Evaluation of tenrec population viability and potential sustainable management under hunting pressure in northeastern Madagascar
A. Annapragada
Harvard John A. Paulson School of Engineering and Applied Sciences, Cambridge, MA, 02138 USA
Search for more papers by this authorC. E. Brook
Department of Integrative Biology, University of California, Berkeley, Berkeley, CA, 94720 USA
Search for more papers by this authorM. S. Luskin
School of Biological Sciences, The University of Queensland, St Lucia, Brisbane, QLD, 4072 Australia
Search for more papers by this authorR. P. Rahariniaina
Madagascar Health and Environmental Research (MAHERY), Maroantsetra, 512 Madagascar
Search for more papers by this authorM. Helin
Madagascar Health and Environmental Research (MAHERY), Maroantsetra, 512 Madagascar
Search for more papers by this authorO. Razafinarivo
Madagascar Health and Environmental Research (MAHERY), Maroantsetra, 512 Madagascar
Search for more papers by this authorR. Ambinintsoa Ralaiarison
Madagascar Health and Environmental Research (MAHERY), Maroantsetra, 512 Madagascar
Search for more papers by this authorH. J. Randriamady
Madagascar Health and Environmental Research (MAHERY), Maroantsetra, 512 Madagascar
Department of Nutrition, Harvard TH Chan School of Public Health, Boston, MA, 02115 USA
Search for more papers by this authorL. E. Olson
University of Alaska Museum, 1962 Yukon Drive, Fairbanks, AK, 99775 USA
Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, IL, 60605 USA
Search for more papers by this authorS. M. Goodman
Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, IL, 60605 USA
Association Vahatra, BP 3972, Antananarivo, 101 Madagascar
Search for more papers by this authorCorresponding Author
C. D. Golden
Madagascar Health and Environmental Research (MAHERY), Maroantsetra, 512 Madagascar
Department of Nutrition, Harvard TH Chan School of Public Health, Boston, MA, 02115 USA
Correspondence
Christopher D. Golden, Department of Nutrition, Harvard TH Chan School of Public Health, Boston, MA 02115, USA.
Email: [email protected]
Search for more papers by this authorA. Annapragada
Harvard John A. Paulson School of Engineering and Applied Sciences, Cambridge, MA, 02138 USA
Search for more papers by this authorC. E. Brook
Department of Integrative Biology, University of California, Berkeley, Berkeley, CA, 94720 USA
Search for more papers by this authorM. S. Luskin
School of Biological Sciences, The University of Queensland, St Lucia, Brisbane, QLD, 4072 Australia
Search for more papers by this authorR. P. Rahariniaina
Madagascar Health and Environmental Research (MAHERY), Maroantsetra, 512 Madagascar
Search for more papers by this authorM. Helin
Madagascar Health and Environmental Research (MAHERY), Maroantsetra, 512 Madagascar
Search for more papers by this authorO. Razafinarivo
Madagascar Health and Environmental Research (MAHERY), Maroantsetra, 512 Madagascar
Search for more papers by this authorR. Ambinintsoa Ralaiarison
Madagascar Health and Environmental Research (MAHERY), Maroantsetra, 512 Madagascar
Search for more papers by this authorH. J. Randriamady
Madagascar Health and Environmental Research (MAHERY), Maroantsetra, 512 Madagascar
Department of Nutrition, Harvard TH Chan School of Public Health, Boston, MA, 02115 USA
Search for more papers by this authorL. E. Olson
University of Alaska Museum, 1962 Yukon Drive, Fairbanks, AK, 99775 USA
Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, IL, 60605 USA
Search for more papers by this authorS. M. Goodman
Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, IL, 60605 USA
Association Vahatra, BP 3972, Antananarivo, 101 Madagascar
Search for more papers by this authorCorresponding Author
C. D. Golden
Madagascar Health and Environmental Research (MAHERY), Maroantsetra, 512 Madagascar
Department of Nutrition, Harvard TH Chan School of Public Health, Boston, MA, 02115 USA
Correspondence
Christopher D. Golden, Department of Nutrition, Harvard TH Chan School of Public Health, Boston, MA 02115, USA.
Email: [email protected]
Search for more papers by this authorEditor: Julie Young
Associate Editor: Pia Lentini
Abstract
Across the Global South, wildlife is an important source of nutrition and income, particularly for rural communities. While wildlife consumption provides a valuable source of nutrition, high levels of hunting can endanger wildlife species. In the Makira region of north-eastern Madagascar, human health is threatened by food insecurity and malnutrition, and spiny tenrecs are a crucial source of subsistence bushmeat with 91% of households consuming tenrecs at least once per year. Moreover, Makira’s human populations are increasing, resulting in forest decline and degradation. In order to inform conservation and public health efforts, we investigated the influence of hunting, habitat loss and forest degradation on spiny tenrec population dynamics in the Makira region. We collected data on tenrec population densities as well as hunting and consumption by humans in 51 communities. We used these data to conduct a population viability analysis for the two most commonly hunted spiny tenrecs (Tenrec ecaudatus and Setifer setosus). We found that current harvest rates for these species are generally sustainable in the Makira region, largely due to tenrecs’ extraordinary fecundity. However, even assuming no change in current hunting rates, tenrec populations could become threatened if fecundity were to decline or background mortality to increase, both possible scenarios under future trajectories of habitat loss and degradation. We find that any future increase in hunting-induced mortality rates for tenrecs are similarly unsustainable – and likely to occur as human populations expand and hunting areas decline. We conclude that there is a vanishing window of opportunity to sustainably manage tenrec hunting in northeastern Madagascar in order to avoid negative conservation and human health outcomes.
Conflicts of interest
We have no conflicts of interest to declare.
Open Research
Data availability statement
HSPH Office for Human Research Administration IRB 22826-01 prevents us from publicly disclosing hunter harvest data. Citations to publicly available datasets are provided in the text.
Supporting Information
Filename | Description |
---|---|
acv12714-sup-0001-Supinfo.docxWord 2007 document , 1.1 MB |
Text S1. Study Sites. Text S2. Study Species. Text S3. Trapping Arrangements. Text S4. Sensitivity Analysis for Impact of T. Ecaudatus Density on Model Results. Text S5. Formulating Generalized Linear Models of Consumption. Text S6. Estimation of Distribution of Tenrecine Population Sizes. Text S7. Derivation of Life History Parameters from the Literature. Text S8. Construction and Analysis of Lefkovitch Matrices. Figure S1. Locations of Study Sites. The full 51 surveyed communities are shown on the map, and the three where live tenrec trapping was conducted are marked in red. Figure S2. Configuration of pit-fall line and Tomahawk Live Traps. Figure S3. Distributions of stochastically simulated densities (a), hunt areas (b) and population (c,d). Figure S4. Sensitivity Analysis for impact of T. Ecaudatus density simulated as 1x that of S. Setosus density on simulated densities (a), population size (b), annual adult mortality (c), and number of communities with sustainable hunting under various parameter estimates (d). Figure S5. Sensitivity Analysis for impact of T. Ecaudatus density simulated as 0.5x that of S. Setosus density on simulated densities (a), population size (b), annual adult mortality (c), and number of communities with sustainable hunting under various parameter estimates (d). Figure S6. Distributions of annual adult mortality for T. ecaudatus (a) and S. setosus (b). Figure S7. Lefkovitch Matrix construction (a), Lefkovitch Matrices (a,c) and Elasticity Matrices (b,d). Figure S8. Predicted maximum number of households for sustainable hunting of T. ecaudatus (a) and S. setosus (b). |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- Annapragada, A., Borgerson, C., Iams, S., Ravelomanantsoa, M.A., Crawford, G.C., Helin, M., Anjaranirina, E.J.G., Randriamady, H.J. & Golden, C.D. (2019). Modeling the impact of newcastle disease virus vaccinations on chicken production systems in northeastern madagascar. Front Veterinary Sci 6, https://doi.org/10.3389/fvets.2019.00305.
- Augusteyn, R.C. (2014). Growth of the eye lens: I. Weight accumulation in multiple species. Molecular Vision 20, 410–426.
- Borgerson, C., Johnson, S.E., Louis, E.E., Holmes, S.M., Gasta, A.E.J., Randriamady, H.J. & Golden, C.D. (2018). The use of natural resources to improve household income, health, and nutrition within the forests of Kianjavato, Madagascar. Madagascar Conserv Develop 13, 45–52.
- Borgerson, C., Vonona, M.A., Vonona, T., Anjaranirina, E.J.G., Lewis, R., Ralainasolo, F. & Golden, C.D. (2018). An evaluation of the interactions among household economies, human health, and wildlife hunting in the Lac Alaotra wetland complex of Madagascar. Madagascar Conserv Develop 13, 25–33–33. https://doi.org/10.4314/mcd.v13i1.5.
- Brook, C.E., Herrera, J.P., Borgerson, C., Fuller, E.C., Andriamahazoarivosoa, P., Rasolofoniaina, B.J.R., Randrianasolo, J.L.R.R., Rakotondrafarasata, Z.R.E., Randriamady, H.J., Dobson, A.P. & Golden, C.D. (2018). Population viability and harvest sustainability for Madagascar lemurs. Conserv. Biol. https://doi.org/10.1111/cobi.13151.
- Brook, C.E., Ranaivoson, H.C., Andriafidison, D., Ralisata, M., Razafimanahaka, J., Héraud, J.-M., Dobson, A.P. & Metcalf, C.J. (2019). Population trends for two Malagasy fruit bats. Biol. Conserv. 234, 165–171. https://doi.org/10.1016/j.biocon.2019.03.032.
- Brooks, M.E., Kristensen, K., van Benthem, K.J., Magnusson, A., Berg, C.W., Nielsen, A., Skaug, H.J., Mächler, M. & Bolker, B.M. (2017). GlmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J. 9, 378–400.
- Burgess, M.G., Costello, C., Fredston-Hermann, A., Pinsky, M.L., Gaines, S.D., Tilman, D. & Polasky, S. (2017). Range contraction enables harvesting to extinction. Proc. Natl. Acad. Sci. 114, 3945–3950. https://doi.org/10.1073/pnas.1607551114.
- Caswell, H. (2006). Matrix population models: construction, analysis, and interpretation (Second). Sunderland, MA: Sinauer Associates.
- Caswell, H. & Trevisan, M.C. (1994). Sensitivity analysis of periodic matrix models. Ecology 75, 1299–1303. https://doi.org/10.2307/1937455.
- Central Intelligence Agency. (2020). Madagascar—The World Factbook. Retrieved May 7, 2021, from https://www.cia.gov/the-world-factbook/countries/madagascar/
- Dennis, B. (2002). Allee effects in stochastic populations. Oikos 96, 389–401.
- Dobson, A.P. & Lyles, A.M. (1989). The population dynamics and conservation of primate populations. Conserv. Biol. 3, 362–380. https://doi.org/10.1111/j.1523-1739.1989.tb00242.x.
- Efford, M. (2021). secr: Spatially Explicit Capture-Recapture (4.4.1). [Computer software] https://CRAN.R-project.org/package=secr.
- Everson, K.M., Soarimalala, V., Goodman, S.M. & Olson, L.E. (2016). Multiple loci and complete taxonomic sampling resolve the phylogeny and biogeographic history of tenrecs (Mammalia: Tenrecidae) and reveal higher speciation rates in madagascar’s humid forests. Systematic Biol. 65, 890–909. https://doi.org/10.1093/sysbio/syw034.
- Farris, Z.J., Golden, C.D., Karpanty, S., Murphy, A., Stauffer, D., Ratelolahy, F., Andrianjakarivelo, V., Holmes, C.M. & Kelly, M.J. (2015). Hunting, exotic carnivores, and habitat loss: anthropogenic effects on a native carnivore community, Madagascar. PLoS One 10, e0136456. https://doi.org/10.1371/journal.pone.0136456.
- Golden, C.D. (2009). Bushmeat hunting and use in the Makira Forest, north-eastern Madagascar: a conservation and livelihoods issue. Oryx 43, 386–392. https://doi.org/10.1017/S0030605309000131.
- Golden, C.D., Anjaranirina, E.J.G., Fernald, L.C.H., Hartl, D.L., Kremen, C., Milner, D.A., Ralalason, D.H., Ramihantaniarivo, H., Randriamady, H., Rice, B.L., Vaitla, B., Volkman, S.K., Vonona, M.A. & Myers, S.S. (2017). Cohort Profile: The Madagascar Health and Environmental Research (MAHERY) study in north-eastern Madagascar. Int. J. Epidemiol. 46, 1747–1748d. https://doi.org/10.1093/ije/dyx071.
- Golden, C.D., Bonds, M.H., Brashares, J.S., Rodolph Rasolofoniaina, B.J. & Kremen, C. (2014). Economic valuation of subsistence harvest of wildlife in Madagascar. Conserv. Biol. 28, 234–243. https://doi.org/10.1111/cobi.12174.
- Golden, C.D., Fernald, L.C.H., Brashares, J.S., Rasolofoniaina, B.J.R. & Kremen, C. (2011). Benefits of wildlife consumption to child nutrition in a biodiversity hotspot. Proc. Natl Acad Sci. 108, 19653–19656. https://doi.org/10.1073/pnas.1112586108.
- Golden, C.D., Vaitla, B., Ravaoliny, L., Vonona, M.A., Anjaranirina, E.G., Randriamady, H.J., Glahn, R.P., Guth, S.E., Fernald, L.C. & Myers, S.S. (2019). Seasonal trends of nutrient intake in rainforest communities of north-eastern Madagascar. Public Health Nutr. 22, 2200–2209. https://doi.org/10.1017/S1368980019001083.
- Goodman, S.M., Raherilalao, M.J. & Wohlauser, S. (2018). The terrestrial protected areas of Madagascar: their history, description, and biota. Antananarivo, Madagascar: Association Vahatra.
- Goodman, S., Soarimalala, V. & Olson, L.E. (2018). Systematics of endemic Malagasy tenrecs (family Tenrecidae). In S.M. Goodman, M.J. Raherilalao & S. Wohlauser (Eds.), The terrestrial protected areas of madagascar: their history, description, and biota (pp. 363–372). Antananarivo, Madagascar: Association Vahatra.
- Halliday, T.R. (1980). The extinction of the passenger pigeon ectopistes migratorius and its relevance to contemporary conservation. Biol. Cons. 17, 157–162. https://doi.org/10.1016/0006-3207(80)90046-4.
- Harper, G.J., Steininger, M.K., Tucker, C.J., Juhn, D. & Hawkins, F. (2007). Fifty years of deforestation and forest fragmentation in Madagascar. Environ. Conserv. 34, 325–333.
- Harrison, T.M. & Harrison, S.H. (2017). Evaluation of Husbandry and mortality in lesser hedgehog tenrecs (echinops telfairi). J. Zoo Wildlife Med. 48, 440–445. https://doi.org/10.1638/2016-0114.1.
- Hayssen, V., Tienhoven, A. & Tienhoven, A. (1993). Asdell’s patterns of mammalian reproduction: a compendium of species-specific data. Ithaca, NY: Cornell University Press.
- Ingram, D.J., Coad, L., Milner-Gulland, E.J., Parry, L., Wilkie, D., Bakarr, M.I., Benítez-López, A., Bennett, E.L., Bodmer, R., Cowlishaw, G., El Bizri, H.R., Eves, H.E., Fa, J.E., Golden, C.D., Iponga, D.M., Minh, N.V., Morcatty, T.Q., Mwinyihali, R., Nasi, R., Nijman, V., Ntiamoa-Baidu, Y., Pattiselanno, F., Peres, C.A., Rao, M., Robinson, J.G., Rowcliffe, J.M., Stafford, C., Supuma, M., Tarla, F.N., van Vliet, N., Wieland, M. & Abernethy, K. (in press). Wild meat is still on the menu: Progress in wild meat research, policy and practice from 2002 to 2020. Annu. Rev. Environ. Resour.
- INSTAT Madagascar (2019). Troisieme recensement general de la population et de l’habitation (rgph-3). Retrieved May 7, 2021, from http://www.instat.mg/wp-content/uploads/Rapport-Prelim-2019_ver_final.pdf.
- INSTAT/DDSS. (2009). Données de la cartographie censitaire mises-à-jour.
- Jones, K.E., Bielby, J., Cardillo, M., Fritz, S.A., O’Dell, J., Orme, C.D.L., Safi, K., Sechrest, W., Boakes, E.H., Carbone, C., Connolly, C., Cutts, M.J., Foster, J.K., Grenyer, R., Habib, M., Plaster, C.A., Price, S.A., Rigby, E.A., Rist, J., Teacher, A., Bininda-Emonds, O.R.P., Gittleman, J.L., Mace, G.M. & Purvis, A. (2009). PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals. Ecology 90, 2648. https://doi.org/10.1890/08-1494.1.
- Künzle, H. (1998). Care and breeding of the Madagascan hedgehog tenrec, Echinops telfairi, under laboratory conditions. Der Tierschutzbeauftragte 5–12. https://tenrec.lima-city.de/kuenzle.htm
- Lefkovitch, L.P. (1965). The study of population growth in organisms grouped by stages. Biometrics 21, 1–18. https://doi.org/10.2307/2528348.
- Leslie, P.H. (1945). On the use of matrices in certain population mathematics. Biometrika 33, 183–212. https://doi.org/10.1093/biomet/33.3.183.
- Leslie, P.H. (1948). Some further notes on the use of matrices in population mathematics. Biometrika 35(3–4), 213–245. https://doi.org/10.1093/biomet/35.3-4.213.
- Levesque, D.L., Lovasoa, O.M.A., Rakotoharimalala, S.N. & Lovegrove, B.G. (2013). High mortality and annual fecundity in a free-ranging basal placental mammal, Setifer setosus (Tenrecidae: Afrosoricida). J. Zool. 291, 205–212. https://doi.org/10.1111/jzo.12063.
- Levesque, D.L., Rakotondravony, D. & Lovegrove, B.G. (2012). Home range and shelter site selection in the greater hedgehog tenrec in the dry deciduous forest of Western Madagascar. J. Zool. 287, 161–168. https://doi.org/10.1111/j.1469-7998.2012.00899.x.
- Lyles, A.M. & Dobson, A.P. (1988). Dynamics of provisioned and unprovisioned primate populations. The ecology and behaviour of food-enhanced primate groups, (Vol. 11, pp 167–198). New York, NY: Alan R. Liss Inc.
- Met Office (2010). Cartopy: A cartographic python library with a matplotlib interface. [Computer software] https://scitools.org.uk/cartopy.
- Nielsen, M.R., Meilby, H., Smith-Hall, C., Pouliot, M. & Treue, T. (2018). The importance of wild meat in the Global South. Ecol. Econ. 146, 696–705. https://doi.org/10.1016/j.ecolecon.2017.12.018.
- Olson, L.E. (2013). Tenrecs. Curr. Biol. R5–R8. https://doi.org/10.1016/j.cub.2012.11.015.
- Petter, J.-J. & Petter-Rousseaux, A. (1963). Notes biologiques sur les Centetinae. La Terre et la Vie 17, 66–80.
- Rakotomanana, H., Gates, G.E., Hildebrand, D. & Stoecker, B.J. (2017). Determinants of stunting in children under 5 years in Madagascar. Maternal Child Nutr. 13, e12409. https://doi.org/10.1111/mcn.12409.
- Ripple, W.J., Abernethy, K., Betts, M.G., Chapron, G., Dirzo, R., Galetti, M., Levi, T., Lindsey, P.A., Macdonald, D.W., Machovina, B., Newsome, T.M., Peres, C.A., Wallach, A.D., Wolf, C. & Young, H. (2016). Bushmeat hunting and extinction risk to the world’s mammals. Royal Society Open. Science 3, https://doi.org/10.1098/rsos.160498.
- Rose, G.A. & Kulka, D.W. (1999). Hyperaggregation of fish and fisheries: How catch-per-unit-effort increased as the northern cod (Gadus morhua) declined. Can. J. Fish. Aquat. Sci. 56, 118–127. https://doi.org/10.1139/f99-207.
- Stephenson, P.J. (2007). Mammals from another time: tenrecs in Madagascar. Africa Geographic 15, 34–41.
- Stephenson, P.J., Racey, P.A. & Rakotondraparany, F. (2007). Maintenance and reproduction of tenrecs Tenrecidae: at Parc Tsimbazaza, Madagascar. Int. Zoo Yearbook 33, 194–201. https://doi.org/10.1111/j.1748-1090.1994.tb03573.x.
- Stephenson, P.J., Soarimalala, V., Goodman, S.M., Nicoll, M.E., Andrianjakarivelo, V., Everson, K.M., Hoffmann, M., Jenkins, P.D., Olson, L.E., Raheriarisena, M., Rakotondraparany, F., Rakotondravony, D., Randrianjafy, V., Ratsifandrihamanana, N. & Taylor, A. (2019). Review of the status and conservation of tenrecs (Mammalia: Afrotheria: Tenrecidae). Oryx 55, 13–22. https://doi.org/10.1017/S0030605318001205.
- Stubbs, T.M., Bonder, M.J., Stark, A.-K., Krueger, F., von Meyenn, F., Stegle, O. & Reik, W. (2017). Multi-tissue DNA methylation age predictor in mouse. Genome Biol. 18, 68. https://doi.org/10.1186/s13059-017-1203-5.
- Tao, J. & Li, Y.O. (2018). Edible insects as a means to address global malnutrition and food insecurity issues. Food Quality Safety 2, 17–26. https://doi.org/10.1093/fqsafe/fyy001.
- UNICEF Madagascar (2018). Fécondité et Planification familiale. Retrieved May 7, 2021, from https://www.unicef.org/madagascar/documents/mics-6-2018-fécondité-et-planification-familiale.
- Vieilledent, G., Grinand, C., Rakotomalala, F.A., Ranaivosoa, R., Rakotoarijaona, J.R., Allnutt, T.F. & Achard, F. (2018). Combining global tree cover loss data with historical national forest cover maps to look at six decades of deforestation and forest fragmentation in Madagascar. Biol. Cons. 222, 189–197. https://doi.org/10.1016/j.biocon.2018.04.008.
- Zaehringer, J., Eckert, S. & Messerli, P. (2015). Revealing regional deforestation dynamics in North-Eastern Madagascar—insights from multi-temporal land cover change Analysis. Land 4, 454–474. https://doi.org/10.3390/land4020454.
- Zullinger, E.M., Ricklefs, R.E., Redford, K.H. & Mace, G.M. (1984). Fitting sigmoidal equations to mammalian growth curves. J. Mammal. 65, 607–636. https://doi.org/10.2307/1380844.