, and Chamaedorea sp . (Table 1). Piper sp . (Piperaceae) is an understory shrub often found in disturbed habitats. This species is pollinated by numerous small insects and dispersed specifically by Carollia bats (Fleming 1983) . Anthurium ob tusilobum (Araceae) is an epiphytic or terrestrial herb . The spad ix flowers for two to three week s and goes through a female phase followed by a rest phase followed by a male phase. Eugloss inae bees visit the flowers during this time and serve as pollinators. The fruit is a juicy red berry dispersed by birds (Zuchowski 2007). Aphelandra sp . (Acanthaceae) is a hummingbird pollinated shrub about 2 m tall found in forested or disturbed areas. The f ruit is a dehiscent capsule from which seeds are dispersed ballistically (Zuchowski 2007). I nga marginata (Mimosaceae) is a large tree whose flowers are pollinated by insects and birds and dispersed by mammals ( Haber 1983 c ). Plants of the genus Psychotria spp . (Rubiaceae) are shrubs found in the understory. These shrubs are pollinated by insects and dispersed by birds ( Haber 2000b ). L onchocarpus oliganthus (Papilionaceae) is a small tree that is pollinated by insects and dispersed by wind (Janzen 1983 c ). Ch amaedorea sp . (Arecaceae) is an understory palm common throughout Costa Rica. This palm is pollinated by insects and wind, and dispersed by birds and mammals ( Haber 2000b , Zuchowski 2007). RESULTS Between 81 86 plantlets of ea ch species were collected . S pecies was shown to have a significan t effect on percent regeneration from fragmentation ( F 6, 72 = 13.56, P < 0.0001) . Both fragments and seedlings were found for all species studied except Chamaedorea sp . , which had zero plantlets derived from fragments . Piper sp. has a specialist dispersal syndrome (Table 1) and showed the greate st regrowth from fragment with a mean percent of 84.22 (Fig. 2) . Percent fragment regrowth by Piper sp. was no t significant ly different from A. obtusilobum , with a specialist pollinator, or Aphelandra sp . , with explosive dispersal ( P > 0.05, Table 1). These species had mean percent age regrowth from fragment s of 66.84 and 56.49, respectively ( Fig. 2). Though it showed almost 3 0 percent greater rates of regene ration from fragments than I. marginata and Psychotria spp . , and almost 35 percent greater rates of regrowth than L. oliganthus , A. obtusilobum was not significantly different from these species ( P > 0.05 ). I. marginata reproduced from fragment 29.92 percent of the time , Psychotria spp . 29.49 percent, and l. oliganthus was fragment derived 22.42 percent of the time (Fig. 2). These species are generalist s in both pollination and dispersal (Table 1 ). Finally, I. marginata and l. oliganthus did not show a significant difference from Chamaedorea sp . ( P > 0.05, Fig. 2), which had zero fragment regeneration and has a generalist po llinator and disperser (Table 1 ) .
TABLE 1. Pollination and dispersal syndromes of focal plant species (S=specialist, G=generalist, E=explosive) Species Pollination Dispersal Piper sp . (Piperaceae) G S Anthurium obtusilobum (Araceae) S G Aphelandra sp . (Acanthaceae) G E Inga marginata (Mimosaceae) G G Psychotria s p p . (Rubiaceae) G G Lonchocarpus oliganthus ( Papilionaceae) G G Chamaedorea sp . (Arecaceae) G G FIGURE 2 . Mean percent of plantlets regenerated from fragments with SE bars shown . 81 86 p lantlets of each species of less that 15 cm were collected from natural habitats and determined to be derived from seed or fragment (see methods for life histories and fragment identification) . Species is shown to have a significant effect on percent regrowth from fragment ( F 6, 72 = 13.56, P < 0.0001). Those species not connected by the same letter are significantly different ( P < 0.05). DISCUSSION This study showed greater rates of fragment reproduction among plant species with specialist pollinators or dispersers, as well as a species with explosive dispersal . Assuming that specialist relationships between plants and animals are more likely to fail than generalist relationships (Feinsinger 1983 , Janzen 1983 b), these results suggest that the ability and probability of resprouti ng is linked to the efficiency of pollinators in successfully transferring pollen and the dispersers in carrying seeds away from parent plants. This is consistent with the findings of Lasso et al. (2009) who showed that this form of asexual reproduction is often associated with 0 10 20 30 40 50 60 70 80 90 100 Piper sp. (Piperaceae) Anthurium obtusilobum (Araceae) Aphelandra sp. (Acanthaceae) Inga marginata (Mimosaceae) Psychotria spp. (Rubiaceae) Lonchocarpus oliganthus (Papilionaceae) Chamaedorea sp. (Arecaceae) Mean Percent Fragment A A A B B C B B C C Species
limited sexual success. My findings also support the hypothesis by Bond and Midgley (2003) that plants with the ability to reproduce from fragments have poorer seed production and vitality ir hypoth esis that fragment regrowth may be selected for in cases where r ecruitment is rare or episodic. The highest rate of fragmentation was 84 percent and was observed in Piper sp . This finding is consistent with the results of Gartner (1989) who found that over 40 percent of Piper plants studied were derived from fragments rather than seeds, and with 58 percent showing no evidence of their origin. Piper sp . has a specialist relationship with bats of the Ca rollia genus as dis persers, which may only remove 5 percent of fruits in a given night (Fleming 1983). This high dependence on single disperser to move a small proportion of seeds could cause a selective pressure for Piper plants to evolve the ability to re produce asexually as a method of increasing in sheer number in order to persist in the understory (Kinsman 1993) . The species showing the next highest rate of reproduction by fragmentation is A. obtusilobum with an average of 67 percent. This species is pollinated by Euglos sinae bees , which must visit a flower in the male phase, and transfer pollen t o a flower in the female phase (Zuchowski 2007) bees a reward of nectar, but rather use scent to attract the bees (Zuchowski 2007). This is similar to some orchids, where the Euglossi n ae bees are actually foraging for nectar or perfume , but may brush up against the pollinarium or stigma in the process (Feinsinger 1983). Like orchids, w hile A. obtusilobum is relying fully on the bees, the bees are able to get the resources they need from many different plant species (Feinsinger 1983) , and therefore they may be u n reliable pollinators . It is possible then that asexual reproduction from fragment is a strategy of this plant to spread and persist. Though Aphelandra sp . did not show a significant difference from some of the generalist species, it also did not show a significant difference in reproductive strategy from both Piper and A. obtusilobum. This species utilizes explosive mechanisms for dispersal and showed 56.5 percent fragment regrowth. Though ballistic dispersal does not rely on any external factors for dispersal, this mechanism has constraints of it s own (Stamp and Lucas 1983) . According to the Janzen Connell hypothesis, dispersal allows seeds to escape high density dependent mortality from pathogens, seed predators and herbivory directly under the parent plant (Wang and Smith 2002). Ther e fore, these plants must rely on secondary disperse rs to maximize the distance of dispersal to avoid density dependent mortality , inbreeding depression and competition (Janzen 1983b , Stamp and Lucas 1983) . With high prevalence of density dependent predation in tropical communities (Janzen 1983b), fragment regrowth in Aphelandra sp . may again be a means of persisting wh en dispersal efficiency is low. This is supported by findings of a previous study describing that plants show ing the ability to sprout from fragments often have low rates of seedling recruitme nt (Bond and Midgley 2003) . Aphelandra sp . did not show a significant difference from I. marginata, Psychotria spp ., or L. oliganthus , though it had 30 35 percent greater mean fragment regrowth than these species. Inga marginata, Psychotria spp ., and L. oliganthus are all generalists in both pollination and dispersal and fragmented less on average than those species with more tightly coevolved relationships. Chamaedorea sp . also has a generalist relationship with both pollinators and dispersers and not a single plant of this species that was collected showed evidence of growth from a fragment. This supports my predictions and , again, suggests fragment regrowth as a strategy of plants with limitations on pollination and dispersal success. There is very lit tle research on the role of fragmentation regeneration in tropical forests, and no previous research attempting to link plant pollination and dispersal syndromes. Still, m ore
research is needed to understand how prevalent this form of asexual reproduction is in tropical systems, as it could play an important role in the maintenance of diversity in the understory, treefall gaps, and disturbed habitats ( Kinsman 1990, Sagers 1993, Dietze and Clark 2008, Lasso et al. 2009). While my findings are consistent with previous studies, there is still poor understanding of the prevalence of this strategy of asexual reproduction in nature and the role it plays in the dynamics of recruitment and genetic structure of understory populations. ACKNOWLEDGEMENTS I thank Anjali Kumar for her assistance in setting up and carrying out my project, for her number crunching and for her enthusiasm about data. I thank Willow Zuchowski and Bill Haber for their botanical knowledge and assistance with plant identification. I would a lso like to thank the LeitÃ³ n family for allowing me to use their property in San Luis and the UGA Ecolodge for kindly granting me access to t heir property for 24 hours. Finally, my thanks go out to Robert Snowden and Valerie Milici fo r their kind introduct ion counseling . LITERATURE CITED B OND , W. J. AND M IDGELY , J. J. 2003. The evolutionary ecology of sprouting in woody plants. International Journal of Plant Science 164: S103 S114. B USH , S.P . 2000. Clonal reproduction through plant fragments in Poikilacanthus macranthus . In N. M. Nadkarni and N. T. Wheelwright (Eds). Monteverde: Ecology and conservation of a tropical cloud forest, p. 88. Ox ford University Press, New York. D IETZE , M. C., AND J. S. C LARK . 2008. Changing the gap dynamics paradigm: v egetative regeneration control on forest response to disturbance. Ecological Monographs, 78: 331 347. F EINSINGER , P. 1983. Coevolution and Pollination In D. J. Futuyma and M. Slatkin (Eds.) Coevolution, pp. 283 307. Sinauer Associates Inc., Sunderland. F LE MING , T.H . Piper (Candela, Candelillos, Piper) In D. H. Janzen (Ed.) Costa Rican Natural History, pp. 303 304. The University of Chicago Press, Chicago. G ARTNER , B. L. 1989. Breakage and regrowth of Piper species in rain forest understory. Biotropica 21: 3 03 307. H ABER , W.A . 2000 a . Plants and Vegetation In N. M. Nadkarni and N. T. Wheelwright (Eds.) Monteverde Ecology and Conservation of a Tropical Cloud Forest, p. 42 . Oxford Universtity Press, New York. H ABER , W.A . 2000 b . Vascular plants of Monteverde In N. M. Nadkarni and N. T. Wheelwright (Eds.) Monteverde Ecology and Conservation of a Tropical Cloud Forest, p. 457 518 . Oxford Universtity Press, New York. H ARMS , K.E., S. J. W RIGHT , O. C ALDER"N , A. H ERNANDÃ‰Z AND E. A. H ERRE . Pervasive density dependent r ecruitment enhances seedling diversity in a tropical forest. Nature 404: 493 495. J ANZEN , D. H. 1977 . Optimal Mate Selection by Plants. The American Naturalist 111: 365 371. J ANZEN , D. H. 1983 a. Dispersal of seeds by vertebrate guts In D. J. Futuyma and M. Slatkin (Eds.) Coevolution, pp. 232 262. Sinauer Associates Inc., Sunderland. J ANZEN , D. H. 1983 b. Food webs: who eats what, why, how and with what effects in a tropical forest? In F.B. Golley (Ed.) Tropical rainforest ecosystems. A structure and functio n, pp. 167 182. Elsevier Scienctific Publishing Co., Amsterdam. K INSMAN , S. 1990. Regeneration by fragmentation in tropical mountain forest shrubs. A merican Journal of Botany 77 : 1626 1633 . L ASSO E., B. M. J. E NGELBRECHT , AND J. W. D ALLING . 2009. When sex is not enough: ecological correlates of resprouting capacity in congeneric tropical forest shrubs. Oecologia 161: 43 56. L UCK , G. W., G. C. D AILY , AND P. R. E HRLICH . 2003. Population diversity and ecosystem services. TRENDS in Ecology and Evolution 18: 331 336. M C K EY , D. 1975 . The ecology of coevolved seed dispersal systems. In L. E. Gilbert and P. H. Raven (Eds.) Coevolution of plants and animals, pp. 159 191. University of Texas Press, Austin. S AGERS , C.L . 1993. Reproduction in neotropical shrubs: the occ urrence of some mechanisms of asexuality. Ecology 17:2 615 618. S TAMP , N . E. AND J. R. L UCAS . 1983. Ecological correlates of explosive seed dispersal. Oecologia 59: 272 278.
W ANG , B. C. AND T. B. S MITH . 2002. Closing the seed dispersal loop. TREE 17: 329 385. W ENNY , D. G. 2000. Seed dispersal of a high quality fruit by specialized frugivores: high quality dispersal? Biotropica 32: 327 337. Z UCHOWSKI W. 2007. Tropical Plants of Costa Rica. Cornell University Press, Ithaca.
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Isabella, Christine, R.
Las plantas con las relaciones especializadas muestran mayores tasas de reproduccin asexual a partir de los fragmentos
Plants with specialist relationships show higher rates of asexual reproduction from fragments
Sexual reproduction increases genetic variation and allows offspring to be transported away from their parent plant.
However, many plants in tropical forests are capable of reproducing from fragments, leading to a high density of clones in close proximity to the parent plant. Most plants require animals for pollen and seed transport, and in some cases plants have a specialist relationship with an animal, relying exclusively on them for successful reproduction. Other plants have generalist relationships with pollinators and dispersers with many animals able to complete reproductive tasks for the plant. This is the first study to examine the relationship between plants pollination and dispersal syndromes and the prevalence of asexual reproduction from fragments in natural habitats. I collected plants species with specialist pollinators (Piper sp.), specialist dispersers (Anturium obtusilobum), generalist pollinators and dispersers (Inga marginata, Psychotria spp., Lonchocarpus oliganthus, and Chamaedorea sp.), and ballistic dispersal (Aphelandra sp.). Each plantlet was identified as growing from a seed or a fragment and the percent of fragment regrowth was compared between species. Piper sp. and A. obtusilobum showed the highest rates of asexual reproduction, followed by Aphelandra sp. The species with generalist pollination and dispersal syndromes showed the lowest rates or asexual reproduction. This study shows specialist syndromes to utilize asexual reproduction as a means of proliferation, presumably due to the inefficiency of specialist syndromes. These results have important implications in understanding the vegetative properties of the understory.
La reproduccin sexual aumenta la variabilidad gentica y permite a la descendencia transportarse lejos de la planta madre. Sin embargo, algunas plantas en los bosques tropicales son capaces de reproducirse con los fragmentos, conllevando a una alta densidad de clones en la proximidad de la planta madre. La mayora de las plantas requieren de animales para el transporte de polen y semillas, y en algunos casos las plantas tienen relaciones especializadas con un animal, dependiendo exclusivamente de ellos para una exitosa reproduccin. Otras plantas tienen relaciones generalistas con polinizadores y dispersores con muchos animales capaces de completar las labores reproductivas para la planta. Este es el primer estudio que examina la relacin entre los polinizadores y sndromes de dispersin y la prevalencia de reproduccin asexual por medio de los fragmentos en hbitats naturales. Colect plantas de especies con polinizadores especializados (Piper sp.), dispersores especializados (Anturium obtusilobum), polinizadores y dispersores generalistas (Inga marginata, Psychotria spp., Lonchocarpus oliganthus, and Chamaedorea sp.), y dispersin balstica (Aphelandra sp.). Cada plntula fue identificada creciendo de una semilla o fragmento y el porcentaje del crecimiento por fragmentos se compar entre las especies de Piper sp. y A. obtusilobum mostraron las mayores tasas de reproduccin asexual, seguidos por Aphelandra sp. Las especies con polinizadores generalistas y sndromes de dispersin mostraron las menores tasas de reproduccin asexual. Este estudio muestra que los sndromes generalistas utilizan la reproduccin asexual como mtodos de proliferacin presumiblemente debido a la ineficiencia de los sndromes especialistas. Estos resultados tienen una importancia en el entendimiento de las propiedades vegetativas del dosel del bosque.
Text in English.
Costa Rica--Puntarenas--Monteverde Zone--San Luis
Plantas del sotobosque
Costa Rica--Puntarenas--Zona de Monteverde--San Luis
Tropical Ecology Spring 2011
Ecologa Tropical Primavera 2011
t Monteverde Institute : Tropical Ecology