THE ROLE OF PLANTATIONS OF THE AFRICAN PALM ( ELAEIS GUINEENSIS JACQ . ) IN THE CONSERVATION OF SNAKES IN COLOMBIA Las plantaciones de palma africana ( Elaeis guineensis Jacq

Monocultures of the African oil palm (Elaeis guineensis Jacq.) were studied between 2006 and 2013 so as to determine which species of snakes frequented them and to estimate the abundances of each species encountered. Thirty five species of snakes (three boas, one coral, 27 colubrids, one tropidophid, one typhlopid, and two vipers) were captured within palmeras. Palm plantations are revealed to (1) augment the densities of ten species of snakes well beyond the densities found by collectors in natural and/or relatively transformed habitats and (2) to not offer benefits to at least 75% of the snake community found in the vicinities of palm plantations. The majority of snake species (60%) found in palmeras are nocturnal species. The most common species (defined by having 15 or more captures) were Atractus univittatus, Bothrops asper, B. atrox, Epicrates maurus, Leptodeira annulata, Liophis melanotus, Ninia atrata, Oxyrhopus petolarius, Pseudoboa neuwiedii, and Tantilla melanocephala. Palm plantations permit substantial local population sizes for a fraction (< 25%) of the local snake community. Internal practices of such plantations could be modified so as to protect a larger share of the fauna by means of two practices: (1) construction and maintenance of paleras as well as (2) creating a mosaic of palm plantations enclosing “islands” of secondary forests.


INTRODUCTION
Snakes constitute a biological group under serious threat in Colombia.The principal threats are (1) destruction of the native habitats and (2) the indiscriminate killing of snakes by persons living or working in rural areas (Lynch, 2013).In the developed and populated part of Colombia, few national parks exist but there are some regional parks maintained by municipalities or private concerns.Some eight years ago, I realized that a cultivation, that of the African oil palm, might play a major role in snake conservation.

The African Palm was introduced into
Colombia some 40-45 years ago and has become a growth industry.New plantations are created on lands that have had recent use as banana or rice cultivations, pasturelands, or natural vegetation (usually represented by secondary forests).The reactions of biologists, conservationists, and ecologists to the expanding palm plantations have been negative, reflecting either distaste for monocultures or the invasion of this agricultural frontier into natural habitats (or both).In my personal experience (Santander, 2007), I have seen parcels of rastrojo alto burned and shortly thereafter planted with this invasive species.African palm has been introduced even into areas never forested (savannahs in eastern Meta and in Vichada).However, plantations of mature African palm occur in areas that once supported humid tropical forest or dry tropical forest.
I first visited a plantation in 2004 but, aside from catching some caecilians and a few snakes there, remained indifferent (or antagonistic) towards the industry until 2006 (see below).Perhaps as a result of the biases of biologists against the industry, biological investigations of palmeras do not exist eventhough, in Colombia, the geographic extension grew by 41,000 Ha in 2010, summing 402,000 Ha (Fedepalma, 2011) and continues to expand (to 452,400 Ha en 2013, El Tiempo, 2 dic. 2013, p. 20).Snake studies in African palm plantations are rare; I am aware of one study in Nigeria that focused upon the snake community of climbing snakes (Akani et al., 2007).
Part of the problem with having Neotropical snakes as an object of study has been the view that they are uncommonly encountered even when one is actively searching for them.My experiences collecting in the tropics of Colombia andEcuador (1967-2005) were such that finding three snake individuals in one day made that day memorable (until 2006).However, memories are not scientific data; fortunately, I can consult my fieldnotes so as to measure the rate of success.In 1983, I collected specimens along the Rio Calima, below Lago Calima, in Valle del Cauca, and later participated in the II Expedición Botánica in the Tayrona National Park (Magdalena).These were two of my most successful trips (based on memories).From my fieldnotes, I collected for 13 days at each atrata, Oxyrhopus petolarius, Pseudoboa neuwiedii y Tantilla melanocephala.Las plantaciones de palma permite la subsistencia de poblaciones locales de tamaños sustanciales, lo cual corresponde a una fracción (< 25%) de la comunidad local de serpientes.Las prácticas internas de las plantaciones pueden ser modificadas para proteger una fracción mayor de la fauna; implicando dos cambios: (1) la construcción y el mantenimiento de paleras y (2) la creación de un mosaico de parcelas de palma intercalada con "islas" de bosque secundario.
place.In May-June, I collected in natural forests along the middle part of the Rio Calima (Valle del Cauca) and captured 48 snakes (20 preserved, fourteen delivered live to the Instituto Nacional de Salud, and 14 liberated) of fourteen species at a rate of 3.6 snakes/ day.In June-July, I collected within the Parque Nacional Natural Tayrona (Magdalena) and secured 32 specimens (22 preserved and ten delivered live to the Instituto Nacional de Salud) of thirteen species at a rate of 2.5 snakes/ day.Excepting our field trip to Antioquia and that to Casanare, fieldtrips to palmeras resulted in better successes of 3.3-13.1 snakes/ day (Table 1) Table 1.Species lists and numbers taken within palmeras.When the Departamento lies outside of the known and inferred distribution of the species, "na" = Not available.When the number of individuals bears an asterisk (in Antioquia, Cesar, Meta, and Santander, it means that the species was also collected in natural or transformed habitats.Larger plants produce not only more fruits, they also produce more leaves (fronds) that must be cut so as to gain easy access to the fruit clumps.Cut fronds fall to the ground where they are gathered into piles within the plantation so that they do not interfere with the collection, fertilization, and fumigation activities of workers.Frond piles (paleras) guard even higher levels of humdity and the discarded plant parts initiate decomposition creating a density gradient (of humidity and humus) from the outside of the pile to its base.
The trunk of the palm during the first third of its productive life is studded with the petiole bases of cut fronds and accumulates a cloak of epiphytes.Trees fifteen to twenty years of age have advanced the decomposition of the petiole studs to the point that the weight of the cloak begins to sag toward the base of the palm, leaving a relatively smooth trunk.
The work of my students and I in palmeras reveals that the best place to find snakes within a palmera is in the frond piles, followed by the cloak or the accumulated debris at the base of the trunks.We had our least success searching in other facies of the palm plantation (canopy, open spaces under the shade of the canopy, and trunks).
African Palm plantations are not distributed uniformly within the country (Fedepalma, 2011) and for many regions where cultivation has begun, production is so low that no extraction plants have been constructed (meaning that cultivations are too young or not yet of a sufficient density).Planning fieldtrips in 2011-13 took into consideration whatever might indicate older palms (extraction plants) so as to improve our chances of finding snakes.
At present, the productive African palm industry of Colombia is distributed mostly within the populated and productive triangle of Colombia (below 500 m elevation above sea level, Appendix 1).This region is also the most severely transformed (ecologically).The Andean zone (slopes of the Andes) is likewise severely transformed ecologically but the impact on snake communities is reduced because snake diversity declines sharply with increased altitude (Lynch, 2013).Within the transformed lowlands few areas are protected (the National Parks of Macuira and Tayrona and the Salamanca Santuary) but available biological data on snake communities for these protected areas are scarce (because most biological collections of the country are younger than 30-50 years).Valuable snake collections were obtained by the Museo de La Salle in the first half of the 20 th century and summarized by Nicéforo María (1942) but transformation of these areas had occurred centuries previously, eliminating the dry tropical forest and severely reducing the extent of the wet tropical forest; the latter remnants were cut early in the early part of the second half of the 20 th century.
For much of the transformed part of Colombia, the habitats offered are drier and experience brusk changes in temperatures during 24 hours (owing to the reduction in vegetative cover).Snake species are known from these regions (Nicéforo María, 1942), but there, snakes are subjected to intense human persecution and vehicular traffic; such specimens rarely are deposited in scientific collections.My impression is that African palm plantations mimic the moderating climates of the dry and wet tropical forests that once covered these transformed lowlands (IGAC, 1962;Espinal, 1977).Additionally, these plantations offer refuges from human persecution and vehicular traffic, at least for species of crepuscular and/ or nocturnal activities (the majority of tropical snake species).(2011).Likewise, I do not adopt the recognition of molecular species within widespread taxa when corroborating morphological evidence has not been presented.

RESULTS
In the course of the fieldtrips during 2006-2013, I and my students have visited 30 palm plantations varying in size from five hectáreas to more than 20,000 Ha.These include privately held palmeras as well as those of organized companies.Success-rates varied widely (generally less success during the dry season than during the wet season and greater success when the palmeras had some internal policies that indirectly, and unintentionally, favored snake collecting and snake density).Fieldwork in the departments of Bolívar, Casanare, Cundinamarca, and Magdalena was carried out during very dry seasons resulting in little (Casanare), or no (Cundinamarca) success as well as very successful visits (Bolívar and Magdalena).Our success-rate was not diminished when we collected in the aseasonal climates of the Chocó biogeográfico (Nariño).Unsurprisingly, species lists do vary geographically.
In all of the collections made in palmeras, a total of 35 species of snakes was taken (Table 1).Of the 35 species of snakes captured in palmeras, only fourteen show some diurnal activity.Chironius carinatus, Leptophis ahaetulla, the two Liophis, Lygophis lineatus, and the three Mastigodryas are exclusively diurnal snake species.The two Enilius, Erythrolamprus bizona, and Urotheca euryzona are best described as crepuscular/ diurnal (Savage, 2002).Clelia clelia is normally active at night but is also frequently encountered active by day.Eunectes murinus is also crepuscular and aquatic; its activity cycle cannot be described as diurnal or nocturnal.Typhlops reticulatus is a burrower but can be found above ground as well even during daylight hours.The remaining 21 species are exclusively nocturnal organisms.
Our visits to palm plantations were normally in the course of a single fieldtrip (fewer than 14 days).Palm plantations in Meta were visited species found in a given palmera is positively correlated with the total number of individuals captured (Fig. 3).During each field trip, five or six persons participated in discovery and capture of specimens for between four and six hours/ day.
In   in municipality of Cumaral, Hacienda La Cabaña; municipality of Villavicencio, Palmera Borrego).These sites of poor results (Table 2) appear to me to derive from two or three causes (not mutually exclusive): (1) Hacienda La Cabaña and Palmera Borrego may well have produced little result because each is an island of palms within a matrix of pastures, not connected to forest remnants, which might serve as sources for species requiring forested habitat; (2) additionally, at Hacienda La Cabaña and Palmeras de Cesar, we found intense application of insecticides; (3) at the remaining poor sites, paleras were not formed or were so shallow as to allow the discarded fronds to dry out completely and few prey items were seen.Because we found few prey items, we abandoned our searches as soon as practical when possible.Nonetheless, we were "trapped" in Hacienda La Cabaña and Palmera Borrego (for lack of transport) and spent nearly two days in Palmeras del Oriente.

DISCUSSION
To date, there are no confiable data on population sizes of any snake species in Colombia.In point of fact, the impression of collectors is that densities are very low, impressions that are contradicted by our work in palmeras.Collecting in natural habitats (Vichada, 2013) has produced success rates equivalent or superior to our work in palmeras.
Fieldwork in palmeras is sometimes as poorly productive as fieldwork in natural or transformed habitats but, in four of the eight departments sampled, can be impressively successful in terms of number of individuals captured/ day (Table 1).In general, looking across these past seven years, my impression is that population sizes of snakes in palmeras are elevated in comparison to natural or transformed habitats.Furthermore, in the only palmera visited repeatedly (Palmeras del Meta), the most abundant species in each of the two visits in 2006, remained the most abundant species in 2012 (in the same order of relative abundance: Ninia atrata > Atractus univittatus > Oxyrhopus petolarius > Tantilla melanocephala > Bothrops atrox), suggesting that relative abundances of species have not changed between 2006 and 2012 (Table 3).
That said palmeras do not represent a panacea for conservation because some species apparently do not use palmeras.A case in point is Imantodes cenchoa, a relatively common snake species in both natural and transformed habitats but absent from palmeras.Two other snake species, Dipsas catesbyi and Sibon nebulatus, each common in its habitat, were not found in our explorations of palmeras.These apparent absences, like that of Imantodes cenchoa, may reflect the absence of critical prey species.For the six departments for which it is possible to estimate snake community sizes, the mean value of species found in palmeras is only 25% of the estimated snake community.This means that although palmeras do enable larger than expected population sizes for certain species, they do not protect snake species diversity even so well as secondary forests (probably for the improverishment of microhabitat diversity).If my argument is sound, that suggests a strategy for improving palm plantations as protectors of snake diversity.That strategy is against extensive monoculture and in favor of a mosaic, with patches of secondary forest interspersed among parcels of monoculture.
The Colombian African palm industry could be a major factor in conservation biology of snakes in Colombia where mortality caused by rural workers exceeds 100 million snakes/ year and no fewer than 50,000 snakes die/ year due to vehicular traffic (Lynch, 2013).However, to be a partner in conservation will require two changes in the industry: (1) that all waste fronds be piled into mounds (paleras) within the plantation and allowed to decompose slowly.This provides refuges for snakes (as well as easy access to prey) and reduces encounters by humans (reducing snake bites and reducing movements which can result in mortality on roads), and (2) that palmeras cease to convert rastrojos (parcels of secondary forest) in more monoculture of palms.Doing so provides a source fauna (the parcels of rastrojo) as well as increasing the number of microhabitats (and the prey base).Each of these activities contributes to preserving the snake fauna (either by elevating population sizes or, most likely, by increasing local species diversity).

Figure 1 .
Figure 1.Relationship of number of species captured based on number of days invested in active searches.Sites with 12 species are combinations of two or three palmeras in the same municipality.That with five species in six days combines palmeras in the municipality of Villanueva, Casanare, and extreme northern Meta.The three day search yielding eight species combines two palmeras in Nariño.That with nine species combines two municipalities (San Alberto and San Martìn) in Cesar (four palmeras).Open symbols represent palmeras collected during the dry season.

Figure 2 .
Figure 2. Relationship of number of individuals captured and days invested in active searches.Symbols can be from single palmeras or a combination of two to four nearby palmeras.Open symbols represent palmeras collected during the dry season.

Figure 3 .
Figure 3. Relationship between number of individuals captured and number of species obtained.Each symbol represents a single visit to a single palmera except for the three open symbols which represent sequential visits to Palmeras del Meta en San Martín, Meta.
several palmeras visited during this investigation, we experienced very poor results in terms of snake captures (in Bolívar, municipality of María La Baja, two private palmeras; in Casanare, municipality of Villanueva: Palmeras del Oriente, Palmera Santa Ana, and Palmeras del Casanare and a private palmera, finca Rio Grande; in Cesar, municipality of San Martín, Palmeras de Cesar; in Cundinamarca, municipality of Paratebueno, private palmera, Hacienda La Europa; in Meta, municipality of Barranca de Upia, Palmera Guaicaramo;

Table 2 .
Results of collecting efforts in palm plantations with poor results.

Table 3 .
Snake collections made in Palmeras del Meta on three occasions (Most abundant species in boldface).
Palm plantations do represent the best of the monocultures available in Colombia because some snake species do quite well within palm plantations (in contrast to other monocultures: Acacia, Eucalyptus, pine, and teka plantations as well as bananas, pasturelands, and rice fields).This affirmation is based not upon systematic field work but on my successes catching snakes in Colombia during the past 35 years.