The Coleopterists Bulletin, 66(3): 253–260. 2012.
OBSERVATIONS ON THE LIFE HISTORY OF ENEMA PAN (F.) (COLEOPTERA: SCARABAEIDAE: DYNASTINAE) AND ITS ASSOCIATION WITH BAMBOO, GUADUA KUNTH (POACEAE: BAMBUSOIDEAE), IN SOUTHWESTERN AMAZONIA JENNIFER M. JACOBS Department of Integrative Biology, University of California Berkeley, 1005 Valley Life Sciences Building #3140, Berkeley, CA 94720-3140, U.S.A. [email protected]
Museum of Vertebrate Zoology, University of California, Berkeley 3101 Valley Life Sciences Building, Berkeley, CA 94720-3160, U.S.A. [email protected]
BRETT C. RATCLIFFE Systematics Research Collections, W436 Nebraska Hall, University of Nebraska Lincoln, NE 68588-0514, U.S.A. [email protected]
ABSTRACT Here we describe the association of Enema pan (F., 1775) (Scarabaeidae: Dynastinae: Oryctini) with bamboo plants in the genus Guadua Kunth (Poaceae: Bambuseae) in a lowland rainforest in southeastern Peru. Mounds at the base of Guadua stems and underground tunnels over one meter long are constructed by adults. Males were found inside these tunnels and in mounds at the base of bamboo stems where they shred and feed on bamboo sap. Males were observed perching at the top of opened mounds only at night, waving their antennae. This study provides the first description of the burrows of E. pan and its association with bamboo plants in southwestern Amazonia. Key Words: ecology, behavior, burrows, Peru, lowland tropical rainforest
Bamboo forests cover approximately 180,000 km2 in southwestern Amazonia and represent the largest bamboo-dominated forest in the Neotropics (Nelson 1994; Griscom and Ashton 2003). The presence of naturally occurring bamboo species in this region dates back to at least the Pleistocene, because fossil records of bamboo predate 45,000 yr BP (Olivier et al. 2008), although new molecular evidence suggests that ancestral lineages may have been present in the Miocene (Ruíz-Sánchez 2011). Bamboo forests of southwestern Amazonia are biologically interesting because they primarily occur as monodominant forests with a patchy distribution throughout terra firma and floodplain forests. Two common species, Guadua sarcoparpa Londoño and Peterson and Guadua weberbaueri Pilger (Poaceae: Bambuseae), dominate the bamboo forests in southwestern Amazonia (Griscom and Ashton 2006). Species of Guadua Kunth (hereafter referred to as bamboo) grow in dense monotypic stands ranging from one to thousands of hectares (Griscom and Ashton 2003;
Griscom et al. 2007). Clonal bamboo patches synchronously flower after approximately 30 years and die over large areas (Janzen 1976; Nelson and Bianchini 2005). Sometimes these areas are recolonized by bamboo and sometimes by other plant species (M. Silman, personal communication). Thus, over time and space, bamboo patches blink in and out of existence. Bamboo forests have been assumed to be a speciespoor, weedy habitat, but researchers are discovering that bamboo forests are an important component of the regional ecosystem in southwestern Amazonia. Bamboo forest provides a distinct vegetative habitat different from that of other forest types, and a number of vertebrate species, including birds, a poison frog, and two rodent species, are closely associated with bamboo forests (Emmons and Feer 1990; Morales 1992; Kratter 1997; Ledesma 2003; Lebbin et al. 2007; von May et al. 2008, 2009). These organisms have evolved to use bamboo in part or all of their life cycle. At least two species 253
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of ants and one species of weevil are bamboo specialists, the former maintaining colonies inside bamboo trunks and the latter ovipositing in bamboo stems (Navarro de Andrade 1928; Davidson et al. 2006a, b; T. Erwin, personal communication). A number of inventories of particular beetle taxa in a variety of habitats in the southeastern portion of the Peruvian Amazon have included minimal sampling in bamboo forests (Pearson and Derr 1986; Erwin 1997; Larsen et al. 2006). However, few quantitative surveys of bamboo habitat have been performed, with the exception of research conducted by the first author (Jacobs 2009). The primary focus of this research was to quantitatively study ground-dwelling beetles collected in pitfall traps in replicated patches of bamboo and terra firma forests. Surprisingly, beetle diversity in bamboo forests was only slightly lower than that of terra firma forest. However, one of the most striking results was the frequent occurrence of one species of large dynastine scarab beetle, Enema pan (F., 1775) (Scarabaeidae: Dynastinae: Oryctini), in the bamboo forest samples. Enema pan was rarely collected in terra firma forest samples. The results of the quantitative sampling that revealed the high abundance of E. pan in bamboo forest, paired with our discovery of a study by Keller (2003), inspired further field investigations on the behavior and natural history of this beetle. Keller (2003) described an ethnobotanical use of the bamboo Chusquea ramosissima Lindman (Poaceae) and dynastine scarabs by the Guaraní amerindians of Paraguay. Keller provided limited natural history accounts of some dynastines, including E. pan, and their connection to Chusquea bamboo. Keller observed four species of dynastine scarabs feeding on the sap of C. ramosissima: Heterogomphus aidoneus Burmeister, Heterogomphus eteocles Burmeister, Heterogomphus pauson (Perty), and E. pan. He noted that all of these beetles made burrows beneath C. ramosissima and fed on the stem or rhizome, and he illustrated the general form of the burrow. However, he did not explain how each particular species made its burrow, whether the burrow-maker was male or female, and whether there were larvae present in the burrow. Keller’s (2003) paper led us to question if a similar feeding and burrowing behavior might be taking place between E. pan and G. weberbaueri in southeastern Peru, and whether or not this potential bamboo association might explain the high abundance of E. pan individuals that were collected in Guadua forests by Jacobs (2009). The main goal of this study was to determine if and how E. pan was using bamboo forest habitat and utilizing the bamboo plants as food and nesting sites. We additionally wanted to record behavioral observations about E. pan. It is known that many
dynastine scarabs feed on plants in the Poaceae (grass) family of which bamboo is a member. In general, little is known about the natural history of E. pan or Enema endymion Chevrolat, the only other species in the genus. Enema endymion is found from Mexico to Bolivia and Brazil, while E. pan is widespread throughout Central and South America (Ratcliffe 2003; Gasca-Alvarez et al. 2008). Both species are nocturnal and come to light, and E. pan may be more restricted to forested areas than E. endymion (Ratcliffe 2003). A recent study by Puker et al. (2011) expanded the range of E. pan into the ecotone of the Brazilian cerrado-pantanal in Mato Grosso do Sul, and documented that adult activity of E. pan is nocturnal and highly seasonal most likely correlated with rainy periods. We hypothesized that we would find burrows of E. pan associated with G. weberbaueri and feeding damage by E. pan on the stems.
Quantitative sampling for beetles in bamboo and terra firma forests was conducted during June– August 2006 and January–March 2007 at the Los Amigos Research Center (LA) (12°34′S, 70°06′W; 270 m elevation), located in Manu province, Madre de Dios region, southeastern Peru. Los Amigos Research Center covers approximately 1,000 ha and borders the Los Amigos Conservation Concession, which includes 145,918 ha of undisturbed lowland rainforest (Pitman 2008). We used pitfall data from this study to analyze relative abundance patterns of adults of E. pan in bamboo and terra firma forest. To search for E. pan, describe its burrow, and observe its behavior, we conducted field work in March–April 2008 at the Tambopata Research Station (TRC) (13°08′30″S, 69°36′24″W; 350 m elevation), Tambopata province, Madre de Dios region, southeastern Peru. Tambopata Research Station is inside the Tambopata National Reserve and has several small and large patches of bamboo forest. Our two study sites in southeastern Peru have five major forest types: terra firma (upland forest, mature floodplain forest), primary successional floodplain forest, swamp forest, and bamboo forest. The bamboo forests at both of these sites are primarily comprised of G. sarcoparpa and G. weberbaueri (Griscom and Ashton 2006), and because it is difficult to distinguish these two species, we hereafter refer to both species, collectively, as Guadua bamboo. LA and TRC include all of these primary forest types, and they are approximately 82 km apart. Mean annual rainfall at TRC is approximately 3,150 mm and 2,850 mm at LA. Greater than 80% of the rainfall in this
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region occurs during the October-May wet season. The monthly temperature ranges between 21–27°C year-round at both sites, and there is a weak seasonal signal in temperature (Brightsmith 2004; Pitman 2008). As part of a larger study at LA that focused on beetle community structure in bamboo and terra firma forest (Jacobs 2009), beetles were collected from 13 different sized patches of bamboo forest and adjacent terra firma forest sites with unbaited pitfall traps. The pitfall traps were 0.5-L plastic containers, with a diameter of 11.0 cm and height of 7.0 cm. Traps were filled with approximately 0.1 L of a mixture comprised of 50% water and 50% ethanol (95% solution). A total of 150 pitfall traps were placed throughout 13 different patches of bamboo, ranging from one to 25 hectares in size, and adjacent terra firma forest. Four sampling periods were conducted in the dry and wet seasons (two in each season) where the pitfall traps were left open for seven continuous days and checked approximately every other day for flooding or drying of trapping liquid. The study conducted by the first author was not specifically designed to capture E. pan, but many E. pan individuals were collected, primarily in bamboo forest. For more detailed information on trap design and distribution, please refer to Jacobs (2009). From the sampling conducted in this larger study, we obtained relative abundance estimates for E. pan in both forest types. We used a Chi-square test to test the null hypothesis that there was no difference in abundance of E. pan individuals in the bamboo versus terra firma forest. Observations of burrow structure and behavior were mainly conducted at TRC, but we also made casual observations of E. pan burrows at LA on a later visit. After confirmation of the burrow presence at TRC, we proceeded to look for additional burrows, excavate burrows, and observe whether or not E. pan individuals were present and, if so, record their behavior. Because we had limited time in the field, and had no prior knowledge of where the burrows would be located or how many we would find, we confined our search and subsequent behavioral observations to areas along the established trail system of TRC and along transects that were created by other researchers. We found and marked a total of five active burrows during 22–30 March 2008. Active burrows were indicated by an entrance hole and a beetle. We found evidence of more than 15 additional inactive burrows at TRC, but focused on the active burrows for the following observations. For each active burrow that we marked, we returned to the burrow to make observations of beetle activity during night and daytime hours. For every burrow, we took detailed field notes and photographs.
We recorded the location, the height (cm) of the push-up (mound portion) of the burrow, the entrance diameter (mm) from the outer portion of the entrance hole, the first and second internode diameter (mm) of the bamboo stem (starting from the ground) to which the burrow was adjacent, the width (cm) of the push-up of the burrow (as an average of two cross-sectional measurements at the base of the mound), and the angle (degrees) between the bamboo stem and the ground adjacent to the stem. We measured this angle because we were interested in whether the beetles preferred a particular configuration of the bamboo (vertically straight or bent) which might give them easier access to the base of the stem when feeding. We excavated two burrows between 10:00 and 16:00 h, and we measured their length (cm) from the entrance to its terminus underground and the burrow height (cm) starting from the top of the entrance to the base of the burrow, perpendicular to the ground. Excavation of the burrows took approximately 4–6 hours each. While excavating the burrows, we took detailed field notes and photographs of the interior. We labeled the external part of the burrow as a “mound” and the internal portion of the burrow, running deep underground, as a “tunnel”.
RESULTS Relative Abundance. We found a highly significant difference in the abundance of individuals of E. pan collected in the bamboo forest versus the terra firma forest at LA (Chi-square results: v2 = 49.48, df = 1, P < 0.001). At LA, we captured 63 individuals of E. pan throughout various patches of bamboo forest separated by up to 6 km, and only five individuals of E. pan in terra firma forests. In addition, every E. pan individual was captured only in the wet season. Burrow Structure. All burrows of E. pan (n = 5) were located at the base of a bamboo plant and appeared as mounds of soil piled against a bamboo stem (Figs. 1, 2). Three of the mounds were initially open at the top, and the others were closed (covered with dirt). All mounds covered the base of a bamboo stem whose wood was stripped and shredded (Figs. 1–3). The underground portion of the burrows consisted of one primary tunnel running deep underground (>100 cm) with a few shorter offshoots extending from the primary tunnel (Figs. 1, 2). See Table 1 for a complete description of the size of the mounds and tunnels. Burrow #1 had the longest tunnel, and we found in it what appeared to be the larva of E. pan. The tunnel of this burrow contained several offshoots from the main tunnel, and one of the offshoots ended at a pile of wet, crushed leaves and sticks (Figs. 1, 3). Behind this pile of organic debris
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Fig. 1. Sketches of the burrow structure made by Enema pan. a) Profile view of entire burrow with offshoots; in this burrow, the end of the main tunnel was approximately 1 m underground, b) Close-up view of the top of the burrow, mound, and shredded portion of bamboo. The top of the mound (hatched marks) illustrates the portion of the soil that is removed at night when the beetle emerges and perches on the top of the mound.
was a small scarab larva. We were unable to confirm the species identification based on morphology because it was too small to identify. We are fairly confident that it was the larva of E. pan because it was located in an E. pan burrow 1 m underground. Additionally, we found this larva at the end of the same tunnel where we found the adult. We collected the organic debris associated with the larva, rinsed it with water, and dried it in order to better identify the material, which was not of bamboo origin but rather was comprised of other types of plants. The origin of the organic material was clearly from aboveground. Behavior. We observed active individuals of E. pan only at night, and all active individuals were males. At three of the five burrows, we observed an adult male perched at the top of the burrow entrance with his body protruding from the soil mound that was piled against the bamboo stem (Fig. 3). We observed these males moving their antennae. We hypothesized that they were waiting for/attracting females, but we never observed a female. When we approached the individual beetles, they would retreat into their tunnels, but re-emerged if we backed away. We additionally observed during daylight hours many other insects, including ants, solitary bees, nitidulid beetles, flies, and wasps, actively hovering and foraging on the exposed bamboo stems that were made accessible by the feeding of E. pan (Fig. 3). We also observed spiders waiting on the mounds, presumably to capture sap-feeding insects. No beetles
were visible when we returned to check the burrows during the day. In each excavated tunnel, we found one adult male at the end of the primary tunnel. We collected one male beetle from burrow #1 for observations and placed it in a container with soil. We observed this individual stridulating on the soil in the container. The beetle immediately began to excavate a tunnel and remain covered with soil. Because we had destroyed this beetle’s burrow, we placed him on top of an open, inactive-looking burrow that was approximately 2 m from the site of his original burrow. We returned to check on the beetle and, though we did not find him, we found fresh soil piled on top of the tunnel entrance indicating new digging activity. After excavating the second burrow, we also removed the male beetle and placed it on the ground outside of the tunnel entrance. He immediately began to dig into the soil. We reconstructed his burrow as well as possible, placed him on the entrance of the mound, and he quickly entered the tunnel entrance. Adult male E. pan do not walk easily in a horizontal direction across the ground and prefer to dig vertically into the soil.
DISCUSSION To our knowledge, our observations are the first report of the burrow structure of E. pan and its association with Guadua. Dynastine scarabs are diverse in South America and are frequently captured in light traps, but little is known about
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Fig. 2. Photographs illustrating the mound and burrow of Enema pan at the base of a bamboo stem. a) The mound at the base of a bamboo stem, b) Excavation of the mound, c) An excavated mound with a Swiss army knife (9 cm length) for perspective, d) The same excavated mound with pieces of pink flagging to illustrate the path of the underground portion of the burrow.
their life history (Puker et al. 2011). Though we observed only a small number of burrows of E. pan for this study, we observed a relatively high number of mound structures in bamboo forest habitat at TRC and LA, suggesting that local E. pan populations can be large. This observation, in addition to the high number of E. pan captured by pitfall traps in the quantitative study by Jacobs (2009), also agree with the observations in Keller’s (2003) study documenting that an area of 100 m2 of Chusquea habitat contained 38 active burrows and 17 inactive burrows. Populations of E. pan potentially represent a large amount of biomass in bamboo habitat because of the large size of both larvae and adults with either sex of the adults weighing, on average, 1.35 g (Puker et al. 2011). Based on our observations, it appears that male E. pan construct burrows at the base of Guadua stems, where they feed on the sap within the protection of their soil mounds. Based on two nest excavations, the beetle’s tunnels can extend at least 1 m underground, with additional side-tunnels.
Our observations contrast with a recent finding conducted under laboratory conditions, where the tunnels of E. pan averaged only 12.0 cm (Puker et al. 2011). It appears that E. pan spends daylight hours underground and emerges at night to feed and possibly attract mates. In shredding the base of the bamboo plant and exposing the soft interior, these beetles are allowing many other insects to have access to a sugary meal. We hypothesize that female beetles will find male burrows, mate with the males, and lay egg(s) inside the burrow where the larvae then develop. An adult beetle will provision the larva(e) with macerated leaves and sticks, although we do not know which sex provides the care. Unfortunately, we never observed female E. pan near or in the burrows. Species of Dynastinae are not known to care for their young, and so provisioning for larvae in a burrow would be highly unusual. Although the behavior of E. pan and its bamboo association appear tightly connected to Guadua, it is probably not a specialist on this genus of bamboo since the beetle has a broad distribution
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Fig. 3. Enema pan adult and larva. a) Male inside mound, b) Male perching on top of mound, c) Larva (inset) collected inside burrow along with wet, crushed leaves and sticks (main image), d) Male near burrow after excavation of burrow; this individual was found at the end of the main tunnel after excavation.
elsewhere where Guadua may not occur. However, the literature documenting the distribution of E. pan does not indicate the presence of bamboo in any of these localities. It is possible, therefore, that E. pan specializes on various bamboo species,
but, because it is taken at light traps, it is not associated specifically with a particular forest type or plant species. Based on laboratory experiments by Puker et al. (2011), E. pan will feed on a variety of foods.
Table 1. Measurements of burrows of Enema pan. Mound height represents the height of the soil push-up on the external portion of the burrow; entrance diameter is the diameter of the opening of the tunnel; 1st internode diameter represents the length of the first bamboo internode on the main stem beginning from ground-level; 2nd internode diameter is the length of the internode following the 1st internode; mound width is the average of two cross-sectional measurements at the base of the mound; angle is the measurement in degrees from the bamboo stem to the ground adjacent to the stem; burrow length is the measurement from the top of the mound entrance to the bottom of the tunnel underground perpendicular to the ground; tunnel length is the measurement of the total length of the primary tunnel beginning from the mound entrance to the end of the tunnel. Burrow numbers in bold italics were excavated. Mound Angle Burrow Tunnel Mound Entrance 1st internode 2nd internode Nest # height (cm) diameter (mm) diameter (mm) diameter (mm) width (cm) (degrees) length (cm) length (cm) 1 2 3 4 5 Mean SE
20.0 20.5 15.0 17.0 9.5 16.4 2.0
40.0 54.0 40.1 49.2 41.0 44.9 2.9
17.0 35.6 21.9 12.8 21.8 5.0
20.8 37.5 23.8 15.0 24.3 4.8
24.0 16.5 21.0 13.0 18.6 2.4
90.0 90.0 50.0 55.0 80.0 68.8 9.7
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A number of organisms, including a poison frog, Ranitomeya sirensis Aichinger (Brown et al. 2011), and bamboo rats, Dactylomus dactylinus Hilaire and Dactylomys boliviensis Anthony (Emmons and Feer 1990; Dunnum and Salazar-Bravo 2004), are strongly associated with Guadua habitat. However, these animals have been found living in areas without bamboo (Emmons and Feer 1990; Brown et al. 2011). The same is true for some bird species that exhibit a strong association with bamboo habitat, though some bird species are considered to be true bamboo specialists (Kratter 1997; Lebbin et al. 2007). Thus, many of these organisms may be facultative users of Guadua. Guadua, in addition to other bamboos, experiences large die-offs after a flowering event, and what was once bamboo habitat can quickly disappear (Nelson 1994; Griscom and Ashton 2003). Therefore, it seems that many organisms have evolved to facultatively use bamboo when it is present, but do not “risk” becoming specialists on this unpredictable resource. In the case of E. pan, more research is needed to understand whether or not this species is, indeed, a bamboo specialist. Regardless of the specialist status of E. pan in Guadua forests, we know that bamboo provides important habitat for this species.
ACKNOWLEDGMENTS The authors thank the Amazon Conservation Concession and Rainforest Expeditions for providing us with resources and access with which to carry out our study. We thank Jesús Ramos, Nigel Pitman, Mario Napravnik, Kurt Holle, and the staff at LA and TRC for facilitating field work logistics. Permits were issued by the Instituto Nacional de Recursos Naturales (INRENA), Peru (permit numbers 11-2008-INRENA-IFFS-DCB and 09-C/C-2008-INRENA-IANP). We thank Karina Ramírez and Carmen Jaimes for advice with permit applications. We thank Gerardo Lamas for support in the Entomology Department at the Museo de Historia Natural, Universidad de San Marcos, Lima, Peru and the Entomology Department at the California Academy of Sciences. This project was supported, in part, by an NSF/BS&I grant (DEB 0716899) to B. C. Ratcliffe and R. D. Cave.
REFERENCES CITED Brown, J. L., E. Twomey, A. Amézquita, M. Barbosa de Sousa, J. P. Caldwell, S. Lötters, R. von May, P. R. Melo-Sampaio, D. Mejía-Vargas, P. Pérez-Peña, M. Pepper, E. H. Poelman, M. Sánchez-Rodríguez, and K. Summers. 2011. A taxonomic review of the Neotropical poison frog genus Ranitomeya (Amphibia: Dendrobatidae). Zootaxa 3083: 1–120.
Brightsmith, D. J. 2004. Effects of weather on avian geophagy in Tambopata, Peru. Wilson Bulletin 116: 134–145. Davidson, D. W., J. A. Arias, and J. Mann. 2006a. An experimental study of bamboo ants in western Amazonia. Insectes Sociaux 53: 108–114. Davidson, D. W., S. R. Castro-Delgado, J. A. Arias, and J. Mann. 2006b. Unveiling a ghost of Amazonian rain forests: Camponotus mirabilis, engineer of Guadua bamboo. Biotropica 38: 653–660. Dunnum, J. L., and J. Salazar-Bravo. 2004. Dactylomys boliviensis. Mammalian Species 745: 1–4. Emmons, L. H., and F. Feer. 1990. Neotropical Rainforest Mammals: A Field Guide. University of Chicago Press, Chicago, IL. Erwin, T. L. 1997. Natural history of the carabid beetles at the BIOLAT Biological Station, Rio Manu, Pakitza, Peru, Supplement I. Additional records [pp. 359–368]. In: Manu: The Biodiversity of Southeastern Peru (D. E. Wilson and A. Sandoval, editors). The Smithsonian Institution Press, Washington, DC. Gasca-Alvarez, H. J., C. R. V. Fonseca, and B. C. Ratcliffe. 2008. Synopsis of the Oryctini (Coleoptera: Scarabaeidae: Dynastinae) from the Brazilian Amazon. Insecta Mundi 61: 1–62. Griscom, B. W., and M. P. S. Ashton. 2003. Bamboo control of forest succession: Guadua sarcocarpa in southeastern Peru. Forest Ecology and Management 175: 445–454. Griscom, B. W., and M. P. S. Ashton. 2006. A selfperpetuating bamboo disturbance cycle in a Neotropical forest. Journal of Tropical Ecology 22: 587–597. Griscom, B. W., D. C. Daly, and M. S. P. Ashton. 2007. Floristics of bamboo-dominated stands in lowland terra-firma forests of southwestern Amazonia. Journal of the Torrey Botanical Society 134: 108–125. Jacobs, J. M. 2009. Beetles in bamboo forests: community structure in a heterogeneous landscape of southwestern Amazonia. MSc thesis, San Francisco State University, San Francisco, CA. Janzen, D. H. 1976. Why bamboos wait so long to flower. Annual Review of Ecology and Systematics 7: 347–91. Keller, H. A. 2003. Mythical origin of Chusquea ramosissima (Poaceae), the ancient knife of the Guaranis. Economic Botany 57: 461–471. Kratter, A. W. 1997. Bamboo specialization by Amazonian birds. Biotropica 29: 100–110. Larsen, T. H., A. Lopera, and A. Forsyth. 2006. Extreme trophic and habitat specialization by Peruvian dung beetles. The Coleopterists Bulletin 60: 315–324. Lebbin, D. J., P. A. Hosner, M. J. Andersen, U. Valdez, and W. P. Tori. 2007. First description of nest and eggs of the white-lined antbird (Percnostola lophotes), and breeding observations of poorly known birds inhabiting Guadua bamboo in southeastern Peru. Boletín SAO 17: 119–132. Ledesma, K. J. 2003. Small mammal community of bamboo forests in the Peruvian Amazon. MSc thesis, Florida Atlantic University, Boca Raton, FL.
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Morales, V. R. 1992. Dos especies nuevas de Dendrobates (Anura: Dendrobatidae) para Peru. Caribbean Journal of Science 28: 191–199. Navarro de Andrade, E. 1928. Praga dos bambús. Rhinastus sternicornis (Germ.). Archivos Instituto Biológico de Defensa Agrícola e Animal 1: 127–144. Nelson, B. W. 1994. Natural forest disturbance and change in the Brazilian Amazon. Remote Sensing Reviews 10: 105–125. Nelson, B. W., and M. C. Bianchini. 2005. Complete life cycle of southwest Amazon bamboos (Guadua spp.) detected with orbital optical sensors. Anais XII. Simpósio Brasileiro de Sensoriamento Remoto, Goiânia, Brasil, 16–21 Abril 2005, INPE, p. 1629–1636. Olivier, J., T. Otto, M. Roddaz, P. Antoine, X. Londoño, and L. G. Clark. 2008. First macrofossil evidence of a pre-Holocene thorny bamboo cf. Guadua (Poaceae: Bambusoideae: Bambuseae: Guaduinae) in south-western Amazonia (Madre de Dios -Peru). Journal of Paleobotany and Palynology 153: 1–7. Pearson, D. L., and J. A. Derr. 1986. Seasonal patterns of lowland forest floor arthropod abundance in southeastern Peru. Biotropica 18: 244–256. Pitman, N. C. A. 2008. An overview of the Los Amigos Watershed, Madre de Dios, southeastern Peru. Amazon Conservation Association. Uncorrected
Draft. Available from: cicra.acca.org.pe/espanol/ paisaje_biodiversidad/los-amigos-overview9.pdf (Accessed 3 December 2011). Puker, A., S. R. Rodrigues, E. F. Tiago, S. Ide, and J. Fuhrmann. 2011. Notes on biology and behavior of rhinoceros beetle Enema pan (Coleoptera: Scarabaeidae: Dynastinae). Annals of the Entomological Society of America 104: 919–927. Ratcliffe, B. C. 2003. The dynastine scarab beetles of Costa Rica and Panama. Bulletin of the University of Nebraska State Museum 16: 1–506. Ruíz-Sánchez, E. 2011. Biogeography and divergence time estimates of woody bamboos: insights in the evolution of Neotropical bamboos. Boletín de la Sociedad Botánica de México 88: 67–75. von May, R., M. Medina-Müller, M. A. Donnelly, and K. Summers. 2008. The tadpole of the bamboobreeding poison frog Ranitomeya biolat (Anura: Dendrobatidae). Zootaxa 1857: 66–68. von May, R., M. Medina-Müller, M. A. Donnelly, and K. Summers. 2009. Breeding-site selection by the poison frog Ranitomeya biolat in Amazonian bamboo forests: an experimental approach. Canadian Journal of Zoology 87: 453–463. (Received 5 December 2011; accepted 6 May 2012. Publication date 20 September 2012.)