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Article history: Forest fragmentation often causes biodiversity loss, but there is no consistent pattern on species' reactions. Con-
Received 24 February 2015 sidering the alarming rate of deforestation in the tropics, and the fact, that large areas of protected continuous
Received in revised form 11 June 2015 forest are limited, it becomes increasingly important to determine the biodiversity value of fragmented forests.
Accepted 9 August 2015
In order to investigate fragmentation effects on rainforest frogs in Madagascar and to assess the conservation
Available online xxxx
value of these fragments, we analyzed amphibian diversity in a continuous rainforest and nearby forest frag-
Keywords:
ments. We hypothesized that species richness is lower in fragments compared to continuous forest, and that frag-
Habitat fragmentation mentation leads to altered assemblage composition. We found no fragmentation effects on species richness,
Rainforest demonstrating that fragments may maintain local species richness comparable to continuous forest. The pres-
Amphibian conservation ence of streams was the most important factor for high species richness, independent of fragmentation status.
Species richness However, we detected fragmentation effects on species composition. As expected, several species were restricted
Species composition to continuous forest, but many species occurred in both forest types, and some species were only found in frag-
Disturbance ments. Rainforest amphibians in our study area were less sensitive to fragmentation than expected. Adaptations
to natural disturbances like cyclones could be one reason to explain this. However, as some species exclusively
occurred in continuous forest and species composition differed between continuous forest and fragments, we
conclude that fragments cannot substitute continuous forest blocs, but are generally important for maintaining
amphibian diversity in Madagascar, especially if they comprise streams. Forest fragments should hence be includ-
ed in conservation planning.
© 2015 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.biocon.2015.08.020
0006-3207/© 2015 Elsevier Ltd. All rights reserved.
708 J.C. Riemann et al. / Biological Conservation 191 (2015) 707–715
studies addressing amphibians so far revealed negative effects on their 2003). It provides most of the remaining rainforest habitat in the
diversity (e.g., Bell and Donnelly, 2006; Cabrera-Guzmán and Reynoso, Ranomafana region. The remaining forest fragments around RNP are
2012; Vallan, 2000). However, increased amphibian diversity in forest embedded in a matrix of cultivated land (slash and burn agriculture;
fragments has also been observed (Tocher et al., 1997). “tavy”), clear cut, and secondary bush and shrub vegetation. We chose
Madagascar is one of the world's biodiversity hotspots with an out- nine different forest fragments that range in size between two and
standing degree of endemism (Myers et al., 2000). Amphibian species 16.5 ha (Fig. 1, Appendix A). Five forest fragments comprise streams, in-
richness, including many so far undescribed candidate species, is cluding one fragment with two streams. Aerial photographs from 1950
expected to comprise up to 465 native and endemic species (Vieites showed that all but two of the studied fragments were separated from
et al., 2009). Madagascar's rich and unique ecosystems are threatened continuous forest by that time already and interviews with local people
by high rates of deforestation and the remaining forest cover is revealed that all studied fragments were at least 50 years separated
highly fragmented (Green and Sussman, 1990; Harper et al., 2007). A re- from RNP.
cent review of species' responses to anthropogenic disturbances in The Ranomafana region corresponds to one of the centers of am-
Madagascar revealed that overall very little is known and responses phibian diversity within Madagascar with almost 120 taxa known
differ even within lower taxonomic levels and between ecoregions (Glaw and Vences, 2007; Vieites et al., 2009; own unpubl. data).
(Irwin et al., 2010).
Our study aims to contribute to a better understanding of the response 2.2. Sampling design
of highly diverse tropical amphibian assemblages to habitat fragmenta-
tion for the implementation of future conservation strategies with special We determined species richness and composition on transects
emphasis on the conservation value of forest fragments. We examined distributed along streams and in terrestrial forest parts inside RNP and
patterns of amphibian diversity in a continuous rainforest and nearby for- forest fragments. We included stream and terrestrial habitats to equally
est fragments to reveal fragmentation effects on rainforest frogs in account for stream depending species (either semiaquatic or stream
Madagascar. A fragmented landscape where a relatively large continuous breeding) and for species that reproduce independent from streams
forest part that can act as control site is still present is an ideal model sys- (i.e., phytotelmata, pond or terrestrial breeders). As not all studied frag-
tem to learn about the value of forest fragments as amphibian habitats. In ments comprise streams, data from stream and terrestrial transects
particular, we compared species richness between forest fragments were analyzed separately. In the following, we refer to stream and ter-
(b 20 ha) and continuous forest (non-fragmented area of Ranomafana Na- restrial transects as habitat types, and continuous forest and forest
tional Park, N40,000 ha), and evaluated patterns of assemblage composi- fragments as forest types.
tion in both forest types. We investigated stream and terrestrial habitats We established a total of 38 independent line transects (50 × 2 m;
to equally account for stream depending species (either semiaquatic Marsh and Haywood, 2010): 22 transects were located inside RNP
or stream breeding species) and for species that are completely inde- (control sites) and represented continuous forest (terrestrial: 11,
pendent from running waters. We hypothesized for both habitat streams: 11), and 16 transects were spread over nine different forest
types that 1) species richness is lower in forest fragments compared fragments (terrestrial: 10, streams: 6). Following the sampling scheme
to continuous forest, and that 2) fragmentation leads to altered as- of terrestrial transects (searching a band of 2 m width), stream transects
semblage composition in forest fragments. included one meter riparian vegetation on each stream bank in addition
to the water body. Terrestrial transects were at least 50 m apart from the
2. Material and methods next stream. We kept a minimum distance of 200 m between transects
of the same habitat type, and stream transects had no direct upstream
2.1. Study system connections. Transects were geographically spread over RNP as far as
possible according to accessibility and logistic constraints to control
Field work was conducted in the Ranomafana National Park (RNP, for geographic distances between fragments and transects located with-
21°02′–21°24′S, 47°20′–47°35′E), East Madagascar, and in forest frag- in RNP. Transects inside forest fragments followed the topography of
ments located east of RNP (Fig. 1). RNP comprises 43,500 ha of continu- the respective fragment and were initially at least 50 m apart from the
ous mid-altitude montane rainforest (500–1300 m a.s.l.) with an annual next forest edge, except two stream transects that were about 25 m
precipitation between 1700 and 4300 mm (Wright and Andriamihaja, from the next forest edge.
Fig. 1. Schematic view of the study area and its position on Madagascar (insert). Shown are study sites (black stars) inside Ranomafana National Park (gray area; black line: park border)
and studied forest fragments (dark gray areas).
J.C. Riemann et al. / Biological Conservation 191 (2015) 707–715 709
We conducted standardized visual and acoustic transect sampling described in Ndriantsoa et al. (2013). We determined sequences at least
(Rödel and Ernst, 2004), visiting each transect nine times. Visual sam- once for species that could be identified by a distinct morphology.
pling was particularly useful for terrestrial leaf litter species, acoustic Concerning highly cryptic species (e.g. taxa of the subgenera Chonomantis
sampling was particularly needed for the sampling of arboreal species and Ochthomantis) and supposed undescribed taxa, barcoding was
and species calling from hidden places, such as tree holes, phytotelmata repeated for each transect sampling. Obtained sequences were com-
or dense leaf litter. Since the suitability of both methods differs between pared to published data on GenBank or own reference sequences (see
species, a combination of acoustic and visual methods is recommended Appendix B for collection and GenBank accession numbers).
to detect all major ecological guilds of frogs (Rödel and Ernst, 2004;
Vences et al., 2008). We may however have missed species with weak 2.3. Data analyses
calls inhabiting tree holes, Pandanus or Ravenala trees, if those habitats
where not present on or close to a transect. We refrained from using We compared species richness (absolute number of species detect-
drift fences with pitfall traps since this method is the least efficient ed) per transect between continuous forest and forest fragments for ter-
one for sampling rainforest amphibians (Rödel and Ernst, 2004; Rosa restrial and stream habitats using Wilcoxon rank sum tests.
et al., 2012). Drift fences with pitfalls are useful when particularly We further compared patterns of species composition between both
targeting fossorial species (Rödel and Ernst, 2004), but although well forest types. A reliable identification of the effects of fragmentation on
investigated, fossorial amphibian species are unknown from RNP species composition requires an understanding of spatial effects,
(Vieites et al., 2009). i.e., the spatial structuring of assemblages. Spatial turnover occurs at
After an initial training phase from February to April 2010, transects all spatial scales and species assemblages can be spatially structured
were sampled by two teams, led by JCR and NSH, each accompanied by even without a spatial environmental signal (Beck and Khen, 2007;
one assistant. All transects were sampled alternately by both teams to Ernst and Rödel, 2008). Since all transects representing continuous for-
avoid a potential observer bias. Forest types were sampled alternately est were located within the same connected forest patch, and due to
to avoid temporal effects on sampling results. Transects were sampled land-use patterns all studied forest fragments were located east of
during day and night as in the study area nocturnal as well as diurnal RNP (Fig. 1), spatial effects could not be ruled out. If spatial structuring
species occur (Glaw and Vences, 2007). Each transect was surveyed occurs, it can be difficult to disentangle fragmentation effects from
twice (once by day, once by night) between May and June 2010, spatial effects. We used Mantel tests to analyze whether differences
which corresponds to a drier period in the year. In 2011 all transects in assemblage composition among transects are related to spatial
were visited seven times (three times by day, four times by night), (i.e., geographic) distance. We tested correlations between composi-
from the beginning of the heavy rainy season in January until the drier tional differences and spatial distance among pairs of transects within
season in June. each forest type, i.e., within continuous forest and among fragments,
Visual sampling covered all visible individuals from leaf litter up to and across the whole data set. If correlations within forest types and
arboreal structures in approximately 2.5 m height and in addition the across forest types are different, this would support the hypothesis
aquatic habitat on stream transects. Transects were walked at constant that fragmentation effects exist and compositional differences are not
speed (approx. 2.5 m/min). We refrained from displacing logs and rocks caused by spatial distance alone (Ghazoul, 2002; Ramage et al., 2013).
and from pulling apart vegetation (e.g. Pandanus leafs) to keep distur- Distance matrices were calculated based on Bray–Curtis dissimilarities
bances of the study system as low as possible and to ensure equal sam- using species presence/absence data for compositional data and the
pling effort in all sites. All visually detected individuals were captured, Euclidean distance for spatial distances calculated from geographic co-
measured, sexed, marked via toe clipping (no functionally important ordinates of transects. Mantel tests were performed with function
toes, following the recommendations by Grafe et al., 2011) and identi- “mantel” from R package vegan (Oksanen et al., 2011) based on
fied by morphology in the field (according to Glaw and Vences, 2007). Pearson's product–moment correlation. P-values were obtained from
Afterwards, all individuals were immediately released at point of cap- 4999 permutations.
ture, except some individuals that were taken as vouchers (see We used non-metric multidimensional scaling (NMDS) to visualize
Appendix B). Visual transect sampling was interrupted for the duration and evaluate patterns of dissimilarity among transects based on their
of handling time and for acoustic sampling at four fixed points (start, species composition. The ordination was constructed from a Bray–
12.5 m, 25 m, 37.5 m). At each point we registered all calling individuals Curtis dissimilarity matrix using species presence/absence data. NMDS
in a 12.5 m distance straight, left and right for 5 min and identified them was performed with function “metaMDS” from R package vegan
to species level. The size of the acoustic transect was chosen according (Oksanen et al., 2011). This method uses random starting configura-
to the ability to determine each species' advertisement call, as calls tions to find a stable global solution. We then performed permutational
from greater distances cannot be precisely identified (Rödel and Ernst, multivariate analyses of variance (perMANOVA) (Anderson, 2001;
2004). Team members learned to distinguish the advertisement calls McArdle and Anderson, 2001) to test the hypothesis of differences in
during the initial training phase (according to Vences et al., 2006). In ad- species composition between continuous forest and forest fragments
dition, own reference data was recorded for several species with a Ro- for terrestrial and stream habitats. This non-parametric permutation
land EDIROL R-09 recorder and a Sennheiser MKE 400 microphone based variant of MANOVA partitions sums of squares of multivariate
(sampling frequency: 44.1 kHz, recording mode: wav 24 bit), including data equivalent to univariate ANOVA and the pseudo F statistic can be
previously unknown calls (see e.g. Riemann et al., 2012). The call re- calculated directly from any distance measure (Anderson, 2001). We
cordings are stored at the Institute of Animal Ecology and Conservation performed perMANOVA based on Bray–Curtis dissimilarities using spe-
at Hamburg University. cies presence/absence data with function “adonis” from R package
Voucher specimens were euthanized in a chlorobutanol solution, vegan (Oksanen et al., 2011). P-values were obtained from 999 permu-
preserved in 75% ethanol, and deposited at the Museum für Naturkunde tations. All statistical analyses were performed in R (R Development
Berlin, Germany (ZMB) and the Department of Animal Biology, Univer- Core Team, 2011).
sity of Antananarivo, Madagascar (UADBA). All toe clips were collected
as tissue samples and stored in pure ethanol for DNA barcoding (or 3. Results
dried and stored for further analyses). Barcoding, based on a fragment
of the mitochondrial 16S rRNA gene, was used to confirm identification 3.1. Species richness
to species level (Vences et al., 2005, 2008). We used primers 16SFrogL1
(CAT AAT CAC TTG TTC TTT AAA) and 16SFrogH1 (GAT CCA ACA TCG Transect sampling revealed a total of 57 species (Table 1) represent-
AGG TCG) of Vences et al. (2010) and followed the molecular protocol ed by 1026 individuals that were detected visually, complemented by
710 J.C. Riemann et al. / Biological Conservation 191 (2015) 707–715
Hyperoliidae
Heterixalus alboguttatus − − + + LC 3.2. Species composition
Heterixalus betsileo − + + + LC
Mantellidae
Aglyptodactylus sp. aff. madagascariensis (A. sp. 3) − − + − LC We detected 26 species that occurred in continuous forest and forest
Boophis albilabris − + + + LC fragments, but 31 species were found in only one forest type (17 species
Boophis cf. albipunctatus − − − + LC in continuous forest and 14 species in forest fragments; Table 1). Ac-
Boophis arcanus − − − + NA
cordingly, overall about two thirds (40) of the detected species occurred
Boophis calcaratus − − − + NA
Boophis elenae − + − + DD in forest fragments. Large and medium-sized microhylids of the genera
Boophis luciae − + − − NA Platypelis and Plethodontohyla were restricted to continuous forest,
Boophis luteus − + − + LC whereas small species of Anodonthyla and Rhombophryne occurred
Boophis madagascariensis + + + + LC in both forest types or only in fragments (Table 1). The species-rich
Boophis cf. majori − − − + NT
Boophis marojezensis − + − − LC
mantellid genera Boophis, Gephyromantis and Mantidactylus all
Boophis picturatus − + − − LC contained several species that were found in both forest types as
Boophis pyrrhus − − − + LC well as species restricted to continuous forest or forest fragments.
Boophis quasiboehmei − + − + NA Two of the three Guibemantis species were found in both forest
Boophis reticulatus − + − − LC
types, the other only in continuous forest. Thus, a distinct phyloge-
Gephyromantis asper + − − − LC
Gephyromantis boulengeri + + + + LC netic signal between inhabitants of continuous forest and fragments
Gephyromantis decaryi − + − − NT could not be observed (Table 1).
Gephyromantis enki + + + + DD Most of the species found in terrestrial habitats also
Gephyromantis plicifer + + − − NT occurred in stream habitats (Table 1). Only two species in each
Gephyromantis redimitus − + − + LC
Gephyromantis sculpturatus + + + + LC
forest type were restricted to terrestrial habitat (RNP: Platypelis
Gephyromantis tschenki + + + + DD tuberifera, Gephyromantis asper; fragments: Anodonthyla moramora,
Gephyromantis ventrimaculatus − − − + LC Aglyptodactylus madagascariensis). One of these species found only in
Guibemantis liber − + − + LC terrestrial habitat in fragments also occurred in stream habitat in con-
Guibemantis cf. depressiceps − + − − LC
tinuous forest (A. moramora).
Guibemantis tornieri − + − + LC
Mantidactylus aerumnalis − − − + LC We found a significant correlation between compositional differ-
Mantidactylus alutus − + − − LC ences and spatial distance in the whole data set for stream habitats
Mantidactylus betsileanus − + − + LC (r = 0.647, p b 0.0001) and terrestrial habitats (r = 0.465, p b
Mantidactylus femoralis − + − + LC 0.0001). We further detected a significant correlation between compo-
Mantidactylus grandidieri − + − + LC
Mantidactylus majori − + − − LC
sitional differences and spatial distance within continuous forest in both
Mantidactylus melanopleura + + − + LC habitat types (stream: r = 0.43, p = 0.011; terrestrial: r = 0.577, p =
Mantidactylus sp. aff. mocquardi (M. sp. 44) − + − + LC 0.003). However, we found no correlation between compositional dif-
Mantidactylus paidroa − + − − NA ferences and spatial distance among forest fragments (stream: r =
Mantidactylus sp. aff. betsileanus “slow calls” (M. sp. 28) − + − + NA
0.279, p = 0.112; terrestrial: r = 0.003, p = 0.478), showing that as-
Mantidactylus sp. aff. biporus “Ranomafana” (M. sp. 24) − + − + NA
Mantidactylus sp. aff. charlotteae “Ambohitsara” (M. sp. 9) − + − + NA semblages in fragments were not spatially structured. These contrasting
Mantidactylus sp. aff. charlotteae “Ranomafana” (M. sp. 13) − − − + NA patterns of spatial structuring in continuous forest and forest fragments
Mantidactylus sp. aff. cowanii “small” (M. sp. 48) − + − + NA
Mantidactylus sp. aff. mocquardi “Ambatolahy” (M. sp. 47) − + − + NA
Mantidactylus sp. aff. mocquardi “Namorona” (M. sp. 64) − − − + NA
Mantidactylus sp. aff. opiparis (M. sp. 58) + + − − NA
Mantidactylus tricinctus − − − + DD
Spinomantis sp. aff. fimbriatus (S. sp. 2) − + − + NA
Microhylidae
Anodonthyla boulengeri + + + + NA
Anodonthyla moramora + + + − DD
Platypelis grandis − + − − LC
Platypelis pollicaris + + − − DD
Platypelis tuberifera + − − − LC
Plethodontohyla brevipes + + − − EN
Plethodontohyla inguinalis + + − − LC
Rhombophyrne mierya − − + + NA
Rhombophryne sp. “Ranomafana”a (Stumpffia sp. 9) − − + + NA
a
RNP taxa formerly assigned to the paraphyletic genus Stumpffia, see Peloso et al.
(2015).
Fig. 2. Species richness per transect for stream (s) and terrestrial (t) habitats in continuous
2140 acoustic records. Generally, species richness was higher in stream forest (CF, gray boxes) and forest fragments (FF, white boxes). Shown are median, inter-
quartile range (box), and location of the minimum and maximum (whiskers). Species
habitats than in terrestrial habitats, independent of forest type. In con- richness was always higher in stream habitats. No differences in species richness
tinuous forest (RNP) a total of 43 species were detected, with 15 species could be detected between continuous forest and forest fragments, neither in stream
found in terrestrial habitat and 41 species in stream habitat. In forest (W = 20, p = 0.204, n = 17) nor in terrestrial habitats (W = 74, p = 0.183, n = 21).
J.C. Riemann et al. / Biological Conservation 191 (2015) 707–715 711
indicated that compositional differences were not caused by spatial dis- forest samples of the same habitat amount. We found that the same
tance alone but forest fragmentation affected assemblage composition. habitat amount (transect area) in forest fragments harbored equal
We found significant differences in species composition be- numbers of frog species than continuous forest. Our result thus indicat-
tween continuous forest and forest fragments in stream habitats ed that effects of fragmentation per se, i.e., the breaking apart of habitat,
(perMANOVA, pseudo F [1,15] = 6.38, p = 0.001) and terrestrial are weaker than expected and may have only minor effects on species
habitats (pseudo F[1,19] = 11.65, p = 0.001). NMDS revealed distinct richness, if any, compared to habitat loss (Fahrig, 2003). Therefore, all
patterns of dissimilarities in species composition between continuous remaining forest patches (independent of patch size) that still provide
forest and forest fragments in both habitat types (Fig. 3). The stress suitable habitat may have an important role in maintaining amphibian
value (0.146) of the final two-dimensional solution indicated a reason- diversity and should be considered in conservation planning.
able preservation of ordering relationships of the multidimensional The diversity of forest fragments may also highly depend on the
among-transect dissimilarities. Terrestrial and stream habitats were structure and usability of the matrix, as it might act either as corridor
separated along axis one, which was basically an effect of lower species or barrier for dispersal. Several species associated with forest habitat
richness in terrestrial compared to stream habitats in both forest types. are able to use some matrix habitats (e.g. Gascon et al., 1999). The vicinity
Forest types, i.e., continuous forest and forest fragments, were separat- to continuous forest areas, that harbor potential source populations, may
ed along axis two. As species richness was equal in both forest types in be also an important factor affecting species richness in forest fragments.
stream and terrestrial habitats respectively, this separation visualizes Thus, highly isolated fragments or fragments located in a more hos-
the significant differences in species composition between continuous tile matrix preventing potential source-sink dynamics might harbor
forest and forest fragments. less species than the originally forested area per habitat amount.
However, even small and isolated fragments can maintain popula-
4. Discussion tions of matrix avoiding species if they contain the necessary habitat
structures for reproduction (Dixo and Metzger, 2010).
Ongoing habitat loss and fragmentation are threatening the globally Important factors for the maintenance of amphibian diversity in for-
outstanding biodiversity of Madagascar (Allnutt et al., 2008) and today's est fragments are vegetation structure, structural heterogeneity and
protected areas might not be sufficient to protect all extant species in especially the availability of breeding habitats (Bickford et al., 2010;
the long-term. It is hence especially important to understand fragmen- Hillers et al., 2008; Pineda and Halffter, 2004; Vallan, 2000). In our
tation effects on biodiversity and assess the diversity and conservation study the presence of a stream was an important factor for high species
value of disturbed habitats (Irwin et al., 2010). richness, independent of the surrounding forest type. Surprisingly, this
We found no effects of forest fragmentation on species richness, also applied for species that are not directly stream depending, i.e., not
which was unexpected since the majority of fragmentation studies stream breeding or semiaquatic. Most of the species found in terrestrial
so far revealed negative effects on amphibian species richness habitats also occurred in stream habitats. Some species may depend on
(e.g., Bell and Donnelly, 2006; Bickford et al., 2010; Cabrera-Guzmán both habitat types, e.g., species that reproduce in streams but inhabit ter-
and Reynoso, 2012; Pineda and Halffter, 2004), including former studies restrial forest parts outside the mating season. Other species (e.g., direct
in Madagascar (Lehtinen and Ramanamanjato, 2006; Vallan, 2000). developers or microhylid species that reproduce in water-filled tree
These former findings mainly reflect patch size effects, being an impor- holes) may occur in the vicinity of streams by chance, as their distribu-
tant aspect of habitat fragmentation. It is well proven that patch size tion may not be affected by the presence of a stream. However, even
affects amphibian species richness as smaller fragments usually con- for those species that are not directly stream dependent the vicinity to
tain less species than larger ones (e.g., Bell and Donnelly, 2006; a stream could be important, as microclimatic factors may be influenced
Cabrera-Guzmán and Reynoso, 2012; Lehtinen and Ramanamanjato, by streams. Forest fragmentation can lead to higher temperatures, in-
2006; Vallan, 2000). Those species-area relationships are well creased wind speed and decreased relative humidity near edges in frag-
established and consistent through different taxa in forest fragments ments and hence changes in microclimatic conditions which affect many
in the tropics (Hill et al., 2011). Tocher et al. (1997) likewise revealed amphibian species (Lehtinen et al., 2003). Streams could buffer against
that amphibian species richness decreased with decreasing fragment microclimatic changes and hence forest fragments comprising streams
size, but found higher species richness in fragments than in primary are especially important for maintaining amphibian diversity.
Although species richness was not affected by forest fragmentation,
our results indicated that amphibian assemblages were influenced by
fragmentation. We found different patterns of spatial structuring in con-
tinuous forest and forest fragments, i.e., assemblages in continuous for-
est were spatially structured but assemblages in fragments were not.
Spatial structuring of species assemblages is a common pattern (Ernst
and Rödel, 2008; Hillers et al., 2008) and could hence be expected in
an intact system. The contrasting patterns of spatial structuring in con-
tinuous forest and forest fragments supported the hypothesis that frag-
mentation affected species composition and compositional differences
between continuous forest and forest fragments were not caused by
spatial distance alone.
As expected, some species were restricted to continuous forest hab-
itats. Large and medium-sized microhylids (genera Platypelis and
Plethodontohyla) seemed to react most sensitive to fragmentation as
they were never found in fragments. Small fragment sizes in our study
could be one reason. Vallan (2000) reported a minimum patch size of
30 ha for microhylids in the highlands due to unfavorable microclimatic
Fig. 3. Non-metric multidimensional scaling (NMDS) showing differences in species com- conditions in smaller fragments. However, small microhylids (genera
position between transects in stream (s) and terrestrial (t) habitats in continuous forest Anodonthyla and Rhombophryne) occurred in both forest types or even
(CF, gray triangles) and forest fragments (FF, white triangles) based on Bray–Curtis dis-
similarity index using species presence/absence data (stress = 0.146). Distances between
predominantly in fragments. A large body size has been identified as
transects in the two-dimensional NMDS plot represent dissimilarities in species composi- one trait associated with high extinction risks in frogs (Lips et al.,
tion. Transects are grouped according to forest and habitat type. 2003; Sodhi et al., 2008). Nevertheless, this was only true for
712 J.C. Riemann et al. / Biological Conservation 191 (2015) 707–715
Appendix A (continued)
(continued) Appendix B (continued)
(continued)
Fragment name Size Peri Dist RNP geographic SR t SR s Species Voucher number GenBank accession
[ha] [km] [km] coordinates
redimitus KT240669 - KT240671
Antaramanavana* 16.42 2.69 1.96 21°14′23.98″S, 5 18 Gephyromantis ZMB 81892, UADBA A 43137 - KT240429 - KT240434,
47°30′20.88″E sculpturatus UADBA A 43139, UADBA A 62087 KT240672 - KT240687
Sahadikaina* 16.52 3.53 2.54 21°14′47.98″S, 3 18 Gephyromantis ZMB 81895–ZMB 81896,
47°31″21.69″E tschenki UADBA A 43140, UADBA A
62088, UADBA A 64024
Gephyromantis ZMB 81897, UADBA A 62089 - KT240688 - KT240689
ventrimaculatus UADBA A 62090
Guibemantis liber ZMB 81901–ZMB 81906, KT240435, KT240692 -
Appendix B. Collection numbers of voucher specimens deposited UADBA A 43141 - UADBA A KT240694
at the Museum für Naturkunde Berlin, Germany (ZMB), voucher 43142, UADBA A 62091 - UADBA
specimens deposited at the Department of Animal Biology, University A 62094
of Antananarivo, Madagascar (UADBA), and GenBank accession num- Guibemantis cf.
depressiceps**
bers. Names in parentheses refer to candidate species according to Guibemantis ZMB 81912, UADBA A 43143, KT240437 - KT240440,
Vieites et al. (2009); * = RNP taxa formerly assigned to the tornieri UADBA A 62095 KT240695 - KT240699
paraphyletic genus Stumpffia, see Peloso et al. (2015); ** = species de- Mantidactylus ZMB 81913 KT240702 - KT240703
termined by their call only (determination according to Vences et al., aerumnalis
Mantidactylus KT240704 - KT240709
2006)
alutus
Mantidactylus ZMB 81914, ZMB 81916, KT240441 - KT240446,
betsileanus UADBA A 43147 KT240710 - KT240712,
Species Voucher number GenBank accession KT240714
Mantidactylus ZMB 81937–ZMB81938, KT240447 - KT240455,
Hyperoliidae
femoralis UADBA A 43163, UADBA A 62099 KT240715 - T240728
Heterixalus ZMB 81830, UADBA A 62096
- UADBA A 62100, UADBA A
alboguttatus
62114
Heterixalus ZMB 81832–ZMB
Mantidactylus UADBA A 43156, UADBA A 43161 KT240456 - KT240466
betsileo 81833, UADBA A 43144, UADBA
grandidieri
A 62097
Mantidactylus ZMB 81940–ZMB 81941,
Mantellidae
majori UADBA A 43157 - UADBA A
Aglyptodactylus ZMB 81834, UADBA A 43111 KT240397 - KT240403,
43158, UADBA A 64029 - UADBA
sp. aff. KT240630 - KT240634
A 64031
madagascariensis
Mantidactylus ZMB 81942–ZMB 81944 KT240467 - KT240471,
(A. sp. 3)
melanopleura KT240729 - KT240734
Boophis albilabris ZMB 81842, UADBA A 43117 KT240636
Mantidactylus sp. ZMB 81947–ZMB 81948 KT240531 - KT240538,
Boophis cf.
aff. mocquardi KT240845 - KT240857
albipunctatus**
(M. sp. 44)
Boophis arcanus ZMB 77315–ZMB 77316 JQ413974–JQ413975
Mantidactylus ZMB 81956–ZMB 81957, KT240472 - KT240485,
Boophis ZMB 81843–ZMB 81844, KT240637, KT240990
paidroa UADBA A 62103, UADBA A 62111 KT240736 - KT240771
calcaratus UADBA A 64013
- UADBA A 62112
Boophis elenae ZMB 81845, UADBA A 64015 KT240991 - KT240992
Mantidactylus sp. ZMB 81918–ZMB 81920, KT240497 - KT240530,
Boophis luciae ZMB 81847–ZMB 81850, KT240638 - KT240639
aff. ZMB 81922, UADBA A 43149, KT240700 - KT240701,
UADBA A 43119 - UADBA A
betsileanus “slow UADBA A 62104 - UADBA A KT240793 - KT240844
43120, UADBA A 62068, UADBA
calls” 62106
A 62070, UADBA A 62075
(M. sp. 28)
Boophis luteus ZMB 81851–ZMB 81853, KT240993 - KT240994
Mantidactylus sp. ZMB 81925, UADBA A 43160 KT240495 - KT240496,
UADBA A 62071, UADBA A 64017
aff. KT240788 - KT240792
Boophis ZMB 81854–ZMB 81856, KT240405 - KT240406,
biporus
madagascariensis UADBA A 43122, UADBA A 62069 KT240642
“Ranomafana”
Boophis cf.
(M. sp. 24)
majori**
Mantidactylus sp. ZMB 81927–ZMB 81930, UADBA KT240602 - KT240613,
Boophis ZMB 81863 KT240643, KT240995
aff. A 43145 - UADBA A 43146, KT240913 - KT240936
marojezensis
charlotteae UADBA A 43154, UADBA A 62110
Boophis ZMB 81867 KT240644 - KT240646,
“Ambohitsara”
picturatus KT240996
(M. sp. 9)
Boophis pyrrhus ZMB 81868, UADBA A 62074 KT240407 - KT240409
Mantidactylus sp. ZMB 81931–ZMB 81932, KT240486 - KT240494,
Boophis ZMB 81869–ZMB 81870,
aff. UADBA A 43153, UADBA A KT240773 - KT240787
quasiboehmei UADBA A 43125 - UADBA A
charlotteae 62098, UADBA A 62108 - UADBA
43127
“Ranomafana” A 62109
Boophis ZMB 81871–ZMB 81873, KT240997 - KT240998
(M. sp. 13)
reticulatus UADBA A 43123 - UADBA A
Mantidactylus sp. ZMB 81933, ZMB KT240571 - KT240583,
43124, UADBA A 64019
aff. 81935–ZMB 81936, KT241005 - KT241009
Gephyromantis ZMB 81878, UADBA A 43131, KT240410 - KT240414,
cowanii “small” UADBA A 43162, UADBA A
asper UADBA A 62081 KT240647
(M. sp. 48) 62113, UADBA A 64037 - UADBA
Gephyromantis ZMB 81879–ZMB 81883, KT240415 - KT240423,
A 64039
boulengeri UADBA A 62082 - UADBA A KT240648 - KT240659,
Mantidactylus sp. ZMB 81949–ZMB 81951, KT240539 - KT240570,
62084 KT240999
aff. ZMB 81953–ZMB 81954, KT240858 - KT240896
Gephyromantis ZMB 81884 KT240660
mocquardi UADBA A 64040 - UADBA A
decaryi
“Ambatolahy” 64041
Gephyromantis ZMB 81885–ZMB 81889, KT240424, KT240661 -
(M. sp. 47)
enki UADBA A 43134 - UADBA A KT240665
Mantidactylus sp. ZMB 81952, UADBA A 62115 KT240600 - KT240601,
43136, UADBA A 62085 - UADBA
aff. KT240909 - KT240912
A 62086
mocquardi
Gephyromantis UADBA A 43132 KT240425, KT240666 -
“Namorona”
plicifer KT240668
(M. sp. 64)
Gephyromantis KT240426 - KT240428,
714 J.C. Riemann et al. / Biological Conservation 191 (2015) 707–715
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