Observations on the nocturnal activity of lizards in a marshy area in Serra do Navio, Brazil

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1 Tropical Zoology ISSN: (Print) (Online) Journal homepage: Observations on the nocturnal activity of lizards in a marshy area in Serra do Navio, Brazil M. S. Hoogmoed & T. C.S. de Avila-Pires To cite this article: M. S. Hoogmoed & T. C.S. de Avila-Pires (1989) Observations on the nocturnal activity of lizards in a marshy area in Serra do Navio, Brazil, Tropical Zoology, 2:2, , DOI: / To link to this article: Published online: 01 Aug Submit your article to this journal Article views: 144 View related articles Citing articles: 5 View citing articles Full Terms & Conditions of access and use can be found at Download by: [ ] Date: 10 December 2017, At: 20:51

2 Tropical Zoolo~ 2: , 1989 Observations on the nocturnal activity of lizards in a marshy area in Serra do Navio, Brazil M.S. HooGMOED 1 and T.C.S. DE AVILA-PIRES 2 1 Nationaal Natuurhistorisch Museum, Postbus 9517, 2300 RA Leiden, The Netherlands 2 Museu Paraense Emilio Goeldi, DZO, Caixa Postal 399, Be/em, Pard, CEP 66001, Brazil Received 20 April 1989, accepted 31 July 1989 Lizards normally considered to be diurnal inhabitants of forest-floor leaf-litter were found, during field work in Serrado Navio, Amapa State in a rather special habitat, the margin of a large, marshy, open area at the side of a creek, completely surrounded by rainforest, with a thick layer of leaf-litter on a very wet and muddy substrate. In this location they were extremely numerous and active during nights with a nearly full moon. Some speculations about the causes for this behaviour are made. KEY WORDS: diurnal/nocturnal activity, rainforest, lizards, Brazil. Introduction Research area Methods Results Discussion Acknowledgements References INTRODUCTION Serra do Navio is situated near the centre of the Brazilian State of Amapa (old Territorio Federal do Amapa), about 170 km NW of the capital Macapa. Zoogeographically this part of Brazil forms part of Guiana as defined by HooGMOED (1979: ) and even of the restricted Guiana of DESCAMPS et al. (1978) and LESCURE (1977). The herpetofauna of this area has received little attention, although it has been visited by herpetologists who published on some species (WEYGOLDT 1980, 1981, 1982, 1983) or on certain groups (SILVERSTONE 1975, 1976) and by collectors for museums in Belem and Sao Paulo. Some data on the lizard fauna may be found in CuNHA (1961, 1967, 1970).

3 166 M.S. Hoogmoed and T.C.S. de Avila-Pires Within the framework of a study of the lizards of Amazonian Brazil (T.C.S. de Avila-Pires) and of a study of toads commonly referred to as the Bufo 'typhonius' group (M.S. Hoogmoed), the area was visited between November 3 and 23, 1988 by the present authors. RESEARCH AREA Our base was the Casa Central de Hospedes of ICOMI in the village of Serra do Navio, which is located on a small hilltop at an altitude of 170 m. The entire area consists of low rounded hills with valleys between them about m lower. Part of the area has been altered greatly because of manganese mining activities. Some hills have been completely stripped; in other places large areas are subject to open-cast mining and have been transformed into deep holes. Some reforestation with Pinus and Eucalyptus in these degraded areas is practiced. Most of the area is undisturbed and covered with primary rainforest (terra firme forest). This rainforest extends to within a few hundred metres of the houses of Serra do N avio and along most roads extending from the village, except in the mining area itself. Due to the well developed net-work of roads near the village, the rainforest is divided into more or less isolated sections. In the immediate vicinity of the village, creeks within the rainforest have been modified because of preventive health measures: in order to lessen the risk of the incidence of malaria the vegetation along the creeks has been cleared in a strip about 10 m wide on each side of the creek, whereas the creek beds themselves have been canalized. Thus, the amount of standing water in the creek-valleys, which could serve as breeding sites for malaria mosquitos, has been greatly diminished to the point of virtual absence. The area immediately adjacent to the creeks is exposed to direct sunlight and hardly shows a cover of leaf-litter. Regular maintenance prevents regeneration of the original vegetation. Fortunately the artificial changes have not visibly interfered with the rainforest on the hill opes bordering the creeks. Flat areas with vegetation remaining in the creek-valleys seem to have undergone some changes towards secondary vegetation. One of the rainforest areas modified in the manner described is enclosed by two roads and has a triangular shape. It is traversed by the Igarape (=creek) Pi~arra, which arises close to the village, descends a rather steep rocky ope, with several cascades and then continues through a nearly level area. Just before reaching another steep ope with cascades, there is a large, round, level, open marshy area just off the left bank of the creek. This area, with a surface of several hundreds of square metres, shows a low vegetation of rushes, grasses and herbs rooted in a very soft muddy bottom covered with a layer of water (Fig. 1). Because of the composition of the bottom and the danger of sinking into the mud the centre of the marsh could not be reached. The marsh is surrounded by rainforest, of which the edge apparently had been cleared away. The rainforest vegetation ends at the base of the gently oping hill-sides surrounding the marsh and is bordered by a swampy area with a soft muddy bottom with a vegetation of Tradescantia and grasses, and a thick layer of leaf-litter which was dry on the surface, but wet directly beneath. In this zone of varying width (10-30 m), there are several isolated trees, and some old logs mostly sunken into the mud, emerging for varying lengths. The history of the area is not known, but, although it is apparent that the area

4 Nocturnal activity of lizards in a marshy area ~ :... Fig Diagrammatic map of the marshy area. Densely stippled: marshy area; lightly stippled: rain forest; hatched: area collected. has been manipulated to a certain degree, especially at the edges, for the greater part it seems to be quite natural. The climate of the Serra do Navio area can be identified as Am of Koppen (SOMBROEK 1966) and has a mean total annual rainfall of about 2400 mm (Srou 1983). Rainfall is seasonal, with a rainy season from December-May and a dry season from June-November (ALDAZ 1971, Srou 1983). Annual mean temperature is 27 C, with daily fluctuations between 25 and 35 C, and temperatures at night between 20 and 25 C. Exact meteorological data of the area are not available to us, though data about the climate of Belem, which is comparable, area provided by ANONYMOUS (1982). METHODS During our stay in Serra do Navio between November 3 and 23, 1988 we spent 174 man-hours in the field, of which 49.5 were at night. During these trips several areas were visited. Due to its easy access the lgarape Pi~arra and the surrounding rainforest was regularly visited during our stay in Serra do Navio, both in daytime (3 times, total 10.5 hr) and at night (5 times, total 14.5 hr), always two people working together. During these visits the leaf-litter in the rainforest, the area at the base of trees between buttresses and leaf-litter and other refuse arranged in longitudinal heaps in the creek valley were carefully searched, as were tree trunks, branches, leaves, rocks and crevices. Specimens collected have been deposited in the Museu Paraense Emilio Goeldi, Belem, Brazil and in the Nationaal Natuurhistorisch Museum, Leiden, The Netherlands. RESULTS The lizard fauna of the lgarape Pi-;arra area turned out to be composed of 18 species: five Gekkonidae, four lguanidae, nine Teiidae, no Scincidae, a number which compares rather well with those given for other areas in lowland Amazonia by

5 168 M.S. Hoogmoed and T.C.S. de Avila-Pires DuELLMAN (1987: 492): Belem and Cuzco Amaz6nica both with 21. Further collecting might increase this number ightly. Eight species were found in both the creek valley, the adjacent forest, and the marshy area, while six were only found in the immediate surroundings of the creek and four were only found in the border area of the marsh (that is, in the open part, not in the forest bordering the marsh) (Table 1). From our observations in adjacent areas it was known that three of the last four species (Pseudogonatodes guianensis, Plica plica, Arthrosaura reticulata versteegii) are not restricted to that habitat, but also occur along creeks and/or throughout the forest, whereas Prionodactylus argulus was observed here only, and in other areas (El Triumfo, Ecuador; Benjamin Constant, Brazil) is known to occur in disturbed situations with primary rainforest bordering secondary vegetation (M.S. Hoogmoed personal observation). Elsewhere, these four species are known to be active in daytime (HooGMOED 1973, DIXON & SmNI 1986, DuELLMAN 1987). Of the six species found only near the creek or in the forest, the two species of Neusticurus are known to Table 1. Lizards species collected and/or observed in the lgarape Pi~arra area, Serra do Navio, Brazil in the period November 3-23, = present, - = absent, = eeping (the question-mark for one species refers to our doubt whether the specimen collected was eeping or active). The term marsh edge only refers to the outer border of the open marshy area, not to the forest surrounding it. Gekkonidae Coleodactylus amazonicus (Anderson 1918) Gonatodes annularis Boulenger 1887 Gonatodes humeralis (Guichenot 1855) Lepidoblepharis heyerorum Vanzolini 1978 Pseudogonatodes guianensis Parker 1935 Iguanidae Anolis c. chrysolepis Dumeril & Bibron 1837 Anolis fuscoauratus kugleri Roux 1929 Plica plica (Linnaeus 1758) Plica u. umbra (Linnaeus 1758) Creek/forest day night Marsh edge day night? Teiidae Alopoglossus angulatus (Linnaeus 1758) Ameiva ameiva (Linnaeus 1758) Arthrosaura reticulata versteegii Lidth de J eude 1904 Iphisa elegans Gray 1851 Kentropyx calcarata Spix 1825 Leposoma guianense Ruibal 1952 Neusticurus bicarinata (Linnaeus 1758) Neusticurus rudis Boulenger 1900 Prionodactylus argulus (Peters 1862) Totals Number of different species present 14 12

6 Nocturnal activity of lizards in a marshy area 169 occur only in association with running water (UzzELL 1966, HooGMOED 1973), the other four are either ubiquists (Gonatodes humeralis), arboreal (Anolis fuscoauratus kugleri, Plica umbra) or semiterrestrial (Anolis c. chrysolepis) forest inhabitants. All are considered to be diurnal lizards, and three of them were found, in the lgarape Pi~arra area, eeping at night: Anolis c. chrysolepis on leaves of low vegetation em above the ground; Neusticurus bicarinatus on branches over the creek or on rocks in it; and the only Plica umbra was collected on a vertical sapling 300 em above the ground. Kentropyx calcarata was active in the daytime and at night was found eeping exposed on low vegetation about 100 em above the ground. Ameiva ameiva was only observed active in daytime. During the night of November 19, 1988 (nearly full moon, cloudless sky, 24 C) starting at hr the swampy area described above was sampled. While working the edge of the area lizards of several species were observed, running over the leaflitter. Observing the first specimens it was thought they had been disturbed by our activity, but it soon became apparent by the sheer numbers and the activity displayed that this was not so. The lizards were active, probably foraging, but also chasing each other, [Alopoglossus angulatus males were actively pursuing females (some of which contained mature eggs), apparently as part of courtship behaviour]. Lizards were present all over the area, which is rather wet, though tending to be concentrated on ightly elevated and drier ground at the base of trees isolated from the closed forest on the hill opes surrounding the marsh. During 1 hr collecting in this area the following active species were obtained: Leposoma guianense, Alopoglossus angulatus, Lepidoblepharus heyerorum, Pseudogonatodes guianensis and Prionodactylus argulus. Moreover, eeping individuals of Plica plica (on a trunk 100 em above ground) and Kentropyx calcarata (three juveniles eeping together under moss on a low buttress) were obtained. A specimen of Gonatodes annularis was discovered under moss on the base of a tree, but it was not clear whether it was eeping or active when found (Table 2). To check whether this observation was just a chance occurrence, or whether it represented some regular pattern, we returned to the same area the next night (November 20, under the same lunar and climatic conditions). The results were comparable to those of the night before. All species active the night before were active again (of Prionodactylus argulus we obtained three recently hatched juveniles) and in addition active specimens of Coleodactylus amazonicus, Arthrosaura reticulata versteegii and Iphisa elegans were obtained (Table 2). From Table 2 it is clear that Leposoma guianense was the most abundant species and our removing 26 specimens the first night did not in the least affect their numbers during the second night. Alopoglossus angulatus was a good second, whereas numbers of the other species were distinctly lower. Of the eight species active at night in the edge of the swamp, five (Coleodactylus amazonicus, Lepidoblepharis heyerorum, Alopoglossus angulatus, Iphisa elegans, Leposoma guianense) had been taken active at daytime in the creek valley or the surrounding forest as well, whereas only Lepidoblepharis heyerorum on November 20, had been observed active at night both in the creek valley and in the swamp. The other three species (Pseudogonatodes guianensis, Arthrosaura reticulata versteegii, Prionodactylus argulus) are known to be diurnally active (HooGMOED 1973, and as stated above). Thus, seven of the eight active species never had been observed to be active at night before. It was remarkable that although Leposoma guianense is by far the most common

7 170 M.S. Hoogmoed and T.C.S. de Avila-Pires Table 2. Species of lizards and numbers of specimens collected (or observed) during two 1 hr nightly collecting periods (two people) in the edge of a swampy area surrounded by rain forest, near lgarape Pi~arra, Serra do Navio, Brazil, on November 19 and 20, XI 20.XI Active species Leposoma guianense 26 (25) Alopoglossus angulatus 9 6 (6) Prionodactylus argulus 1 4 Lepidoblepharis heyerorum 2 1 Pseudogonatodes guianensis 2 1 Coleodactylus amazonicus 1 Arthrosaura reticulata versteegii 1 Iphisa elegans 1 Sleeping species Kentropyx calcarata 3 Plica plica 1 Gonatodes annularis (31) forest leaf-litter inhabitant in the Serra do Navio area, numbers nowhere were approximately as high as in the swamp edge area (51 specimens in four personhours) '. Alopoglossus angulatus was rather common in the swamp edge area at night (21 specimens in four person-hours), whereas in the creek and adjacent forest area only one specimen was collected during 21 person-hours of daytime collecting. This might indicate that this species is less diurnal than we assumed. It should be noted here, that half the species observed at night in the wet swamp edge area, were also found in other places close to water (within 5 m, mostly within 1 m) (Leposoma guianense, Alopoglossus angulatus, Lepidoblepharis heyerorum, Pseudogonatodes guianensis). Of these, Leposoma guianense could also regularly be found further away from water. Coleodactylus amazonicus, Arthrosaura reticulata versteegii, Iphisa elegans and Prionodactylus argulus normally are not closely associated with water. DISCUSSION The large numbers of diurnal lizards, active at night in the swamp edge area, the same species not being active at the same time in adjacent areas where they were known to occur and had been observed to be active in daytime, led us to question what caused this extraordinary behaviour. All of the species active at night were not observed active during daytime in the swamp edge area (Table 1), and with one exception (Lepidoblepharus heyerorum), they were not active either at night in the ' During 21 person-hours of daytime collecting in the lgarape Pi~arra area only 16 specimens were obtained.

8 Nocturnal activity of lizards in a marshy area 171 creek valley and/or adjacent forest. An explanation for this behaviour might be found in the lunar phase and climatic conditions at the time of observations. On November 19 and 20 the moon was nearly full (full moon on November 23, 1988) and due to a cloudless sky in open places like the swamp there was a lot of light. This light, together with the agreeable air temperature of 24 C may have been the factor that caused these diurnal lizards in this specific area to become active at night. At the same time these species were neither active in the creek valley, which is covered by the crowns of trees overhanging it, nor in the adjacent forest, where the moonlight could not penetrate to the ground. Both on November 19 and 20 a little rain fell during the afternoon, but not a real shower. Unfortunately we were not equipped to measure light-intensities or rainfall, so our observations are rather incidental. Generally night-time activity of small nocturnal terrestrial animals from mammals to insects is reduced on full-moon nights (FRANKENBERG & WERNER 1979: 224). FRANKENBERG & WERNER (1979) and WERNER & FRANKENBERG (1982) did some laboratory tests with three taxa of related desert inhabiting geckos (Ptyodactylus hasselquistii group), now considered good species (HElMES 1987), one of which was diurnal, another nocturnal and the third (P. guttatus) diurno-nocturnal. It was established that in P. guttatus the amount of nocturnal and other activity gradually increased as the moon waxed and sharply decreased as it waned. The differences observed were significant. It is expected that moonlight suppresses the nocturnal activity of animals that run the risk of being preyed upon, but on the other hand will enhance that of predators hunting visually. Based on this assumption, it could be concluded that P. guttatus under full-moon conditions behaved like a predator rather than prey, with the moonlight extending the daily period of effective visual foraging. It was also established that the moonlight activity was not directly triggered by light level or photoperiod, because the experimental conditions ruled this out. To our knowledge comparable observations on rainforest lizards have not been made yet, but our observation in Serra do Navio seems to point in the same direction as the data obtained by FRANKENBERG & WERNER (1979). All of the lizards observed to be active at night during a nearly full-moon in Serra do Navio are small predators (active, visual hunters) on minute to small invertebrates of several groups, which normally inhabit rainforest leaf-litter. It can be hypothesised that in the daytime microclimatic conditions, especially air and water temperature and light intensity, at the edge of the swamp, at least during part of the day, are unfavourable to the small lizards concerned and that they consequently shifted their activity period to benefit from the bright moonlight and thus extend their active foraging period. Daytime microclimatic conditions in the creek valley and adjacent forest are more stable, as sunlight only can reach small areas on the forest floor for short periods, after which adjacent areas are illuminated and heated, due to the shifting of sunlight spots caused by openings in the foliage. In these areas moonlight intensity would be too low, due to the same principle, to activate diurnal lizards (assuming that the moonlight directly triggers the activity, for which, however, we do not have evidence). At the edge of the swamp, however, the moonlight reaches the ground unimpeded and microclimatic conditions may just be right for small diurnal lizards. The fact that not just some specimens were active, but on the contrary quite a number (in most species even more than in the daytime when calculated on the basis of time spent collecting), seems to strengthen the assumption that full-moon conditions in that specific area are more favourable than daytime conditions. It would be

9 172 M.S. Hoogmoed and T.C.S. de Avila-Pires worthwhile to test this hypothesis in suitable areas during long term studies. However, this hypothesis does not indicate what activity these lizards are engaged in on dark nights. Apart from being an interesting behavioural phenomenon, these massaggregations provide a ready opportunity to sample these lizard populations and to obtain at least some species that seem to be rarer in the datytime. Our present observations of nocturnal activity in lizards contradicts the widespread opinion that, except for Thecadactylus rapicauda and (the introduced) Hemidactylus mabouia, lizards in the Amazon basin are diurnally active (RAND & HUMPHREY 1968, DuELLMAN 1987). This may generally be true under normal conditions, but apparently it is not true in certain situations, where normally diurnal (to our present knowledge) lizards shift their activity to moonlit nights. It would be interesting to study the importance of this shift of activity for the life histories of the lizards concerned. Is it a regular part of their behaviour, does it only occur under special conditions, or have these «diurnal» lizards become nocturnal during part of the month? Such questions, and several others only can be solved by long-term studies. ACKNOWLEDGEMENTS Fieldwork was executed with the permission (EX-15/88) and the support of CNPq (grant /88.9 to O.R. da Cunha and grant /88-3 to T.C.S. de Avila-Pires). ICOMI (Industria e Comercio de Minerios S.A.) provided transport and lodging on their premises and put its staff at our service. Mr Loboto Goyana and Mr Rosa went out of their way to provide good working conditions for us. Dr Paulo Roberto Neme de Amorim of Serra do Navio shared with us his extensive knowledge of the local fauna, flora and topography. We gratefully acknowledge support for the fieldwork by O.R. da Cunha. REFERENCES ALDAZ L A partial characterization of the rainfall regime of Brazil. Report no. 4 DEMET/ SUDENE/WMO. Rio de Janeiro: National Department of Meteorologs of Brazil. ANONYMOUS Lander und Klima. Nord- und Siidamerika. Brockhaus Texte und Tabellen: Wiesbaden: F.A. Brockhaus. CuNHA O.R. DA II. Lacertilios da Amazonia. Os lagartos da Amazonia brasileira, com especial referenda aos representados na cob;:ao do Museu Goeldi. Boletim do Museu Paraense Emilio Goeldi 39: CuNHA O.R. DA Lacerdlios da Amazonia III: 0 genero «Arthrosaura» Boulenger, 1885 (Lacertilia, Teiidae). Atas do Simposio sabre a Biota Amazonica 5: CUNHA O.R. DA Lacertilios da Amazonia. IV. Urn novo genero e especie de lagarto do Territorio Federal do Amapa (Lacertilia-Teiidae). Boletim do Museu Paraense Emilio Goeldi 74: 1-8. DESCAMPS M., GASC J.P., LESCURE J. & SASTRE c Etude des ecosystemes guyanais. II. Donnees biogeographiques sur la partie orientale des Guyanes. Comptes Rendus des Seances de la Societe de Biogeographie 467: DIXON J. & SoiNI P The reptiles of the upper Amazon basin, Iquitos region, Peru. Milwaukee: Milwaukee Public Museum, VII 154 pp. DUELLMAN W.E Lizards in an Amazonina rain forest community: resource utilization and abundance. National Geographic Research 3: FRANKENBERG E. & WERNER Y.L Effect of lunar cycle on daily activity rhythm in a gekkonid lizard, Ptyodactylus. Israel Journal of Zoologs 28:

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