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Comparison of fruit removal in tropical tree species between forest and urban areas – Monteverde, Costa Rica

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Title:
Comparison of fruit removal in tropical tree species between forest and urban areas – Monteverde, Costa Rica
Translated Title:
Comparación de la eliminación de frutos de especies arbóreas tropicales entre el bosque y las zonas urbanas - Monteverde, Costa Rica ( )
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English
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Derenge, Dominic
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Subjects / Keywords:
Frugivores--Costa Rica--Puntarenas--Monteverde Zone   ( lcsh )
Fragmented landscapes--Costa Rica--Monteverde Zone   ( lcsh )
Deforestation--Costa Rica--Monteverde Zone   ( lcsh )
Mutualism (Biology)   ( lcsh )
Frugívoros--Costa Rica--Puntarenas--Zona de Monteverde
Paisajes fragmentados--Costa Rica--Zona de Monteverde
Deforestación--Costa Rica--Zona de Monteverde
Mutualismo (Biología)
Tropical Ecology 2008
Destruction of habitat--Costa Rica--Monteverde Zone
Ecología Tropical 2008
Destrucción del hábitat--Costa Rica--Zona de Monteverde
Genre:
Reports   ( lcsh )
Reports

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Abstract:
Tropical frugivorous birds are facing the effects of increased human land development. The conversion of forests to road and buildings interrupts the interaction forest trees and their frugivorous dispersers. This study uses the tree/frugivore mutualism to asses the effect proximity to human influences has upon a forest health. Measurements of the removal rates of Citharexylum costaricensis (Verbenaceae) fruits in a fragment near to the forest displayed significantly higher removal rates than in the urban fragment (Paired T-Test, T=0.996 df=15, p = 0.043, n =16). Separate trials with Solanum rugosum (Solanaceae) fruit displayed the same trend (Paired T-Tests, T = 0.695, df = 10, P = 0.404, n = 11 ). These results show that the human development influences near the urban fragment have a detrimental effect upon this important relationship, which in turn may lead to a loss of stability and biodiversity in urban forest fragments.
Abstract:
Las aves frugívoras tropicales se enfrentan a los efectos del incremento del desarrollo humano. La transformación de los bosques en carreteras y en edificios interrumpe las interacciones entre los arboles y sus dispersores. Este estudio usa el mutualismo del árbol/frugívoro para evaluar el efecto de la proximidad que tiene las influencias humanas sobre la salud del bosque.
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Text in English.
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Born Digital

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usfldc doi - M39-00027
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1 Comparison of fruit removal in tropical tree species between forest and urban areas – Monteverde, Costa Rica Dominic Derenge College of Liberal Arts and Sciences, Arizona State University ABSTRACT Tropical frugivorous birds are facing the effects o f increased human land development. The conversion of forests to road and buildings interrupts the intera ction forest trees and their frugivorous dispersers This study uses the tree/frugivore mutualism to asses th e effect proximity to human influences has upon a f orest health. Measurements of the removal rates of Citharexylum costaricensis (Verbenaceae) fruits in a fragment near to the forest displayed significantly higher removal rates than in the urban fragment (P aired T-Test, T=0.996 df=15, p = 0.043, n =16). Separate trials with Solanum rugosum (Solanaceae) fruit displayed the same trend (Paired T-Tests, T = 0.695 df = 10, P = 0.404, n = 11 ). These results show that the human development influences near the urban fra gment have a detrimental effect upon this important relationship, which in turn may lead to a loss of s tability and biodiversity in urban forest fragments RESUMEN Las aves frugivoras tropicales se enfrentan a los e fectos del incremento en el desarrollo humano. La transformacin de bosques a carreteras y edificios interrumpe las interacciones entre los rboles y su s dispersores. Este estudio usa el mutualismo rbol/f rugvoro para evaluar el efecto de la proximidad a los asentamientos humanos para la salud del bosque. La tasa de remocin de frutos de Citharexylum donnellsmithii (Verbenaceae) en un fragmento cerca del bosque fue mayor que el fragmento urbano. Solanum rugosum (Solanaceae) mostr la misma tendencia. Estos resu ltados demuestran que el desarrollo humano tiene un efecto negativo en esta importante relaci n, que a la larga puede llevar a la perdida de esta bilidad y biodiversidad en fragmentos urbanos de bosque. INTRODUCTION As forests are cleared and replaced by residential areas, the animal species that depend on the trees in these habitats for food are directly a ffected (Belisle and Fortin 2001, Cordeiro and Howe 2003, Crooks et al. 2004). This relations hip between frugivores and trees is essential to the organism removing the seed, as wel l as, to the tree itself. While the animal obtains nutrients the tree is able to disper se its seeds. Fruit removal is witnessed in forests around the world. Urbanization is often th e reason behind forest loss and disruption of important intraforest interactions. This may result in the worst of consequences; extinction (Marzluff 2001), not to mention many less publicized environmental changes. A loss of species or a read justment of the environment around a species would directly affect the relationship betw een trees and frugivores by directly

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2 reducing the available frugivores or dispercers. An d as anthropogenic changes disrupt this mutualism, it may become more difficult for it to function effectively (Cordeiro and Howe 2003). Previous studies have examined how different levels of deforestation have impacted fruit/frugivore mutualisms. The removal o f fallen seeds by Nasua narica (Procyonidae) was studied in different sized forest fragments. I t was determined that the seed removal rate was slower under more isolated tr ees. This suggests that dispersers visit solitary trees at lower frequencies than that of the non-solitary trees (Jurando 2006). Fragmentation and urbanization often lead to more s olitary and exposed trees. This concept could be expected to apply to avian communi ties as well. Many forest avians have difficulties adjusting to differences in habit at quality (Githiru 2006). Furthermore, scientists determined that trees in disturbed fores t areas in Tropical Africa showed a significant decrease in frugivore community species richness, as well as, overall visitor density This decrease in frugivores in deforeste d areas resulted in a decrease in overall fruit removal, which was not compensated by disturb ance adapted frugivores moving in from the already disturbed areas (Kirika et al. 200 7). Another study compared the richness of birds in a developed forest with an orc hard and found that the orchard only displayed 75% of the richness found in the forest, and also consisted of smaller birds (Round 2006). This may have an impact upon the dis persal levels and richness of fruiting trees in cleared or altered habitat. Finally, it has been shown that birds homing abili ties actually decreased in accordance to the amount of cleared land in their f light paths (Belisle 2001). This would decrease the likelihood of forest birds traveling t hrough cleared lands to urban trees. Contrary to this idea that the bird/tree relationsh ip is strongest in continuous forest, Aldrich and Hamrick (1998) stated that tree s in cleared areas were dominant over individuals in a continuous forest or in fragments. These trees received much more attention from their pollinators and dispersers, an d therefore were more successful There are many species of animals that are forage i n cleared and developed areas very well (Mckinney 2002). These animals may serve to f ill the trophic niche that is left by frugivore that cannot survive in cleared areas. Be cause of this, it is possible that trees that are in urban forests may still have an effecti ve frugivore population to disperse their seeds. The forests of the Monteverde/Santa Elena area in C osta Rica, are a complex web of interactions that have already been effected by urban development. Much of this premontane wet forest was cleared roughly sixty years ago to make way for cattle pasture and eventually urban development (Nadkarni 2000). These forests are the primary habitat of a huge diversity of frugivores, which fo rage from many forest trees. Two examples being Solanum rugosum (Solanaceae) and Citharexylum costaricensis (Verbenaceae). These trees are found both in urban settings and at the forest edge. Their fruit could therefore be a useful tool in measuring the properties and tendencies of disperser flocks between developed and forested lan d. The objective of this study is to determine if the type of habitat affects the fruit removal process. If the clearing of land, truly doe s impacts the frugivore-tree relationship, and fruit in the forest is more effec tively removed than fruit in developed areas there should be a difference in fruit removal rates between urban and forest fragments. Then I proposed that trees in urban sett ings will experience a lower level of

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3 fruit removal than similar trees in the forest. A higher removal rate for the forest trees could give further evidence that trees near to citi es do little to maintain this mutualism and emphasize the importance of forested corridors between forest fragments. Materials and Methods This study took take place between, 10 April 2008 a nd 8 May 2008 in the area surrounding the towns of Monteverde and Santa Elena Costa Rica. Study Species S. rugosum is a small to medium sized tree found in forest ed ge, as well as, urban areas in this region, and fruits from May to September. Its fruits form bunches of small berries that provide a food source for many avian species i n the area (Gargeullo 2008). C. costaricensis is another slightly larger species that is very co mmon in this area and produces a large amount of fruit from January to Ju ne (Gargeullo 2008). Study Sites There were two main study sites. The first consist ed of a small patch of trees near the center of Santa Elena. The second was located in a small cleared area in the protected forest of the Escuela Creativa. These two sites ar e less than half a kilometer apart and were at roughly the same elevation. They both consi sted of a small portion of forest and a forest edge. The major differences between the sit e at the Escuela Creativa and at Santa Elena was the urban effects near to the Santa Elena site. The Santa Elena site was less than a hectare in area and was within 50 meters of paved roads. This area experiences moderate to light traffic and noise. The forest si te at Escuela Creativa is far enough from the town to avoid most sounds, or influences of urb an factors and is continuous with the Monteverde Cloud Forest Reserve and the Santa Elena Cloud Forest Reserve. Procedure Fruiting C. costaricensis and S. rugosum were located outside of each study area and bunches of ripe fruit were harvested from each tree In each study site the same 16 tree/treelet species were identified. Each pair of trees were similar in height and in relatively open areas, which increased their visibi lity. All trees were not producing fruit at the time nor were they adjacent to any large fru iting trees. Using twine, five bunches of C. costaricensis or five bunches of S. rugosum fruit were attached to each species at roughly two meters above the ground. All the unrip e fruits were then removed from each bunch and the number of ripe fruit was recorded. F inally, each tree was inspected every 24 hours for four days and the rate of removal of e ach species of fruit was noted. Data Analysis Percent removal of was calculated by dividing the number of berries removed after three days from the total initial number of berries attac hed to each tree. This was important to calculate because the number of berries attached to each tree was not constant. A paired T-test was run for each location to determine if th ere was a significant difference in the percent removal of C. costaricensis or S. rugosum fruits at each site. The total percent removal for each species of tree, in both study sit es, was calculated by averaging the

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4 percent removal (Standard Deviation) of berry for Santa Elena and Escuela Creativa. A final T-test was used to determine if there was sig nificant difference between the total amount of C. costaricensis and S. rugosum fruit removed. RESULTS It was determined that there was no difference in the percent removal of S. rugosum berries between the forest and town (Paired T-Tests, T = 0.695, df = 10, P = 0.404, n = 11 ). On average, each Escuela Creativa tree with S. rugosum fruit showed 42.46% (34.41%) removal, while the trees in Santa Elena showed an average of 29.23% (35.82%). The large standard deviations indicate that there was a large range of removal values in both sites. There is a higher removal rate in the forest than in the town for C. costaricensis (Paired T-Test, T=0.996, df=15, p=0.043, n = 16; Fig. 1). The trees in the Escuela Creativa study site showed an average of 34.42% (28.21%). removal, while those in the Santa Elena study site displayed a 20.12% (17.00%). removal average (Figure 1). When the data from the two berry trials were combin ed and averaged, a trend was shown that there was a higher total percent removal in the Escuela Creativa fragment trees than in the Santa Elena fragment trees (Paire d T-Test, T=0.928, df=11, p=0.093). The tree species in each fragment used to test the removal rates of the berries showed varying amounts of removal. DISCUSSION The removal rates of C. costaricensis and S. rugosum berries displayed trends that frugivores in forested areas have a higher rate of removing fruit than do frugivores in more developed areas. The results indicate that f rugivores remove a higher percentage of berries in the forested regions, than in urban d evelopment. This implies a disruption of the tree/disperser relationship, and therefore a ne ed for conservation of the tree/frugivore relationship. this will require environmentally mi nded urban planning and conservation of multiple ecological functions in forest fragment s near developments. Figure 1: Percent removal for Citharexylum costaricensis fruit from various tree species found in forest and town study sites in Santa Elena, Costa R ica during a three day trial. The percent of Citharexylum costaricensis fruit removed was greater in the forest study site (34.41% 28.21%). than the town study s ite (20.12% 17.00%). (Paired T-Test, T=0.996 df=15, p = 0.043, n =16). 0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1 Percent Removal Forest Percent removal Town Percent removal `

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5 The S. rugosum data showed the trend resulted in data that failed to provide statistical significance, yet still displayed a tre nd of higher fruit removal in the forest than in Santa Elena. The number of tree species studied for this portion of the experiment was small (n = 11) this was because as the project pr ogressed, the fruiting season ended for this berry and the berry supply began to dry out. This resulted in a decreased amount of berries available for testing and may have led to a decreasing removal rate. Nevertheless, the average percent removal values of 42.46% (34.41%) for the Escuela Creativa study site and 29.23% (35.82%) for the Sa nta Elena site still show the trend that frugivore species guilds in the forest are mor e effective in removing fruits than they were in the more developed area. This low sample si ze could be overcome by selecting a species, which was in prime fruiting season. The results from the C. costaricensis trial show that trees near continuous forest tend to be more successful in dispersing their frui t than trees that have to deal with the near developed areas. There are several possibilit ies for this: the study area is small, and it is very near an urbanized area. Fragmentation ca uses problems because it not only isolates the species from more intact forest, but i t also means that there is a reduced diversity and abundance of species available for di spersal (Crooks et al., 2004). It is important to relate the results from this stu dy to the health of the Monteverde/Santa Elena area. Trophic interactions play an important role in forest stability (Worm and Duffy 2003). In order for both trees and their dispersers to survive the tree/frugivore relationship must be upheld. These results also influence the way developed area s are viewed near Santa Elena. Proponents of the Intermediate Disturbance Hypothes is may state that areas near disturbance can be an important center of biodivers ity when near to a forest (Molino and Sabatier 2001). Also species that can successfully survive alongside humans can fill some of the tropic roles left by forest specialists (McKinney 2002). It has been determined that in the Canary Islands, bird species acclimated to urban surroundings ( Palomino and Carrascal 2005). The results of my study suggest that this is not t he case in Santa Elena. The higher level of biodiversity, connectedness, and complexity in the tropics (Mittelbach et al. 2007), may prevent the f rugivore/tree relationship in developments rival the that of the forest. The reduction in fruit removal will lead to both a decrease in trees and frugivore success. This will therefore cause a reduction in diversity (Crooks et al. 2004), and a decrease in stability (Wang and Smith 2002), as wel l. Therefore, without a change of policy in the Monteverde/Santa Elena area, these sm all urban forest fragments may have a very limited and unstable future. The solutions to the disruption of this tree/frugiv ore relationship are the same as the solutions to the problem of forest fragmentatio n worldwide. This truly complicates the situation. With a large portion of tropical ha bitats being developed and fragmented (Peres et al. 2006), it is essential for measures t o be taken to retain the diversity held in these small patches of forest. Furthermore, the Monteverde/Santa Elena has an adva ntage over many other areas with fragmented forest because much of its su rrounding forest is protected. A solution to this problem would be to build forested corridors from forests to fragments. This “greenway” technique has been applied in many temperate zones and has seen

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6 measurable success (Linehan et al. 1995). This wo uld increase the biodiversity of these urban forest patches and would increase the stabili ty and health of these patches forest Further studies should increase the size and breadt h of the sample size. A wider of variety of fruits should be used increase the ac curacy of the study, representing more diverse species interactions. Also, specific tree species and their frugivores should be monitered in an attempt to determine the best way t o protect biodiversity near developments. Cooperation is needed between the di fferent specializations inside the biological studies in an attempt to clean up the ur ban fragments of the forest around Santa Elena. For example, the fragment size cannot just be increased, because it will still be disrupted by the illegal pollution from the nearby developments. Instead fragments must be cared for by local governments on all levels. I f this is successful, it could be possible to see the biodiversity and stability of urban frag ments in Santa Elena be a better representation of the amazing forests that surround the area. ACKNOWLEDGEMENTS I would like to thank the Escuela Creativa for pres erving the forest surrounding their school and allo wing me to study it. I would like to thank the citizens of Santa Elena for clearing forest, building roads and driving the cars which allowed for the completion o f this study. Also, I would like to thanks my Mam Tica for giving me the motivation to wake up and co mplete the research. A big thank you to Alan and Karen Masters for the guidance in determining what I was going to do for my project, and to my TA’s Pablo Allen and Taegan McMahon for statistical supp ort and fresh baked cookies. And finally, a huge thank you to my good friend Tania Chavarra for wis dom, guidance, and moral support throughout the project. Literature Cited Aldrich, P. R. and J. L. Hamrick, 1998. Reproductiv e dominance of pasture trees in a fragmented tropical forest mosaic. SCIENCE 281: 10 3. BELISLE, M., A Desrochers, and M.J. Fortin. 2001. Influence of Forest Cover on Movements of Forest Birds: A Homing Experiment. E cology 82: 1893-1904. Cordeiro, Norbert J. and H.F. Howe. 2003. Forest fr agmentation severs mutualism between seed dispersers and an endemic African tre e. PNAS 100: 14052-14956. Crooks, K. R., A.V. Suarezb, 2 and D.T. Bolger. 2004. Avian assemblages along a gradient of urbanization in a highly fragmented lan dscape biological conservation 115: 451-462. GARGUILLO, M.B., B. Magnuson, and L. Kimball. 2008 A Field Guide to Plants of Costa Rica. pp. 202. Azona Tropical Publication. Oxford Univer sity Press. GITHIRU, M. and L. Lens. 2006. Application of fragm entation research to conservation planning for multiple stake holders: A n example from the Tatia Hills, southeast Kenya. Biological Conservation. 1 34: 271. Henderson, S.P.B., N.H. Perkins, and M. Nelischer. 1998. Residential lawn alternatives: A study of their distribution, form and structure. Landscape and Urban Planning. 42: 135-145. JURADO, E., J. Flores, A.G. Endress, M. Flores, E. Estrada and M. Pando. 2006. Seed removal rates under isolated Trees and continu ous Vegetation in Semiarid Thornscrub. Restoration Ecology 14: 204–209. KIRIKA, J. M, N. Farwig, and K. Bohning-Gaesek. 200 7. Effects of Local

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7 Disturbance of Tropical Forests on Frugivores and S eed Removal of a Small Seeded Afrotropical Tree. Conservation Biology. Marzluff, J. M. 2001. Worldwide urbanization and it s effects on birds. Pages 19–47. In: Marzluff JM, Bowman R, Donnelly R. (eds). Avian Eco logy in an Urbanizing World. Mittelbach, G. G., D.W. Schemske, H.V. Cornell, A.P Allen, J.M. Brown, M.B. Bush, S.P. Harrison, A.H. Hurlbert, N. Knowlton, H.A. Lessios, C.M. McCain, A.R. McCune, E.A. McDade, M.A. McPeek, T.J. Near, T. D. Price, R.E. Ricklefs, K. Roy, D.F. Sax, D. Schluter, J.M. Sobel and M. T urelli. 2007. Evolution and the latitudinal diversity gradient: speciation, ext inction and biogeography. Ecology Letters 10: 315–331. Mckinney, M.L. 2002. Urbanization, Biodiversity, an d Conservation. BioScience Article: pp. 883–890. NADKARNI, N.M. 2000. Monteverde: Ecology and Conservation of a Tropical Cloud Forest. pp. 3. Oxford University Press, Oxford. Peres, C. A., J. Barlow, and F. W. Laurance. 2006. Detecting anthropogenic disturbance in tropical forests. Trends in Ecology and Evoluti on. 21:227–229. ROUND, P. D., G.A. Gale, and W.Y. Brockelman. 2006 A comparison of bird communities in mixed fruit orchards and natural fo rest at Khao Luang, southern Thailand. Biodiversity and Conservation 15: 2873–2 891. Wang, B. C. and T.B. Smith. 2002. Closing the seed dispersal loop. TRENDS in Ecology and Evolution. 17: 379. Worm, B. and J.E. Duffy. 2003. Biodiversity, produ ctivity and stability in real food webs. TRENDS in Ecology and Evolution. 18: 368.


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Comparacin de la eliminacin de frutos de especies arbreas tropicales entre el bosque y las zonas urbanas Monteverde, Costa Rica
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Comparison of fruit removal in tropical tree species between forest and urban areas Monteverde, Costa Rica
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Tropical frugivorous birds are facing the effects of increased human land development. The conversion of forests to road and buildings interrupts the interaction forest trees and their frugivorous dispersers. This study uses the tree/frugivore mutualism to asses the effect proximity to human influences has upon a forest health. Measurements of the removal rates of Citharexylum costaricensis (Verbenaceae) fruits in a fragment near to the forest displayed significantly higher removal rates than in the urban fragment (Paired T-Test, T=0.996 df=15, p = 0.043, n =16). Separate trials with Solanum rugosum (Solanaceae) fruit displayed the same trend (Paired T-Tests, T = 0.695, df = 10, P = 0.404, n = 11 ). These results show that the human development influences near the urban fragment have a detrimental effect upon this important relationship, which in turn may lead to a loss of stability and biodiversity in urban forest fragments.
Las aves frugvoras tropicales se enfrentan a los efectos del incremento del desarrollo humano. La transformacin de los bosques en carreteras y en edificios interrumpe las interacciones entre los arboles y sus dispersores. Este estudio usa el mutualismo del rbol/frugvoro para evaluar el efecto de la proximidad que tiene las influencias humanas sobre la salud del bosque.
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Fragmented landscapes--Costa Rica--Monteverde Zone
Deforestation--Costa Rica--Monteverde Zone
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Deforestacin--Costa Rica--Zona de Monteverde
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