The Effects of a National Highway on the Endangered Golden-Brown Mouse Lemur Microcebus Ravelobensis in Ankarafantsika National Park, Madagascar

The effects of a national highway on the Endangered golden-brown mouse lemur Microcebus ravelobensis in Ankarafantsika National Park, Madagascar

M ALCOLM S. RAMSAY,ANDRIAMAHERY R AZAFINDRAKOTO and S HAWN M. LEHMAN

Abstract Although roads are often assumed to be barriers Ree et al., ). However, many road ecology studies have to the dispersal of arboreal species, there has been little focused on terrestrial species in temperate environments, empirical testing of this assumption. If arboreal animals especially in areas with highly developed road infrastruc- are unable to cross roads, population subdivision may ture, such as Europe and North America (Holderegger & occur, or resources may become inaccessible. We tested Di Giulio, ). These studies have focused on large, the hypothesis that Route Nationale  (RN), a paved high- paved freeways and finding practical solutions to the pro- way, was a barrier to movement and dispersal of the blems posed by roads (Smith et al., ). Arboreal animals Endangered golden-brown mouse lemur Microcebus ravelo- face additional challenges, as they must descend to the bensis in Ankarafantsika National Park, in north-west ground to cross roads (Soanes & van der Ree, ). Madagascar. During June–August  we conducted a cap- However, connectivity of habitat across roads, both natural ture–mark–recapture study at three sites: two adjacent to and anthropogenic, can mitigate the negative effects of RN and one within intact forest without a potential barrier. roads if arboreal animals traverse these connections (Van During , trap nights we captured  golden-brown der Hoeven et al., ). There are relatively fewer data on mouse lemurs , times. In roadside habitats we captured how arboreal animals respond to roads in tropical forest re- significantly more males than females, whereas the opposite gions, particularly for species found in rare tropical dry for- was the case in interior forest habitat. We detected eighteen ests, which are amongst the world’s most threatened crossings of highway transects by nine individuals; however, ecosystems (Sagar & Singh, ). Thus, hypothesis-driven all potential dispersal events involved males. In roadside studies are needed in the tropics to determine the impact of habitat, movement was significantly inhibited in both roads, rather than an a priori assumption of roads as males and females. We present some of the first data on barriers or vice versa. the effects of roads on movement patterns in arboreal Road ecology in Madagascar is particularly important Malagasy mammals, showing species- and sex-biased effects because % of lemur taxa are currently listed by IUCN of roads as dispersal barriers. Our findings indicate that as threatened with extinction (Schwitzer et al., )and roads may not be complete barriers to dispersal in lemurs. expanding road construction may be a major cause of We recommend that conservation managers and scientists lemur habitat loss (Rogers et al., ), although there examine explicitly the effects of roads and natural arboreal has been little empirical testing of this assumption. The bridges in Madagascar in future studies. lack of data is surprising given that roads bisect or border some of the largest and best-known protected areas on the Keywords Dispersal, lemur, Madagascar, Microcebus rave- island, such as Ranomafana and Ankarafantsika National lobensis, movement, road ecology, sex-biased effects, ve- Parks. hicular mortality We investigated whether individual golden-brown mouse lemurs Microcebus ravelobensis were able to cross roads, and how their movement was affected in road envir- Introduction onments with various levels of canopy connectivity and un- interrupted forest habitat along a national highway in here is an extensive literature on the effects of roads on Ankarafantsika National Park. We predicted that () indi-  Twildlife and environments (e.g. Forman, ; van der vidual lemurs would be able to cross roads when canopy connectivity was present, () individual lemurs in uninter- MALCOLM S. RAMSAY (Corresponding author) and SHAWN M. LEHMAN Department rupted forests would not be hindered in their ability to of Anthropology, University of Toronto, Canada move, and () there would be no significant effect of sex E-mail [email protected] on the ability of lemurs to cross roads, as both males and ANDRIAMAHERY RAZAFINDRAKOTO Department of Animal Biology, University of Antananarivo, Madagascar females of the species disperse. These predictions were eval- Received  April . Revision requested  May . uated to test the hypothesis that roads were a barrier to Accepted  August . First published online  November . movement in M. ravelobensis.

Oryx, 2019, 53(4), 727–731 © 2017 Fauna & Flora International doi:10.1017/S0030605317001284 Downloaded from https://www.cambridge.org/core. IP address: 170.106.39.137, on 08 Oct 2021 at 06:43:28, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605317001284 728 M. S. Ramsay et al.

Methods studies have suggested M. ravelobensis populations may be affected by roads, but because the road construction was – – We conducted a capture mark recapture study during the relatively recent, no explicit genetic barrier was found –  dry season (May August) of in the Ampijoroa Forest (Radespiel et al., ). Mouse lemurs are excellent model Reserve within Ankarafantsika National Park. There are organisms to distinguish between the direct and secondary various microhabitats within the Park (Rakotondravony & effects of roads because they are under less direct hunting  Radespiel, ), and Ampijoroa is characterized by infer- pressure than larger-bodied animals (Garcia & Goodman, tile sandy soils with low water-holding capacities, gallery ). forest alongside Lake Ravelobe, and a high occurrence of We established six parallel trap lines of  m length at non-native plantation trees, such as Mangifera indica and three locations in Ampijoroa (Fig. ): two on either side of   Tectona grandis (Rendigs et al., ; Crowley et al., ). RN where there was canopy connectivity across the high-    Route Nationale (RN )isa km two-lane paved highway (Road ), two on either side of RN at a site with no can- way from Antananarivo to Mahajanga, which runs directly opy connectivity (Road ), and two within the interior – through Ankarafantsika National Park in a north south forest, c.  km from the road or forest edge, as a control   direction for c. km (Fig. ), dividing the Park into two (Forest Control). We sampled trap lines on a -day rando-      sections, of , and , ha (Radespiel et al., ). mized schedule; no trap line was sampled on  consecutive – Mouse lemurs are small-bodied ( g), nocturnal and nights and monthly trapping intensity was equal at all sites.  solitary omnivores (Kappeler & Rasoloarison, ). We set live animal traps (Sherman, Tallahassee, USA) at Individuals of our study species, M. ravelobensis, establish  m intervals along each trap line, giving a total of  trap- mixed-sex sleeping sites, their diets contain a higher per- ping sites per trap line and  traps at each location. We centage of arthropods, and they have a slightly sex-biased established the parallel interior transects at similar distances system of female philopatry, but both sexes disperse to those on the roads, c.  m apart. Upon capture, indivi-    (Radespiel et al., , ; Weidt et al., ). Previous duals were categorized by sex and age-class and were marked subcutaneously with a Trovan microchip. For a more detailed description of trapping procedures see Burke & Lehman (). Our study was approved by the University of Toronto Office of Research Ethics (Protocol #) and complied with all legal requirements of Madagascar. A crossing event was defined as when an individual was captured on one trap line and then recaptured on the  parallel trap line. We used t-tests, χ tests, a one-way ANOVA, and Tukey’s post-hoc analysis with α = . to test for differences in movement and capture rates between locations and sex categories. Movement was quantified by rounding distances between adjacent non-diagonal traps to  m. All tests were performed in Rv... (R Development Core Team, ).

Results

We captured  M. ravelobensis individuals in , capture events at the three locations over , trap nights (, traps set, with  rodent captures and  trap malfunctions). There were no significant differences between trapping locations in terms of rates of rodent captures (t = .,df=,P=.) or trap malfunctions (t = ., df = ,P=.). There were significantly more males caught at Road  and Road  than at Forest Control; males were also caught at a higher rate than females at Road  and FIG. 1 Major national highways (dashed lines) and protected  areas (grey shading) in Madagascar. The inset shows the division Road , whereas at Forest Control there were no significant of Ankarafantsika National Park by Route Nationale  (RN) differences in the number of individuals caught by sex into areas of c. , and , ha. (Table ).

We found no significant differences in mean distance TABLE 2 Distance moved (± SD) by male and female individuals of travelled by males and females at any of the three trapping M. ravelobensis at the Road  (connection across RN), Road  (no  locations (Fig. , Table ). There was a significant difference connection across RN ) and Forest Control (interior forest with no  in total movement between the three locations (Table ). barrier) sites in the Ampijoroa Forest Reserve (Fig. ), with results of t-tests and ANOVA (* denotes significance P , .). Tukey’s post hoc analysis indicated there was a significant difference between Forest Control and Road  (Q = ., Distance moved ±SD df = ,,P, .) and Road  (Q = .,df=,, (m) P , .), but no significant difference between Roads  Location Males Females t df P      .   and (Q = . ,df= , ,P . ). Road 1 123 ± 144 112 ± 126 0.26 42 0.79 We detected road crossing on  occasions, by  males Road 2 208 ± 166 175 ± 203 0.54 39 0.59 (Table ). Of these  captures,  (seven individuals) were Forest Control 299 ± 220 428 ± 290 1.48 33 0.15 at Road . At Road  we captured two individuals four Total 183 ± 182 262 ± 259 16.25 2,117 , 0.01* times. Individuals (n = ) at both locations were recaptured on their original trap line after being caught on the parallel line. At Forest Control we recaptured M. ravelobensis   Cyclone Hudah resulted in the destruction of %of times on a different trap line than that on which they trees and an % reduction in mean tree crown volume in were previously caught, corresponding to %(n= of the Masoala Peninsula (Birkinshaw & Randrianjanahary, ) of individuals. ). Cyclones of a similar nature and intensity occur in Ankarafantsika National Park (Aymoz et al., ). Additionally, if construction occurs along RN, anthropo- Discussion genic damage to these natural arboreal bridges may also occur (Weller, ). Thus, it would also be prudent for Our study is the first to directly test the permeability of managers to investigate the efficacy of permanent anthropo- roads to mammal movement in Madagascar, and our find-  genic crossing structures, such as bridges or culverts. ings indicate that RN affects the movement of M. ravelo- Our third prediction was not supported: only male bensis in Ankarafantsika National Park. Our first two M. ravelobensis were observed crossing RN and there predictions were validated: although the lemurs were able were significantly more males alongside RN than within to cross RN, they did so at a lower rate than if there had the interior forest. Although we captured significantly been undisturbed canopy. Thus, it is important for conser- more males than females at Roads  and , we captured  vation managers to protect existing crossings and encourage and  individual females, respectively, over  times at more canopy growth, as our results suggest that crossing each location. Additionally, at Forest Control we observed movement of M. ravelobensis would be further reduced if an equivalent number of crossings by males and females existing arboreal bridges were lost. However, Madagascar ( and , respectively), and thus we consider our results is prone to extreme climatic events, such as cyclones,  to be robust. A sex-biased effect of roads has also been ob- droughts and wildfires (Ingram & Dawson, ), and in served in North American freshwater turtles (Order Testudines), with female turtles more likely to be killed by TABLE 1 Number of individuals captured (individuals identified vehicles than males while crossing roads to find nesting and given a unique ID) and total number of captures (including sites, leading to skewed sex ratios (Steen et al., ). recaptures) of golden-brown mouse lemurs Microcebus ravelobensis at the Road  (connection across RN), Road  (no connection across RN) and Forest Control (interior forest with no barrier) sites in the Ampijoroa Forest Reserve within Ankarafantsika TABLE 3 The number of individuals of M. ravelobensis captured on  National Park, Madagascar (Fig. ), with χ and P (* denotes sig- both parallel trap lines (individuals crossing), and the total number of captures in which the previous capture was on the parallel trap nificance at P , .). line (crossing events), at the Road  (connection across RN), Road Location Males Females χ2 P Total  (no connection across RN) and Forest Control (interior forest  Individuals captured with no barrier) sites in the Ampijoroa Forest Reserve (Fig. ). Road 1 29 15 4.45 0.03* 44 No. of individuals Road 2 28 13 6.25 0.01* 41 crossing No. of crossing events Forest Control 17 18 0.11 0.74 35 Total 74 46 120 Location Males Females Total Males Females Total Total captures Road 1 7 0 7 14 0 14 Road 1 177 101 20.78 0.01* 278 Road 2 2 0 2 4 0 4 Road 2 227 117 45.30 , 0.01* 344 Forest 14 13 27 70 87 157 Forest Control 183 227 2.36 0.31 410 Control Total 587 445 1,032 Total 23 13 36 88 87 175

However, our results indicate that male M. ravelobensis are SML assisted in designing the study and preparing the more likely to face mortality, as the crossing sex. Given that article. male and female M. ravelobensis have home ranges of equivalent size and both sexes disperse, this effect must be attributable to other factors, such as competition between References males (Weidt et al., ) or home range pile-up, in which the lemurs are not affected by roads as direct barriers AYMOZ, B.G.P., RANDRIANJAFY, V.R., RANDRIANJAFY, Z.J.N. & to dispersal, but through many individual or group home KHASA, D.P. () Community management of natural resources: a ranges abutting roads (Riley et al., ). This phenomenon case study from Ankarafantsika National Park, Madagascar. Ambio, , –. can have significant genetic and social consequences in gre- BIRKINSHAW,C.&RANDRIANJANAHARY,M.() The effects of garious species such as mouse lemurs. Cyclone Hudah on the forest of Masoala Peninsula, Madagascar. Our results on the roadside movement of M. ravelobensis Madagascar Conservation and Development, , –. are some of the first such data available for mammals in BURKE, R.J. & LEHMAN, S.M. () Edge effects on morphometrics Madagascar, and contribute valuable data on the effects of and body mass in two sympatric species of mouse lemurs in Madagascar. Folia Primatologica, , –. roads on the understudied guild of arboreal mammals, for CROWLEY, B.E., MCGOOGAN, K.C. & LEHMAN, S.M. () Edge which research is especially needed in tropical environ- effects on foliar stable isotope values in a Madagascan tropical dry ments such as Madagascar (Lehman et al., ). forest. PLoS ONE, (), e. Managers of protected areas such as Ankarafantsika that FORMAN, R.T.T., SPERLING, D., BISSONETTE, J.A., CLEVENGER, A.P.,  are intersected or abutted by roads should investigate the ef- CUTSHALL, C.D., DALE, V.H. et al. ( ) Road Ecology: Science and Solutions. Island Press, Washington, DC, USA. ficacy of mitigation measures such as bridges or culverts   GARCIA,G.&GOODMAN, S.M. ( ) Hunting of protected animals (Smith et al., ) in aiding the movement of wildlife. in the Parc National d’Ankarafantsika, north-western Madagascar. However, anthropogenic bridges are potentially costly for Oryx, , –. developing nations, and have shown mixed results in aiding HOLDEREGGER,R.&DI GIULIO,M.() The genetic effects of movement across barriers in Madagascar specifically (Mass roads: a review of empirical evidence. Basic and Applied Ecology, , – et al., ). Our results suggest that natural bridges can aid . INGRAM, J.C. & DAWSON,T.P.() Climate change impacts and movement, but further study comparing the efficacy of nat- vegetation response on the island of Madagascar. Philosophical ural and anthropogenic bridges along RN and other roads Transactions of the Royal Society: Mathematical, Physical and in Madagascar is needed to clarify which is more effective. Engineering Sciences, , –. Given the urgent conservation needs and the rapid develop- KAPPELER,P.&RASOLOARISON, R.M. () Microcebus, mouse ment of roads within Madagascar, more hypothesis-driven lemurs, Tsidy. In The Natural History of Madagascar (eds S. M. Goodman & J. Benstead), pp. –. University of Chicago studies are needed on the effects of roads, to inform conser- Press, Chicago, USA. vation initiatives. LEHMAN, S.M., RADESPIEL,U.&ZIMMERMANN,E.() Conservation biology of the Cheirogaleidae: future research directions. In The Dwarf and Mouse Lemurs of Madagascar (eds S. Acknowledgements M. Lehman, U. Radespiel & E. Zimmermann), pp. –. Cambridge University Press, Cambridge, UK. We thank the staff of Madagascar Institute pour la MASS, V., RAKOTOMANGA, B., RAKOTONDRATSIMBA, G., Conservation des Environnements Tropicaux, Madagascar RAZAFINDRAMISA, S., ANDRIANAIVOMAHEFA, P., DICKINSON,S. et al. () Lemur bridges provide crossing structures over roads National Parks and La Maison du Pyla. We also thank within a forested mining concession near Moramanga, Toamasina Becky Raboy, Ute Radespiel, Elke Zimmerman, Jhonny Province, Madagascar. Conservation Evidence, , –. Kenedy, Hajanirina Ravelonjanahary, Annette Klein, RDEVELOPMENT CORE TEAM () R: A Language and Environment Mamy Rina Evasoa and Alida Hasiniaina for theoretical for Statistical Computing. R Foundation for Statistical Computing, and practical assistance, and Amy Mui and two anonymous Vienna, Austria.  reviewers for valuable comments on this article. Funding for RADESPIEL, U., EHRESMANN,P.&ZIMMERMANN,E.( ) Species-specific usage of sleeping sites in two sympatric mouse this study was provided by Primate Conservation Inc., lemur species (Microcebus murinus and M. ravelobensis)in Sigma Xi Grants-in-Aid of Research, University of northwestern Madagascar. American Journal of Primatology, , Toronto Department of Anthropology, and Natural –. Science and Engineering Research Council of Canada grants RADESPIEL, U., RAKOTONDRAVONY,R.&CHIKHI,L.() Natural to SML (Discovery Grant) and MSR (CGS-M). and anthropogenic determinants of genetic structure in the largest remaining population of the endangered golden-brown mouse lemur, Microcebus ravelobensis. American Journal of Primatology, , –. Author contributions RAKOTONDRAVONY,R.&RADESPIEL,U.() Varying patterns of coexistence of two mouse lemur species (Microcebus ravelobensis MSR conducted all data analysis and drafted the article. and M. murinus) in a heterogeneous landscape. American Journal of MSR and AR collected the data, assisted by SML. AR and Primatology, , –.

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