Introduction
The lack of scientific information on the ecology and biology of valuable tropical tree species impairs the development of adequate legislation and management guidelines for ecologically sustainable forestry (Mostacedo & Rumiz, Reference Mostacedo and Rumiz2010). A common argument for continuing to log tropical forests is that if native forests do not provide an economic alternative they are more likely to be cleared for agriculture or plantations (Merry et al., Reference Merry, Soares-Filho, Nepstad, Amacher and Rodrigues2009). Such arguments are based on the assumption that appropriate laws and regulations guide management (Shearman et al., Reference Shearman, Bryan and Laurance2012). However, enacting legislation does not improve forest management unless the laws are enforced. This is a problem given that it is estimated that 40% of the world's tree species are threatened with extinction (Oldfield et al., Reference Oldfield, Lusty and MacKniven1998;; Newton & Oldfield, Reference Newton and Oldfield2008). Therefore assessment of the conservation status of threatened tree species is a priority for designing appropriate conservation plans and policies (López-Toledo et al., Reference López-Toledo, Gonzalez-Salazar, Burslem and Martinez-Ramos2011), particularly as the portion of natural tropical forest area under timber production has increased steadily over time (Guariguata et al., Reference Guariguata, Sist and Nasi2012). Despite the increase in sustainable forest management plans throughout the tropics (ITTO, 1990;; Poore & Sayer, Reference Poore and Sayer1991) an estimated 127,300 km2 of tropical forest is lost annually (FAO, 1999). Over 90% of tropical forests are managed unsustainably (Blaser et al., Reference Blaser, Sarre, Poore and Johnson2011) and only a small percentage of the total area of tropical forest is under certified sustainable management (Bowles et al., Reference Bowles, Rice, Mittermeier and da Fonseca1998).
Amburana cearensis (Fr. Allem.) A.C. Smith (South American oak, known locally as roble) is a Neotropical tree species of the family Fabaceae, subfamily Papilionoidea, with a geographical range covering the seasonal dry tropical forests and transition zones of Brazil, Paraguay, Bolivia, Peru and Argentina (Dimitri, Reference Dimitri1997). This region constitutes a phytogeographical entity: Seasonally Dry Tropical Forests of the Pleistocenic Arc (Prado, Reference Prado2000). Although A. cearensis has high economic value and is categorized as Endangered on the IUCN Red List there has been no effort to delineate a conservation and management plan for the species (Leite, Reference Leite2005;; Americas Regional Workshop, 1998). The species’ distribution, population structure and regeneration pattern are poorly documented, making it difficult to develop management guidelines (Osinaga Eguez, Reference Osinaga Eguez1997). A. cearensis attains large dimensions: 15–25 m height and 40–110 cm diameter at breast height (DBH; López et al., Reference López, Little, Ritz, Rombold and Hahn1987) and has a moderate growth rate (0.89 cm year−1 in diameter), although initial growth is slow (Calzon & Palma, Reference Calzón and Palma2008). It starts reproducing when DBH reaches > 60 cm; 90% of individuals attain reproductive age when they reach DBH > 67 cm (van Rheenen, Reference van Rheenen2005;; Ayarde, Reference Ayarde2006). The species bears seeds every 3–4 years, during September–October (Ayarde, Reference Ayarde2006). Ripe seeds are dispersed from the open legume and lose viability quickly (López et al., Reference López, Little, Ritz, Rombold and Hahn1987).
In Argentina A. cearensis is restricted to the provinces of Salta and Jujuy, in a narrow belt (400–750 m altitude) of the Sub-Andean Piedmont Forest (Prado, Reference Prado2000). This forest harbours a high number of species (e.g. 300 woody species, of which 113 are trees, 39 amphibians, 137 birds, and 106 mammals) and is the most threatened forest ecosystem of Argentina (Brown et al., Reference Brown, Pacheco, Lomáscolo, Malizia, Brown, Martínez Ortiz, Acerbi and Corchera2006). Analysis indicates that the remaining area of piedmont forest is < 37% of its original cover, and most of the remaining stands are confined to steep and less accessible areas (Brown et al., Reference Brown, Blendinger and Lomáscolo2009). The remaining piedmont forests are degraded and almost all stands have been affected by logging (Brown et al., Reference Brown, Grau, Lomáscolo and Gasparri2002), in which harvesting is focused on a few valuable timber species, with virtually no inventory or planning. Forestry statistics show a decreasing trend overall in timber volume of all species harvested and a concomitant increase in the area logged, probably associated with a depleted timber stock (Eliano et al., Reference Eliano, Badinier and Malizia2009).
Unplanned and extractive logging in the piedmont forest has compromised most valuable timber species, including A. cearensis. In the province of Salta the decrease in the number of individuals of A. cearensis prompted a 1960 decree (No. 15.742/1960) restricting logging to individuals of > 60 cm DBH (minimum legal cutting diameter). In Jujuy province logging of the species was banned in 1972 (Decree No. 676-H-72). The mismatch between legislation in these neighbouring provinces and the lack of control has made law enforcement difficult. Furthermore, forest management plans do not prioritize the protection of this valuable resource. For these reasons information about the status of this species is needed. We analysed the size and structure of the population of A. cearensis in the two provinces, to assess whether different legislation has influenced the conservation status of the species.
Study area
The study was conducted in the Sub-Andean Piedmont Forest of the Upper Bermejo River in north-west Argentina (Fig. 1). The forest covers c. 900,000 ha (80% steep terrain and 20% flat terrain; Brown et al., Reference Brown, Blendinger and Lomáscolo2009). Annual rainfall is variable (800–1,000 mm), with a pronounced dry season during March–November; Bianchi et al., Reference Bianchi, Elena and Volante2008). Mean annual temperature is 18–20 °C, with peaks of > 40 °C in the summer (Bianchi et al., Reference Bianchi, Elena and Volante2008). Mature piedmont forest stands in north-west Argentina have a continuous canopy 25–35 m in height, a basal area of 25–30 m2 ha−1and c. 35–40 tree species ha−1 (Brown & Malizia, Reference Brown and Malizia2004). They also have thorny shrubs and a number of xerophytic elements (Prado, Reference Prado, Brown and Grau1995).
Fig. 1 Location of study sites (Table 1) in the piedmont forest of north-west Argentina. The rectangle on the inset indicates the location of the main map in Argentina.
Methods
We surveyed, using distance sampling (Buckland et al., Reference Buckland, Anderson, Burnham, Laake, Borchers and Thomas2001), at 13 sites (five in Jujuy and eight in Salta; Table 1;; Fig. 1) in areas where the species could be present based on its potential distribution in north-west Argentina, an area of 1,732 km2 (Malizia et al., Reference Malizia, Pacheco, Loiselle, Brown, Blendinger and Lomáscolo2009). Distance sampling methodology is more appropriate than conventional sampling methods for estimating the density of rare species that are sparsely distributed across large geographical areas (Cochran, Reference Cochran1977;; Buckland et al., Reference Buckland, Anderson, Burnham, Laake, Borchers and Thomas2001). From May 2007 to May 2008 we established 20 100 m transects of variable width at each site to detect individuals of A. cearensis. Its characteristic bark makes the species particularly easy to detect. When an A. cearensis tree was detected we measured the perpendicular distance from the transect line to the tree, using a metric tape. The DBH of each individual was measured 1.3 m above ground, using a metric tape. We conducted a more detailed survey from October 2010 to October 2011, covering 70 ha at Finca Río Seco (in Salta province), owned by the forestry company Forestal Santa Bárbara, and 72 ha at Finca Yuchán (in Jujuy province), owned by the agribusiness firm Ledesma. To our knowledge these stands represent the best piedmont forest in north-west Argentina.
Table 1 Details of sites surveyed for Amburana cearensis in the provinces of Jujuy (where harvesting is banned) and Salta (where harvesting is permitted), Argentina (Fig. 1) during 2007–2008.
1 CTL, conventional timber logging; FSC, Forest Stewardship Council certification; NL, no logging since 1979
2 Harvesting banned by the Forest Stewardship Council in 2008, pending the development of a management plan for the species
We used Distance v. 5.0 (Thomas et al., Reference Thomas, Laake, Strindberg, Marques, Buckland and Borchers2006) for data analysis at two levels: province (Jujuy and Salta) and country (i.e. both provinces together). For each province we estimated density in three diameter size classes. Detection functions were selected based on Akaike's information criterion (Burnham & Anderson, Reference Burnham and Anderson1998), χ2 model fit statics and visual inspection of detection probability and probability density plots (Buckland et al., Reference Buckland, Anderson, Burnham, Laake, Borchers and Thomas2001). Grouped cut points and truncation distances were used to remove outliers from the analysis.
Results
A total of 813 individuals of A. cearensis were detected in 1,114 ha of the area surveyed in both provinces, yielding an estimated density of 1.12 ha−1 (95% CI 0.48–2.63). There was no significant difference between the density of the species in Salta (5.15 ha−1;; 95% CI 3.14–8.45) and that in Jujuy (3.67 ha−1;; 95% CI 2.59–5.17) although DBH was significantly lower in Salta (23 ± SD 12 vs 41 ± SD 18 cm; P < 0.05). Density estimates decreased consistently with increasing DBH class, approximating a reverse J-shape (Fig. 2). The density of stems in the 5–20 cm DBH class was greater in Salta than in Jujuy and the density of stems in the > 40 cm DBH class was lower in Salta than in Jujuy (Fig. 2). Most individuals (84%) encountered in Salta were found at one site (Piquirenda), which had a high proportion of individuals in the lower diameter classes (Fig. 3). Most sites (60%) had a bell-shaped distribution of diameter class (Fig. 3). The detailed diameter-class distribution in Finca Yuchán and Finca Río Seco also showed a bell-shape (Fig. 4). The density of the species was 1.5 ha−1 in Finca Yuchán and 0.4 ha−1 Finca Río Seco; there was no significant difference in DBH at the two sites (44.23 ± 17.49 cm vs 47.02 ± 14.17 cm; P = 0.20).
Fig. 2 Density (with 95% CI) estimates for Amburana cearensis, using distance sampling methodology based on diameter class distribution, in Jujuy and Salta provinces in Argentina (Fig. 1). An asterisk (*) indicates significant differences between provinces for a given diameter class.
Fig. 3 Proportion of individuals of A. cearensis detected in each diameter size class (5–20; 20–40; 40–60; > 60 cm DBH) at each site surveyed. The dashed line indicates the legal cutting limit in Salta. The numbers above the bars indicate the number of individuals detected at each site.
Fig. 4 Density of A. cearensis detected in Yuchán, Jujuy province and Finca Río Seco, Salta province, according to the diameter size class distribution. The dashed line indicates the legal cutting limit in Salta.
Discussion
Our data show differences in the characteristics of the populations of A. cearensis in the two provinces that may be attributable to the application of different legislation. Nevertheless, although legislation in Jujuy has probably prevented further decline of the species there, it has not been accompanied by incentives to encourage research on the species. Conventional unsustainable timber management in Salta province appears to be having a negative effect on the population structure (there is a low density of individuals > 60 cm DBH). Sustainable use and trade in timber have been proposed as an economic incentive for forest conservation (Putz et al., Reference Putz, Blate and Redford2001;; Pearce et al., Reference Pearce, Putz and Vanclay2003;; Newton, Reference Newton2008) but the conservation-through-use argument requires that technical uncertainties, including lack of appropriate ecological information, are overcome (Dickinson et al., Reference Dickinson, Dickinson and Putz1996;; Newton, Reference Newton2008). For example, to make appropriate decisions regarding effective silvicultural treatments for A. cearensis the reproductive biology of the species (Leite, Reference Leite2005) must be understood. If logging continues in Salta province the species will probably decline further, leading to its economic extinction in this part of Argentina.
A. cearensis was categorized as Endangered on the IUCN Red List in 1998 but its status requires updating (IUCN, 2013). To identify regional bias as a result of population differences it is necessary to conduct national categorizations and integrate those regional assessments to determine the species’ current status globally (Gárdenfors et al., Reference Gárdenfors, Hilton-Taylor, Mace and Rodriguez2001). Our results suggest that the categorization as Endangered is correct for Argentina, where the species has a low density. Previous stand-scale forest inventory surveys in Argentina also reported that A. cearensis has a low density (Ayarde, Reference Ayarde2006;; Malizia et al., Reference Malizia, Pacheco, Loiselle, Brown, Blendinger and Lomáscolo2009) and it was assumed that the species was rare historically (Calzón & Palma, Reference Calzón and Palma2008). The species is threatened by deforestation of the piedmont forest of north-west Argentina for agricultural and urban development (Eliano et al., Reference Eliano, Somma and Quintana2010). Superimposed on this threat is the high logging pressure (Quiroga & Salinas, Reference Quiroga and Salinas1996), which decreases the density of the species, impairs its natural regeneration and could lead to local extinction (Fredericksen & Putz, Reference Fredericksen and Putz2003). In our study the low proportion of stems that occur in the > 60 cm DBH class (i.e. the class at which the species starts reproducing) in Salta is an indication of the logging pressure on the species. The populations of A. cearensis in Finca Yuchán and Finca Río Seco were dominated by individuals of the intermediate size classes, with few individuals in the small and mature size classes. A similar bell-shaped distribution has also been reported from studies of A. cearensis in Bolivia, where most individuals were concentrated in the 30–50 cm DBH class (Osinaga Eguez, Reference Osinaga Eguez1997). However, the Finca Yuchán population structure was skewed more to the left and had higher density in all diameter size classes compared to Finca Río Seco, which may indicate that the ban on harvesting in Jujuy has reduced pressure on the A. cearensis population in Finca Yuchán.
Conservation management must encompass social, economic and political trade-offs to reach practical solutions (Newton, Reference Newton2007). In the absence of reliable scientific information on which to base management decisions it is wise to employ multiple strategies. We make the following recommendations for the conservation of A. cearensis in Argentina. (1) Incorporate areas that contain the largest populations and best age structure (i.e. those with a broad range of diameter classes represented) into the regional protected area network. Finca Yuchán, Fraile Pintado, and Rio Colorado are priority areas for conservation because the largest populations, with the best age structure, are found here (only 1% of the piedmont forest is currently under any legal protection; Brown et al., Reference Brown, Grau, Lomáscolo and Gasparri2002). (2) Reinforce the population to facilitate natural regeneration (Doucet et al., Reference Doucet, Kouadio, Monticelli and Lejeune2009);; this will probably require using nursery-sourced seedlings and, in the absence of genetic research, it is essential to ensure that these seedlings come from local seed stocks. (3) Develop the support and cooperation of a broad array of stakeholders (governmental policy-makers, NGOs, landowners, local citizen representatives and scientists) for restoration, conservation planning and protection of the species. (4) Legislate to protect remnant individuals of the species during land conversion, to conserve the genetic diversity of the species (Hamrick et al., Reference Hamrick, Godt and Sherman-Broyles1992;; Manning et al., Reference Manning, Fischer and Lindenmayer2006).
Improved knowledge of the ecology of A. cearensis is required (Hutton & Leader-Williams, Reference Hutton and Leader-Williams2003) before logging can be allowed in Jujuy province or continued in Salta province. Stringent forest management standards, such as forest certification criteria, provide an opportunity to develop management and conservation plans for threatened species (SmartWood, 2005). This strategy is currently being followed by the Forestal Santa Bárbara forestry company, which adheres to the principles and criteria of the Forest Stewardship Council. This company halted logging of A. cearensis in 2008 and has promoted research to develop a species conservation action plan (Forestal Santa Bárbara, 2011). Listing A. cearensis in Appendix I of CITES could restrict its international trade but could also inhibit the emergence of sustainable management practices and result in conversion of A. cearensis habitat to agriculture because of a lack of economic alternatives (Turner et al., Reference Turner, Cortina, Foster, Geoghegan, Keys and Klepeis2001). In contrast, listing A. cearensis in CITES Appendix II, accompanied by management guidelines based on knowledge of the species’ ecology and high forest management standards, could help promote improved management for timber exploitation and international trade. For example, forest management guidelines for the species should include a minimum cutting diameter of 90 cm DBH and retain 70% of the individuals recorded in forest inventories to ensure stems of medium-size diameter classes as seed sources for future regeneration. In Argentina management standards can be framed and supported by the National Forest Conservation Law (26.331), which has established a fund to promote restoration of degraded stands and develop sustainable forest management.
We have provided evidence that the approach to logging established in Salta province is not ensuring the conservation of A. cearensis. It is imperative that the status of this species be assessed and appropriate legislation and management be enacted, based on the species' ecology and biology (Schulze et al., Reference Schulze, Grogan, Landis and Vidal2008). We have passed our recommendations to the relevant decision-makers but they have not adopted them in management plans and forestry regulations. Therefore, we have begun an outreach programme to promote stakeholder involvement to implement silvicultural procedures for sound forest management. We are also conducting further research to determine the reproductive ecology and establishment requirements of this threatened and valuable timber species to refine our silvicultural prescriptions.
Acknowledgements
We are grateful to Diego Regondi, Pamela Fierro, Roque Yapura, Sebastían Albanesi, Patricia Puechagut, Marisol Mata, Ana Magdalena Gutierrez and Ramiro Carrillo for field assistance, and to Ledesma SAAI and Forestal Santa Bárbara SRL, the National Park Administration and the Environmental Ministries of Salta and Jujuy for granting the permits to conduct the study. The project was funded by Agencia Nacional de Promoción Científica y Tecnológica (PICT 2008-1165, Préstamo BID), Conservation Leadership Programme, Mohamed bin Zayed Species Conservation Fund, Forestal Santa Bárbara SRL and Idea Wild.
Biographical sketches
Natalia Politi is developing management guidelines for sustainable timber harvesting activities that ensure the conservation of biodiversity. Luis Rivera leads projects on threatened species and promotes regional conservation strategies for these species in north-west Argentina. Leónidas Lizarraga is a geographical information system specialist studying spatial–temporal human and ecological relationships between protected areas and their surroundings. Malcolm Hunter Jr studies the interface between maintaining biodiversity and managing ecosystems for natural resources. Guillermo E. Defossé’s research focuses on the effect of fire on forests and grasslands, and ecological restoration of disturbed forest ecosystems.
