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The Effects of Active vs. Natural Reforestation on Bird Diversity Jessica Springstead Abstract With rapid deforestation rates and loss of diversity the a bility to reforest degraded landscapes faster than they would naturally regrow could be an effective tool for conservation. Many different methods of active reforestation have been proposed (Holl et al. 2000, Lamb et al. 2005, Martinez and Howe 2003) but b ecause it is impossible to plant every species of plant that would be found in an area much of the diversity after planting must come from vertebrate dispersers of which most are birds (Fang and Peng 1997, Holl et al. 2000, Lamb et al. 2005, Martinez and H owe 2003). I wanted to know if active reforestation with trees whose fruits are normally bird dispersed effected the diversity of birds in that area. I observed bird in two areas of the Calandria reserve in Los Llanos, Costa Rica that have been reforesting for approximately nine years. One area was a naturally reforesting coffee plantation and the other a fallow pasture that has been planted with over a thousand trees. Using a Shannon Weiner index and a modified t test, I found that bird diversity was muc h higher in the pasture area than the coffee area. (H' Pasture = 3.419, H' Coffee = 1.192, p< 0.001; E Pasture = 0.927, E Coffee = 0.370) Though there was high overlap of species between areas there were only seven species seen only in the coffee area while 22 wer e seen only in the pasture area. My results show that actively planting trees results in higher bird diversity than natural reforestation. Because the diets of many of these birds includes fruit and so they disperse seeds, it is also likely they will act as agents to increase reforestation even further. Resumen Con ndices de la tala de rboles y la prdida rpidos de diversidad la capacidad de reforestar paisajes degradados ms rpidamente que ellos regrow naturalmente podan ser una herramienta eficaz p ara la conservacin. Muchos diversos mtodos de repoblacin forestal activa se han propuesto (Holl et al. 2000, Lamb et al. 2005, Martnez y Howe 2003) pero porque es imposible plantar cada especie de planta que sera encontrada en un rea mucho de la dive rsidad despus de plantar debe venir de los dispersores vertebrados cuyo la mayora son pjaros (Fang y Peng 1997, Holl et al. 2000, Lamb et al. 2005, Martnez y Howe 2003). Quise saber si la repoblacin forestal activa con los rboles cuyas frutas son nor malmente pjaro disperso efectu la diversidad de pjaros en esa rea. Observ el pjaro en dos reas de la reserva de Calandria en Los Llanos, Costa Rica que han estado reforestando por aproximadamente nueve aos. Una rea era una plantacin de caf natur almente que reforestaba y la otra un pasto en barbecho que se ha plantado con sobre mil rboles. Usando un ndice de Shannon Weiner y una t prueba modificada, encontr que la diversidad del pjaro era mucho ms alta en el rea del pasto que el rea del caf . (H' Pasture = 3.419, H' Coffee = 1.192, p< 0.001; E Pasture = 0.927, E Coffee = 0.370) Aunque haba alto traslapo de la especie entre las reas haba solamente siete especies vistas solamente en el rea del caf mientras que 22 fueron vistos solamente en el re a del pasto. Mis resultados demuestran eso que planta activamente resultados de los rboles en una diversidad ms alta del pjaro que la repoblacin forestal natural. Porque las dietas de muchos de estos pjaros incluyen la fruta y as que dispersan las se millas, es tambin probable ellas actuar como agentes para aumentar la repoblacin forestal incluso ms futura.
Introduction Millions of hectares of tropical forests are being cleared each year, mainly for agricultural purposes that rapidly degrade s oils and are then abandoned for newly deforested lands. (Daily et al. 2001,Holl et al. 2000, Kelm et al. 2008, Lamb et al. 2005, Martinez and Howe 2003). Depending on the intensity and length of time an area was used for agriculture and distance from fore st patches the forest can eventually restore itself but with fewer species than before due to lack of dispersers and suboptimal growing conditions. (Fang and Peng 1997, Holl et al. 2000, Lamb et al. 2005, Martinez and Howe 2003) The most important limitin g factor to reforestation of fallow lands is low rates of seed dispersal. In general, factors that limit seedling establishment include high seed predation, herbivory, intensity of light, low nutrient availability and competition with pasture grasses. (Ho ll et al. 2000, Martinez et al. 2003) There are several techniques being explored to enhance and accelerate reforestation. These techniques generally start by planting fast growing trees or shrubs to create canopy cover, attract animal dispersers and begin restoring soil nutrients (Fang and Peng 1997, Holl et al. 2000, Lamb et al. 2005, Martinez and Howe 2003). Three active reforestation regimens are generally employed: to plant fast growing native timber species, a few species of native successional tree s or many more species to imitate a mature successional stage. Planting timber species is meant to help offset the high cost of planting trees and interest rural landowners in reforesting fallow land. Planting short lived early successional trees is less expensive than trying to recreate a more species rich late successional stage but depends on dispersal of other species from nearby intact forests. (Fang and Peng 1997, Holl et al. 2000, Kelm et al. 2008, Lamb et al. 2005, Martinez and Howe 2003) Whichever technique is used the presence of pollinators and dispersers, particularly birds, are important to the establishment of subsequent plant species. Previous studies have found varying levels of bird diversity in different types of land uses and forest types the levels descending from primary forest, fragmented forest, secondary growth forest, agroforestry systems, shaded cacao plantations, monoculture crops and open pasture (Daily et al. 2001, Frumhoff 1995, Greenberg et al. 2000, Petit et al. 1999, Renjifo 2001, Sodhi et al 2008, Waltert et al. 2003). While there are many studies similar to these or on the effect of reforesting techniques on plant diversity, I have found none that compare the bird diversity and abundance specifically for areas with active an d natural reforestation. I surveyed bird species richness and abundance between two different reforesting areas. One was an old coffee plantation that had been left to reforest on its completely on its own and the other was an old pasture that is being actively reforested. Slightly more than half of the trees planted were Lauraceae with bird dispersed fruits. The planting of a variety species is meant to bypass the early successional stages and the presence of fruiting trees should attract bird disperser s to further increase the plant species diversity. I expected that an actively reforested area would have higher bird species diversity and abundance than a naturally reforesting area.
Methods Study sites I observed birds in two reforesting areas in the Calandria reserve in Los Llanos, Costa Rica. The reserve is 27 hectares and is surrounded on three sides by farmland and on the fourth are houses with more farmland beyond them. One of the areas where I observed birds is a fallow pasture that has been actively reforested and the other is a fallow cafetal that has been regenerating without aid. The pasture area has been planted with 1191 trees of 15 different species from six families. Even though many fruiting trees were planted the only trees that I s aw with fruits were Citharexylum species (Family), Cecropia species (Family) and P. guajava and I only observed two species of birds eating the fruits of the Cecropia. I did not see many fruiting Citharexylum or Psidium guajava and the ones I did see were in the pasture area and did not have ripe fruits. On the other hand the Cecropia were very abundant in the coffee area with a few in the pasture area as well. Both sites have been regenerating for approximately nine years. Each area is approximately two hectares and they are next to each other in the reserve. When the areas were left there were many remnant trees in the coffee area, including some coffee plants ( Coffea arabica : Rubiaceae) and a few remnant trees and guajava ( Psidium guava : Myrtaceae) i n the pasture area. Field Observations Using binoculars, the book A Guide to the Birds of Costa Rica and a notebook, I observed, identified and recorded the species of birds and the number of individuals in each area for eight days. I did point counts a t seven points within each area for 20 minutes each, which ends up as 2 and a half hours per area per day and a grand total of 20 hours per area. Since birds are more active earlier in the morning I alternated which area I visited first each day. Unidentif ied birds were included when they were different enough not to be confused with already identified species. Statistics I compared the daily bird count in the coffee and pasture areas using a t test. I analyzed the species diversity and evenness using Sh annon Weiner diversity index and compared them with a modified t test (Zar 1984). I charted species area curves for both sites. I calculated the overlap of species richness using a Sorenson index. I compared the daily numbers of species seen and daily abu ndances seen between the two areas with a t test. Lastly I compared the overall species richness and abundance using a chi square test. Results The pasture area had both a higher diversity index and evenness than the coffee area (H' Pasture = 3.419, H' Coff ee = 1.192, E Pasture = 0.927, E Coffee = 0.370). The modified t test showed a significant difference in diversity between the two areas (p< 0.001). The average number of species seen per day was significantly higher in the pasture area than in the coffee area (p= 0.01). The average abundance of birds seen daily was nearly significantly higher in the pasture area (p= 0.0560). The total abundance of individuals
between areas was not significantly different (p= 0.125). In the pasture area I saw a total abundan ce of 95 individuals and a daily average abundance of 11.875 individuals. In the coffee area I saw a total abundance of 75 individuals and a daily average abundance of 9.375 individuals. Two species, the Brown Jay ( Cyanocorax morio ) and Grey headed Chachal aca ( Ortalis cinereiceps ), accounted for 40% of the overall abundance of the coffee area (see Figure 1). Whereas the two species with the highest abundances in the pasture area, the Brown Jay and Orange billed Nightingale Thrush ( Catharus aurantiirostris ) accounted for 20% of the overall abundance in that area. (see Figure 2) The chi square for the total number of species found in each place was nearly significantly different (p= 0.063). There were seven species seen only in the coffee area and 22 seen on ly in the pasture area. The species area curves did not asymptote and the line for the pasture remained steadily above the like for the coffee area. (see figure 3)The Sorenson index showed 50.6% similarity in species between areas (Cn= 0.506). Out of 47 sp ecies the two areas shared 18 species. Of the 47 species seen I was able to identify 39 of them of which all are commonly or only found in various open habitats and second growth forest (Stiles and Skutch, 19XX). Of the 47 total species seen, 22 were see n only in the pasture area and seven were seen only in the coffee area (see Table 1). Only six of the identified species were migrants of which four were seen only in the coffee area. Nearly all of identified species were insectivores or omnivores. Out of the 39 identified species, fruit was part of the diet for 21 species. The most frugivorous bird I saw was the Long Tailed Manakin ( Chiroxiphia lanceolata) which also preferred the most dense habitat of all the birds I saw, (Stiles 1989) No mixed species f locks were observed and only six species were seen in groups of more than two 7% 3% 4% 1% 3% 23% 1% 1% 1% 1% 3% 17% 8% 4% 1% 3% 3% 1% 4% 1% 1% 1% 3% 3% 1% Keel Billed Toucan Rufous Tailed HB White Ear Sparrow Rufous Cap Warbler Dusky Capped FC Brown Jay Lesser Greenlet Plain Wren Squirrel Cuckoo Little Hermit HB Emerald Toucannet Grey Head Chachalaca Orange Billed NT Alder FC Masked Tityra Red Billed Pigeon Long Tailed Manakin Streak Headed WC Swainson's Thrush Northern Waterthrush Wilson's Warbler Bright Rumped Atilla Grey Brested Wren Olive Sided FC Unk. stripe HB Firgure 1: Chart of abundances by species in the coffee area of the Calandria reserve in Los Llanos, Costa Rica. The majority of the species abundanc e is from only a few species. (E= 0.370)
4% 1% 4% 3% 3% 1% 1% 4% 3% 1% 9% 2% 1% 4% 2% 1% 2% 11% 4% 2% 1% 4% 1% 1% 2% 3% 3% 1% 1% 2% 1% 1% 1% 1% 1% 1% 1% 4% 2% 1% Keel Billed Toucan Rufous Tailed HB Unk. Swallow White Ear Sparrow Rufous Cap Warbler White Tail Emerald HB Olive Striped FC Dusky Capped FC Swallow Tail Kite Grey Crown Yellowthroat Brown Jay Lesser Greenlet Yellow Throat Euphonia Plain Wren Squirrel Cuckoo Little Hermit HB Emerald Toucannet Black Vulture Grey Head Chachalaca Blue Tailed HB Orange Billed NT Alder FC Green Brested Mango HB Fork Tailed Emerald HB Yellow Faced Grassquit White Winged Becard Masked Tityra White Tipped Dove Red Billed Pigeon Long Tailed Manakin Hoffman's Woodpecker Barred Antshrike Streak Headed WC Unk.brownGround bird Unk. Yellow & brown Unk. Small Grey&yellow Unk Warbler Unk greythroat Unk grey & white Unk. Green throat HB Figure 2 Chart of abundances by species in the pasture area of the Calandria reserve in Los Llanos, Costa Rica. The pasture area had both a higher number of species and a higher evenne ss index. (E= 0.927) 0 5 10 15 20 25 30 35 40 45 0 2 4 6 8 10 Day # Species Pasture Coffee Figure 3 Species accumulation curves for bird species within actively reforested pasture and naturally reforesting coffee plantation in the Calandria reserve in Los Llanos, Costa Rica. Both lines indicate that more species could be found in each area.
Discussion The data supported my prediction that there would be higher bird species diversity in the actively reforested pasture area than in the naturally reforesting coffee area. Based on conclusions fr om previous studies the higher number of tree species in the pasture area leads to higher structural complexity and thus higher diversity of bird species. (Renjifo 2001, Sodhi et al. 2008) From my results it appears that planting a high number of tree spec ies has a large impact on bird species diversity especially given that both areas were next to each other in the same reserve as well as the fact that the coffee area started out with more remnant trees than the pasture area. Taking into account the positi ve effect of remnant trees on new seedling growth and establishment, my results indicate a very strong effect of reforestation techniques on bird species diversity (Holl et al. 2000). The data did not support my prediction that bird abundance would be high er in the pasture area than in the coffee area. Even though abundances between areas are similar, 40% of the overall abundance in the coffee area was from only two species. The species area curves did not asymptote and so more species could be found in bo th areas. I believe that with more sampling days I could have found more species and significantly higher abundances in the pasture. The high species overlap between sites could be explained by the high number of species with preferences for open and sem i open habitats and that the two areas were located next to each other. Also, that many of the birds had diets that included fruit and the majority of the fruiting Cecropia trees at the time were in the coffee area could account for the high species overl ap. Planting trees over a large area is an expensive and labor intensive process and as such it would be too difficult to replant all the possible species of trees and also abiotic conditions prevent many seedlings from establishing. (Holl et al. 2000 ) Because of this further inputs of plant species must come from nearby forest, generally brought by birds or other animal dispersers. It is likely that a higher diversity of birds would lead to a higher diversity of plants and structural complexity which would further increase the diversity of birds and so on, especially since many of the species I found had diets that included much fruit. It would be interesting to go back to these areas after another ten years or another fifty years and to see how the d iversity has increased and if it remained higher in the pasture area. Taking all these things together, the eventual success of returning forest to its original state could depend on the diversity of dispersers bringing in new species. Though the amount o f time needed to get back to primary forest state is on the order of centuries, the overall effect of high diversity early on may persist allowing an actively reforested area to grow back much faster than a naturally reforested area. Since I found that di versity of birds was so much higher in the actively reforested area, further study and refinement of reforestation techniques could have a significant impact on the way recovering forests are managed. Acknowledgements I would like to thank Alan Masters f or helping me find my study sites and patently answering all my questions. I would like to thank Yimen Araya for coming out to Los Llanos to help me find a study site, helping me with my statistics tests and questions and helping me to identify all those confusing species of
birds. Thanks to Lorenzo for showing me around the Calandria reserve and suggesting other study sites and to Amber Fandel for coming with him to translate. Thanks also to Deb Hamilton for answering all my questions about the Calandria reserve. Literature Cited Daily G.C, Ehrlich P.R.,Sanchez Azofeifa G. A. 2001. Countryside Biogeography:Use of Human Dominated Habitats by the Avifauna of Southern Costa Rica. Ecological Applications. 11:1 13 Fang W., S.L Peng. 1997. Development of Sp ecies Diversity in the Restoration Process of Establishing a Tropical Man Made Forest Ecosystem in China. Forest Ecology and Management. 99: 185 196 Frumhoff P.C. 1995. Conserving Wildlife in Tropical Forests Managed for Timber. Bioscience. 45:456 464 Gr eenberg R., P. Bichier, A.C. Angon. 2000. The Conservation Value for Birds of Cacao Plantations with Diverse Planted Shade in Tabasco, Mexico. Animal Conservation. 3: 105 112 Haber W.A., W. Zuchowski, E. Bello. 2000. An Introduction to Cloud Forest Trees: Monteverde, Costa Rica. 2 nd ed. Puntarenas, C.R: Mountain Gems Publications, 202 p. Holl K.D, M.E Loik, E.H Lin., I. A Samuels. 2000. Tropical Montane Forest Restoration In Costa Rica: Overcoming Barriers to Dispersal and Establishment. Restoration Ecolo gy. 8: 339 349 Lamb D., P.D. Erskine, J.A. Parrotta. 2005. Restoration of Degraded Tropical Forest Landscapes. Science. 310. Kelm D.H., K.R. Wiesner, O.V. Helversen. 2008. Effects of Artificial Roosts for Frugivorous Bats on Seed Dispersal in a Neotrop ical Forest Pasture Mosaic. Conservation Biology. 22: 733 741 Martinez Garza C., H.F. Howe. 2003. Restoring Tropical Diversity: Beating the Time Tax on Species Loss. Journal of Applied Ecology. 40:423 429 Petit M.J., Petit D.R., Christian D.G., Powell H. D.1999. Bird Communities of Natural and Modified Habitats in Panama. Ecography. 22:292 304 Renjifo L.M. 2001. Effect of Natural and Anthropogenic Landscape Matrices on the Abundance of Subandean Bird Species. Ecological Applications. 11:14 31 Sodhi N.S, Posa M.C.,Lee T.M., Warkentin I.G. 2008 Effects of Disturbance or Loss of
Tropical Rainforest on Birds. The Auk 125:511 519 Stiles G.F., Skutch A.F. 1989. A Guide to the Birds of Costa Rica. Ithaca, New York. Cornell University Press. 511p. Waltert M., A. Mardiastuti, M. Muhlenberg. 2003. Effects of Land Use on Bird Species Richness in Sulawesi, Indonesia. Conservation Biology. 18: 1339 1346 Zar J.H. 1984. Biostatistical analysis. 2 nd ed. Englewood Cliffs, New Jersey. Prentice Hall Inc. 718p Append ix Table 1 Species seen in only one area of the Calandria reserve in Los Llanos Species only seen in Pasture area Species only seen in Coffee area Unk. Swallow Swainson's Thrush White Tail Emerald Northern Waterthrush Olive Striped Flycatcher Wilson' s Warbler Swallow Tail Kite Bright Rumped Atilla Grey Crowned Yellowthroat Grey Breasted Wood Wren Yellow Throat Euphonia Olive Sided Flycatcher Black Vulture Unk. Stripe Hummingbird Blue Tailed HB Green Breasted Mango Fork Tailed Emerald Yell ow Faced Grassquit White Winged Becard White Tipped Dove Hoffman's Woodpecker Barred Antshrike Unk. Brown Ground bird Unk. Yellow & brown Unk. Small Grey&yellow Unk Warbler Unk Grey throat Unk Grey & white Unk. Green Throated Hummingb ird Table 2 Total number of species and individuals seen in each area of the Calandria reserve in Los Llanos
Species Pasture Coffee Keel Billed Toucan 4 5 Rufous Tailed Hummingbird 1 2 Unk. Swallow 4 0 White Eared Ground Sparrow 3 3 Rufous Cap W arbler 3 1 White Tailed Emerald 1 0 Olive Striped Flycatcher 1 0 Dusky Capped Flycatcher 4 2 Swallow Tail Kite 3 0 Grey Crowned Yellowthroat 1 0 Brown Jay 9 17 Lesser Greenlet 2 1 Yellow Throated Euphonia 1 0 Plain Wren 4 1 Squirrel Cuckoo 2 1 Little Hermit HB 2 1 Emerald Toucanet 4 2 Black Vulture 1 0 Grey Headed Chachalaca 2 13 Blue Tailed Hummingbird 1 0 Orange Billed Nightingale Thrush 10 6 Alder Flycatcher 4 3 Green Breasted Mango 2 0 Fork Tailed Emerald 1 0 Yellow Faced Grassqui t 4 0 White Winged Becard 1 0 Masked Tityra 1 1 White Tipped Dove 2 0 Red Billed Pigeon 3 2 Long Tailed Manakin 3 2 Hoffman's Woodpecker 1 0 Barred Antshrike 1 0 Streak Headed WC 2 1 Swainson's Thrush 0 3 Northern Waterthrush 0 1 Wilson's Warble r 0 1 Bright Rumped Attila 0 1 Grey Breasted Wood Wren 0 2 Olive Sided Flycatcher 0 2 Unk. Brown Ground bird 1 0 Unk. Yellow & Brown 1 0 Unk. Small Grey&Yellow 1 0 Unk. Warbler 1 0 Unk. Grey throat 1 0 Unk. Grey & White 1 0 Unk. Green Throated Hu mmingbird 1 0 Unk. Stripe Hummingbird 0 1
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Los efectos de la reforestacin activa vs. natural en la diversidad de las aves
The effects of active vs. natural reforestation on bird diversity
With rapid deforestation rates and loss of diversity the ability to reforest degraded landscapes faster than they would naturally regrow could be an effective tool for conservation. Many different methods of active reforestation have been proposed (Holl et al. 2000, Lamb et al. 2005, Martinez and Howe 2003) but because it is impossible to plant every species of plant that would be found in an area much of the diversity after planting must come from vertebrate dispersers of which most are birds (Fang and Peng 1997, Holl et al. 2000, Lamb et al. 2005, Martinez and Howe 2003). I wanted to know if active reforestation with trees whose fruits are normally bird dispersed affected the diversity of birds in that area. I observed birds in two areas of the Calandria reserve in Los Llanos, Costa Rica that have been reforesting for approximately nine years. One area was a naturally reforesting coffee plantation and the other a fallow pasture that has been
planted with over a thousand trees. Using a Shannon-Weiner index and a modified t-test, I found that bird diversity was much higher in the pasture area than the coffee area. (HPasture= 3.419, HCoffee= 1.192, p<
0.001; EPasture= 0.927, ECoffee= 0.370) Though there was high overlap of species between areas there were only seven species seen only in the coffee area while 22 were seen only in the pasture area. My results
show that actively planting trees results in higher bird diversity than natural reforestation. Because the diets of many of these birds includes fruit and so they disperse seeds, it is also likely they will act as agents to increase reforestation even further.
Con las rpidas tasas de la deforestacin y prdida de la diversidad, la posibilidad de reforestar zonas degradadas ms rpido de lo que naturalmente volveran a crecer puede ser una herramienta eficaz para la conservacin. Se han propuesto muchos diferentes mtodos de reforestacin activa (Holl et al. 2000, Cordero et al. 2005, Martnez y Howe 2003), pero porque es imposible sembrar cada especie de planta que se encuentra en una zona, gran parte de la diversidad de la siembra debe provenir de los vertebrados dispersores de los cuales la mayora son aves (Fang y Peng 1997, Holl et al. 2000, Cordero et al. 2005, Martnez y Howe, 2003). Quera saber si la reforestacin activa con rboles cuyas frutas son normalmente dispersadas por aves afectaba la diversidad de aves en la zona.
Text in English.
Regeneracin del bosque
Aves -- comportamiento
Tropical Ecology Spring 2009
Bellbird field station
Ecologa Tropical primavera 2009
Diversidad de aves
Estacin pajaro campana
Reserva pajaro campana
t Monteverde Institute : Tropical Ecology