Successional stage, fragmentation and exposure to extraction influence the population structure of Euterpe precatoria (Arecaeae) Influencia de la etapa de sucesión, fragmentación y exposición a la extracción en la estructura poblacional de Euterpe precatoria (Arecaeae)
Gerardo Avalos1*,2*, Mauricio Fernández Otárola1,3* & James Theodore Engeln4*
The neotropical palm Euterpe precatoria is subject to extraction for its valuable palm heart. The development of management ]]>
E. precatoria varies with successional stage, fragmentation, and exposure to extraction. Since E. precatoria recruitment increases with disturbance, we expected seedling density to be higher in secondary forests and fragments relative to primary ]]>
La palma neotropical Euterpe precatoria sufre un proceso de extracción ilegal debido al sabor ]]>
E. precatoria varió con el estadio sucesional, la fragmentación y la exposición a la extracción. Esperábamos que la densidad de plántulas fuera mayor en bosques secundarios y fragmentos en relación con los bosques primarios. El estudio se realizó entre 2007-2008 en la vertiente ]]>
Palabras clave: Euterpe precatoria, productos forestales no maderables, conservación de palmas, ecología de palmas, palmito, manejo de palmas. The intensification of the use of non-timber forest products over the last half century has increased the extent of human impacts on tropical ecosystems, thereby threatening the ]]>
et al. 1995). In many cases, resources are over-extracted surpassing the recovery capacity of the target species (Hall & Bawa 1993, Ticktin 2004). This is particularly true for palms, which represent one of the most economically important groups of Angiosperms in tropical forests (Johnson 1996, Campos & Ehringhaus 2003, Dransfield et al. 2008). Arecaceae has been a traditional source of construction materials, food, and fiber for human groups (Macía ]]>
et al. 2011). Palm use is intrinsically linked to local knowledge, passed from generation to generation, but this age-old human-palm relationship is changing dramatically due to large scale commercial trade (Kahn 1991, Morcote-Ríos & Bernal 2001, Campos & Ehringhaus 2003, Manzi & Coomes 2008, Weinstein & Moegenburg 2004), which is influencing the population structure and geographic distribution of many species through cultivation, extraction, and fragmentation (Bonesso-Sampaio et al. 2007, Endress et al. 2004, ]]>
Intensive palm extraction is linked to habitat fragmentation; the combination of both factors cause significant changes in population structure and genetic diversity. Sezen et al. (2007) showed that fragmentation and changes in land uses significantly reduced the genetic diversity of seedlings and saplings ]]>
Iriartea deltoidea in second growth forests in the vicinity of La Selva, Costa Rica. Harvesting of palm heart from I. deltoidea and similar species usually targets the largest individuals, which produce the most palm heart. The harvesting of specific size classes significantly determines population growth and tolerance to extraction (Freckleton et al. 2003).
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In Costa Rica, the core of illegal palm heart harvesting is concentrated on Euterpe precatoria Mart. Park rangers estimate that around 2 000 palms per year are illegally extracted from Braulio Carrillo National Park (Avalos 2007). A typical extraction bout lasting three days could remove more than 300 individuals close to 20m in height (Avalos 2007). This practice started as a cultural Easter tradition involving the extraction of a handful of stems per household, but now has evolved into an important underground ]]>
et al. 1997) has continued throughout much of the region (even though it has been banned by local laws, and consumers have the alternative choice of using commercially-produced palm heart from Bactris gasipaes). The consumption of E. precatoria is centered on Costa Rican Holy Week ]]>
B. gasipaes. Today the commercial and domestic cultivation of B. gasipaes is ubiquitous in many rural communities while the tradition of using wild palm heart has been abandoned. A decline in traditional extraction has ]]>
Geonoma undata subsp. edulis, has become exceedingly inaccessible as its palm heart is now provided by local poachers (Sylvester & Avalos 2009). Poachers, as opposed to families, now exert the majority of extraction pressure on wild palms, and the overexploitation caused by this activity threatens forest ]]>
Here, we pursue to answer the question: how does the population structure of E. precatoria change with successional stage, forest fragmentation, and exposure to extraction? We predict that seedling density increases with disturbance, being higher in secondary forests, extracted forests, and ]]>
Materials and Methods ]]>
Study sites: This study was conducted during April, August and November from 2007 to 2008 at four sites along the Caribbean Slope of Costa Rica: Braulio Carrillo National Park (BCNP), La Selva Biological Station (LSBS), Manú Center (Manú) and Finca El Progreso (FEP). The first two sites have continuous primary and secondary forests, whereas the latter two consisted of fragments maintaining primary forests. In BCNP, data were ]]>
Manú and FEP were previously utilized for selective logging, but have been left undisturbed since 1996 and 1987, respectively. Historically, palm heart extraction took place with high intensity at both sites but has decreased in the last decade, likely due to local reduction in abundance of E. precatoria. ]]>
Study species:Euterpe precatoria Mart. belongs to the subfamily Arecoideae and the tribe Euterpeinae along with five other genera (Prestoea, Neonicholsonia, Hyospathe, Oenocarpus and Jessenia).
Euterpe precatoria is divided into two varieties by Henderson (1995), longevaginata (stems solitary or cespitose, low and high elevations in the Andes and Central America) and precatoria (stems solitary, low elevations in the Amazon). In Costa Rica, E. precatoria var longevaginata is commonly described as a single-stemmed, solitary subcanopy palm distributed from sea level to ]]>
et al. 1995). The vertical stem may reach 26m in height with a diameter at breast height (DBH) of up to 15cm, and a cone of stilt roots that in extreme cases may reach over 1.5m in height. This monoecious species has protandrous inflorescences, is pollinated by beetles and bees (Küchmeister et al. 1997), and is dispersed by birds (Galetti & Aleixo 1998, Henderson 2002), and by
Cebus monkeys in Colombia (Zona & Henderson 1979). Across its latitudinal range, E. precatoria is found in inundated forests (where it reaches high densities), as well as in drained terra firme forests (Henderson 1995). In Costa Rica, the overall density of E. precatoria tends to be lower relative to what has been recorded in the Western Amazon, occurring in highly diverse lowland as well as premontane forests (Clark
et al. 1995, Homeier et al. 2002, Vormisto et al. 2004). It colonizes a variety of substrata including fallen logs and the buttresses of dead canopy trees. Because it is a monopodial species, the extraction of its palm heart results in the death of the individual. The disturbance created by the extraction process favors seedling and juvenile growth, which increases the overall abundance of E. precatoria in extracted ]]>
Population structure determination: We used square plots to quantify the population structure of E. precatoria at each site. Plot establishment was as follows: - In ]]>
Table 1).
Within each plot, all E. precatoria ]]>
E. precatoria in fragmented forest conditions. We measured stem height from the ground to the first frond (excluding the crown shaft) using basic trigonometry rules, and a Suunto PM-5 clinometer in palms higher than 8m. Stem height was corrected by subtracting the height of the cone of stilt roots.
Palm-use history: To establish the history of palm use as a forest resource, we conducted semi-structured interviews with members of the Buenos Aires (Manú) and Colinas (FEP) communities, with each household representing a sample unit. The purpose of these interviews was to gather information on previous land-use of these sites and the surrounding areas as well as the history of palm extraction. Questions gathered information on ]]>
]]>
Palm population structure was compared among sites by determining the distribution of individuals in each height class. We used correspondence analysis to compare the distribution of E. precatoria across sites in terms of the similarity in abundance of different ontogenetic stages. E. precatoria undergoes an ontogenetic transition at about 1m in stem height and reaches maturity at 10m stem height (Avalos & Fernández ]]>
Results
Palm density: Considerable differences in absolute abundance of E. ]]>
were found among sites. Palm density varied almost two orders of magnitude among studied sites (920 individuals per Ha at LSBS secondary forest compared with 36 individuals per Ha in the primary forest of BCNP, Table 1). Greater concentrations of E. precatoria were found in primary and secondary continuous forests compared to the primary forest fragments of Manú and FEP. Palm concentration in sites exposed to frequent extraction (BCNP extracted forest) showed the highest density.
Population structure: The population structure of E. precatoria varied among sites. There was a lack of tall palms (>10m) in secondary forests (LSBS and BCNP) as well as in the extracted forest of BCNP. The primary forest fragments of Manú and FEP exhibited similar trends as those of primary forests without extraction at LSBS and BCNP, both having a lower ]]>
Euterpe precatoria was predominantly represented by individuals <5m across all study sites. Combined proportions of individuals <5m varied between 50-90% of the total number of individuals (Fig. 2). ]]>
Palm-use: Ninety percent of participants had lived in their respective communities for more than 10 years. An equal number of men and women were interviewed, ranging from 17-64 years old with an average age of 44. The average family size ]]>
Interviews revealed a tendency to consume commercially-produced palm heart from Bactris gasipaes (locally known as “pejibaye”) over wild palm heart harvested from the surrounding forests. Families who had consumed E. precatoria (locally ]]>
E. precatoria are relatively available (see Sylvester & Avalos 2009), the traditional use of palm heart from this species has been abandoned. No recent accounts of E. precatoria harvest/consumption were provided in the interviews. Nevertheless, selected interviewees in both sites referenced poaching activity in ]]>
Discussion
Habitat disturbance increases E. precatoria abundance: Palm recruitment and establishment ]]>
et al. 1996), as well as by the palm dispersion strategy (Cintra & Horna 1997, Fragoso et al. 2003), previous history of land use practices (Clark et al. 1995, Sezen et al. 2007) and human intervention (Wright & Duber 2001). For many palm species, increased disturbance ]]>
E. precatoria preferentially recruited in slightly disturbed environments such as secondary and extracted forests. The density of this species increased with the magnitude of disturbance, as reflected by the steep rise in seedling number with increasing disturbance regime. However, E. precatoria was also ]]>
E. precatoria grows best at intermediate light levels (50% of canopy cover), which is consistent with our observations of increased growth and abundance with increasing canopy openings, such as those brought about by extraction and early successional environments. The regeneration behavior of E. ]]>
falls within the concept of cryptic pioneer, since it regenerates under moderately disturbed conditions but can survive under moderate shade (Kitajima & Poorter 2008). The extraction of E. precatoria creates low intensity canopy and understory disturbance. The canopy opening created by a palm fall is small, as the crown and trunk are compact and most of the disturbance is restricted to the forest understory (Avalos 2007). While small, the increase in canopy aperture and the removal of adult palms favors an increase in the abundance of juveniles and seedlings. A dynamic ]]>
E. precatoria establishment.
Aguilar-Barquero & Jiménez-Hernández (2009) analyzed changes in diversity and abundance of the palm assemblage at FEP using three fragments with different degrees of human intervention (primary forest, logged primary forests left to natural regeneration, and secondary forest). Their ]]>
2), compared to our study. Among the 15 species of palms recorded in that study, E. precatoria was found (but with low frequency) only in primary forest fragments, showed higher density in the primary forest with some degree of human disturbance, and was intermediate in abundance relative to other palms. The authors concluded that E. precatoria could be an indicator of primary forest conditions. In our study, the preference for disturbed habitats was clear at the seedling and juvenile stages, ]]>
Iriartea deltoidea, in lowland Amazonian Ecuador.
Forests under ]]>
et al. 2000). Freckleton et al. ]]>
E. edulis and predicted that palm populations may recover following low or moderate harvesting, but that sustained high levels of harvesting targeting adults and pre-adults (so that reproductive individuals take longer to be replaced) may lead to local population extinction. Because E. precatoria has a large minimum reproductive size of 10m, and a slow growth rate compared to commercial palm heart species, its population size may require more time to ]]>
E. precatoria’s slow growth; there may not have been sufficient time post-disturbance to allow establishment of adult palms. This is why adults are more associated with primary forests.
Resilience to ]]>
Euterpe precatoria is a long lived forest palm, which makes it more resilient to the extinction and thinning processes associated with fragmentation. Palm populations within recently fragmented forests, such as Manú and FEP (12 years and 21 years respectively), may not demonstrate the full effects of fragmentation -i.e., decrease in adult density-. The adults at FEP denote a time-lag effect since this area has not yet begun to express fragmentation effects. This could be related to their larger size compared to Manú. Continued monitoring of the population ]]>
The apparent abundance of seedlings in relation to adult palms in the studied fragments suggests that E. precatoria seeds are being dispersed into these fragments from ]]>
et al. 2007). Beyond seedling input, preliminary processes related to fragmentation may occur. The low density and higher proportion of large juveniles and adults in forest fragments suggests that seedling recruitment rates have declined, and that mortality rates have probably increased. Preliminary data monitoring changes in canopy cover in our study fragments (using ]]>
E. precatoria seedlings under deep canopy cover show higher mortality rates and slower growth than those in forest fragments with greater canopy aperture. An increase in seedling predation or a decline in the number and quality of safe habitats (a characteristic of fragmented forests) could contribute to the reduced number of recruits. Without incoming seeds from outside sources, the effects of fragmentation and dense canopy conditions could be much more pronounced. The effects of forest fragments, such as the ones studied here, are combined with a previous history of extraction. ]]>
Changing traditional uses of E. precatoria: The preservation and incorporation of traditional resource use in conservation strategies is important for natural resource ]]>
E. precatoria extraction has arrived at a critical juncture. With the increased remoteness of palm populations, traditional practices (i.e., low intensity extraction done sparingly by communities themselves to satisfy religious purposes) are either ]]>
E. precatoria and the survival of the important cultural activity of palm harvesting are interdependent. Outside of national parks and protected areas, few alternatives exist to absorb extraction pressures. Conservation policies must consider programs to promote to moderate intensity extraction, such as cultivation in fragments owned by local communities, or even the introduction of alternative uses that ]]>
E. precatoria fruits, which have significant antioxidant capacity (Kang et al. 2012) and represent a major source of income for human communities in the Amazon basin (Stoian 2004, Macía et al. 2011).
Acknowledgments
The authors thank the Alpízar family at Finca El Progreso, and the staff of Manú Center for facilitating field work within these forest fragments. Students and staff of The School for Field Studies helped during fieldwork. The park rangers of Quebrada González (C. Mora, P. Ezeta-Salicetti and S. Barquero) and the staff of La Selva provided significant logistical support. M.F.O. was supported by the ]]>
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*Correspondencia a: Gerardo Avalos. Escuela de Biología, Universidad de Costa Rica, 2060 San Pedro, San José, Costa Rica. The School for Field Studies, Center for Sustainable Development Studies, 100 Cummings Center Suite 534-G, Beverly, Massachusetts 01915-6239; avalos@fieldstudies.org Mauricio Fernández Otárola. Escuela de Biología, Universidad de Costa Rica, 2060 San Pedro, San José, Costa Rica. Programa de Pós-graduação em Ecologia, Instituto de Biologia, Universidade Estadual de Campinas (Unicamp) 13083-970, CP 6109, Campinas, São Paulo, Brazil; maufero@gmail.com James Theodore Engeln. Macalester College, Saint Paul, MN 55105 USA; james.engeln@gmail.com 1. Escuela de Biología, Universidad de Costa Rica, 2060 San Pedro, San José, Costa Rica. 2. The School for Field Studies, Center for Sustainable Development Studies, 100 Cummings Center Suite 534-G, Beverly, Massachusetts 01915-6239; avalos@fieldstudies.org 3. Programa de Pós-graduação em Ecologia, Instituto de Biologia, Universidade Estadual de Campinas (Unicamp) 13083-970, CP 6109, Campinas, São Paulo, Brazil; Correspondence author: maufero@gmail.com 4. Macalester College, Saint Paul, MN 55105 USA; james.engeln@gmail.com
Received 04-VI-2012. Corrected 20-X-2012. Accepted 15-XI-2012.