A Case Study of the African Dwarf Crocodile (Osteolaemus Spp.) in Cameroon

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Co-occurring cryptic species pose challenges for conservation: a case study of the African dwarf crocodile (Osteolaemus spp.) in Cameroon

N ICOLE L. SMOLENSKY

Abstract The conservation status of threatened taxa may be that several species on the Red List may actually be com- obfuscated by the detection of cryptic species complexes, in plexes of cryptic species (Pfenninger & Schwenk, ; both vertebrate and invertebrate species. African dwarf cro- Murray et al., ). This taxonomic challenge can have sig- codiles (Osteolaemus spp.) are hunted throughout their nificant ramifications for our understanding of the distri- range but their conservation status is unknown. Few popu- bution, population status, management and legislative lation assessments have been carried out and there has been protection of these threatened cryptic species (Bell et al., a taxonomic revision of the number of species in the genus. ; Mace, ; Sattler et al., ). For example, two spe- The similar morphologies of Osteolaemus tetraspis and cies of woolly spider monkeys, the Endangered Brachyteles Osteolaemus osborni pose a challenge for conservation in arachnoides and the Critically Endangered Brachyteles Cameroon, where they are still managed as a single species. hypoxanthus, were previously thought to be a single species. Nocturnal spotlight surveys were conducted in three Captive-breeding programmes intended to augment regions during August–November  and December B. arachnoides populations included hybrids of the two spe- –February  to provide population assessments of cies, which, if introduced into the small population of O. tetraspis and O. osborni and raise awareness of the two B. hypoxanthus could have resulted in its genetic extinction species in Cameroon. The mean encounter rates of O. tetra- (Brito, ). The status and management of threatened spis and O. osborni were . ± SD . ( individuals in  taxa must be assessed on an ongoing basis as taxonomies surveys) and . ± SD . (three in four surveys) croco- are refined. diles per km, respectively. The O. tetraspis population com- The African dwarf crocodiles (Osteolaemus spp.) provide prised juveniles predominantly and had a male-biased sex an example of the heuristic approach needed to manage and ratio. The few O. osborni detected comprised both adults conserve biodiversity effectively as species’ taxonomies and juveniles. Both species are threatened in Cameroon, change. Osteolaemus was formerly a monotypic genus con- based on low encounter rates, young population structures taining two subspecies, Osteolaemus tetraspis tetraspis and and the threats of habitat loss and hunting pressure. This Osteolaemus tetraspis osborni, which were widely distributed study provides distribution maps and serves as a baseline in equatorial lowland rainforests of West and Central Africa. to quantify population trends and inform conservation They were managed as a single species, listed in Appendix I strategies. of CITES (CITES, ) and categorized as Vulnerable on the IUCN Red List (IUCN, b) because of the threats of Keywords Cameroon, crocodile, cryptic species, hunting habitat loss and hunting pressure (Eaton, ). However, pressure, Osteolaemus, population status studies have shown the genus comprises three species: Osteolaemus sp. nov., O. tetraspis and O. osborni (Eaton et al., ; Franke et al., ; Shirley et al., ; Smolensky et al., ). Efforts are underway to characterize Introduction the distribution and population status and develop he conservation status of a species is determined by its captive-breeding programmes for all three species (Eaton    distribution, population size, demographic structure, et al., ; Eaton, ; Franke et al., ; Shirley et al., T   and associated threats (IUCN, a). This information is ; Smolensky et al., ; Schmidt et al., in press). also used as a basis for management and conservation stra- Osteolaemus sp. nov. occurs in the upper Guinean rain-  tegies (Meffe & Carroll, ; Mills, ). However, these forests (Fig. ). It has been extirpated from the extreme west- data are lacking for % of species categorized on the ern part of its range. The southern coasts of Ghana and Côte ’ IUCN Red List (IUCN, b). Molecular evidence indicates d Ivoire may be the last remaining strongholds for this species (Waitkuwait, ; Kofron, ; Shirley et al., ; Eaton, ). Osteolaemus tetraspis and O. osborni occur NICOLE L. SMOLENSKY Department of Wildlife and Fisheries Sciences, 210 Nagle in the lower Guinean and Congo rainforests, respectively Hall, Texas A&M University, College Station, Texas 77843-2258, USA  E-mail [email protected] (Fig. ). Population assessments of O. tetraspis and O. osbor- Received  January . Revision requested  April . ni are few, mostly outdated, and indicate low densities where Accepted  August . First published online  December . they are exploited for bushmeat (Riley & Huchzermeyer,

Oryx, 2015, 49(4), 584–590 © 2014 Fauna & Flora International doi:10.1017/S0030605314000647 Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.14, on 30 Sep 2021 at 08:52:53, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605314000647 African dwarf crocodile in Cameroon 585

FIG. 1 The West, South-west and South-east study sites in the lowland Congo–Guinean rainforest in Cameroon, where surveys were conducted for the African dwarf crocodiles Osteolaemus tetraspis and Osteolaemus osborni.The rectangle on the inset shows the location of the main map in Africa.

; Wild, ; Eaton, , ). In light of these taxo- I conducted surveys within the Mone River Reserve, on nomic revisions and current threats to the species, popu- the southern border of the Takamanda National Park, and lation assessments are needed to update their conservation near the villages of Okpambe and Ebinsi, located between status and inform appropriate management to conserve the Reserve and the Park (Fig. ). The South-west region their evolutionary diversity. provided an additional site for a spatial comparison of O. The co-occurrence of cryptic taxa further complicates tetraspis populations, facilitating assessment of the status conservation status assessments of species. Smolensky of the species at a broad scale. In this region surveys were et al. () confirmed the co-occurrence of O. tetraspis conducted during – in the Campo Ma’an and O. osborni in Cameroon. Osteolaemus tetraspis is widely National Park, specifically in the sections known as Ile distributed there but is threatened by hunting and defores- Dipikar and Corridor. The Congo Basin in the South-east tation (Wild, ; Gonwouo & LeBreton, ). These lat- is the only region known to harbour O. osborni, and was est assessments were conducted during – and were chosen to provide the first assessments for this species in presence/absence surveys, except at one site where popu- Cameroon (Smolensky et al., ). lation density surveys were conducted (Wild, ). There Study sites in each region were selected based on road ac- have been no population density assessments of O. osborni. cess, proximity to a protected area, and anecdotal evidence Here I provide information on the population ecology of of Osteolaemus presence. All sites were at low elevation O. tetraspis and O. osborni in Cameroon to facilitate inde- (,  m), with dense canopy cover and gallery forest veg- pendent conservation of these species. I present the first etation. Streams in the West and South-west were – m population assessments of O. osborni and O. tetraspis, a re- wide and had clear, slow-flowing water of depth , .– assessment of the western population of O. tetraspis, and m but typically , . m. The Dja River, in the South-east distribution maps for both species. study region, is a major tributary of the Congo Basin, with turbid waters, maximum width  m, and mean annual dis-  − charge – m s (Seyler et al., ). Study area  –   During August November and December Methods – February  I conducted population surveys in three study regions (West, South-west and South-east) in Nocturnal spotlight surveys were conducted to obtain a cen- the lowland Congo–Guinean rainforest in Cameroon sus of crocodile populations (Chabreck, ). The number of (Fig. ). The West study region was where Wild () con- surveys was reduced at sites where initial surveys yielded few ducted an assessment of O. tetraspis in , facilitating a encounters. Surveys entailed wading, walking or canoeing temporal comparison of population estimates with this along the edges of the Dja River. I surveyed the edges of the study, and an assessment of the population trend. river, where flow was reduced and canopy cover was dense.

TABLE 1 Mean encounter rates for the African dwarf crocodiles Osteolaemus tetraspis in the South-west and West and Osteolaemus osborni in the South-east study sites of the lowland Congo–Guinean rainforest in Cameroon (Fig. ).

Mean encounter rate ± SD (indi- Study region Site No. of surveys Survey distance (km) No. detected No. captured viduals per km) Osteolaemus tetraspis South-west Ile Dipikar 16 40.54 35 25 1.01 ± 0.98 Corridor 11 26.20 10 7 0.48 ± 0.58 Total 27 66.70 45 32 0.79 ± 0.88 West Mone river 5 3.38 9 6 2.16 ± 2.75 Okpambe 2 3.70 2 1 0.56 ± 0.11 Ebinsi 1 1.30 0 0 0.00 Kekukesem* 3 3.91 9 5 2.17 ± 0.84 Takamanda* 1 1.70 0 0 0.00 Total 12 13.99 20 12 1.54 ± 2.04 Total for both regions 39 80.69 65 44 1.02 ± 1.34 Osteolaemus osborni South-east Nki 4 24.71 13 3 0.61 ± 0.38

* In the Takamanda National Park (c.f. Wild, )

Each survey began  hours after dusk and ended – test was used to compare encounter rates and population hours before dawn. Each stream was searched during – structure between years. nights, covering different sections of the stream each night. Start and end points were recorded using a global po- Results sitioning system, to map the location and length of each survey. A white LED headlamp ( lumens) was used to detect Forty-three nocturnal spotlight surveys were conducted ( crocodiles, which typically were solitary. The waters were in the South-west,  in the West and four in the South-east), clear and shallow, which facilitated detection of submerged covering a total of . km of stream and river habitat crocodiles. I attempted to capture all crocodiles to obtain across the three study regions. Sixty-five O. tetraspis and morphometric measurements and tissue samples for species  O. osborni were encountered. Crocodiles were detected identification via genetic analyses. Smaller individuals were in all regions and at % of the eight survey sites (Table ), grabbed by hand and larger individuals were captured using although in general the encounter rate at individual sites was a snare-pole (Hutton et al., ). For each crocodile, I re- low (Table ). The mean encounter rates for O. tetraspis and corded its location, snout-vent length, total length and O. osborni were . ± SD . ( individuals in  surveys) sex. Crocodiles were given unique identifying marks by re- and . ± SD .  crocodiles per km (three in four sur- moval of caudal scutes (Webb & Messel, ), and released veys), respectively. Encounter rates did not differ among at the site of capture. regions (H = .,P=.) or among sites (H = ., Sex was determined for individuals of total length .  P=.). cm. Crocodiles were categorized according to life-stage, The mean encounter rate of O. tetraspis populations based on studies of captive and wild Osteolaemus popula- from Takamanda and Kekukesem, sites previously surveyed tions (Beck, ; Teichner, ; Tryon, ; Eaton, in  (Wild, ), declined from three to . crocodiles ): hatchlings (,  cm), juveniles (– cm) and per km. Encounter rates in the South-west also declined, adults (.  cm). Crocodiles that evaded capture were from . ± SD . (n =  surveys) in  to . ± SD . not categorized. crocodiles per km (n = )in but the decrease was not Encounter rates and population structure were used to significant (W = −.,P=.). No crocodiles marked in assess the population status of O. tetraspis and of O. osborni.  were re-captured in . Encounter rates were recorded as the number of crocodiles O. tetraspis populations were composed predominantly detected per km of river habitat, and served as relative popu- of juveniles (Fig. ). In the South-west juveniles comprised lation density indices. Population structure was the relative %(n=) of the population, and adults %(n=). No proportions of captured individuals in each size category. hatchlings were detected although % of the juveniles had Encounter rates and population structures in the three recently entered this size category and were – cm in study regions were compared using Kruskal–Wallis and total length (Fig. ). The population structure was un- Fisher’s exact tests, respectively. For the South-west, where changed between  and . In the West, juveniles com- surveys were conducted for  years, a Wilcoxon signed-rank prised .%(n=) of the population, and adults .%

habitat, with encounter rates of two or more crocodiles per km being more common in the West. The habitats were similar in their physical and vegetation characteristics but differed in levels of anthropogenic disturbance. The sites adjacent to or in the protected areas of the West were re- mote, with lower human population densities and fewer log- ging concessions and roads in the surrounding area compared to sites in the South-west. Sites far from protected areas (e.g. Ebinsi) had even lower encounter rates, which may be attributable to degraded habitats, lack of enforce- FIG. 2 Population structure of O. tetraspis at study sites in the west (n = ) and south-west (n = ) of the lowland Congo– ment of hunting regulations, and fishing methods involving Guinean rainforest in Cameroon (Fig. ), and of O. osborni in the use of poisonous organo-chloride insecticides the south-east (n = ). Dashed vertical lines represent the (Gonwouo & LeBreton, ). Cameroon’s human popu- divisions between hatchlings (,  cm total length), juveniles lation density, infrastructure development and agriculture ,   ( cm total length) and adults, based on Beck ( ), sector have doubled since  (de Wasseige, ; World    Teichner ( ), Tryon ( ) and Eaton ( ). The numbers to Bank, ). Thus the decline in encounter rates, from the right of the median are mean encounter rates, and error bars    represent minimum and maximum sizes of captured crocodiles. three (Wild )to . crocodiles per km in the West, may be a result of increased exploitation. Alternatively, lower encounter rates may be associated with edge effects (n = ). Two of the juveniles were – cm in total length. around protected areas (Woodroffe & Ginsberg, ), as There was no significant difference in the population struc- my surveys were conducted on the edge of the ture between regions (F = .,P=.). The sex ratio was Takamanda National Park whereas those of Wild () male-biased (. : ,n=) in the South-west and female- were conducted in the interior of the Park. biased in the West (. : ,n=) and South-east ( : , In the South-west encounter rates also decreased during n=). – although not significantly. Although it may take Two adult and one juvenile O. osborni were captured in several years to detect changes in population structures of the South-east study region. O. osborni detected but not crocodiles (Webb et al., ), the observed differences captured also fell within these size categories. may reflect a change in activity rates. In  surveys were conducted at the end of the rainy season, which probably coincides with the end of the mating season and the begin-  Discussion ning of the nesting period (Waitkuwait, ; Kofron & Steiner, ; Eaton, ), whereas in  surveys were These results provide information on the population status of conducted at the end of the dry season, when the availability O. tetraspis throughout its range in Cameroon, and the first of aquatic prey is low, and therefore more individuals may estimate of O. osborni population densities in Cameroon. be inactive, remaining in burrows until the onset of the rainy Encounter rates of both species were low. They were compar- season (Brummett & Teugels, ). able to exploited populations of these species in similar habi- The lowest encounter rates were recorded for the O. osborni tats in the Republic of the Congo, and . times lower than population, which may be attributed to the combined threats encounter rates of unexploited O. tetraspis populations in of hunting pressure and drowning in gillnets. The turbidity of Gabon (Eaton, ). Both species are hunted throughout the waters of the Dja River, compared with the clear-water Cameroon but the intensity of hunting pressure is unknown streams surveyed for O. tetraspis, may also have resulted in (Wild, ). The low encounter rates of both species, and the lowerdetectionrates(Bayliss,; Hutton & Woolhouse, juvenile-biased population structure of O. tetraspis, may be in- ). It is unlikely that low encounter rates were a result of dicative of unsustainable exploitation (Webb et al., ). poor habitat, as Osteolaemus species use a variety of aquatic Additional factors not associated with hunting that may habitats, including rivers (Eaton, ). have influenced observed encounter rates are discussed Population structure may be influenced by the type of below. The wide distribution of O. tetraspis throughout aquatic habitat. Although few O. osborni individuals were Cameroon may be critical for its persistence in the country caught they were adults and large juveniles detected at the (Smolensky et al., ). Osteolaemus osborni has a much nar- edges of a large river, whereas small and large O. tetraspis rower distribution and the low encounter rate implies a tenu- were detected in small tributaries in the West and ous status in Cameroon. South-west. These findings may be a result of ontogenetic Encounter rates of O. tetraspis were similar across its shifts in habitat use, whereby small crocodiles are less com- range. In many of the surveys in the South-west and West mon in larger rivers because of the higher predation risk one or no individuals were encountered in . km of river (Subalusky et al., ). In the South-west and West the

population structure was skewed towards juveniles, a situ- overexploitation. Further studies on reproductive phe- ation that is often attributed to size-selective hunting press- nology and seasonal activity patterns would facilitate our ure (Montague, ; Webb et al., ). However, the understanding of the spatial and temporal variability of population structures were similar to those of populations O. tetraspis populations. Although crocodile ranching and in Gabon not subject to hunting pressure (Eaton, ). farming has been a successful conservation strategy for Thus, proportionally higher numbers of juveniles in the exploited crocodile species (Crocodile Specialist Group, population may be typical of O. tetraspis populations sur- ), preliminary assessments indicate this would not be veyed during the dry season. Females are nesting during an economically viable strategy for Osteolaemus species in this period and may be located several metres away from Cameroon (Behra, ). My results suggest that protected water, which may account for the male-biased sex ratio ob- areas are important havens for populations of O. tetraspis served in the South-west population (Waitkuwait, ). and that they should be extensive, with enforcement of wild- Cameroon provides an important case study for life laws and limited access to their interiors. Sustainable Osteolaemus species and cryptic taxa in general, as it is livelihood opportunities must be created for local com- one of two countries known to harbour two Osteolaemus munities to offset the costs of reduced hunting. species, the other being the Republic of the Congo (Eaton, ; Smolensky et al., ). Separate population assessments were conducted and distribution maps provided to Acknowledgements raise awareness of the two cryptic species in Cameroon, pro- Funding for this research was provided by the Alfred P. Sloan viding a baseline to determine the stability of the density and Foundation, the Crocodile Specialist Group Student Research structure of the country’s O. tetraspis and O. osborni popu- Assistance Scheme, the LT Jordan MSC International lations. The low encounter rates of both species, the young Awareness Fellowship, the Rufford Foundation, and Texas population structure of O. tetraspis, and the increasing A&M University Diversity Fellowship. Drs Chuyong, Fotso, threats of habitat loss and hunting pressure indicate that Hanson, Legrand, and Nchanji, and Messrs Foguekem, both species are threatened in Cameroon, and both merit Mulema, Ikfuengi, and Kilanga assisted with permits from categorization as Vulnerable there. The conservation status the Ministries of Scientific Research and Forests and of O. osborni may worsen if national and international pol- Wildlife. I thank local councilmen, chiefs, conservators, and icy and management are not revised to protect this unique regional delegates for granting access to the study regions. species. Logistical support was provided by local hunters and Mr The similar morphologies of O. tetraspis and O. osborni Fouda and family. Drs Fitzgerald, Hibbitts and Ryberg, and pose a hybridization risk for both in situ and ex situ man- two anonymous reviewers, provided comments that im- agement programmes. Hybridization has been detected in proved this article. This publication is number  of the captive-breeding programmes in European zoos, and efforts Biodiversity Research and Teaching Collections and was ap- are underway to mitigate this and curtail translocations or proved by Texas A&M University: Animal Use Protocol— reintroductions of hybrids into wild populations (Franke -. et al., ; Schmidt et al., in press). In Cameroon, management authorities and conservation organizations confiscate live crocodiles from the bushmeat trade and release them References back into the wild but not necessarily into their original populations (NLS, pers. obs.), creating the potential for hybri- BAYLISS,P.() Survey methods and monitoring within crocodile dization. The distribution maps provided here and management programmes. In Wildlife Management: Crocodiles and Alligators (eds G. Webb, C. Manolis & P. Whitehead), pp. –. elsewhere (Smolensky et al., ) should mitigate some of Surrey Beatty & Sons, Chipping Norton, Australia. these hybridization risks. I recommend that confiscated cro- BECK,C.() Breeding the West African dwarf crocodile codiles be released back to their original populations. Osteolaemus tetraspis tetraspis at Memphis Zoo. International Zoo Regional and national reports of these findings are being dis- Yearbook, , –. tributed to governmental ministries and non-governmental BEHRA,O.() Area reports: Cameroon FAO Crocodile   agencies. Plans for continued monitoring are underway, in Management Project. Crocodile Specialist Group Newsletter, , . Http://www.iucncsg.org/_docs/attachments/protarea/CSG% addition to further delineation of O. tetraspis and O. osborni -e.pdf [accessed  September ]. distributions, particularly where contact zones may occur. BELL, B.D., DAUGHERTY, C.H. & HAY, J.M. 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.InCrocodiles: Their Ecology, Management, and Conservation WORLD BANK () World Development Indicators. Https://www. IUCN Publication New Series, pp. –. IUCN, Gland, google.com/publicdata/explore?ds=dbncppjoff_ Switzerland. &met_y=sp_pop_grow&hl=en&dl=en#!strail=false&bcs= WEBB, G.J.W., BRITTON, A., MANOLIS, S., OTTLEY,B.&STIRRAT,S. d&nselm=h&rdim=region&idim=country: CMR&ifdim= () The recovery of Crocodylus porosus in the Northern region&tstart=&tend=&hl= Territory of Australia: –.InProceedings of the th Working en_US&dl=en&ind=false [accessed  July ]. Meeting of the Crocodile Specialist Group, pp. –. IUCN, Gland, Switzerland. WEBB, G.J.W. & MESSEL,H.() Crocodile capture techniques. The Journal of Wildlife Management, , –. Biographical sketch WILD,C.() Report on the status of crocodilians in the Cameroon Forest Zone. In Proceedings of the th Working Meeting of the NICOLE SMOLENSKY’s research interests lie in the population ecology and Crocodile Specialist Group, pp. –. IUCN, Gland, Switzerland. conservation of reptiles. She uses a combination of field methods and WOODROFFE,R.&GINSBERG, J.R. () Edge effects and the molecular and biochemical techniques to study the status, sustainable extinction of populations inside protected areas. Science, , – use, distribution, and trophic ecology of reptiles in the USA and . Cameroon.