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Bird communities in forested and human-modified landscapes of Central Panama: a baseline survey for a native species reforestation treatment

Bird communities in forested and human-modified landscapes of Central Panama: a baseline survey... International Journal of Biodiversity Science, Ecosystem Services & Management, 2013 Vol. 9, No. 4, 281–289, http://dx.doi.org/10.1080/21513732.2013.842187 Bird communities in forested and human-modified landscapes of Central Panama: a baseline survey for a native species reforestation treatment a,b b b Sunshine A. Van Bael *, Ruby Zambrano and Jefferson S. Hall a b Department of Ecology and Evolutionary Biology, Tulane University, 400 Lindy Boggs, New Orleans, LA 70118, USA; Smithsonian Tropical Research Institute, Apartado 0843–03092, Balboa, Ancon, Panama, Republic of Panama While deforestation continues to be a threat to species diversity in the tropics, reforestation either by natural succession or human tree planting is also occurring. Very little is known about how bird communities respond to human-mediated reforestation schemes in tropical areas. We surveyed bird communities in Central Panama to compare their abundance and richness in mature forest, young natural succession (fallow pastures), active cattle pastures, and native species reforestation areas. We found the greatest abundance of birds in mature forest, while natural succession areas had slightly greater species richness relative to mature forest. Bird communities were most similar in forest and natural succession areas, and were distinct from bird communities in cattle pastures and reforestation areas. Migratory bird species were most abundant in the young natural succession areas. Reforestation areas that were closer to mature forest had a greater abundance of birds relative to areas further from forests. Our study provides a baseline for future studies at this site that will allow assessment of the speed at which reforestation efforts with tree plantations will support a more diverse and abundant bird community. Moreover, our finding of the greatest species richness and migratory bird abundance in a natural succession habitat supports previous bird community studies in agroforestry and successional habitats. Keywords: agroecosystem; biodiversity; canopy; feeding guilds; migratory birds; restoration; species richness; succession; tropical birds Introduction scrub species (Petit et al. 1999; Petit & Petit 2003). At the same time that deforestation is occurring, other parts of Many species are suffering declines in their population Panama are being reforested either by natural succession numbers, with habitat loss due to land-use change cited as or by establishment of tree plantations (Wright & Muller- the major cause (Millenium Ecosystem Assessement 2005). Landau 2006; Wright & Samaniego 2008; Hall et al. 2011; Since >90% of the land area in tropical areas occurs outside van Breugel et al. 2011). Very little is known about how the boundaries of forest reserves, planning for conservation bird communities are responding to various types of will require a better understanding of the value of human- reforestation schemes in Panama, although recent work in modified landscapes for supporting biological diversity Costa Rica has shown that some migratory birds preferred (Chazdon et al. 2009). Birds are often used to assess or plantation-style reforestation treatments (Lindell et al. 2011) predict the effects of land-use change (Hughes et al. 2002; and that overall bird community composition and species Petit & Petit 2003;Harvey etal. 2006), because they are richness was similar in actively and passively restored easy to observe and provide important ecosystem services patches (Reid et al. 2012). (Sekercioglu 2006; Whelan et al. 2008). Moreover, many In Central Panama, many forests have been protected birds have diverse and specialized requirements for food, along the banks of the Panama Canal (Ibáñez et al. 2002). which makes them good indicators for habitat change. A Despite this, approximately half of the canal’s watershed is variety of types of agricultural development have reduced deforested, and reforestation of the watershed is the official forest cover and thereby decreased the abundance and policy (Law 21) of Panama Canal Authority (ACP). Since diversity of bird species relative to forest habitats in the 2009, the Agua Salud Project (ASP), an ecosystem services Neotropics (Petit et al. 1999;Estrada &Coates-Estrada project in the Panama Canal Watershed, has begun to 2005; Faria et al. 2006;Harvey et al. 2006; Scales et al. investigate the effects of different types of reforestation 2008;Milder etal. 2010) as well as the Paleotropics efforts and land uses on hydrology, carbon storage, and (Waltert et al. 2004, 2005; Marsden & Symes 2008; species conservation (Stallard et al. 2010). Due to the Scales et al. 2008). Like other countries in Central America, Panama has large quantities of data being collected on the environment increasingly become fragmented due to forest clearing for and the 25–40-year project horizon, the ASP offers a cattle pastures and subsistence agriculture (Kaimowitz unique opportunity to monitor changes in bird communities 1996). The result of forest clearing or human modification among different landscape types in Central Panama. is a simplification of bird communities and a shift toward Here, we present data from bird surveys conducted communities comprising of open woodland, grassland, and between 2010 and 2011 within the treatment sites of the *Corresponding author. Email: svanbael@tulane.edu © 2013 Taylor & Francis 282 S.A. Van Bael et al. ASP. We surveyed bird communities in mature forest, contained large streams or rivers, as in mature forest. natural succession areas, cattle pastures, and a newly These transects were situated approximately 1.5 km from installed reforestation site. Our overall hypothesis is that the edge of Soberania National Forest. In our transect human plantation efforts can eventually mimic natural areas, canopy cover averaged 51%, with tree heights succession for providing bird habitat. We predict that (1) ranging from 4 to 8 m. bird communities in newly planted reforestation areas will most resemble bird communities in cattle pastures, and (2) Pasture when a canopy forms in the reforestation area, the bird communities in reforestation areas will resemble those of Two transects were in active cattle pasture either within or natural succession areas. This paper provides data to test near the ASP principle area. Both pastures had a small the first prediction. Our specific goals in surveying the river running through the center with gallery forest, and bird communities were to estimate and compare the abun- each had isolated, large, remnant trees in them. Each area dance, species richness, and species composition of birds of pasture included ~40 ha and the surrounding matrix of using the four habitat types at the baseline, when refores- land uses included young naturally regenerating secondary tation sites were first planted. We also wanted to assess forest (rastrojo) and other pastures. Cattle were grazed at whether distance from the forest edge affected bird abun- the intensity of ~1.3 heads/ha. These transects were situ- dances within the newly planted reforestation site. ated approximately 2–3 km from the edge of Soberania National Forest. Canopy cover was approximately 16% in our transect areas, with all cover coming from 20 to 25 m Methods tall remnant trees. Study sites We received permission for our observational field study Reforestation with native species from the Panama’s National Authority for the Two transects were set up in two distinct areas where Environment (ANAM) and the Panama Canal Authority reforestation with native species was occurring with the (ACP). The principle study site of the ASP borders ASP site. All land was cleared completely before planting Soberania National Park in Central Panama (9°13′ N, to homogenize the light environment, a requirement for the 79°47′W). Following is a description of each habitat type experimental design of the plantations that would not where we conducted bird surveys in 2010–11. Our survey necessarily be followed to this extreme in a production areas could not be placed randomly in the landscape due to plantation. Its previous use included active cattle pasture the constraint that we had permission to work only in and and young regenerating secondary forest (<5-years old). alongside ASP-owned areas. Further floristic details about The reforestation treatments in 2008 included 75 ha of these sites and representative photographs and maps are at land area where five native timber species (Anacardium http://www.ctfs.si.edu/aguasalud/page/catchments/#forest. excelsum, Dalbergia retusa, Pachira quinata, Tabebuia rosea, and Terminalia amazonia) and five companion Mature forest native species (Erytrina fusca, Gliricidia sepium, Inga punctata, Luehea seemannii, and Ochroma pyramidale) Two transects were established in forested areas of were planted either as a monoculture or as polycultural Soberania National Park (22,000 ha total). One transect mixes. The bird survey transects were not situated with was accessed from Pipeline Road near the Limbo River, respect to particular plots of monoculture or polycultural in an area where previous studies have described the avi- treatments, but rather covered a much larger area that fauna (Robinson et al. 2000). A second transect was encompassed many treatments (each reforestation treatment accessed from the ASP. Neither site included large streams plot was 45 × 39 m). At the time of the 2010 survey, most or rivers within 30 m of our bird count points. The forest in plantation trees were ~1–2 m in height. There was no Soberania is a mix of mature second growth and old growth canopy cover above the transects with native species refor- forest, both of which were represented in our transects (one estation. The grassy vegetation between trees was cleared each). Canopy cover was approximately 96% in our mature four times a year since planting. One reforestation area was forest transect areas, with canopy heights ranging from 23 directly adjacent to Soberania National Forest while another to 28 m (see vegetation survey methods below). was ~2 km away from the forest edge. Natural succession Bird and vegetation survey methods Two transects were in natural succession within the prin- ciple ASP area. These sites were abandoned pasture In order to compare bird species richness and abundance, (approximately, 5–6 years previously) and reforestation we sampled 80 points across the various land uses was occurring via natural regeneration. Another term for described above. The sample points fell along transects this type of habitat is rastrojo. The area contained trees within each habitat type (see sample sizes in Table 1). that were about 4 m high, but taller, remnant trees from Within transects, each point was separated by >100 m cattle pastures or live fences were also present. Neither site and at least 50 m from the edge of a particular habitat. International Journal of Biodiversity Science, Ecosystem Services & Management 283 Table 1. Density estimates (number of birds per ha, D) and the concave densiometer at the center of the bird count point. corresponding coefficients of variation (CV) and 95% confidence For canopy and emergent tree heights, we used a digital intervals (CI95) generated by the program DISTANCE based on rangefinder to improve our estimates. These vegetation mea- the number of bird detections (n). surements were not taken in the reforestation treatments Density because no canopy existed. Further, due to constraints, our estimate Percentage vegetation sampling was not complete across all bird count Land use n (no/ha) CV CI points, but at least 10 points per habitat type were sampled. Mature forest 571 57.8 1.06 56.6–59.0 Natural 658 15.9 16.94 10.7–20.7 Statistical analyses succession Reforestation 77 0.596 0.39 0.590–0.600 We used the program DISTANCE 6.0 (Thomas et al. Cattle pasture 423 11.47 17.04 8.22–16.00 2010) to estimate and compare the bird density among the four habitat types, pooled over all 480 counts. We fit at least six detection functions per habitat and used AIC model selection to choose the best-fit models. These were In particular, if a stream or river ran through our land-use a half-normal model with a hermite polynomial expan- type, we consistently set up our bird counts to avoid the sion for mature forest, and a uniform model with cosine stream-associated vegetation. We used a hand-held GPS to polynomial expansion for all other habitat types. The set up the points and confirm distances. detection functions allowed an estimation of bird density For this study, we define a transect as a collection of (number of birds per hectare) in each of the four habitat 10 sample points, and a survey as one of the three distinct types. We compared 95% confidence intervals to assess time periods when transects were walked and points were differences in bird density. The DISTANCE program visited. All 80 points were visited twice within a survey, requires a minimum of 60–100 observations within a with at least 5 days between visits. The first survey category to give reliable estimates, so we did not do occurred during the dry season, in January and February this analysis for migratory birds. While DISTANCE is of 2010. The second survey happened in June and July often used to estimate detection probabilities and density 2010, during the wet season. The final survey occurred estimates for individual bird species, we did not pursue during the dry season in January and February of 2011. this approach since only two bird species in our dataset Since there were three surveys, each sample point was had more than 60 individuals. In addition to the visited a total of six times during the study for a total of DISTANCE bird density estimates, we calculated the 480 bird count samples. mean number of bird detections in different landscape At the sample points, we counted birds using 10-min- types based on count data with no distance corrections, ute fixed radius point counts (25 m radius) to record all so that our results could be compared to previous studies. visual and aural signs of birds. The point-count method is This also gives a relative abundance of birds in habitats best suited for obtaining a broad sample of bird commu- with similar detection probabilities. To compare bird nities across a patchy landscape (Petit et al. 1995). abundances in reforestation areas that were close and far Moreover, limiting our counts to a 25-m radius increased from the forest edge, we relied on bird detections per the detectability of birds across the different landscape point, as detection likelihood was similar in the same types (Petit et al. 1995) and decreased the likelihood of type of habitat. We used a two-tailed t-test to compare counting the same birds from one point to the next. We the abundance of birds in reforestation areas near and far surveyed for 10 minutes to improve the quality of our raw from the forest edge. To further describe the bird com- count data in terms of detectability (Etterson et al. 2009). munity, we used the point count data to list the three most During the hours of 6:00–10:00 am, on non-rainy days, abundant species per habitat, and classify the species one observer (RZ) was responsible for conducting the using diet and habitat information from Ridgely and visual and aural surveys. For each bird detected, the Gwynne (1989). observer estimated and recorded the radial distance from We used both point count data and our cumulative list herself to the individual bird. An assistant, who made of birds to report the total number of species observed in digital audio recordings during each point count, accom- each habitat. With the point count data only, we used panied the observer. We did not count birds that were EstimateS (2010) to construct sample-based rarefaction flying over the count circle. Along with point count data, (or species accumulation) curves for comparison of spe- we kept an ongoing list of additional sightings outside of cies richness among the habitats, scaling the curves to the points as we walked the transects. On most days we number of individuals and the number of samples (Gotelli completed one transect (or 10 sample points). & Colwell 2001; Colwell et al. 2004). Since our curves did To compare canopy characteristics among land-use not reach asymptotes, we also used an asymptotic species types, we rapidly estimated canopy cover, average canopy richness estimator for species abundance data, Chao1, to height, and the height of the tallest emergent tree in our 25 m represent species estimations in each land-use type (Chao radius sample circle. To estimate the canopy cover, we took 2005). For these analyses we used data from point counts four readings (facing N, S, E, and W) with a hand-held in all of the surveys combined. 284 S.A. Van Bael et al. We also wanted to compare the species community (a) composition among the habitats using point count data. We followed the techniques outlined in Clarke (1993), which include calculating the Bray–Curtis index of similarity (Bray & Curtis 1957), followed by non-metric multidimen- sional scaling (NMDS) and analysis of similarity (ANOSIM). These analyses were all completed using the program PAST (Hammer et al. 2001). The community composition analyses compared the bird communities among sample points, with the bird species identities summed up over all surveys at each point. We also calculated 6 (b) an overall Bray–Curtis similarity value to numerically com- pare between the sites. Results Data from complete bird list We recorded 225 bird species in our complete list, which combined fixed radius point counts and additional obser- vations between points (Table S1). We recorded 109 spe- (c) cies that occurred in mature forests only, and 143 species 0.6 in natural succession. In cattle pasture and reforestation areas, we recorded 97 and 61 species, respectively for our 0.4 complete list. Across all land-use types, we recorded 26 migratory bird species in our complete list (Table S1). 0.2 Data from point counts 0.0 MF NS C R We counted 1729 individual birds in fixed radius point Land-use type counts. Using distance corrections, bird density estimates were significantly different in the four land uses, with the Figure 1. Abundance estimates for birds in various landscapes of Central Panama. (a) Density estimates and 95% confidence greatest density estimate in mature forest, then natural suc- intervals (error bars) for birds (no. of birds per hectare) using cession (Figure 1a, Table 1). Bird density estimates in natural distance corrections. (b) Mean detections (or no. of birds) per succession had overlapping confidence intervals with esti- point count survey for all bird species, error bars are one standard mates from cattle pastures, although the overall estimate was error. (c) Mean detections (or no. of birds per point count survey greater in natural succession areas. Reforestation areas had for migratory birds only, error bars are one standard error. For all very low bird density estimates (Table 1). When using the panes, MF = mature forest, NS = natural succession, C = cattle pasture, R = reforestation with native species. number of birds per point (or mean detections per point), we observed similar values in mature forest and natural succes- sion (Figure 1b). Relative to these two habitats, we observed R = 0.8301, p < 0.001). The low similarity between com- lower mean detection values for birds in cattle pasture and munities in forested and non-forested landscapes is also reforestation habitats (Figure 1b). In contrast, detection apparent when comparing the most abundant species of values for migratory bird species were greatest in natural each habitat (Table 4). The mature forest was dominated succession and similarly low in the other habitats (Figure 1c). by forest specialists and woodland generalists, while the The accumulation of species occurred most rapidly other habitats were dominated by woodland and agricul- during surveys in natural succession and mature forest tural generalists (Table 4). The primary bird species in the (Figure 2). The curves demonstrate the high species rich- reforestation areas were those that foraged in open, scrub ness observed and estimated for natural succession, forest, habitats with seed-eating birds highly represented (Table 4). and pasture, which differed from the reforestation area Distance to the mature forest edge had an effect on bird where abundances and species diversity estimates were abundance and species richness in the reforestation areas. relatively low (Table 2). The NMDS comparison of species Using data from point counts at these two transects only, we found that the site adjacent to the forest had a significantly similarity composition, however, suggests that species higher mean bird detections per point (mean ± 1 s.e. was composition was more similar between mature forest and 1.48 ± 0.10 for adjacent and 1.15 ± 0.10 for far transect; natural succession, while cattle pasture bird communities t = 2.339, d.f. = 18, P = 0.031 (two-tailed)). The number of were more similar to those in the reforestation treatments species observed in each transect were 17 and 8 for adjacent (Table 3, Figure 3). Among all habitats, the bird community and far transects, respectively. Abundances in this habitat compositions were significantly different (ANOSIM No. of migratory birds/point No. of birds/point Estimated birds/hectare International Journal of Biodiversity Science, Ecosystem Services & Management 285 (a) were very low in general, and most sample points (81/120 or 68% of the points) had zero birds. MF According to the IUCN Red List, nearly all of the NS species we observed were in the category of Least 80 C Concern for their conservation status. The only exceptions were two species in the Near Threatened category. These were Harpia harpyja (Harpy Eagle, observed in mature forest, known to be a reintroduction in the area) and Vermivora chrysoptera (Golden-winged Warbler, observed in natural succession). 0 20 40 60 Discussion No. of samples (b) Our study recorded the greatest abundance and species rich- ness of birds in mature forest and natural succession habitats. Cattle pastures and the early stages of tree plantations sup- ported fewer bird species and had more similar species composition. We discuss these results with respect to differ- ences in bird abundances in other parts of Central America, differences in bird-feeding guilds, and similarity of bird communities among the different land-use types. Further, we discuss several caveats in our interpretation due to aspects of the ASP study design and our bird survey methods. 0 200 400 600 The mean bird detections per point in our study were No. of individuals (c) similar to previous studies in natural succession and restoration areas of Central America (Petit et al. 1999; Reid et al. 2012). The shift from dominance by understory insectivores and omnivores in mature forest to scrub gran- ivores in more open habitats is similar to previous descrip- tions for bird communities in Central America (Petit et al. 1999; Milder et al. 2010; Karp et al. 2011). In general, birds were very sparse in the reforestation habitat. These sites lacked foliage and canopy cover, resulting in greater exposure to high temperature and low humidity, a lack of perching structures, and greater exposure to predators. The 0 20 40 60 bird communities in the reforestation area were dominated No. of samples by 2–3 bird species that are adapted to grassy, edge, or meadow-like habitats (Table 4). We observed these birds Figure 2. Species richness curves and estimators for birds in various landscapes in Central Panama. Species rarefaction curves using the young reforestation trees as perches from which are scaled by (a) sample and (b) number of individual birds they foraged on seeds and insects associated with the grass counted. (c) The Chao1 species richness estimator scaled by growing between the trees. Similar results of low-bird number of samples. For all panels, error bars represent 95% of counts were observed in agricultural situations relative to confidence intervals and closed circles = mature forest, open circles = natural succession, closed triangles = cattle pasture, forests or shaded plantations (Petit et al. 1999; Estrada & and open triangles = native species reforestation. Estrada-Coates 2005). Table 2. Cumulative numbers of species observed and estimated number of species present in each land use, using point count data only from the Agua Salud Ecosystem Services Project in Central Panama. No. of spp. observed Chao1 estimated no. of spp. No of individual No. spp. Land use N points birds value 95 low 95 high value 95 low 95 high observed/sample Mature forest 120 580 91 77 105 116 100 157 1.52 Natural succession 120 660 98 83 113 131 111 179 1.63 Cattle pasture 120 442 73 59 86 86 77 110 1.22 Reforestation native 120 158 21 12 29 30 23 59 0.35 Estimated number of species (chao1) No. of species No. of species 286 S.A. Van Bael et al. Table 3. Similarity of species composition for total bird com- 0.2 munities based on the Bray–Curtis index of similarity, among all pairs of habitats sampled in Central Panama. 0.1 Mature Natural Cattle forest succession pasture Reforestation Mature 1* * * 0.0 forest Natural 0.34 1 * * succession –0.1 Cattle 0.07 0.21 1 * pasture Reforestation 0.05 0.05 0.24 1 –0.2 The cattle pasture sites in our study had intermediate levels of bird abundances relative to the other habitat types –0.2 –0.1 0.0 0.1 0.2 (Table 1). The pastures in our study had both isolated trees NMDS axis 1 within pastures as well as live fences, both of which were Figure 3. NMDS ordination plot using the Bray–Curtis index to used heavily by birds. Previous studies have also docu- show similarity among habitats, with 95% confidence ellipses. mented high bird use of isolated remnant trees (Guevara Each point represents the bird community species composition at et al. 1986) and live fences in cattle pastures (Estrada et al. one count point, summed over the different counts. Habitat labels 2000; Estrada & Coates-Estrada 2005; Harvey et al. 2006). are: mature forest = crosses, natural succession = open squares, reforestation = open circles, cattle pasture = filled triangles. Live fences are increasingly being recommended as a management tool for increasing connectivity in agricul- tural landscapes (Leon & Harvey 2006). in shaded coffee and cacao farms. For example, in our The high abundance and species richness of birds in mature forest and natural succession areas, the mean secondary or successional areas has been documented in number of bird detections per point was ~5± 0.5 many studies (Karr 1976; Martin 1985; Petit & Petit (Figure 1b), while studies in these agrosystems have 2003), supporting the hypothesis that intermediate levels found a relatively greater mean bird detections per point, of disturbance lead to high-species richness (Connell with mean values closer to ~8 birds per point (Petit et al. 1978). A similar type of intermediate habitat between 1999; Reitsma et al. 2001; Van Bael et al. 2007). The forests and pastures occurs in agroforestry systems. The increase in bird abundance in these shaded agroforestry bird abundances observed in our study, however, are lower systems is also represented by high abundances of than other studies that have measured abundances of birds migratory bird species, with mean values of ~1 bird per Table 4. Most abundant bird species in each land-use type at the Agua Salud Ecosystem Services project in Central Panama, primary foraging substrate, diet and habitat affinity. Percentage of No. all Substrate/ Habitat 1,2 3 Land-use rank Common name Scientific name individuals observations Diet affinity Mature forest (n = 571 individuals) 1 Western Slaty-antshrike Thamnophilus atrinucha 36 6.3 U/CI WG 2 Southern Bentbill Oncostoma olivaceum 34 6.0 U/I WG 3 White-flanked Antwren Myrmotherula axillaris 32 5.6 U/I FS Natural succession (n = 658 individuals) 1 Red-throated Ant-tanager Habia fuscicauda 45 6.8 U/FI WG 2 Red-legged Honeycreeper Cyanerpes cyaneus 40 6.1 C/FIN AG 3 Black-bellied Wren Thryothorus fasciatoventris 36 5.5 U/I WG Pasture (n = 423 individuals) 1 Lesser Elaenia Elaenia chiriquensis 34 8.0 C/FI AG 2 Yellow-faced Grassquit Tiaris olivaceus 32 7.6 SC/FGI AG 3 Blue-headed Parrot Pionus menstruus 31 7.3 C/FG WG Reforestation native species (n = 77 individuals) 1 Blue-black Grassquit Volatinia jacarina 18 23.4 SC/FGI AG 2 Lesser Elaenia Elaenia chiriquensis 13 16.9 C/FI AG 3 Yellow-faced Grassquit Tiaris olivaceus 13 16.9 SC/FGI AG 1 2 Codes for Foraging substrate: C = canopy, U = understory, SC = scrub, ST = streams. Codes for diet: C = carnivore, F = frugivore, G = gramnivore, I = insectivore, N = nectarivore. Habitat affinity: FS = forest specialist, WG = woodland generalist, AG = agricultural generalist, inferred from information in Ridgely and Gwynne (1989). NMDS axis 2 International Journal of Biodiversity Science, Ecosystem Services & Management 287 point in shaded cacao (Van Bael et al. 2007) and 0.6 birds vegetation in the cattle pasture or reforestation sites. If per point in shaded coffee (Petit et al. 1999). These values we had, the bird abundances and diversities would for migratory species are equal to or greater than any of undoubtedly have been higher. A companion study at the the landscapes in our study (Figure 1c), emphasizing the ASP will focus exclusively on comparing the stream-asso- importance of shaded agroforestry systems for migratory ciated birds in the human-modified and forested land- bird species (Greenberg et al. 1994; Wunderle & Latta scapes (G. Toral and S. Van Bael, in prep.) 1996; Greenberg et al. 1997; Van Bael et al. 2007). In general, the effects of human-mediated reforestation Our measurements of species richness are likely under- on bird communities are not well known. For conservation estimated. The bird community in one of our transect areas purposes, it is important to know how human-mediated Soberania National Park (bordering the Limbo River) has restoration efforts compare with natural succession. We been very well studied (Robinson et al. 2000). We com- show that bird abundances and species diversity remain pared our species number from the complete list to very low in tree plantations within 1–2 years of planting, Robinson et al. (2000) and found that we counted 74% and that the birds using reforestation areas are very similar of the number of species reported in their study, which was to bird communities in active cattle pastures. This work much more extensive in terms of time and types of survey provides a baseline to compare subsequent periods, test methods. Looking solely at migratory birds, in our list the our predictions for future development of bird commu- total species number was only 54% of the number of nities in reforestation sites, and thereby assess the speed species reported in Robinson et al. (2000). These compar- at which reforestation efforts with tree plantations will isons, as well as the fact that our rarefied species accumu- support a more diverse and abundant bird community. lation curves did not plateau, suggest that future surveys Such information will be useful for land managers who will identify more species in these areas. are trying to balance economic sustainability with biodi- The proximity of a reforestation site to mature forest versity management, as well as for aiding ecosystem ser- was an important factor in our study, even when the vice evaluation of different land management schemes. plantation trees were very small. Birds that use the edges of mature forest may be more likely to venture out into the Supplementary material ‘open’ setting of the new plantation, as our study showed a greater abundance and number of species near the forest. Supplementary Table S1 is available online. Graham and Blake (2001) found that proximity to contin- uous forest was the most influential element for separating Acknowledgements bird communities in a mixed agricultural and forested The authors thank Charles Perrings, Ann Kinzig, Michiel van landscape in Southern Mexico. Breugel, Federico Davis, Daniela Weber, Raineldo Urriola, In our study there are some important factors to Argelis Ruiz for help with planning, facilities, and logistics. For address regarding comparability among the habitat types. help in the field, they thank Andrea Concepcion, Robert Rich, These factors include (1) bird detection differences among Jack Hruksa, Isis Ochoa, and Katherine Arauz. The authors also the habitats, (2) differences in age since previous land use thank the Smithsonian Tropical Research Institute, Arizona State University initiative, the Ruth Povo Foundation, and an anon- and (3) differences in treatment methodology. Not surpris- ymous donor for funding. ingly, the best-fit detection function types were different in mature forest relative to the other habitat types. In mature forest, bird detections decreased with distance from the References observer, while the other habitat types showed a uniform Bray JR, Curtis JT. 1957. An ordination of the upland forest com- detection probability across our point count fixed radius. munities of southern Wisconsin. Ecol Monogr. 27:325–349. This resulted in relatively higher abundance estimates for Chao A. 2005. Species richness estimation. Encyclopedia Stat mature forest when the distance correction was used com- Sci. 12:7907–7916. Chazdon RL, Peres CA, Dent D, Sheil D, Lugo AE, Lamb D, Stork pared to mean detections per point (Figure 1a vs. 1b). With NE, Miller SE. 2009. The potential for species conservation in respect to age, native species reforestation trees had been tropical secondary forests. 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Neotrop. 7:19–34. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png International Journal of Biodiversity Science, Ecosystem Services & Management Taylor & Francis

Bird communities in forested and human-modified landscapes of Central Panama: a baseline survey for a native species reforestation treatment

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10.1080/21513732.2013.842187
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International Journal of Biodiversity Science, Ecosystem Services & Management, 2013 Vol. 9, No. 4, 281–289, http://dx.doi.org/10.1080/21513732.2013.842187 Bird communities in forested and human-modified landscapes of Central Panama: a baseline survey for a native species reforestation treatment a,b b b Sunshine A. Van Bael *, Ruby Zambrano and Jefferson S. Hall a b Department of Ecology and Evolutionary Biology, Tulane University, 400 Lindy Boggs, New Orleans, LA 70118, USA; Smithsonian Tropical Research Institute, Apartado 0843–03092, Balboa, Ancon, Panama, Republic of Panama While deforestation continues to be a threat to species diversity in the tropics, reforestation either by natural succession or human tree planting is also occurring. Very little is known about how bird communities respond to human-mediated reforestation schemes in tropical areas. We surveyed bird communities in Central Panama to compare their abundance and richness in mature forest, young natural succession (fallow pastures), active cattle pastures, and native species reforestation areas. We found the greatest abundance of birds in mature forest, while natural succession areas had slightly greater species richness relative to mature forest. Bird communities were most similar in forest and natural succession areas, and were distinct from bird communities in cattle pastures and reforestation areas. Migratory bird species were most abundant in the young natural succession areas. Reforestation areas that were closer to mature forest had a greater abundance of birds relative to areas further from forests. Our study provides a baseline for future studies at this site that will allow assessment of the speed at which reforestation efforts with tree plantations will support a more diverse and abundant bird community. Moreover, our finding of the greatest species richness and migratory bird abundance in a natural succession habitat supports previous bird community studies in agroforestry and successional habitats. Keywords: agroecosystem; biodiversity; canopy; feeding guilds; migratory birds; restoration; species richness; succession; tropical birds Introduction scrub species (Petit et al. 1999; Petit & Petit 2003). At the same time that deforestation is occurring, other parts of Many species are suffering declines in their population Panama are being reforested either by natural succession numbers, with habitat loss due to land-use change cited as or by establishment of tree plantations (Wright & Muller- the major cause (Millenium Ecosystem Assessement 2005). Landau 2006; Wright & Samaniego 2008; Hall et al. 2011; Since >90% of the land area in tropical areas occurs outside van Breugel et al. 2011). Very little is known about how the boundaries of forest reserves, planning for conservation bird communities are responding to various types of will require a better understanding of the value of human- reforestation schemes in Panama, although recent work in modified landscapes for supporting biological diversity Costa Rica has shown that some migratory birds preferred (Chazdon et al. 2009). Birds are often used to assess or plantation-style reforestation treatments (Lindell et al. 2011) predict the effects of land-use change (Hughes et al. 2002; and that overall bird community composition and species Petit & Petit 2003;Harvey etal. 2006), because they are richness was similar in actively and passively restored easy to observe and provide important ecosystem services patches (Reid et al. 2012). (Sekercioglu 2006; Whelan et al. 2008). Moreover, many In Central Panama, many forests have been protected birds have diverse and specialized requirements for food, along the banks of the Panama Canal (Ibáñez et al. 2002). which makes them good indicators for habitat change. A Despite this, approximately half of the canal’s watershed is variety of types of agricultural development have reduced deforested, and reforestation of the watershed is the official forest cover and thereby decreased the abundance and policy (Law 21) of Panama Canal Authority (ACP). Since diversity of bird species relative to forest habitats in the 2009, the Agua Salud Project (ASP), an ecosystem services Neotropics (Petit et al. 1999;Estrada &Coates-Estrada project in the Panama Canal Watershed, has begun to 2005; Faria et al. 2006;Harvey et al. 2006; Scales et al. investigate the effects of different types of reforestation 2008;Milder etal. 2010) as well as the Paleotropics efforts and land uses on hydrology, carbon storage, and (Waltert et al. 2004, 2005; Marsden & Symes 2008; species conservation (Stallard et al. 2010). Due to the Scales et al. 2008). Like other countries in Central America, Panama has large quantities of data being collected on the environment increasingly become fragmented due to forest clearing for and the 25–40-year project horizon, the ASP offers a cattle pastures and subsistence agriculture (Kaimowitz unique opportunity to monitor changes in bird communities 1996). The result of forest clearing or human modification among different landscape types in Central Panama. is a simplification of bird communities and a shift toward Here, we present data from bird surveys conducted communities comprising of open woodland, grassland, and between 2010 and 2011 within the treatment sites of the *Corresponding author. Email: svanbael@tulane.edu © 2013 Taylor & Francis 282 S.A. Van Bael et al. ASP. We surveyed bird communities in mature forest, contained large streams or rivers, as in mature forest. natural succession areas, cattle pastures, and a newly These transects were situated approximately 1.5 km from installed reforestation site. Our overall hypothesis is that the edge of Soberania National Forest. In our transect human plantation efforts can eventually mimic natural areas, canopy cover averaged 51%, with tree heights succession for providing bird habitat. We predict that (1) ranging from 4 to 8 m. bird communities in newly planted reforestation areas will most resemble bird communities in cattle pastures, and (2) Pasture when a canopy forms in the reforestation area, the bird communities in reforestation areas will resemble those of Two transects were in active cattle pasture either within or natural succession areas. This paper provides data to test near the ASP principle area. Both pastures had a small the first prediction. Our specific goals in surveying the river running through the center with gallery forest, and bird communities were to estimate and compare the abun- each had isolated, large, remnant trees in them. Each area dance, species richness, and species composition of birds of pasture included ~40 ha and the surrounding matrix of using the four habitat types at the baseline, when refores- land uses included young naturally regenerating secondary tation sites were first planted. We also wanted to assess forest (rastrojo) and other pastures. Cattle were grazed at whether distance from the forest edge affected bird abun- the intensity of ~1.3 heads/ha. These transects were situ- dances within the newly planted reforestation site. ated approximately 2–3 km from the edge of Soberania National Forest. Canopy cover was approximately 16% in our transect areas, with all cover coming from 20 to 25 m Methods tall remnant trees. Study sites We received permission for our observational field study Reforestation with native species from the Panama’s National Authority for the Two transects were set up in two distinct areas where Environment (ANAM) and the Panama Canal Authority reforestation with native species was occurring with the (ACP). The principle study site of the ASP borders ASP site. All land was cleared completely before planting Soberania National Park in Central Panama (9°13′ N, to homogenize the light environment, a requirement for the 79°47′W). Following is a description of each habitat type experimental design of the plantations that would not where we conducted bird surveys in 2010–11. Our survey necessarily be followed to this extreme in a production areas could not be placed randomly in the landscape due to plantation. Its previous use included active cattle pasture the constraint that we had permission to work only in and and young regenerating secondary forest (<5-years old). alongside ASP-owned areas. Further floristic details about The reforestation treatments in 2008 included 75 ha of these sites and representative photographs and maps are at land area where five native timber species (Anacardium http://www.ctfs.si.edu/aguasalud/page/catchments/#forest. excelsum, Dalbergia retusa, Pachira quinata, Tabebuia rosea, and Terminalia amazonia) and five companion Mature forest native species (Erytrina fusca, Gliricidia sepium, Inga punctata, Luehea seemannii, and Ochroma pyramidale) Two transects were established in forested areas of were planted either as a monoculture or as polycultural Soberania National Park (22,000 ha total). One transect mixes. The bird survey transects were not situated with was accessed from Pipeline Road near the Limbo River, respect to particular plots of monoculture or polycultural in an area where previous studies have described the avi- treatments, but rather covered a much larger area that fauna (Robinson et al. 2000). A second transect was encompassed many treatments (each reforestation treatment accessed from the ASP. Neither site included large streams plot was 45 × 39 m). At the time of the 2010 survey, most or rivers within 30 m of our bird count points. The forest in plantation trees were ~1–2 m in height. There was no Soberania is a mix of mature second growth and old growth canopy cover above the transects with native species refor- forest, both of which were represented in our transects (one estation. The grassy vegetation between trees was cleared each). Canopy cover was approximately 96% in our mature four times a year since planting. One reforestation area was forest transect areas, with canopy heights ranging from 23 directly adjacent to Soberania National Forest while another to 28 m (see vegetation survey methods below). was ~2 km away from the forest edge. Natural succession Bird and vegetation survey methods Two transects were in natural succession within the prin- ciple ASP area. These sites were abandoned pasture In order to compare bird species richness and abundance, (approximately, 5–6 years previously) and reforestation we sampled 80 points across the various land uses was occurring via natural regeneration. Another term for described above. The sample points fell along transects this type of habitat is rastrojo. The area contained trees within each habitat type (see sample sizes in Table 1). that were about 4 m high, but taller, remnant trees from Within transects, each point was separated by >100 m cattle pastures or live fences were also present. Neither site and at least 50 m from the edge of a particular habitat. International Journal of Biodiversity Science, Ecosystem Services & Management 283 Table 1. Density estimates (number of birds per ha, D) and the concave densiometer at the center of the bird count point. corresponding coefficients of variation (CV) and 95% confidence For canopy and emergent tree heights, we used a digital intervals (CI95) generated by the program DISTANCE based on rangefinder to improve our estimates. These vegetation mea- the number of bird detections (n). surements were not taken in the reforestation treatments Density because no canopy existed. Further, due to constraints, our estimate Percentage vegetation sampling was not complete across all bird count Land use n (no/ha) CV CI points, but at least 10 points per habitat type were sampled. Mature forest 571 57.8 1.06 56.6–59.0 Natural 658 15.9 16.94 10.7–20.7 Statistical analyses succession Reforestation 77 0.596 0.39 0.590–0.600 We used the program DISTANCE 6.0 (Thomas et al. Cattle pasture 423 11.47 17.04 8.22–16.00 2010) to estimate and compare the bird density among the four habitat types, pooled over all 480 counts. We fit at least six detection functions per habitat and used AIC model selection to choose the best-fit models. These were In particular, if a stream or river ran through our land-use a half-normal model with a hermite polynomial expan- type, we consistently set up our bird counts to avoid the sion for mature forest, and a uniform model with cosine stream-associated vegetation. We used a hand-held GPS to polynomial expansion for all other habitat types. The set up the points and confirm distances. detection functions allowed an estimation of bird density For this study, we define a transect as a collection of (number of birds per hectare) in each of the four habitat 10 sample points, and a survey as one of the three distinct types. We compared 95% confidence intervals to assess time periods when transects were walked and points were differences in bird density. The DISTANCE program visited. All 80 points were visited twice within a survey, requires a minimum of 60–100 observations within a with at least 5 days between visits. The first survey category to give reliable estimates, so we did not do occurred during the dry season, in January and February this analysis for migratory birds. While DISTANCE is of 2010. The second survey happened in June and July often used to estimate detection probabilities and density 2010, during the wet season. The final survey occurred estimates for individual bird species, we did not pursue during the dry season in January and February of 2011. this approach since only two bird species in our dataset Since there were three surveys, each sample point was had more than 60 individuals. In addition to the visited a total of six times during the study for a total of DISTANCE bird density estimates, we calculated the 480 bird count samples. mean number of bird detections in different landscape At the sample points, we counted birds using 10-min- types based on count data with no distance corrections, ute fixed radius point counts (25 m radius) to record all so that our results could be compared to previous studies. visual and aural signs of birds. The point-count method is This also gives a relative abundance of birds in habitats best suited for obtaining a broad sample of bird commu- with similar detection probabilities. To compare bird nities across a patchy landscape (Petit et al. 1995). abundances in reforestation areas that were close and far Moreover, limiting our counts to a 25-m radius increased from the forest edge, we relied on bird detections per the detectability of birds across the different landscape point, as detection likelihood was similar in the same types (Petit et al. 1995) and decreased the likelihood of type of habitat. We used a two-tailed t-test to compare counting the same birds from one point to the next. We the abundance of birds in reforestation areas near and far surveyed for 10 minutes to improve the quality of our raw from the forest edge. To further describe the bird com- count data in terms of detectability (Etterson et al. 2009). munity, we used the point count data to list the three most During the hours of 6:00–10:00 am, on non-rainy days, abundant species per habitat, and classify the species one observer (RZ) was responsible for conducting the using diet and habitat information from Ridgely and visual and aural surveys. For each bird detected, the Gwynne (1989). observer estimated and recorded the radial distance from We used both point count data and our cumulative list herself to the individual bird. An assistant, who made of birds to report the total number of species observed in digital audio recordings during each point count, accom- each habitat. With the point count data only, we used panied the observer. We did not count birds that were EstimateS (2010) to construct sample-based rarefaction flying over the count circle. Along with point count data, (or species accumulation) curves for comparison of spe- we kept an ongoing list of additional sightings outside of cies richness among the habitats, scaling the curves to the points as we walked the transects. On most days we number of individuals and the number of samples (Gotelli completed one transect (or 10 sample points). & Colwell 2001; Colwell et al. 2004). Since our curves did To compare canopy characteristics among land-use not reach asymptotes, we also used an asymptotic species types, we rapidly estimated canopy cover, average canopy richness estimator for species abundance data, Chao1, to height, and the height of the tallest emergent tree in our 25 m represent species estimations in each land-use type (Chao radius sample circle. To estimate the canopy cover, we took 2005). For these analyses we used data from point counts four readings (facing N, S, E, and W) with a hand-held in all of the surveys combined. 284 S.A. Van Bael et al. We also wanted to compare the species community (a) composition among the habitats using point count data. We followed the techniques outlined in Clarke (1993), which include calculating the Bray–Curtis index of similarity (Bray & Curtis 1957), followed by non-metric multidimen- sional scaling (NMDS) and analysis of similarity (ANOSIM). These analyses were all completed using the program PAST (Hammer et al. 2001). The community composition analyses compared the bird communities among sample points, with the bird species identities summed up over all surveys at each point. We also calculated 6 (b) an overall Bray–Curtis similarity value to numerically com- pare between the sites. Results Data from complete bird list We recorded 225 bird species in our complete list, which combined fixed radius point counts and additional obser- vations between points (Table S1). We recorded 109 spe- (c) cies that occurred in mature forests only, and 143 species 0.6 in natural succession. In cattle pasture and reforestation areas, we recorded 97 and 61 species, respectively for our 0.4 complete list. Across all land-use types, we recorded 26 migratory bird species in our complete list (Table S1). 0.2 Data from point counts 0.0 MF NS C R We counted 1729 individual birds in fixed radius point Land-use type counts. Using distance corrections, bird density estimates were significantly different in the four land uses, with the Figure 1. Abundance estimates for birds in various landscapes of Central Panama. (a) Density estimates and 95% confidence greatest density estimate in mature forest, then natural suc- intervals (error bars) for birds (no. of birds per hectare) using cession (Figure 1a, Table 1). Bird density estimates in natural distance corrections. (b) Mean detections (or no. of birds) per succession had overlapping confidence intervals with esti- point count survey for all bird species, error bars are one standard mates from cattle pastures, although the overall estimate was error. (c) Mean detections (or no. of birds per point count survey greater in natural succession areas. Reforestation areas had for migratory birds only, error bars are one standard error. For all very low bird density estimates (Table 1). When using the panes, MF = mature forest, NS = natural succession, C = cattle pasture, R = reforestation with native species. number of birds per point (or mean detections per point), we observed similar values in mature forest and natural succes- sion (Figure 1b). Relative to these two habitats, we observed R = 0.8301, p < 0.001). The low similarity between com- lower mean detection values for birds in cattle pasture and munities in forested and non-forested landscapes is also reforestation habitats (Figure 1b). In contrast, detection apparent when comparing the most abundant species of values for migratory bird species were greatest in natural each habitat (Table 4). The mature forest was dominated succession and similarly low in the other habitats (Figure 1c). by forest specialists and woodland generalists, while the The accumulation of species occurred most rapidly other habitats were dominated by woodland and agricul- during surveys in natural succession and mature forest tural generalists (Table 4). The primary bird species in the (Figure 2). The curves demonstrate the high species rich- reforestation areas were those that foraged in open, scrub ness observed and estimated for natural succession, forest, habitats with seed-eating birds highly represented (Table 4). and pasture, which differed from the reforestation area Distance to the mature forest edge had an effect on bird where abundances and species diversity estimates were abundance and species richness in the reforestation areas. relatively low (Table 2). The NMDS comparison of species Using data from point counts at these two transects only, we found that the site adjacent to the forest had a significantly similarity composition, however, suggests that species higher mean bird detections per point (mean ± 1 s.e. was composition was more similar between mature forest and 1.48 ± 0.10 for adjacent and 1.15 ± 0.10 for far transect; natural succession, while cattle pasture bird communities t = 2.339, d.f. = 18, P = 0.031 (two-tailed)). The number of were more similar to those in the reforestation treatments species observed in each transect were 17 and 8 for adjacent (Table 3, Figure 3). Among all habitats, the bird community and far transects, respectively. Abundances in this habitat compositions were significantly different (ANOSIM No. of migratory birds/point No. of birds/point Estimated birds/hectare International Journal of Biodiversity Science, Ecosystem Services & Management 285 (a) were very low in general, and most sample points (81/120 or 68% of the points) had zero birds. MF According to the IUCN Red List, nearly all of the NS species we observed were in the category of Least 80 C Concern for their conservation status. The only exceptions were two species in the Near Threatened category. These were Harpia harpyja (Harpy Eagle, observed in mature forest, known to be a reintroduction in the area) and Vermivora chrysoptera (Golden-winged Warbler, observed in natural succession). 0 20 40 60 Discussion No. of samples (b) Our study recorded the greatest abundance and species rich- ness of birds in mature forest and natural succession habitats. Cattle pastures and the early stages of tree plantations sup- ported fewer bird species and had more similar species composition. We discuss these results with respect to differ- ences in bird abundances in other parts of Central America, differences in bird-feeding guilds, and similarity of bird communities among the different land-use types. Further, we discuss several caveats in our interpretation due to aspects of the ASP study design and our bird survey methods. 0 200 400 600 The mean bird detections per point in our study were No. of individuals (c) similar to previous studies in natural succession and restoration areas of Central America (Petit et al. 1999; Reid et al. 2012). The shift from dominance by understory insectivores and omnivores in mature forest to scrub gran- ivores in more open habitats is similar to previous descrip- tions for bird communities in Central America (Petit et al. 1999; Milder et al. 2010; Karp et al. 2011). In general, birds were very sparse in the reforestation habitat. These sites lacked foliage and canopy cover, resulting in greater exposure to high temperature and low humidity, a lack of perching structures, and greater exposure to predators. The 0 20 40 60 bird communities in the reforestation area were dominated No. of samples by 2–3 bird species that are adapted to grassy, edge, or meadow-like habitats (Table 4). We observed these birds Figure 2. Species richness curves and estimators for birds in various landscapes in Central Panama. Species rarefaction curves using the young reforestation trees as perches from which are scaled by (a) sample and (b) number of individual birds they foraged on seeds and insects associated with the grass counted. (c) The Chao1 species richness estimator scaled by growing between the trees. Similar results of low-bird number of samples. For all panels, error bars represent 95% of counts were observed in agricultural situations relative to confidence intervals and closed circles = mature forest, open circles = natural succession, closed triangles = cattle pasture, forests or shaded plantations (Petit et al. 1999; Estrada & and open triangles = native species reforestation. Estrada-Coates 2005). Table 2. Cumulative numbers of species observed and estimated number of species present in each land use, using point count data only from the Agua Salud Ecosystem Services Project in Central Panama. No. of spp. observed Chao1 estimated no. of spp. No of individual No. spp. Land use N points birds value 95 low 95 high value 95 low 95 high observed/sample Mature forest 120 580 91 77 105 116 100 157 1.52 Natural succession 120 660 98 83 113 131 111 179 1.63 Cattle pasture 120 442 73 59 86 86 77 110 1.22 Reforestation native 120 158 21 12 29 30 23 59 0.35 Estimated number of species (chao1) No. of species No. of species 286 S.A. Van Bael et al. Table 3. Similarity of species composition for total bird com- 0.2 munities based on the Bray–Curtis index of similarity, among all pairs of habitats sampled in Central Panama. 0.1 Mature Natural Cattle forest succession pasture Reforestation Mature 1* * * 0.0 forest Natural 0.34 1 * * succession –0.1 Cattle 0.07 0.21 1 * pasture Reforestation 0.05 0.05 0.24 1 –0.2 The cattle pasture sites in our study had intermediate levels of bird abundances relative to the other habitat types –0.2 –0.1 0.0 0.1 0.2 (Table 1). The pastures in our study had both isolated trees NMDS axis 1 within pastures as well as live fences, both of which were Figure 3. NMDS ordination plot using the Bray–Curtis index to used heavily by birds. Previous studies have also docu- show similarity among habitats, with 95% confidence ellipses. mented high bird use of isolated remnant trees (Guevara Each point represents the bird community species composition at et al. 1986) and live fences in cattle pastures (Estrada et al. one count point, summed over the different counts. Habitat labels 2000; Estrada & Coates-Estrada 2005; Harvey et al. 2006). are: mature forest = crosses, natural succession = open squares, reforestation = open circles, cattle pasture = filled triangles. Live fences are increasingly being recommended as a management tool for increasing connectivity in agricul- tural landscapes (Leon & Harvey 2006). in shaded coffee and cacao farms. For example, in our The high abundance and species richness of birds in mature forest and natural succession areas, the mean secondary or successional areas has been documented in number of bird detections per point was ~5± 0.5 many studies (Karr 1976; Martin 1985; Petit & Petit (Figure 1b), while studies in these agrosystems have 2003), supporting the hypothesis that intermediate levels found a relatively greater mean bird detections per point, of disturbance lead to high-species richness (Connell with mean values closer to ~8 birds per point (Petit et al. 1978). A similar type of intermediate habitat between 1999; Reitsma et al. 2001; Van Bael et al. 2007). The forests and pastures occurs in agroforestry systems. The increase in bird abundance in these shaded agroforestry bird abundances observed in our study, however, are lower systems is also represented by high abundances of than other studies that have measured abundances of birds migratory bird species, with mean values of ~1 bird per Table 4. Most abundant bird species in each land-use type at the Agua Salud Ecosystem Services project in Central Panama, primary foraging substrate, diet and habitat affinity. Percentage of No. all Substrate/ Habitat 1,2 3 Land-use rank Common name Scientific name individuals observations Diet affinity Mature forest (n = 571 individuals) 1 Western Slaty-antshrike Thamnophilus atrinucha 36 6.3 U/CI WG 2 Southern Bentbill Oncostoma olivaceum 34 6.0 U/I WG 3 White-flanked Antwren Myrmotherula axillaris 32 5.6 U/I FS Natural succession (n = 658 individuals) 1 Red-throated Ant-tanager Habia fuscicauda 45 6.8 U/FI WG 2 Red-legged Honeycreeper Cyanerpes cyaneus 40 6.1 C/FIN AG 3 Black-bellied Wren Thryothorus fasciatoventris 36 5.5 U/I WG Pasture (n = 423 individuals) 1 Lesser Elaenia Elaenia chiriquensis 34 8.0 C/FI AG 2 Yellow-faced Grassquit Tiaris olivaceus 32 7.6 SC/FGI AG 3 Blue-headed Parrot Pionus menstruus 31 7.3 C/FG WG Reforestation native species (n = 77 individuals) 1 Blue-black Grassquit Volatinia jacarina 18 23.4 SC/FGI AG 2 Lesser Elaenia Elaenia chiriquensis 13 16.9 C/FI AG 3 Yellow-faced Grassquit Tiaris olivaceus 13 16.9 SC/FGI AG 1 2 Codes for Foraging substrate: C = canopy, U = understory, SC = scrub, ST = streams. Codes for diet: C = carnivore, F = frugivore, G = gramnivore, I = insectivore, N = nectarivore. Habitat affinity: FS = forest specialist, WG = woodland generalist, AG = agricultural generalist, inferred from information in Ridgely and Gwynne (1989). NMDS axis 2 International Journal of Biodiversity Science, Ecosystem Services & Management 287 point in shaded cacao (Van Bael et al. 2007) and 0.6 birds vegetation in the cattle pasture or reforestation sites. If per point in shaded coffee (Petit et al. 1999). These values we had, the bird abundances and diversities would for migratory species are equal to or greater than any of undoubtedly have been higher. A companion study at the the landscapes in our study (Figure 1c), emphasizing the ASP will focus exclusively on comparing the stream-asso- importance of shaded agroforestry systems for migratory ciated birds in the human-modified and forested land- bird species (Greenberg et al. 1994; Wunderle & Latta scapes (G. Toral and S. Van Bael, in prep.) 1996; Greenberg et al. 1997; Van Bael et al. 2007). In general, the effects of human-mediated reforestation Our measurements of species richness are likely under- on bird communities are not well known. For conservation estimated. The bird community in one of our transect areas purposes, it is important to know how human-mediated Soberania National Park (bordering the Limbo River) has restoration efforts compare with natural succession. We been very well studied (Robinson et al. 2000). We com- show that bird abundances and species diversity remain pared our species number from the complete list to very low in tree plantations within 1–2 years of planting, Robinson et al. (2000) and found that we counted 74% and that the birds using reforestation areas are very similar of the number of species reported in their study, which was to bird communities in active cattle pastures. This work much more extensive in terms of time and types of survey provides a baseline to compare subsequent periods, test methods. Looking solely at migratory birds, in our list the our predictions for future development of bird commu- total species number was only 54% of the number of nities in reforestation sites, and thereby assess the speed species reported in Robinson et al. (2000). These compar- at which reforestation efforts with tree plantations will isons, as well as the fact that our rarefied species accumu- support a more diverse and abundant bird community. lation curves did not plateau, suggest that future surveys Such information will be useful for land managers who will identify more species in these areas. are trying to balance economic sustainability with biodi- The proximity of a reforestation site to mature forest versity management, as well as for aiding ecosystem ser- was an important factor in our study, even when the vice evaluation of different land management schemes. plantation trees were very small. Birds that use the edges of mature forest may be more likely to venture out into the Supplementary material ‘open’ setting of the new plantation, as our study showed a greater abundance and number of species near the forest. Supplementary Table S1 is available online. Graham and Blake (2001) found that proximity to contin- uous forest was the most influential element for separating Acknowledgements bird communities in a mixed agricultural and forested The authors thank Charles Perrings, Ann Kinzig, Michiel van landscape in Southern Mexico. Breugel, Federico Davis, Daniela Weber, Raineldo Urriola, In our study there are some important factors to Argelis Ruiz for help with planning, facilities, and logistics. For address regarding comparability among the habitat types. help in the field, they thank Andrea Concepcion, Robert Rich, These factors include (1) bird detection differences among Jack Hruksa, Isis Ochoa, and Katherine Arauz. The authors also the habitats, (2) differences in age since previous land use thank the Smithsonian Tropical Research Institute, Arizona State University initiative, the Ruth Povo Foundation, and an anon- and (3) differences in treatment methodology. 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Journal

International Journal of Biodiversity Science, Ecosystem Services & Management – Taylor & Francis

Published: Dec 1, 2013

Keywords: agroecosystem; biodiversity; canopy; feeding guilds; migratory birds; restoration; species richness; succession; tropical birds

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