Review of the Status and Conservation of Tenrecs (Mammalia: Afrotheria: Tenrecidae)

Home , Afrosoricida, Hemicentetes, Insectivora, Marojejy National Park, Marotandrano Reserve, Microgale

Review of the status and conservation of tenrecs (Mammalia: Afrotheria: Tenrecidae)

P. J. STEPHENSON,VOAHANGY S OARIMALALA,STEVEN M. GOODMAN M ARTIN E. NICOLL,VONJY A NDRIANJAKARIVELO,KATHRYN M. EVERSON M ICHAEL H OFFMANN,PAULINA D. JENKINS,LINK E. OLSON M ARTIN R AHERIARISENA,FELIX R AKOTONDRAPARANY D ANIEL R AKOTONDRAVONY,VOLOLOMBOAHANGY R ANDRIANJAFY N ANIE R ATSIFANDRIHAMANANA and A NDREW T AYLOR

Abstract The mammal family Tenrecidae (Afrotheria: and-burn agriculture, but some species are also threatened Afrosoricida) is endemic to Madagascar. Here we present by hunting and incidental capture in fishing traps. In the the conservation priorities for the  species of tenrec that longer term, climate change is expected to alter tenrec habi- were assessed or reassessed in – for the IUCN tats and ranges. However, the lack of data for most tenrecs Red List of Threatened Species. Six species (.%) were on population size, ecology and distribution, together with found to be threatened ( Vulnerable,  Endangered) and frequent changes in taxonomy (with many cryptic species one species was categorized as Data Deficient. The primary being discovered based on genetic analyses) and the poorly threat to tenrecs is habitat loss, mostly as a result of slash- understood impact of bushmeat hunting on spiny species (Tenrecinae), hinders conservation planning. Priority conservation actions are presented for Madagascar’s tenrecs for the first time since  and focus on conserving forest habi-

P. J. STEPHENSON* (Corresponding author, orcid.org/0000-0002-0087-466X) tat (especially through improved management of protected IUCN SSC Species Monitoring Specialist Group, c/o Ecosystem Management areas) and filling essential knowledge gaps. Tenrec research, Group, Department of Environmental Systems Science, ETH Zürich, Zürich, Switzerland. E-mail [email protected] monitoring and conservation should be integrated into broader sustainable development objectives and pro- VOAHANGY SOARIMALALA† ( orcid.org/0000-0002-2455-2956) and STEVEN M. GOODMAN‡ ( orcid.org/0000-0001-9318-0570) Association Vahatra, grammes targeting higher profile species, such as lemurs, Antananarivo, Madagascar if we are to see an improvement in the conservation status MARTIN E. NICOLL ( orcid.org/0000-0003-2647-5808) Conservation of tenrecs in the near future. Programme, WWF-Madagascar, Antananarivo, Madagascar Keywords VONJY ANDRIANJAKARIVELO ( orcid.org/0000-0001-9025-073X) Madagascar Afrotheria, conservation, IUCN Red List of Program, Wildlife Conservation Society, Maroantsetra, Madagascar Threatened Species, Madagascar, Microgale, Oryzorictes,

KATHRYN M. EVERSON ( orcid.org/0000-0003-1495-7076) and LINK E. OLSON Tenrecidae, threats ( orcid.org/0000-0002-2481-5701) Department of Biology and Wildlife, University of Alaska Museum, Fairbanks, Alaska, USA

MICHAEL HOFFMANN ( orcid.org/0000-0003-4785-2254) Global Conservation Programmes, Zoological Society of London, London, UK

PAULINA D. JENKINS ( orcid.org/0000-0002-8250-0601) Life Sciences Department, The Natural History Museum, London, UK Introduction MARTIN RAHERIARISENA,FELIX RAKOTONDRAPARANY and DANIEL RAKOTONDRAVONY ’ Mention Zoologie et Biodiversité Animale, Université d Antananarivo, he mammal family Tenrecidae (Supercohort Afrotheria: Antananarivo, Madagascar Order Afrosoricida), endemic to the Indian Ocean is- OLOLOMBOAHANGY ANDRIANJAFY T V R Faculté des Sciences, de Technologie et de  l’Environnement, Université de Mahajanga, Mahajanga, Madagascar land of Madagascar, contains currently recognized extant species in three subfamilies: the Geogalinae ( species), NANIE RATSIFANDRIHAMANANA WWF-Madagascar, Antananarivo, Madagascar Oryzorictinae () and Tenrecinae (). The tailless tenrec ANDREW TAYLOR ( orcid.org/0000-0002-2896-5168) Wildlife in Trade Programme, The Endangered Wildlife Trust, Johannesburg, South Africa Tenrec ecaudatus has been introduced by humans to neigh- *Also at: Science & Knowledge Unit, IUCN, Gland, Switzerland bouring archipelagos. Tenrecs exhibit a diverse array of †Also at: Institut des Sciences et Techniques de l’Environnement, Université de body sizes and morphological, behavioural, physiological Fianarantsoa, Fianarantsoa, Madagascar and ecological specializations, representing an adaptive ‡Also at: Integrative Research Center, Field Museum of Natural History, Chicago, Illinois, USA radiation that is a model for evolutionary research   Received  May . Revision requested  July . (e.g. Eisenberg & Gould, ; Stephenson & Racey, ; Accepted  September . First published online  April . Olson & Goodman, ; Everson et al., ).

This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, Downloadeddistribution, from https://www.cambridge.org/core and reproduction in any medium,. IP address: provided 170.106.202.8 the original work, onis 30 properly Sep 2021 cited. at 22:09:45, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/termsOryx, 2021, 55(1), 13–22 © The. https://doi.org/10.1017/S0030605318001205 Author(s), 2019. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605318001205 14 P. J. Stephenson et al.

Most tenrecs are dependent on forest habitats, and, with can also be considered Data Deficient ‘when there is inad- Madagascar having lost c. % of its forests in the last  equate information to make a direct or indirect assessment years (Harper et al., ), the conservation status of of its risk of extinction’ (IUCN, ). During the second many species is of concern. If the biodiversity of the country stage of the review, a workshop was held in April  is to be conserved, its fauna and flora need to be assessed by the Tenrec Section of the IUCN Species Survival regularly and relevant conservation strategies must be Commission (SSC) Afrotheria Specialist Group, associated developed. with the th African Small Mammals Symposium in The IUCN Red List of Threatened Species (IUCN, ; Mantasoa, Madagascar, to review the data collected and hereafter the IUCN Red List) is the most widely used tool the draft assessments. At that time, we also developed for assessing the conservation status of species. Any new conservation priorities based on identified threats (as per data for the IUCN Red List not only advances the knowl- the Open Standards for the Practice of Conservation; edge needed to define conservation action but also pro- Conservation Measures Partnership, ). During the vides countries with data against which to report on their third stage, we conducted a literature review on broader environmental goals, such as those defined in the Aichi conservation issues in Madagascar, to refine and finalize Targets and Sustainable Development Goals (Brooks the priorities. et al., ). There is ongoing discussion about tenrec systematics Here we review the current conservation status of the (e.g. Poux et al., ; Asher & Helgen, ; Everson Tenrecidae, as defined in the last species assessments con- et al., ). To ensure we consider the latest recognized ducted for the IUCN Red List in –,withtheaimof taxonomies, here we treat the three species of otter-shrew identifying trends in extinction risk, habitat needs and on mainland Africa (once considered tenrecs) as a separate threats. We also identify conservation priorities to ensure family, the Potamogalidae (following Everson et al., ). a future for these poorly known small mammals. This is We similarly follow those authors’ synonymization of the the first time the conservation needs of tenrecs have genus Limnogale with Microgale (see also Asher & Helgen, been compiled for almost  decades (Nicoll & Rathbun, ) and placement of the large-bodied shrew tenrecs ). Microgale dobsoni and Microgale talazaci in the genus Nesogale.

Methods Extinction risk We conducted this review in three stages. Firstly, during –, we reassessed the status of all species in the Of the  species assessed,  (.%) were categorized as Tenrecidae for the IUCN Red List (IUCN, ). Least Concern, one species (.%) as Data Deficient Grandidier’s shrew tenrec Microgale grandidieri had not (Oryzorictes tetradactylus), four species (.%) as Vulner- been assessed before as it was described only in  able (Microgale dryas, Microgale mergulus, Microgale mon- (Olson et al., ), subsequent to the last comprehensive ticola, Microgale nasoloi) and two (.%) as Endangered assessment of all mammals (Schipper et al., ). Using (Microgale jenkinsae, Microgale jobihely; Table ). In this information available for each species from the literature, assessment, all species were placed in the same Red List such as the latest georeferenced distribution data collated category as in previous assessments in  and  by Goodman et al. () and past and recent assessments (Hoffmann et al., ). The status of some species has re- of threats to and conservation priorities for tenrecs (e.g. mained constant for much longer. For example, the aquatic Nicoll & Rathbun, ; Stephenson, a,b, , a; tenrec M. mergulus was also considered Vulnerable  years Stephenson et al., ; Jenkins et al., ; Nicoll & ago when it was first assessed. This consistency across as- Ratsifandrihamanana, ), and based on the assessors’ sessments probably reflects the lack of concrete data on knowledge, we collated data on geographical range (includ- the impact of continued forest loss on population numbers. ing area of occupancy or extent of occurrence), estimated Grandidier’s shrew tenrec M. grandidieri, which had not population trends (or relative abundance), habitat use, life previously been assessed, was categorized as Least Concern. history traits, use and trade, threats, conservation actions Five of the six threatened species were categorized as currently in place and conservation actions needed. We Vulnerable or Endangered under criterion B, in which status then used this information to assess the risk of extinction is determined primarily on geographical range and number for each species by applying the IUCN Red List categories of locations. The two Endangered species had an extent of  and criteria (IUCN, ) which allowed us to assign each occurrence (EOO) , , km and were both known species to a category of threat ranging through Extinct, from less than five sites: Jenkins’ shrew tenrec M. jenkinsae Extinct in the Wild, Critically Endangered, Endangered, is known only from Mikea National Park (Goodman & Vulnerable, Near Threatened and Least Concern. A species Soarimalala, ; Stephenson et al., c) and there are

Oryx, 2021, 55(1), 13–22 © The Author(s), 2019. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605318001205 Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.8, on 30 Sep 2021 at 22:09:45, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318001205 The status and conservation of tenrecs 15

TABLE 1 Malagasy tenrecs categorized as threatened or Data Deficient following the IUCN Red List assessment of –. The remaining  of the  Malagasy species assessed were considered Least Concern. Note that in the IUCN Red List, the aquatic tenrec was assessed as Limnogale mergulus, whereas the IUCN SSC Afrotheria Specialist Group now recognizes this as a synonym of Microgale. For full details on each species, including data sources, see Stephenson et al. (a,b,c,d,e,f,g). For species assessed and considered Least Concern, see IUCN Afrotheria Specialist Group ().

Red List status1 Justification for listing Species & criteria AOO/EOO2 Locations Habitat Offtake3 Dryad shrew tenrec Microgale dryas VU B1ab(iii) EOO 7,911 km2 9 Declining No (, 20,000 km2)

Jenkins’ shrew tenrec Microgale jenkinsae EN B1ab(iii) EOO , 2,000 km2 1 Declining No (, 5,000 km2)

Northern shrew tenrec Microgale jobihely EN B1ab(iii) EOO , 5,000 km2 3 Declining No (2 populations)

Aquatic tenrec Microgale mergulus VU B2ab(ii, iii) AOO , 2,000 km2 10 Declining Yes

Montane shrew tenrec Microgale monticola VU D2 EOO 3,496 km2 4 Declining No (, 5,000 km2)

Nasolo’s shrew tenrec Microgale nasoloi VU B1ab(iii) EOO 10,183 km2 4 Declining No (, 20,000 km2)

Four-toed mole tenrec Oryzorictes tetradactylus DD Most specimens caught Unknown No . 100 years ago

 VU, Vulnerable; EN, Endangered; DD, Data Deficient.  Data on area of occupancy (AOO) and extent of occurrence (EOO) were derived from Goodman et al. ().  Offtake refers to direct capture (intentional or unintentional).

 only two widely disjunct populations of the northern relatively small EOO of , km (Goodman et al., ). shrew tenrec M. jobihely (Soarimalala et al., ; However, it is assumed that its relatively high local abun- Stephenson et al., d). All four Vulnerable species dance and apparent tolerance of anthropogenic habitats are known from  sitesorless,ofwhichthreehadan mean that the species does not meet any of the subcriteria  EOO , , km (and were categorized under criterion for a threatened category (Stephenson et al., h). Most B), and one, the aquatic tenrec M. mergulus,which species assessed as Least Concern are probably declining lives exclusively in riverine habitat, had an estimated because of continued habitat loss across Madagascar, and  area of occupancy (AOO) of , , km and was cate- their status will need to be monitored. gorized under criterion B. The montane shrew tenrec M. monticola was categorized as Vulnerable under criterion D (which relates to small and very restricted popula- Habitats tions), as it is known from only four sites in an EOO of  , , km . Subtropical/tropical moist lowland forest and subtropical/ A single species, the four-toed mole tenrec Oryzorictes tropical moist montane forest are the habitat types (as de- tetradactylus, was considered Data Deficient because fined by IUCN, ) with the highest number of tenrec spe- there is no recent information on its EOO, population cies and whose conservation will ensure the greatest tenrec and threats (Stephenson et al., g), which meant we diversity (Table ). However, western dry forests are key for could not assess its status. Like many fossorial and semi- some species, especially the threatened Jenkins’ shrew tenrec fossorial species, mole tenrecs are difficult to trap, and the and Nasolo’s shrew tenrec (Fig. ; Goodman & Soarimalala, majority of records of this species are from more than a ; Soarimalala & Goodman, ). Riparian habitats are century ago. important for the aquatic tenrec (Plate ), and the four-toed Amongst the species categorized as Least Concern, mole tenrec is known from montane ericoid thicket (cate- the highland streaked tenrec Hemicentetes nigriceps has a gorized by IUCN as high-altitude grass or shrublands).

TABLE 2 Habitat types important for tenrec species in Madagascar. Habitat categories are derived from the IUCN Red List of Threatened Species (IUCN ).

Threatened or Data Deficient tenrec Habitat types (IUCN Classification System) No. of tenrec species species in the habitat 1.5 Subtropical/tropical dry forest 6 Microgale jenkinsae Microgale nasoloi 1.6 Subtropical/tropical moist lowland forest 20 Microgale mergulus Microgale dryas 1.9 Subtropical/tropical moist montane forest 20 Microgale jobihely Microgale monticola Oryzorictes tetradactylus 3.5 Subtropical/tropical dry shrubland 2 Microgale jenkinsae 3.7 Subtropical/tropical high altitude shrubland 1 Oryzorictes tetradactylus 4.7 Subtropical/tropical high altitude grassland 1 Oryzorictes tetradactylus 5.1 Permanent rivers, streams, creeks 1 Microgale mergulus 5.4 Bogs, marshes, swamps, fens, peatlands 1

Some species, such as the Hova mole tenrec Oryzorictes is low (Allnutt et al., ; Eklund et al., ; Gardner hova, the tailless tenrec and the lowland streaked tenrec et al., ). Hemicentetes semispinosus, tolerate human-altered habitats, Spiny tenrecs of the subfamily Tenrecinae are hunted such as gardens or rice fields, to an unknown extent. across most of the island, within and outside protected areas, and the meat is consumed for subsistence or sold in local restaurants and urban markets (Garcia &   Threats Goodman, ; Randrianandrianina et al., ; Jenkins et al., ; Reuter et al., ). The tailless tenrec, The main threats facing tenrecs are habitat loss, fragmen- which is widespread and occurs in many habitats, is the tation and degradation (% of species) and hunting most commonly consumed species. It is legal to hunt for subsistence or bushmeat trade (% of species). tenrecs in Madagascar (e.g. the tailless tenrec is on the Incidental capture (bycatch) in fishnets and traps is a game species list in decree –), even though the threat to the aquatic tenrec. Climate change is considered government acknowledges that hunting and the bush- a long-term threat to most species. Lack of knowledge meat trade are a significant threat to these mammals curtails our ability to assess threats and species status (Rabarison et al., ). The level of offtake is uncertain and therefore hinders our ability to identify conservation but can be significant locally. For example, hunters catch priorities accurately. up to  tenrecs per hunt (Randrianandrianina et al., Deforestation rates are estimated to range from . to ) and ,–, tenrecs are consumed per year in .% per year for the humid forest and from . to .% the city of Antsiranana (Reuter & Sewall, ). Until per year for dry forest (Grinand et al., ). The main the impact of hunting on population levels is better cause of forest loss is traditional slash-and-burn agricul- understood, all exploited species were categorized as ture, as well as commercial logging for timber, mining of Least Concern. precious metals and semi-precious gems (such as sap- Climate change is a direct threat to biodiversity and a phires), uncontrolled fires and infrastructure develop- driver of other threats (Hannah et al., ). Madagascar ment. Dry deciduous forest is increasingly cleared for ranksthirdintheworldforextremeclimaterisk cash crops such as peanuts for foreign markets (NR, (Verisk Maplecroft, ).Climatechangeispredicted pers. obs.). to lead to altered habitats and niche availability and Five of the six threatened tenrec species are dependent on changes in species ranges, as demonstrated in lemurs native forest habitats, and the aquatic tenrec inhabits clear, where the range of % of species is expected to decline free-flowing streams with stony beds that are threatened in  years (Brown & Yoder, ). Tenrec habitat, species by the siltation resulting from forest loss. Although the distribution and abundance are similarly expected to coverage of Madagascar’s protected area network quad- change, but no projections have been made on the likely rupled since  (Gardner et al., ), and all tenrec extent of the change. Because species restricted to moun- species occur in at least one protected area (Nicoll & tains have less scope to disperse, montane forest-dwelling Ratsifandrihamanana, ), deforestation is occurring in species of shrew tenrecs could be most vulnerable to many parks and reserves where law enforcement capacity climate change.

PLATE 1 The aquatic tenrec Microgale mergulus is categorized as Vulnerable because of its restricted number of known sites ()  and limited area of occupancy (, , km ). © P.J. Stephenson.

morphometric studies of museum specimens. The genus Microgale has been the subject of taxonomic revisions and reorganization (e.g. Stephenson b; Everson et al., ), five new species were described in the last  years and numerous new species are expected in the next two years (Everson et al., ; LEO, unpubl. data). Other key data gaps include the impacts of hunting on spiny tenrecs and the relative dependence of species on intact forest habitats.

FIG. 1 Distribution map of threatened tenrecs in Madagascar, Conservation priorities showing the known key areas for tenrec habitat (map courtesy of  Natalia Ocampo; data from IUCN, , based on Goodman Our review suggests conservation efforts for tenrecs need to  et al., ). focus primarily on the seven species identified as threatened or Data Deficient in the IUCN Red List (Table ). There is a Madagascar’s environment is now more degraded than need to improve the management and protection of key  years ago (Freudenberger, ; Goodman et al., in habitats and enhance our knowledge base. press). Pressures on natural resources are increasing, largely   because the human population has risen from . million Priorities for tenrec habitat conservation in  to . million in  (World Bank, ). The national economy is weak (gross domestic product has The main action required to conserve threatened tenrecs is halved since ) and the World Bank () calculates the protection of adequately sized, interconnected blocks of that % of the population live below the international suitable forest habitat, primarily through the creation and poverty line (USD . per person per day), making it effective management of protected areas. Deforestation one of the  poorest countries in the world. Most needs to be halted, particularly within the ranges of threa- Malagasy rely on the direct use of natural resources for tened tenrecs (Fig. ). Habitat restoration will be needed in their livelihoods, which affects many mammals and their some sites affected by mining or logging. If protection habitats. and restoration measures also incorporate riverine forest All threatened tenrec species are known from only a few corridors, enhance connectivity between forest blocks and individuals captured at  or fewer locations, making it hard conserve areas with high levels of altitudinal variation, to determine accurately their distribution, abundance, habi- they will help maximize species’ capacity to respond to a tat preferences, or population trends. There have been few changing climate (Hannah et al., ). Climate models ecological studies and little information exists on tenrec that overlay the distribution of threatened tenrecs with behaviour. Few Malagasy protected areas have monitoring protected areas and remaining habitat are needed to iden- schemes in place. In addition, tenrec taxonomy is chang- tify priority areas for protection and restoration efforts in ing regularly as a result of ongoing genetic analyses and Madagascar.

The most important habitat types for tenrecs are dry considered in their monitoring and conservation pro- forest, moist lowland forest, moist montane forest and dry grammes (see Table ). shrubland, as well as permanent rivers, streams and creeks Efforts to conserve and sustainably manage forests im- (Table ). The inclusion of a representative sample of these portant for tenrecs and other species need to increase habitats in the protected area network, especially in tenrec their investments in capacity building (Waeber et al., ). range, needs to be verified. There are  protected areas cur- Priorities should include supporting local communities rently known to be important for threatened taxa (Table ) engaged in resource management and staff from agencies and these sites should be prioritized for conservation action. managing protected areas, such as Madagascar National Government agencies, protected area managers, NGOs, Parks and the Direction de Système des Aires Protégées in local communities and the private sector will need to the Ministry of Environment, Ecology, Seas and Forests. work together to improve the integrity and management Approaches also need to be diversified. For example, local effectiveness within protected areas. Priorities, as identified village governance bodies, such as dina, which oversee the by Gardner et al. (), include enhancing stakeholder application of traditional community regulations, could be participation, improving law enforcement and reducing supported in improving the internal control of habitat the natural resource dependence of local communities exploitation and hunting, in some instances by reinforcing through the development of alternative livelihoods. local taboos on tenrecs. The livelihood needs of local people need to be addressed In protected areas harbouring threatened tenrecs if conservation efforts are to succeed (Waeber et al., ). (Table ), the monitoring of key species population trends Developing alternatives to forest resources such as timber, needs to be integrated into site management. This will re- fuelwood and wild meat would reduce the impact on natural quire training and capacity building and the development forests. Community forest management schemes, especially of standardized monitoring protocols adapted to local needs those excluding commercial logging (Rasolofoson et al., and habitats, using modern techniques such as camera trap- ), and broader forest restoration programmes have de- ping and specialized techniques for fossorial, arboreal and monstrated some promising results in improving resource aquatic species that are difficult to trap. Most of the tools access and livelihoods in Madagascar (e.g. Mansourian and skills are already present in-country, but need to be et al., ). Rural demand for wild meat can be reduced scaled up. To improve adaptive management, additional through price increases driven by law enforcement efforts monitoring is required to track changes in forest cover, frag- to reduce supply (see Golden et al., ). The protection mentation and intactness (using data from satellite-based efforts to reduce supply should be complemented with remote sensing and aerial surveys). In parallel, threats and efforts to reduce demand, for example by increasing the illegal activities need to be tracked, for example with the supply of meat from domesticated animals, such as poultry Spatial Monitoring and Reporting Tool (SMART, ), (Apaza et al., ; Golden et al., ), as long as this supply which has been adopted nationally but is not yet used in is environmentally sustainable. all protected areas. Madagascar National Parks, the national Multi-taxonomic approaches to prioritization can enhance agency responsible for managing c. % of the island’spro- biodiversity conservation (Kremen et al., ). Given tected areas, already uses the Management Effectiveness tenrec habitats are also home to higher profile species Tracking Tool (WWF, ). This tool applies a score such as lemurs, for which more concerted conservation card approach to measure a range of variables important efforts are being made (Reuter & Venart, ; Schwitzer for effective management, from legal status and planning et al., ), it would be prudent to integrate tenrecs into to budgets and equipment. It could be introduced to new conservation projects targeting other threatened species sites, together with a peer-review process to enhance con- by, for example, promoting protection of areas critical for sistency in application. threatened tenrecs and including tenrecs in education and awareness campaigns. Five of the  protected areas conserving threatened tenrecs are also priorities for lemur Priorities for advancing knowledge on tenrecs conservation (Schwitzer et al., ): Anjanaharibe-Sud Special Reserve, Ankeniheny-Zahamena Corridor, Makira To improve the data available for IUCN Red List assess- Natural Reserve, Marojejy National Park and Ranomafana ments and conservation planning, knowledge gaps in tenrec National Park. The national and international NGOs and biology, ecology, taxonomy and distribution need to be research institutes that work in and around these five pro- filled. All research programmes should incorporate oppor- tected areas (including Association Mitsinjo, Centre ValBio, tunities for building capacity among Malagasy students, Conservation International, Duke Lemur Center, Lemur scientists and academic institutions to ensure the sustain- Conservation Foundation, The Aspinall Foundation, the ability of research and monitoring work. Small mammal Wildlife Conservation Society and WWF), as well as those ecology and conservation should also be integrated into operating in other sites, should ensure tenrec diversity is the curricula of national universities. Citizen science

TABLE 3 Key protected areas for the conservation of threatened tenrecs in Madagascar, with local names given in parentheses. Determining the status of tenrecs and other species in these reserves, and establishing systems to monitor them, is an urgent priority.

Priority Examples of NGOs and Threatened lemur Critically Endangered associations active in and Protected Area1 tenrecs present site2 lemurs present3 around the protected area Ambatovaky Special Reserve Microgale dryas Madagascar National Parks (Réserve Spéciale d’Ambatovaky) Ambositra-Vondrozo Forest Corridor Microgale mergulus Conservation International (Paysage Harmonieux Protégé du Corridor Forestier Ambositra-Vondrozo) Alandraza-Analavelo sacred forest Microgale nasoloi Missouri Botanical Garden (Monument Naturel de la Forêt Sacrée Alandraza Analavelo) Andringitra National Park Microgale mergulus Madagascar National Parks (Parc National d’Andringitra) Anjanaharibe-Sud Special Reserve Microgale dryas, Yes Propithecus candidus, Duke Lemur Center, Lemur (Réserve Spéciale d’Anjanaharibe-Sud) Microgale Indri indri Conservation Foundation, monticola Madagascar National Parks Ankeniheny-Zahamena Corridor Microgale dryas, Yes Prolemur simus, Varecia Conservation International, (Réserve de Ressources Naturelles du Microgale jobihely variegata, Indri indri, Association Mitsinjo, Corridor Ankeniheny-Zahamena) Propithecus diadema The Aspinall Foundation AZE tenrec site Bemanevika Landscape Microgale jobihely Durrell Wildlife (Paysage Harmonieux Protégé de Conservation Trust, Bemanevika) AZE tenrec site Madagascar National Parks, The Peregrine Fund, WWF Makira Natural Reserve Microgale dryas, Yes Propithecus candidus, WCS (Parc Naturel Makira) Microgale Varecia variegata, monticola Varecia rubra, Indri indri Menabe Antimena Microgale nasoloi Association Fanamby, (Paysage Harmonieux Protégé de Durrell Wildlife Menabe Antimena) Conservation Trust, WWF Marotandrano Special Reserve Microgale dryas Madagascar National Parks (Réserve Spéciale de Marotandrano) Marojejy National Park (Parc National Microgale Yes Propithecus candidus, Duke Lemur Center, Lemur Marojejy) monticola Indri indri Conservation Foundation, Madagascar National Parks

Mikea National Park Microgale Madagascar National Parks (Parc National Mikea) jenkinsae AZE tenrec site Nosy Volo Landscape Microgale mergulus (Paysage Harmonieux Protégé de la (B. Ramahefasoa, Rivière Nosivolo) pers. comm.) Ranomafana National Park Microgale mergulus Yes Prolemur simus, Centre International de (Parc National Ranomafana) Cheirogaleus sibree, Formation pour la Varecia variegata, Valorisation de la Hapalemur aureus Biodiversité (Centre ValBio), Madagascar National Parks Zombitse-Vohibasia National Park Microgale nasoloi Madagascar National Parks (Parc National Zombitse-Vohibasia)

 Alliance for Zero Extinction (AZE) sites contain % or more of the remaining population of one or more tenrec species listed as Endangered or Critically Endangered (sensu Ricketts et al., ).  Priority lemur site details from Schwitzer et al. (, ).  Lemur species are listed only for priority lemur sites.

research projects conducted in collaboration with local peo- of species distribution and status. Although our knowledge ple could help access traditional knowledge and improve of tenrecs has advanced considerably since , no con- our understanding of tenrec distribution, habitats and servation projects have targeted the Tenrecidae explicitly. threats (especially for larger species). Therefore, in the next  years, there needs to be a Priority areas for research include investigating: () The strategic effort to integrate the forest habitats of key threat- ecology, distribution and abundance of the four-toed mole ened endemic species such as tenrecs into broader conser- tenrec, using appropriate pitfall trapping techniques to vation and sustainable development programmes, and to survey areas close to its known range (e.g. in and around increase the scientific study and monitoring of tenrecs Andringitra National Park). () The distribution of the and other mammals. The conservation priorities we have aquatic tenrec, using live trapping or camera trapping identified need to be translated into fundable projects, fol- and/or scat surveys. Success would be enhanced by engaging lowing consultative planning processes (e.g. Conservation the help of protected area managers and fishing communi- Measures Partnership, ) that involve key stakeholders, ties. () The range of the highland streaked tenrec, to verify such as government agencies, civil society bodies, local com- whether it is threatened under B criteria. () The extent to munities, business and industry, and donors. The existence which tenrec species diversity and abundance are affected by of numerous conservation projects across Madagascar, and forest structure, habitat degradation, fishing bycatch, hunt- the continued interest of international donors and NGOs, ing and climate change. () Methods and protocols required suggests that implementing tenrec projects will be econom- for monitoring tenrecs, including the compilation of suit- ically and practically feasible, especially if linked to higher able guidelines and tools (e.g. identification guides, manuals profile taxa. Ultimately, however, only a more concerted describing trapping methods, collecting DNA samples, etc.). effort by the government of Madagascar and its civil society () Habitat cover trends and land use changes, using open- partners and donors to conserve and sustainably manage source satellite-based remote sensing data. the country’s remaining forests will ensure the continued The study of Tenrecidae systematics, including tax- survival of endemic tenrec species. onomy, needs to be continued to identify cryptic species and clarify species limits and diversity. Two newly deli- Acknowledgements We thank Natalia Ocampo (ETH Zürich) for compiling Fig. 1. neated but unnamed species of Oryzorictes need to be described, which will involve confirming the identities of Author contributions IUCN Red List assessments in 2015–2016: several holotypes (Everson et al., ). The likely presence PJS, VS and SMG; data contribution: MEN, VA, KME, MH, PDJ, of a cryptic species in the genus Geogale also requires LEO, MR, FR, DR, VR and NR; review of assessments: AT; first investigation (Poux et al., ; Everson et al., ). draft: PJS, with subsequent input from all co-authors. PJS, VS, SMG, MEN, KME, MH, PDJ, LEO, MR and AT are current members of Research data need to be made available to decision the IUCN SSC Afrotheria Specialist Group. makers in governmental and non-governmental agencies to inform and influence policy, especially relating to pro- Conflicts of interest None. tected area management and the control of hunting and mining. The presence of long-term research teams in pro- Ethical standards This review complies with the journal’s Code of tected areas may also help deter illegal hunting and logging Conduct for authors contributing articles. (Schwitzer et al., ). References

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