Camera trapping article; blogged but not published

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  This is a copy of a recent submission for publication. The results of the editing process have changed the paper to the point where it will be different enough from its current form that I feel comfortable in posting it on Biokryptos. I omitted figures in the paper which appear in a previous post on the same subject.  Enjoy!





Abstract
The Guiana Highlands of northern South America contain a unique ecoregion known as Pantepui, a biogeographic unit composed of topographically semi-isolated plateaus known as tepuis, which are host to a high level of endemic vascular plants. The current scholarly consensus defines the fauna of Pantepui as being being primarily composed of partially endemic herpetofauna, some endemic avifauna, no endemic mammals and depauperate of >5 kg wide ranging lowland mammals. Despite this, periodic sightings of wide ranging lowland Guiana Shield mammals have been reported from the summits of the eastern sector of Pantepui since initial exploration in the 1930s to the current date: the presence of which represents an epistemological discontinuity in the scientific knowledge of Pantepui faunal distribution. In an attempt to resolve this discontinuity a camera trapping pilot study was initiated in January 2012 on the summit of Auyan Tepui. The camera traps recorded images of the crab-eating fox Cerdocyon thous thous on the southern slopes of Auyan Tepui at 1010 metres. This pilot study is the first instance of camera trapping on a tepui summit, and confirms that wide ranging Guiana Shield hypocarnivorous mesopredators are able to access tepui talus slopes and by extension tepui summits. The range, distribution, and population dynamics of C. t. thous in the Pantepui remains unclear, as does its interaction with tepui summit biota. Establishing the interactions between lowland organisms and tepui summit biota has important immediate conservation implications, as anthropgenic climate change is predicted to result in a >80% habitat loss in the Pantepui by 2100 C.E. The 2012 camera trapping pilot study indicates that the use of camera trapping surveys can contribute positively to future conservation efforts and scientific research in the Pantepui.

Article

INTRODUCTION

The tepuis of northeastern South America are topographically isolated mesas comprised of uplifted Precambrian rock, which compose a 5,000 square kilometre biogeographical region known as the Pantepui (Huber 1988, McDiamid and Donnelly 2005) located in the Guiana Highlands (GH) situated on a craton known as the Guiana Shield (GS). The region is host to a high level of endemic vascular plants; 65% endemic to the GS, 33% are endemic to the GH, and 25% of organisms are endemic to individual tepui summits (Nogue et al. 2009). Pantepui is considered to be an important element for both the current and future biodiversity of northern South America (Rull 2005, Vegas-Vilarrubia et al. 2012). Conservation of the GS and the GH vary from country to country, though the region is sparsely populated and considered to be pristine. Venezuela has conserved some 30% of the GS in its borders in a variety of parks and national monuments, including Canaima National Park. Canaima is a 30,000 square kilometre UNESCO World Heritage Site which hosts ecotourism and acts as watershed for the Guri Dam (Gutman 2002, Hallowell and Reynolds 2005). Canaima contains tepuis classified by Huber as belonging to the Eastern Sector of Pantepui, which comprises Roraima, Auyan Tepui and the Chimanta Massif as well as 14 other smaller tepuis (Huber 1988, Berry and Huber 1995). Surveying of the summits of the tepuis has been conducted periodically by major universities and scientific institutions since their formal discovery; however long term expeditionary research is lacking (Myers 2000, Nogue et al. 2009). The known fauna of the tepui summits is composed almost exclusively of birds and reptiles, and the herpetofauna has a high degree of endemicity (Senaris and MacCulloch 2005, De Avila Pires 2005), although the paleofaunal origin theory for tepui faunal distribution has been largely disproved (Rodder et al. 2010, Salerno et al. 2012). No endemic mammal species have been observed or catalogued on tepui summits; even the Roraima mouse Podoxymys roraimae is considered to be present outside of Roraima where it was originally catalogued (Linares 1998, Patton et al. 2012). Lowland organisms which reside in the GH or were intermittently reported on the tepui summits tend to be members of wide ranging GS clads, as larger organisms in the five kg and above range have not been recorded as being consistently present on any tepui summit (Huber 1988, Lim et al. 2005). However, recent articles indicate that the brown-nosed coati Nasua nasua vittata is present on the summits of Roraima and individual tepuis in the Chimanta Massif (Havelkovaet al. 2006, Robvinskyet al. 2007), and some lowland mammals have been observed rarely on the tepui summits (Tate 1939, Huber 1988, Ochoa et al 1993). The extent to which larger mammals and members of carnivora are present on the summits and talus slopes of the tepuis has never been assessed due to the lack of long term field studies on the fauna of the tepui ecosystems. This lack of long duration field work has produced a knowledge gap concerning the faunal composition of the tepui summits, in which the influx of wide ranging lowland GS organisms is unknown.


In an effort to close this knowledge gap, a camera trapping pilot study was initiated from January 6th to January 13th 2012, conducted by an expeditionary team travelling along a path to the summit of Auyan Tepui colloquially referred to as the “Laime Trail”. With a summit area of nearly 700 square kilometres and a talus slope area of 200 square kilometres, Auyan is the largest tepui in terms of continuous summit area, (Huber 1988) and may hold the highest biological carrying capacity of any tepui (implied by species diversity; see Jaffe et al. 1993, Myers and Donnely 2005). Camera trapping was selected as the most effective methodology to investigate the presence of larger lowland mammals on the tepui summits, based on the methods' proven success in capturing cryptic and/or elusive species, as well as species with low population densities (Carbone et al. 2001, Silveria et al. 2003, Srbek-Araujo and Chiarello 2005, Rovero et al. 2008, Tobler et al. 2008).

Survey area

  Satellite image of Auyan Tepui showing camera trapping locations on the 'Laime Trail'; southern portion of Auyan Tepui (yellow pins denote camera trap/camp locations). Pin # 1 is Campo Guayaraca, 1,010 metres in located in mid-altitude mountain forest.  Pin no. 2 is camp Peñón 1,838 metres altitude, pin # 3 marks camp Naranja  2,161 metres altitude.  Image obtained courtesy of Google Earth (c) Google 2012. Satellite image taken by U.S.G.S. 12/31/1969



The survey area is the southern talus slopes and summit of Auyan Tepui (N 5°55' W 62°32'), along the Laime Trail, which is roughly identical to the trail used by the first scientific expedition to the summit of Auyan Tepui led by G. H. H. Tate in 1937-38 (Tate 1938, Chapman 1939). This area also serves as the primary point of entry for tourist expeditions to the summit. Camera traps were placed at Campo Guayaraca, (1,010 metres altitude, N 5º 41.084' & W62º 31.483) on the tepui talus slopes, and on the tepui summit at Peñón (1,838 metres altitude, N 44.665' & W62º 32.452) and Naranja (2,161 metres altitude,N 46.415' & W62º 31.969'). The ecosystems encountered on the trail and camera trap locations varied from mountain forests to rocky tepui summit meadows dominated by herbaceous assemblages (fig. 1).

METHOD

The pilot study methodology was the nocturnal utilization of camera traps at multiple camp locations as the expedition proceeded along the Laime Trail on the summit of Auyan Tepui. The expedition team also performed an ad hoc transect survey of the south of Auyan Tepui, and reconnaissance of locations for future camera trapping exercises was undertaken. Two Moultrie D55 IR GameSpy (Moultrie, Alabama, U.S.A) camera traps were utilized, using different settings and designated Biokpt 1 and Biokpt 2. Biokpt 1 was set up to include still shots and five second videos at a low resolution (1280 x 969; 1.3 mega pixel photographs, 320 x 240 video segments); Biokpt 2 was configured to take multiple photographs at medium resolution (2048 x 1536; 3.2 mega pixels). The info strips and infrared flash were set to “on”; all other functions were left on the default settings. The traps were baited with leftover food scraps from the expedition team, and two cameras were positioned in close proximity to obtain optimum images of animals attracted to this bait. Cameras were located as far away from camp as feasible, in practicality between 10 and 50 metres. The cameras were placed approximately 60 centimetres above ground, and were attached to trees along natural trails using straps provided with the cameras or placed on rocks when trees or bushes were not available. Altitude and GPS coordinates of the camera trap locations were recorded (fig. 2 and 3).
 Camera trap placement at Campo Guayaraca, 1,010 metres in mountain forest. Camera s were placed facing baited capture zone.
 Camera trap placement on the summit of Auyan Tepui at Pemon 1,838 metres on rocky surfaces amid tepui meadows. Suitable trees for camera attachment were not found.

RESULTS

Each camera was operational for 166 hours in the field, producing 332 camera hours, or approximately 13.8 camera days (a “camera day” is the number of cameras multiplied by the number of days they are operational). At Campo Guayaraca, the camera traps recorded images of a crab-eating fox (fig 4, video 1), Cerdocyon thous thous 50 metres from the camp in an upland to low-mountain forested environment. Fox subspecies classification is based upon the physical features of the fox, as well as the known distribution of foxes in this region (Bisbal 1988, Hallowell and Reynolds 2005, Tchaick et al. 2006). A medium sized canid, Cerdocyon thous weighs on average 5-7 kg, and is identifiable by a moderately bushy tail with a black or dark tip, narrow pointed head, dark pelage from the dorsum to the midline, and light coloured ventral pelage, although significant pelage colour variation is known (Berta 1982). Two subspecies are known in Venezuela; C. t. aquilis in the eastern portion of the country, and the GS subspecies recorded in this camera-trapping study C. t. thous (Bishal 1988). All five subspecies of Cerdocyon thous are classified as stable through their range, and have a IUCN classification of Least Concern (LC), though all subspecies are subject to variable rates of hunting (IUCN 2012). From the images recorded in the camera trap video sequences, it seems as though the fox is startled by the infrared flash of the cameras, but is not engaged in trap avoidance behaviour; a concern in camera trap studies (Sequin et al. 2003). Vertebrates sighted during the transect survey are: one lizard, one frog and several small rodents at Naranja camp (2,161 metres), one frog at Guayaraca (1,010 meters). Species identification for these animals are were not stated (Pomares, personal communication).

DISCUSSION

There exists no study of the general population dynamics for crab eating foxes in the Guiana Highlands, and the total population of C. thous across South America can only be inferred from studies on localized populations (Tchaick et al. 2009). There are numerous studies involving camera trapping that did included C. thous captures that were conducted across various ecosystems across South America. In the Bolivian Chaco, four years of camera trapping (2001-2005) resulted in 215 photos of Cerdocyon thous (Maffei et al. 2007). A study in the Emas National Park in Brazil, conducted over the span of one year using eighty two camera traps, produced a capture rate of 93 captures out of 157968 camera trap hours, with a calculated photographic rate defined in photographs/hour at between 0.000106 to 0.000980 depending on habitat (Jacomo et al. 2004). Camera trapping the Parque Estadual Carlos Botelho using seven to ten camera traps over 922 days produced 17 photos of Cerdocyon thous, with the time from set up to initial capture being 31 days (Beisiegel 2009). The 2012 Auyan Tepui pilot study capture per camera hour rate is comparatively high at between 0.0421 and 0.0361 for the two cameras with set-up to capture being a single day; however the brevity of the study makes any statistical comparison with other studies problematic. Only a longer study or series of short term studies in the Pantepui region would yield enough data to make valid and useful comparisons. Beyond brevity, the camera trapping study was hampered by constant rain which prevented camera set-up more than 50 meters from camp sites, a lack of suitable trap sites and problematic trap set up on tepui summit meadows. In future efforts, pre-built structures must be made to attach the cameras to, as tepui meadows do not contain sufficiently thick trees to affix the traps. It is unfortunate this is the first instance of camera trapping and investigation into the fox population of the tepui slopes; a contemporary analysis would provide a baseline for comparison.


Despite the knowledge gap regarding the distribution of larger carnivores on the tepui summits, C. t. thous has been noted as being a resident of the Auyan Tepui by G.H.H. Tate (Tate 1939), though no collection altitude is listed. Tate made several anatomical observations comparing the Auyan Tepui Cerdocyon thous specimens with those found in the Cotiga savannah and the Orinoco river basin. The two groups differ in their auditory bullae, the proportions of the basiocciptial, and in their dentition, in which Auyan tepui foxes have “small teeth” (Tate 1939). With regard to the external feature of Cerdocyon thous, Tate remarks that the Auyan tepui foxes possess smaller short haired tails with black markings limited to the tip of the tail (Tate 1939). Tate asserts that Guiana Highlands C. t. thous can be differentiated by these features, representing a transitional form between the northern Brazilian foxes and those found in the Venezuelan llanos. Although this camera trapping experiment did not obtain enough information to verify Tate's observations regarding the derivation of C. t. thous across northern South America, it does confirm his observations regarding the distribution of foxes into the upper elevations of Auyan Tepui. Recent phylogenetic analysis of the mitochondrial DNA of Cerdocyon thous supports a differentiation into two phylogeographic clades, where C. thous in the Guyanas and south-eastern Amazonia is present in a “mixture zone between the two major phylogeographic clades” (Tchaicka et al. 2006). One theory presented in Tchaicka et al. (2006) for the differentiation of C. thous into two clades is the possible origin of its ancestral population in Venezuela and Guyana. If this is the case, C. t. thous would have a long history in the GH, and its interaction with tepui summit biota should be analysed in a paleoecological perspective (Rull 2010). Phylogenetic analysis places the differentiation of the two major C. thous clades at between 600 kya and 400 kya, when glacial conditions dominated. Glacial conditions allowed for the downward displacement of tepui flora while paramo-like floral assemblages dominated the summits. This placed tepui-like ecosystems 1,000 metres below their current levels, in contact with the lowlands (Rull 2005). Climate Envelope Distribution Models projected the Last Glacial Maximum (21 kya) expansion of tepui climate envelopes far beyond their current range; corresponding to modern upland regions in all of Estado Bolivar in Venezuela, and in Guyana up to approximately 100 kilometres from the coast (Rödder et al 2010). As C. thous dispersed into South America during the Pleistocene, the majority of its evolutionary history in the G.H. would have occurred during these glacial conditions, allowing C. thous subspecies to interact with tepui-like biota for extended periods of time. The presence of tepui-like ecosystems in the lowlands during glacial periods may therefore predispose certain GS organisms like C. t. thous to ranging into current tepui summits, though topographic and biological constraints on individual tepuis may be a limiting factor. Tate's expeditionary work in the GH failed to produce evidence of foxes on Mt. Duida, and upon further investigation he confirmed with the indigenous people that C. t. thous is unknown in the region (Tate 1939). One possible explanation is that that higher elevation tepuis do not maintain the same levels of ecosystem diversity and carrying capacity, representing a barrier to range expansion. If this is the case, then the distribution of C. t. thous in the Pantepui region would be predicted to include the Chimanta Massif, and other large low elevation, floristically diverse tepuis. Establishing the range, population dynamics and niche of C. t. thous on the tepui talus slopes and summits is crucial for understanding the current and future ecosystem dynamics of the Pantepui. C. t. thous is a potential seed disperser, and its gut may encourage the germination of certain plant seeds, a phenomena also observed in N. nasua ( Alves-Costa 2007, João Vasconcellos-Neto et al. 2009, Cazetta et al. 2009,). Seed dispersal mechanisms are not well known in the GH, and tepui floral dispersal capabilities are considered to be minimal (Rull 2010). C. t. thous and N. nausa may change the distribution of current and future floral assemblages on the tepui summits, introducing non-endemic plant species by acting as seed dispersers (Nathan et al. 2008, Thuiller et al. 2008). This possibility is pertinent given the dramatic effects anthropogenic climate change will have on the distributions of future tepui ecosystems. Analysis of the predicted future distribution of tepui vascular plants using Altitudinal Range Displacement, Species Area Relationships, and spatial analysis indicates that some 80% of tepui habitats will be lost to upward vertical displacement, producing 100% extinction in some tepuis and 34-57% on the least threatened tepuis by 2100 (Vegas-Vilrrubia et al. 2012). This is a conservative estimate, as remaining habitat area will be severely restricted and spatially disjointed, leading to unpredictable interactions of floral and faunal assemblages in refuge areas. How anthropogenic climate change will effect the range, population dynamics, and behaviour of C. t. thous in the GH is unknown at this time, as is the impact of seed dispersal from lowland animals on the tepui summits under global warming conditions.


From an epistemological stand point, the photographic capture of C. thous is somewhat surprising, as is this animals lack of documentation on the tepui summits or talus slopes outside of the 1939 publication of Mammals of the Guiana Highlands. It could be that the absence of C. t. thous on the summit is the result of a sampling error; C. t. thous is mostly active during the night and at dawn, and therefore unlikely to be encountered during a transect walk or under the usual conditions of daytime scientific field activity. In this case, when a survey methodology was used that was biased towards nocturnal organisms, (ie nocturnal camera trapping), the presence C. t. thous was recorded successfully. In all likelihood this nocturnal carnivore would not have been recorded without the camera trapping experiment, as it was not observed by the expedition team during the transect survey.


The epistemic discontinuity of GH fauna distribution is addressed in Havelkova et al. (2006) and Robivinsky et al. (2007) with their observations of tepui summit coati distribution. The authors concluded that the presence of coatis on Roraima Tepui and the Chimanta Massif is standard for the distribution of coatis in the GH. Their conclusion is based on reviews of published expeditionary literature regarding the Chimanta Massif and the falsification of the hypothesis that tourist activity entices coatis to the summits by providing food sources for these animals to scavenge. Further support of the conclusions of Havelkova et al. (2006) and Robvinsky et al. (2007) can be found in video and photographic evidence of coatis on the summit of Auyan Tepui recorded in video documentary form in the late 1980s by Terramar expedition teams and in 2008 with photographs taken on the summit by Alberto Pomares, who assisted in the 2012 Auyan Tepui camera trapping pilot study (Artz and Kirchner 1991, Barkoczy 2009, Alberto Pomares; personal communication 2011). These sightings verify the observed distribution of coatis in the GH by Tate during the 1937-38 Phelps expedition, although they do not necessarily support Tates' classification of a coati subspecies Nasua dichromatica as distinct from Nasua nasua vittata in in this area (Tate 1939). Both N. n. vittata and C. t. thous are hypocarnivouous mesopredators (Aguiar et al. 2011). This trait is important to the analysis of carnivora on the tepui summits, as poor soils and continual erosion restrict vegetational growth in tepui ecosystems and would limit range expansion of hypercarnivorous species in the GH (Forget and Hammond 2005).

Conclusion

The verification of C. t. thous on the talus slopes of Auyan Tepui raises questions regarding the paleodistribution, current range and ecological role of this canid in the GH and Pantepui. It is unknown how C. t. thous interacted with Pleistocene tepui ecosystems, and how this interaction may effect the current and future distribution of this animal into the tepui slopes and summits. Future camera trapping on the slopes and summit of the Auyan Tepui and the eastern sector tepuis of Venezuela would be useful in deducing the sum total biodiversity of the tepui summits, bearing in mind that camera trapping results would be biased toward capturing images of larger bodied endothermic vertebrates. Such a camera trapping survey would require mapping analysis of Auyan Tepui focusing on both key regions of interest and entrance points along the talus slopes, an increase in both the number of camera traps used and and their duration of time in the field, and proper post camera trapping data analysis, following the Tropical Ecology And Monitoring Network protocols (TEAM Network 2011). Finally, survey gap analysis tools would be helpful in analysing expeditionary work in the Pantepui, and perhaps even on individual tepui summits (Funk et al. 2005). Survey gap analysis, GIS analysis, and target oriented camera trapping would make future research and expeditionary work more cost efficient, and would help to identify and catalogue the Pantepui organisms before climate change alters this environment permanently.

Acknowledgements

I am deeply indebted to the entire expedition crew for the realization of my pilot study; Alberto Pomares, Vittorio Assandria, Daniel Abgrall, Cedrig Abgrall, Dr. Douglas Olivares, Nelson Gonzalez, Richard Dittmar, Ana Cristina Fernandez, Dr. Carlos Acevedo, and Paul Stanley. I would also like to especially thank the Pemon guides who assisted with the completion of the camera trap: Santos Ugarte (the principle guide), Arturo Berti (Guide and Camera Trap assistant) and Nixson (Camera trap assistant).
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