Patrones de visita a saladeros por el tapir (Tapirus terrestris) y la paca (Cuniculus paca) en la selva Amazonica de Ecuador.
Geophagy, or the intentional consumption of soil by animals, is a behavior frequently observed in several species of mammals and birds (Klaus and Schmid, 1998; Gilardi et al., 1999; Krishnamani and Mahaney, 2000; Brightsmith and Munoz-Najar, 2004; Montenegro, 2004; Tobler et al., 2009; Blake et al., 2010). Although several hypotheses regarding the potential benefits that animals obtain from soil eating have been proposed, the two most accepted hypotheses suggest that geophagy (1) may provide minerals not readily available in an herbivorous diet (Kreulen, 1985; Johns and Duquette, 1991; Holdo et al., 2002; Mills and Milewski, 2007) and (2) may aid in detoxifing plant secondary compounds consumed by herbivores (Oates, 1978; Krishnamani and Mahaney, 2000). Studies conducted in several tropical ecosystems have shown that, in general, soils at mineral licks contain higher concentrations of certain physiologically important elements (e.g., sodium, calcium, potassium, iron) when compared to those collected in other areas of the forest floor (Emmons and Starck, 1979; Klaus and Schmid, 1998; Brightsmith and Munoz-Najar, 2004; Lizcano and Cavalier, 2004; Montenegro, 2004; Mahaney et al., 2005). Despite the lack of a complete understanding on the potential function of geophagy, animals seem to obtain benefits from soil consumption.
Geophagy can vary seasonally and geographically, and could serve different purposes for different taxa. For example, geophagy is widespread in most howler monkey and spider monkey populations living in western Amazonian forests near the northern Andes (Izawa, 1993; Blake et al., 2010; Link et al., 2011) but has not been reported for Meso-american populations (Ferrari et al., 2008). In white-tailed deer (Odocoileus virginianus) soil consumption is seasonally sex-biased, with females visiting licks more frequently during lactating periods, while males visit licks more frequently during the annual periods of antler growth (Atwood and Weeks, 2003). Also, some species in Bornean inland forests, such as sambar deer (Cervus unicolor) and bearded pigs (Sus barbatus), preferentially visit licks with the highest concentration of minerals, whilst other species do not (Matsubayashi et al., 2007).
In the Neotropics, mineral licks are common in western Amazonian lowland rain forests (Ferrari et al., 2008; Lee et al., 2009). Frequent visitors to lowland mineral licks include tapir (Tapirus terrestris), peccaries (Tayassu pecari, Tayassu tajacu), brocket deer (Mazama americana), paca (Cuniculus paca), as well as several bat species, howler monkeys (Alouatta sp.), and spider monkeys (Ateles sp.) (Izawa, 1993; Montenegro, 2004; Voigt et al., 2008; Tobler et al., 2009; Blake et al., 2010; Link et al., 2011). Only scant information is available on mineral lick visitation patterns by animals over long periods of time (Ferrari et al., 2008; Lee et al., 2009; Tobler et al., 2009). Long-term studies, however, are crucial for investigating the proximate factors that trigger mineral-lick visitation (Burger and Gochfeld, 2003; Brightsmith, 2004; Montenegro, 2004).
The diet of tapirs (Tapirus spp.) is based almost exclusively on leaves, fiber and fruits (Bodmer, 1990; Henry et al., 2000; Galetti et al., 2001). Although both lowland tapirs (T. terrestris) and mountain tapirs (T. pinchaque) visit mineral licks frequently (Lizcano and Cavalier, 2000; Montenegro, 2004; Tobler et al., 2009), there are only scant data available on temporal patterns of mineral lick use by either species. Montenegro (2004) proposed that lowland tapirs (T. terrestris) might use mineral licks as a source of sodium as the fruits and leaves included in their diet had much lower sodium concentrations when compared to the lick soil. Lowland pacas (C. paca) mainly rely in fallen fruits and nuts in their diets (Emmons and Feer, 1997) and have been reported to also use licks frequently in western Amazonia (Blake et al., 2011)
Here, we report data on patterns of visitation by lowland tapirs and lowland pacas to mineral licks located in lowland Amazonian Ecuador. We first describe the frequency and temporal patterns of mineral lick visitation and then evaluate the influence of several environmental variables on lick visitation patterns by these two Neotropical mammals.
Data were collected at the Tiputini Biodiversity Station (TBS) in the Yasuni Biosphere Reserve in eastern Ecuador. The study area is an undisturbed tropical rain forest located on the northern bank of the Rio Tiputini (0[degrees]37'S, 76[degrees]10 W) at approximately 200-270 m a.s.l. Mean annual precipitation is 2800 mm with peak rainy season between April and August (Blake et al., 2010). The study area is mainly comprised by varzea and terra firme forests with small patches of swamps dominated by Mauritia flexuosa palms. TBS has a diverse community of mammals, including at least 10 primate species and several other terrestrial mammals, many of them that visit mineral licks frequently (Blake et al., 2011). The spatial distribution of mineral licks at the study area is described in Link et al. (2011) and Blake et al. (2010; 2011).
Camera- and video-trap methods
We monitored four mineral licks that were each regularly visited by forest mammals and birds using both still camera and video camera traps (Link et al., 2011). Based on camera placement, we were able to obtain data on all visits by lowland tapirs at two of those licks and on all visits by pacas at one lick. The first mineral lick (ML-1) is a small cave where animals enter to eat soil and drink water. All animals that visit this mineral lick must pass through the cave's narrow entrance, thus allowing us to record all visits as well as the duration of each visit. We set two camera traps and a video camera trap aimed at the entrance of the cave, thus recording all visits from both tapir and pacas. The second mineral lick (ML-2) consists of a swampy area in the forest floor. One camera trap and one video camera were set at this lick, but given their placement within the lick, they could only reliably detect all visits by large animals such as tapirs. Smaller ground mammals (including pacas) could have been missed by the cameras on some visits, and thus we exclude data from this lick from our estimates of the lick visitation rate by pacas.
Camera settings, data collection and analyses are described in detail in Link et al. (2011). Still and video camera traps were used to monitor the two mineral licks. Video cameras (Hunter's Harvest) recorded the activity at the lick continuously while still cameras (Snapshot Sniper) were set to take pictures at 10 sec intervals. Briefly, for every photograph or video recording containing a tapir or paca, we recorded the date and time of the picture, as well as the beginning and ending time of the visit. We considered "independent visits" those that were spaced by at least 1 h from another conspecific visit.
We estimated the "monthly frequency" of mineral-lick use by tapirs and pacas by calculating visitation rates at each site as the number of visits per day that cameras were working during the month. We only estimated visitation rates for months that were sampled for at least seven days. For ML-1, "visit durations" for tapirs and pacas were estimated by calculating the time between when an individual entered and left the cave during each independent visit to the lick.
In order to test if the frequency of mineral-lick visitation was associated with either monthly rainfall or with the number of dry days per month, we collected daily data on rainfall using a RainWise Tipping Bucket Rain Gauge, and for those months that had missing data we estimated the expected rain and number of dry days per month based on the proportion of days sampled during that particular month. Spearman rank correlation was used to assess the relationship between frequency of visits by tapirs and pacas versus both monthly rain and the number of dry days per month.
During each day of the study, we also collected qualitative data on weather conditions at 5-minute intervals between 06:00 and 18:00 h using the following index that describes cloud cover, precipitation, and luminosity: 1 = dark/rain; 2 = dark/overcast; 3 = clear/overcast; 4 = partly cloudy; 5 = sunny. For each sampling night, we also obtained data on lunar phase, as well as on lunar rise and set times, from the website www.timeanddate.org, for Quito, Ecuador, the nearest large city. These data were used to calculate the percent of lunar illumination for each night in order to evaluate if either tapir or paca had preferences (1) for visiting mineral licks during nights with greater illumination and/or (2) for hours when the moon was present relative to other, darker hours of each night.
From August 2006 through April 2009 we completed a total of 888 days and nights of camera trapping, split amongst the two mineral licks we monitored at TBS (Table 1); an additional 49 days and nights were also sampled for ML-1 during pilot work in June-July 2005 and January-July 2006. ML-1 was monitored for 369 days and nights between August 2006 and November 2007, and ML-2 was monitored from July 2007 until April 2009 for a total of 519 days and nights.
We recorded a total of 480 independent visits by lowland tapirs during the main study phase, and an additional 38 visits were noted during the pilot phase. For pacas, we recorded a total of 191 mineral lick visits during the main study period and an additional 31 visits were noted during pilot work. Multiple other species of birds and mammals also visited these licks frequently (Link et al., 2011). Not unexpectedly, tapir and paca used the mineral licks strictly during the night (Fig. 1). Lowland tapirs visited the mineral licks on 293 out of the 888 nights sampled, or roughly 33% of nights. On a monthly average, tapirs visited the ML-1 lick at higher rates (0.54 [+ or -] 0.20 visits per night; range 0.28-0.86 visits per day, N = 16 months) than ML-2 (0.21 [+ or -] 0.15 visits per night; range 0-0.52 visits per day, N = 22 months). Pacas visited the lick on 122 out of the 369 nights sampled at ML-1, also approximately 33% of nights. Pacas visited the lick on a monthly average (0.32 [+ or -] 0.31 visits per night; range 0 - 0.89 visits per day, N = 16 months). On nights of visitation, up to five tapir visits (mean [+ or -] SD = 1.6 [+ or -] 0.8) and up to four paca visits (mean [+ or -] SD = 1.6 [+ or -] 0.7) were recorded per mineral lick. Due to the lack of individual recognition, we were unable to determine the exact number of unique animals that visited the mineral licks each night. Nevertheless, based on body marks such as scars, we were able to confirm that individual tapirs and pacas occasionally made multiple visits to a lick during a single night and also that several individuals from each species sometimes visited the lick on the same night.
[FIGURE 1 OMITTED]
Tapirs visited the mineral licks almost evenly throughout the night with peak visitation at around 21:00 h, nonetheless there was an evident decrease in visitations from just before to around sunrise: visits between 04:30 h and dawn only accounted only for 3% of all visitations. Pacas visited the mineral lick most frequently during the first half of the night, with 83% of their visitations taking place between 19:30 h and 01:30 h.
The position of our cameras focused on the entrance to the cave at ML-1 allowed us to record the entrances and exits of individual tapir and paca. Out of 323 visits where we were able to record the duration of tapir visitations at ML-1, individual animals spent an average of 21.8 [+ or -] 9.2 min (range = 2-63 min) inside the cave, and 50% of the visitations were between 16 and 26 min long. Out of 214 paca visits, the average duration of visits was 15.0 [+ or -] 8.8 min (range = 1-51 min), and 50% of visitations were between 9 and 18 min long.
We found no support for the hypothesis that either tapir or paca visitation rates were influenced by seasonality, as assessed through either monthly rainfall (tapir: Spearman's Rho, = 0.179, P = 0.51; paca: Spearman's Rho, = -0.092, P=0.74) or the proportion of dry days per month (tapir: Spearman's Rho = 0.213, P = 0.43; paca: Spearman's Rho, = -0.076, P = 0.78). On the other hand, tapirs visited mineral licks more frequently on nights following days with higher daily average weather scores than expected by chance ([chi square] = 11.5, df = 3, P=0.009). This pattern, however, was not found for paca [chi square] = 2.73, df= 3, P=0.435) (Fig. 2).
[FIGURE 2 OMITTED]
[FIGURE 3 OMITTED]
The percentage of the night illuminated by moonlight did not influence the nocturnal visitation patterns of either lowland tapir or paca. Both species visited the mineral lick throughout the lunar cycle, visitations were relatively evenly spread across phases of the cycle (Fig. 3), and there were no differences in the rates of visitation by tapir ([chi square] = 6.69, df = 9, P=0.67) or paca [chi square] = 4.18, df= 9, P=0.90) on nights with different percent of lunar illumination.
Finally, within nights, neither tapir nor paca preferentially visited the mineral lick during either the dark or illuminated periods of the night. Assuming that the expected number of visitations occurring while the moon was present (i.e. above the horizon) was proportional to the number of nights that the moon was above the horizon, visitations to mineral licks showed no deviation from what was expected by chance alone, either for tapir ([chi square] = 10.01, df = 9, P = 0.350) or for paca ([chi square] = 11.9, df = 9, P = 0.220).
Several studies on vertebrate geophagy have found seasonal variation in the use of mineral licks (Jones and Hanson, 1985; Atwood and Weeks, 2003). The two main hypotheses to explain this seasonality refer to either (1) observations of seasonal variation in animal diets (possibly associated with periods of fruit availability and scarcity) and thus to periods in which animals may have to contend with higher concentrations of plant secondary metabolites or seasonal shortages of key mineral nutrients, or (2) animals' need to supplemental diet with certain minerals during particular life history episodes (e.g. pregnancy or lactation) (Brightsmith, 2004; Voigt et al., 2007). However, contrary to expectations, we did not find that the visitation patterns of either tapirs or pacas to mineral licks varied across the year, as has indeed been found for mammals (Montenegro, 2004) and birds (Brightsmith, 2004) living elsewhere in Amazonia. One reason for this may be the fact that at the TBS site, rainfall patterns and fruit availability are relatively non-seasonal when compared to other Neotropical forests (Di Fiore, 1997; Link, 2011).
We did find, however, that patterns of mineral lick visitation by tapirs and pacas were related to weather conditions both before and around the time of visitation, as has been described for parrots at Tambopata, Peru (Brightsmith, 2004) and for primates at the same site in lowland Ecuador (Link et al., 2011). For at least lowland tapirs, mineral lick visitation was strongly biased towards the nights preceded by clear and sunny days, while visits after rainy conditions were rare.
The use of mineral licks by tapirs and pacas seems to be intensive and habitual, rather than opportunistic, thus highlighting the importance of these sites to these taxa in western Amazonian rainforests. To date, the precise environmental, structural, and chemical characteristics of mineral licks that make them important sites for so many different animal species remain unclear, but prior research highlights several possibilities. Other studies have found distinct differences in mineral composition between licks and control sites, with licks mostly characterized by higher concentrations of certain metabolically-important elements such as sodium and calcium (Brightsmith and Munoz-Najar, 2004; Montenegro, 2004; Voigt et al., 2008). Tapir and paca visited mineral licks at the TBS site frequently throughout our study period, suggesting that licks provide key resources for them as well (Montenegro, 2004). Nevertheless, not much is known of the ranging behavior of individual tapirs in western Amazonian forests (but see Tobler, 2008), and further study is needed to evaluate individual rates of visitation and to determine whether individual tapirs restrict their visitations to just one mineral lick or, rather, visit multiple ones.
As more data are gathered at the regional and local level on (1) the geographical availability and characteristics of mineral licks used by mammals (as it has been recently done for parrots: Lee et al., 2009) and on (2) the overall use of these sites by mammals, both through the direct study of mineral licks themselves and through more indirect study of the ranging patterns of animal visitors, the more we will continue to expand our current understanding of geophagy and mineral lick use by Neotropical rain-forest mammals.
Recibido 5 agosto 2011. Aceptado 8 octubre 2011. Editor asociado: J Pereira
We are very grateful to the Ecuadorian government and the Ministerio de Ambiente for permission to work in the Yasuni region, and we especially thank the Waorani communities of Guiyero and Timpoka for allowing us to work in their traditional lands. Special thanks are also due to Drs. David Romo and Kelly Swing and to 'los tigres' of the Tiputini Biodiversity Station, who have all provided us with invaluable scientific and logistical support over many years. This research would not have been possible without the field assistance of numerous students and colleagues, especially A. C. Palma, M. Ramirez, and M. Montague. An earlier version of this manuscript was improved with valuable comments from D. Brightsmith, J. Rothman, J. Pereira and two anonymous reviewers. Funding was provided by the National Science Foundation, the Wenner-Gren Foundation for Anthropological Research, the L.S.B. Leakey Foundation, the Faculty and GSAS at New York University (NYU), and the New York Consortium in Evolutionary Primatology (NYCEP). This research project was done in full agreement with Ecuadorian legislation and complied with host country and institutional policies concerning ethical research and treatment of wildlife.
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Andres Link (1,2,3), Anthony Di Fiore (1,3), Nelson Galvis (1,2), and Erin Fleming (1)
(1) Proyecto Primates, Carrera 11a No. 91-55, Bogota, Colombia [Correspondence: Andres Link <firstname.lastname@example.org>]. (2) Departamento de Ciencias Biologicas, Universidad de Los Andes, Carrera 1 No. 18A-12, of. J-301, Bogota, Colombia. (3) Department of Anthropology, University of Texas, 1 University Station, C3200, Austin, TX 78712 USA
Table 1 Camera and video trap sampling effort at two mineral licks in Tiputini Biodiversity Station, Ecuador. Mineral Sampling period Sampling Sampling frequency Total days lick period (d [mo.sup.-1]) and nights (mo) sampled Median (range) ML-1 01-August-06 to 16 25 (10-30) 369 19-November-07 ML-2 19-July-07 to 22 26 (7-31) 519 23-April-09
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|Author:||Link, Andres; Di Fiore, Anthony; Galvis, Nelson; Fleming, Erin|
|Date:||Jun 1, 2012|
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