Understanding small-scale disturbances in Guayana’s montane : gap characteriZation in the ,

Cristabel Durán Rangel, Albert Reif and Lionel Hernández

Summary

This case study describes the structure of gaps in a montane Gap formation resulted in a loss to the basal area and volume of in Sierra de Lema, Bolivar State, Venezuela. The sizes of the stand of ~5.8 and ~0.5%, respectively. Canopy gaps occupied the gaps were measured in the forest canopy (canopy gaps) and 1.4% of the forest area, which is in the range reported for tropi- at ground level (extended gaps), and the corresponding micro- cal forests. The microhabitat ‘undisturbed ground’ accounted for habitats assessed. The trees involved in the formation of gaps the largest area within the gaps. The predominance of uproot- were recorded, and their basal areas and volumes calculated. A ing as a cause of gap formation in the forests of the Sierra de distinction was made between gap makers and those trees that Lema was probably due to the superficial rooting of the trees. were brought down by gap makers. The mode of fall was record- The larger gap area is explained by the frequent occurrence of ed for all fallen trees. The main gap formation mode was the up- multiple tree-falls. From the large gap sizes and the high pro- rooting of trees, bringing about multiple tree-falls. The gap sizes portion of undisturbed ground in the gaps, high survival rates of observed (canopy gaps: 31-896m², extended gaps: 83-1235m²) advanced regeneration, and of numerous new maidens of pioneer were 30-90% larger than those reported for most tropical forests. species, might reasonably be expected.

he Guayana forests rep- The forests of the Sierra ing of permanent plots established in the resent ~90% of the Ven- de Lema, a located in the forests as part of a long-term study of ezuelan forest area and eastern part of Venezuelan Guayana and tropical forest dynamics. At present, this are part of the Guayana Shield. About in the upper Caroní river basin, are rela- is the only ecological research being car- 60% of the species present in Vene- tively unknown from either a botanical or ried out in the montane forest area of the zuela (15500 species) can be found in the an ecological perspective (Huber, 1995; Guayana Shield (Hernández and Castella- Guayana Shield (Llamozas et al., 2003). Hernández and Ortíz, 2004). To date nos, 2006). The study of the structure of Around 22% of the vascular are there have been several botanical expedi- forest gaps (openings in the canopy ex- endemic (native to a geographic region) tions to the area (Sanoja, 2009), but there tending down through the forest under- to Venezuelan Guayana (Berry et al., are many areas within these forests that story) presented in this paper was carried 1995). In addition to the huge biodiver- have not been visited thus far and it is out within the framework of this research sity of the region, these forests are also likely that there are numerous plant spe- project. important because of the environmental cies that have not yet been reported, The forests of the Sierra de Lema services they provide, specially logging some of which might not yet have been have not been cleared and are almost in- and the generation of , described at all. The ecology of the Sier- tact (Duellman, 1997; Huber meeting ~70% of the country’s electricity ra de Lema forests has only been studied et al., 2000; Blanco, 2001). The forests of demand (Belvilacqua et al., 2002). over the last decade, through the monitor- the study area have been classified as

Keywords / Gap Formation / Gap Structure / Guayana / Sierra De Lema / Small-Scale Disturbance / Tropical Forest / Venezuela / Received: 06/16/2010. Modified: 03/15/2011. Accepted: 03/18/2011.

Cristabel Durán Rangel. Forest Engineer, Universidad de los Andes (ULA), Venezuela. Doc- toral student in Natural Sciences, University of Freiburg, Germany. Researcher, Universidad Nacional Experimental de Guayana (UNEG), Venezuela. Address: Tennenbacher Str. 4, 79104 Freiburg, Germany. e-mail: [email protected] Albert Reif. Biologist, University of Wuerzburg, Germany. Ph.D. in Natural Sciences, Univer- sity of Bayreuth, Germany. Professor, University of Freiburg, Germany. Lionel Hernández. Forest Engineer, ULA, Venezuela. Ph.D. in Forest Sciences, Goettingen University, Germany. Professor, UNEG, Venezuela.

272 0378-1844/11/04/272-09 $ 3.00/0 APR 2011, VOL. 36 Nº 4 ‘very humid submontane forest’ (Ewel and Madriz, 1968; Holdridge et al., 1971). The main canopy of the stands reaches 20- 25m, with emergent trees over 40m in height. Zona en These forests are charac- reclamación terized by moss-covered tree trunks, abundant epi- phytic and semi-epiphytic plants, fern trees (Cy- atheaceae) and palms of the species Geonoma in- terrupta and Prestoea tenuiramosa. The most Figure 1. The location of the study area, the Sierra de Lema forests of La Escalera, Bolívar State, Venezuela, is depicted on the left. The inventoried area is shown to the right. Dark grey bars correspond to transects inventoried diverse tree families are in 2005 and the light grey bars the transects inventoried in 2006. Lauraceae, Clusiaceae, Rubiaceae, Sapotaceae, Melastomataceae, Myrtaceae, Moraceae, py remains closed. Gaps create mosaics opening in the canopy) fall? Do second- Burseraceae, Chrysobalanaceae and Eu- and gradients of light (Sanford et al., ary gap trees (non-gap maker trees that phorbiaceae (Sanoja, 2009). The most fre- 1986), and change forest microclimate also become involved in gap formation) quent tree species are Licania intrapetio- and structure (van Dam, 2001). Differ- fall in the same direction? Do thinner laris, Sextonia rubra, Micropholis specta- ences in gap sizes, gap shapes and trees tend to snap, whereas larger diame- bilis, Eschweilera sp. and Protium spp. modes of gap formation result in gap ter trees are uprooted? Are gap maker (Durán, 2001; Hernández and Castella- heterogeneity and microclimate variabil- trees larger in diameter than secondary nos, 2006). These forests have a large ity (van der Meer and Bongers, 1996a; gap trees? Are gap sizes correlated with proportion of endemic plants (Picón, van Eysenrode et al., 1998; Brokaw and the dimensions (diameter and height) of 1994), with ~13% endemic tree species Busing, 2000; Carvalho et al., 2000). the fallen trees? What are the spatial pro- (Sanoja, 2009). Light, temperature, radiation and wind portions of the different microhabitats oc- The high diversity lev- speed all increase in gaps, and relative curring in gaps? What is the range of els present in tropical forests have been humidity decreases (Swaine and Whit- variation in gap sizes? What gap shapes partially explained by the regeneration more, 1988; van Dam, 2001). Nutrient occur? To what degree are the basal area niche hypothesis (Grubb, 1977), which cycling processes are altered (van Dam, and volume of the forest stand reduced states that plant species coexist by oc- 2001). The size of a gap influences the by gap formation? What proportion of the cupying different habitats (Denslow, extent of the change of the spatial mosa- study area is covered by gaps? 1987; Brokaw and Busing, 2000). How- ic and, therefore, the floristic composi- ever, the hypothesis of functional tion of the next successional phase Methods equivalence (Hubbell, 2005) states that, (Whitmore, 1989). Gap shape influences specially in the case of species-rich the penetration of light into gaps (van Study area tropical vegetation, many species over- Eysenrode et al., 1998). Long gaps have lap in terms of their functions within a lower overall area exposed to direct The forests of the Sier- the , and the species that are sunshine than round gaps. Finally, infor- ra de Lema cover a continuous area of present and those that are regenerating mation about total gap areas and their more than 1000km2, and have an altitu- relate to their dispersal and recruitment size distribution is useful for comparing dinal distribution ranging from 150 to limitations. Natural forests can be re- ecosystems (Denslow, 1987). A knowl- 1490masl (Hernández and Castellanos, garded as being a mosaic of structural edge of these structural characteristics 2006; Sanoja, 2009; Figure 1). The Si- patches (Whitmore, 1989) of develop- of gaps is needed (Kapos et al., 1990) erra de Lema comprises an igneous- ing, developed and decaying phases. for many ecosystems. These gap charac- metamorphic basement, sedimentary This successional process is initiated teristics have not yet been researched in rocks of the Group of the Pre- after damage occurs to a part of the the forests of the Sierra de Lema or of cambrian Age, and diabase intrusions of stand, creating a forest patch (Hallé et the Caroní basin. Forest gap studies and the Mesozoic (Huber, 1995). The study al., 1978; Oldeman, 1983; Whitmore, forest dynamics research and monitoring area (53.5ha) is situated on a 1988). Gaps, which correspond to the will contribute to the understanding of that is deeply rived by small gullies. first years of the developing phase, are hydrological cycles in the Caroní basin. The soils are character- created in natural forests by small scale The structure of gaps ized by a low nutrient content, low pH disturbances; e.g., the fall of branches, present in a 53.5ha site in the high Sierra in KCl of 4.6-5.3 and low cation ex- crowns, or single or multiple trees de Lema forests was characterized in this change capacity (Durán, 2001) and are (Brandani et al., 1988). Gaps in tropical case study; the aim was to provide a de- deeply weathered. Most derive from sed- forests create a variety of microclimatic scription of the patterns of gap formation, imentary rocks, and a few from diabase niches and microhabitats for species gap structure and changes in the struc- outcrops. The latter soils are more fertile (Brown, 1993). ture of these forests caused by the forma- (Dezzeo and Foelster, 1994; Huber, The environmental con- tion of gaps. The questions specifically 1995). The rooting of the vegetation of ditions in the stand after gap formation asked were: How are gaps created? In the region is only superficial, down to differ considerably to those present in which direction do the gap maker trees just 30cm in the mineral soil (Foelster et the understory of areas where the cano- (those trees that fall and so create the al., 2001).

APR 2011, VOL. 36 Nº 4 273 A very humid premon- tane climate predominates across the study area (Ewel and Madriz, 1968; Holdridge et al., 1971), with a mean an- nual temperature ranging 18-24°C (Hernández and Castellanos, 2006). Mean annual precipitation is ~4800mm (data for 1988-2004, from CVG-EDELCA cli- mate station, at 1412masl, ~20km from the study area).

Structural characterization of the gaps

The study was carried out at ~1430masl, in the ‘very humid Figure 2. Illustration of the canopy and extended gap measurements, and of the 5m bor- submontane’ (Holdridge et al., 1971) for- der zone. ests of the Sierra de Lema. A total of 50 gaps met the gap definition criteria (see Gap maker trees and breviations in parentheses) were distin- below) and were inventoried over an secondary gap trees with a diameter guished at ground level: fallen crown area of 53.5ha over the course of two >10cm (measured at 1.3m from the base (crown), fallen large branch with diameter field campaigns. In 2005, an area of of the broken trunk of fallen trees) were <20cm (branches), lying large trunk with 25ha was delimited in eleven transects considered. Each was classified according diameter ≥20cm (trunk), and undisturbed separated by a distance of 50m (nine to one of the following categories: up- ground (undisturbed). The undisturbed for- transects of 50×500m and two transects rooted tree, tree snapped at the base, tree est floor area of the closed forest adjacent 25×500m; Figure 1), and all of the gaps snapped above the base, crown fall, and to the gap (border) was classified as a non- found there were inventoried. As most of branch fall (van der Meer and Bongers, gap microhabitat. The border was defined the gaps were located on plateaux, for 1996b). The fall direction of the gap as a 5m wide zone stretching from the the purposes of a subsequent tree regen- maker and any secondary trees were edge of the extended gap into the adjacent eration study only those gaps on a pla- measured (azimuth in degrees). The di- forest (Figure 2). Although the border zone teau were considered in the next field ameters of all fallen trees were recorded does not belong to the actual gap, it is in- campaign. In 2006, the areas between and their basal areas calculated. The fluenced by the physical and climatic condi- the transects (25ha) and an adjacent area length and width of fallen crowns were tions within the gap. Several environmental (3.5ha) were inventoried. Gaps were de- measured and, using the formula to cal- factors influencing the establishment and fined and measured (Figure 2) at the culate the area of an ellipse, the area of growth of tree regeneration (Poorter, 2002) canopy level (canopy gap) and the the crown projection onto the ground (re- may differ between the various gap zones ground level (extended gap). A canopy ferred to subsequently as the crown area) (Núñez-Farfán and Dirzo, 1988). For in- gap was defined using the gap definition was calculated. stance, plant growth in forest gaps on tier- developed by Brokaw (1982), namely as The perimeter of each ra firme near San Carlos de Río Negro, “a hole in the forest extending through gap (canopy and extended gap) was identi- Venezuelan Amazon, was found to be in- all levels down to an average height of fied on the ground, drawn in a scaled fluenced by microhabitats (Uhl et al., 1988). two meters above ground.” The extended sketch and digitized. Gap area was calcu- The microhabitats were illustrated in the gap was defined as “the ground area un- lated using ArcGIS 9.1 (ESRI Inc., 1999- sketch and their areas were calculated. der a canopy opening that extends to the 2005). An index was developed and ap- bases of the canopy trees surrounding plied to characterize the breadth of each Proportion of the gap area the canopy opening” (Runkle, 1981). For gap: both gap definitions three criteria were The magnitude of gap applied: 70% of the ground vegetation BI = L / ((wc + w1 + w2) / 3), disturbances on the forest stand was as- had to be <2m in height; the gap area sessed using three indicators: the basal 2 had to be >16m and the gap diameter where BI: gap breadth index; L: longest area of the fallen trees in gaps, their had to be >4m. As the formation of a axis through the gap; wc: width of the deadwood volume, and the proportion of gap might not disturb all of the existing gap, measured perpendicular to the main the study area covered by gaps as a per- vegetation completely (some trees may axis at the midpoint; w1 and w2: widths centage. The total volume of a downed remain standing), the first criterion en- measured perpendicular to the main axis stem, which comprised the stem section sured the consideration of several gaps midway between the midpoint and the from the base to the crown onset, was that might not have been comprised two ends of the main axis. BI = 0 means calculated by the following regression solely of vegetation <2m in height. The that the breadth of the gap is similar in formula developed for trees of Venezue- last two criteria where applied in order each direction; i.e., an almost circular lan forests (Konrad, 1990): to avoid the inclusion of overly small shape. The narrower the gap, the higher v= d² × (0.39682 + 0.46013 × h) forest gaps that are partially closed by the index value. the branches of adjacent trees. The ex- As the ground level envi- where v: volumen of the fallen tree stem tended gaps were only measured in 2006 ronment of a gap is heterogeneous (Rick- (m3), d: diameter (m), and h: length of the after refinements were made to the gap lefs, 1977; Brown, 1996), which was sug- tree stem (m). The results for all of the mea- definition used on the basis of field ob- gested to be a reason for the huge species sured stems were then added for each gap. servations from the first year of data diversity in the tropics (Ricklefs, 1977), in The proportion of the study area collection. each gap the following microhabitats (ab- that was occupied by canopy gaps was

274 APR 2011, VOL. 36 Nº 4 calculated only for the A simple linear first field campaign model was fitted with (25ha), where all of the the canopy gap area as gaps occurring were in- the independent vari- ventoried. The areas of able and the extended all of the canopy gaps gap area as the depen- present within the 25ha dent. This formula was were added up, and used to estimate the ex- their proportion relative tended gap areas for to the total area of those gaps not mea- 25ha was calculated. sured in the field. In As the extended gap order to meet the nor- area was not measured mality assumption of for gaps during the first the linear regression, field campaign, these the original data was areas were calculated square root trans- by means of a regres- Figure 3. Orientation of the fallen trees (diameter >10cm). Numbers next to formed. sion equation derived the shaded areas indicate the number of trees with a fall-orientation corre- All statistical using the areas of the sponding to the particular azimuth section (e.g., 30-60°). a: gap maker trees, analyses were con- canopy gaps and their b: secondary gap trees. ducted using R ver- corresponding extended sion 2.10.1 for Win- gaps measured in the dows (R Development second campaign in 2006. The relative were not normally distributed, further Core Team, 2008). proportion of the 25ha occupied by ex- analysis of the data relied on non-para- tended gaps was then calculated also. metric tests. The Wilcoxon rank sum test Results was applied to determine whether the Statistical analysis medians of the data sets stemmed from Gap formation similar populations. Spearman’s rank cor- The normality of the distributions relation was used to analyze the relation- The main mode of gap formation of the variables studied was checked us- ships between variables (Hartung et al., was the fall of uprooted trees (51%), fol- ing the Shapiro-Wilk test. As the values 1986). lowed by the snapping of trees at the base (29%). Only 9% of Table I the gap maker trees Range, mean, median and standard deviation of several parameters snapped above the base, measured in the gaps in the Sierra de Lema and crown and branch fall caused 2% and 9% of the Range Mean Median sd Shapiro test gaps, respectively. In most Diameter of uprooted trees (cm) 10 - 110 30.95 25 19.92 W= 0.84*** a gaps several trees were Diameter of snapped trees (cm) 10 - 120 31.87 24.5 20.98 W= 0.81 ***a pulled down by an adja- Diameter of gap maker trees (cm) 11.59 - 120 58.80 58.57 21.92 W= 0.95 ns b cent gap maker, to which Diameter of secondary gap trees (cm) 10 - 56.34 24.21 22.92 10.05 W= 0.92 ***c they were frequently con- Correlation of canopy gap sizes with total - - - W= 0.76 *** nected by lianas, an exam- number of trees (m²) ple of the so called ‘domi- Total number of trees& - - - W= 0.82 *** no effect’ (van der Meer and Bongers, 1996b). Most Correlation of canopy gap area with total - - - W= 0.77 *** basal area& (m²) of the fallen trees present Total basal area& (m²) - - - W= 0.93 ns in the gaps lay in a north- easterly direction (Figure Correlation of canopy gap sizes with total - - - W= 0.96 ns crown areas& (m²) 3). The majority of the gap maker and secondary trees Total crown area& (m²) - - - W= 0.80 * were oriented in the range Canopy gap sizes (m²) 31 - 896 207.12 179.5 146.65 - 0-120° and 30-120° azi- Correlation of total canopy gap sizes with 31 - 896 235.23 184 186.16 W= 0.77 *** muth, respectively. extended canopy sizes (m²) No signif- Extended canopy gap sizes (m²) 83 - 1235 422 377 268 W= 0.87 * icant difference in the di- Gap shape index 1.51 - 5.62 2.93 2.86 1.13 - ameter of fallen trees was Correlation of square root of total canopy - - - W= 0.93 ns found in relation to the gap sizes with extended gap sizes (m²) mode of tree fall (Table I). Square root of extended gap areas (m²) - - - W= 0.96 ns The diameters of uprooted Number of secondary gap trees in the Si- 1 - 16 6.72 5 4.7 W= 0.91 ns d and snapped trees did not erra de Lema differ significantly. A total Number of secondary gap trees in Carlos 1 - 4 1.67 1 0.90 W= 0.74 ***e of 186 fallen trees were Botehlo National Park measured, 18% of which were gap maker trees and .&: per gap; sd: standard deviation; ns: p>0.05, *: p<0.05, **: p<0.01, ***: p<0.001. Different letters indicate sig- nificant differences between rank sums. Wilcoxon rank sums were a: W= 2512; ns, b and c: W= 4697.5***; d and 82% were secondary gap e: W= 239***. trees. The diameters of

APR 2011, VOL. 36 Nº 4 275 Gap structure Discussion

The sizes of the canopy gaps Modes of gap formation ranged from 31 to 89 m². About 85% of the gaps were 50 to 350m² in size The observation of up- (Figure 4, Table I). The extended rooting as the main mode of gap for- gap areas ranged from 83 to 1235m². mation in the study area coincided The canopy gaps were 15-70% small- with the findings for Counami (Colson er than their corresponding extended et al., 2006) and Nouragues (van der gaps (Figure 5a), and their areas Meer and Bongers, 1996b) in French were highly correlated (Figure 5b). Guiana, for La Selva (Brandani et al., The gaps varied in breadth, from 1988) and Cordillera de Tilarán (Law- broad to narrow. The majority of the ton and Putz, 1988) in Costa Rica, and gaps were broad (BI = 0.2-3.5). Christmas Island in the Indian Ocean The proportions of (Green, 1996). the various microhabitat areas The predominance of within a gap varied greatly be- uprooting as a cause of gap formation tween gaps. Undisturbed ground in the forests of the Sierra de Lema covered the largest combined area was probably due to the superficial (4442.71m²), whereas fallen crowns, rooting. The soils of the study region large trunks and large branches ex- have a humus layer with a dense root Figure 4. Frequency of canopy gaps per gap size hibited smaller total areas (1601.77, mat and high humus content. The fine class (areas in m2). 2435.28 and 1610.99m², respective- root (<2mm diameter) systems in the ly). The border area, identified as a soils of the region are superficial due non-gap microhabitat, covered to the acidity combined with a Ca de- gap maker trees and secondary gap trees about twice the area classed as undis- ficiency and high Al3+ concentration did differ significantly, however. Those turbed ground (12008.74m²). (Dezzeo et al., 2004; Dezzeo and trees causing gaps had significantly larg- Foelster, 1994; Foelster, 1986; Foelster er diameters than those that were either Magnitude of gap disturbances et al., 2001). There are as yet no esti- pushed or pulled down by the gap mak- mates for thicker roots (>2mm diame- er. Gap makers with larger diameters The loss of tree basal ter) and their depths in the region, but also created bigger gaps; and the more area in the forests of the Sierra de shallow rooting (Priess and Foelster, fallen trees, the greater the gap size. Lema due to gap formation ranged be- 1994) and shallow soils (<50cm depth; Gap size was positively, but only weak- tween 2.4 and 2.7m²·ha-1, corresponding Dezzeo et al., 2004) have been report- ly, correlated with the total number of to a trunk deadwood volume of be- ed. Similar relationships between soil fallen trees (Spearman’s rank correlation tween nearly 0 and 19.75m²·ha-1 (mean= infertility, superficial rooting and gap S= 1847.163, p= 0.002, rho= 0.5) and 4.86m²·ha-1). The area of the 25ha sub- creation caused by the uprooting of their total basal area (S= 1374.693, p= plot covered by the canopy and extend- trees have also been reported for oth- 4.375e-06, rho= 0.7), but was not corre- ed gaps amounted to 3558 and er tropical forests (Jans et al., 1993; lated with their total crown area (n= 10, 7550.75m², respectively, corresponding van der Meer and Bongers, 1996b; S= 76, p= 0.1133, rho= 0.5). 1.4 and 3.7% of the subplot area. Gale and Barfod, 1999). The most plausible explanation for the direction of tree fall is the wind direction. The prevailing wind direction recorded at the nearest mete- orological station (EDELCA, at Paru- pa) coincides roughly (70-130°) with the direction of the fall of gap maker and secondary gap trees.

Modes of tree fall in gaps in the Sierra de Lema

The gap maker trees were found to be thicker than the second- ary gap trees. The high proportion of secondary gap trees that were smaller than the neighboring gap maker indi- cates that these are not strong enough to withstand the downward push of the larger gap makers, or the downward pull in the case of second- Figure 5. a: sizes of canopy and extended gaps (n=21). Each box contains 50% of the respective gap areas. Horizontal line: median value, whiskers: maximum und minimum gap area values, unless outli- ary trees attached to a gap maker by ers (black dots) are present, different letters indicate significant differences between gap areas. b: rela- lianas (domino effect). The shallow tionship between canopy and extended gap areas. Spearman’s rank correlation S= 127.0825, p<0.001, root systems of the trees may also rho: coefficient. In the formula y: extended gap area, and x:canopy gap area (n = 21). play a role.

276 APR 2011, VOL. 36 Nº 4 Around 80% of the fallen trees er (Table I) than in gaps in the latter and the tree volume determined for a in the gaps of the Sierra de Lema National Park. This highlights the role forest stand located close to the study were pushed down by a single large played by the domino effect in gap area, at about the same altitude (97m³ gap maker tree. Each gap maker often formation in the forests of the Sierra per 0.1ha, trees with diameters ≥10cm; pulled down several adjacent smaller de Lema. Hans Georg, Karsten Heyn and Lionel trees. This underlines the importance The large gap sizes Hernández, personal communication). of shallow tree rooting and lianas in were not explained by tree height. The Gap formation resulted in a loss of the context of disturbance patterns in literature consulted (see Table II) re- ~5.7% of the basal area per ha. This the region. The results of a study car- vealed that the canopies of other for- finding was based on basal areas as- ried out in Nouragues, French Guiana, ests studied have heights similar to certained for two 1ha reference plots also showed that the diameters of the those of the fallen trees in the gaps in within the study area and the gap fre- trees initiating forest disturbances the Sierra de Lema, but often the quency value obtained (basal areas: 41 were significantly larger than those of emergent trees found elsewhere are and 46m²·ha-1 for trees with diameter secondary gap trees (van der Meer much taller than those in Sierra de ≥10cm; basal area data provided by and Bongers, 1996b) and consequently Lema (the longest fallen tree measured Litzinia Aguirre, Carolina González it could be assumed for these forests in a gap had a length of 38.5m, and Elio Sanoja, personal communica- that tree size is a determinant of can- whereas examples from the literature tion). It is, therefore, important that opy disturbance (Jansen et al., 2008). refer to emergent trees with lengths these gap creation events be consid- The positive relationship between the >50m). In spite of this, most gaps in ered when studying changes to forest number of trees involved in gap for- the study area were larger than the av- structure. mation with gap sizes also agrees erage gap sizes observed in tropical It was expected that with the pattern found in other tropi- forests with similar canopy heights the area of canopy gaps relative to the cal forests (Lawton and Putz, 1988; and taller emergent trees. entire forest area would be larger, the Jans et al., 1993; Arévalo and Fernán- From the large gap reason for this being that the gaps in dez-Palacios, 1998; Ferreira de Lima sizes and their broad shapes, charac- the study area are large compared to and Cunha de Moura, 2008; Jansen et teristics allowing for the high avail- those found in other tropical forests al., 2008). ability of direct light within the gaps, (considering that all used the same the potential for the abundant regener- gap definition). Nevertheless, the total Gap size, breadth and regeneration ation of pioneer species exists, and gap area derived for the study area in potential also that of species characteristic of the Sierra de Lema is in the range the subsequent successional phase. (0.2-6.3%) reported for tropical forests The average gap size However, this potential for the regen- (Table II). An explanation for this indicated that gaps in the Sierra de eration of pioneer woody species is could be the low frequency of gaps in Lema are amongst the largest natural suppressed in part by the presence of the Sierra de Lema (1.1 gaps/ha) com- gaps recorded in tropical forests (Ta- considerable quantities of advanced re- pared to other areas (Table II), such ble II), exhibiting sizes similar to generation in the gaps. Around 44% of as the Ivory Coast (16.9 gaps/ha), those recorded in Nouragues, French the total gap area was categorized as which has the highest reported fre- Guiana (van der Meer and Bongers, undisturbed ground. Here the vegeta- quency. In order to better compare 1996b), Río Hoja Blanca, Ecuador tion was not damaged in the process different forests, larger study areas (Gale, 2000) and on Christmas Island of gap formation, meaning that the ad- are necessary. Some of the sites stud- (Green, 1996). vanced regeneration remained intact ied to date were too small (1.2 and These large gap areas (Uhl et al., 1988; van der Meer et al., 5ha; Lang and Knight, 1983; Lawton in the forests of the Sierra de Lema 1998; Poorter, 2002; Ferreira de Lima and Putz, 1988; Jans et al., 1993). may be explained by the large number and Cunha de Moura, 2008). Replications are also required within of trees that fall during a gap creation Also, if it is assumed each region studied, as it has been event (domino effect, Table II) and that microhabitats in gaps differ with shown that gap frequency is not con- also by the occasional occurrence of respect to the prevailing environmen- sistent even within a particular region heavy windstorms (Foster and Ter- tal conditions and, therefore, in how (Kapos et al., 1990). borgh, 1998; Nelson et al., 1994). Un- they determine patterns of tree regen- fortunately, there is no meteorological eration, as a function of the adaptation Conclusions information for wind speeds in the Si- of different species to these microhab- erra de Lema, but wind speed tends itats (Ricklefs, 1977), then a distinc- This study represents to increase at higher altitudes (Este- tive tree species regeneration or even the first recording of gaps across a ban Perdomo, personal communica- species assemblages in the different large forest area in either Venezuela tion). The frequency of the domino microhabitats within gaps would be or the mountain areas of the Guayana effect documented for tropical forests expected. Shield. Some of the characteristics of cited in the relevant literature (Table gap formation observed in the Sierra II) was in all cases <30%, with an ex- Effects of gap disturbances on forest de Lema, such as the large gap sizes ception being the Carlos Botelho State stands and the high frequency of multiple Park, , at 63% (Ferreira de tree falls, were clearly distinct from Lima and Cunha de Moura, 2008). The loss of tree vol- the patterns of gap formation docu- Even though the frequency of the ume caused by gap formation in the mented for other tropical forests situ- domino effect in the Sierra de Lema study area was equivalent to a mean ated on fertile soils, such as Barro was only slightly higher (70%), the 0.5% of the stand volume per ha, cal- Colorado Island in Panama, La Selva number of secondary trees involved in culated on the basis of the gap fre- in Costa Rica and in Ecuador (soils of each gap event was significantly high- quency derived in this study (Table II) volcanic origin). Further studies of

APR 2011, VOL. 36 Nº 4 277 Table II Gap sizes and frequencies in tropical forests

Range Mean Location of research area, Measr. Gap area Freq. Canopy h Emergent Domino country (reference) gap size gap size h (m) (m²) (m²) in forest (%) (gaps/ha) (m) tree h (m) effect La Selva, Costa Rica (Brandani et al., 1988) 25 - 1273 144 “few” La Selva, Costa Rica (Ostertag 1998) 2 9 - 154 65 La Selva, Costa Rica (Sanford et al., 1986) 5 40 - 781 161 6.3 2.1 30 - 40 55 “few” Monte Verde, Costa Rica (Lawton and Putz, 1988) 3 4 - 135 1.4 5 - 23 Barro Colorado Island, Panama (Dalling et al., 5 25 - 125 33 11% 1998) Barro Colorado Island, Panama (Hubbell et al., 5 25 - 1550 1999) Barro Colorado Island, Panama (Brokaw, 1982) 2 85 Barro Colorado Island, Panama (Lang and Knight, 2 3.8 8.7 20 - 25 35 1983) Carlos Botelho State Park, Brazil (Ferreira de Lima 2 6 - 227 56 63% and Cunha de Moura, 2008) Santa Genebra County Reserve (Venâncio Martins 2 20 - 468 126 20% and Ribeiro Rodrigues, 2002) Río Sumino, Ecuador (Kapos et al., 1990) 2 10 1.4 Río Quilla Pacay, Ecuador (Kapos et al., 1990) 2 15 5.1 Río Hoja Blanca, Ecuador (Gale, 2000) 2 50 - 1100 206 0.2 5.3 31 55 3% Counami, French Guiana (Colson et al., 2006) 2 56 - 991 359 30 55 Nouragues, French Guiana (van der Meer and 2 4 -100 26 0.2 8.5 24 60 25% Bongers, 1996a) Four tropical forests: La Selva, Barro Colorado 2 20 - 490 140 Island, Cocha Caschu, Peru, and km 41 close to Manaos, Brazil (Poorter, 2002) Anaga Natural Park, Tenerife, Canary Islands 2 17 - 125 41 10 – 20 (Arévalo and Fernández-Palacios, 1998) Christmas Island, Indian Ocean (Green, 1996) 3 17 - 700 169 40 “few” Täi, Täi National Park, Ivory Coast (Poorter et al., 2 11 - 204 42 0.8 16.9 55 25% 1994) Para, Täi National Park, Ivory Coast (Poorter et al., 2 11 - 244 44 0.8 16.9 55 30% 1994) Zagné, Täi National Park, Ivory Coast (Poorter et 2 11 - 231 36 0.8 16.9 55 33% al., 1994) Sierra de Lema, Venezuela (this study) 2 31 - 896 296+ 1.4 1.1 22 $ 39 § 70%

The gap areas referred to the canopy level. h: height; Measr. h: height above the ground (m) at which the gap area was measured; Domino effect: frequency of gap events with a corresponding occurrence of the domino effect (“few” is a qualitative estimation of this frequency cited in the literature), elsewhere the proportion (%) is given; +: mean gap size (excluding a very large gap of 896m² it is 192m²; $: mean length of fallen trees in the gaps; §: length of the largest fallen tree in the gaps. gap structure in the montane forest proved as a result of discussions with tional Ph.D. Programme (IPP), Faculty ecosystems of the Guayana Shield are Hernán Castellanos. The Institute for of Forest and Environmental Sciences, necessary in order to draw firm con- National Parks in Venezuela, Petróleos University of Freiburg, Germany, partly clusions about the gap structures oc- de Venezuela and Parupa Research Sta- funded this work; the IPP provided sup- curring in these forests. Gaps should tion in supported this port in the correction and improvement be deemed to be a structural feature study as hosts. Comments made on an of the language. Financial support was of forests when studying forest func- earlier version of the manuscript and provided through grants (for Cristabel tion and process. recommendations provided by David Durán) by the Verband der Freunde der Butler Manning, Carl Burhop and two Universitaet Freiburg, the Dr. Leo-Rick- Acknowledgments anonymous reviewers served to improve er-Stiftung Freiburg im Breisgau, and it. The Spanish summary was improved the Landesgraduiertenfoerderung, Ba­ The authors are grate- thanks to Osvaldo Vidal. The authors den-­Wuert­temberg Ministry of Science, ful to Haiddye Durán Rangel, Moritz thank specially Stefanie Gaertner for Research and Art, Germany. Moessner, Rosita Pabón, Leandro Sala- repeatedly reading and commenting on zar, Marc Urlich, Seth Kaupinnen, the paper, and reviewing the statistical References Philipp Loeper, Jesús Salazar and analysis. This study was made possible Arévalo JR, Fernández-Palacios JM (1998) Jaqueline Ortíz for their help in field. by the support of several institutions. Treefall gap characteristics and regenera- The marking out of the study area and The State Electricity Enterprise EDEL- tion in the laurel forest of Tenerife. J. the gap sampling method were im- CA C.A., Venezuela, and the Interna- Veget. Sci. 9: 297-306.

278 APR 2011, VOL. 36 Nº 4 Berry PE, Holst BK, Yatskievych K (Eds.) Ewel JJ, Madriz A (1968) Zonas de Vida de Guayana. Vol 1: Introduction. Timber (1995) of the Venezuelan Guayana. Venezuela. Memoria Explicativa sobre el Press. Portland, OR, USA. pp. 1-61. Vol 1: Introduction. Timber Press. Port- Mapa Ecológico. , Venezuela. Huber O, Febres G, Arnal H (2000) Ecologi- land, OR, USA. pp. 320. 264 pp. cal Guide to the Gran Sabana National Bevilacqua M, Cárdenas L, Flores AL, Hernán- Ferreira de Lima RA, Cunha de Moura L Park - Venezuela. Nature. Conservancy. dez L, Lares BE, Manusutti A, Miranda M, (2008) Gap disturbance regime and com- Caracas, Venezuela. 192 pp. Ochoa J, Rodríguez M, Selig E (2002) The position in the Atlantic montane for- Jans L, Poorter L, Renaat SARvR, Bongers F State of the Venezuela´s Forest. A case study est: the influence of topography. Plant (1993) Gaps and forest zones in tropical of the Guayana region. World Resources In- Ecol. 197: 239-253. moist forest in Ivory Coast. Biotropica stitute. Caracas, Venezuela. 152 pp. Foelster H (1986) Forest-savanna dynamics 25: 258-269. Blanco, C. (2001) Levantamiento Estructural de and desertification processes in the Gran Jansen PA, Van der Meer PJ, Bongers F la Vegetación Boscosa en las Áreas Inmedi- Sabana. Interciencia 11: 311-316. (2008) Spatial contagiousness of canopy disturbance in tropical rain forest: an in- atas al Corredor de Servicios de la Línea de Foelster H, Dezzeo N, Priess JA (2001) Soil- Transmisión 230 Kilovatio. Sector Las Clari- dividual-tree-based test. Ecology 89: vegetation relationship in base-deficient 3490-3502. tas - Santa Elena de Uairén. Informe. (sin premontane moist forest-savanna mosaics número de página) of the Venezuelan Guayana. Geoderma Kapos V, Pallant E, Bien A, Freskos S (1990) Brandani A, Hartshorn GS, Orians GH (1988) 104: 95-113. Gap frequencies in lowland rain-forest Internal heterogeneity of gaps and spe- sites on contrasting soils in Amazonian Foster MS, Terborgh J (1998) Impact of a Ecuador. Biotropica 22: 218-225. cies richness in Costa Rican tropical wet rare storm event on an Amazonian forest. forest. J. Trop. Ecol. 4: 99-119. Biotropica 30: 470-473. Konrad V (1990) Estudio Comparativo de Re- gresiones de Volumen para Árboles en Brokaw NVL (1982) The definition of treefall Gale N (2000) The relationship between can- Pie de Cuatro Tipos de Bosques Natura- gap and its effect on measures of forest opy gaps and topography in a western les Venezolanos. Universidad de Los An- dynamics. Biotropica 14: 158-160. Ecuadorian rain forest. Biotropica 32: des. Venezuela. 40 pp. Brokaw N, Busing RT (2000) Niche versus 653-661. Lang GE, Knight DH (1983) Tree growth, chance and tree diversity in forest gaps. Gale N, Barfod AS (1999) Canopy tree mode mortality, recruitment, and canopy gap Trends Ecol. Evol. 15: 183-188. of death in a western Ecuadorian rain formation during a 10-year period in a Brown N (1993) The implications of climate forest. J. Trop. Ecol. 15: 415-436. tropical moist forest. Ecology 64: 1075- 1080. and gap microclimate for seedling growth Green PT (1996) Canopy gaps in rain forest conditions in a Bornean lowland rain for- on Christmas Island, Indian Ocean: size Lawton RO, Putz FE (1988) Natural distur- est. J. Trop. Ecol. 9: 153-168. distribution and methods of measure- bance and gap-phase regeneration in a ment. J. Trop. Ecol. 12: 427-434. wind-exposed tropical cloud forest. Ecol- Brown N (1996) A gradient of seedling ogy 69: 764-777. growth from the centre of a tropical rain Grubb PJ (1977) The maintenance of species Llamozas S, Stefano RDd, Meier W, Riina R, forest canopy gap. Forest Ecol. Manag. richness in plant communities: the im- 82: 239-244. Stauffer F, Aymard G, Huber O, Ortiz R portance of the regeneration niche. Biol. (2003) Libro Rojo de la Flora Venezolana Carvalho LMTd, Fontes MAL, Oliveira-Filho Rev. Camb. Phil. Soc. 52: 107–145. Fundación Polar/Fundación Instituto Bo- ATde (2000) Tree species distribution in Hallé F, Oldeman RAA, Tomlinsin PB (1978) tánico de Venezuela/Provita. Caracas, canopy gaps and mature forest in an area Tropical Trees and Forest. An Architec- Venezuela. 640 pp. of cloud forest of the Ibitipoca Range, tural Analysis. Billings WD, Golley F, Nelson BW, Kapos V, Adams JB, Wilson JO, south-eastern Brazil. Plant Ecol. 149: Lange, Olson JS (Eds.). Springer, New 9-22. Braun OPG (1994) Forest disturbance by York, USA. 441 pp. large blowdowns in the Brazilian Ama- Colson F, Gond V, Freycon V, Bogaert J, Hartung J, Elpelt B, Kloesener KH (1986) zon. Ecology 75: 853-858. Ceulemans R (2006) Detecting natural Statistik: Lehr- und Handbuch der Ange- Núñez-Farfán J, Dirzo R (1988) Within-gap canopy gaps in Amazonian rainforest. wandten Statistik. En Hartung, R. Olden- spatial heterogeneity and seedling perfor- Bois et Forêts des Tropiques. pp. 69-79. burg. München, Germany. 973 pp. mance in a Mexican tropical forest. Oikos 51: 274-284. Dalling JW, Hubbell SP, Silvera K (1998) Hernández L, Castellanos H (2006) Creci- Seed dispersal, seedling establishment miento diamétrico arbóreo en bosques de Oldeman RAA (1983) Tropical rain forest, ar- and gap partitioning among tropical pio- Sierra de Lema, Guayana Venezolana: chitecture, silvigenesis and diversity. In neer trees. J. Ecol. 86: 674-689. primeras evaluaciones. Interciencia 31: Sutton SL, Whitmore TC, Chadwick AC (Eds.). Tropical Rain Forest: Ecology Denslow JS (1987) Tropical rainforest gaps 779-786. and Management. Blackwell. Oxford, and tree species diversity. Annu. Rev. Hernández L, Ortíz J (2004) Avances del estudio UK. pp. 139-150. Ecol. Syst. 18: 431-451. sobre dinámica de bosques a lo largo de un Ostertag R (1998) Belowground effects of Dezzeo N, Foelster H (1994) Los suelos. In gradiente climático entre Sierra de Lema y la Gran Sabana. Mem. IV Cong. Forestal canopy gaps in a tropical wet forest. Dezzeo N (Ed.) Ecología de la Altiplani- Ecology 79: 1294-1304. cie de la Gran Sabana (Guayana Venezo- Venezolano. UNELLEZ, SVIF, EMALLCA, lana) I. Scientia Guaianae. 205. ULA. Barinas, Venezuela. 16 pp. Picón G (1994) Rare and Endemic Plant Spe- cies of the Gran Sabana, Venezuela. De- Dezzeo N, Chacón N, Sanoja E, Picón G Holdridge LR, Gremke WC, Hatheway WH, velopment of a Geographic Information (2004) Changes in soil properties and Liang T, Tosi J Jr (1971) Forest Environ- System (GIS) for Conservation. University vegetation characteristics along a forest- ments in Tropical Life Zones: A Pilot of Missouri. St. Louis, MI, USA. 100 pp. Study. Pergamon. Oxford, UK. 747 pp. savanna gradient in southern Venezuela. Poorter L (2002) Gap heterogeneity and its Forest Ecol. Manag. 200: 183-193. Hubbell SP (2005) Neutral theory in commu- implications for regeneration. In Orians Duellman WE (1997) Amphibians of La Es- nity ecology and the hypothesis of func- GH, Deindert E (Eds.) Advanced Com- calera Region, Southeastern Venezuela: tional equivalence. Funct. Ecol. 19: 166- parative Neotropical Ecology. Organiza- Taxonomy, Ecology, and Biogeography. 172. tion of Tropical Studies 01-25. pp. 200- Scientific Papers. Natural History Muse- Hubbell SP, Foster RB, O’Brien ST, Harms 214. um The University of Kansas 1-52. KE, Condit R, Wechsler B, Wright SJ, de Poorter L, Jans L, Bongers F, Rompaey RSARv Durán C (2001) Estructura y composisción Lao SL (1999) Light-gap disturbances, (1994) Spatial distribution of gaps along three florística de los bosques de Sierra de recruitment limitation, and tree diversity catenas in the moist forest of Tai National Lema, con especial énfasis en Pourouma in a neotropical forest. Science 283: 554- Park, Ivory Coast. J. Trop. Ecol. 358-398. bolivarensis C. C. Berg. Universidad de 557. Priess J, Foelster H (1994) Carbon cycle dy- Los Andes y Universidad Nacional Ex- Huber O (1995) Geographical and physical namics and soil respiration of forests under perimental de Guayana. Mérida, Venezu- features. In Berry PE, Holst BK, Yatski- natural degradation in the Gran Sabana. Inter- ela. 56 pp. evych K (Eds.) Flora of the Venezuelan ciencia 19: 317-322.

APR 2011, VOL. 36 Nº 4 279 Ricklefs RE (1977) Environmental heterogeneity and Uhl C, Clark K, Dezzeo N, Maquirino P (1988) cal rain forest at Nouragues, French Guiana. J. plant species diversity: a hypothesis. Am. Nat. Vegetation dynamics in Amazonian treefall Trop. Ecol. 14: 119-137. 111: 376-381. gaps. Ecology 69: 751-763. van Eysenrode DS, Bogaert J, Hecke PV, Impens I Runkle JR (1981) Gap regeneration in some old- van Dam O (2001) Forest Filled with Gaps: Effects (1998) Influence of tree-fall orientation on cano- growth forests of the eastern United States. of Gap Size on Water and Nutrient Cycling in py gap shape in an Ecuadorian rain forest. J. Ecology 62: 1041-1051. Tropical Rain Forest: A Study in . Pub- Trop. Ecol. 14: 865-869. lisher Tropenbos-Guyana Programme. George- Venâncio Martins S, Ribeiro Rodrigues R (2002) Sanford RL Jr, Braker HE, Hartshorn DS (1986) town, Guyana. 208 pp. Gap-phase regeneration in a semideciduous me- Canopy openings in a primary neotropical low- van der Meer PJ, Bongers F (1996a) Formation and sophytic forest, south-eastern Brazil. Plant Ecol. land forest. J. Trop. Ecol. 2: 277-282. closure of canopy gaps in the rain forest at 163: 51-62. Sanoja E (2009) Lista dendrológica de los bosques Nouragues, French Guiana. Plant Ecol. 126: Whitmore TC (1988) The Influence of tree popula- montanos de la escalera, Sierra de Lema, Esta- 167-179. tion dynamics on forest species on forest spe- do Bolívar, Venezuela. Acta Bot. Venez. 32: 79- van der Meer PJ, Bongers F (1996b) Patterns of tree- cies composition. In Davy AJ, Hutchnis MJ, 111. fall and branch-fall in a tropical rain forest in Wathinson AR (Eds.) Plant Population Ecology. Swaine MD, Whitmore TC (1988) On the definition French Guiana. J. Ecol. 84: 19-29. Blackwell. Boston, MA, EEUU. pp. 271-291. of ecological species groups in tropical rain for- van der Meer PJ, Sterck FJ, Bongers F (1998) Tree Whitmore TC (1989) Canopy gaps and the two ma- ests. Plant Ecol. 75: 81-86. seedling performance in canopy gaps in a tropi- jor groups of forest trees. Ecology 70: 536-538.

DISTURBIOS A PEQUEÑA ESCALA EN UN BOSQUE TROPICAL MONTANO DE GUAYANA: CARACTERIZACIÓN DE CLAROS EN LA SIERRA DE LEMA, VENEZUELA Cristabel Durán Rangel, Albert Reif y Lionel Hernández Resumen

El presente estudio describe la estructura de claros en el ría de los bosques tropicales. La reducción del área basal y bosque tropical montano de Sierra de Lema, Estado Bolívar, volumen de fustes generada por los claros fue de 5,8 y 0,5% Venezuela. Para ello se determinaron las superficies del claro respectivamente. Los claros configuran cerca del 1,4% de la a nivel del dosel (CAN) y del suelo (EXT), así como las su- superficie de los bosques. El microhábitat más importante en perficies de los microhábitats. Se calcularon también las áreas los claros es el suelo no perturbado. El predominio de árbo- basales y los volúmenes de madera de los fustes de los árboles les desraizados como formadores de claros estaría relacionado que formaron los claros. Para cada claro se diferenciaron entre con un enraizamiento superficial de los mismos. Las grandes los árboles que iniciaron la formación del claro y los árboles superficies de los claros en Sierra de Lema se explican por el secundarios, determinándose para ambos el modo de caída. Los alto número de árboles involucrados en los eventos. La regene- claros fueron formados principalmente por árboles desraizados, ración remanente del suelo no perturbado puede ser un compo- y la caída múltiple de árboles fue un evento frecuente. Los cla- nente importante en la regeneración del claro, aunque el gran ros tienen superficies (CAN= 31-896m2; EXT= 83-1235m2) que tamaño de los mismos harían posible una abundante regenera- superan entre 30 a 90% a aquellas reportadas para la mayo- ción de especies pioneras.

Disturbios a pequeNa escala dO bosque tropical montano de guayana: CaracterizaÇÃO dAs clarEIRAs Na sierra de lema, Venezuela Cristabel Durán Rangel, Albert Reif e Lionel Hernández ResumO

O presente estudo descreve a estrutura de clareiras no das para a maioría dos bosques tropicais. A redução da área bosque tropical montano de Sierra de Lema, Estado Bolívar, basal e volume de troncos gerada pelas clareiras foi de 5,8 e Venezuela. Para isto foram determinadas as superficies das cla- 0,5% respectivamente. As clareiras configuram cerca de 1,4% reiras a nível do dossel (CAN) e do solo (EXT), assim como da superficie dos bosques. O microhábitat mais importante nas as superfícies dos microhábitats. Calcularam-se também as clareiras é o solo não perturbado. O predomínio de árvores áreas basais e os volumes de madeira dos troncos das árvores desraizadas como formadores de clareiras estaria relacionado que formaram as clareiras. Para cada clareira foram diferen- com um enraizamento superficial das mesmas. As grandes su- ciados os grupos de árvores que iniciaram a formação da cla- perfícies das clareiras na Sierra de Lema se explicam pelo alto reira e o das árvores secundárias, determinando-se para ambos número de árvores envolvidas nos eventos. A regeneração em o tipo de queda. As clareiras foram formadas principalmente remanescente de solo não perturbado pode ser um componen- por árvores desraizadas, e a queda múltipla de árvores foi um te importante na regeneração em clareira, ainda que o grande evento frequente. As clareiras têm superfícies (CAN=31-896m2; tamanho dos mesmos fariam possível uma abundante regene- EXT=83-1235m2) que superam entre 30 a 90% a aquelas relata- ração de espécies pioneiras.

280 APR 2011, VOL. 36 Nº 4