Spatial distribution of Guaiacum sanctum (Zygophyllaceae) seedlings and saplings relative to canopy cover in Palo Verde National Park, Costa Rica Distribución espacial de Guaiacum sanctum (Zygophyllaceae) en relación con la cobertura de dosel en el Parque Nacional Palo Verde, Costa Rica
Eric J. Fuchs1*,2*, Tatiana Robles3* & James L. Hamrick1
The spatial distribution of individuals is a fundamental property of most species and constitutes essential information for the development of restoration and conservation strategies, especially for endangered plant species. In this paper we describe the spatial distribution of ]]>
Guaiacum sanctum and the effect of canopy cover on spatial aggregation. Adult G. sanctum were located and mapped in a 50ha plot in Palo Verde National Park, Costa Rica. Seedlings, saplings and juveniles were mapped to the nearest centimetre and permanently marked in three 50x50m subplots. Within each subplot spatial aggregation was assessed using Ripley’s K statistic and canopy opening readings were performed every 5m using a densitometer. Kriging spatial interpolation and Monte Carlo simulations ]]>
G. sanctum were spatially aggregated at all size classes with seedlings being the most frequent size class in all subplots. Seedlings were found predominantly in areas with significantly higher canopy cover. In contrast, juveniles were more likely found in areas with higher light availability. The high number of seedlings, saplings, and juveniles relative to adults suggests that populations of G. sanctum in PVNP are expanding. Light availability and ]]>
G. sanctum is dependent on forest gap dynamics and changes in human disturbance during the past 25 years.
Key words: gap dynamics, bird dispersal, microenvironment selection, desiccation avoidance.
Resumen
La distribución espacial es una característica fundamental de las especies y es importante para el desarrollo de estrategias de conservación y manejo. Aquí presentamos la distribución espacial de varias ]]>
Guaiacum sanctum, una especie en vías de extinción. Todos los adultos de G. sanctum se geo-referenciaron en una parcela de 50ha en el Parque Nacional Palo Verde. Las plántulas, los briznales y juveniles se mapearon en tres sub-parcelas de 50x50m. En cada sub-parcela se estimó la agregación espacial de los individuos mediante la K de Ripley. Observamos que los individuos de G. sanctum se ]]>
Palabras clave: dinámica de claros, ornitocoria, selección de microambientes, escape a la desecación.
Spatial distribution and patterning of plants is an important characteristic of communities and is a fundamental property of most species. Hutchinson (1953) determined that at least five causal factors shape the spatial pattern of plant species: 1) environmental factors such as nutrients or light availability, 2) reproductive factors including propagule dispersal and sea-sonality, 3) interspecific or social factors such as territoriality, predation and competition, 4) intraspecific components such as competition and density dependent factors and 5) stochastic variation in any of these causal factors. Evidence for ]]>
et al. 1999, Palmiotto et al. 2004), localized seed dispersal (Russo & Augspurger 2004) and density-dependent factors affecting spatial distribution have been previously determined for many tree species (Gilbert et al. 1994, Grau 2000, John et al. 2002, Lambers et al. 2002, Schupp 1992), with some ]]>
et al. 1997). Many authors have shown that most tropical tree species have aggregated spatial distributions (Armesto et al. 1986, Condit et al. 2000, He et al. 1997, Hubbell 1979, Okuda et al. 1997), generally attributed to a combination of dispersal limitation and micro-site ]]>
et al. (2000) showed that rare species are generally ]]>
Guaiacum sanctum (Zygophyllaceae) ]]>
Guaiacum sanctum was believed to cure syphilis (Voeks 2004). Therefore, most populations of G. sanctum were decimated ]]>
G. sanctum is distributed throughout the dry forests of the Northwest Pacific coast (Fuchs & Hamrick 2010a). Tropical dry forests are the most endangered biome in the Neotropics with less than 0.1% of its original cover remaining (Janzen 1988), and currently many sites suitable for G. sanctum populations have been transformed to agricultural fields or pastures. ]]>
G. sanctum in Costa Rica are rare, and generally restricted to national parks or reserves that continue to be menaced by habitat loss, fire or exploitation (Oldfield et al. 1998). Because of its restricted distribution and reduced population sizes, G. sanctum is now included in Appendix I of the CITES convention (CITES 2000) and is also termed “Endangered” in the World List of Threatened ]]>
et al. 1998).
Recent work on G. sanctum showed high levels of intra population genetic diversity and a lack of fine-scale genetic structure (Fuchs & Hamrick 2010b), congruent with high rates of seed dispersal and seed mixture from multiple maternal plants. Based on these results, we hypothesize a random spatial distribution of G. sanctum ]]>
et al. 1999, Okuda et al. 1997, Yamada & Suzuki 1997). In this study we described the ]]>
G. Sanctum in a dry forest from North-western Costa Rica. We also used spatial statistics to analyse the effect of light availability on regeneration and the spatial distribution of age classes of this endangered tropical tree.
Materials and Methods ]]>
Study site: This study was conducted within Palo Verde National Park (PVNP) in the lower Tempisque River basin on the Pacific lowlands of North-western Costa Rica (10°21’ N-85°21’ W). Upland portions of the 19 000ha park are mainly composed of dry tropical forest on limestone outcrops, with mean annual rainfall below 1 500mm and mean annual temperature of 30°C. The area is characterized by an extended dry season from December through April and a wet season from May to November. Palo Verde ]]>
Guaiacum sanctum in Costa Rica occurs on its dry limestone slopes. Soil type on these hills isof the Inceptisols order (lithic ustropept subgroup), which is a well-drained low fertility soil with a shallow calcic horizon (Vaughan et al. 1982).
]]>
Spatial distribution: In 2003, a 50ha plot (i.e. 1km x 500m) was created on the South-western slope of “Guayacan” hill in PVNP (Fig. 1). All adult G. sanctum within the plot were marked and mapped using a GPS and densities and spatial distribution of G. sanctum adults were determined. To determine the density and spatial distribution of seedling and juvenile
G. sanctum, three permanent 50x50m subplots were established in areas of high G. sanctum density within the 50ha plot (Fig. 1).
The three sub-plots have recent tree-falls (i.e. within 5-10 years) and hence vary in canopy structure. ]]>
G. sanctum were mapped to the nearest centimetre using tape measures and were marked with permanent aluminium or plastic tags. Height (h) and diameter at ground level (DGL) were determined for all individuals within the subplots; DBH was also measured for individuals with DBH>5cm. All data were collected during the wet season, between June and December 2004.
Individuals within ]]>
h<15cm), saplings (15<h<30cm), juveniles (30cm<h<2m), sub-adults (2<h<5m) and adults (h>5m). Height is used as a proxy for age, since no prior information exists on growth rates for this species. Size and height will be used ]]>
t) function (Ripley 1977). This function describes two-dimensional spatial distribution patterns. The K(t) function tallies the expected number of points that fall within a circle of radius t at any point in two-dimensional space based on the Poisson distribution. That is, K(t) shows the proportion of points that fall ]]>
t distance class. The L(t) square-root transformation of K(t):
]]>
is generally preferred since it linearizes the function and homogenizes confidence interval widths, which allows easier interpretation (Diggle 2003). Graphical representation of the L(t) function may be interpreted as follows: complete random distribution of points if L(t) does not deviate from ]]>
t)>0; and L(t)<0 suggests a regular distribution. For each subplot, we analyzed the spatial distribution of the three youngest size classes (juveniles and sub-adults were pooled due to a low number of individuals in the latter category) at 1m intervals, for t distances ranging from 1 to 25m (i.e. half the length of the subplot). Due to their low densities, the spatial pattern of adult trees was analyzed by means of Ripley’s K function using data for the entire 50ha plot.
We analyzed the spatial distribution between different size classes with Ripley’s second order analysis (Ripley 1976). This function describes the spatial relationship between two size classes (i.e. aggregated, random or repulsion). Categories are aggregated when individuals from different groups are found at closer distances than expected by random. Repulsion is the contrary effect, when individuals from different size classes ]]>
t) function. A 95% confidence envelope was created for all L(t) functions by means of 10 000 Monte Carlo simulations, where the position of individuals is randomly shifted in a toroidal plane. All calculations were performed using the SpatStat library in R (R Development Core Team ]]>
Canopy cover: To determine the effect of canopy cover on seedling and sapling abundances, we created a ]]>
G. sanctum individual in each subplot using this canopy cover map.
We compared the average canopy opening index of different size classes from those expected by a null distribution produced by re-sampling random points from each sub-plot. ]]>
Results
A total of 35 adults were marked within the 50ha plot (i.e. 0.7 adults per hectare;
Fig. 1.). Adults had an average DBH of 35cm (?8.2) with a skewed distribution towards lower diameters. Adults were spatially aggregated forming clumps of two to four individuals within »20m of one another (data not shown).
A total of 2 155 G. sanctum individuals were marked in the three sub-plots. Over 65% of these individuals belonged to the seed-ling category: saplings and juveniles ]]>
2=445.61, df=8, p<0.001; Fig. 2.) with juveniles being the most common size class in sub-plot three. Overall, the average seedling to adult ratio was 106.33 (?49.38). Sapling and juvenile to adult ratios were 35.5 (?6.22) and 43.9 (±20.56), respectively. There was a two-fold decline in the ]]>
Seedlings, saplings and juveniles were distinctly clumped (i.e. L(t)>0; Fig. 3.). Seedlings have the highest aggregation across all distances, and juveniles are more aggregated than saplings. The spatial distribution of saplings becomes ]]>
Fig. 3.). Across all subplots, seedlings, saplings and juveniles are always aggregated with each other (data not shown). Seedlings, saplings and juveniles are randomly distributed relative to adults, with seedlings showing sporadic departures from random (data not shown). Average distance to the nearest adult increases significantly with size (Fig. 4; F=159.73, ]]>
Seedlings tend to be found in areas ]]>
Fig. 5.); the COI for juveniles is 58.2% (±0.63). Sapling distribution in reference to light availability does not differ from random expectations (COI=49.1; Fig. 5). Overall, a positive relationship between size class and light availability is observed (Spearmans r=0.76, p<0.001), with larger size classes more common in areas with higher light availability. Average canopy opening ]]>
Discussion
Populations of G. sanctum in PVNP are characterized by highly skewed size distributions, with disproportionate numbers of young plants and few representatives in the ]]>
G. sanctum in PVNP is almost negligible (Jiménez 1993), both studies (OTS course and ]]>
G. sanctum were removed by logging. This could have impacted the reproductive success of the population, by reducing the number of individuals recruiting into younger size categories. Seedlings, saplings and juveniles are sensitive to fire, while adults and sub-adults are more resistant (Otterstrom
et al. 2006).
Seasonal fires tend to reduce the number of individuals in younger cohorts of climax tropical tree species, and repeated fires (i.e. within 15 years) increase local extinction probabilities of many climax tree species (Slik & Eichhorn 2003). Fires in Palo Verde are generally anthropogenic in origin, although lightning strikes occur infrequently. Most adults in ]]>
et al. (2006) showed that regeneration of G. sanctum is greatly increased in post-fire treatments. Additionally, sub-adults spared during logging may have become reproductive, increasing the number of progeny produced. Insufficient time had passed for new recruits to contribute ]]>
Spatial genetic ]]>
G. sanctum individuals in PVNP are spatially aggregated at all size classes, with more aggregation in the seedling category. Spatial aggregation may occur due to two non-mutually exclusive processes: localized seed dispersal (Howe & Smallwood 1982, Barot et al. 1999, Bleher & ]]>
et al. 1999, Silla et al. 2002, Souza & Martins 2004). Localized seed dispersal has been proposed as a major factor contributing to aggregated distributions, with evidence in animal and wind dispersed species (Nathan & Muller-Landau 2000, Greene et al. 2004). Howe (1989) defined bird ]]>
G. sanctum has ornithochorous fruits (Wendelken & Martin 1987), whose seeds are dispersed by a large array of frugivorous birds, the most common species observed actively foraging on G. sanctum were: Trogon melanocephalus, Trogon elegans, ]]>
Tityra semifasciata, Eumomotus momota, Pitangus sulphuratus and Calocitta formosa (EJF pers. obs). These birds generally swallow the entire seed, either during flight (i.e. Trogons) or while foraging at the tree (i.e. Tityras and Magpiejay’s), suggesting that most consumed seeds are dispersed away from maternal trees. In this population, the genetic relatedness of seedlings was independent of distance between individuals (i.e. no SGS, Fuchs & ]]>
et al. 2009).
However, G. sanctum individuals may still exhibit clumped or aggregated spatial distributions in the absence of SGS via contagious seed dispersal. Birds may become “clumped dispersers” (sensu Howe 1989) if they defecate or regurgitate seeds in ]]>
G. sanctum have conspicuous coloration and may move to areas with dense canopy cover to reduce predation risk, thus depositing seeds in closed canopy ]]>
A more likely explanation and congruent with previous genetic results, suggest that birds disperse seeds randomly and that preferential seedling germination occurs in specific spatially clumped microhabitats resulting in an aggregated distribution of seedlings. Seed germination and seedling establishment in tropical dry forests is often regulated by moisture and light (Gerhardt 1993, Ray & Brown 1995). Research conducted in tropical ]]>
G. sanctum. Although McLaren & McDonald (2003) showed that plants in high light environments produced more above ground biomass, this advantage could not overcome the increase in mortality caused by dehydration in these environments. Heterogeneity in the distribution of nutrients or suitable environments for germination may also generate spatially aggregated seedlings. Although we do not have information on ]]>
et al. 1982). Given the slope of the hill and precipitation regimes in PVNP, humidity is more likely to affect seedling recruitment than a patchy distribution of nutrients. Therefore we conclude that the high proportion of G. sanctum seedlings in shaded environments, which results in an aggregated distribution, is the result of greater recruitment in more mesic microhabitats. Clumped distributions arise through the combined effects ]]>
Juvenile and adult G. sanctum are randomly distributed relative to each other, nonetheless, the average distance between adults and juveniles is significantly higher than ]]>
et al. 1986, Condit et al. 1992, Itoh et al. 1997, Okuda et al. 1997). Density dependent mortality (Grau 2000) and selection for specific environments (Itoh et al. 2003) have been proposed as the predominant explanations for repulsion between these two size categories. A large proportion of ]]>
G. sanctum seedlings or juveniles. Also, our spatial analysis shows that seedlings, saplings and juveniles are randomly distributed relative to adults with no signs of repulsion, suggesting that areas suitable for germination, establishment and growth, are randomly dispersed relative to adults. ]]>
The distribution of juveniles indicates that light availability shapes the spatial distribution of older size categories. Juveniles were predominantly found in areas with ]]>
G. sanctum adults. Therefore, suitable sites for growth may only become available during gap formation. Delayed ]]>
Hymenaea courbaril and Swietenia macrophylla, increased light availability was negatively correlated with dry season survival. Nonetheless, higher irradiance associated with canopy openings were positively correlated with high growth rates. ]]>
G. sanctum seedlings are established in shaded areas, they are able to develop root systems that access moisture in deeper soil strata, allowing them a more desiccation resistance. Canopy openings caused by tree falls provide juveniles with increased light regimes, which translate into higher growth rates. These gaps not only allow increased photosynthetic activity, but also signal the availability of space for saplings and juveniles to grow into the sub-adult and adult categories. As mentioned previously, all ]]>
In conclusion, populations of G. sanctum in PVNP appear to be expanding due to the large number of seedlings, saplings and juveniles observed. Spatial patterns observed ]]>
G. sanctum is dependent on forest gap dynamics which has direct implications for its conservation. Endangered species require detailed descriptions of their life history, so that well suited management and conservation strategies can be devised to insure their future survival.
Acknowledgments
The authors thank C. Alvarado and U. Chavarria from ACAT, C. Deen and D. Trapnell for laboratory assistance, G. Barrantes for bird identification, and P. Smouse and E. Gonzales for statistical support. Special thanks to J. Ross-Ibarra and M. Poelchau for improving previous versions of this manuscript. This work was supported by IdeaWild, Vicerrectoría de Investigación-UCR, Organization for Tropical Studies to EJF and ]]>
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*Correspondencia a Eric J. Fuchs. Plant Biology Dept. University of Georgia, Athens, GA. 30602, USA; Escuela de Biología, Universidad de Costa Rica, 2060 San José, Costa Rica; e.j.fuchs@gmail.com, eric.fuchs@ucr.ac.cr Tatiana Robles. Escuela de Ciencias de la Educación, Universidad Estatal a Distancia, San José, Costa Rica; ttrobles@gmail.com James L. Hamrick. Plant Biology Dept. University of Georgia, Athens, GA. 30602, USA; hamrick@plantbio.uga.ed 1. Plant Biology Dept. University of Georgia, Athens, GA. 30602, USA; hamrick@plantbio.uga.ed 2. Escuela de Biología, Universidad de Costa Rica, 2060 San José, Costa Rica; e.j.fuchs@gmail.com, eric.fuchs@ucr.ac.cr 3. Escuela de Ciencias de la Educación, Universidad Estatal a Distancia, San José, Costa Rica; ttrobles@gmail.com
Received 14-VI-2012. Corrected 30-X-2012. Accepted 19-XI-2012.
