FREDERICKSEN et al. 185

Tropical Ecology 44(2): 185-196, 2003 ISSN 0564-3295 © International Society for Tropical Ecology

Importance of granitic rock outcrops to in a Bolivian tropical forest

NELL J. FREDERICKSEN, TODD S. FREDERICKSEN*, BETTY FLORES, ELIZABETH McDONALD & DAMIAN RUMIZ

Proyecto, BOLFOR, Santa Cruz, Bolivia

Abstract: Rock outcrops occur commonly throughout the Brazilian shield region of eastern Bolivia. These outcrops represent a unique habitat within a matrix of forest vegetation that in- crease regional plant diversity and may also be important for many wildlife species. Surveys of mammal, , reptile and amphibian species on an outcrop in a tropical dry forest in eastern Bolivia were conducted during an 18-month period to determine the abundance and composi- tion of wildlife that use rock outcrops. A total of 956 individuals of 95 species were observed. The most common species observed during diurnal surveys were Pyrrhura molinae, Cebus apella and Tropidurus torquatus. of the family Caprimulgidae all had high relative abundances and frequencies on the rock outcrop during nocturnal surveys. The most common bats captured in mist nets were Platyrrhinus dorsalis and Tadarida brasiliensis. The most common species captured using small mammal traps was Thrichomys apereiodes, which ap- pears to be an outcrop specialist. Other probable outcrop specialists include the T. tor- quatus, and the nocturnal gecko Homonota horrida. Wildlife was attracted to the rock outcrop for a variety of reasons including nocturnal heat retention, diurnal thermal uplift, water-filled concavities, and various food sources common on or near rock outcrops.

Resumen: Los afloramientos rocosos son comunes en toda la región del Escudo Brasileño de Bolivia oriental. Estos afloramientos constituyen un hábitat único inmerso en una matrix de vegetación forestal que incrementa la diversidad vegetal regional y que también puede ser im- portante para muchas especies de vida silvestre. Durante un periodo de 18 meses se llevaron a cabo reconocimientos de especies de mamíferos, aves, reptiles y anfibios en un afloramiento en un bosque tropical seco en el este de Bolivia con el fin de determinar la abundancia y la com- posición de la vida silvestre que utiliza los afloramientos rocosos. Se observaron en total 956 individuos de 95 especies. Las especies más comunes observadas durante los reconocimientos diurnos fueron Pyrrhura molinae, Cebus apella y Tropidurus torquatus. Todas las aves de la familia Caprimulgidae tuvieron abundancias y frecuencias relativas altas en el afloramiento rocoso durante los reconocimientos nocturnos. Los murciélagos más comúnmente capturados en las redes de niebla fueron Platyrrhinus dorsalis y Tadarida brasiliensis. La especie más comúnmente capturada usando trampas para mamíferos pequeños fue Thrichomys apereiodes, la cual parece ser especialista de los afloramientos. Otros probables especialistas de los aflo- ramientos incluyen la lagartija T. torquatus y el gecko nocturno Homonota horrida. La vida silvestre es atraída al afloramiento rocoso debido a una variedad de razones que incluyen re- tención nocturna del calor, elevación térmica diurna, concavidades llenas de agua y varias fuentes de alimento comúnes en o cerca de los afloramientos rocosos.

Resumo: Os afloramentos rochosos ocorrem frequentemente através da região da escarpa Amazónica da Bolívia oriental. Estes afloramentos representam um habitat único no conjunto da matriz da vegetação florestal que faz aumentar a diversidade vegetal regional e pode ser também importante para muitas espécies do bravio. Pesquisas das espécies mamíferas, aves,

*Corresponding Author: Life Sciences Division, 80 Wiley Drive, Ferrum College, Ferrum VA 24088, USA. 186 VERTEBRATE USE OF A GRANITE ROCK OUTCROP

répteis e anfíbios num afloramento numa floresta tropical seca na Bolívia oriental foram con- duzidas num período de 18 meses afim de determinar a abundância e composição do bravio que usa os afloramentos rochosos. Foi observado um total de 956 indivíduos pertencentes a 95 espé- cies. As espécies mais frequentemente observadas durante as pesquisas diurnas foram a Pyrrhura molinae, Cebus apella e Tropidurus torquatus. As aves da família Caprimulgidae apresentaram todas alta abundância relativa e frequências nos afloramentos rochoso durante a pesquisa nocturna. Os morcegos mais comuns, capturados em redes, foram os Platyrrhinus dorsalis e a Tadarida brasiliensis. A espécie mamífera mais frequentemente capturada com o uso de pequenas armadilhas para mamíferos foi a Thrichomys apereiodes, que parece ser um especialista do afloramento. Outro provável especialista inclui o lagarto T. torquatus, e a lagar- tixa nocturna Homonota horrida. O bravio é atraído ao afloramento rochoso por um conjunto de razões variadas incluindo a retenção nocturna do calor, a exaltação termal diurna, cavidades cheias de água e várias fontes de alimento frequentes nos ou junto dos afloramentos.

Key words: Biodiversity, Bolivia, Inselberg, Laja, rock outcrop, tropical dry forest, wildlife.

Introduction rock for cover and ground bromeliad patches that provide shelter from predators. Areas immediately The Brazilian shield is an extensive physi- surrounding rock outcrops may also be important. ographic region that occupies a large part of west- Water runoff from rock outcrops may enrich soils ern Brazil and extends into eastern Bolivia. This surrounding them (Isichei et al. 1990) or increase province is characterized by acidic soils, rolling local moisture availability (Navarro 1995). These topography and expansive forests. Emerging spo- enriched sites may support vegetation important radically from the forests are large dome-like gran- for wildlife. Similarly, Freeland et al. (1988) noted itic or gneissic rock outcrops, also known as insel- that water runoff from rocky escarpments in Aus- bergs which make up less than 5% of the overall tralia resulted in greater water availability close to landscape. These rock outcrops tend to occur the escarpment and provided a greater variety of throughout the landscape but are clustered re- foods for herbivores. In the Lomerío region of east- gionally, occurring in groups at the terminus of the ern Bolivia, densities of fig trees surrounding rock Brazilian shield. In the Lomerio region of Bolivia, outcrops are much higher in comparison to the for- distances between outcrops average from 5-10 km ests (Fredericksen T.S. et al. 1999; Mostacedo et al. and not all of these are large domes. The largest 2001). Killeen et al. (1990) noted a lack of plant domes are approximately 50 m in elevation above endemics on rock outcrops in eastern Bolivia, but the surrounding forest. These large outcroppings the possibility of wildlife endemics on rock out- are usually black in color due to a surface layer of crops remains unexplored. If these rock outcrops cyanobacteria. They typically are sparsely vege- support an abundant and diverse wildlife, they tated with islands of low vegetation that colonize should perhaps be treated as reserves within forest concavities within the rock that fill with organic management areas or where human development material and gradually build a shallow soil (Ibisch is encroaching. et al. 1995). Some, however, have well developed While several studies of plant communities on forest vegetation on their surface. rock outcrops in Bolivia have been conducted Because of their unique flora (Killeen et al. (Killeen et al. 1990; Navarro 1995; Ibisch et al. 1990; Navarro 1995; Ibisch et al. 1995), rock out- 1995; Mostacedo et al. 2001) apparently no exten- crops increase regional plant diversity and may sive surveys of wildlife use of this habitat type also provide important habitat for wildlife. Impor- have yet been conducted. The objective of this tant habitat features for wildlife may include study was to determine the species composition sources of heat, food and water as well as other and relative abundance of wildlife on rock outcrops special characteristics, such as weathered pieces of in the Lomerío region of eastern Bolivia. FREDERICKSEN et al. 187

Methods (Ananas ananassoides, Pseudonanas sagenarius and Bromelia serra) occupy the understory (Fig. 1). Study site The rock surface is covered by dark gray cyanobacteria and has islands of sparse vegetation Las Trancas is a seasonally dry tropical forest colonizing concavities and crevices in the rock. owned and managed by the Chiquitano indigenous These vegetated islands are dominated by moss community within the Lomerío region located and bromeliads (Deuterocohnia chrysantha) and o o south of the town of Concepción (16 13′ S, 61 50′ some shrubs and small trees. More complete de- W). Mean annual temperature in the region aver- o o scriptions of plant communities on rock outcrops in ages 24.3 C (ranging from 3 to 38 C) with a mean the Lomerío region are contained in Navarro annual precipitation of 1100 mm (less than 20% of (1995) and Killeen et al. (1990). A description of this rainfall amount occurs during the dry season). rock outcrop flora in other parts of eastern Bolivia Most of Las Trancas is upland forest with the can- is included in Ibisch et al. (1995). opy stratum becoming mostly deciduous during a The secondary rock outcrop, located 2 km from six to seven month dry season. The upland por- the primary outcrop, was smaller with a surface tions of the site are dominated by a number of tree area of 1.9 hectares and less dome shaped. Sur- species, most numerous of which are Anadenan- rounding forest and surface vegetation islands thera colubrina and Acosmium cardenasii. The were similar to the primary outcrop. This secon- Lomerío region has an abundance of rock outcrops, dary outcrop had a lower elevation (approximately several of which are located within or near the 400 30 m) than the primary outcrop and had a large ha area in Las Trancas used for research on sus- temporary pool on its upper surface. Surveys of tainable forest management. birds, reptiles and amphibians and mammals were Wildlife sampling primarily occurred on one carried out in March and November 1998 and only outcrop close to the BOLFOR (Bolivian Forest included diurnal observations, gecko census and Management Project) camp “Las Trancas 95”. track plots. Data collected from this outcrop were However, less intensive surveys were also con- only used to verify that observations on the pri- ducted on one other rock outcrop within the 400 ha mary outcrop were not site specific and were not research area to verify that observations were not included in any data analysis. site-specific to the principal study outcrop. On the principal study outcrop, surveys of birds, reptiles, Diurnal wildlife observations amphibians and mammals were carried out from June 1997 to November 1998 to determine the Three observation sites were selected, each relative abundance and species composition of providing a view of approximately 1/3 of the upper wildlife using the outcrop and surrounding areas. surface of the rock and the surrounding forest The principal outcrop has a 2.24 ha area. It edge. Observations were made at each of these has a steep north-facing slope, which then gradu- sites one day each sampling period (3 days per ally rises to a level area at the southern end hav- month for each of the 16 months that this field site ing an elevation of approximately 50 m. The out- was accessible during the study) for a total of 48 crop is entirely surrounded by forest with a 16-20 observation days. Each observation day consisted m canopy height. The perimeter of the outcrop was of three 1.5 hour periods (morning, midday and not significantly affected by selective forest har- afternoon). For all birds, mammals and reptiles vesting that was carried out in 1995. At the base of observed, the number seen, their location on the the north-facing slope is a seasonal stream sur- outcrop and their behaviour/activity at the time of rounded by gallery forest tree species. The most observation was recorded. Bird flyovers were not abundant of these are Ficus gomelleira, Syagrus counted. To be sampled, birds had to be perched on sancona, Cariniana ianeirensis, Hymenaea courba- the outcrop periphery or within its vegetated is- ril, Tabebuia serratifolia, Capparis prisca and At- lands. Soaring birds were counted when obviously talea phalerata. The sides and top perimeters of using the thermals caused by rising hot air off the the rock outcrop are dominated by upland dry for- rock. est tree species, such as Tabebuia impetiginosa, Twice during the study period (July and No- Aspidosperma rigidum, Sterculia apetala and As- vember 1998) an additional census of a nocturnal tronium urundeuva. Numerous ground bromeliads gecko population (Homonota horrida) was con- 188 VERTEBRATE USE OF A GRANITE ROCK OUTCROP

Fig 1. Photo showing a section of the primary rock outcrop with the characteristic moss and bromeliad vege- tated islands on the rock surface, bare rock, the edge and surrounding forest. ducted by searching under each loose rock slab on 1900 h to 2100 h for bats and birds. cap- the outcrop surface. These were surveyed in this tured were identified to species and released. manner due to their small size and cryptic colora- tion that made them difficult to see during the Small mammal trapping nocturnal surveys. The number of was re- Trapping of small mammals on the rock out- corded by age class. Snout-vent-length, tail length crop was carried out at the end of the rainy season and weight were also recorded for those individu- (March), the middle of the dry season (May/June), als captured to aid in identification. and at the end of the dry season (late August). Each trapping cycle consisted of a minimum of 360 Nocturnal wildlife observations trap nights per period. Fifteen trap sites were es- For four months in 1998 (April, May, July and tablished with two large Tomahawk cage traps August), observations were made of nocturnal spe- and two small Sherman traps, one of each type cies using the rock outcrop. Observations were baited with tuna/oatmeal or peanut butter/oatmeal conducted for two nights each month for a period mixtures. Traps were opened and checked each of two hours just after sunset. Counts of nocturnal morning for a minimum of six nights each period. birds were made by walking the area of the rock Trap sites were evenly spaced within five habitat surface with a flashlight and locating birds by eye- types on the outcrop: the outcrop base (the forest shine, identifying them to species when possible. border at the bottom of the steep north facing Mammals and reptiles were also noted. In addi- slope), the rock/forest edge, the surrounding forest tion, four mist nets were located out on the rock (30-50 m into the forest surrounding the rock), surface and checked every 15-30 minutes from vegetated islands on the rock, and the bare rock FREDERICKSEN et al. 189 surface. Animals captured were identified to spe- on the rock surface, rock/forest border, and 50 m cies and ear tagged. Measures of weight as well as into the surrounding forest. body, tail, ear and hindfoot lengths were also noted to assist in species identification. Recaptures were Data analysis noted but not included in the analysis. The number of animals observed for both diur- nal and nocturnal censuses was summed over the Track plot surveys total 18 month study period. Relative abundance Track plots were utilized during March and (total number of each species observed/total num- July of 1998 for the principal outcrop and during ber of animals of that wildlife group observed), as March only for the secondary outcrop. Track plots well as frequency of occurrence (number of days were created by clearing all vegetation in a 1 x 0.5 m each species was observed/total number of obser- area and covering that area with a layer of sifted vation days) was determined. Analysis of variance fine soil. All track plots were located along visible, was used to compare microhabitat (bare rock, active trails (most likely armadillo trails) vegetated islands or forested border) use by small in the forest surrounding the outcrops (within 30- mammals captured during trapping. 50 m of the upper and lower rock edge). Four track plots were installed in March and five in July for Results the principal outcrop and six track plots were in- stalled for the secondary outcrop. Plots were Diurnal wildlife observations opened and checked each morning for four nights in March (an effort of 16 plot nights) and three A total of 733 individuals of 56 vertebrate spe- nights in July (an effort of 15 plot nights) on the cies were recorded during diurnal observations. principal outcrop and three nights on the secon- Birds were the most common wildlife group ob- dary outcrop (an effort of 18 plot nights). served consisting of 474 individuals of 39 species (Table 1). The most common species observed was Diurnal mistnet surveys Pyrrhura molinae with a relative abundance of 33.3% of all birds. Ninety-six mammals of five spe- Mist net surveys were carried out during cies were recorded, the most common of which was March, April and May of 1998. Four mist nets the monkey Cebus apella (relative abundance measuring 12 x 2.5 m were erected on the rock be- among mammals = 59.4%), however, this consisted tween zero and five meters from the upper border of repeated measures of one troop consisting of ap- of the forest and at intervals of approximately 30 proximately 18 members. Reptiles consisted of 163 m. Nets were opened for five hours each morning individuals of six species, the most common of (0600 to 1100), and checked hourly for captures which was Tropidurus torquatus (relative abun- during two days each field visit. Individuals cap- dance among reptiles = 79.8%). Animals having tured were identified to species, marked with me- the highest frequency of observation were tallic numerical bands and released. Recaptures Pyrrhura molinae and Tropidurus torquatus, were noted but not included in the analysis. (41.3% and 65.2% of all observations, respectively). Incidental sightings on the principal outcrop Temperature and humidity measurements included several bird species that were not re- Measures of diurnal temperature and humid- corded during formal observations: Amazona aes- ity were taken approximately every two hours dur- tiva, Ara severa, Basileuterus culicivorus, Camp- ing each of the diurnal observation days. Ambient tostoma obsoletum, Chaetura brachyura, Cnemo- air temperature was measured at a height of 1.5 m triccus fuscatus, Coragyps atratus, Penelope super- in shade on the rock surface and 50 m into the sur- ciliaris, Sittasomus griseicapillus and Tapera rounding forest. Ground level temperatures were naevia. In addition, one incidental sighting was of also measured in several habitat types: rock/forest the tropical rat snake Spilotes pullatus, seen edge, forest 50 m from rock edge, vegetated islands drinking from a temporary water hole on the rock and bare rock surface. Relative humidity was surface, and another of a juvenile turtle, Geoche- measured at a height of 5-10 cm above the ground lone carbonaria, encountered along the border of the outcrop. 190 VERTEBRATE USE OF A GRANITE ROCK OUTCROP

Table 1. Abundance and frequency of wildlife observed during diurnal observations (3 days per month for 16 months for a total of 48 observation days) on a rock outcrop in a tropical dry forest in eastern Bo- livia. Relative abundance is given as the (total number of each species observed/total number of animals of that wildlife group) x 100. Frequency is given as the (number of days a species was observed/total num- ber of observation days) x 100.

Total # Relative Species Frequency Type of Behaviour Animals Abundance Birds Ara auricollis 3 0.63 4.3 Foraging in trees on border Aratinga leucophthalmus 15 3.16 13.0 Foraging in trees on border Brotogeris versicolurus 4 0.84 4.3 Foraging in fruit tree on border Buteo magnirostris 1 0.21 2.1 Perched in tree on border Cacicus cela 4 0.84 4.3 Calling on border Campephilus rubricollis 3 0.63 4.3 Foraging on trunks of trees on border Casiornis rufa 1 0.21 2.1 In mixed foraging flock on border Cathartes aura 8 1.69 17.3 Soaring on thermals created by the rock Celeus lugubris 12 2.53 17.3 Foraging in trees on border and on cactus in vegetated islands Columbina picui 1 0.21 2.1 Foraging in trees on border Crax fasciolata 2 0.42 2.1 In the forest bordering rock Crypturellus tataupa 1 0.21 2.1 Calling on border Crypturellus undulatus 5 1.05 6.5 Foraging on ground on border Cyanocorax cyanomelas 35 7.38 32.6 Foraging on border and on cactus fruits on edge and islands Cyanocorax chrysops 19 4.01 19.5 Calling and foraging in vegetated islands Chlorostilbon aureoventris 27 5.70 39.1 Foraging on bromeliad flowers in vegetation islands on the rock Elanoides forficatus 10 2.11 8.7 Soaring on thermals created by the rock Euphonia chlorotica 3 0.63 2.1 In vegetated islands Glaucidium brasilianum 1 0.21 2.1 Perched in tree on border Herpetotheres cachinnans 1 0.21 2.1 Perched in tree on border Hydropsalis brasiliana 2 0.42 4.3 Roosting on ground on border Leptotila verreauxi 12 2.53 19.5 In trees and on ground on border Leptopogon amaurocephalus 3 0.63 2.1 In trees on border Monasa nigrifrons 24 5.06 19.5 Calling in trees on border Myiarchus tyrannulus 14 2.95 21.7 Foraging in vegetated islands Parula pitiayumi 4 0.84 4.3 In mixed flock on border Phaetornis subochraceus 3 0.63 6.5 Foraging on bromeliad flowers in vegetated islands Pionus menstruus 19 4.01 15.2 Feeding in fig trees on border Psarocolius decumanus 16 3.38 28.2 Display calling in trees on border Pteroglossus castanotis 31 6.54 13.0 Feeding in fig and Sterculia apetala trees on border Piaya cayana 6 1.27 10.8 In trees on border Pyrrhura molinae 158 33.33 41.3 Foraging in trees on border, including figs Contd... FREDERICKSEN et al. 191

Table 1 Contd. Total # Relative Species Frequency Type of Behaviour Animals Abundance Sarcoramphus papa 1 0.21 2.1 Soaring on thermals created by the rock Spizastur melanoleucus 1 0.21 2.1 Perched in tree on border Thalurania furcata 3 0.63 4.3 Foraging on bromeliad flower in islands Thamnophilus punctatus 2 0.42 2.1 Pair calling on border Thryothorus guarayanus 2 0.42 4.3 Calling on border Trogon curucui 5 1.05 4.35 In trees on border Xiphocolaptes major 1 0.21 2.17 Foraging in tree on border Tyrannidae sp. 1 5 1.05 4.35 In mixed flock on border Tyrannidae sp. 2 2 0.42 2.17 Foraging on border Tyrannidae sp. 3 1 0.21 2.17 In trees on border Accipitridae sp. 1 1 0.21 2.17 Soaring on thermals created by the rock Accipitridae sp. 2 1 0.21 2.17 Perched in tree on border Dendrocolaptidae sp. 1 1 0.21 2.17 In trees on border Mammals Tadarida brasiliensis 14 14.58 4.35 Roosting under rock slabs on the rock surface Cebus apella 57 59.38 15.22 Foraging in trees along border Mazama americana 2 2.08 2.17 Foraging at border and along vegetated is- lands Nasua nasua 22 22.92 4.35 Foraging in bromeliads on border and in vege- tated islands Sciurus spadiceus 1 1.04 2.17 Foraging in trees on border Reptiles Ameiva ameiva 25 15.33 28.26 Foraging on rock surface along border and vegetated islands Mabuya frenata 2 1.23 4.35 Juvenile on log in border vegetation Tropidurus torquatus 130 79.75 65.23 Population inhabiting edge and island vegeta- tion Tupinambus tequixin 4 2.45 8.70 Foraging and basking on rock surface Gonatodes sp. 1 0.61 2.17 On log in border vegetation Micrurus frontifasciatus 1 1.04 2.17 Foraging on rock surface

Diurnal observations made on the secondary surface were occupied by geckos, and in November outcrop also included Tropidurus torquatus and (wet season) 59% were occupied. Pyrrhura molinae as the most common species, which is consistent with results for the principal Nocturnal observations outcrop studied. One species that was encountered Birds of the family Caprimulgidae (Nyctidro- on the secondary study outcrop in Las Trancas, mus albicollis, Hydropsalis brasiliana and Copri- but not on the principal outcrop, was the frog Phy- mulgus rufus) all had high relative abundances salaemus biligonigerus, which was inhabiting a and frequencies on the rock outcrop during noc- large temporary pool on the rock surface. turnal surveys (Table 2). Only one terrestrial The census of the nocturnal gecko (Homonota mammal was frequently observed during noctur- horrida) revealed six adults and two juveniles for nal observations, the spiny rat Thrichomys July and 12 adults and 7 juveniles for November. apereoides. In July (dry season) 23% of the loose rocks on the 192 VERTEBRATE USE OF A GRANITE ROCK OUTCROP

Table 2. Abundance and frequency of wildlife observed during nocturnal observations (2 nights for each of 4 months during 1988 for a total of 8 observation nights) on a rock outcrop in a tropical dry forest in eastern Bolivia. Relative abundance is given as the (number of each species observed/total number of animals observed) x 100. Frequency is given as the (number of days a species was observed/total number of observation days) x 100.

Species # Animals Relative Frequency Habitat use or Behavior Abundance Birds Nyctidromus albicollis 8 12.31 50.0 Roosting and foraging on rock surface Hydropsalis brasiliana 23 35.38 87.5 Roosting and foraging on rock surface Caprimulgus rufus 10 15.38 62.5 Roosting and foraging on rock surface Caprimulgidae sp. 12 18.46 50.00 Roosting and foraging on rock surface Mammals Thrichomys apereoides 8 12.31 37.5 Foraging on rock surface Reptiles Oxyrhopus petola 2 3.08 12.5 Foraging and/or basking on rock surface Tropidurus torquatus 1 1.54 12.5 Under flat rock on rock surface

Table 3. Bird and bat species captured in mist nets during the early evening (two nights for each of 4 months during 1998 for a total of 8 trap nights) on a rock outcrop in a tropical dry forest in eastern Bo- livia. All species were captured while foraging above the rock surface. Relative abundance is given as the (number of each species captured/total number of animals captured) x 100. Frequency is given as the (number of days a species was captured/total number of netting days) x 100.

Species # Animals Relative Abundance Frequency Birds Nyctidromus albicollis 2 7.1 25.0 Hydropsalis brasiliana 3 10.7 25.0 Caprimulgus rufus 1 3.5 25.0 Bats Glaucidium brasilianum 1 3.5 12.5 Tadarida brasiliensis 5 17.8 25.0 Artibeus sp. 1 3.5 12.5 Uroderma bilobatum 2 7.1 25.0 Glossophoga soricina 2 7.1 12.5 Platyrrhinus dorsalis 8 28.5 25.0 Macrophyllum macrophyllum 1 3.5 12.5 Chiroptera spp. 2 7.1 25.0

Mist net captures consisted mostly of bats, the tured was the nocturnal Echimyidae Thrichomys most common species of which were Platyrrhinus apereiodes. No significant preference by small dorsalis and Tadarida brasiliensis with relative mammals for any of the microhabitat types (forest abundances of 17.8% and 28.6% of all bat captures, 50 m from rock edge, rock/forest edge, vegetated respectively (Table 3). islands, bare rock surface) within the rock outcrop was observed (P = 0.37). However, the number of Small mammal trapping animals captured was approximately 2 x and 1.5 x at the outcrop base and within forested border mi- A total of 55 individuals of six species were crohabitats, respectively, than were captured in captured (Table 4). The most common species cap- FREDERICKSEN et al. 193

Table 4. Abundance and frequency of mammals captured (3 trapping periods in 1998 consisting of 5-6 trapnights per period) by species on a rock outcrop in a tropical dry forest in eastern Bolivia. Relative abundance is given as the (number of each species captured/total number of animals captured) x 100. Fre- quency is given as the (number of days a species was captured/total number of trapping days) x 100.

Species # Animals Relative Abundance Frequency Didelphis marsupialis 1 1.8 4.7 Cavia tschudii 4 7.2 19.0 Monodelphis domestica 4 7.2 33.3 Oryzomys megacephalus 4 7.2 19.0 Proechimys longicaudus 6 10.9 23.8 Thrichomys apereiodes 36 65.4 100.0 the other microhabitats (Fig. 2). There was no dif- roborated by the presence of two scat piles contain- ference in captures among seasons (P = 0.21). ing the remains of a juvenile Tayassu sp. Track plots on the secondary outcrop revealed the pres- Track plot surveys ence of the same species as on the primary outcrop with the addition of Mazama gouazoubira. A total of 24 animals tracks were recorded on the primary rock outcrop over a period of seven Diurnal mist net surveys trapping nights. Echimyidae sp. (probably Thrichomys apereiodes) and Dasypus novemcinctus A total of 20 individuals of 10 species were had the highest relative abundances (0.38 and captured during the six days of mist netting. The 0.21, respectively). These same species also had number of captures was so low that frequency is the highest frequency of occurrence (0.71 and 0.57 not considered for this survey. The species most respectively, Table 5). The tracks of Puma concolor commonly captured were Cnemotriccus fuscatus, were those of an adult and juvenile traveling to- Thamnophilus punctatus and Phaethornis subo- gether. Their presence on the outcrop was also cor- chroaceus (Table 6). Four species were captured that were not recorded for the diurnal observa- tions; Basileuterus culicivorus, Cnemotriccus fus- catus, Elaenia parvirostris and Pipra fascicauda. Interestingly, with the exception of the humming- bird, Phaethornis subochraceus, all species cap- tured were insectivorous.

Thermal characteristics of the study sites Mean temperature of the forest border (50 m from rock edge) followed ambient temperatures throughout the day. Mean temperatures of the for- est/rock edge and vegetated islands followed the same general pattern as ambient air temperatures in the morning and late afternoon but average 2- o 4 C higher during the early afternoon. Mean tem- o Fig. 2. Mean number of mammals (±1 Standard Error) perature of the rock surface averaged 5 C higher in each of five habitat types on a granitic rock outcrop- than ambient in the morning and late afternoon rock base, rock/forest edge, surrounding forest (50 m and reached 10oC higher than ambient during the from rock/forest edge), vegetated islands on the rock middle of the day (Fig. 3). The mean relative hu- surface, and bare rock surface. There was no significant midity of the forest (50 m from rock edge) was con- difference in small mammal preference for any of these habitats (P = 0.37). Also there was no significant sea- sistently higher than that of the rock surface and sonal differences (P = 0.21). No mammals were captured the forest/rock edge (Fig. 4). in the border habitat type for the month of August. 194 VERTEBRATE USE OF A GRANITE ROCK OUTCROP

Table 5. Relative abundance and frequency of animal tacks in track plots (two trapping periods during 1998 for a total of 7 trap nights) on the outcrop border in a tropical dry forest in eastern Bolivia. Relative abundance is given as the (number of each species observed/total number of animals observed) x 100. Fre- quency is given as the (number of days a species was observed/total number of trapping days) x 100.

Species # Animals Relative Abundance Frequency Mammals Dasypus novemcinctus 5 0.21 0.57 Echimyidae sp. 9 0.38 0.71 Puma concolor 2 0.08 0.14 Dasyprocta azarae 2 0.08 0.14 Sylvilagus brasiliensis 2 0.08 0.14 Birds Crypterellus undulatus 4 0.17 0.43

Discussion the rock outcrop. Factors likely attracting wildlife include latent heat radiating from the rock surface Sporadically located within the forest matrix of after sunset, higher temperatures during the day, eastern Bolivia, rock outcrops provide areas dras- areas of water availability and high moisture and tically different from the surrounding forests and several unique structural characteristics that are therefore, provide habitat elements that act as at- important habitat features for some wildlife spe- tractants to the forest inhabitants. They also pro- cies. vide specialized habitats for some species that al- low them to exist in a forest that otherwise would not support them. Nine hundred fifty-six individu- als of 95 species of animals were observed using

Table 6. Abundance of birds captured during diurnal mist net surveys (3 trapping periods con- sisting of 2 days each for a total of 6 trap days) on a rock outcrop in a tropical dry forest in eastern Bolivia. Relative abundance is given as the (num- ber of each species captured/total number of ani- mals captured) x 100. Frequency is given as the (number of days a species was captured/total num- ber of trapping days) x 100.

Relative Species # Animals Abundance Fig. 3. Mean temperatures throughout the day for am- Basileuterus culivorus 1 0.05 bient air temperature and four microsites – bare rock surface, vegetated islands on the rock surface, Celeus lugubris 1 0.05 rock/forest edge, and surrounding forest (50 m from Cnemotriccus fuscatus 4 0.20 rock/forest edge). Temperatures were taken hourly for Elaenia parvirostris 1 0.05 three days per month for 16 months for a total of 48 sample days. Temperatures of the islands and edge fol- Phaethornis subochraceus 1 0.05 lowed ambient temperatures (taken at a height of 1.5 m Pipra fascicauda 1 0.05 in the shade at the center of the rock outcrop and 50 m Psaracolius decumanus 1 0.05 into the surrounding forest) in the morning and late afternoon but averaged 2-4 degrees higher during mid- Thalurania furcata 2 0.10 day. Rock temperatures were on average 5 degrees Thamnophilus punctatus 4 0.20 higher than ambient in the morning and late afternoon Thryothorus guarayanus 4 0.20 and averaged 10 degrees higher during midday. Forest temperatures followed ambient throughout the day. FREDERICKSEN et al. 195

seeds of the vegetated islands on the rock. Ground bromeliads (Deuterocohnia chrysantha and Ananas ananassoides) were abundant on the outcrop bor- der and capuchin monkeys (Cebus apella) often descended to the ground to feed on their fruits. A troop of coatimundis (Nasua nasua) was twice ob- served digging among the large leaf scales at the base of these plants in search of . The pres- ence of these larger mammals near the outcrop may serve to attract large carnivores such as Puma concolor. While these rocks are generally very dry habi- tats, depressions collect and hold water during the Fig. 4. Mean relative humidity throughout the day for rains and provide a source of drinking water for three microsites – bare rock surface, rock/forest edge, wildlife that often lasts long into ensuing dry peri- and surrounding forest (50 m from rock/forest edge). ods. Several bird species and one snake (Spilotes Humidity measurements were taken hourly for three pullatus) were seen drinking water from a deep days per month for 16 months for a total of 48 sample depression in the rock. These temporary pools may days. Humidity for the forest was consistently higher also provide an important water source for some than for the rock face or rock/forest edge throughout the day. amphibians. A large pool on the secondary outcrop was found to contain adult Physalaemus biligoni- These rock outcrops heat up rapidly during the gerus as well as their tadpoles. Runoff from the day, but also gradually release the heat during the outcrop increases soil moisture at the northern night. The higher temperature of the rock during base of the rock and supports many species of trees early evening hours may have been responsible for that grow only in areas of high soil moisture. For attracting a number of animals observed in this example, fig trees (Ficus gomelleira, Ficus eximia study. During the morning hours a large variety of and Ficus calyptroceras) were very abundant on insects and lizards were active on the rock outcrop the bottom and lower slopes of the principal out- that may serve as prey for larger animals. crop. The fruits of these trees also attracted birds Tropidurus torquatus was especially numerous, and other wildlife to the area around the outcrop. but other lizards were commonly observed. Noc- Parrots, such as Pyrrhura molinae, Pionus men- turnal bird species, like the scissor-tailed nightjar struus and Aratinga leucophtalmus, were com- (Hydropsalis brasiliana) and paraque (Nyctidro- monly seen feeding on figs near the outcrop during mus albicollis), were perhaps attracted to the la- the day, while rodents such as Thrichomys tent heat of the rock or perhaps to feed on the apereiodes were seen feeding on figs at night. The abundant insects flying in the early evening. Heat fruits of Sterculia apetala were heavily fed upon by that rises from the rock also creates thermals dur- chestnut-eared Aracaris (Pteroglossus castanotis). ing the mid-morning hours that were used by large Additional fruit and nectar producing plants such soaring birds, such as Cathartes aura, Elanoides as Cecropia concolor, Cissus sicyoides, Maclura forficatus and Sarcoramphus papa. tinctoria, Phoradendron hieromyrni and the cacti The apparently high quantity of flying insects Monvillea cavendishii, Cleitocactus baumannii and near rock outcrops also attracts many insectivo- Cereus tacuaralensis, may also provide food rous birds, including the Tyrannidae that use the sources for many of the species observed. open space of the outcrop to sally from branches of In addition to heat, food and water, rock out- shrubs and low trees to catch their prey. Note that crops also provide special habitats that may en- the three most common bird species captured us- hance regional species richness. Weathering ing mist nets were insectivores. The abundance of causes fragmentation of the rock surface, leaving lizards likely accounted for the presence of preda- loose flat slabs of rock with space underneath was tory birds such as the laughing falcon (Herpeto- habitat for some species of animals. Nocturnal theres cachinnans). Small rodents were also abun- animals, such as the bat (Tadarida brasiliensis) dant on the rock outcrop, feeding on plants and and the nocturnal gecko (Homonota horrida) find 196 VERTEBRATE USE OF A GRANITE ROCK OUTCROP shelter under broken rocks during the heat of the plans. In areas of human settlement, deforestation day, emerging at night to forage for insects. Be- around outcrops should be prevented. Rock out- cause of their spiny leaves, thick patches of ground crops and their bordering forests actually appear bromeliads also provide shelter for rodents and to be centers of high biodiversity and should be lizards from their predators. given consideration as reserves in forest manage- Of the species observed on the outcrop, four ment plans. appear to be outcrop specialists: Tropidurus tor- quatus, Homonota horrida, Cavia tschudii and Acknowledgements Thrichomys apereiodes. These four species were not recorded within the surrounding forests of Las The authors would like to thank Bonifacio Mo- Trancas (greater than 150 m distant from any rock stacedo, Jose Carlos Herrera, Marisol Toledo and outcrops) during small mammal and herpetofaunal Yussett Lino for their helpful imput on this manu- trapping carried out in another study concurrent script. with this one (Fredericksen N.J. et al. 1999). Sev- eral isolated populations of Tropidurus have been References discovered inhabiting rock outcrops in the Amazon region (Vitt et al. 1996) and T. apereiodes has been Fredericksen, N.J., T.S. Fredericksen, B. Flores & D. referred to as an outcrop specialist by Redford & Rumiz. 1999. Wildlife use of different-sized logging Eisenberg (1989). Very little is known about the gaps in a tropical dry forest. Tropical Ecology 40: 1- nocturnal gecko H. horrida and the small mammal 9. C. tschudii, but their absence in the forest and Fredericksen, T.S., D.M. Rumíz, J. Justiniano & R. high abundance on the outcrops indicates that Agaupe. 1999. Harvesting free-standing figs for they may also be outcrop specialists. timber in Bolivia: potential implications for sustain- ability. Forest Ecology and Management 116: 151- Conservation implications 161. Freeland, W.J., J.W. Winter & S. Raskin. 1988. Austra- With increasing tree harvesting and human lian rock-mammals: a phenomenon of the seasonally population pressures on the tropical forests of Bo- dry tropics. Biotropica 20: 70-79. livia, these rock outcrops, imbedded within the Ibisch, P.L., G. Rauer, D. Rudolph & W. Barthlott. 1995. forest landscape, should be considered for designa- Floristic, biogeographical and vegetational aspects tion as reserves. New laws in Bolivia now require of pre-Cambrian rock outcrops (inselbergs) in east- all landowners conducting timber harvesting to ern Bolivia. Flora 190: 299-314. develop management plans that include the desig- Isichei, A.O., A.J. Morton & F. Ekeleme. 1990. Mineral nation of such reserves. Forests immediately sur- nutrient flow from an inselberg in south-western rounding outcrops have been traditionally avoided Nigeria. Journal of Tropical Ecology 6: 479-492. because of problems with harvesting on steep ter- Killeen, T.J., B. Louman & T. Grimwood. 1990. La rain and the poor quality of tree stems produced by ecología paisajística de la región de conceptión y the relatively harsh environmental conditions near Lomerío en la provincia Nuflo de Chávez, Santa the outcrops. Interestingly, however, valuable tim- Cruz, Bolivia. Ecologia en Bolivia 16: 1-46. ber species, such as Cedrela fissilis, Amburana Mostecedo, B., M. Toledo & T.S. Fredericksen. 2001. La cearensis, Astronium urundeuva and Tabebuia im- vegetación de las lajas en la región de Lomerío, petiginosa are often relatively abundant in forests Santa Cruz, Bolivia. Acta Amazonica 31: 11-25. adjacent to rock outcrops. Protection of these sur- Navarro, G. 1995. Clasificación de vegetatión de la re- gion de Lomerío en el Departmento de Santa Cruz, rounding forests could provide a valuable source of Bolivia. Doc. Tec. 10, Proyecto Bolfor, Santa Cruz, seed trees for these valuable species. Surveys by Bolivia. Mostacedo et al. (2001) indicated that the influence Redford, K.H. & J.F. Isenberg. 1989. Mammals of the of these outcrops on the surrounding forest can Neotropics, Vol. 2, The Southern Cone. University of extend up to 150 meters. Harvesting should be Chicago Press, Chicago. avoided within this region. Because water runoff Vitt, L.J., P.A. Zani & J.P. Caldwell. 1996. Behavioral can create gallery forests at the base of the steep ecology of Tropidurus hispidus on isolated rock out- slopes of rock outcrops, this lower border is already crops in Amazonia. Journal of Tropical Ecology 12: likely to be protected under existing management 81-101.