Phenological patterns in a southern Amazonian tropical forest: implications for sustainable management

Forest Ecology and Management 160 (2002) 19–33

Phenological patterns in a southern Amazonian tropical forest: implications for sustainable management Robert B. Wallacea,b,*, R. Lilian E. Paintera,b a

Wildlife Conservation Society, 185th Street and Southern Boulevard, Bronx, New York, NY 10460, USA b Proyecto BOLFOR, Casilla 6204, Santa Cruz, Bolivia Received 27 February 2000; accepted 3 December 2000

Abstract Phenological transects were employed to assess monthly leaf, flower, unripe fruit and ripe fruit abundance for a total of 1732 individual plants within five tropical forest habitats at the ‘Lago Caiman Research Camp’, Noel Kempff Mercado National Park, northeastern Santa Cruz Department, Bolivia. Fruit surveys along trails were conducted concomitantly to assess fruit availability for the resident terrestrial frugivore community. The results of the two methodologies are compared and discussed with respect to wildlife and forest management in the region. Phenological transects revealed that Cerrado forest, tall forest, low vine forest, Sartenejal (swamp) forest, and pied mont (premontane) forest, showed seasonal variations in flower, unripe fruit and ripe fruit abundance, however, the broad temporal patterns were significantly different across habitats. Seasonal variation in overall foliage abundance was only marked for Cerrado forest. Ripe fruit production within the study site was not significantly different across months, with different habitats peaking asynchronously in abundance. From a frugivory perspective, overall ripe fleshy fruit abundance also varied considerably between habitats, and again showed asynchronous peaks in habitat production. However, both methodologies revealed the early dry season (June–July) as a period of ripe fleshy fruit scarcity throughout the study area. This period represents a resource ‘bottleneck’ for the resident frugivore community and phenological results allowed the identification of a number of keystone fruit resources for the region. Furthermore, fruit resources which are super-abundant in the early–mid wet season (November–February) might also be considered keystone resources for the region, given that they are available in an otherwise fruit scarce forest. The dynamic spatial patterning of fruit availability at Lago Caiman suggests that certain habitats might be considered keystone habitats, since they provide the majority of fruit resources on a seasonal basis. Finally, the potential of phenological information in tropical forest management plans is discussed and underlined by the observation that rainfall in itself fails to predict fruit availability in the dominant habitats at Lago Caiman. # 2002 Elsevier Science B.V. All rights reserved. Keywords: Phenology; Keystone fruit resources; Frugivores; Bolivia; Natural forest management; Amazonia

1. Introduction In recent years, wildlife conservation biologists have recognized the potential of forestry reserves as *

Corresponding author. Present address: Wildlife Conservation Society, Casilla 3-35181, San Miguel, La Paz, Bolivia. E-mail address: [email protected] (R.B. Wallace).

conservation units in an ever developing tropical landscape (Johns, 1985; Salafsky et al., 1993; Fimbel et al., 2001). Similarly, as sustainable forestry products become more popular with ecologically informed consumers in the developed world, the logging industry is beginning to appreciate the economic importance of considering wildlife needs within forestry concessions (ITTO, 1990). Over the last

0378-1127/02/$ – see front matter # 2002 Elsevier Science B.V. All rights reserved. PII: S 0 3 7 8 - 1 1 2 7 ( 0 0 ) 0 0 7 2 3 - 4

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50 years, community ecologists have also demonstrated the critical role that wildlife plays in tropical forest ecology. For example, wildlife play key functions within the forest ecosystem as pollinators, seed dispersers, seed predators, herbivores and insectivores (Terborgh, 1988, 1992; Redford, 1992). Wildlife biologists are expected to generate broad management recommendations applicable on a wide scale. However, the complexity and diversity of tropical forests makes this an especially difficult task. Nevertheless, conservation biologists are well aware of the need for haste given the rate of development in many forested regions in the tropics. The development of widely applicable management recommendations is therefore an immediate priority for tropical conservation biologists (Wallace and Painter, 1997; Rumiz et al., 1998). 1.1. Forestry, frugivores and fruit From the perspective of wildlife populations, one of the major effects of logging is a change in the distribution patterns and abundance of important food resources. Apart from the removal of certain target timber species, selective logging activities are also characterized by considerable incidental damage to overall forest vegetation structure (Burgess, 1971; Johns, 1988). In order to understand the behavioral ecology of tropical wildlife the study of food availability and distribution is critical. Primatological studies have shown that feeding behavior, ranging patterns, territoriality, reproductive seasonality, and social behavior can all be influenced by patterns of resource availability (Leighton and Leighton, 1983; Terborgh, 1983; Chapman, 1987; van Schaik et al., 1993; Barrett, 1995; Zhang, 1995; Olupot et al., 1997; Lycett et al., 1998). In the tropics many wildlife species are frugivorous to a lesser or greater degree (Emmons et al., 1983; Janson and Emmons, 1990), and in terms of biomass frugivores are the dominant trophic group in most tropical forest mammalian communities (Emmons et al., 1983; Terborgh, 1983). This is reflected by the dominance of fleshy fruit producing tree and shrub species in tropical forests (Howe and Smallwood, 1982). Furthermore, although habitat alterations are likely to influence all trophic groups in tropical forests, frugivore specialists are thought to be at particular risk (Leighton and

Leighton, 1983; Johns and Skorupa, 1987; White, 1994). In tropical forests ripe fleshy fruits are ephemeral in nature, patchily distributed, seasonally fluctuate in density, and are relatively scarce when compared to other dietary constituents such as foliage or insects (Leigh and Windsor, 1982; Howe, 1984; Richard, 1985). Phenological information is therefore critical for interpreting the ecology and behavior of wildlife in tropical forests. 1.2. Phenological studies Chapman et al. (1992, 1994) recently reviewed several more commonly employed tropical forest phenological methodologies. Phenology transects and fruit trails were considered the most appropriate methods and generally produced similar results in the Kibale forest of Uganda. Fruit trails are more appropriate for terrestrial frugivores since they measure terrestrial fruit abundance (White, 1994; Painter, 1998), and are most useful when tree densities are known for the area (Chapman et al., 1994). Phenology transects are especially appropriate for arboreal frugivores such as primates since they provide an index of arboreal fruit abundance (McFarland Symington, 1988; Kinnaird, 1992; Peres, 1994). Lowland Bolivia is virtually bereft of quantitative phenological data. Simultaneous to this study phenological data was being collected at two sites within the region (Justiniano Bravo, 1998; Justiniano Bravo and Fredericksen, 2001; Aguape, in preparation). However, these studies were more selective concentrating on a few commercially important species and/or known frugivore resources. This paper presents results from one of the first detailed quantitative phenological studies in lowland Bolivia, compares results from two of the most popular methodologies, and demonstrates how these data are useful for the sustainable management of wildlife and production forests. Phenological studies in the Neotropics have revealed temporal variations in ripe fruit availability; both in seasonal and annual terms (Foster, 1982; Terborgh, 1986; Peres, 1994). Given the seasonality associated with this Neotropical region, we expected marked variations in monthly ripe fruit abundance at Lago Caiman, a tropical humid forest in eastern Bolivia. Seasonal variations in rainfall, temperature, day length, cloud cover, and solar elevation have all been shown to

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influence phenological patterns in tropical forests (van Schaik et al., 1993; White, 1994).

2. Methods 2.1. Study site This study was conducted as part of long-term research on the behavioral ecology of black spider monkeys (Ateles chamek; Wallace, 1998) and ecology of forest ungulates (Painter, 1998) in Noel Kempff Mercado National Park in the northeastern corner of Santa Cruz Department, Bolivia (Fig. 1). The Itenez river defines the park’s eastern and northern edges, and represents the border with the neighboring Brazilian states of Rondonia and Mato Grosso. The park and its immediate vicinity are situated on the Brazilian

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Shield geological formation which is characterized by kaolinitic clay and podsol soils poor in nutrients (PLUS-CORDECRUZ, 1994; Peres, 1997). The tropical forests of northeastern Santa Cruz Department are broadly classified as humid forests of the Precambrian shield (Killeen et al., 1993). Research was based at ‘‘Lago Caiman’’ (138360 S, 608550 W), a large oxbow lake situated at the base of the northern tip of the Huanchaca escarpment and approximately 21 km upstream from an international tourist center ‘‘Flor de Oro’’. Lago Caiman is considered a pristine site having historically experienced low impact human activities such as small-scale rubber tapping in the immediate vicinity of the lake and Itenez river. The region is defined by a marked dry season in the austral winter. The nearest official weather station, San Ignacio de Velasco (168260 S, 608580 W) had a

Fig. 1. Map showing location of Noel Kempff Mercado National Park, Bolivia.

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Fig. 2. Lago Caiman—rainfall and temperature—April 1996–April 1997.

mean annual temperature of 24.85 8C ðS:D:  2:32Þ, and a mean annual precipitation of 1185.5 mm ðS:D:  372:41Þ over a 5-year period between 1989 and 1993. Our climatic data for the park demonstrate the striking seasonality of the region (Fig. 2). Between May 1996 and April 1997 the Lago Caiman research camp received 1636.9 mm of rainfall with a mean temperature for this period of 26.13 8C. A variety of distinct habitat types were recognized at Lago Caiman:  Tall forest was found on slightly undulating lowland terrain with relatively deep and well-drained clay soils. Forest floor vegetation was relatively sparse.  Low vine forest was found on well-drained lowland terrain. Dense liana tangles occupied the forest floor stratum.  Sartenejal forest was predominantly found along the forest–savannah border and in the vicinity of small forest streams. During the wet season (October/November–March/April), these areas became waterlogged due to heavy rains and were typified by small undulations that formed around the roots of larger canopy trees. Forest floor vegetation was relatively sparse.

 Pied mont forest was found on the steep slopes at the base of the Huanchaca escarpment, as well as on lower lying surrounding hills. The canopy height of this habitat decreased with increasing proximity to the escarpment. Forest floor visibility varied according to liana densities, and the terrain was uneven and littered with large rocks.  Cerrado forest was found on top of the northern regions of the Huanchaca escarpment, as well as in gullies running down the escarpment cliffs. Forest floor vegetation was extremely dense and rock strewn, with open areas confined to patches of exposed rock.

2.2. Vegetation plots A 500 ha study plot with a grid system of trails spaced every 100 m was established (Wallace, 1998). A total of 50 vegetation plots measuring 20 m  50 m were distributed along the trails in a stratified random fashion with sampling effort distributed according to the relative abundance of each habitat. This arrangement sampled 1% of the study area. The vegetation plots were botanical plots measuring 20 m  50 m, where the first 20 m  25 m considered

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all plant stems above 20 cm in dbh, and the second 20 m  25 m considered all plant stems above 10 cm in dbh. Each plant stem within the plots was identified and the diameter at breast height (dbh) measured. Species were either identified in the field or through collected specimens at the herbarium in Santa Cruz or at the Missouri Botanical Gardens in the USA. 2.3. Phenological transects The vegetation plots were also used to document the phenological patterns occurring in the forest. Phenological data for 1732 trees were collected over a 6-day period on a monthly basis. In order to avoid under representing plant species that reproduce at smaller sizes, we generated a duplicate of each reproductively active plant of between 10 and 20 cm in dbh that occurred in a monthly phenological sample. This analytical step was taken in preference to reducing the amount of data considered, for example, by ignoring half of each vegetation plot, because in general few plants were reproductively active in any 1 month. A six-point linear scoring methodology was used to estimate the percentage of the total crown area of each tree for the various plant part categories considered (van Schaik, 1986; Kinnaird, 1992), such that the total scores in each category pool could not exceed ‘‘5’’ (0 ¼ 0%; 1 ¼ 120%; 2 ¼ 2140%; 3 ¼ 4160%; 4 ¼ 6180%; 5 ¼ 81100%). The following plant part categories were recognized for scoring purposes, in one category pool: foliage (including leaves, new leaves and leaf buds), and in a separate pool: flower buds, flowers, unripe fruit, and ripe fruit. In order to minimize inter-observer variability problems, to which phenological methods are particularly prone (Chapman et al., 1992), phenological transects were performed by a team of two observers. A potential problem with this scoring method is a lack of previous knowledge regarding how much fruit a tree species is capable of producing. In this case, the observers had several years experience working in the forests of this region and had spent over a year at Lago Caiman before the onset of phenological data collection, and so had experience of crop sizes for the majority of common tree species. The mean phenological score for foliage was calculated on a monthly basis for each habitat. This measure was considered an index of foliage density.

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A separate index was also calculated for each of the reproductive parts considered in phenological surveys; flower buds, flowers, unripe fruit, and ripe fruit. Phenological scores were multiplied by the corresponding dbh of each tree to gain an estimate of individual monthly productivity. The dbh measurement reflects tree size which is assumed to give an indication of a tree’s ability to produce fruit (Leighton and Leighton, 1982; Peters et al., 1988), and is an accurate and simple parameter to measure in the field (Chapman et al., 1992). For each habitat, the sum of individual monthly productivity scores was calculated for each of the reproductive plant parts considered. This value was then standardized to a per hectare value for comparisons of habitat production. 2.4. Terrestrial fruit trails Fruit trails consisted of a transect 100 m  1 m in length beginning at each of the randomly placed vegetation plots ðn ¼ 50Þ. In addition, two fruit trails were placed in the sixth major habitat found at Lago Caiman; Igapo forest, found bordering the Itenez river. These trails were sampled once a month by counting and identifying all ripe fruit, unripe fruits, and seeds encountered. In order to obtain a measure of fruit production from fruit trail data, for each species the number of fruits and seeds encountered was multiplied by their individual average weight and weighted by the number of days one of those fruits or seeds typically remained visible on the forest floor. These persistence rates were calculated from up to 10 individual fruits/ seeds per species placed along the trail leading from camp to the study plot. Each fruit/seed was placed at distances not closer than 10 m from another experimental fruit/seed. The data were weighted in this way because of species-specific variations in (a) removal rates by terrestrial frugivores and (b) decomposition rates on the forest floor. Persistence rates were monitored each month a fruit/seed species was sampled on a fruit trail, due to the possible effect of rainfall on decomposition rates. Fruits or seeds which remained on the forest floor longer than 3 weeks, without a change in their appearance, were removed after sampling each fruit trail. Monthly weight of ripe fleshy fruit produced per hectare in each habitat was calculated by summing the species total for each month (Painter, 1998).

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3. Results 3.1. Phenology transects Only the Cerrado forest on the escarpment had a marked deciduous period, which occurred during the late dry season or austral winter (July–September; Fig. 3a–e). Of the other habitats, pied mont forest had the most variation in leaf abundance. The three

lowland habitats show similar seasonal patterns with lower variations in leaf abundance throughout the year. Clear differences in patterns of flower and fruit phenology existed between the five habitats (Fig. 4a–e). Table 1 indicates the months of maximum production for ripe fruit, unripe fruit, and flower buds and flowers in each of the five habitats. Overall monthly flower and unripe fruit production were significantly different,

Fig. 3. Patterns of foliage abundance within five habitats at Lago Caiman.

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Fig. 4. Phenological patterns in fruit and flower production within five habitats at Lago Caiman, Noel Kempff Mercado National Park, Department Santa Cruz, Bolivia.

as opposed to flower bud and ripe fruit productions that showed no significant differences across months (Table 2). All reproductive parts showed significant differences in production across habitats, except

flower buds (Table 2). Thus, there is significant habitat and temporal variation in the availability of flowers and unripe fruit at Lago Caiman. Although ripe fruit production showed significant variation among

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Table 1 Summary of phenological data for five sampled habitats at Lago Caiman Habitat

Maximum ripe fruit

Maximum unripe fruit

Maximum bud/flower

Minimum ripe fruit

Cerrado Low vine Pied mont Sartenejal Tall

June March January–February March–April September–October

December October October–December August/February August

July–August April/September June January April–June

December/April June March–April June–July/November–December June–July/December

habitats, there were no significant seasonal variations in availability. Given that frugivores are generally interested in ripe fleshy fruits, ripe fruit production was divided into two categories; fleshy and non-fleshy fruits. This was done by considering each fruit from the point of view of the consumer (Painter, 1998), such that only fruits with no flesh or aril were considered non-fleshy. Seasonal and spatial variations in fleshy and nonfleshy fruit abundance were then examined. Clear temporal fluctuations in abundance of each fruit category occurred within each habitat (Fig. 5a–e). Tall forest ripe fleshy fruit production peaked between August and October. This was due to the synchronous fruiting of three abundant species of Pseudolmedia, and the peaking of fruit production by two common species of another Moraceae genus, Brosimum. Sartenejal forest peaked in production at the end of the wet season (February–April) due to the presence of large numbers of fruiting Euterpe precatoria and Socratea exhorriza. Although virtually bereft during the dry season, low vine forest produced low levels of ripe fleshy fruit during the wet season (October–April), with a slight peak in November. Pied mont forest peaked in ripe fleshy fruit production in the middle of the wet season

(December–February), mainly because of one abundant species associated with this habitat; Spondias mombin. Finally, Cerrado forest showed a small peak in ripe fleshy fruit production in October due to the synchronous fruiting of one species; Vitex cymosa. Thus, the five habitats seem to peak in ripe fleshy fruit production asynchronously, with the early dry season (June–July) being the only period not covered by at least one habitat peak in ripe fleshy fruit production. The graphs also underline the differences across habitats in absolute ripe fruit production. Significant differences existed between habitats in overall abundance of ripe fleshy fruit on a per hectare basis (Friedman test: w2 ¼ 22:07, P < 0:001), but not for ripe non-fleshy fruits (Friedman test: w2 ¼ 7:43, P ¼ 0:12). However, across all habitats there were no significant differences in seasonal availability of either ripe fruit category (ripe fleshy fruit Friedman test: w2 ¼ 5:3, P ¼ 0:87; ripe non-fleshy fruit Friedman test: w2 ¼ 10:69, P ¼ 0:38). From a frugivory perspective, low vine forest consistently produced very little fruit of any type, and Cerrado forest fruit production was dominated by non-fleshy fruit species (Fig. 5a–e). Pied mont forest and tall forest showed similar intermediate levels of

Table 2 Results of Friedman two-way analysis of variance examining whether reproductive part production was significantly different across months and/or habitatsa Reproductive part

Overall month, w2

Significanceb, P-value

Overall habitat, w2

Significancec, P-value

Flower buds Flowers Unripe fruit Ripe fruit

17.67 30.81 32.53 9.48

0.061 0.001* 0.001* 0.487

7.22 14.38 37.02 9.53

0.125 0.006* 0.001* 0.049*

a

Production is measured as the sum of dbh  phenology score=ha. Ten degrees of freedom. c Four degrees of freedom. * Significance at the P < 0:05 level. b

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Fig. 5. Seasonal variations in ripe fruit availability in five habitats at Lago Caiman.

overall fruit production, although differences existed in the levels of each fruit category. In the Sartenejal forest, ripe fruit production was dominated by fleshy fruits with a relatively large peak towards the end of the dry season (February–April), largely due to two

palm species, E. precatoria and S. exhorriza, which were found in extremely high densities in this swamp forest type. However, it should be noted that dbh and/or basal area may not be a particularly good predictor of relative resource abundance for palm

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species; palms lack secondary thickening and hence dbh shows very little variation among reproductively active adults which continue to grow vertically (Gentry and Terborgh, 1990). 3.2. Fruit trails and methodological comparison Fruit trails also revealed that habitats had significantly different overall production of ripe fleshy fruits on a per hectare basis (w2 ¼ 12:97, d:f: ¼ 5, P < 0:05). Again, there was no significant difference in overall monthly production of fleshy fruit (w2 ¼ 13:71, d:f: ¼ 9, P ¼ 0:15), although considerable variation existed between months of maximum and minimum production (Painter, 1998). Overall monthly fruit availability for the Lago Caiman study plot, according to both phenological transects and terrestrial fruit trails, was calculated by weighting monthly habitat values by the relative abundance of each habitat in the study plot (Fig. 6). A statistical comparison of the results from the two methodologies revealed no correlation using all common months (Spearman rank: Rs ¼ 0:286; N ¼ 7; P ¼ 0:535). However, this lack of a relationship stems from the early wet season (November/December; see Fig. 6) when fruits of Ampelocera ruizi were very abundant in pied mont forest and immediately adjacent lowland habitats. The vegetation plots in pied mont forest only included one A. ruizi individual, whereas the fruit trails linearly sampled a greater distance and included several

Fig. 7. Comparison of months for which phenology transect and fruit trail data were collected simultaneously (see text).

patches of this locally abundant species which was generally found in clumped aggregations at Lago Caiman (Wallace, pers. obsv.). If we remove these months from the analysis, the correlation between the remaining five common months shows a strong trend towards significance (Spearman rank: Rs ¼ 0:8; N ¼ 5; P ¼ 0:104; Fig. 7). In fact, using this subset of sample months, a 1 month lag on fruit trail data correlates significantly with the phenology transects (Spearman rank: Rs ¼ 0:9; N ¼ 5; P ¼ 0:037; see Fig. 6). This makes sense given that fruit is initially available in the crowns of trees, only subsequently falling to the forest floor. Indeed, a similar relationship was recently demonstrated between two analogous methods in French Guiana (Zhang and Wang, 1995). 3.3. Other potential measures of fruit abundance

Fig. 6. Overall fruit production at Lago Caiman according to two quantitative methodologies.

A third index of fruit production was calculated based on data from a concurrent long-term study on black spider monkey (A. chamek) foraging ecology (Wallace, 1998). The number and total dbh of all sources of ripe fleshy fruit visited by the spider community during monthly follows was summed and then standardized according to the sample effort each month. This index assumes that spider monkeys are efficient fruit foragers, visiting all fruit producing trees within their home range in a given month. The fission–fusion social system found in Ateles allows

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(dbh  phenology score=ha  correlation coefficient ¼ 0:63; P < 0:05). One month rainfall lag was also positively correlated with low vine forest (dbh phenology score=ha  correlation coefficient ¼ 0:87; P < 0:001). Two month rainfall lag was positively correlated with low vine forest (dbh  phenology score=ha  correlation coefficient ¼ 0:88; P < 0:001), Sartenejal forest (dbhphenology score=ha  correla tion coefficient ¼ 0:80; P < 0:01), and negatively correlated with Cerrado forest (dbh  phenology score=hacorrelation coefficient ¼ 0:65; P < 0:05).

4. Discussion Fig. 8. Comparison of monthly number of fruit sources visited by A. chamek with phenological transect results.

4.1. Resource bottlenecks in a seasonal forest

them to do just that by splitting into several subgroups and foraging across the home range (McFarland Symington, 1988; Wallace, 1998). The number of fruit sources visited by spider monkeys in a given month was significantly correlated with the fruit trail results (Spearman rank: Rs ¼ 0:82; N ¼ 7; P < 0:05) and the phenology transect results (Spearman rank: Rs ¼ 0:74; N ¼ 11; P < 0:01; Fig. 8). Correlations using the total dbh of fruit sources visited during a month were approaching significance for both of the other methodologies (fruit trails: Rs ¼ 0:75; N ¼ 7; P ¼ 0:052; phenology transects: Rs ¼ 0:58; N ¼ 11; P ¼ 0:062). Finally, total dbh visited was obviously highly correlated with the number of fruit sources visited ðRs ¼ 0:88; N ¼ 11; P < 0:001Þ. The general agreement with the standard phenological methods suggests that this analytical method may be useful for studies where information regarding the location of all visited fruit trees is available, at least for wide ranging and efficient frugivores such as spider monkeys. Finally, these results provide further evidence that the early wet season (November/ December) is indeed a period of higher ripe fleshy fruit abundance (Fig. 8). Finally, we examined the validity of using monthly rainfall as a crude measure of fruit production within the five habitats at Lago Caiman. Monthly rainfall was significantly correlated with ripe fruit production (phenology score  dbh) in only one of the five habitats; a positive correlation existed for low vine forest

This study represents the first attempt to document forest fruiting patterns and quantify fruit availability across an entire year within lowland Bolivia. Northern Department Santa Cruz represents the southern limit of Amazonian tropical forests and displays a marked seasonality in terms of precipitation (Killeen, 1996; Painter, 1998; Wallace, 1998; Fig. 2). The three phenology indices described above generally produced similar results in terms of broad phenological patterns, however, the results also underline the need for large sample sizes if individual trees are to be the methodological focus. All indices demonstrated that the early to mid-dry season (June/July) is a period of extreme ripe fleshy fruit scarcity at Lago Caiman (Figs. 6 and 8). More selective phenological studies within several forest types at four other sites in northern Santa Cruz also indicate that the transitional period between the wet and dry seasons (April–July) is a time of fruit scarcity for this region (Justiniano Bravo, 1998; Fredericksen et al., 1999; Aguape, in preparation). Indeed, previous phenological studies across the tropics indicate that resource bottlenecks generally occur during the late wet season and early dry season of a given site (Terborgh, 1983; Peres, 1994; White, 1994). Nevertheless, rainfall in itself is not an accurate predictor of fruit abundance within the Lago Caiman habitats. Strikingly, production measures for ripe fruit in pied mont forest failed to correlate with any of the rainfall variables. Furthermore, tall forest is the dominant lowland habitat type and yet the rainfall

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measures failed to predict ripe fruit production in this habitat, and were actually negatively correlated with the dominant upland habitat type. Two month rainfall lag positively correlated with low vine forest and Sartenejal forest, but both of these appear to be localized and less abundant habitats within the region. It is therefore important to recognize that seasonal variations in other abiotic factors such as day length, cloud cover, temperature, and solar elevation are also important when interpreting phenological patterns, and hence production (Leigh and Wright, 1990; van Schaik et al., 1993; White, 1994). 4.2. Keystone resources and local habitat diversity During June and July spider monkeys at Lago Caiman fed on the following fleshy fruit resources: Ficus americana, F. mathewsii, Byrsonima sp., Brosimum acutifolium, and Bellucia sp. (Wallace, 1998), and these may be considered keystone resources (Terborgh, 1983, 1986). At times of fleshy fruit scarcity Ateles also relied on other dietary constituents, such as young liana leaves and the seeds of unripe non-fleshy fruits of the Bombacaceae family (e.g. Huberodendron swietenoides, Chorisia sp., Ceiba pentandra and Eriotheca globosa; Table 1). Terrestrial frugivores relied on many of the above species as well as others such as Cheiloclenium cognatum, Eschweilera turbinata, Enterolobium sp., and Hymenaea courbaril (Painter, 1998; Wallace, in preparation). It has been recently suggested that the definition of keystone resources should be redefined because of abundant species that provide a period of relatively high fruit abundance in an otherwise fruit scarce forest (Wallace, 1998, in preparation). At Lago Caiman, this was certainly the case during the study year for both A. ruizi (November/December) and S. mombin (January/ February; Wallace, 1998), and a similar phenomenon was observed within the terrestrial frugivore community with regards to Astrocaryum aculeatum (November/December; Painter, 1998). Apart from the seasonality within the study year demonstrated above, anecdotal observations from previous years indicate that large inter-annual differences in fruiting patterns also occur at this site. These inter-annual differences can be absolute or relative in nature. For example, A. ruizii was very abundant in November and December during the study year, but

did not fruit during the previous year. Conversely, Talisia cerasina did not fruit during the study year but was very abundant in pied mont forest during October and November of the previous year (Wallace, unpublished data). Relative differences were also apparent. Fruiting individuals of Brosimum lactescens and Pseudolmedia spp. appeared far more abundant in the study year whilst fruiting individuals of B. acutifolium, Helicostylis tomentosa and Perebea mollis appeared far more abundant during the previous year. The results also indicate that not only are the local habitats at Lago Caiman structurally and floristically distinct (Painter, 1998; Wallace, 1998), but they also differ with regards to broad phenological patterns. Thus, ripe fleshy fruit availability at Lago Caiman is dynamic in nature, both in spatial and temporal terms, providing an almost year-round relative abundance of fruit resources (Wallace, 1998). Frugivores therefore shift their ranging patterns according to ripe fruit distribution at Lago Caiman (Painter, 1998; Wallace, 1998). Certain habitats might be considered ‘keystone habitats’, since they provide the vast majority of fruiting resources on a seasonal basis, for example, Sartenejal and pied mont forests (Wallace, 1998). Shifting patterns of ranging in response to fruit availability and the importance of local habitat diversity for large tropical frugivores has been demonstrated previously at several sites across the tropics (e.g. Neotropics: Foster, 1980; Terborgh, 1983; Peres, 1994; SE Asia: Leighton and Leighton, 1983; Africa: Olupot et al., 1997). 4.3. Phenological monitoring and forest management From a management perspective, a number of phenological plots that adequately sampled the major habitats of a forestry reserve would identify keystone resources and habitats, thereby providing critical management information. The large inter-annual variations in phenological patterns mentioned above stress the importance of long-term monitoring; ideally a system of continual monitoring would be installed in a given forestry reserve. Whilst a measure of production would clearly be preferable (i.e. phenological scoring), data detailing the number and dbh of fruiting sources would suffice and be far easier to collect. Phenological methodologies could be included within

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the long-term ecological monitoring activities recommended by the ITTO sustainable forestry management policy (ITTO, 1990). Sustainable forestry operations could arrange to scatter phenology plots across the concessions of a forestry reserve, thereby individually reducing the relatively low projected costs of this management scheme. The installation of vegetation plots is already undertaken by foresters wishing to manage a concession, and this sampling effort could be extended in order to adequately sample each habitat from a phenological standpoint. Although the initial establishment of such plots would be relatively time consuming, the subsequent monitoring of them could easily be incorporated into management plans. Many forestry employees are able to recognize numerous tree species within the forest. Thus, whilst training programs would be necessary before the development of a phenological monitoring program, these courses would be complementing large amounts of background knowledge rather than introducing a completely alien concept. Indeed, local people are a potential source of various forms of biological information including phenological patterns and the identification of keystone fruit resources (Townsend, 1999; pers. obsv.). To date not enough information exists to predict the effect of different degrees of keystone resource loss on particular frugivore species, and hence on the frugivore community as a whole. In order to address this information dearth, studies looking at the effect of selective logging on wildlife must also identify keystone fruiting resources and measure the effects of selective logging on their abundance. Nevertheless, as shown by our results it is possible to identify candidate keystone resources and subsequently adopt management practices to avoid damage to these species, for example, directional felling. Furthermore, the presence of habitats which provide the majority of fruit resources on a seasonal basis provides us with a clear indication that wildlife refuges within forestry concessions should be designed ensuring adequate representation of these habitat types.

5. Conclusions Phenological methodologies are able to identify fruit resource bottlenecks and keystone fruit resources

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in tropical forests. In addition, in areas with considerable local habitat diversity phenological data can determine seasonally important habitats and help in interpreting wildlife ranging behavior. This information is critical if successful wildlife management is to be achieved within forestry reserves, thereby ensuring the ecological integrity of the forest. Furthermore, rainfall in itself is not a good predictor of monthly ripe fruit production. These observations demonstrate that collecting phenological data at a regional level in forestry reserves should be a management priority for ecologically sustainable initiatives.

Acknowledgements The research referred to in this document and the production of this manuscript was financed by the Wildlife Conservation Society (WCS) through a grant from the Bolivian Sustainable Forestry Project (BOLFOR) which is supported by the Bolivian Government and USAID. Fundacion Amigos de la Naturaleza also provided logistical support throughout the field study. Permission to work in the park was kindly provided by the Bolivian National Secretariat for Protected Areas. Damian Rumiz and Todd Fredericksen provided comments on an earlier version of the manuscript.

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