Madagascar Forest Conservation Programme

Nosy Be, Madagascar

Ryan M. Clark

October 2018 - December 2018

Field Staff

Staff Member RoleRyan M. Clark (RC) Principal Investigator (PI)

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Contents

1 Introduction 31.1 Madagascar . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3

1.1.1 Geologic Origins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31.1.2 Modern Biogeography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4

1.2 Measuring Biodiversity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4

2 Study Area 42.1 ’Big Island’ . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4

2.1.1 Sambirano . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 52.2 Survey Routes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5

3 Research Program 63.1 Lemur Abundance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6

3.1.1 Lemurs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63.1.2 Lemurs on Nosy Be . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63.1.3 Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63.1.4 Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63.1.5 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7

3.2 Herpetofauna abundance and species richness . . . . . . . . . . . . . . . . . . . . . . . . . 83.2.1 Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83.2.2 Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83.2.3 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10

4 Summary 11

5 Future Work 11

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1 Introduction

1.1 Madagascar

”Continental Island of the first rank”—Island Life 1892. Most animals and plants on Madagascar arefound nowhere else on earth (Goodman and Benstead 2005; World Regional Geography 2008; “Taxonomyand Ecology of African Plants: Their Conservation and Sustainable Use” 2006). The island’s uniquespecies are nested in ancient clades that host endemism up to the family level (e.g. Callmander et al.2011). This has led some to claim that higher taxa distinctness leaves Madagascar peerless in globalbiological uniqueness (Ganzhorn, Wilme, and Mercier 2014).Modern estimates hold that over 90% of Madagascar’s endemic animals live in, or rely on forests (“Thenatural history of Madagascar” 2003). Although our understanding of the historic relationship betweenMadagascar’s human population and the island’s forests is mired in conflicting interpretations and in-nuendo (Kline 2002), humans have undoubtedly shaped significant aspects of Madagascar’s modernvegetative cover (Madagascar: A Short History 2009). Factors that threaten Madagascar’s remainingwoodlands include: international resource extraction, soil erosion of gallery forests, and uncontrolledfires that can spread from traditional swidden agriculture, widely practised across the island (Clark2012; Gade 1996; Marcus 2001; “Conservation and environmental management in Madagascar” 2014a;“Conservation and environmental management in Madagascar” 2014b). Forest clearance for agricultureusing methods such as ’tavy’ (slash and burn) and oxen grazing are central to Malagasy culture, widelypractised, and thought to reduce biodiversity (Clark 2012; Gade 1996; Marcus 2001). The tavy systemconsists of primary or secondary forests being cut and burnt for either cropland rice and root crops to becultivated, it is Eastern Madagascar’s predominant land use practise and is the major cause for uplanddeforestation in the region (Styger et al. 2007).The above factors, exacerbated by stochastic socioeconomic climes across Madagascar have largely con-tributed to the island being classified as a biodiversity ’hotspot’ (Myers et al. 2000) and being considereda global conservation priority (Goodman and Benstead 2005; Mittermeier et al. 2005). Continuing alter-ations to Madagascar’s forests are changing the biology and nature of ecological interactions across hugeareas of habitat, and growing evidence has highlighted the impacts that this change has had on some ofthe island’s most enigmatic and precious species.

1.1.1 Geologic Origins

Much of Madagascar’s extraordinary biological distinctness is thought to have arisen due to its isolationfrom other landmasses, which has lasted at least 90 million years (Storey et al. 1995). Compoundedby the Cretaceous–Tertiary extinction event (K–T) ∼ 65 million years ago (mya) (Alvarez et al. 1980),geographic isolation has allowed Madagascar’s taxa to radiate into previously impoverished niche space(Ali and Krause 2011; Life: A Natural History of the First Four Billion Years of Life on Earth 1999;Renne et al. 2013).Throughout the latter half of the 20th century, the role of dispersal in the post-Mesozoic faunal colonisa-tion of Madagascar was largely ignored in favour of a vicariance dominated narrative (Yoder and Nowak2006). The first years of the 21st century have seen this status quo reversed; current thinking is thatmost of Madagascar’s basal fauna stocks originated from Cenozoic colonisation events from 65 millionyears ago onwards (Salmonds et al. 2012; Salmonds et al. 2013). Fossil records buttress this model byrevealing that most extant Malagasy vertebrate taxa were not present during the Cretaceous (Krause etal. 1997; Krause et al. 1998; Krause et al. 1999) hence their arrival must have been later. However, someclades are known to have survived from Madagascar’s shared plate tectonic history with Gondwanaland(Gaffney and Forster 2003; Noonan and Chippendale 2006).Stochastic dispersal post-K–T has given rise to peculiar taxonomic assemblages on Madagascar (e.g.Poux et al. 2005; Reinthal and Stiassny 1991), where a handful of speciose radiations make up most ofthe fauna (Bossuyt and Milinkovitch 2001; Nagy et al. 2003; Vences 2004) and entire animal groups, suchas large mammals, are absent. However, human driven extinctions of certain taxa during the Holocenemay compound our ability to assess ’natural’ patterns of Madagascan biodiversity (Crowley 2010). Nev-ertheless, modern biological communities on Madagascar are widely thought to be unique in structureand composition (Ganzhorn, Wilme, and Mercier 2014; Horvath et al. 2008; Reddy et al. 2012; Salmondset al. 2012; Salmonds et al. 2013).

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1.1.2 Modern Biogeography

Often cited as a pseudo-continent (Wit 2003), Madagascar is the world’s fourth largest island (587, 000km2),lying ∼ 400km east of mainland Africa in the Indian Ocean. Madagascar’s topography is dominated byan eastern massif running north-south, dividing the island into two slopes: a steep eastern escarpmentand a gentler western slope (27% and 73% of land cover respectively: Ganzhorn, Wilme, and Mercier2014). This topography determines large aspects of moisture deposition across Madagascar. Humidprevailing winds rolling in off the Indian Ocean are forced upward by eastern mountains and unload pre-cipitation on the east coast and central highlands; western Madagascar is left in a seasonal rain shadowand experiences pseudo-monsoon conditions (“The Natural History of Madagascar” 2003). What resultsis a fine-grain diversity of microclimes: discrete abiotic pockets of different weather conditions (Dewarand Richard 2007; Rakoto-Joseph et al. 2009). These heterogeneous moisture patterns shape much ofMadagascar’s local landscape diversity. Although ∼ 65% of the island’s land cover is savannah (Atlas ofthe Vegetation of Madagascar 2007), habitat mosaics of scrub, wetland, and forests typify most regions(Mayaux, Bartholome, and Fritz 2004). The centrepieces of these landscapes are scattered woodlandblocks; forest archipelagos that support most of Madagascar’s species (“The natural history of Mada-gascar” 2003).The unique structure, composition, and history of Madagascar’s biological communities leaves them asexquisite examples of radiation in isolation (Glaw and Vences 2007; Herrera 2017), and bolster calls forconservation of these ecosystems.

1.2 Measuring Biodiversity

More biodiverse communities are considered to be ecologically healthier; generally having greater stabil-ity, productivity, and resistance to disturbance (Purvis and Hector 2000). Thus, measuring biodiversitycan provide insights into the condition of biological communities, track changes over space and time,and inform practical management and conservation (Estimating animal abundance by distance samplingtechniques 1999; “Encyclopedia of Biodiversity” 2013).Estimating biodiversity provides a snapshot in biological time but regular and consistent repeat measurescan provide a window onto the trends and trajectories of species in an area with reference to externalfactors, such as human driven reordering of biological communities (Magurran and Baillie 2010). Ergo,at the beginning of this, our project’s new five-year research plan, we build surveys around a frameworkof measuring the abundance and proportions of various taxa in our research area over time; variousestimates that denote richness and evenness will be made at least once per dry and wet season forcore animal clades (lemurs, reptiles and amphibians). In exploring finer-grained aspects of ecologicaldynamics we hope to expand our repertoire of surveys to include habitat descriptions, more completeinventories of terrestrial invertebrates, and ecomorphological investigations of certain reptiles. Further,we aim to measure different aspects of human disturbance in our study area and to pair this data withthat of our ecological investigations. It is hoped that elucidating these relationships, and others, willnot only develop a more complete understanding of these ecosystems but also spread awareness of theseforests and support future conservation management in the area if required.

2 Study Area

2.1 ’Big Island’

The Madagascar Frontier project (MGF) is currently located on Nosy Be, Madagascar’s largest offshoreisland (25,000 ha), Nosy Be lies ∼ 8km from the mainland and is itself part of an offshore archipelagoof several islands and many more small islets (figure 1).

Within Madagascar, Nosy Be is a relatively developed area. The island’s thriving tourist industryhas fuelled the development of several large holiday resort areas that provide a large proportion of theislands 75,000 inhabitants a sustainable income. Ecotourism on Nosy Be takes the form of guided toursof the island’s forests or seas; these are very popular as Nosy Be has a large area of pristine woodlandand has several coral reefs in its coastal waters.The MGF study area is located at the southeast tip of Nosy Be, on a peninsula bordered by LokobeNational Park. The small adjacent village of Ambalahonko has a population of ∼ 100 people that arelargely a subsistence community. No road access exists for this area; hence, small local boats are theonly method of reaching our study area.

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Figure 1: Map showing Nosy Be, its surrounding islands, and MGF’s camp

2.1.1 Sambirano

Named after a mainland watershed, the Sambirano region is a semi-distinct biogeographic domain ofwhich Nosy Be occupies the northern extreme locality. This region is a transitional zone between thedry deciduous forests of western Madagascar and the humid eastern rainforests. As such, characteristicsof both habitats are found on Nosy Be. This transitional arrangement defines much of the ecology inour research area.

2.2 Survey Routes

MGF has 13 terrestrial survey routes that run through forests in our research area. Each route is 400min length and present on pre-existing forest trails, many are used extensively by local populations toaccess the forest or other human populations. Routes run as straight as possible, to (a) reduce variationin visual overlap between observers, i.e. over/under-surveying on bends (b) simplify routes to flatten thelearning curve for new researchers attempting to memorise the complex network of forest trails in ourstudy area. Routes run along a gradient of human disturbance where many see a significant and regularamount of footfall, yet on others, people are rarely, if ever, encountered. We measure the human use ofroutes to pair with data from ecological surveying.Routes are predominantly used to maintain long-term biodiversity monitoring projects on herptiles andlemuriforms.

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3 Research Program

3.1 Lemur Abundance

3.1.1 Lemurs

Lemuriforms are old world prosimians endemic to Madagascar, and perhaps the most famous of theisland’s fauna. Placing their date of divergence from the other primates is still the subject of robustscientific debate; some studies argue this is around 60 million years ago (Yoder and Nowak 2006; Horvathet al. 2008), while others have suggested dates tens of millions of years later (Godinot 2006; Primate Ecol-ogy and Social Structure 2003). Nevertheless, most authors on the subject agree that this date was afterMadagascar split from India. Hence, lemurs are thought to have colonised the island transoceanicallysometime later, most likely their ancestors being carried over on vegetation rafts (Andriaholinirina et al.2006). Once on mainland Madagascar, lemurs underwent several million years of adaptive innovationand radiated into diverse niche space provided by the island’s unique landscape and climatic conditions(Herrera 2017). Today there are over 130 species of lemur on Madagascar (Wildlife of Madagascar 2016).Modern lemurs are near exclusively arboreal and are commonly found in all layers of the Malagasy canopy(Wildlife of Madagascar 2016). From the world’s smallest primate, the mouse lemur, to the largest ex-tant lemur, the Indri, these animals occupy a broad range of ecological roles within their respectivehabitats (Herrera 2017). While lemurs are generally predominantly frugivours, some species commonlyfeed on leaves, nectar, and opportunistically predate smaller animals such as small lizards (Mammals ofMadagascar: A Complete Guide 2007).

3.1.2 Lemurs on Nosy Be

Three lemur species are found on Nosy be: the black lemur (Eulemur macaco macaco), Hawk’s sportivelemur (Lepilemur tymerlachsonorum), and Clair’s mouse lemur (Microcebus mamiratra). These specieshave different niches and life histories and may use their habitat in different ways. For instance, bothL. tymerlachsonorum and M. mamiratra are nocturnal and are found in relatively small groups (oftensolitary) (Harcourt and Thornback 1990; Seiler, Holderied, and Schwitzer 2015); this is not true fordiurnal, group-living E. macaco macaco (Wildlife of Madagascar 2016). Thus, impacts from externalstimuli such as human disturbance or environmental catastrophe may be different among these species.We aim to address this question.

Aims

• Determine if lemuriform abundance varies in our research area as a function of habitat type.

• Determine if lemuriform abundance varies in our research area as a function of human disturbance.

3.1.3 Methods

During phase 184 (October-December 2018) lemur surveys were walked along nine pre-existing 400 mroutes that run through our study area. Teams of trained research staff walked these routes at a regularpace (roughly 500 m/per hour) and visually scanned the path and surrounding area for lemurs. Observersleft at least 2 m between each other. When an individual was spotted the survey leader—a member ofresearch staff—identified the species and confirmed the group size and measurements. A tape measurewas used to measure the distance from path. Height of individuals was estimated by eye as most lemurswere well above a height that could be recorded using a tape measure. Both day and night surveyswere conducted, starting at 0800 hours and 1900 hours respectively; electric light was used to assistobservations during night routes. As estimates are given, the height and distances, accuracy may bereduced, however, as a trained member of staff is present on all surveys, it is assumed precision will bemaintained. Data was then analysed using R studio.

3.1.4 Results

During Phase 184 MGF performed 21 lemur transects (nine diurnal and 12 nocturnal) over approximately15 hours of surveying; six on degraded forest routes, 12 on secondary, and three on primary. Thissurveying identified 89 lemurs; 48 sportive, 39 black, and two mouse lemurs. Most lemurs were seen onsecondary routes (57 individuals), 20 individuals were seen on degraded routes and 12 on primary routes.Non-parametric Mann-Whitney U testing revealed that sportive lemurs were found significantly morefrequently on secondary and degraded routes than on primary (P < 0.05). Similar testing indicated that

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black lemurs were found significantly less often on degraded routes than secondary or primary routes(P < 0.001) (figure 2.), in fact, no black lemurs were seen on degraded routes during phase 184.

Figure 2: Barplot showing the gross number of lemurs found in different forest types duringphase 184. D = Degraded; S = Secondary; P = Primary

3.1.5 Discussion

Based on significant results of non-parametric that are commensurate with the results of previous phases,our data tentatively suggest that sportive lemurs are generally found more frequently on degraded andsecondary forest routes than on primary routes. Further, owing to similar testing our research indi-cates that black lemurs are found significantly more often on primary forest routes than secondary ordegraded routes. Similar results have been found in the Sahamalaza peninsula for both black (Eulemurmacaco flavifrons; Schwitzer et al. 2007) and sportive (Lepilemur sahamalazensis; Seiiler, Holderied, andSchwitzer 2014) lemur species. This supports the idea that sportive lemurs are resilient to human distur-bance and habitat degradation, and that black lemurs prefer forest habitat with higher, denser canopies.These conclusions, if further confirmed, could be important to future conservation of these charismaticspecies adjacent to Lokobe national park. However, as data taken on black lemurs was dominated bytwo large groups (13 and 18 individuals) found on secondary forest routes, conclusions on this speciesmay be heavily biased and unreliable to describe aspects of black lemur ecology. This data should beadded to the data from previous and future phases to confirm any potential correlations.

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3.2 Herpetofauna abundance and species richness

Reptiles and amphibians are by far the most diverse groups of vertebrates on Madagascar (Glaw andVences 2007). These hold such enigmatic clades as the leaf-nosed snakes and several chameleons—one ofa handful of taxa thought to have dispersed across continents from a Madagascan epicentre. Shaped byMadagascar’s geographic isolation and unique ecological pressures, herpetofauna on the island has takenon a unique form, full of peculiarities not found anywhere else on earth with 100% of amphibians and92% of terrestrial retiles endemic to the island (Glaw and Vences 2007).All wild amphibians on Madagascar are frogs. These species are near exclusively restricted to woodlandhabitat, not being able to withstand long periods in direct sunlight and needing humid conditions andaccess to water bodies for reproduction. As such, amphibian diversity is heavily concentrated in theisland’s eastern rainforests (Glaw and Vences 2007). The heterogeneity of these habitats has helpedcatalyse microendemism of frogs along Madagascar’s eastern coast. These amphibians fill broad nicheranges in their respective habitats, from leaf litter dwelling Stumpfia, to Boophids capable of boundingbetween high tree tops, Madagascar’s frogs can be very locally abundant and occupy many key positionsin their trophic webs (Glaw and Vences 2007).Reptiles on Madagascar are generally less restricted to the island’s forests, their scaled dermis allowsthem to thrive in areas of intense ultraviolet exposure and to store water so as to go much longer betweenhydrating. Therefore, Madagascar’s reptiles can occupy areas of scrub and savannah—the most commonhabitat type on the island. These reptiles include a number of charismatic and well-known species, suchas the chameleons; Madagascar holds ∼ 50% of the globes chameleon species (Glaw and Vences 2007).Most reptiles and amphibians on Madagascar are found nowhere else on earth (Glaw and Vences 2007).Owing predominantly to a unique pattern of stochastic transoceanic dispersal to the island after bi-ological impoverishment ∼ 65 million years ago (Ali and Krause 2011; Alvarez et al. 1980), peculiarassemblages have taken hold; for instance, Madagascar is the global hub for chameleon species diversity,yet hosts no salamander species (Glaw and Vences 2007). These disharmonic biological communitiescame about due to a few speciose taxa radiating into unoccupied niche space on Madagascar—they nowtypify the ecology of the island (Goodman and Benstead 2005; Poux et al. 2005; Salmonds et al. 2013).Investigating the ecology of these strange communities can provide unique lenses onto evolutionary biol-ogy, consequences of environmental change, and practical conservation potential.

Aims

• Determine if herpetile abundance and species diversity varies in our research area as a function ofhabitat type

• Determine if herpetile abundance and species diversity varies in our research area as a function ofhuman disturbance level

3.2.1 Methods

During phase 184 herpetofauna surveys were walked along thirteen pre-existing 400 m routes that runthrough our study area. Teams of trained research staff walked these routes at a regular pace and visuallyscanned the path and surrounding area for reptiles and amphibians. Observers left at least 2 m betweeneach other. When an individual was spotted the survey leader—a member of research staff—identifiedthe species and confirmed the group size and measurements. A tape measure was used to measurethe distance from path and height above ground, if individuals were too high the height above groundwas estimated by eye. Both day and night surveys were conducted; electric light was used to assistobservations during night routes.

3.2.2 Results

During Phase 184, 42 herpetofauna surveys (24 diurnal and 18 nocturnal) were walked over approximately46 hours of surveying; eight were walked on degraded forest survey routes, 24 on secondary, and 10 onprimary routes. Zonosaurus rufipes was the most frequently encountered species (37% of all encounters).In total, 34 different species were seen during this phase, including some rare frogs that have emergedduring the transition into southern hemisphere wet season such as Gephromantis horridus.Non-parametric Mann-Whitney U testing confirmed that species richness of herpetiles was significantlyhigher on primary routes compared to secondary and degraded routes (P < 0.05) (figure 3). The total

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number of individuals was also significantly higher on primary routes than degraded (P < 0.01), but notthan that of secondary routes (P = 0.34) (figure 4).

Figure 3: Barplot showing the average species richness of herptiles found in different foresttypes during phase 184. D = Degraded; S = Secondary; P = Primary.

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Figure 4: Barplot showing the gross number of herptiles found in different forest types duringphase 184. D = Degraded; S = Secondary; P = Primary.

3.2.3 Discussion

In line with previous 2018 reports, findings for 184 support our growing body of evidence that primaryforest routes support a greater species richness of herptiles than secondary or primary routes. Whiletesting on abundance differentials on secondary and primary routes was non-significant, testing primaryvs degraded routes produced a clear result: primary routes support a greater abundance of herptilesthan degraded. Similar patterns have been found in many other herptile assemblages both worldwide(Gibbon2000) and throughout Madagascar (Glaw and Vences 2007).This asymmetry in ecology could be due to several factors. Firstly, there are distinct structural differencesbetween our primary and degraded sites. Generally, our primary forest has a higher, denser canopy; theshrub layer is also likely thicker. Water ways are more prominent in the humid, hilly forests aroundour primary research area, with rivers and small streams frequently crossing our survey routes and inconstant change as the level of precipitation varies from season to season. These differences in habitatstructure, particularly the abundance of waterways to amphibian species, is likely to play a large part inthe greater species richness observed here. Also, the level of human disturbance we suspect is differenton our primary routes. As we frequently use these routes, we can say with some confidence that weencounter people less often on primary routes compared to degraded and secondary routes. Disturbancecan have negative ecological consequences and extirpate certain species from an area. Hence, a lowerlevel of human disturbance on primary route may have generated a more attractive habitat for someherptile populations. Over the coming phases as our point centred quadrant surveying of forest routecontinues, we will be collecting a plethora of habitat structure data and continuing to quantify humandisturbance on our route, with this data we can have a fresh look at our long-term monitoring of herptilepopulations and possibly explain some of the ecological differences that we have observed across ourresearch area.

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4 Summary

Phase 184 saw the ushering in off the rainy season, where precipitation and humidity rose dramaticallyacross our research area and Madagascar as a whole. The difficulties that this environmental changebrings to the practicalities of research, such as increasingly slippery slopes and difficulty in spottingindividual animals, can have negative impacts on our research output. Despite these hindrances ourlong-term biodiversity monitoring of reptiles, amphibians, and lemurs went as planned and we continueto gather valuable data for ongoing analysis. The main findings for this phase were that secondaryforests supported the largest abundance of lemurs, whilst primary forest supported higher diversities ofherpetiles.Invertebrate catalogues played a smaller role in our schedule during this phase as we wanted to focus ongathering habitat data to support not only our long-term data but lemur behaviour and microhabitat-chameleon work from 181, 182, and 183 also. However, we did continue with the surveying of butterfliesand spiders—we continue to build a broader picture of their assemblages throughout our research area.Additionally, we were able to construct three new forest survey routes. These trails have been, so far,very productive and a joy to walk. In the coming phases, data from these routes will be integratedwith our main dataset to improve the reliability of our scientific conclusions. The continued collectionof baseline data allows for long term monitoring of species diversity, the trends of which can be used toinfluence local land use, and hopefully, prevent habitat degradation.

5 Future Work

In phase 191 we have several goals. Firstly, we would like to integrate a new avian project into ourschedule as we now have the expertise on the team to do so. This project aims to analyse bird’s use ofour research area, habitat preferences, and some basic observation of behaviour. Survey’s will include acombination of point counts, to determine species assemblages, and transects, to identify behaviour andhabitat use of specific species. To buttress this, we would like to expand our cataloguing of terrestrialinvertebrates to include beetles—at the height of the wet season is the perfect time to do so.In the coming phases our surveying on human disturbance along our forest survey routes will begin to beanalysed. This data can then be compared to the data on lemur encounters to determine the covariancebetween apparent lemur abundance in different forest types and the quantum of human disturbance onthat route. This comparison will allow us to better describe the impact of human use of the forests inour research area and to further explain the pattern of lemur distribution and habitat use over space andtime.

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