MADAGASCAR FOREST RESEARCH PROJECT

NOSY BE, NORTH WEST MADAGASCAR

MGF 133 SCIENCE REPORT

Phase Dates: 8th

July 2013 to 16th

September 2013

AUTHOR: SAM HYDE ROBERTS (PRINCIPLE INVESTIGATOR)

CO-AUTHOR: KELLY GIMSON

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Contents

1. Introduction....................................................................................................................................3

1.1 The Location of the MGF Project.......................................................................................3

1.2 History of the MGF Project................................................................................................5

1.3 The Study Area...................................................................................................................6

2. Training.........................................................................................................................................11

2.1 Briefing Sessions..............................................................................................................11

2.2 Science Lecture................................................................................................................11

2.3 Field Training...................................................................................................................12

2.4 BTEC Projects..................................................................................................................13

3. Research Programme...................................................................................................................14

3.1 Overview..........................................................................................................................14

3.2 The Impacts of Forest Clearance In Madagascar.............................................................16

3.3 Statistical Analysis...........................................................................................................19

3.4 Reptile & Amphibian Project...........................................................................................20

3.5 The Influence of Human Disturbance on Black Lemur Behaviour..................................54

3.6 Bird Monitoring Project....................................................................................................65

3.7 Small Mammal Surveying................................................................................................72

3.8 Butterfly Surveys..............................................................................................................75

3.9 Pilot Bat Project................................................................................................................79

4. Future of Lokobe Reserve............................................................................................................80

5. Proposed Science Programme for Next Phase...........................................................................82

5.1 Overview and objectives of next phase............................................................................82

6. Community work and public awareness....................................................................................84

7. Acknowledgements.......................................................................................................................84

8. References.....................................................................................................................................84

9 Appendixes.....................................................................................................................................90

9.1 Avian species list..............................................................................................................90

9.2 IUCN conservation status.................................................................................................92

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1. Introduction

1.1 The location of the MGF project – Nosy Be:

The MGF project is currently situated on Madagascar’s largest offshore island, Nosy Be, whose

name translated from Malagasy simply means ‘Big Island’. Situated approximately 8km off the

northwest coast of mainland Madagascar (Fig 1), laying out in the Mozambique channel, Nosy Be

has a total surface area of around 25,000 ha. The project itself is based on the outskirts of a small

village named Ambalahonko in the southeast of Nosy Be, (Fig 1) and is positioned within the buffer

zone of Lokobe Special Forest Reserve. Ambalahonko currently has a population of around 60

people, with access to the village being attained only by boat.

Figure 1 – Images showing the location of Nosy Be (a) in relation to mainland Madagascar (b) and

the position of MGF within the village of Ambalahonko (c) next to Lokobe Integral Reserve.

The island falls within the Sambirano bio-geographic domain, with its natural vegetation sharing

characteristics of a mix of both the Eastern rainforests and Western dry deciduous forests. The

region receives significantly less rainfall annually than the Eastern rainforests (2,000-3,000mm) but

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substantially more than the forests in the West (500-2,000mm), making the Sambirano domain

(>2,000mm) a unique forest ecotone. Figure 2 displays the scale and location of the Sambirano

domain in relation to other broad habitat zones in Madagascar.

Acting as a transitional region between the Eastern rain forests and Western dry forests the

Sambirano region is classified as a seasonal moist forest with a sub-humid climate. Its dry

deciduous forests are characterised by high levels of species diversity and endemism and the

Lokobe reserve on Nosy Be, adjacent to the MGF camp, is now one of the last remaining fragments

of untouched Sambirano forest to be found. Although Nosy Be is itself an island, it has a high level

of biodiversity typical of the Sambirano domain, not surprisingly for as recently as 8,000 years ago

Nosy Be and its surrounding islands were all connected to the mainland, with sea level being

substantially lower than it is presently. At this time the Sambirano forests formed part of a

continuous unbroken belt running from north to south Madagascar; however it now only demarcates

the northern end of the islands central mountain range. The reserve is classified as a lowland forest

reserve, with its highest peak just 432m above sea level.

Lokobe is currently the only protected area on Nosy Be and is designated a strict terrestrial nature

reserve (Special Integral Reserve), allowing entry only to staff and researchers with appropriate

permits. The park first attained its protected status in 1966; however it has been unofficially

protected since 1927. The Lokobe Strict Integral Reserve is small, at only 740Ha, and the

surrounding narrow belt of forest encircling it is safeguarded to an extent as a Madagascar National

Park (MNP). The Lokobe MNP acts as a buffer to the main reserve providing protection to the

wildlife and providing resources for the local communities. The MNP was implemented in 2010

with the intention of increasing development in the area for tourism, with potentially large benefits

for local tour operators, registered guides and the MNP itself. However it remains a controversial

decision as the parks small size (740Ha) already makes it vulnerable and increased human

disturbance may have a negative impact upon the wildlife and forest. Control of the MNP forests is

the responsibility of the community conservation council or Community Local Base (CLB), a group

under the authority of the Ministry of Environment and Forest, but whose members consist also of

local community representatives. In recent years however, a severe lack of funding has resulted in

the absence of enforcement officers within the community and forests and has led to uncontrolled

deforestation and exploitation of valuable hardwoods. One positive feature of the current

establishment however is its intention to extend the boundaries of the MNP into the local marine

zone, and provide much needed relief to the marine ecosystems in the area from over-fishing. How

well the reserve, as a whole, is regulated in the future will be key to its long-term survival, as both a

refuge for its diverse flora and fauna and as an important economic resource for the local

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communities. This brings the potential for Frontier to offer technical support to the CLB via

training, resource assessment and ecotourism.

Outside of Lokobe, Nosy Be is almost entirely deforested. The remaining land area is divided

between pastures and crops to the west and dense scrub and taller crop types such as ylang-ylang

and banana to the east. Within the past several decades the sugar industry on the island has rapidly

declined, and the majority of land has reverted back to being used for various forms of subsistence

and commercial agriculture. Some land has instead been bought up, converted and developed for

hotels and tourism, a trade that developed on Nosy Be significantly before its rise on mainland

Madagascar. An official population estimate conducted in 2001 put the number of inhabitants on

Nosy Be at 36,363.

1.2 History of Frontier Madagascar Forest Project

The Madagascar Forest Project (MGF) first combined with the Madagascar Marine Project (MGM)

in the South East of Nosy Be in 2011, during the inter-phase period 111. The combined project is

now situated on the outskirts of the village Ambalahonko, approximately 60 minutes by boat from

Nosy Be's capital, Hell-Ville, where all Frontiers re-supply takes place. There is no road access to

the project and any overland transport therefore is unfeasible, restricting the level of access to the

village. Ambalahonko literally translates from Malagasy as 'Fence of Mangroves', a name which

accurately reflects the setting well.

Ambalahonko has a population of approximately 60 people. The camp and village are surrounded

by an enclosed bay, through which access to the mainland is possible through one of two openings

in the mangrove fence. To the West of MGF is degraded secondary forest (MNP) backing on to the

Lokobe Reserve and to the North lies a mosaic of dense scrub, agricultural land and fruit trees.

Prior to its re-location to Nosy Be in 2011, MGF had worked at four field sites in Northern

Madagascar since its initial move there from Tulear in March 2005. The first of these sites was

located in Montagne de Français, an area approximately 8km to the east of Antsiranana (formerly

known as Diego-Suarez). Subsequent to MGF’s research there, the area has been promoted into a

temporary reserve, with the management of the region still under discussion between the local

communities and governing agencies. It is highly likely that the area will now become an important

national park, as a substantial amount of money has been invested into the area.

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The forest research project then moved to the northern side of the Bay of Antsiranana, adjacent to

the village of Ampombofofo, where the close proximity to the coast and the sandstone geology

created a unique habitat matrix of primary, semi-humid dry deciduous forest fringed by primary

coastal forest. At the beginning of 2008 however, the project moved south of Antsiranana, near the

small village of Tsarakibany. The purpose was to assess whether the remaining forest fragments in

the area act as corridors and refuges for wildlife between two existing protected areas (Montagne

D’Ambre National Park and Ankarana Special Reserve). MGF remained in this area for 3 years and

in 2011 moved to Ambalahonko, Nosy Be where it currently presides, adjacent to the Lokobe

Integral reserve.

1.3 Study Area

The studies undertaken in this report were conducted at sites around the village of Ambalahonko,

amidst the Lokobe buffer zone and out towards the boundary of Lokobe Strict Nature Reserve

(Réserve Naturelle Integral de Lokobe). The reserve is surrounded by forest under the supervision

of the Ministére des Environment et Forets (MEF). This forest not only enhances the level of

protection to the forest reserve but also allows us to conduct our research across a gradient of

human disturbance, completely outside of the reserve, minimizing our footprint on the forests.

Within the buffer zone, the forests integrity ranges from pristine forest, through both recovering and

exploited forest, to completely modified habitats.

For our study the research sites were selected along a gradient of human disturbance, based on the

time since they were last cleared and their previous usage. The sites range from primary forest sites

that have never experienced clearing, to those that are cleared annually for agricultural purposes.

Details for each of sites used in our surveys are shown in Table 2. All of the research sites are

located within close proximity to the village of Ambalahonko (Figure 3) and are accessible via the

beach except at times when the tide is high. The sites are situated roughly in a sequence where the

primary survey sites are the furthest away heading west towards Lokobe, whilst the most disturbed

sites are those nearest Ambalahonko. A distance of about a mile and a half separates all of the

survey sites. To account for the effect of human disturbance and habitat degradation on vertebrate

communities, sites were selected carefully and chosen for their contrasting histories.

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Table 2 – An overview of each of the 7 survey sites used this during phase plus the three new

proposed sites (8,9 and 10), describing their exact locations, the time since they were last cleared

and their present usages. * Tavy is the local term for slash and burn land clearing.

Survey Site Overview: Table 2.

Site

#

GPS Location Time Since Last

Cleared:

Habitat Usage:

South East

1 13 24' 48'' 48 20' 2'' Never Cleared Primary Riparian Forest.

2 13 24' 43'' 48 20' 6'' Never Cleared Primary Mature Forest.

3 13 24' 26'' 48 20' 18'' ~ 30 years Secondary re-growth forest

previously used for timber

extraction. Has recently

undergone some minor

clearance.

4 13 24' 14'' 48 20' 32'' ~ 18 years.

Major clearing

within the past 3

months.

Secondary re-growth Forest, a

matrix of mature trees and

secondary growth. Vanilla

plantation to one side.

Previously used for timber

extraction. Has undergone

significant clearing this phase.

5 13 24' 0'' 48 20' 36'' 0 years Ylang-ylang, vanilla & Banana

Plantation. Secondary forest

fragment to one side and rice

paddy on the other. Cleared

annually by means of slash and

burn.

6 13 24' 10'' 48 20' 46'' 0 years Pineapple & Banana

Plantation. Harvested annually.

Situated on a small hill, with

clay-like substrate.

7 13 24' 22'' 48 20' 49'' Historically thinned

out.

Mangrove site. Beach

separates mangrove cluster

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from secondary forest with

enclosed small rice paddy.

8 13 24’ 28’’ 48 21’ 6’’ A few years. A hilltop site ideal for bird

surveying. Overlooks

secondary forest but is

primarily scrubland.

9 13 23' 72'' 48 20' 48'' Historically A mosaic of primary and

secondary forest, bordered by

small-scale vanilla plantations.

A large and relatively

undisturbed site.

10 13 24’ 15’’ 48 21’ 10’’ Within 3 months. Regularly cleared secondary

forest patch near the village of

Atafondro. Well connected but

regularly undergoes small-

scale logging and is often

disturbed by humans. *Tavy

site.

Over the course of the phase a further 3 study sites have been added to our project, with another

primary habitat and additional secondary and degraded sites. Although these new sites have been

surveyed lightly over the course of the phase, they have not been sampled enough to include in the

phase's scientific analysis unless stated, due to an unequal number of repeats. The new sites will be

necessary during the beginning of the next phase where we expect large numbers of research

assistants, and the extra sites will help keep our own disturbance to a minimum and allow sites to be

sampled infrequently enough to allow adequate recovery between surveys. The new sites are shown

as blue dots on Figure 3 although they have not yet been fully incorporated into our research, whilst

the per-existing sites are indicated by red dots.

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Figure 3 – A map showing the location of all previous 7 survey sites (red dots) in relation to MGF

and Lokobe Special Reserve and the three additional survey sites (blue dots). Image taken from

Google Earth.

For comparison we selected one site that is a pristine gallery forest situated on the very border of

Lokobe Integral Reserve (Site 1) and another that has not been cleared within local community

memory (Site 2) and as far as we can determine is primary. For secondary sites we selected two

areas that have had significant time pass since they were last cleared substantially, although minor

disturbance does still occur at both locations occasionally. Both sites still show clear signs of their

pasts and now comprise of a mixture of mature trees, secondary re-growth and agricultural pest

plants and trees. Sites 5 and 6 were selected to observe the effects of agricultural clearing and the

impact of losing mature forest on vertebrate communities. Both sites are active plantations, site 5

being primarily a banana and ylang-ylang growth whereas site 6 is a pineapple and banana grove.

Site 7, used only for bird monitoring is a mangrove site, comprising of a band of mangrove trees, a

beach and secondary forest. It should be noted that there is a rice paddy relatively nearby. An

overview of the sites is given in Table 2 and a map showing their distribution in relation to the

MGF camp is depicted in Figure 2. Plate 1 shows photographs of each of the 7 sites and gives an

indication of the habitat type.

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Plate 1 – A series of photographs showing the characteristic habitats at each of the 7 survey sites.

Top Left = Site 1, Left Middle = Site 2, Bottom Left = Site 3, Bottom Right = Site 4, Top Right =

Site 5, Bottom Middle = Site 6 and Top Middle = Site 7.

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2. Training

2.1 Briefing Sessions

Introductory briefings were given on site during the first two days of phase (Table 1), whilst further

science presentations, revision exercises and tests were conducted at various stages throughout the

10-week phase.

Table 1. Lectures given at deployment briefing day

Lecture Presented by

Introduction to Madagascar and Nosy Be Sam Hyde Roberts (SHR)

Introduction to MGF Projects Sam Hyde Roberts (SHR)

Health & Safety and Medical Tests

Flavia Diotallevi (FD), Natascha

Neuiwenhuis (NN) and Emily White

(EW)

2.2 Science Lectures

1. Project briefing (Regularly updated)

2. Natural and Human History of Madagascar (Recently updated)

3. Introduction to reptiles and identification practical (Recently updated) – Includes ID training on

all families present on Nosy Be, with natural history presentation, frog call ID and regular tests.

4. Introduction to birds and practical tests – Includes ID, natural history presentation and regular

call tests.

5. Introduction to mammals – Includes natural history and identification aspects.

6. Principles of Biodiversity.

7. Biodiversity Conservation.

8. Conservation strategy – Infrequently given.

9. Survey and monitoring techniques – Specific for each project.

* These presentations, training sessions and tests are given by any of the staff team.

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2.3 Field Training

Field training was given in the early stages of the phase and then repeated several times throughout

at appropriate intervals (every 2 weeks) to maintain high levels of competency in terms of species

identification and data recording. Initial training consisted of a series of group sessions, each

focusing on a specific topic, where Research Assistants (RA’s) were shown how to identify and

equally as important, how to avoid misidentifying certain species and families as well as how to

record a range of data to a level that can later be analysed.

Training sessions included:

Amphibian Identification - How to identify and differentiate between similar species in the field as

well as handling techniques. Particularly focused on the Gephyromantis, Stumpffi and Boophis

families that are perhaps the most challenging from an identification perspective.

Bird Identification – Emphasis on main diagnostic features, flight patterns and descriptive

terminology.

Bird Calls and Song Recognition - Repeated sessions and quizzes on call and song recognition

using recordings from a CD.

Butterfly Surveying Techniques – The correct procedure for collecting butterflies was demonstrated

and assessed. Identification was taught and the finer points of butterfly ecology were discussed

during each survey. Careful manipulating of specimens was shown but not instructed.

Reptile Identification - How to identify and differentiate between species in the field. The

appropriate handling techniques used for chameleons and snakes and the health and safety issues

associated. Demonstrations were given on how to record and accurately collect useful information

such as lengths, weight, gender, damage, height in canopy etc.

Observing Mammals - The appropriate behaviour during mammal surveying was explained, along

with useful surveying techniques. Instruction on how to record consistent and useful behavioural

data was given, along with the correct procedure for collecting samples.

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Environmental Data Collection - How to accurately collect environmental data such as rainfall,

humidity temperature and salinity (soil + water).

Repeat sessions were conducted regularly to both reinforce the knowledge learnt with regards to

accurate species identification and to ensure good, consistent data collection was maintained.

During the sessions, several different formats were introduced, such as quizzes tests and games.

2.4 BTEC’s

MGF 10-Week Diploma in Tropical Habitat Conservation:

Elijah Denham – An Assessment of Habitat preference and the impact that Habitat Degradation has

upon the Pygmy Leaf Chameleon, Brookesia stumpffi. Mentor – Sam Hyde Roberts.

Jack Thirkell – Snake Diversity in Association with Habitat Type. Mentor – Sam Hyde Roberts +

Flavia Diotallevi.

MGF 4-Week Certificate in Tropical Habitat Conservation:

Photini Knoyle – Anthropogenic impacts on the amphibian fauna of Nosy Be. Mentor – Sam Hyde

Roberts.

Zoe Turcotte – Social structure of the Hawk Sportive Lemur (Lepilemur tymerlachsonorum).

Mentor Charlotte Daly.

Constance Lynch – Habitat preference and abundance of Hawk Sportive Lemur (Lepilemur

tymerlachsonorum) outside of primary forest. Mentor – Charlotte Daly.

Roberto Correa – Butterfly diversity of the Ambalahonko region. Mentor – Samuel Ferguson.

Tiera Owen – Butterfly diversity of the Ambalahonko region. Mentor – Natascha Neuiwenhuis &

Emily White.

Felicity Allen – The abundance and habitat preference of Phelsuma day Gecko’s within the

Ambalahonko region. Mentor – Flavia Diotallevi.

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3. Research Work Programme

3.1 Overview

During phase MGF 133, we continued to assess the impact that forest clearance, human disturbance

and agricultural development has upon on the diversity of pre-existing vertebrate communities

(amphibians, reptiles and birds). This phase fell in the middle of the austral winter, which generally

falls between the months of May and October, but has become less fixed over recent decades partly

due to the process of global warming. The season appears to have had a substantial effect on many

of the animal groups and has affected them each in different ways. Most notably, many bird species

appear to have returned from their seasonal migrations, whether internal or continental, whilst

several species have gone the other way, and migrated away from Nosy Be. The reptile and

amphibian groups have each responded to the season in their own particular way, depending on the

nature of their ecological needs.

During this phase we continued to investigate the influence of human disturbance and habitat

fragmentation on the behaviour of the Black Lemur (Eulemur macaco macaco), and specifically its

effect on the animals dietary habits. We continued focusing our attention on the seed dispersal

project and have also began mapping out the territories and group compositions of as many troops

as possible in an attempt to establish the population of Black Lemurs in the area. As with the last

phase we have continued with our long-term study, collecting any seeds from either dropped fruit or

in the Lemur scat and have used these to help quantify the dietary effects of living in areas of forest

experiencing varying levels of human disturbance. Once fecal samples are collected the number of

seeds and the diversity of seed species is analysed before they are all planted in our seed nursery for

future sapling identification. Although only a small number of seeds have so far been collected and

planted, permissions were obtained from the Madagascan Ministry of the Environment and Forest.

Activity budgets for the Black Lemur groups undergoing varying levels of human disturbance are

also continually being recorded and run in conjunction with the seed dispersal project. It allows

good opportunity to observe the Lemurs feeding behaviour and for the collection of scat samples.

We propose that the groups of Black Lemur, each with a territory experiencing a different level of

human disturbance, have different dietary habits and are therefore dispersing different combinations

of seed species to an altered extent than they would in a wild ecosystem.

A full years data has now been collected on the diversity and abundance of vertebrate communities

in the Ambalahonko region, encompassing the amphibian, reptile and bird faunas. All data can now

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therefore be analysed and compared to variables such as changing season, weather type and human

disturbance.

In additional to the completion of the main studies, an assessment of the butterfly fauna of the

Lokobe / Ambalahonko region is now complete, with a modern species list for the area compiled.

To compliment this, a photographic library of Moths, Spiders and Mantises is presently being

compiled in an online repository with the aim of identifying the vast majority of species for a future

ID guide. This process will undoubtedly take time as many museums and insect collections will

have to be viewed for accurate identification.

Small mammal surveying has been completed for several sites using Sherman trapping across a

gradient of human disturbance and a nocturnal lemur abundance project is also now finished. The

abundance and distribution of the Hawk Sportive Lemur (Lepilemur tymerlachsonorum), and their

behavioural relationship to the lunar cycle that was began at the beginning of phase 132 is now

completed.

Our recent genetic verification project concerning some of the less common reptiles and amphibians

is currently on hold, as permits remain difficult to attain. However there is a huge potential for work

in this field once the correct permissions are in place. Our group recently discovered a species of

Chameleon, (Furcifer petteri) which has gone undiscovered on Nosy Be for 150 years despite

intense international surveying. Establishing the exact phylogenetic position of several reptiles and

amphibian species in the Lokobe region could give a huge boost to the reserve in terms of

protection and counter-intuitively, eco-tourism. To determine the exact relationships certain species

have with their closest relatives or con-specifics on the mainland, and the genetic distance between

them will hopefully shed light on the selective forces that have been at work over the past 8,000

years.

It may also shed light on the impacts human disturbance is having on different animal populations

on a genetic level. I am currently awaiting the necessary permits from both ANGAP and the MEF in

order to both collect voucher specimens and to have permission to export them to Munich

University for genetic verification.

In addition to our ongoing research being conducted on Nosy Be, a rapid biodiversity assessment of

the nearby island Nosy Komba was undertaken during this phase. The previously un-studied island

was found to hold a wealth of herpetological life and we discovered many species that were

previously thought to be absent. Despite this, the real aim of our research expedition to Nosy

Komba was to uncover the mystery behind the disappearance of the northern Sportive Lemur

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(Lepilemur tymerlachsonorum). Unfortunately although intense and wide-ranging surveys were

conducted, no evidence for their continual existence was discovered. Our questionnaire surveys

only served to shroud the circumstances around the animal’s departure from the island, with many

interesting and varied reports of sightings and tales documented.

3.2 The Impact of Forest Clearance in Madagascar

Today, Madagascar is renowned not only for its high levels of biodiversity and high degree of

endemism, but sadly also for the ongoing loss of its original primary vegetation (Ganzhorn et al,

2001). The rapid and extensive rates at which deforestation has occurred since the relatively recent

colonisation by humans (between 200BC and 500AD), and indeed over the past century, has made

Madagascar one of the worlds foremost biodiversity conservation priorities (Whitehurst et al, 2009).

It has previously been conjectured that historic estimates of deforestation are often inflated and are

likely to suffer from bias (Jarosz, 1993), and that even recent rates of deforestation are controversial

and have often been stymied by lack of high quality data. In Madagascar’s case, the original extent

of forest cover to begin with is also contentious (Quémére et al, 2012). However recent analysis

using satellite and aerial imagery shows that over 40% of the remaining forest cover was lost

between 1950 and 2000 (Harper et al, 2007). When it is considered that an estimated 90% of

species endemic to Madagascar are entirely dependent on forest and woodland habitats, the

situation comes sharply into focus. Brooks et al, (2002) predicted that if current deforestation rates

were to continue unabated, that Madagascar would be amongst the areas that will suffer most

species extinctions in the near future.

In Madagascar currently, forests are managed through a number of governmental and community

actors, with technical support supplied by NGOs. Madagascar national parks (MNP, formerly

ANGAP) are responsible solely for managing the areas that hold the higher protected status.

However, even forests outside of the MNP reserves have been found to hold substantial biodiversity

and provide significant services to human users (Ingram and Dawson, 2005), thus have a

considerable conservation value. An assessment of Madagascar’s forests found there to be 40246

km2 of forests outside reserves (Nicoll, 2003), compared to a total reserve area of approximately

170000km2 (Randrianandianina, et al. 2003). Conservation efforts within these unprotected forest

formations has been low compared to those in the evergreen rainforest of eastern Madagascar, and

due to fragmentation some forests are now critically vulnerable. As a result of their now

discontinuous nature, and the high levels of diversity remaining within these unprotected forest

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fragments, these small-scale ecosystems urgently require reinforced conservation programmes

(Gazhorn et al, 2001).

The Sambirano bio-geographic domain, of which the Lokobe Integral Reserve is a vitally important,

yet threatened example habitat, is located in the north west of Madagascar, around the Sambirano

River and the regional centre town of Ambanja (Fig 2). The forests unique character is due in part

to the regions substrate, sandstone, as opposed to the much more widespread igneous and

metamorphic basement rocks found in the surrounding domains (Du Poy and Moat, 2003). The

region has a short and mild dry season (3-4 months) and receives over >1800mm rain annually

(Wells, 2003). The forests do not extend above 1,000m in altitude anywhere in the biome with the

climax vegetation being lowland rain forest (Goodman & Ganzhorn 2004). The forest has an

average canopy height of around 30m, with some emergent’s (IUCN data). It has been speculated

that the Sambirano is probably the most recent of Madagascar’s biomes, arising as a result of the

onset of the Indian Monsoons approximately 8 mya (Wells, 2003).

Floral surveys of the region have found it to consist of a mixture of Sambirano endemics (14%),

species that are shared with either the western and eastern domains (21% and 16%), and those

which are (49%) widespread throughout Madagascar (Gautier & Goodman 2003). The Sambirano

forests are often considered a composite habitat consisting of elements from both the eastern and

western regions (Nicoll and Rathbun, 1990) but also having its own endemic species. The area is

subject to slash and burn agriculture, charcoal making, selective logging, and the collection of

timber for fuel and cooking. Due to its limited extent, along with the high mountain domain, it is

considered one of the most threatened Madagascan forest habitats (Langrand, 1990).

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Figure 2 - A map showing the distinct habitat domains in Madagascar, showing the unique but

limited range of the Sambirano forests.

Indeed, throughout the world, habitat destruction, primarily for agriculture, has been one of the

greatest drivers of anthropogenic extinction (Diamond, 1989). In the Southern spiny forests, Scott et

al. (2006) found that the composition of small mammal, lizard and bird communities differed in

‘forest’ and ‘cleared’ sites. Overall, species richness was lower in ‘cleared’ areas for all taxa

studied. Impacts were particularly significant within the families of lizards, with a 50% drop in

species richness in ‘cleared’ areas. However, individual species responded differently to the

clearance, with reptiles and forest specialist species being worse affected. In addition to the

reduction of species richness in areas that have been recently deforested, it has been observed that

some species become locally extinct, sometimes after a significant time delay (Kuussaari et al,

2009).

Despite this there is substantial literature on community recovery following forest clearance and

habitat destruction. In a review of plant and bird community recovery, Dunn (2004) found that over

time communities approached their pre-clearance species richness in the overwhelming majority of

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cases. Bowen et al (2007), having reviewed 68 studies of re-growth forests concluded that there was

a general trend for the recovery of species richness over time, but that factors such as the land-use

history were extremely important and must be considered. To date very few studies have assessed

the responses of multiple taxa to habitat degradation, despite the likelihood that different groups of

animals, particularly at family level respond to habitat change at very different rates.

We are not aware of any study that has documented both the effect of habitat destruction and human

disturbance on multiple vertebrate communities and the subsequent recovery of these populations

over time in Madagascar, or specifically in the Sambirano domain. The first of our studies presented

here examines the effect that habitat degradation and the influence of human disturbance have on

the reptile and amphibian communities within Sambirano forests. We compare species diversity

recorded across six sites for an entire calendar year, with each location situated along a gradient of

human disturbance, encompassing primary, secondary and cultivated habitat types.

3.3 - Statistical Analysis

All statistical analysis conducted in this report was conducted using the IBM software package

SPSS version 20 and on occasion Microsoft Excel. All statistical analysis was undertaken

independently by two separate individuals and compared to ensure no errors were made.

Comparisons of diversity and abundance were completed using the One-Way ANOVA tool and

accompanied by Post hoc Turkey HSD tests for increased power and analytical clarity. Factorial

ANOVA’s were undertaken to assess and estimate the impact of multiple independent factors on the

dataset.

Shannon - H analysis was completed to analyse the evenness of the diversity within each site, and

was completed using the following formula:

s

H = ∑ - (Pi * ln Pi)

i=1

Where H = the Shannon Diversity Index, Pi = the fraction of the population made up of species i,

S = the total number of species encountered, ∑ = sum from species 1 to species S.

Simpsons Diversity Index was calculated to confirm the results of Shannon – H analysis and was

calculated using the following equation:

D = (n / N)2

20

Where D = the Simpson’s Diversity Index, n = the number of organisms of a particular species, N =

the total number of organisms in all species.

Simpson’s Index of Diversity was calculated using 1-D, while Simpson’s reciprocal Index was

calculated using 1/D.

3.4 - The Effect of Human Disturbance and Habitat Degradation on Reptile and

Amphibian Communities

3.4.1 Introduction

Madagascar is recognised as being a global hotspot for amphibian diversity with 284 endemic

species (number as of December 2011) currently described with many others awaiting formal

verification (Andreone et al, 2012). Similarly the reptile fauna, currently standing at over 300

species, is equally impressive and is likely to swell with future research. With 99.6% of the

amphibian fauna present on Madagascar being endemic, and the reptile fauna also showing 92%

endemicity it makes Madagascar a high global conservation priority. Combined, the two groups

make up the most threatened group of vertebrates on Earth (IUCN 2013). The IUCN currently

places Madagascar as having the fourth largest amphibian species richness on Earth, whilst its

reptile fauna remains relatively understudied.

Current estimates place the percentage of original forest cover lost on Madagascar as high as 90%

(Andreone et al, 2008) and with most reptiles and amphibians occupying small and specific regions,

with many being considered as micro or regional endemics, such large-scale habitat loss ultimately

threatens the majority of species to some extent. Presently all historically sampled amphibians have

been recorded in the past 10-15 years, however there are a worrying number of threats to both fauna

globally, and Madagascar is certainly not immune to any of these. Collins and Storfer (2003)

summarised the main threats into direct and indirect categories, with habitat change, over-

exploitation and the introduction of exotic or invasive species falling into the first category, and

global climate change, the polluting and acidification of habitats and the emergence of infectious

disease belonging in the latter category.

The herpetofauna of Nosy Be has been relatively well studied over the past century or so, however

there is still much work to be done, both from an ecological and genetic point of view, but more

21

pressingly from a conservation angle. The large scale habitat degradation on the island has put

many species under intense pressure; especially considering the small size of the islands only

remaining forest patch, Lokobe, yet the habitat modification allows us assess how each species is

responding to the changes. In our study we have collected data over a full year period, assessing the

species richness and biodiversity of forests surrounding Lokobe.

3.4.2 Aims

The aim of the investigation ultimately was to determine whether there are any differences within

the reptile and amphibian communities across each of the 6 survey sites, and 3 habitat types –

primary, secondary and degraded. This would indicate that the level of human disturbance in the

area might be affecting the composition of the herpetofauna in that particular habitat type. We were

specifically interested in understanding how the species composition and abundances compared

between habitat types, if at all. Although each site does have its own respective characteristics,

potentially making it either favourable or unfavourable for certain reptile and amphibian species, we

hypothesised that broad patterns should emerge that indicate the impacts of human disturbance. The

study aimed to monitor the reptile and amphibian fauna over the period of a full year, encompassing

any seasonal changes in diversity and abundance throughout the habitat types. The investigation

should highlight how individual species, or indeed families are responding to human disturbance,

and which are therefore most susceptible to its progression in the future.

3.4.3 Methodology:

The research carried out this phase is a continuation of the research that started at the beginning of

Phase 124 in September 2012 and follows the same methodology exactly as the previous phases. At

the outset of Phase MGF 131 the time period per active search was increased, from 30mintues per

survey, to 60 minutes per survey. This was a result of our methodology developing, and made our

active searches and our data collection more profitable and efficient.

Each active search survey consisted of a team with a maximum of 4 members, who carefully

examine a specifically selected survey site, recording all of the reptile and amphibians observed

within a time-constrained period. A trained Frontier field staff member, who was responsible for the

group’s safety and the quality of the data collected, always led each survey. The remainder of the

group was made up of voluntary Research Assistants (RA’s). On occasions where the group

consisted of just 3 members, survey time was increased to account for any disparity in sampling

effort. The recording sheets, which were used, can be found in the appendages (Fig 15).

22

One person in each group was selected to record the data, whilst another was responsible for

collecting any additional information such as length or weight. This person was always the Frontier

staff member. The other members of the group are observers only unless assistance measuring an

animal was required. During an active search each microhabitat is explored and checked thoroughly

yet carefully, minimising our impact at the survey site. Each level of the forest is scrutinised, with

binoculars used to identify any species seen high up in the canopy, and a thin stick used to agitate

and reveal any species hidden in the leaf litter. If any animals could not be identified in the field,

photographs were taken and identification was achieved back in the research camp. Any individuals

who still could not be positively identified were omitted from the results.

To ensure that no survey site was over sampled, and to minimise the disturbance caused by our

researchers, each site was only surveyed at most twice a week, and during the second visit we

would try to survey a different area within the site. The boundaries of each site are clearly defined

in most cases, with biodegradable tape being used to help distinguish the site perimeters. Sites 3-6

are for the most part, naturally enclosed by sharp habitat edges, plantations, trails or rice paddies.

The exceptions are the two primary forest sites, whose borders are harder to define, as they are

continuous with Lokobe reserve. Both sites have limits, which were decided and imposed by us.

Site 1, a riparian habitat was simply explored upstream until the survey time constraint expired. Site

2 is deeper into the forest and is approximately 100m2 in size. Brightly coloured biodegradable tape

was used to delineate the boundary and acted as a point of reference at night.

In addition to the visual active search observations, two 100m long drift fences are in place at both

sites 2 and 4 with the endorsement of the local landowners. Each fence is 40cm high and made out

of tough plastic sheeting to prevent it being destroyed. Along the drift fences are positioned 11

pitfall traps, set 10m apart from one another and dug into the substrate so that they are flush with

the ground. The pitfall traps consist of buckets that have a catchment area (diameter) of 29cm, and

are deep enough to withhold all but the largest of lizards. A small amount of soil and leaf litter

deposited into each bucket acts as a refuge for captured animals and allows them somewhere to

shelter. Each trap has several holes in the bottom to allow any water to drain out. Pitfall traps are

checked every 2 days, or after any period of heavy rain, and captured animals are recorded and

released nearby to ensure they remain within their home range.

From a safety perspective, it is essential that each surveying group carried with them a charged 2-

way radio for communication with base camp, a small medical kit, a compass and a whistle.

23

Casual observations

A substantial amount of time was spent out in the forests and other habitats outside of survey times

and animals were often encountered whilst walking between sites or during BTEC surveys. Animals

observed at such times are deemed as casual observations and although they are not included in our

final analysis, they were still identified and recorded for our species inventory.

3.4.4 Results:

During phase MGF 133 a total of 78 time-constrained hour-long active searches were conducted

with a total of 13 surveys (10 daytime and 3 night time surveys) being conducted at each of the

standard 6 survey sites, whilst an additional 13 surveys were conducted at site 9. Pilot surveys were

also trialled at three other sites (7, 8 and 10) and were considered for study, but due to a lack of

findings and ultimately time, this data was omitted from the analysis. Together, sites 1+2 represent

the primary habitat, sites 3+4 the secondary forest habitat and sites 5+6 the degraded / human-

modified habitats.

During this phase a total of 36 separate herpetological species were observed (compared to 42

during the last phase, MGF 132) across sites 1-6, with a total of 1,145 individual animals recorded

during both day and night time active searches. A further 19 individual animals were captured and

then subsequently released from the pitfall traps. The pitfall traps set up at sites 2 and 4 captured a

total of 5 species, with each sites trap yielding 4 separate species. The daytime active searches

contributed the greater number of individuals during the phase, with a total 794 individuals being

observed across 28 species. Night time active searches contributed 351 individual amphibian and

reptiles across 27 species. The pitfall traps were not set up for the entire data collection period, due

to a combination of our temporary absences, but each was active and checked 10 times. Overall the

study ran for a period of 70 days between July 8th and September 18th 2013.

Initial analysis of the results show that the primary sites held the highest species richness in three of

the four phases of data collection and joint highest during the last phase (Fig. 4). During Phase

MGF 133 24 different species were recorded in both primary and secondary habitats, whilst 20

species were recorded in the degraded habitats. Pitfall trap data provided no species that were not

observed during our active searches during the past phase, and therefore did not influence the

comparative species richness. Again it should be noted at this point that it was only the degraded,

highly disturbed sites that do not have pitfall traps and drift fences installed, after they proved

ineffectual and extremely high maintenance during phase 131.

24

Figure 4 – The total species richness found within the primary, secondary and degraded habitat

zones. Graph includes data collected from both day and night active searches combined, as well as

pitfall trap data. The graph shows a comparison of the data collected this phase with that collected

during the previous 3 phases.

In terms of the overall abundance of individuals recorded over the four phases (Fig 5), a similar yet

slightly different pattern emerges from the data. The primary sites host the greatest number of

individuals in all four of the study phases, with 466 individuals recorded during the previous phase.

However the data shows that the secondary forest habitats hold the second largest number of

individuals only during phases 132 and 131, whilst the degraded habitats were found to host the

second greatest number of individuals during phases 124 and 133. During the last phase, MGF133,

323 individuals were observed in the secondary forest habitats whilst 356 individuals were recorded

in both of the degraded sites, 5+6 combined.

Amphibian & Reptile Species Richness per Habitat Type

23

16 16

2927

22

3433

20

24 24

21

0

5

10

15

20

25

30

35

40

Primary Secondary Degraded

Habitat Type

Sp

ecie

s R

ich

ne

ss

Phase 124

Phase 131

Phase 132

Phase 133

25

Figure 5 – The total number of individuals observed during active searches, both day and night in

primary, secondary and degraded habitats. Data for phases MGF 132, MGF131 and MGF124

included for comparison. Pitfall data omitted.

Further breakdown of the MGF133 results show that both primary sites, 1+2 contained the highest

species richness with 21 species being recorded at each location. Site 3 hosted the third largest

number of herpetological species found during the survey, with 20 species being recorded. Site 4,

the secondary forest fragment with high levels of disturbance was found to be the fourth

biologically rich locality, with a total of 18 separate species whilst site 5 had a species richness of

16 species. Finally site 6, the relatively baron pineapple plantation, had a species richness of 15

species. A comparison of species richness recorded for each survey site can be seen in Table 3,

along with a complete breakdown of results for the entire year’s data.

In terms of abundance during MGF 133, the greatest number of individual animals were observed at

site 1 (244) with the other primary site, site 2 also showing high levels of abundance with 222

individuals being recorded. The secondary forest site, site 3 had the third greatest number of

observations (188) whilst site 6 contained the fourth largest number of individuals (183). 173

individuals were recorded at site 5, while only 135 individual amphibian and reptiles were observed

at site 4. Pitfall data was not included in these abundance figures as the pitfall traps were only

present at sites 2 and 4, and so could skew the data unfairly. However species were added to the

overall habitat richness figures if they had not been seen already during active searches. The results

Total No. Individual Amphibian and Reptiles per Habitat Type

300

131172

404

300270

647

454

378

466

323356

0

100

200

300

400

500

600

700

Primary Secondary Degraded

Habitat Type

To

tal

No

. In

div

idu

als

Ob

serv

ed

Phase 124

Phase 131

Phase 132

Phase 133

26

show that the primary habitats have greater species richness when all of the year’s data is collected,

with a total of 46 distinct amphibian and reptile species being observed between sites 1+2. The

primary habitats also received the greatest number of individual observations (1739).

Table 3 – A summary of the data showing richness and abundance collected over all 4 phases, covering the

surveying period 1st October 2012 until 16

th September 2013.

The secondary forest environments were found to hold the second largest species richness, with 41

species of amphibian and reptile observed in these habitats. A total of 1209 individual sightings

were made throughout all four phases in the secondary forest, only slightly more than were

observed in the degraded habitats (1076). The species richness was found to be noticeably lower in

Site number/ Habitat type

1 2 3 4 5 6 Primary Secondary Degraded

MGF 133

Richness 21 21 20 18 16 15 24 24 21

Abundance 244 222 188 135 173 183 466 323 356

MGF 132

Richness 23 29 25 21 18 17 34 33 20

Abundance 365 282 242 212 165 213 647 454 378

MGF 131

Richness 18 26 14 22 17 17 29 27 22

Abundance 188 216 89 211 147 123 404 300 270

MGF 124

Richness 8 22 12 13 15 12 23 16 16

Abundance 178 122 56 76 94 78 300 131 172

Total Year

Richness

Abundance

31

868

40

779

33

507

32

605

22

565

20

541

46

1739

41

1209

27

1076

27

the degraded habitats, those which experience the most human disturbance, with only 27 species of

amphibian and reptile found in both sites 5+6 throughout the year.

Table 4: Summary of the year’s output for both sets of pitfall traps.

Analysis of the pitfall traps for Phase MGF 133 shows that 4 separate species were recorded and

then subsequently released from both the traps at site 2 (primary forest) and site 4 (secondary

forest). A total of 9 individuals were captured at site 2 and 10, whilst 10 were recorded at site 4.

Trap efficiency at site 2 was 40% and it was 60% at site 4. A summary of pitfall trap data for the

entire collection period is presented in Table 4 above. Analysis shows that both sets of traps have a

capture rate of above 50% and that both the number of individuals captured in each were similar, as

was the variety of species captured. The pitfall traps at site 2, within primary forest captured a frog

species (Boophis tephraeomystax) and a gecko species (Phelsuma madagascariensis), which were

Pitfall Trap Analysis

Primary (Site 2) Secondary (Site 4)

MGF 133

Richness 4 4

Abundance 9 10

Efficiency 40% 60%

MGF 132

Richness 5 6

Abundance 27 26

Efficiency 70% 80%

MGF 131

Richness 4 6

Abundance 13 17

Efficiency 40% 40%

MGF 124

Richness 6 3

Abundance 27 4

Efficiency 70% 50%

Total Year 55% 57.50%

Richness 11 12

Abundance 76 57

28

unique to that particular trap line. The series of traps situated at site 4, secondary forest, captured

one skink species (Trachylepis gravenhorstii), one gecko species (Ebenavia inunguis) and a

primitive snake species (Ramphotyphlops braminus), which were not shared by the traps in primary

forest. A further 6 species were common to both sets of traps: 2 species of plated lizards -

Zonosaurus madagascariensis and Zonosaurus rufipes, a species of skink – Madascincus polleni,

and 3 species of Microhylid frogs – Rhombophyrne testudo, Stumpffia pygmaea and Stumpffia

psologlossa.

Statistical analysis (SPSS v.20) concluded that there was no significant difference between the

species richness of reptiles and amphibians found per survey across the 6 survey sites (Anova

F=1.399 p=0.235) during phase MGF 133. Similarly there was found to be no significant difference

between the numbers of individuals found per survey at each of the 6 survey locations (Anova

F2.012, p=0.087). However Tukey Post-hoc testing revealed there to be a significant difference in

the mean number of individuals found per survey between sites 1+4 (p=0.040).

When the dataset was condensed, with the 6 surveying sites being abbreviated into the 3 habitat

types, analysis revealed there to be still no statistical significance in the number of species found

per survey (Anova F=2.583, p=0.082). The mean number of species observed per survey, for each

habitat was very similar with primary habitat 5.8 species, secondary 5.2 species and degraded 4.7

species. A statistically significant result was found however when analysis of the number of

individuals found per survey was run (Anova F=3.328 p=0.041). The subsequent Post-hoc Tukey

test showed that the significant result lay between the number of individuals recorded per survey

between both the primary forest sites and the secondary forest sites (p=0.033). The overall mean

number of individuals animals observed throughout the Phase was 14.7 per hour of surveying; with

the most productive site in terms of abundance being site 1 with an average of 18.8 individuals

recorded each survey. The least productive site was the secondary forest fragment, site 4, with an

average of just 10.4 individual reptiles and amphibians discovered per hour.

Full Year Analysis:

In order to test our dataset thoroughly, a series of null hypotheses were formulated:

Ho1 – Habitat type (primary, secondary or degraded) has no effect on amphibian and reptile species

richness.

Ho2 – Habitat type (primary, secondary or degraded) has no effect on the abundance of reptiles and

amphibians.

29

Ho3 – Species richness is not affected by location (sites 1-6).

Ho4 – The abundance of amphibians and reptiles is not affected by location (sites 1-6).

Ho5

– The number of amphibian and reptile species recorded does not vary between phases.

Ho6 – The number of individual amphibians and reptiles observed does not vary between phases.

Ho7 – The interaction between data collection phase and habitat has no bearing on species richness.

Ho8 – The interaction between data collection phase and habitat has no bearing on abundance.

Through a series of statistical tests these null hypotheses were then tested and either rejected or

accepted.

When the dataset was combined to include the full years results, analysis revealed that there was no

significant difference between the mean values for species richness, either between habitat types or

between the individual sites (p=0.140, F=1.982 & p=0.080, F=1.990 respectively). Significance was

determined to 95% confidence level. When the data was scrutinised for differences between habitat

type and the mean number of individuals recorded per survey, ANOVA gave a significant result

(p=0.000, F=8.643), allowing us to reject the null hypothesis Ho2. Further analysis using Tukey

HSD Post-hoc testing revealed that the significant result lay between the primary and secondary

habitats (p=0.000) and between the primary and degraded habitats (p=0.000). No significant

difference was found between the secondary and degraded habitats, in terms of the number of

individual reptile and amphibians recorded.

To investigate further, ANOVA was run using each site (1-6) as a step within our independent

variable. This allowed us to infer whether specific sites were responsible for the significant

difference found between the abundances per habitat type. The result was significant (p=0.000,

F=5.178) and allowed us to reject the null hypothesis that site has no bearing on the abundance of

reptiles and amphibians. Tukey Post-hoc testing showed that the mean number of individuals found

at site 1 was significantly different from sites 3, 4, 5 and 6 but not from site 2 (p=0.002, p=0.019,

p=0.015, p=0.005 and 0.951 respectively). The mean number of individuals observed also differed

significantly between site 2 and 3 also (p=0.039), whilst no further significance was found between

other sites.

30

When the dataset was analysed for differences between each phase, both one-way ANOVA and

factorial ANOVA statistical techniques were used. One-way ANOVA showed a significant

difference in the mean species richness between phases (p=0.000, F=8.643). Subsequent Tukey

Post-hoc analysis revealed the statistical differences to be between phase’s 133+132, 132+131 and

132+124 (p=0.010, p=0.017 and p=0.000 respectively). The total number of individual amphibians

and reptiles recorded per phase was also shown to vary significantly (p=0.000, F=16.928). Again,

Tukey Post-hoc testing revealed the significance to reside between phase’s 133+132, 133+124,

132+131 and 132+124 (p=0.010, p=0.002, p=0.000 & p=0.000 respectively).

Analysis revealed that the levels of species richness and abundance change over the course of the

phases. This is not surprising as a year’s data has to include seasonality, and in tropical countries

this is often pronounced. Figure 6 shows the mean climatic data for a location approximately 17km

away from our survey sites, and the only weather station on Nosy Be. The phase dates are included

in the legend.

Figure 6 – Graph showing the climatic conditions on Nosy Be for the duration of the data

collection. Data obtained from Facene Airport weather station, situated approximately 17km from

Frontier base-camp. Phase dates: MGF 124 = 1st October – 10th December 2012, MGF 131 =

10th January – 15th March 2013, MGF 132 = 1st April – 17th June 2013 and MGF 133 = 8th July

– 16th September 2013.

31

Simple one-way Anova showed that the total species richness did not change significantly over the

course of a year within primary forest habitats. However the abundance of amphibians and reptiles

did change (p=0.000, F=7.841). Analysis of the individual primary sites showed significant changes

to the herptile community at site 1 through the year (p=0.006, F=4.690), no such changes were

observed at site 2. This indicates that site 2 may be more stable than site 1 throughout the year. Both

primary sites saw the levels of abundance vary throughout the phases (p=0.003, F=5.275 &

P=0.015, F=3.896 respectively). At site 1, the main variance was found between phases 132+131

(p=0.008) whilst at site 2 it was between phases 132+124 (p=0.012).

In secondary forests the situation was different, with both the levels of richness and abundance

fluctuating throughout the year (p=0.000, F=7.293 & p=0.000, F=12.041). Significant variation in

species richness was found between secondary forest habitats between phase’s 133+124, 132+131

and 132+124 (p=0.027, p=0.039 & p=0.000 respectively). Individual abundance varied dramatically

throughout the phases with variation between almost all periods of data collection. A breakdown of

the two secondary forest sites showed that site 3 showed strong variation in both species richness

and abundance between the first and second half of the year. Site 4 showed a pattern of significant

variation between phases 132+124 and 131+124 in terms of both species richness (p=0.032 &

0.088) and abundance (p=0.015 & 0.016).

In the degraded habitats, no significant change in species richness was observed throughout the

year, yet similarly to the primary forest habitats, significant changes in abundance were found

(p=0.007). The weighting of this result is influenced mainly by the results from obtained from site

6, as no significant changes to either species richness or abundance were found from site 5

throughout the different phases. Individual breakdown of site abundances over the year showed the

main variance to lay between sites 132+131 and 132+124 (p=0.023 & p=0.008).

Finally the interaction of phase and habitat / site was then analysed using a factorial ANOVA, again

using SPSS. As our dataset was un-even due to the reduced number of surveys during Phase MGF

124, in order to protect against type 1 error I elected to use a reduced significance level of 0.01

instead of 0.05. This would allow for confidence to be held in the alpha values. Analysis showed

that there was no interaction present between phase and habitat type in relation to species richness

(p=0.205, F=1.425). When the dependent variable was changed to the abundance data, the number

of amphibians and reptiles across each habitat type, the result was again insignificant (p=0.043,

F=2.206). This result would normally be regarded as a significant finding; however with our dataset

32

being uneven and the Levene’s test being violated I do not consider this to be so. Analysis of the

interaction between the phase in which the data was collected in, and the site at which the data was

collected, in regard to the species richness, produced an insignificant result (p=0.052, F=2.221).

However when the interaction was tested against the abundances per site, the result was significant

(p=0.002, F=2,482). The Partial Eta squared

result indicates that the interaction between the phase

and the site made up for 12.1% of the total variation within the dataset.

The findings from the pair wise comparison show that at site 1, the significant interactions were

between phases 132+131, 132+124 and between 131+133 (p=0.000, p=0.005 & p=0.002). The

significant interaction found at site 2 was the result of variation between phase 132+124 (p=0.001),

whilst at site 3 it was between sites 133+124, 132+131 and 132+124 (p=0.003, p=0.000, & p=0.000

respectively). Significant results for site 4 were revealed to be between phase’s 132+124 and

131+124 (p=0.006 & p=0.007). There was no significant difference found in the variance between

the interactions of phase and site number at site 5 and only between phase 133+124 at site 6

(p=0.003).

Measures of diversity were then calculated, combining both the species richness of each habitat and

its relative evenness. Two separate sets of diversity index were determined, the Shannon-Weaver

index and Simpson’s Diversity Index and the results are summarised in Table 5.. The Shannon H

values suggest that despite having the largest species richness, the primary habitats are the least

diverse (2.1189), whilst the degraded habitats are the most diverse (2.46). The Shannon eH values

agree with these findings and suggest that the primary habitats are also the least evenly distributed

(0.6), whilst the degraded have the greatest level of evenness (0.7464).

Interpretation of the Simpson values also recognises these counter-intuitive results, concurring that

the primary habitats, when combined show the lowest level of diversity (0.178), with the degraded

habitats again show the highest (0.112). The same pattern follows for both the Simpson’s Index of

Diversity results and the Simpson’s Reciprocal Index.

33

Table 5 – A summary of the diversity indices calculated for the entire years data. Shannon H and

eH given to 4 decimal places and Simpson’s indices given to 3 decimal places. Simpson’s Index of

Diversity = 1-D and Simpson’s Reciprocal Index = 1/D.

Diversity

Index

Site 1 Site 2 Site 3 Site 4 Site 5 Site 6 Primary Secondary Degraded

Shannon H 1.8325 2.3587 2.3631 2.3635 2.4916 2.1189 2.2709 2.468 2.46

Shannon eH 0.5336 0.6438 0.6758 0.7093 0.7946 0.696 0.6 0.6785 0.7464

Simpson Index (D) 0.309 0.198 0.151 0.141 0.12 0.167 0.178 0.137 0.112

Simpson's Index of

Diversity

0.691 0.802 0.849 0.859 0.88 0.833 0.822 0.863 0.888

Simpson's

Reciprocal Index

3.236 5.05 6.622 7.092 8.333 5.988 5.618 7.299 8.928

Table 6 shows the breakdown of the overall richness and abundances for each site per phase and

along with Figure 7 show that the majority of richness found across all habitat types are attributable

mainly to species within the reptile family Gekkonidae, the amphibian Order, Anura and the general

snake family Colubridae. These three groups do however contain the largest number of species out

of the 8 families and 1 order found on Nosy Be, with the Anura consisting of 19 species, whilst the

Gekkonidae and Colubridae are represented by 17 species and 16 species respectively.

Table 6 also includes several families that contain only a few very elusive and uncommon species,

but they are included for completeness. The family Typhlopidae (blind snakes), believed to

comprise of 4 species on Nosy Be is one such example. Their fossorial, secretive and probably

highly seasonal habits make them extremely unlikely to encounter. Similarly, the family

Crocodylidae is included, which is represented by only 1 species (Nile Crocodile - Crocodylus

niloticus) in Madagascar and is particularly scarce due to persecution. It is therefore unlikely to be

observed in any of our research sites.

34

Table 6 – Breakdown of species richness across all sites and phases into Order (Anurans only) and

Family groups. The results indicate that the Order Anuran and the family Gekkonidae and

Colubridae are responsible for the bulk of the species richness in the majority of habitats.

Richness: Site Number Primary Secondar

y

Degrade

d

Total

Richnes

s

1 2 3 4 5 6

Anura MGF 133 5 6 7 3 3 1 6 7 4 8

MGF 132 9 9 7 5 4 2 11 9 4 14

MGF 131 5 9 4 5 4 2 9 6 4 11

MGF 124 4 3 1 2 2 1 4 2 2 6

Testudinidae MGF 133 x x x 1 x x x 1 x 1

MGF 132 x x x x x x x x x x

MGF 131 x x x 1 x x x 1 x 1

MGF 124 x x x x x x x x x x

Crocodylidae MGF 133 x x x x x x x x x x

MGF 132 x x x x x x x x x x

MGF 131 x x x x x x x x x x

MGF 124 x x x x x x x x x x

Chamaeleonidae MGF 133 4 3 3 3 3 1 4 3 3 4

MGF 132 3 3 3 3 3 1 4 3 1 4

MGF 131 2 2 2 3 2 1 2 3 2 3

MGF 124 1 2 2 2 1 1 2 2 1 2

Gerrhosauridae MGF 133 2 2 2 2 1 1 2 2 2 2

MGF 132 2 2 2 2 2 2 2 2 2 2

MGF 131 2 2 2 2 2 2 2 2 2 2

MGF 124 2 2 2 2 2 1 2 2 2 2

Scincidae MGF 133 x x 1 1 1 1 x 1 1 1

MGF 132 1 2 1 1 1 1 2 2 1 4

MGF 131 2 2 x 1 1 1 2 1 1 2

MGF 124 1 2 1 x 1 1 2 1 1 2

Gekkonidae MGF 133 8 7 4 6 4 7 9 7 7 13

MGF 132 7 8 6 7 6 7 9 9 7 13

MGF 131 5 7 3 8 4 7 7 8 7 12

MGF 124 x 6 4 6 6 7 6 7 7 13

35

Boidae MGF 133 x x x x x x x x x x

MGF 132 x 1 1 x 1 x 1 1 1 2

MGF 131 x 1 x x x x 1 x x x

MGF 124 x 1 x x x x 1 x x 1

Colubridae MGF 133 2 3 3 2 4 4 3 3 5 7

MGF 132 1 4 5 3 3 4 5 5 4 8

MGF 131 2 3 3 2 4 4 4 4 6 8

MGF 124 x 5 2 1 3 1 5 2 2 5

Typhlopidae MGF 133 x x x x x x x x x x

MGF 132 x x x x x x x x x x

MGF 131 x x x 1 x x x x x x

MGF 124 x x x x x x x x x x

Figures 7 and 8 reveal more intimately the distribution of species richness and abundance within

families (Order in the case of the Anura), and allow comparisons of habitat type and phase to be

drawn. Figure 7 shows that the richness within the Gekkonidae family was fairly consistent

throughout the year, whereas although the amphibian fauna was similarly rich, the richness was not

as consistent throughout the year. It is important to note here however that Phase 124 had a lesser

number of repeat surveys, and this is most likely to be the cause of the reduced observable

richness’s common to several families. This is also certainly a factor that must be considered when

interpreting Figure 8, the abundances of individual reptiles and amphibians recorded per Order or

Family.

36

Figure 7 – The distribution of species richness across each phase and between each Order/Family

of Amphibians and Reptiles. The peaks can are clearly visible in the Order Anura and the Reptile

families Gekkonidae and Colubridae. Pitfall data included.

37

Table 7 - Breakdown of abundance across all sites and phases into Order (Anurans only) and

Family groups. The results indicate that the Order Anuran and the families Gerrhosauridae and

Gekkonidae are responsible for the bulk of the species richness in the majority of habitats. Pitfall

data is excluded.

Abundances: Site Number Primary Secondary Degraded Total

1 2 3 4 5 6

Anura MG133 156 65 81 33 54 2 221 114 56 391

MG132 298 54 112 39 17 21 352 151 38 541

MG131 152 49 33 112 33 5 201 135 38 374

MG124 154 21 1 32 10 3 175 33 13 221

Testudinidae MG133 x x x 1 x x x 1 x 1

MG132 x x x x x X x x x x

MG131 x x x 1 x x x 1 x 1

MG124 x x x x x x x x x x

Crocodylidae MG133 X x x x x X x x x x

MG132 X x x x x X x x x x

MG131 X x x x x X x x x x

MG124 X x x x x X x x x x

Chamaeleonidae MG133 29 59 38 26 25 8 88 64 33 185

MG132 14 42 27 22 12 6 56 49 18 123

MG131 6 29 4 19 12 3 35 23 15 73

MG124 2 8 6 5 2 1 10 11 3 24

Gerrhosauridae MG133 35 56 49 19 2 1 91 68 3 162

MG132 42 145 91 79 43 12 187 170 55 412

MG131 17 103 40 29 10 8 120 69 18 207

MG124 21 70 33 23 12 7 91 56 19 166

Scincidae MG133 x x 1 9 37 38 x 10 75 85

MG132 2 4 1 7 35 59 6 8 94 108

MG131 4 5 x 6 40 29 9 6 69 84

MG124 1 4 1 x 31 20 5 1 51 57

Gekkonidae MG133 21 39 15 44 41 130 60 59 171 290

MG132 9 26 11 49 40 108 35 60 148 243

MG131 7 21 13 38 27 73 28 51 100 179

MG124 x 11 9 13 28 46 11 22 74 107

38

Boidae MG133 x x x x x x x x x x

MG132 x 1 2 x 1 x 1 2 1 4

MG131 x 1 x x x x 1 x x 1

MG124 x 1 x x x x 1 x x 1

Colubridae MG133 2 4 4 3 14 4 6 7 18 31

MG132 1 9 8 6 14 10 10 14 24 48

MG131 2 8 4 7 25 5 10 11 30 51

MG124 x 7 6 2 11 1 7 8 12 27

Typhlopidae MG133 x x x x x x x x x x

MG132 x x x x x x x x x x

MG131 x x x x x x x x x x

MG124 x x x x x x x x x x

39

Figure 8 – The distribution of abundance across each phase and between each Order/Family of

Amphibians and Reptiles. The peaks are clearly visible in the Order Anura, the Reptile families

Gerrhosauridae and Colubridae. Pitfall data excluded.

By comparing figures 7 and 8 it is clear that species richness does not correlate strongly with

overall abundance. Although the Order Anura show peaks on both graphs, the Gekkonidae show a

lesser degree of dominance in terms of overall abundance than they do in richness within the

family. Similarly the family of plated Lizards(the Gerrhosauridae) are represented by only 2 species

yet both are extremely common, whilst the family Colubridae are a relatively rich group but most

species are seldom observed and recorded. Analysis of Table 7 & Figure 8 reveals that the herptile

community in the area is dominated by the amphibian fauna, which made up 36.12% of all

40

individual animals recorded throughout the year. More amphibians were found than any other group

during each of the four phases. Interestingly, 62.15% of all amphibian observations came from

within primary forest, whilst 28.36% were recorded from secondary forest and just 9.5% were made

in degraded habitat.

Further breakdown revealed that almost half of all of the frogs surveyed (49.77%) were found at

site 1, exposing the stark importance of this location to the areas diversity. The second most

abundant family throughout the year were the Gerrhossauridae who composed 23.04% of the total

number of amphibians and reptiles seen. Unlike the amphibians however, the two species of

Zonosaurus were distributed in both primary and secondary habitats fairly evenly, but similarly

were most uncommon in degraded habitats. Despite having the highest species richness recorded

(14), the Gekkonidae made up only 19.37% of the overall herptile community. Figure 7 shows that

the gecko diversity is relatively equally spread throughout each habitat type, yet figure 8 shows that

the majority of their abundance is found in degraded habitats. This suggests that whilst several

species are seemingly well suited to degraded habitats and human disturbance, a similar number of

species exist in fairly low populations in primary and secondary forest.

A year’s data collection also shows that many of the animals living in the area are extremely elusive

and again almost certainly exist only within small populations or small areas of habitat. Although

extremely diverse in the region, all members of the Colubridae family were seen fairly infrequently,

with the hognose (Leioheterodon madagascariensis) being easily the most abundant. Other

members of the family were observed only on a few occasions and several were never seen at all. In

addition, only 1 species of the 4 representative Typholidae species were recorded, and this

individual was captured in a pitfall trap during the rainy season. There were also many species of

skinks, frogs, gecko’s and chameleon that we did not observe, and it is most likely that these species

are forest specialists and may be extremely sensitive to human disturbance.

Interestingly, throughout the years surveying work, two curious specimens were discovered. The

first of which, and possibly the most exciting discovery of all was a chameleon species found on the

very edge of Lokobe Integral Reserve (GPS – S 13 24’42’’25 E 48 20’279). The specimen was

instantly recognised as something different to the common species found on Nosy Be and after

consulting the amphibian and reptile guide, we tentatively identified it as a Furcifer petteri. Further

consultation with Dr Frank Glaw confirmed that this specimen was indeed a young male Furcifer

petteri – and the first of the species to be found on Nosy Be despite over 150 years of international

surveying. This finding recognises F. petteri as a very rare animal within the Lokobe forests.

41

Plate 2 – Photographs of young male Furcifer petteri found on the border of Lokobe Integral

Reserve. Photographs show the distinct dual nasal appendages and depressed casque that marked

the specimen out as unusual. Photographs by Charlotte Daly.

The young male specimen was measured and had a total length of 16.4cm, SVL – 7.3cm and a tail

length of 9.1cm. The individual was found asleep on a branch at night approximately 50m away

from the border of Lokobe reserve. It was discovered at a roosting height of 1.75m, at a sharp

habitat edge in an area recently cleared to distinguish the Lokobe reserve border.

The second interesting specimen was a species of pygmy leaf frog, similar in size to both the

Pygmaea stumpffi and P. psologlossa. This specimen however was unusual in that its dorsal surface

was covered in large whiteish tubercules. Again consultation with the guidebook ‘A Field Guide to

the Amphibians and Reptiles of Madagascar’ indicated that this was possibly a specimen of

Stumpffia gimmeli. The theory was corroborated in a way by the fact that the specimen was found in

an area used for agriculture, near a man made irrigation ditch surrounded by plants often imported

from the mainland. Further scrutiny led to several more similar individuals being discovered later.

A description of the species distribution included a nearby trading town, Ambanja, where plants are

often purchased before being shipped to Nosy Be. I believe it is likely that several S. gimmeli have

arrived on Nosy Be as stowaways.

Analysing the reptile and amphibian community on a broad, family level is necessary to establish

whether or not any significant patterns of decline are taking place, however it is clear that in order

42

to protect many of the forests most threatened species, assessment of individual species must be

made in order to inform future conservation management strategies. Individual species analysis is

therefore extremely important alongside broader family level analysis, in order to fully understand

the ecology of the community. Species level analysis also allows us to visualise how particular

species are responding to human disturbance, a major objective of our research. This can help

evaluate which species are most threatened and can help to direct conservation effort. Family level

analysis is a great tool for long-term monitoring and can reveal underlying symptoms of pressure on

a community or habitat. However many large families are comprised of species with diverse

ecological needs and specialisations and therefore react differently to stimulus such as human

disturbance and habitat loss. As a result it is critical to combine family level monitoring and species

level analysis to effectively conserve a regions biodiversity.

Figure 8 displays the amphibian diversity found throughout the year, with observations for each

species divided up into habitat type. The abundance and dominance of just 1 species is very

obvious. Mantella ebenaui, the Bronze Mantella is common in all suitable habitats and made up

61% of all amphibians recorded. This species made up 61.84% of all amphibians found in primary

habitats, 71.54% in secondary forests and 18.6% in degraded habitats. This is interesting as they

themselves were fairly scarce in disturbed habitats, illustrating the paucity of amphibian’s diversity

in such sites. Preference appears to be for shaded environments with a nearby water source and

deep leaf litter. They are abundant around all forest streams, even if they are dry, but thrive in

primary habitats with little disturbance. Our previous data has shown this species to be statistically

more abundant in primary habitats, and significantly more abundant at site 1, a riparian habitat

(Anova F=12.523 p=0.000). Our current data suggests that this species reacts strongly and rapidly

to human disturbance (unpublished) with populations seemingly disappearing within a short period

of time after the event. Our data also suggests that populations are able to recover fairly quickly.

Amphibian richness is higher in primary forest habitats than in any other, along with total

abundance. Figure 9 shows that Mantidactylus ulcerosus, Gephyromantis horridus, Gephyromantis

granulatus and Boophis jaegeri were observed solely in primary habitat. Two species were found to

inhabit degraded habitats almost exclusively, being sometimes found in adjacent secondary forest

(Ptychadena mascareniensis & Heterixalus tricolor). This indicates that they are well adapted to

cope with rapid changes to the environment and to regular human disturbance. However the most

adaptable species appears to be the tree-frog Boophis tephraeomystax, whose abundance seems to

be evenly distributed between all three habitats states.

43

It was also the third most common amphibian species in our surveys. It is noteworthy however that

besides the Mantella, most frog species appear to exist in relatively low abundances.

Figure 9 - Summary of the amphibian diversity and habitat distribution. Mantella ebenaui clearly

dominates in terms of abundance at both primary and secondary forests whilst most other species

were recorded in very small numbers. Pitfall data is excluded.

The only other species that was found in any real abundance during our study was the species

Gephyromantis pseudoasper. A total of 216 individual recordings were made during our surveying

period, and were distributed within primary and secondary forest and absent from degraded areas.

This frog appears to have a preference for primary forest but is able to tolerate low levels of

degradation. Similarly, the 2 species of pygmy frog; Stumpffi pygmaea and S. psologlossa were

found only in primary and secondary forests also, along with the fossorial and secretive species

Rhombophyrne testudo, which was mainly observed through its capture by pitfall trapping.

44

With regard to the three-species of frog which we did not observe during the year, it is highly likely

that they are either restricted to certain micro-habitats or small localities, or live away from the

forest reserve elsewhere on Nosy Be. In the case of Platypelis milloti, which are known from only a

few locations, they are restricted to within the strict Integral Reserve, and are therefore rightly

considered endangered by the IUCN. Hoplobatrachus tigrinus is known from other regions on

Nosy Be, and exists outside of primary forest. It is considered an introduced edible species and

under no threat due to its widespread nature. The third species, Cophyla occultans is found in a

number of different habitats, including degraded habitats, and its arboreal lifestyle is likely

responsible for its absenteeism from our surveys.

As mentioned previously, the family Gerrhosauridae was represented by only two of the 4 species

presumed to be present in the area. Throughout the entirety of the study, both Zonosaurus

madagascariensis and Z. rufipes combined made up 20.3% of the total abundance of all animals

found. Z madagascariensis contributed 6.6% of the total reptile and amphibian abundance whilst Z.

rufipes made up 15.6%. Results show that Z. rufipes is an extremely common species in the

Ambalahonko region. Figure 8 suggests that both species are most abundant within primary and

secondary habitats, with few found in degraded areas. Previous statistical analysis found there to be

a significant difference in abundance between primary and degraded habitats (anova p=0.000) but

no difference between primary and secondary habitats for Z madagascariensis. Similarly 60.4% of

Z. rufipes were recorded in primary habitat, 36.5% were recorded in secondary forests and 3.02% in

degraded habitats. Statistical analysis showed a significant difference in the mean number of Z.

rufipes found between habitat types, with Post-hoc tukey testing revealing the significance to lie

between the abundance found in primary environments and those in both secondary and degraded

habitats (Anova p=0.0149 & p=0.000 respectively).

Examination of the herptile data set reveals that the family Gekkonidae are an abundant and diverse

group. In total the gecko’s make up 17.5% of the reptile and amphibian community in terms of

abundance and 27% of the community richness. Figures 7 & 8 show that the species richness within

the Gekkonidae is distributed evenly amongst the primary and secondary habitats, with 12 separate

species being recorded in both, showing a high level of commensality. Only 8 gecko species were

recorded in degraded habitats, however these 8 species made up the vast majority (63.92%) of the

individual geckos observed. The 12 species of gecko found in primary forests made up just 10.81%

of the total abundance of geckos whilst the 12 species from secondary forest contributed 25.27%.

45

Figure 10 shows that again, the Gekkonidae diversity is dominated by 1 species, Phelsuma

madagascariensis grandis. This species is a great deal more abundant than any other (353

observations) and was found to be present in all 3-habitat types, along with Gekolepis maculata.

Phelsuma madagascariensis was found to be present at 5 of the 6 survey sites, absent only from the

pristine gallery forest site 1. This species has a clear habitat preference and appears to thrive in

degraded habitats such as plantations and can tolerate very high levels of human disturbance. Of the

353 individual observations for this species, 67% of these corresponded to degraded habitat, whilst

30% came in secondary forest and 3% from primary. Analysis from previous phase MGF 132

showed that there was statistically significant difference between the abundance of P.

madagascariensis found in primary and degraded habitats (Anova p=0.000). This preference for

degraded environments seems to be fairly common within the subfamily Phelsuma, with both P.

laticauda and P. abbotti showing similar trends.

However the pattern does not seem to fit with P. dubia or P. seippi, whilst P. quadriocellata was

extremely uncommon in the area and so no inferences about its habits can be drawn.

46

Figure 10 - Summary of the gecko diversity and distribution amongst habitat type. Phelsuma

madagascariensis clearly dominates in terms of abundance at both primary and secondary forests

whilst most other species were recorded in relatively low abundance. Pitfall data is excluded.

Besides from a few species within the Phelsuma family, all other species of gecko were observed

relatively infrequently (<50) and appear to live in low population densities. 7 species in total were

observed only in either primary or secondary forest, being absent from degraded habitat, whilst 6

species were found in both secondary and degraded habitats but absent from primary forest. The

Gekkonidae as a family show a great deal of variety within its subfamilies, in terms of habitat

preference or possibly even dependency. 3 species of gecko appear to be restricted to primary

habitat and were not recorded in any habitat experiencing human disturbance. The subfamily

Uroplatus (Leaf-tailed geckos) contained 2 species (U. henkeli & U. ebenaui) that seem to be the

most intolerant to disturbance. U. henkeli inparticular was only observed in primary forest;

consistent with previous studies (IUCN 2013.1) whilst U. ebenaui was occasionally observed in

secondary forest as well as primary, however only during periods of low-level human activity. Out

47

of all of the gecko species within the area, U. henkeli is the most likely candidate to be designated

an indicator species.

Other species shown in Figure 10 include Hemidactylus frenatus, a nocturnal gecko which was only

ever casually observed inside human residences and never in any other habitats. Ebenavia inunguis

is another species which seems extremely uncommon in the area, and was only observed on a

handful of occasions and only twice during surveys. All sightings of this species have been made in

secondary forest.

Analysis of the Snake families, Colubridae, Boidae and Typhlopidae shows predictably that the

Colubridae family predominate. The Colubridae is the largest of the three families with a total of 16

species reported in the area historically, whilst only 4 of the secretive blind snakes, Typhlopidae are

thought to inhabit the area. Two species of constrictors from the family Boidae complete the

serpentine diversity. Analysis of the Colubridae family (Figure. 11) shows that a total of 11 species

were recorded throughout our surveying period, meaning that 5 species were not recorded in our

data. Only 1 species of Typlopidae was discovered during our study period, Ramphotyphlops

braminus, while both species of Boa constrictor were recorded.

48

Figure 11 - Summary of the Colubridae diversity and their distribution amongst habitat type.

Leioheterodon madagascariensis clearly dominates in terms of abundance and is the most evenly

distributed species. Two other species, Mimophis mahfalensis and Dromicodryas quadrilineatus

are also abundant, but mostly in degraded habitats.

The overall abundance of snakes was low in relation to the entire amphibian and reptile community

(3.74%), as you would expect from a group of animals, most of which are predatory and hold fairly

high positions within the food chain. The abundance of blind snake species though is

undeterminable due to their fossorial and secretive lifestyle and it may be that they are common

beneath the substrate. Similarly to both the amphibian and gecko faunas, the snake family harbours

species which exist along a gradient of tolerance towards human disturbance and habitat

dependency. Figure 11 shows the range of species that were found during our surveys and the

habitats they associated with.

With regards to abundance, the most commonly sighted snake was the Madagascan Hognose snake,

Leioheterodon madagascariensis, which was recorded a total of 52 times (34.44% of all snakes)

and was one of 4 species observed in all three habitat types along with Madagascarophis

49

colubrinus, Dromicodryas quadrilineatus and Mimophis mahfalensis. L. madagascariensis, M.

mahfalensis and D. quadrilineatus were clearly the most abundant species of snake found during

our study, comprising 81.46% of the total snake abundance, with all the other species being found

in very low numbers (<10 observations). Both M. mahfalensis and D. quadrilineatus were

associated most noticeably with degraded environments whereas L. madagascariensis was the most

evenly distributed species, indicating that it is the most adaptable snake species. Of the 5 species of

snake that we did not encounter during the study, 4 are associated with primary habitats, and are

most likely only to exist in the Lokobe strict reserve. Some species such as the Micropisthodon

ochraceus are strictly arboreal, reducing our opportunities to witness it, whilst others are known

only from primary rivers and streams (Pseudoxyrhopus microps). Allaudina bellyi is a forest

restricted nocturnal species with secretive habits and also evaded us during our surveying.

Three species of Colubridae found on our surveys were only recorded outside of primary forest. The

unusual Langaha madagascariensis was found mainly in secondary forest, but also in degraded

habitat. It is possible that this species is also common in primary forest, with its cryptic nature and

arboreal habits making it extremely difficult to observe. This species was extremely uncommon for

most of the year, however several male individuals were observed in June. Lycodryas granuliceps

(formerly Stenophis) was found only in secondary forest, but just on a few occasions, making any

inferences about its habitat preference unreliable. Dromicodryas bernieri, a closely related species

to D. quadrilineatus and similar in appearance to M. mahfalensis seems to share their habitat

preference for scrubland and degraded sites. Only observed a few times on survey this species

seems to be restricted to dry scrub type habitat. Conversely, 2 species were found to only inhabit

primary and secondary habitat, with Bibilava stumpffi only found in primary forest. Finally, both

species of Boa constrictors do not appear to have any habitat preference and were found in low

abundance throughout all habitat types.

3.4.5 Discussion

The herpetological diversity that exists on Nosy Be is extensive considering the size of remaining

primary forest, with 80 confirmed species on the island (including our recent discovery of Furcifer

petteri) and at least 60 confirmed within the boundaries of Lokobe Integral Reserve (Andreone et al,

2003, Glaw & Vences, 2008). After completing a successful yearlong study of the amphibian and

reptile fauna outside the Lokobe forest Reserve certain patterns have become evident. Contrary to

expectation at the beginning of the project, the overall species richness does not decrease

significantly along a gradient of human disturbance. Although during our study we found a greater

number of species in total within the primary forests (46 species) than both the secondary forests

50

(41 species) and degraded habitats (27 species), the overall result proved insignificant. We have

however found there to be a significant difference in the overall abundance of reptiles and

amphibians found within each habitat category.

Our findings show that the carrying capacity of primary forest (1739 individuals) exceeds that of

both secondary forest (1036) and degraded environments (1076 individuals), and decreasing with

the level of human disturbance. The most modified landscapes appear to be able to support the

fewest number of species and individuals. Overall, forest clearance appears to have had a negative

impact on the reptile and amphibian diversity in this area, however in congruence with a lot of

literature, the response and sensitivity to habitat destruction and clearing varies on both a family and

species level (Scott et al, 2005).

Our study has shown that the constituent families and species that make up the total species richness

in each habitat are markedly distinct. The different species within each family and subfamily seem

almost partitioned into different habitat types in accordance with the level of degradation. However,

obviously there are no definitive categories, and each species responds to human disturbance and

forest clearance in a unique way. The level of disturbance a species can tolerate lies along a

continuous gradient, and rarely is the level of deforestation and clearing in balance with the

ecological needs for sustained diversity. It may therefore be surmised that certain species are either

able to tolerate human disturbance to a level where a population can be sustained, or it cannot.

Whilst particular species are able to tolerate human disturbance, adapt and therefore thrive, others

are more sensitive to it and are forced back into the remaining forest fragments as disturbance

continues. Many of the species that we have observed in secondary forest may already depend upon

supplementation from a principal or reserve population within primary forest, in order to sustain

their presence within forest areas experiencing human pressure. Other species, which we have

infrequently observed in secondary forest, may already be on a slow retrograde course as illegal

logging and further forest clearing has increased over the past few months.

Our results show that the amphibian fauna, both in terms of richness and abundance, seemingly

dominate the primary forest habitats, yet their diversity is greatly diminished in degraded

environments. The large amphibian diversity found in primary habitat can only partially be

attributed to the fact that both sites contained water bodies, as both secondary forest sites also

encompassed a permanent and seasonal stream respectively. The greater number of frog species

found in primary habitat suggests that these sites also constitute a greater vulnerability, with a large

number of amphibian species only found in primary forest during our survey. Andreone et al 2003

suggested that the amphibian fauna on Nosy Be was represented by generalist species, with the

51

majority of species having distributions along the western coast of Madagascar as well as on Nosy

Be. However the absence of many species from secondary and degraded habitats around the Lokobe

area found by our study, suggests that disappearances may take several years to become evident

(Kuussaari et al, 2009), and many species are in fact dependent on primary forest. Our study shows

that habitat disturbance and forest clearing has already had an impact on the anuran diversity in the

area.

Fresh water habitats are at a premium in Lokobe due mainly to the reserve’s small size, making

each microhabitat incredibly valuable. Amphibians are of course a special case, as they require

water for their reproductive cycle and their permeable skins make them susceptible to pollution.

However their sensitivity towards humidity, canopy cover and leaf litter depth also diminish their

adaptability (Wells, 2007). Despite both diversity indices deducing that the primary habitats had the

lowest diversity overall, this is almost certainly a consequence of the highly unequal distribution of

the amphibian fauna. Similar finding have also been reported from Ugandan and Costa Rican

forests (Vonesh 2001, Folt & Reider 2013). The Bronze Mantella is an incredibly abundant species

in our study area, and although it is also highly adaptable, its abundance is greatest within suitable

primary habitat. Mantellinae anurans have previously been described as highly sensitive to low

level logging and forest clearance (Vallan, 2004), and our work supports this observation. Often

present in high numbers at a location, large populations seemed to disappear almost entirely after a

period of human disturbance. The fact that this species naturally exists in high population densities

may impact on the diversity indices for the forest, with disturbance artificially skewing the dataset

in a more even direction.

In the case of the secondary forests, there is no real dominant group or individual species, instead

almost all families are fairly well represented and the diversity is more evenly distributed

throughout all species. This is encouraging as it suggests that the reptile and amphibian fauna is

resilient enough to withstand a certain level of interference, without significant detriment to

community diversity overall. However the reduction in suitable habitat for those species that are

less tolerant to disturbance remains a problem and populations are potentially in decline. The result

may also indicate that the responses to anthropogenic pressures have yet to show in the population

data (Kuussaari et al, 2009). It is however short sighted to make predictions about the long-term

responses of species to forest clearing and human disturbance due to the stochastic nature of

population trends and the future condition of the forests.

52

The family Gekkonidae accounts for the largest overall component of diversity in the secondary

forests, but the family itself is a large and complex one. When viewed in closer detail, there appears

to be a distinct separation between the species of different genus, with each appearing to have a

particular propensity for certain habitats or alternatively, have varying levels of tolerance and

adaptability. A suitable example of this phenomenon can be observed in the Phelsuma genus of day

geckos. Once a forest dwelling family of diurnal Gecko's, they are now relatively uncommon in

mature forests, instead opting to inhabit human-modified environments (Van Heygen, 2004). Our

results testify to this end, with the majority of species being best represented in degraded habitats.

There is also a marked transition in the abundance of several other Phelsuma species, with

abundances swelling as you pass further along the disturbance gradient towards high levels of

degradation. Glaw and Vences (1994) concluded that some Phelsuma species benefit from

deforestation and undergo population expansions after the initial destruction, and our results would

suggest that Phelsuma madagascariensis grandis is such a species.

Conversely, other species of Gecko's, particularly the species belonging to the genus Uroplatus, and

to a lesser extent the Paroedura, appear to be mostly intolerant to human disturbance and are

dependent on mature forests (Raxworthy & Vences, 2010), whilst Geckolepis maculata is

distributed fairly evenly throughout all of the habitats surveyed. The Gekkonidae are a good

example of why conservation plans should consider the ecological requirements of individual genus

and species on their own merits, as there can be a huge amount of variability within a family with

regards to how they adapt to a changing environment. It is my opinion that members of the

Gekkonidae are reliant on the presence of certain vegetation types or even certain species of tree or

palm, and it is this that factors considerably in their distribution. It is likely that vegetation

preference is linked strongly to their ability to avoid predation, through their cryptic colouration

(Van Hagen 2004).

It is clear that degraded habitats are very important and can support a large and diverse herptile

community (Andreone et al 2003, Folt & Reider 2013). However the type of degraded habitat, its

purpose and management influences the variety of species that exist within it (Andreone et al 2003).

Our study showed that despite having a lower species richness and carrying capacity than both

primary and secondary habitat, the degraded environments were actually the most diverse in our

study. This result echoes that of Andreone et al 2003, who stressed that, agricultural lands were

important in safeguarding biodiversity. The conversion of forest to farmland does leave a telltale

signature on species composition, and this is clear in our findings. Logging, habitat degradation and

human disturbance all commonly result in a shift in species composition, with species typical of

53

rainforests being replaced by species adapted to disturbed habitats (Vallen 2004). Eventually, this

results in the replacement of more specialist and less abundant species, with those which are more

generalist and widespread.

Similarly to the tale of the Phelsuma day geckos, several other species representing various families

also appear to have a preference for plantation type environments. These most notably include the

frog species Ptychadena mascareniensis, the skink species Trachylepis gravenhorstii, the

chameleon Furcifer pardalis and the two colubrid snakes Dromicodryas quadrilineatus and

Mimophis mahfalensis. The family Colubridae make up a substantial portion of the diversity found

within the agricultural survey sites, and I believe that this is primarily the result of certain species

benefitting indirectly from human habitat modification. Some species are known to undergo

population expansions as a result of habitat change, as selective forces such as the competition for

food or predation mortality are relaxed.

In the case of the 2 aforementioned snake species, along with the Hognose snake (Leioheterodon

madagascariensis) and both species of Boa constrictor (Acrantophis madagascariensis & Sanzinia

madagascariensis volontany), their success may be a result of being able to exploit a new and

abundant source of food. Many of their prey items, such as rats, insects and some species of gecko

and chameleon, proliferate in plantation habitats for various reasons and have drawn these species

into such areas. Similarly, the Panther chameleon may also benefit from the same circumstances as

a habitat edge specialist, the combination of open space, short vegetation and increased levels of

direct sunlight suit this species. Insects are also extremely abundant in most plantations allowing for

a large and accessible food source. Population expansions of the frog P. mascareniensis are believed

to be the result of a different selective advantage. Vences et al 2004 surmised that this species is

particularly able to exploit new habitats such as rice paddies, and essentially dominate them, due to

a physiological adaptation. The frogs are more resilient to saline water, and therefore can access and

breed in habitats which other frogs cannot (Glaw & Vences, 2004).

The way a species reacts to habitat change and human disturbance depends on not only their

physiological ability to adapt, but also to a complex web of ecological interactions. Combined these

can determine whether a species is able to persist in degraded environments. For example both the

tiny microhylid frog Stumpffia pygmaea and the pygmy leaf chameleon Brookesia stumpffi are

considered adaptable species common to both primary and secondary forests. However both species

are virtually absent from cultivated habitats. Their presence in an environment is dependent on a

thick layer of humid leaf litter (Vences & Andrenone 2004), within which the environment is

54

suitable for their survival. Humid leaf litter not only retains humidity, essential particularly for S.

pygmaea, but also provides refuge and is home to entire miniature ecosystem of invertebrates and

fungi. Such biotic factors are critical to the needs of every species, and the loss of any component of

a habitat will have some impact. Conditions such as the presence and depth of humid leaf litter,

invertebrate and fungal diversity, vegetation type, canopy height and cover, light level and habitat

complexity all interact to provide the essential variety of niches and microhabitats essential for

diversity to exist (Wells 2007).

With demand for forest clearance set to increase with the need for agricultural expansion and

development, specialist species such as Uroplatus henkeli, Gephyromantis horridus, Platypelis

milloti and Thamnosophis stumpffi will become increasingly threatened as suitable habitats become

fewer in number and those that do remain intact become more isolated. It is unclear whether or not

the population sizes of many species, thought to exist in low population densities contain enough

genetic heterogeneity to be considered viable. A lack of genetic diversity within a small population,

in a species restricted to a forest fragment on an island, suggests an inevitable outcome. However if

Lokobe is carefully and considerately managed as a conservation reserve in the future, its unique

diversity may well persist for a long time to come. Many of the species recorded in our study are

classified as data deficient according to the IUCN, and a list of each species and their current

conservation status is included in the Appendix.

3.5 The Black Lemur Project (Eulemur macaco macaco) Behaviour.

3.5.1 Introduction

3.5.1.1 Seed Dispersal:

The Black Lemur, (Eulemur macaco macaco) is distributed across the Northwestern tip of

Madagascar and the two adjacent small islands of Nosy Be and Nosy Komba. Recent estimates

presented by the International Union for the Conservation of Nature (IUCN) indicate that the

species is in decline and is currently listed as vulnerable to extinction. The main cause for their

decline is the continual destruction and fragmentation of their habitat, which is now restricted to

less than 20,000km² (IUCN, 2012). The remaining Sambirano humid forest of Lokobe remains a

stronghold for the Black Lemur, representing one of their last natural wild refuges, however the

species is relatively adaptable and also inhabits the surrounding secondary forests and agricultural

and plantation habitat mosaics (Bayart & Simmen, 2005, Garbutt, 2007).

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Figure 11 – A map showing the current range of the Black Lemur (Eulemur macaco macaco).

Black Lemurs are recognised as important seed dispersers within their home ranges, particularly of

native palm species such as the traveller palm Ravanala madagascariensis (Colquhoun &

Birkinshaw, 1998), an abundant species around Ambalahonko. One study conducted within Lokobe

Integral Reserve found the Black Lemur to be responsible for up to 88% of all dispersal within the

primary forest (Birkinshaw, 1999). There integral role in the propagation of the Sambirano forest

ecosystems makes them a species of great importance to the forests they inhabit, however they are

still subject to illegal hunting and are regularly collected for the pet trade (IUCN). The considerable

role the Lemurs play in dispersal within the Sambirano forests make them an essential part of the

ecosystem, and the continuation of the species in the form of a healthy and viable population will be

paramount in maintaining a healthy, diverse and functioning forest ecosystem. They may also be an

important propagator of the forest in times to come, helping regenerate degraded lands or by

facilitating the establishment of habitat corridors between disconnected and currently isolated forest

fragments.

During their study in 2005, Bayart & Simmen revealed that although the Black Lemurs inhabiting

regions outside of mature forest fragments persisted, the influence of human disturbance did have

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an affect on their behaviour. They discovered that the average group size, the size of the home

territories and their feeding behaviours were altered and were dependant upon the level of human

disturbance and the composition of the forest. Changes in behaviour have been widely associated

with environmental variation (Mertl-Millhollen et al, 2003) and responses such as the alteration of

feeding patterns, shifts in activity schedules and reduced group fecundity and fitness may be viewed

as a stress response to environmental degradation. The Black Lemur’s dietary habits and ability to

disperse seeds has previously been studied within primary Sambirano forests however their role and

potential for forest expansion and regeneration has not and remains unstudied.

In primary forest habitat Black Lemurs are known to consume over 70 species of fruit, of which 57

species are known to be subsequently dispersed (Birkinshaw, 1999). Fruit is known to make up

78% of the Black Lemurs natural diet (Rakotosamimanana et al, 1999) and is often supplemented

by flowers, leaves, fungi and some invertebrate species such as Cicada. However in secondary and

degraded habitats, the diversity of tree and plant species is often greatly reduced, leading to a

disparity in the variety and sometimes quantity and availability of food between the groups

inhabiting primary and degraded habitats. In this regard, the tree and plant diversity within a habitat

is directly linked to the extent of the role that Black Lemurs play in the ecosystem, which may be

particularly exaggerated in small forest fragments. By maintaining the maximum amount of

diversity within forest patches, and by managing agricultural lands with this is mind, cleared areas

with nearby forest fragments and Black Lemur groups living in them could potentially be

regenerated more rapidly than those which are cleared indiscriminately. The potential benefits

Black Lemurs could provide for habitat remediation is at present still unstudied however could be

useful in future habitat management schemes.

3.5.1.2 Activity Schedules

The Black Lemur (Eulemur m. macaco) is considered a cathemeral species, seemingly displaying

sporadic and random intervals of activity during both day and night, yet there is still much

speculation concerning the drivers behind their waking activity schedules. Current literature

describes a behavioural disparity between the populations of Black Lemur found on the mainland,

and those found on the islands of Nosy Be and Nosy Komba (Garbutt, 2007). A study conducted by

Andrews and Birkinshaw in 1998 described the resident population of Black Lemurs in Lokobe

Integral Reserve, as being totally inactive during the night throughout the dry season, and as having

their activity cycles dominated by nocturnal activities from October to December. It was postulated

that this was in response to the fruiting of certain tree species. In stark contrast however, the

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populations of Black Lemur studied on the mainland have been known to be predominantly diurnal

during those months (Colquhoun, 1996 and 1998). In 1995 Colquhoun reported that mainland Black

Lemurs showed both daily and seasonal rhythms of diurnal behaviour and increased nocturnal

activity was associated with the waxing and full moon lunar phases, as opposed to being in relation

to food availability (Colquhoun, 1995, Andrews & Birkinshaw, 1998).

It now appears that distinct Black Lemur groups display varying behavioural patterns and it is

possible that behaviours may be influenced by their immediate environment, meaning that human

activity or anthropogenic environmental disturbance may affect the activity patterns of this species

(Bayart & Simmen, 2005).

Over the forthcoming 3 month phase this study will become more focused and ambitious in its

scope, with the project effectively having a three pronged approach. The behavioural study of the

Lemur groups distributed within several habitat types, and along a gradient of habitat destruction

will become hopefully much more efficient with the arrival of 2-way radios. The study troops will

now also include captive specimens held in a 'public zoo' in Hell-ville, Nosy Be, the habituated

population residing on Nosy Komba and groups found in primary, secondary and plantation type

environments in the Ambalahonko area. Preliminary studies have taken place during this first phase

and trial behavioural data collection has began.

3.5.2 Aims

To determine whether there is a significant behavioural difference between groups of Black Lemur

as a result of anthropogenic habitat disturbance. Behaviours examined will include activity

schedules, time budgets and feeding ecology as well as other species specific traits which may

prove to be malleable under selective pressure, such as group composition, troop size, population

dynamics and feeding ecology.

To quantify the importance of the Black Lemur as a seed disperser within degraded areas of

Sambirano forest and their potential for forest regeneration.

To assess the vulnerability of different Black Lemur groups in relation to their habitat type and it’s

level of disturbance, by mapping out each Lemur troop in our area. This will hopefully allow us to

assess the abundance in different habitat types, and also to visualise and determine their territories.

This will then add to the protection of each group as we will be able to monitor each troops health

and status.

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3.5.3 Methodology

During this phase groups of Black Lemurs were located and observed within defined habitat

‘zones’, each of approximately the same area. The zones basically comprise of the merging of our

survey sites (see Table 2 and Plate 1) and include the areas connecting them. Zone 1 is a

combination of the 2 primary survey sites, 1 and 2 and the area between them, zone 2 consisted of

sites 3 and 4 and the forests distributed between them and zone 3, sites 5 and 6.

At least one trained Frontier staff member was present on every survey, and a maximum group size

policy of 3 members was strictly adhered too. Once a group of Black Lemurs had been discovered a

2-hour survey began and observations could start. If the Lemur group decided to move of their own

accord then we would track them as well as we could, depending on the density of the forest at

ground level, however if the group of Lemurs became disturbed, started vocalising and were clearly

agitated, then we left the troop and our survey ended at that point. When a group was first located, a

focus individual would be chosen at random, and the group composition would be carefully

assessed and recorded.

Behaviours were recorded and categorised using an Ethogram (Table 8) which was made during the

previous phase (MGF132) by Charlotte Daly, and edited recently to include more behaviours by

Sam Ferguson. During the last phase, the investigation was primarily a pilot study enabling us to

confirm and determine the behaviours displayed by the Black Lemurs and to catalogue basic traits

such as group size, group composition, habitat utilisation and their responses to disturbance. This

allowed us to adjust our survey methodology for this phase in order to minimise our impact upon

the study groups whilst still gathering useful data.

Table 8 – Ethogram of behavioural key used for the Black Lemur study. A copy of the current

Lemur Data sheet is included in the Appendix.

Black Lemur Behavioural Ethogram

Behaviour Description

Vigilance Guarding of the troop either when resting, sleeping or feeding. Usually performed by 1

individual.

Travel Movement through canopy was recorded and linked to any triggers. Fast and Slow travel

recorded separately.

Rest / Sleep Combination of resting and sleeping. Defined by 'eyes open' or 'eyes closed'.

Feeding Combination of foraging and eating (recorded separately).

Self Grooming Self cleaning and grooming.

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Allo-grooming Cleaning or grooming another Lemur.

Play Chasing, grappling etc.

Watching Observer Looking directly at the observer.

Social interaction Scent marking each other, greeting etc.

Vocalisation Any noises made e.g. grunts. Grunts and screams were interpreted differently and so were

recorded separately. Cause recorded if possible.

Out of Sight. Unseen and hidden from view.

Allo-mothering Not currently relevant as all young are now almost adult size. An adult mothering another

ones young.

Aggression An uncommon feature of Lemur behaviour, but interesting if observed.

Scratching Could be an important indicator of health. Could indirectly inform us about parasite

prevalence.

As the Lemurs were often found high in the canopy, binoculars were used to continuously monitor

the focus animal from a distance, reducing disturbance and allowing for accurate and detailed

observation. The behavioural category ‘watching observer' was introduced as a means of recording

our own impact on the Lemurs, in order to quantify our own levels of disturbance. Any visible

triggers which resulted in vocalisation, particularly alarm calls, were recorded, however if alarm

calls persisted for longer than 10 minutes with no obvious sign of a cause, the survey was ended.

For phase 132 observational surveys were conducted during the day light hours only, and between

the hours of 06.00 and 18.00. By spending so many hours observing and studying the Lemurs we

had ample to time observe and collect any scat which was dropped. Samples were collected using

latex gloves, and placed into plastic zip-lock bags with the age and sex of the Lemur, the habitat it

was found in and the time and date recorded on the bag. Soil was also collected from the area and

taken back to the Seed Nursery on camp. In the nursery each sample is dried and analysed. The

components of the sample are assessed, and the number of different seed species are counted and

recorded, as well as the number of seeds from each species. Seeds planted in the nursery are grown

in soil collected from the area in which the scat samples were collected in order to give as natural a

germination success rate as possible. Soil is first sieved to ensure that no other seeds are present

when the samples are planted, and the samples too are sorted, the seeds counted and identified

where possible and then planted together with the scat which acts as a natural fertiliser. Each

sample is planted in its own container, which is marked with a reference number that corresponds to

information recorded in a record book. Environmental data is recorded three times a day in the

nursery and growth rates of the seeds / saplings are monitored.

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The third part of our Black Lemur project is the mapping project, where we actively seek new areas

of forest, be it either primary or secondary and any un-surveyed degraded habitats searching for

new troops of Black Lemur. If successful we then record the troop size, sex ratio, the number of

adults, young and the type of habitat they are found within. A GPS location is also recorded and we

can then accurately plot the troop’s position onto a map obtained from Google Earth.

3.5.4 Results

A total of 40 hours of surveying during this phase has led to a total number of 10.4 direct observer

hoursbeing completed, with 8 hours of behavioural data collected for groups of Black Lemur found

in zone 2 and 8 hours for those found in zone 3, with just 2 hours of data collected for zone 1. The

behaviour was recorded between the hours of 6am and 6pm in each instance, spread out throughout

the phase. The results show that there was very little difference between the activity budgets for

troops observed within secondary and degraded habitats (zones 2 and 3) with the overriding activity

in both being a combination of resting and sleeping (excluding unseen). Feeding and foraging

behaviour accounted for 47 and 71 minutes of the 12 hour survey period respectively (Figure 12).

When compared to the data collected for the same group of Black Lemurs in zone 3 during the last

phase, where a total of 112 minutes (32% longer) of feeding and foraging were recorded it suggests

that more time was spent feeding during daylight hours in the drier period last phase. These results

suggest a dichotomy in terms of the time spent between feeding and foraging with season.

Figure 12 A - A breakdown of the time spent by Black Lemur groups on each activity, within

different habitat zones. Categories are amalgamated (Travel = Fast travel, Slow travel and

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stationary, Feeding = Foraging and Feeding, Rest = At rest or Sleeping, Grooming = Self

grooming or Allo grooming, Social = Play, Aggression or Interacting, Unseen = Out of Sight,

Vocal = Vocalising and Vigilance = On guard).

Figure 12 B - A breakdown of the time spent by Black Lemur groups on each activity, within

different habitat zones. Categories are amalgamated again, but data is standardised for surveying

effort.

A total number of 9 seed laden scat samples were collected in total with 5 being collected from

individuals in zone 2 and 6 from zone 3. In total, the number of species dispersed appears to be

greater in zone 2, with 19 distinguishable seeds species collected compared to 14 in Zone 3. Of the

11 samples which have been planted, 6 are showing growth, with 3 samples from each zone

beginning to grow. Currently all saplings are too small to identify with any confidence, with the

largest being 11cm in height and originating from secondary forest. At present, 18 saplings are

growing from the zone 3 samples whereas only 12 are showing any signs of development from zone

2.

The remaining 5 planted samples are yet to show any signs of development. Interestingly the

samples obtained from scats deposited in the degraded habitats (zone 3) have shown the quickest

growth rates, with 2 of the 3 growing samples germinating within several days of being planted. At

this stage of the seed dispersal project I have differed the use of statistical analysis until more

samples have been collected and analysed.

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3.5.5 Discussion

During our observations this phase we studied at least 9 distinct groups of Black Lemurs whose

territories at least partly fell within our 3 survey zones (primary and secondary forest and degraded

agricultural lands). Each of the troops were close to the standard range of group sizes of between 2

and 15 members (Garbutt, 2007), with the smallest group we documented having 6 members and

the largest exceeding the standard by one, at 16. The smaller group consisted of the semi habituated

Black Lemurs who inhabit the small forest fragment at site 6. This group, typical to all Lemur

groups we have observed this phase, consisted of male, female and large juvenile individuals, with

the 2 young group members now only slightly smaller than the adults, with a balanced sex ratio.

The largest group we encountered were located in secondary forest and totalled 16 observable

members, of which just 3 were female. Garbutt, 2007 suggested that the Black Lemur groups

contain roughly equal numbers of males and females plus associated offspring, so it is possible that

there were more males present but hidden from sight. Until more data collection has been carried

out we cannot compare group sizes between habitats confidently, however previous studies have

shown that larger groups are often associated with secondary and degraded habitats (Colquhoun,

1993).

During this phase, our reduced amount of direct observational hours is chiefly down to the changing

of season, and the end of the Mango season. This undoubtedly has changed the diet of all Black

Lemur troops substantially, and locating Lemur groups is now fairly taxing in comparison to the

previous phase. The Black Lemurs appears to have larger territories or ranges than we previously

thought and are now absent from previously frequented areas from areas. Causal observations of

one group of Black Lemurs in zone 3 showed intense nocturnal feeding behaviour at a flowering

kapok tree between the hours of 19.00 and 21.30. This behaviour was observed on four occasions.

These observations combined with the large proportion of time spent by the study groups either at

rest or sleeping during the day could suggest that the Lemurs are conducting a portion of their

activities during the hours of darkness. Andrews and Birkinshaw in 1998 conjectured that nocturnal

behaviour dominated over diurnal activity, particularly between the period ranging between August

to December and this activity mainly comprised of feeding and foraging. This study however was

conducted strictly in primary forest, within the Lokobe Integral Reserve, and not in any secondary

or degraded areas. The situation is complex though and the species is known to show behavioural

variation within their activity patterns (Colquhoun, 1996, 1998) and are able to adapt their

schedules to suit either a mostly diurnal or nocturnal existence.

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Variation in both habitat use and activity scheduling have been recorded in response to fruiting and

flowering trees (Garbutt, 2007) and the variation displayed during this phase in the absence of the

fruiting mango trees and combined with the observed nocturnal feeding activities support this. It is

likely then that Black Lemur groups inhabiting different areas, each with differing levels of

disturbance and therefore vegetation, will tune their activity patterns differently to one another, as

some territories will contain some food sources not present in others, resulting in change in habitat

utilisation and range. Through our observations it has become apparent that troops of Black Lemur

can adapt to, and tolerate the presence of humans in close proximity given that there is enough

forest cover and food for them to survive. One of our study groups, comprising of 6 Lemurs,

appeared to be tolerant of a high level of human interference and regularly endured intense

anthropogenic noise disturbance. The edge of their small territory (approx 150m2), and the region

with the tallest trees was situated around 5-55 metres from the busy village hub, indeed the village

presidents house no less.

However deforestation is much more detrimental to Lemur troops than noise alone, as it changes the

available habitat and reduces the overall amount of food trees available. It is likely that recent

deforestation had a detrimental effect on the number of lemurs observed around site 4 this phase

with fairly substantial levels of logging in the area, where previously Black Lemurs had been

observed resting, feeding and conducting social interaction. The forest patch at site 4 is now more

isolated as many of the adjoining trees have been felled, leaving access to the mature trees within

the site more difficult.

Our study also suggested that Black Lemurs preferentially utilise different vegetation types and

structures for different behaviours. For example it was clear through observation that the Lemurs

depended upon the older and taller trees within their territories for rest, social interaction and as a

safety retreat whenever a potential threat was observed. Both sexes slept at approximately 30m up

in the canopy, and whilst at rest, it was the males whom tended to do position themselves slightly

lower. New growth trees and vegetation were never observed being used for anything other than for

transitory purposes, mostly travelling between mature trees and fruiting Mango trees. This

dependency on mature trees and utilisation of secondary growth, within a mixed plantation habitat

was also found by Ganzhorn in 2005. Ganzhorn also found that without the secondary growth

patches within plantation habitats, Black Lemurs were absent. This suggests that the vegetational

complexity of a habitat has a significant impact on the Black Lemurs ability to persist within an

environment.

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The level of vocalisation this phase fell when compared to that of last phase, which was believed to

be the result of changes within troop dynamics, with young individuals now being more mobile and

subsequently more vulnerable. The cessation of the rainy season may also play a part in the

reduction in the levels of vocalisations, as it is believed that a lack of sleep making the troops tired

and again therefore more at risk. One theory also suggests that vocalisation may be used for

‘predator deterrence’ rather than to communicate an actual threat amongst the group (Fichtel &

Kappeler, 2002). Vocalisations were more easily triggered in the groups in both zones 1 and 2 and

the troops observed in primary habitats certainly issued vocalisations more frequently than those in

the other habitats. The fairly large disparity between the amount of time a study animal spent

classified as being 'Unseen' can be best explained both by the habitat type and behavioural

variation, as the forests in some parts within Zone 1 and 2 are extremely dense, with thick

vegetation and tall tree's, in contrast to the largely short and restricted type found in degraded

habitat. The higher proportion of both out of sight behaviour and vigilance were found within the

Zone 2 groups, and perhaps this could be explained in terms of cautious behaviour, with many

individuals choosing to avoid human contact. It is also likely that out of sight behaviour will be at

least as prevalent in the Zone 1 animals; however the data collected was possibly not sufficient to

show this trend.

The larger group sizes found in secondary and degraded areas could also be a result of the greater

abundance of food found in these regions because of the careful attention paid to such fruit trees by

humans. It may be that foraging in such areas is more efficient than in the primary forests. In effect

by managing the secondary forest, adjoining plantations or rice paddies, and by ensuring the success

of fruit trees for their own gain, human communities are also indirectly helping Black Lemur

groups. The group at site 6 again are potentially an example of this incidental success, with the two

couples successfully raising a baby each, despite inhabiting a territory with only a tiny fragment of

forest. This theory is further supported by the observation that groups in the dreaded habitats do not

appear to supplement their diet with Cicada's despite their massive abundance in the area. Contrary

to this, the groups observed in secondary forests spent a substantial proportion of their foraging time

catching and eating cicadas. The difference in diet between human impacted Black Lemur groups

currently appear to be providing more questions than answers and the project is looking to develop

further over the course of the next phase.

During the forthcoming phase the quantity of Lemur scat samples collected will hopefully be much

greater and stronger, statistically backed conclusions will be able to be drawn concerning how the

role of seed dispersal is being altered by human interference. The number and variety of seeds

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collected from each habitat zone, along with continual behavioural study should provide enough

evidence to draw solid inferences about how the continual modification of the forests surrounding

Lokobe Integral Reserve is affecting the population of Black Lemurs. All data for the Black Lemur

project will be analysed in its entirety at the end of the next phase.

3.6 The Impact of Habitat Degradation on the Diversity of Bird Species.

3.6.1 Introduction

Since the evolutionary appearance of the modern bird lineage, Madagascar has been a

geographically isolated island, separated from the nearest landmass, mainland Africa, by at least

200km of open-ocean (Morris & Hawkins, 1998). Despite its closer proximity to mainland Africa,

Madagascar was last connected to the Indian and Seychelles Gondwana land block 84m.y.a

(Plummer et al, 1995) and its unique bio-geographic history is evident when observing the native

bird fauna. Despite the islands continental size, the avifauna of Madagascar is considered

depauperate, or species poor with just 258 species (204 breeding species) when compared to other

landmasses of equivalent size (Reddy et al, 2012). Despite its low avian diversity, nearly half of the

species found in Madagascar are endemic (115 species) and are found nowhere else on

Earth,meaning the fauna is particularly significant and has high ecological value. Another very

striking feature of the Madagascan avifauna is the high degree of specialisation found within the

endemic lineages, most notably their dependence on forest environments, with 80 of the 115

endemic species (representing 37 endemic genera) being restricted to forest habitats (Morris &

Hawkins, 1998).

Considering the high rate of endemism in the Malagasy bird community, and the continued threat of

further deforestation and habitat degradation on the island, it is critical to monitor and assess each

community in order to define future conservation strategies (Dumetz, 1999,Watson et al, 2003). In

2005, Scott et al found that forest clearing in Southern Madagascar had a significant detrimental

effect on both the species richness and community structure of the bird inhabitants, resulting in a

decline in species richness of 26%. The study also reported a dramatic effect on community

structure. There remains a lot to be learnt about how different populations react to anthropogenic

disturbance; however it is generally negative for biodiversity and often results in declining species

diversity (Irwin et al, 2010). Coupled with the heavy pressure currently facing all native forest

types, the transformation of wetland areas across Madagascar is also extracting a heavy toll on the

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more specialised species, with the Alaotra Grebe (Tachybaptus rufolavatus) officially being

announced extinct in 2010.

With the forests depleted and the forest habitats being divided into reduced fragment sizes, the more

specialised, forest dependant birds are becoming less and less common. The once common

specialist forest endemics are quickly being replaced by the more generalist and widespread species,

whose populations are large and who are able to expand into new habitats quickly. This turnover of

species appears to be a common trait or result of anthropomorphic habitat destruction, with rare

species being replaced by common species and endemic species being replaced by non-endemic

species (Irwin et al, 2010). During this year-long monitoring project, we hope to assess the impact

of such habitat fragmentation within the Sambirano forests, collecting as much data as possible on

species distributions and the population status of as many bird species as possible. Our study will

also encompass a range of habitat types all positioned along a gradient of human disturbance,

allowing us to view the impact of habitat destruction on temporal and spatial scales.

3.6.2 Aims

To establish whether or not there is a difference between the bird communities found within

undisturbed, semi disturbed and degraded or altered habitats in the Ambalahonko area.

To continually monitor the abundances, species diversity and bird populations as they react to

anthropogenic habitat loss.

To contribute information concerning population status to countrywide conservation projects such

as Bird Life International.

3.6.3 Methodology

Point transects were conducted within 7 selected sites around the Ambalahonko region, with the

furthest site bordering the Lokobe Integral Reserve. The study uses the same 6 sites that are used in

the reptile and amphibian active searches, with the addition of a Mangrove habitat (site 7) (see

Table 2, Plate 1). Each survey lasted exactly 20 minutes and was carried out between the hours of

6-8am, 12-2pm and 4-6pm in order to record during peak bird activity times, and also to record a

broad spectrum of time with the idea of observing as wide a range of species as possible. Bird

observations were carried out 6 times a week, each time conducting 2 surveys at different sites.

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Each survey was led by a trained Frontier staff member familiar with birdcalls and songs and is able

to identify all of the local birds visually. The birds were recorded as being present in an area if they

were either seen or heard. The distance to either a visual or aural observation was also assessed and

recordings of observations made within 50m and over 50m were recorded separately. This

maximum recording distance was implemented to control for the 'openness' of sites which may

impart an unfair skew to the dataset. For analysis, when a species of bird was first seen or heard it

was designated a score, where the sooner the species was recorded, the higher the Index number.

This method can be used to record the relative abundance of a species within a habitat and allows

comparisons to be drawn between survey sites. A recording boundary of 50m was set and only birds

recorded within this range were assigned a score, to ensure fair comparison between sites with

dense vegetation where visibility is reduced and more open sites.

Due to survey time restraints, a score of 5 was assigned to a species observed within the first 4

minutes of the survey, 4 to a species recorded in the time period of between 4-8 minutes, 3 to those

recorded between 8-12minutes, 2 to between 12-16minutes and 1 between 16-20minutes. Any birds

species not recorded were assigned a score of 0. The research group on each survey consisted of

either 3 or 4 members (1 Frontier staff member and RA’s) with one person being given the role of

designated recorder while the rest were spotters. Data sheets were provided and a simply tally

system was used (see Appendix). Researchers remained silent during the entire survey period,

scanning with the naked eye before using binoculars to focus in on any birds seen for accurate

identification. Each site was surveyed 5 times in total this phase, with 3 early morning surveys each,

1 dusk survey and 1 afternoon survey. Any behaviour such as mating, nest building, feeding and

flying within a mixed flock was noted. Identification was aided by the use of the book The Birds of

Madagascar by Peter Morris.

3.6.4 Results

During this phase a total of 70 bird surveys were conducted, with 10 carried out at each of the 7

survey locations. An additional 3 sites have been successfully trialled for the beginning of the next

phase. For each site, 4 surveys were completed in the early morning, between 6.00am and 8.00m, 3

in the afternoon and 2 at dusk. The results this phase show a dramatic increase in the total number

of individual birds recorded compared to the previous phase, with 1,912 birds being recorded either

visually or aurally within 50m of the observers.. A total of 34 separate bird species were recorded

throughout the duration of the phase, making up 13.18% of the total Madagascan avifauna diversity.

Both site 7 and site 5, a plantation site and the mangrove habitat, had the highest species richness of

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all of the sites studied each with a species diversity of 22. The second most diverse locality was the

pineapple plantation, site 6 with 21 different species being observed, whilst the sites sharing the

third highest species richness were sites 1 and 4. Site 3 contained the lowest number of species,

with just 13 different species being recorded. In terms of habitat type, the degraded environments

held the highest amount of separate species (29) whilst the primary forest habitats and the

Mangrove site (site 7) both had a total number of 22 bird species. The secondary forest habitat

contained the fewest number of bird species (20).

Statistical analysis showed there to be no significant difference between the avian diversity between

the 7 survey sites (F=1.190, p=0.335) or within the 3 habitat zones (F=3.780, p=0.633). Similarly to

the previous phase, there is a fairly large disparity between the overall number of individuals

observed between the sites with a difference of 83 individuals between the secondary forests and

the degraded habitats. One-way Anova testing showed that there was a significant difference in the

mean number of birds recorded between the 7 sites (F=3.177, p=0.036), or between the mean

number of birds observed in each habitat zone (F=4.977, p=0.024).

The relative abundances of the 10 most common each species can be seen in Table 9. The

Madagascar Bulbul was the most commonly observed species, and was distributed fairly evenly

throughout all of the surveyed habitats, as was the Madagascar Red Fody, which was the second

most commonly observed species. The crested Drongo, which was the third most readily observed

species, appears to have a slight preference for open habitats over primary forest, yet was still well

represented in all environments. The Souimanga sunbird was evenly distributed throughout the 7

survey locations, whilst the Paradise Flycatcher showed a habitat preference for forest habitats,

particularly primary sites where it was most abundant. Further breakdown can be seen in Table 9.

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Figure 13 A+B- The total species diversity at each survey site and the diversity across habitat type,

indicating the effect of human disturbance and habitat degradation.

Figure 14 A+B - Graphs showing the total number of individuals birds recorded at each site (A)

and at each habitat type (The mangrove site is not combined with any other site).

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Table 9 - The relative abundances of the 10 most commonly observed birds, with their total scores

shown for each site.

Relative Abundances of 10 Most Common Birds

Species Site

1

Site 2 Site 3 Site 4 Site 5 Site 6 Site 7 Total RA

Madagascar Bulbul 34 32 38 44 47 37 39 271

Madagascar Red Fody 35 27 28 31 47 40 42 250

Crested Drongo 22 16 24 34 43 49 33 221

Souimanga Sunbird 36 27 36 46 33 25 40 207

Paradise Flycatcher 23 14 35 26 9 8 13 128

Madagascar Bee-eater 0 9 7 18 28 31 25 118

Madagascar White-eye 14 20 19 27 14 5 13 112

Common Newtonia 20 22 22 13 0 1 13 91

Madagascar Turtle

Dove

14 17 13 4 17 10 4 79

African Palm Swift 0 0 0 8 18 22 22 70

3.6.5 Discussion

With a total of 34 bird species (13% of Malagasy avifauna) being recorded during the second phase

of bird monitoring conducted by MGF on Nosy Be, the project appears to be highly successful. The

results from Phase 132 show a decline in species richness in the area, most likely caused by the start

of the Austral Winter and migrations; however we have seen an increase in the overall number of

individual birds. Firstly the data collected over the previous phase coincided with the Madagascar

cyclone season, running from December to March. It is likely that bad weather seriously detracted

from the number of birds observed during our surveys. Similarly it impacted upon our sampling

effort, with a reduced number of surveys being conducted during last phase. The decrease in overall

species richness is most likely to be due to migrations, either internally or continental, with species

such as the Broad-billed Roller already having moved to mainland Africa (Eurystomus glaucurus).

However the fact that no bird other than the Hook-billed Vanga (Vanga curvirostris) was found to

inhabit solely the primary, or even the primary and secondary forests, indicates that the forest

dependent specialist species may have already vacated the region and may have been forced back

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into the Lokobe Integral Reserve. This conclusion may be bolstered by the fact that no statistical

difference was to be found between the avian diversities across the three habitat zones. In contrast

to this, many more widespread and adaptable species were recorded only in the cultivated habitats,

particularly at site 5, the banana plantation, with an adjacent large clearing used for rice paddy

fields and zebu grazing. This area attracted many species such as the Green-backed Heron

(Butorides striatus), Squacco Heron (Ardeola ralloides), Dimorphic Egret (Egretta dimorpha) and

Cattle Egret (Bubulcus ibis), birds which are not found in forest environments but were undoubtedly

drawn to the large numbers of frogs and insects within the paddy fields.

Interestingly, the large flocks of Madagascar Mannikin which contributed hugely to phase 124's

data, and which seemingly disappeared during the last phase, have returned. At the beginning of the

phase none were observed but sporadically they have appeared and can now be seen in large flocks.

It may be that this species undergoes a seasonal migration to the central highlands or south of

Madagascar to escape the rainy weather. Conversely, the large numbers of Madagascar Red Fody in

breeding plumage have appeared to die down. In breeding season, which began at the very start of

our data collection for last phase, the males are extremely conspicuous, and this has likely

influenced their abundance in the data in comparison to some more secretive species.

Our findings also suggest that the most common birds in our survey are those with the largest

distributions, benefitting from the adaptable nature. The Bulbul's, Drongo's and Souimanga

Sunbirds are all highly adaptable species and are extremely common birds over their entire ranges.

It appear that their territories have expanded as the forests have been cleared, or as pathways are cut

into the forest, these species are able to exploit the new habitat edges, benefitting from forest

fragmentation. The type of habitat however obviously influences our observations, with more birds

being visible at sites where there is a large expanse of open habitat or sky to observe, as opposed to

within the dense forested site such as 1 and 2. Even when a maximum observational range was

introduced this effect is still clear. For example the species with the loudest calls may be accurately

represented for each habitat type whereas the quieter or silent species may be under-represented. At

times it was difficult to tell how far away a call was coming from, and at times calls may have been

recorded when the bird was actually outside of the study site. In part this was due to the fact that

some species, such as the Madagasacr Coucal (Centropus toulou) have very loud and distinct calls,

but also can be quite ventriloquial.

The ability to decipher and record bird species by call is extremely useful in Madagascar, with so

many species being forest dependant, uncommon and often shy,meaning it is often the only means

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of determining their presence. Continual training and learning will continue into the next phase as

there remain bird calls which we so far cannot recognise, particularly nearer the border of Lokobe

Integral Reserve. In conclusion, at this stage of the monitoring programme, it appears that the most

common species found in and around the Ambalahonko region are those which are capable of

adapting, and indeed thriving in deforested and human disturbed areas. However the forest

specialist birds appear to be almost entirely absent from the study, despite intensive recording

within apparently suitable areas.

3.7 - Small Mammal Project:

3.7.1 Introduction and aims

The terrestrial small mammal fauna of Madagascar comprises species from the Insectivora and

Rodentia (Garbutt, 2009). The majority of the insectivores belong in the endemic family Tenrecidae

and are all native rodents belong to the endemic subfamily Nesomyinae, yet both taxa are poorly

studied. Several species are known only from type specimens and modern distribution is very

poorly documented. However what known data does indicate is that species richness and the

greatest diversity is centred around the eastern rain forests (Carleton & Schmidt). According to

Garbutt, 2009 there are no small mammal species indicated as being present on the island of Nosy

Be. Our project aims to update the distribution maps for any small mammals present in the area.

3.7.2 Methodology

In order to sample the small mammal diversity in the surrounding areas of Lokobe Integral Reserve

we once again used our 6 carefully selected survey sites (1-6). We intended to sample the small

mammal communities within 2 primary forest habitats, 2 secondary forest habitats and two areas

which are used for moderate and subsistence agriculture, although whose land has been totally

transformed for this purpose (see Table 2 and Plate 1). However due to time restrictions during

Phase 131 we were only able to sample 1 secondary and 1 agricultural habitat, each with 5 repeats.

To sample the diversity of small mammals we used a series of 12 Sherman traps, a box style animal

trap designed for the live capture of small mammals. The traps were set in the early evenings and

checked once later that night after several hours had elapsed and again early the next morning. The

traps were baited with a mixture of peanut butter and whole peanuts, contained within a small open

container placed to the back of the Sherman trap. The traps themselves were set so that the closing

mechanism, once triggered would shut at around ¾ of the maximum speed.

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We carefully positioned the traps so that as many microhabitats, and habitat layers as possible were

sampled during each trapping period. Each site was then surveyed over a period of 5 nights. Site 6

was the first habitat to be sampled and we divided the 12 traps up into 3 groups of 4 and varied the

position of the traps as much as possible in an attempt to sample as broad a range of habitats as

possible. Four traps were positioned within the banana plantation, set both in amongst the leaves

(approximately 2m off the ground) and at the base of the trees. Four traps were positioned in the

pineapple grove, again with 2 traps set up in the larger open branched trees with the remaining 2 set

on the ground. The third groups of traps were set in a small fragment of forest situated next to the

banana plantation.

After a sampling period of 5 nights, the traps were removed and bought back to the research camp

for cleaning. They were then re-set at a different survey site. Group size during this project was

fixed at three, including one fully trained Frontier staff member and 2 RA’s. The second site to be

surveyed during Phase MGF131 was site 4, a secondary forest fragment in recovery after being

cleared approximately 18 years ago. It is still in close proximity to a small vanilla plantation plot

and is transected by a forest path which is regularly used by local villagers. At this site, 4 Sherman

traps were positioned within the vanilla plantation, 4 were placed in the secondary forest patch, on a

variety of mature and young trees and the third group were placed on the ground, amid the shallow

layer of leaf litter.

On capture, the animal was carefully emptied into a high-sided bucket with a lid which was quickly

put on, preventing the animal’s escape. Once the animal was calm the lid could be removed and the

animal observed and identified. Gloves were worn at all times during the removal and identification

phase of the investigation and identification was achieved by photographing the animal and

consultation of the book Mammals of Madagascar by Nick Garbutt back at the research camp. The

animals were always released as soon as possible and were released within their home ranges, as

near as possible to where they were captured.

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3.7.3 Results

Over the course of the phase, 12 Sherman traps, set over a period of 10 nights captured a total of 5

species and a total of 8 individuals over the 2 survey sites. The first phase of Sherman trapping, set

at site 6 captured a total of 4 individuals, with 3 different species being recorded. Trapping at site 4,

the secondary forest fragment (see Table 2 and Plate 1) also resulted in the capture of 4 individuals,

with a total number of 4 individuals being recorded, with 1 of each species. Table 10 shows the

results obtained this phase. This is an on-going project and requires more trapping at different sites

in order to obtain any meaningful comparisons.

The results show that four out of the five species captured and identified during this study were

invasive, with just 1 species, the Madagascar Pygmy Shrew (Suncus madagascariensis) being the

only native small Mammal caught. Capture rates during this initial investigation were surprisingly

low, with the trap success of 6.67% at both sites. All species were captured in low numbers, with

the Black Rat being the most common species caught. More repeats and a higher sampling effort

are required during the next phase to obtain a larger sample size, which is capable of providing

suitable statistical analysis. More sites also need to be sampled however the capture of 5 species is a

promising beginning, regardless of the low numbers captured.

Table 10 – The results of the Sherman trapping at site 6 and site 4. Results show that the majority

of individuals captured were invasive species.

Species Site 4 Site 6

Brown Rat (Rattus norvegicus) 1 2

Black Rat (Rattus rattus) 1 0

House mouse (Mus musculus) 1 1

Asian Musk Shrew (Suncus murinus) 1 0

Madagascar Pygmy Shrew (Suncus madagasciensis) 0 1

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3.7.4 Discussion

During our very brief surveying we have confirmed the presence of 5 species on Nosy Be, four of

which are introduced species (Rattus rattus, Rattus norvegicus, Mus musculus and Suncus murinus)

whilst one, the Madagascar pygmy shrew is a contentious species (Garbutt, 2009). Some authorities

describe this species as an endemic subspecies whilst others report it as being the same common

species which is widespread across the old world. An investigation of the initial immigration of the

shrew into Africa and Madagascar reported the species as being a definite species unique to

Madagascar (Hutterer & Trainer, 1990). The presence of the invasive species in the area is typical

of a village community and it is probable that they exist in very large numbers outside of the

primary forest. The extent to which these species have penetrated into Lokobe reserve and the

surrounding primary forest buffer zone is of great interest, as there is a possibility that other

endemic species exist in the region and therefore may be competing for resources. During the next

phase I propose to continue surveying different habitats across a disturbance gradient to determine

firstly whether there are any more species as yet un recorded for the area, and also to chart the

penetration of the invasive species into the primary forest.

3.8 The Butterfly diversity of the Ambalahonko Region

3.8.1 Introduction

Previous studies into Lepidopteron diversity and abundances have shown that habitat modification

and loss have significant detrimental affects (Bono et al, 2006). Butterflies are known to be good

indicator species as they are extremely sensitive to minor changes within their micro habitats and

especially so towards altered light levels (Kreman, 1992). They are therefore useful tools in

assessing and monitoring the levels of habitat degradation through forest clearance, reacting rapidly

to any changes in light concentrations associated with the loss of canopy cover (Steer & Vater,

2009). On the nearby Comoros Islands, a study conducted on the affects of habitat loss on the

Lepidopteron communities showed that more geographically widespread species replaced those

species which were more specialised and who had smaller distributions, in some cases restricting

their distributions further and forcing some species to become endangered (Lewis et al, 1998).

Such habitat modification and forest extraction is clear in the Ambalahonko region and although the

use of indicator species is in some cases contentious (Lawton et al, 1998), by surveying these taxa

along with the other vertebrate communities we should have a more complete overview of the effect

of deforestation in this important forest area. Butterflies are often used as indicator species as they

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are conspicuous, relatively easy to identify and survey, however Steel & Vater in 2009 suggested

that a broad guild approach is not particularly useful, and that specific and specialist groups such as

the Hesperiidae would be more enlightening.

3.8.2 Aims

The Ambalahonko area is a relatively un-studied area with previous work done here many years

ago. The primary aim of this project is to sample another layer of diversity in the area, adding to our

overall understanding of how deforestation, human disturbance and habitat modification is altering

the existing diversity. Secondarily, we hope to produce a modern-day species list of the region,

which can then be compared with the older study which was conducted here and look for any more

long term patterns in the Butterfly fauna. Biotic inventories such as this are often crucial for

conservation planning, forming the foundations of good management strategies. Such studies

provide critical data however conservation decisions are frequently made without surveys (Kremen,

1994).

3.8.3 Methodology

During this phase butterfly surveying was conducted merely by sweep netting. We surveyed several

sites with a high abundance of butterflies in order to become adept at catching and identifying them

without causing any damage. This is in preparation for the next phase where we aim to survey a

total of 12 sites, with 4 primary, 4 secondary and 4 degraded habitats. Each survey site will have

per-defined boundaries and surveys will be conducted over a period of 1 hour by a pair of

researchers. Identification will be achieved by means of an incomplete set of photographic plates

before the butterfly is released. Unfortunately an insect museum specialising in butterflies has

recently closed in Antananarivo, making the identification of any new species more difficult.

Although sweep netting is a commonly used method in butterfly surveying, it has its limitations.

The method is biased towards slow flying understory species, leaving the fast flying, canopy

dwelling species unlikely to be sampled (Molleman et al, 2006). During our proposed surveys, we

will set up baited canopy traps at each of the survey sites to assist with the capture of a diverse data

set. Any observations of large infrequently glimpsed species will be recorded if they can be

positively identified and seen during survey time. Environmental data will also be collected during

our surveys, and will later be combined with our disturbance data for each site.

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3.8.4 Results

During this phase long identification period, a total of 40 species were confirmed as being present

in the very near vicinity to MGF camp, with another 2 species which we have not yet been able to

identify with our current literature. A species list is given below in Table 11. The species recorded

so far shows both the Lycaenidae and Nymphalidae to be the dominant family's in the area, both

contributing substantially to the overall species diversity in the area.

Table 11 - A list of butterfly species captured and identified during MGF phase 132, assorted by

family.

Family Subfamily Genus Species

Papilionidae Papilioninae Papilionini P. grosesmithi

Pieridae Coliadinae Catopsilia C. thauruma

Pieridae Coliadinae Catopsilia C. florella grandidieri

Pieridae Coliadinae Eurema E. floricola floricola

Pieridae Coliadinae Catopsilia C. florella

Pieridae Coliadinae Eurema E. brigitta brigitta

Pieridae Pierinae Leptosia L. alcesta inalcesta

Pieridae Pierinae Colotis C. evanthe

Pieridae Pierinae Appias A. sabina confusa

Pieridae Pierinae Belenois B. antsianaka

Nymphalidae Heliconiinae Eurytela E. dryope dryope

Nymphalidae Heliconiinae Biblini B. anvatava

Nymphalidae Heliconiinae Acraeini A. ranavalona

Nymphalidae Heliconiinae Acraeini A. masamba

Nymphalidae Heliconiinae Acraeini A. eponina

Nymphalidae Heliconiinae Acraea A. stratiipodes albescus

Nymphalidae Heliconiinae Acraea A. andaramba

Nymphalidae Satyrinae Heteropsis H. turbata

Nymphalidae Satyrinae Strabena S. martini

Nymphalidae Satyrinae Henotesia H. narcissus fraterna

Nymphalidae Limenitinae Aterica A. rabena

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Nymphalidae Nymphalinae Junonia J. oenone epidelia

Nymphalidae Nymphalinae Junonia J. goudoti

Lycaenidae Lycaeninae Lampides L. boeticus

Lycaenidae Lycaeninae Actizera A. lucida

Lycaenidae Lycaeninae Euchrysops E. malathana

Lycaenidae Lycaeninae Lepidochrysops L. caerulea

Lycaenidae Lycaeninae Lepidochrysops L. grandis

Lycaenidae Lycaeninae Eicochrysops E. sanguigutta

Lycaenidae Lycaeninae Zizeeria Z. knysna

Lycaenidae Lycaeninae Chilades C. minisculata

Lycaenidae Lycaeninae Zizula Z. Hylax

Lycaenidae Lycaeninae Cupidopsis C. cissus

Lycaenidae Lycaeninae Pseudonacaduba P. scintilla

Lycaenidae Lycaeninae Pseudonacaduba P. sichela reticulum

Lycaenidae Lycaeninae Leptotes L. rabefaner

Lycaenidae Lycaeninae Leptotes L. pirithous

Hesperiidae Hesperiidae Borbo B. gemella

Hesperiidae Heteropterinae Hovala H. arota

Hesperiidae Heteropterinae Fulda F. imorina

3.8.5 Discussion

Although our sampling was relatively short term and only a trial at this stage, the Butterfly diversity

appears to be very high in the area. We only surveyed a total of 8 sites during this phase but we

found that the family's Lycaenidae and Nymphalidae dominated the fauna in the surrounding area in

terms of both species and overall abundance, particularly those Nymphalidae belonging to the

family Heliconiinae. The areas we surveyed in this phase were all degraded habitats with a large

amount of human disturbance, yet clearly they hold large species diversity with many species

apparently present in great abundance. The degraded areas were selected to make the training of

catching, manipulating in the net and identification of the butterflies simpler for those inexperienced

research assistants. To sample the area more thoroughly we intend to introduce a canopy trap

system, as our sweep net technique is biased to catching the slower, lower dwelling species.

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3.9 Bat Project

This phase we have been lucky enough to have the experience and passion of a Research Assistant

named Rebecca Wilson who has helped us to begin assessing the bat diversity in the local area.

According to the book the Mammals of Madagascar (Garbutt, 2008) there is only 1 species of bat

known to reside on Nosy Be (Emballonura tiavato). However with the use of a Magenta Bat 4

heterodyne detector, and by undertaking baseline surveys across 6 localities we can confirm the

presence of 5 echo-locating species in the area and from visual sightings at least 3 frugivorous

species, including 5 individual Pteropus rufous, the Madagascar Flying Fox.

Since Rebecca's arrival we have undertaken 12 surveys, with 8 surveys at dusk and 4 in the hours

just before dawn. With no data being presented in the book the Mammals of Madagascar with

regards to the frequencies used by, or even the inclusion of a photograph of Emballonura tiavato, it

is impossible to determine with any confidence whether or not we have sampled this species on our

surveys or not. Documentation of the frequencies we have observed are listed below. From

obtaining a photograph and through online research (bats.mampam.com) I believe that we may have

identified the species Miniopterus manavi, heard at 55-60KHz.

Miniopterus manavi is a relatively small species with a total length of just 55mm making it

distinctive, however its wing span is listed as unknown and so accurate identification is difficult

without capturing an animal. In the cases of the other species we have separated as potential

different species, we have used a combination of recording their echo location frequencies, noting

their habitat preference, the number of individuals in a group, feeding buzzes and lengths, flight

patterns, emergence times, size and coloration.

Frequencies Used:

15 KHz

28-30 KHz

55-60 KHz

70-75 KHz

90-110 KHz

Note: Feeding buzzes were heard in all species.

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The presence of Pteropus rufous is interesting, as 'scouting individuals' have been known to seek

out foraging sites as far away as 30km away from the main colony. This distance could potentially

place their colony on Nosy Tannikely (known roosting site) or even on mainland Madagascar.

However it is possible that there is a colony in Lokobe Integral Reserve. For the smaller species,

our limited data suggests that all species feed in the area, with notably shorter feeding buzzes heard

in close proximity to water and near to the rice paddy fields. Early estimations suggest that the

species using 30KHz frequency emerges immediately after sunset whilst the species heard at

75KHz, along with Miniopterus manavi appear before complete darkness.

With more detectors and the permission and equipment such as mist nets a more in depth

identification and abundance study could be undertaken, to fully assess and understand which

species are present in the area, and what role they play in the ecosystem.

4 Future of the Lokobe Reserve

As with the majority of reserves in Madagascar, the protected forest that makes up the Strict

Integral Reserve of Lokobe is out of bounds to anyone without the correct permit. The surrounding

forests are classified as a Madagascar National Park, forests where researchers with a lower level

permit can study, guided tourists can visit and local communities can obtain resources within a

quota. I agree with Andreone et al (2003), in that very careful management of the area is needed as

the reserve contains great species diversity and is one of the last undisturbed, low altitude

Sambirano forests.

The reserve is currently without any protection and illegal logging has increased markedly over the

past 6 months (unpublished questionnaire data). The CLB controlled forests within the MNP are

being decimated by over-exploitation and the spread of agricultural crops is rapid and extensive.

The guard posts situated on the border of the Integral Reserve have been abandoned for several

years and the community representative for the MEF has been absent from Ambalahonko for at

least 4 years. The community representative is supposed to aid the community and monitor and

control how the MNP forests are used, oversee their condition, and to maintain healthy forests.

Previous reports concerning the removal of precious woods, and the illegal collection of animals for

the international pet trade from within Lokobe Reserve have been made (particularly for species

such as U. henkeli and U. ebenaui), however I have not witnessed or heard anything about this

suggesting that the levels have dropped.

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The recent felling of a 5m wide swathe of forest, fragmenting and separating the Integral forest and

the community managed MNP forest, has recently taken place and now marks the border of the

Strict Integral Reserve. This action has been undertaken in the apprehension of a relaxing of the

forests protected status. With the parks unique forest habitat and great diversity it attracts a large

number of tourists and it is thought that allowing controlled access to at least parts of the Reserve

will help generate revenue and raise awareness of the importance of the area. The scheme is hoped

to further contribute to the sustainable management of Nosy Be’s natural resources (Andreone et al,

2003). However I believe that this is a controversial move, firstly due to the already small size of

the reserve and the well-studied responses of many species towards the current levels of human

disturbance in the area. I believe this would put added pressure on many already threatened species

and further restrict their populations. Secondly I believe that due to the apparent lack of funding,

resources and commitment to protecting the existing forests presently, I do not believe that reducing

the forests size will result in better management practices.

Awareness and appreciation of the environment must come through the channel of education, and

not by simply demonstrating that its exploitation can generate an income for a small section of the

people. Currently, environmental education in local schools informs pupils that the primary role of

the forest is to generate income, and therefore must be preserved (personal communication).

Investments should be made in environmental education, particularly in fields that are essential to

the regions future sustainability. A helpful curriculum would include advice on modern agricultural

practices and the importance of re-forestation. The human population is growing rapidly on Nosy

Be that will in time put further pressure on the reserve (Clark 2012). A large leisure tourism industry

already exists on the island and by degrading one of the last and most valuable Sambirano forest

fragments to cater for this seems in my opinion capricious. The current political system offers little

in the way of constructive or beneficial action plans, and their lack of interest in environmental

preservation should not go unnoticed. I believe that improvements to the current forests

management need to be made now, and if they are successful, sustainable and of no detriment to the

ecosystem then further small-scale developments for eco-tourism could be implemented in the

future.

Presently I believe a whole new approach to forest management in the area is needed, starting with

the repair and restoration of the existing forests. By reinstalling a community officer, answerable to

the MEF, into each community bordering the MNP, charged with restoring MNP forests and

managing them effectively would be a good starting place. Secondly, the installation of active

rangers at the guard posts will help protect both the forest itself from illegal logging and many

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threatened species from illegal collecting from the pet trade. It will also prevent trespassing and

therefore reduce the level of human disturbance within the park. Each of these three simple steps

would help protect the forests and their diversity, provide employment and safeguard future eco-

tourism, as currently the level of exploitation will degrade the eco-tourism experience and make it

unsustainable.

5 Proposed Science Programme for Next Phase:

5.1 Overview and Objectives of Next Phase.

The three main projects, ‘The Effect of Human Disturbance and Habitat Degradation on Reptile and

Amphibian Communities’, ‘The Role of the Black Lemur as an Important Seed Disperser outside of

the Lokobe National Park’, and ‘The Effect of Human Disturbance and Habitat Degradation on Bird

Communities’ are set to continue throughout the next phase (MGF133). The continual monitoring

of vertebrate communities in the area is essential for enhancing the clarity of any patterns which

may be developing, as habitats either recover from historic clearances or how they are being

affected by modern agriculture. It also allows us to observe any seasonal changes present in the

vertebrate communities that may otherwise go unnoticed and have affected conclusions drawn over

shorter surveying periods.

The forthcoming phase will also see the promotion of several previously subordinate projects to the

fore after the arrival of a new GPS device. The two other species of Lemur present in the area

(Hawk’s Sportive Lemur and Claire’s Mouse Lemur) will be studied and their abundances assessed,

along with other basic population descriptive’s and hopefully their dietary habits can be studied. A

habitat mapping project can now also begin, which will dramatically improve all of the data we

collect as each observation can then be plotted onto a map and more powerful conclusions can be

drawn not only about the habitat utilisation of each species, but which areas are of most ecological

value. With the Lokobe Integral Reserve soon to become an MNP we also have the chance to advise

which areas surrounding the park are of the most importance to the local biodiversity.

With the new GPS device at our disposal, we can now assess and plot the impact of forest clearance

and habitat degradation in the area, and this will hopefully help our assessment of the disturbance at

each of our survey sites. We are also hoping to analyse the level of pollution and contamination

present at each of our survey sites, but also the surrounding areas, by monitoring the pH of the soil

and waterways. A community project, in the form of questionnaires and interviews will also help us

83

to establish the scale of the human impacts upon the forests. We hope to uncover the extent to

which species such as the Panther Chameleon (Furcifer pardalis) are removed and sold into the

illegal pet trade, whether there is a bush-meat problem in the area and whether there is a problem

with illegal logging in the protected forests. It will also be very interesting to discover which

botanical species are of most use in the community, either for medicinal treatments or for the use in

construction, for the building of houses and pirogues.

An investigation into the diversity of butterflies and moths of the area surrounding Lokobe will

begin properly this phase as we now have the appropriate equipment to catch, identify and preserve

specimens. The photographic catalogue will also be expanded and over the next two phases we

hope to produce a modern species list. Ecological data will also be collected and hopefully some

blanks in the species life histories can be filled. Similarly a catalogue of Spider and Mantid

diversity in the area will be started, with habitats and localities also being recorded. The insect

communities are extremely diverse in this region and are certainly unmonitored with some species

potentially unknown to science.

Overall diversity will hopefully be assessed with regard to each habitat type and the impact of

habitat alteration or recovery can be viewed in terms of invertebrate diversity and abundance. We

are also hoping to have permits to survey within the Lokobe Reserve over a short period of time

now that the rainy season has ended. Surveys within the reserve would act as a true control and

could give useful insights on how the region and its diversity would have been historically, before

the onset of anthropogenic interference. We have also managed to obtain several permits to allow us

to collect specimens of amphibian and reptile for genetic analysis in Munich, working with the

esteemed Herpetologist Frank Glaw, who has requested the samples. It may be the case that the

species he has requested for voucher specimens may prove to be sub-species, restricted to Nosy Be.

I also will attempt to obtain a permit for the collections of butterfly species, again for genetic

comparison and in order to produce a butterfly guide to the local area. Both sets of specimens will

also require export licenses which I hope to be granted from the ANGAP office in Ambilobe.

84

6. Community Work and Public Awareness

Unfortunately it was not possible to have any feedback sessions with members of the CLB during

this phase. However this is an area that has been discussed in great detail and planning has already

begun for next phase. A community outreach day is currently planned to take place in

Ambalahonko village on the 28th June, just before the beginning of the new Phase. The aim of the

project is to engage with the local community, help them to understand exactly why we are based in

the village and to raise environmental awareness. It is necessary that we take a sensitive approach,

but it is important that we help the community to realise how important and special the wildlife in

their area is and attempt to install a respect for it, particularly within the younger generations. There

is a lot of enthusiasm for this event to take place, and currently the MGF Interns are leading the

project with help from higher staff and RA's.

7. Acknowledgements:

I wish to thank all members of staff for their hard work during this phase, particularly Charlotte

Daly, whose tireless passion for conservation is a constant source of motivation. Thanks also to all

the RA's for without whom the data could not have been collected. I particularly wish to thank

Zhichao Gao, Jack Parsonage and Patrick Ferguson for their commitment and enthusiasm for the

projects, and for no doubt improving each of our projects. Finally, I wish to thank Rebecca Wilson

for helping us to get started with Bat surveying in the area, with her passion for the work as well as

the amazing initial results encouraging us to hopefully set up a full scale monitoring project in the

area.

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9. Appendix

9.1 Avian Species List for Nosy Be:

White-tailed Tropicbird – Phaethon lepturus,

Brown booby – Sula Leucogaster,

African Darter – Anhinga ruff,

Lesser Frigatebird – Fregata ariel,

Squacco Heron – Ardeola ralloides,

Cattle Egret – Bubulcus ibis,

Green-backed Heron – Butorides striatus,

Dimorphic Egret – Egretta dimorpha,

Great Egret – Egretta alba,

Madagascar Fish Eagle – Haliaeetus vociferoides,

Madagascar Buzzard – Buteo brachypterus,

Frances’s Sparrowhawk – Accipiter francesii

Madagascar Kestrel – Falco newtoni

Helmeted Guineafowl – Numida meleagris,

Madagascar Buttonquail – Turnix nigricollis,

White-throated Rail – Dryolimnas cuvieri,

Lesser Sand Plover – Charadrius mongolus,

Whimbrel – Numenius phaeopus,

Greater Crested Tern – Sterna bergii,

Rock Dove / Feral Pigeon – Columba livia,

Madagascar Turtle Dove – Streptopelia picturata,

Namaqua Dove – Oena capensis,

Madagascar Green Pigeon – Treron australis,

Madagascar Blue Pigeon – Alectroenas madagascariensis,

92

Grey-headed Lovebird – Agapornis canus,

Madagascar Lesser Cuckoo – Cuculus rochii,

Madagascar Coucal – Centropus toulou,

Madagascar Long-eared Owl – Asio madagascariensis

Madagascar Scops Owl – Otus rutilus,

Madagascar Nightjar – Caprimulgus madagascariensis

Madagascar Palm Swift – Cypsiurus parvus,

Alpine Swift – Apus melba,

Madagascar Malachite Kingfisher – Alcedo vintsiodes,

Madagascar Pygmy Kingfisher – Corythornis madagascariensis,

Madagascar Bee-eater – Merops superciliosus,

Broad-billed Roller – Eurysomus glaucurus,

Madagascar Hoopoe – Upupa marginata,

Ashy Cuckoo-shrike – Coracina cinerea,

Madagascar Bulbul – Hypsipetes madagascariensis,

Long-billed Bernieria – Bernieria madagascariensis,

Hook-billed Vanga – Vanga curvirostris,

Chabert’s Vanga – Leptopterus chabert,

Madagascar Brush Warbler – Nesillas typical,

Common Newtonia – Newtonia brunneicauda,

Madagascar Paradise Flycatcher – Terpsiphone mutata,

Souimanga Sunbird – Nectarina souimanga,

Long-billed Green Sunbird – Nectarina notata,

Madagascar White-eye – Zosterops maderaspatana,

Madagascar Mannikin – Lonchura nana,

Nelicourvi Weaver – Ploceus nelicourvi,

Madagascar Red Fody – Foudia madagascariensis,

Common Myna – Acridptheres tristis,

Crested Drongo – Dicurus forficatus,

Pied Crow – Corvus alba.

9.2 IUCN Conservation Status

Category

Anurans

Ptychadena mascareniensis Least Concern

93

Heterixalus tricolor Least Concern

Rhombophryne testudo Vulnerable

Stumpffia pygmaea Vulnerable

Stumpffia psologlossa Data Deficient

Boophis tephraeomystax Least Concern

Boophis brachychir Data Deficient

Boophis jaegeri Vulnerable

Mantella ebenaui Least Concern

Gephyromantis horridus Endangered & Declining

Gephyromantis pseudoasper Least Concern

Gephyromantis granulatus Least Concern

Platypelis milloti Endangered & Declining

Cophyla phyllodactyla Least Concern

Cophyla occultans Data Deficient

Blommersia wittei Data Deficient

Mantidactylus ulcerosus Least Concern

Testudines

Pelusios castanoides Least Concern

Crocodylidae

Crocodylus niloticus Least Concern

Chamaeleonidae

Brookesia minima Vulnerable (Decreasing)

Brookesia ebenaui Vulnerable (Decreasing)

Brookesia stumpffi Least Concern

Calumma boettgeri Least Concern

Calumma gallus Endangered & Declining

Calumma nasutum Least Concern

Furcifer pardalis

Furcifer petteri

Least Concern

Vulnerable (Decreasing)

Gerrhosauridae (Plated

Lizards)

Zonosaurus madagascariensis Least Concern

Zonosaurus rufipes Near Threatened

Zonosaurus subunicolor Endangered & Declining

Zonosaurus boettgeri Vulnerable (Decreasing)

Scincidae

Trachylepis elegans Least Concern

Trachylepis gravenhorstii Least Concern

Trachylepis lavarambo Vulnerable

Cryptoblepharus boutonii Not Assessed

94

Madascincus polleni Least Concern

Amphiglossus alluaudi Vulnerable

Pseudoacontias unicolor Vulnerable (Decreasing)

Paracontias hildebrandti Least Concern

Gekkonidae

Geckolepis maculata Least Concern

Hemidactylus frenatus Least Concern

Hemidactylus mercatorius Least Concern

Hemidactylus platycephalus Not Assessed

Ebenavia inunguis Least Concern

Paroedura stumpffi Least Concern

Paroedura oviceps Near Threatened (Decreasing)

Uroplatus henkeli Vulnerable (Decreasing)

Uroplatus ebenaui Vulnerable (Decreasing)

Lygodactylus h. heterurus Least Concern

Lygodactylus

madagascariensis

Least Concern

Phelsuma madagascariensis Least Concern

uma abbotti Least Concern

Phelsuma seippi Endangered

Phelsuma laticauda Least Concern

Phelsuma dubia Least Concern

Phelsuma quadriocellata Least Concern

Boidae

Sanzinia madagascariensis Least Concern

Acrantophis madagascariensis Least Concern

Colubridae

Madagascarophis colubrinus Least Concern

Stenophis granuliceps Least Concern

Leioheterdon

madagascariensis

Least Concern

Alluaudina bellyi Least Concern

Langaha madagascariensis Least Concern

Micropisthodon ochraceus Least Concern

Ithcyphus miniatus Least Concern

Ithcyphus perineti Not Assessed at present

Pseudoxyrhopus microps Least Concern (Decreasing)

Pararhadinaea melanogaster Vulnerable (Decreasing)

Liophidium torquatum Least Concern

Liophidium rhodogaster Least Concern (Decreasing)

95

Bibilava stumpffi Vulnerable

Dromicodryas bernieri Least Concern

Dromicodryas quadrilineatus Least Concern

Mimophis mahfalensis Least Concern

Typhlopidae

Ramphotyphlops braminus Not Assessed at present

Typhlops madagascariensis Data Deficient

Typhlops mucronatus Data Deficient

Typhlops reuteri Data Deficient