On-line version ISSN 0718-1620
Cienc. Inv. Agr. vol.37 no.1 Santiago Apr. 2010
Cien. Inv. Agr. 37(1):29-43. 2010
Diversity and singularity of the avifauna in the austral peat bogs of the Cape Horn Biosphere Reserve, Chile
Diversidad y singularidad de la avifauna en turberas esfagnosas australes de la Reserva de Biosfera Cabo de Hornos, Chile
José Tomás Ibarra1 2, Christopher B. Anderson2, Tomás A. Altamirano1, Ricardo Rozzi2 3, and Cristián Bonacic1
1Laboratorio Fauna Australis, Facultad de Agronomía e Ingeniería Forestal, Pontifcia Universidad Católica de Chile, Casilla 306-22, Santiago, Chile.
2Parque Etnobotánico Omora (Instituto de Ecología y Biodiversidad, Universidad de Magallanes), Reserva de Biosfera Cabo de Hornos, Puerto Williams, Chile.
3Department of Philosophy and Religion Studies, University of North Texas, Denton, Texas, USA.
Sphagnum-dominated peat bogs that are strongly embedded within the southern temperate forest matrix are increasingly being used for agriculture. Nevertheless, little is known about their biodiversity. Moreover, the remote areas of southern Chile where peat bogs are found, such as the Cape Horn Biosphere Reserve (CHBR, 54-55ºS), where birds are the most diverse and best represented group of vertebrates, have not been well-investigated. With the aim to broaden this knowledge in the CHBR, we studied the diversity of the avian assemblage in peat bogs on Navarino Island. We compared the composition of avian species between wetlands with and without peat bogs to test if Sphagnum bogs represented a singular habitat for birds in this area. Furthermore, the 37 bird species recorded in these habitats were classifed according to guild structure. The community similarity values showed that peat bogs hosted a bird composition that was different from that present in wetlands without Sphagnum, suggesting that peat bogs are a singular type of habitat for birds in the CHBR. The most frequently feeding groups recorded in these wetlands were insectivores (48.7%), followed by omnivores (23.1%). Our results showed that, in contrast to previous studies of birds in peat bogs, these environments constituted a distinct wetland habitat for feeding, reproduction and sheltering for some species in the CHBR. Thus, plans for the conservation and rational use of peat ecosystems should consider the high value of these habitats for biodiversity on a landscape scale, especially for birds of the southernmost extreme of the Americas.
Key words: Assemblage, Cape Horn Biosphere Reserve, Navarino Island, Patagonia, Sphagnum spp., wetlands.
Las turberas esfagnosas que se encuentran fuertemente embebidas en la matriz de bosques templados australes, se utilizan de forma creciente en agricultura. Sin embargo, el conocimiento de su biodiversidad es escaso. Más aún, zonas remotas del sur de Chile donde se encuentran las turberas, como la Reserva de Biosfera Cabo de Hornos (RBCH, 54-55º S), donde las aves constituyen el grupo de vertebrados más diverso y representativo, aún han sido escasamente estudiadas. Con el objetivo de aportar en su conocimiento en la RBCH, se estudió la diversidad del ensamble de aves en turberas esfagnosas de la isla Navarino. Se exploró si su composición específca es igual al de los humedales sin turbera, probando si las turberas constituyen o no un hábitat singular para las aves. También se clasifcó a las 37 especies de aves registradas en estos hábitats de acuerdo a la estructura de gremios. Los valores de similitud taxocenótica señalaron que la composición de aquellos con turbera difrió de aquellos sin turbera, sugiriendo que este hábitat es singular para las aves. El tipo de alimentación más frecuente fue la insectivoría (48,7%), seguido por la omnivoría (23,1%). Los resultados muestran que, a diferencia de lo señalado en trabajos previos sobre aves de turberas, estos ambientes constituyen un humedal-hábitat singular para la alimentación, reproducción y refugio de algunas especies en la RBCH. De esta manera, la conservación y uso racional de turberas debe considerar el valor que tienen como hábitat para la biodiversidad a escala de paisaje, especialmente para las aves del extremo sur americano.
Palabras clave: Ensamble, humedales, isla Navarino, Patagonia, Reserva de Biosfera Cabo de Hornos, Sphagnum spp.
Sphagnum-dominated peat bogs are being in creasingly used in extractive industries, such as the removal of the organic layer of peat for agricultural uses because of its high quality as a substrate for horticulture, foriculture, fruticulture, clearings and hydroponic activities (de la Balze et al., 2004). Peat is also used as a cover that improves other soils and as organic matter for thecultivation of fungi (Arroyo et al., 2005).
The third article of the Chilean Organic Law considers peat to be a mining resource, licensable for exploitation to any interested party (Henríquez, 2004), although anyone planning to exploit peat is now obliged to undergo an environmental impact study (Hauser, 1996). Lappalainen (1996) estimates that 1,400,000 ha of peat bogs (c. 33% of the total surface of the wetlands) are potentially exploitable in the Aysén and Magallanes Regions of southern Chile.
Peat bogs are embedded throughout the southern temperate forest matrix in southern South-America (Arroyo et al., 2005), and they are the result of high precipitation and low temperatures (Roig et al., 2001). Wetland environments cover 23.5% of the total surface of the Magallanes and the Chilean Antarctic Region, where peat bogs are the most representative type of wetland (Arroyo et al., 2005), reaching 800,000 ha (Henríquez, 2004). In the Cape Horn Biosphere Reserve (CHBR, 54 to 55º S), vast terrestrial zones are covered by peat bogs dominated by Sphagnum spp., particularly the southern and western portions of the archipelago (Rozzi et al., 2006).
Similarly, birds are an abundant and diverse portion of the biotic assemblage in the CHBR (venegas and Sielfeld, 199; Anderson et al., 2006). The frst ornithological studies in these Sub-Antarctic environments covered different islands of the archipelago south of the Beagle Channel (e.g., Oustalet, 1891; Reynolds, 1935; Olrog, 1950; Barros 1971, 1976; Sielfeld, 1977; venegas, 1981, 1991; venegas and Sielfeld, 1998). However, none were focused on the ecology of birds inhabiting peat bogs. After these surveys, and principally during the last decade because of the establishment of the Omora Sub-Antarctic Bird Observatory, knowledge about forest birds has increased substantially in Cape Horn, spe-cifcally on Navarino Island (e.g., Anderson and Rozzi, 2000; Anderson et al., 2002; Mcgehee et al., 2004; Ippi and Rozzi, 2004; Mcgehee and Eitniear, 2006; Brown et al., 2007; Mcgehee and Eitniear, 2007a, 2007b, Ippi et al., 2009). Nevertheless, the bird assemblages that use peat bog habitats in this area have not yet been studied, unlike the zones north of the Magallanes Region (51º to 53º S) such as Puerto Natales and Tierra del Fuego (TDF) (e.g., Humphrey et al., 1970; venegas, 1976; venegas and Jory, 1979; guzmán et al. 1986; Blanco et al., 2004; Schlatter, 2004).
Therefore, the scarcity of knowledge about the ecology of bird assemblages that use peat bogs south of TDF, the vast extent of the peat bog environment in the area, and the availability of peat bogs for licensable exploitation makes peat bogs and their biodiversity subjects for priority study in the CHBR. It also bears mentioning that this area has been identifed as one of the 24 remaining "pristine wilderness areas" in the world (Mittermeier et al., 2002); however, it is under increasing pressures due to growing connectivity, urban growth, alien species invasion and tourism development (Anderson et al., 2006; Rozzi et al., 2006; Arango et al., 2007; Ibarra et al., 2009a; Schüttler et al., 2010).
In this context, the objectives of this study were: i. to determine the species composition, richness, and relative abundances of birds using Sphagnum-dominated peat bog wetlands, ii. to explore whether bird composition in Sphagnum peat bogs differs from wetlands without Sphagnum, to determine whether peat bogs represent a distinct habitat for birds in this landscape, and iii. to carry out classifcation according to habitat requirements, guild structure and the most frequent activities for bird species inhabiting peat bogs in the CHBR.
Materials and methods
The study was carried out on Navarino Island (54º55`S, 67ºW, 2,528 km2), which is part of the CHBR (Figure 1). The area has a mean annual temperature of 6ºC and rainfall of 467.3 mm (di Castri and Hajek, 1976). The eco-re-gion belongs to the Sub-Antarctic Magellanic forests, where the mosaic of different habitats includes: 1. evergreen forests; 2. deciduous forests; 3. high-Andean habitats; 4. tundra formations (which include Sphagnum-dominated peat bogs); and 5. freshwater ecosystems (Pi-sano, 1977).
Regarding peat bogs, Sphagnum magellani-cum is the dominant bryophyte species in these formations (Rozzi et al., 2006). In some cases, Nothofagus antarctica, a tree species adapted to fooded zones, and Marsippospermum gran-diforum, are also present (Moore, 1983). The peat bog-forest ecotone includes tree species like N. pumilio and N. betuloides, which never reach a growth that is comparable to forest sites (Sielfeld, 1977). In peat bog-shrub ecotones, bush species like Berberis buxifolia, B. ilici-folia, Chiliotrichum diffusum, and Empretrum rubrum are also present. Finally, there are several sites presenting peat bog-grassland transitions.
A total of 49 wetlands were surveyed on Navari-no Island in preliminary avian surveys. Next, a random subsample of 10 wetlands was selected for systematic bird sampling. These 10 wetlands were identifed as natural lentic waterbodies ("natural lentic"), following the classifcation system proposed by Ramírez and San Martín (2006). These authors categorized peat bogs and other types of wetlands that were exclusively freshwater and fooded. Accordingly, fve wetlands surrounded by a Sphagnum matrix (i.e., Sphagnum-dominated peat bogs, wetlands 3, 4, 5, 6, and 7 in this study), and fve without peat bogs (wetlands 1, 2, 8, 9, and 10) were sampled (Table 1). All sites were situated between sea level and an elevation of 379 m, and they were separated by a minimum distance of 1.5 km and a maximum distance of 7.5 km.
During 2006, we conducted a seasonal sampling of birds to obtain the best representation of the avian assemblages because there is high bird dynamism in the area throughout the year (Ibarra et al., 2009b). However, the compositional statistical analysis (i.e., a comparison between the assemblages found in wetlands that were or were not within peat bogs) was concentrated only on the breeding season, as all bird species recorded in the breeding season were present during the non-breeding season as well.
Bird species and individuals were recorded in each wetland between 6:00 a.m. and 11:30 a.m. The number of individuals belonging to each bird species was identifed and recorded by the bird vocalizations or using binoculars (10x30 and 10x42). Sampling stations with a variable radius of 25 m were used (Ralph et al., 1995; gonzález and victoriano, 2005). To obtain a good representation of the habitats adjacent to bodies of water, the location where these habitats show if they are actually embedded in a Sphagnum-dominated peat bog or not, 12 sampling stations were arranged per wetland. These stations were confgured systematically and separated by a distance of at least 100 m, to avoid recording of the same individuals in neighboring stations (Bibby et al., 1992; Rozzi et al., 1996a). Sampling stations were arranged in four 200 m transects, starting from the edge of each body of water, established according to the cardinal points. Therefore, the frst station was placed in each transect at the edge of the water surface (north, south, east and west), and from that station the other two stations were established at 100 and 200 m from the edge of the body of water inwards. Wetlands were actually considered "Sphagnum-dominated peat bogs" if at least 70% of the stations at 100 and 200 m from the shore were established over Sphagnum spp. The remaining sampling stations (<30%) of Sphagnum-dominated peat bog wetlands were mainly present in either bog-forest, bog-shrub or bog-grassland ecotones.
Birds heard or observed from the center of the station were recorded during a period of 5 min, and their activity was described as: resting or swimming, fying, alarming, feeding, fght-ing, courting or vocalizing, (Ralph et al., 1995; Rozzi et al., 1996b). The vocalizing (i.e., sound record) category was attributed to a species when it was only identifed by its vocalization, without determining its specifc activity. A total of 2,400 min of bird sampling were completed.
Finally, guild structure of the assemblage was determined for aquatic and aquatic/terrestrial birds recorded in peat bogs. Microhabitat associations were determined by means of direct observation (species present on shores, sea-coasts, open waters or rushes at the moment of its registration). Feeding habits for these species were described according to feld observations and the available literature (Rottmann, 1995; Araya and Millie, 1996; Ippi et al., 2003; Martínez and gonzález, 2004; Mcgehee and Eitniear, 2006; Mcgehee and Eitniear, 2007a, 2007b).
The bird species composition, richness and relative abundances, in terms of the total number of individuals recorded in all wetlands within a Sphagnum-dominated peat bog, were determined. The Shannon-Weaver (H') diversity index was calculated (Zar, 1984). A Student's t test was performed to determine if the richness and abundance values of birds in peat bogs were different from those obtained in other types of wetlands (Scheiner and gurevitch, 1993).
The Jaccard (Cj) index of taxonomic similarity was calculated to explore how similar wetlands and their respective matrices were in terms of their bird-specifc compositions (Magurran, 1988). Jaccard values range between 0 and 1, where 1 indicates complete similarity (equal clustering of species) and 0 indicates dissimilarity (no common or shared species) (Schem-nitz, 1980). With this information, the difference in the levels of similarity was tested both within and between two different habitat types, Sphagnum-dominated peat bog wetlands and wetlands without peat bog. A one-way analysis of variance (ANOvA) was performed, and the means were separated according to the Posthoc Tukey's test (Koenen and gale, 2000). All analyses were performed with the program SPSS 10.0 (SPSS, Chicago, USA, 1999).
A total of 56 bird species were recorded in the p e at bogs a nd ot her t y p e s of we t l a nd s pre sent on Navarino Island. From the total number of bird species found in these sub-Antarctic wetlands, 66.1% (37 species) were recorded in Sphagnum-dominated peat bog wetlands (Table 2), which constitutes 7.9% of the birds found in Chile (Martínez and gonzález, 2004) and 23.8% of the species recorded south of the Beagle Channel (Couve and vidal, 2000). The species richness values varied between 13 and 21 for peat bog wetlands, while the abundance ranged from 102 to 244 individuals per station and diversity was between 2.29 and 2.68 (Table 2). All three of these variables (richness, abundance and diversity) did not show signifcant differences (p > 0.05) between Sphagnum-dominated peat bogs and wetlands without peat.
The highest similarity values were obtained be- tween wetlands 4 and 5 (0.769) and wetlands 3 and5 (0.640) (all Sphagnum-dominated peat bogs). In contrast, the lowest values were obtained between wetlands 1 and 10 (0.250) (wetland 1 was a lagoon and 10 was a pond at 379 m.a.s.l.) and wetlands 2 and 10 (0.250) (wetland 2 was a lake near the sea). Overall, the community similarity values between wetlands indicated that the bird composition in Sphagnum-dominated peat bogs signifcantly differed from that in wetlands with out peat (F2,42 = 9.028; p = 0.0005) (Figure 2).
Regarding the guild structure of aquatic and aquatic/terrestrial birds in terms of feeding habits and microhabitat association, the most abundant categories were the omnivores that were associated with open waters (n=5: Anas favirostris;A. georgica; Larus dominicanus; Lophonetta specularioides; and Tachyeres patachonicus), followed by the omnivores that were associated with shores (n=3: Charadrius modestus; L.dominicanus; and Vanellus chilensis) (Table 3).
Considering all of the recorded species, including the aquatic, aquatic/terrestrial and terrestrial birds, the most frequent feeding habit was that of the insectivores (48.7%), followed by the om-nivores (23.1%), herbivores (17.9%), and carnivores (10.3%) (Table 3).
In relation to the categories of activity, birds were observed fying in 40% of the cases. Anas sibila-trix, Caracara plancus, Carduelis barbata, En-icognathus ferrugineus and L. dominicanus were the species that presented the highest proportion of birds performing this activity, reaching 74% of the records. The second most represented category, in relative terms, was the sound record (23%). Colorhamphus parvirostris, Elaenia al-biceps, Pygarrhichas albogularis and Scytalopus magellanicus were detected in high proportions by means of their vocalization (>74%). Resting (15%) was the third most represented category: A. georgica, Curaeus curaeus, and T. patachoni-cus showed this activity in more than 63% of the cases. Two species, Aphrastura spinicauda and T. patachonicus, often showed an alarm behavior (>32%). Campephilus magellanicus (38%), Cinclodes patagonicus (33%), L. specularioides (50%) and V. chilensis (50%) were the four species with the highest dedication to feeding. Only one species, Chloephaga poliocephala (33%), was observed fghting. Finally, only Cistothorus platenses (20%) presented courting behavior during the sampling (Table 4).
This work provides new information on the natural history, diversity and community structure of the birds that inhabit Sphagnum-dominated peat bogs in the CHBR. Our results show that, unlike previous works on the avifauna present in peat bogs in other zones in Patagonia (Sielf-eld, 1977; venegas, 1976, 1981, 1991; guzmán et al. 1986; venegas and Sielfeld, 1998; Blanco et al., 2004; and Schlatter, 2004), these environments shelter a signifcant portion of the avian diversity found on Navarino Island in the Cape Horn Biosphere Reserve. Our records of species richness (n = 37) in peat bogs is much higher than those obtained in studies conducted farther north in the Magallanes Region (e.g., venegas, 1976, n = 3 species; guzmán et al., 1986, n = 6 species; Blanco et al., 2004, n = 6 species; and Schlatter, 2004, n = 25 species). In general, the previously mentioned studies consisted of spe-cifc samplings of a few days during one season (except Schlatter 2004), which could explain the lower numbers of species recorded, and in turn highlight the value of long-term research programs (Anderson et al., 2008). Furthermore, ec-otone zones were considered in our study (e.g., bog-forest, bog-shrub and bog-grassland), and freshwater birds were included; both of these aspects could have infuenced the high number of species observed in this study.
The increasing exploitation and consecutive isolation of peat lands have been reported as main factors affecting bird diversity at the landscape scale (Calmé and Desrochers, 2000). In contrast, in the CHBR the mosaic of different habitat types represents a very rare example of the non-fragmented areas in the world (Rozzi et al., 2006). This characteristic of the study area, in addition to our results showing a higher diversity of birds in peat bogs within the CHBR than in other nearby areas, suggests that the importance of peat bog ecosystems for a particular area is probably contingent on the matrix of habitats found in the broader landscape. Consequently, in the CHBR, where peat bogs are more abundant and connected with other heterogenic and undisturbed habitats, this environment could occupy a more prominent role in determining the landscape-level species assemblages of avifauna. Therefore, landscape measures are necessary, but probably not suffcient, to describe the patterns of bird diversity found in the CHBR.
Based on our fndings, we put forward that Sphagnum-dominated peat bogs represent a unique wetland habitat for a signifcant portion of the avian community in the CHBR. This position is supported by the fact that the assemblages found in these peat bogs are highly divergent from those of other wetland types (Similarity index, Figure 2). At the same time, the species composition within peat bogs tends to be the very uniform (i.e., displaying a high degree of similarity among these peat bogs). This result could be interpreted at least in two different ways: (1) when the rest of the wetlands are grouped as "of other type", their intrinsic variability is not being considered, as the different types of associated in turn defne different types of assemblages habitats (shrubs, rushes, forest, grassland, etc.) that do not necessarily need to be similar; or (2) should be considered; this information would that peat bogs actually tend to be more similar to each other than do "other types" of wetlands in terms of their specifc composition. Consequently, and regardless the frst alternative, our study indicates that peat bogs represent a distinct habitat within the sub-Antarctic landscape matrix whose biodiversity is insuffciently studied and has previously been unappreciated. However, the underlying mechanisms explaining the biodiversity present in peat bogs, and the organization and processes involved, still need to be further studied (Arroyo et al. 2005).
The bird assemblage that used peat bogs and their ecotones included mainly insectivores (e.g., G. paraguaiae) but also species from a complete suite of other feeding guilds, including omni-vores (e.g., C. modestus), herbivores (e.g., C. picta), granivores (e.g., Phrygilus patagonicus) and carnivores (e.g., Nycticorax nycticorax). Community composition is known to be strongly related to food availability (Cody, 1981), a factor that might be relevant for birds in the Sphagnum wetlands as well (guzmán et al., 1986). This fnding also agrees with what has been reported by Schiavini (2000), who associates the presence of birds in peat bogs mainly to food searching.
In general, in peat bog systems small birds (in-sectivores) are predominant; these species must feed frequently and, therefore, must have a food source that allows them to feed at regular intervals (griffths et al., 1982; guzmán et al. 1986). The presence of a high proportion of small birds in peat bogs may indicate that these environments have a reliable food source, at least for the predominant insectivorous species. These species form the dominant feeding guild in sub-Antarctic wetlands during the coldest months, when wetlands are completely frozen (Ibarra et al., 2009b). In the case of the herbivorous species (excluding the granivorous species such as P. patagonicus or C. barbata) and omnivores species, fundamentally the Anatidae, food is frequently obtained from the open waters or shores where there might be a higher production of food resources, in contrast to the fact that Magellanic peat bogs have been considered to be a system of low productivity where plant species present scarce palatability (Pisano, 1977).
In the case of reproduction, Matteazzi (1997) and Schiavini (2000) pointed out that the peat bog-forest ecotone is a nesting site for non-pas-seriform species such as C. picta and G. para-guaiae. C. picta usually nests in inland peat bog wetlands in the CHBR (Ibarra et al., 2009b), while G. paraguaiae was commonly recorded in peat bogs during the spring and summer seasons, in twilight, performing nuptial fights with a characteristic buzz that is made with the tail. This reproductive behavior is characteristic for this Scolopacidae (Rottmann, 1995). The results for the activity categories also allowed for the identifcation of C. platensis while performing courting activity and C. poliocephala while fghting for territory during the breeding season. Likewise, the records of C. magellanicus were obtained in a transition bog-forest, even though this species is always associated with the presence of old-growth trees. This Picidae is usually found in the old-growth forests of Cape Horn (Arango et al., 2007), which constitute the main matrix of Sphagnum-dominated peat bogs in the Magallanes (Arroyo et al., 2005).
In light of the fact that, currently, Sphagnum-dominated peat bogs are under a growing pressure for extraction in southern South America, conservation-oriented policies and policies for sustainable use should consider their high value for feeding, reproduction and sheltering for an important diversity of birds. According to Arroyo et al. (2005), peat bogs and forests are intrinsically linked at the ecosystem level in austral South America; therefore, the destiny for peat bogs will determine the future of Southern temperate forests, and vice versa.
This work was fnanced by the project FPA 12-001-06 of CONAMA, granted to the Omora Foundation, and by Wildlife Trust Alliance. The Institute of Ecology and Biodiversity (IEB) also provided fnancial contributions through grant ICM P05-002, and the Puerto Williams Branch-UMAg provided logistic support to the team. Special thanks to A. Barreau, E. Firmani, g. gonzález and S. Mcgehee for their support in the feld. The comments by B. Latorre helped to improve preliminary versions of the manuscript. JT Ibarra and TA Altamirano are CONICYT research grant holders. This study is part of the long-term programs of conservation Biosphere Reserve and the founding member of and research of the Omora Ethnobotanical Park, Chile's long-term socio-ecological research net-the scientifc research center of the Cape Horn work (http://www.ieb-chile.cl/ltser).
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Received 10 March 2009. Accepted 15 July 2009.
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