Landscape patterns influence communities of medium-to large-bodied vertebrates in undisturbed terra firme forests of French Guiana

Abstract

Whereas broad-scale Amazonian forest types have been shown to influence the structure of the communities of medium-to large-bodied vertebrates, their natural heterogeneity at smaller scale or within the terra firme forests remains poorly described and understood. Diversity indices of such communities and the relative abundance of the 21 most commonly observed species were compared from standardized line-transect data across 25 study sites distributed in undisturbed forests in French Guiana. We first assessed the relevance of a forest typology based on geomorphological landscapes to explain the observed heterogeneity. As previously found for tree beta-diversity patterns, this new typology proved to be a non-negligible factor underlying the beta diversity of the communities of medium-to large bodied vertebrates in French Guianan terra firme forests. Although the species studied are almost ubiquitous across the region, they exhibited habitat preferences through significant variation in abundance and in their association index with the different landscape types. As terra firme forests represent more than 90% of the Amazon basin, characterizing their heterogeneity – including faunal communities – is a major challenge in neotropical forest ecology.

Full text

Landscape patterns influence communities of
medium- to large-bodied vertebrates in
undisturbed terra firme forests of French Guiana
Cécile Richard-Hansen 1*, Gaëlle Jaouen 2, Thomas Denis 1, Olivier Brunaux 3, Eric
Marcon 2 and Stéphane Guitet 4
Abstract
Whereas broad-scale Amazonian forest types have been shown to influence the structure of the communities of medium-
to large-bodied vertebrates, their natural heterogeneity at smaller scale or within the terra firme forests remains poorly
described and understood. Diversity indices of such communities and the relative abundance of the 21 most commonly
observed species were compared from standardized line-transect data across 25 study sites distributed in undisturbed
forests in French Guiana. We first assessed the relevance of a forest typology based on geomorphological landscapes to
explain the observed heterogeneity. As previously found for tree beta-diversity patterns, this new typology proved to be a
non-negligible factor underlying the beta diversity of the communities of medium- to large bodied vertebrates in French
Guianan terra firme forests. Although the species studied are almost ubiquitous across the region, they exhibited habitat
preferences through significant variation in abundance and in their association index with the different landscape types. As
terra firme forests represent more than 90% of the Amazon basin, characterizing their heterogeneity – including faunal
communities – is a major challenge in neotropical forest ecology.
Keywords
animal communities, diversity, environmental heterogeneity, French Guiana, landscape ecology, species-habitat associa-
tion.
1 ONCFS, UMR EcoFoG, BP 316, F-97310 Kourou, French Guiana.
2 AgroParisTech, UMR EcoFoG, BP 316, F-97310 Kourou, French Guiana.
3 ONF, Direction Régionale de Guyane, F-97307 Cayenne, French Guiana.
4 INRA, UMR Amap, TA A51/PS2, F-34398 Montpellier Cedex 5, France.
* Corresponding author: cecile.richard-hansen@ecofog.gf
Contents
Introduction 1
1 Methods 2
1.1 Study area: French Guiana 2
1.2 Animal abundance 3
1.2.1 Environmental characteristics of the study sites 3
1.2.2 Data analysis 3
2 Results 6
2.1 Structure of animal communities in various landscapes 6
2.1.1 Diversity of landscape communities 6
2.1.2 Characterization of landscape communities 7
3 Discussion 8
3.1 Landscape communities characteristics 9
3.2 Relevance of the landscape typology for communities of
medium- to large-bodied vertebrates 10
Acknowledgements 10
Literature Cited 10
Introduction
Although they are often iconic and well known to forest
dwellers, precise information is lacking on the distribu-
tion and ecological preferences of most vertebrate spe-
cies in neotropical forests. In central Amazonia, previous
studies revealed that the structure of communities of
medium- to large-bodied vertebrates varies according to
the two major forest types: seasonally inundated forests
(várzea) and terra firme forests (Haugaasen & Peres
2005a, b, 2008). According to these studies, seasonally
inundated forests appeared to be less diverse but carry
higher densities and biomass of primates compared to
the well-drained uplands (terra firme). However, at finer
geographical scale (i.e. within each category), the inher-
ent heterogeneity of these faunal communities remains
poorly documented, with the exception of some mainly
descriptive studies focused on primate communities
(Buchanan-Smith et al. 2000, Freese et al. 1982, Hey-
mann et al. 2002, Sussman & Phillips-Conroy 1995),
and a more recent and detailed analysis in western Ama-
zonia (Palminteri et al. 2011). According to these au-
thors, although hunting pressure and/or human impact
are often the best predictors of primate community struc-
ture, biogeographic and environmental factors also drive
community structure. The main descriptive parameter for
forest types was still flooded vs. unflooded areas, but this
parameter was refined as gradient. The same authors also
pointed out that the drivers may be more a combination
of environmental factors rather than any one factor.
In French Guiana, the whole territory was until re-
cently considered as apparently homogeneous terra firme
forest. However, recent research demonstrated the exist-
ence of several types of terra firme forest across Amazo-

Vertebrate communities in rain-forest landscapes —2/12
nia (Anderson et al. 2009) or within the Guiana Shield
(Fayad et al. 2014, Gond et al. 2011). Even in a regional
context where environmental gradients are quite weak,
as is the case of the Guiana Shield, the hyper-diversified
tropical rain forest shows a significant gradient of tree
composition and strong subregional patterns (Guitet et
al. 2015). The best factor identified to explain these
broad-scale patterns in the floristic and structural diversi-
ty of the terra firme rain forest was the geomorphologi-
cal landscape type (Guitet et al. 2013). In the Amazon
region, other studies have also linked geomorphological
landscape type with forest physiognomy (Anderson et al.
2009) and/or biological diversity or community structure
(Deichmann et al. 2011, Figueiredo et al. 2014, Som-
broek 2000). Such an integrative variable is thus a good
candidate to combine local ecological conditions and to
approximate forest structure and composition, but its
influence on vertebrate communities has never been
tested to date.
In French Guiana, abundance data on medium- to
large-bodied vertebrates revealed strong differences
across undisturbed forest sites (Richard-Hansen 2006).
This study scale is below that typically used for turnover
in most Amazonian large-vertebrate species, thereby
focusing the analysis of community heterogeneity on
niche differentiation and community structure (abun-
dances) rather than dispersal limitation and species re-
placement
(http://www.iucnredlist.org/mammals/data_types, , Pat-
terson et al. 2005). We therefore hypothesized that envi-
ronmental parameters and forest types can partially ex-
plain this heterogeneity in French Guiana, as document-
ed in other forested environments of Amazonia. The
influence of the landscape type on the forest structure
has been proved (Guitet et al. 2015), and the aim of the
present study was to assess the relevance of this classifi-
cation as an underlying driver of the distribution patterns
of the communities of medium- to large-bodied verte-
brates, with respect to its ability to describe the combina-
tion of local environmental factors.
1 Methods
1.1 Study area: French Guiana
French Guiana covers about 85000 km² in the east of the
Guiana shield between Suriname and the Brazilian state
of Amapa (4◦N, 53◦W). Altitude generally ranges be-
tween 0 and 200 m asl (mean 140 m asl) with few moun-
tain peaks exceeding 800 m. The climate is equatorial
with annual rainfall ranging from 3600 mm in the north-
east to 2000 mm in the south and the west, with a mean
annual temperature of about 26°C. The number of con-
secutive months with less than 100 mm precipitation
(dry season) ranges from two in the north to three in the
south with high interannual variation (Sombroek 2001).
Savannas and mangroves occur only in the coastal sedi-
mentary plain, while the evergreen rain forest covers
more than 90% of French Guiana (http://www.fao.org,
Guitet et al. 2015). Natural habitats show slight variabil-
ity and high species diversity, with a complex tree com-
munity and often more than 150–200 species ha-1 (Saba-
tier et al. 1997).
Figure 1: Location of 25 undisturbed study sites in French
Guiana, and their distribution within the five landscape types,
characterized from a geomorphological analysis based on a
digital elevation model.
Overall human density is below 3 inhab. km-2, and
75% of the population is restricted to the five major
towns, with the remaining population living in a few
small villages and settlements (http://www.insee.fr)
mainly along the two main rivers that form the borders
with Suriname and Brazil (Figure 1). A National Park
covers 34 million ha, 20 million ha of which comprise
the core area where only the resident population is al-
lowed to hunt for subsistence. Roads are limited to a less
than 50 km-wide northern coastal strip, while the rest of
the country is accessible only by boat or by small air-
plane from Cayenne to a few main settlements. Timber
harvesting and agriculture are contained in subcoastal
areas, covering currently around 2 million ha, close to
the biggest towns and main roads. Consequently, most of
the hunting pressure is applied on the northern coastal
strip, along main rivers and streams and around the scat-
tered villages.

Vertebrate communities in rain-forest landscapes —3/12
1.2 Animal abundance
Standardized line transect surveys (Buckland et al. 1993)
were conducted at 25 different study sites across French
Guiana. The study sites are very isolated and most can
be accessed only by helicopter or several days walking,
so we consider that there was no strong or recent hunting
pressure, even by autochthonous populations. The same
field design was implemented at each site, consisting of
four 3-km-long trails radiating from a central place
(campsite). This design makes it possible to account for
small local variations in the environment, including
topographic features or scattered resources (fruiting
trees), within a single global abundance index, character-
izing a similar area for each site surveyed. Transects
were walked at less than 1 km h-1 every morning (7h00-
11h00) and afternoon (14h30-18h00) by only one ob-
server per trail, systematically alternating transects on
consecutive days to avoid observer bias. All encounters
with focal species and their localization on the trail were
systematically recorded and the perpendicular distance
between the animal and the transect was measured to the
nearest metre with a laser range finder. Transects were
surveyed an average ± SD of 13.7 ± 1.9 times each,
during an 8-d field session. Total survey effort per site
ranged from 140 to 210 km (average ± SD = 163
± 17.7 km), with a cumulative survey effort of 4073 km
across 99 individual transects at 25 sites. The minimum
effort required for reliable estimates of abundance and
richness in this environment was estimated at 100 km
(de Thoisy et al. 2008). The surveys were all conducted
during the dry season (September-December) to avoid
interference with potential seasonal variation. Thirty-
seven species were recorded (mammals weighing
> 0.5 kg and large terrestrial birds), and diversity esti-
mates were based on this pool of species. For abundance
comparisons, we focused on the 21 most frequent spe-
cies, including primates, ungulates, caviomorph rodents,
large terrestrial birds (cracids, tinamous, trumpeters,
guans) and tortoises, for which reliable index of abun-
dance could be calculated. Tinamidae species (Cryp-
turellus spp. and Tinamus major) were grouped because
many observations lacked clear identification.
1.2.1 Environmental characteristics of the
study sites
The environment was characterized by the geomorpho-
logical landscape type defined by Guitet et al. (2013).
This typology was developed from a multi-scale geo-
morphological diversity analysis based on a digital ele-
vation model computed from a fine Shuttle Radar To-
pography Mission images (SRTM, 30 m resolution).
Variations in micro-relief defined 12 landform types
whose spatial distribution drew 82 different patches
classified in 10 landscape types that can be grouped
under five main categories: (1) coastal plain, (2) plateau,
(3) mountain, (4) multi-convex and (5) multi-concave
landscape. The joint-valleys are considered with the
multi-convex category (Guitet et al. 2013). Recent re-
sults showed that the structure and composition of the
forest is clearly influenced by these landscape types
(Guitet et al. 2015). Coastal plains (N = 2 sites in this
study), located in the northern part of French Guiana, are
lowland forests on Quaternary marine sediments. They
are characterized by a relatively low canopy (28 m in
height), high density of small trees, and relative high
abundance of Clusiaceae, Caesalpinioideae and Lecythi-
daceae. The plateau category (N = 8 sites) includes sev-
eral types of relatively flat relief of moderate elevation
dissected to a varying extent by rivers, exclusively cov-
ered by well-drained ferralsols with very localized hy-
dromorphic soils. Burseraceae, Mimosoideae and Caes-
alpinioideae are dominant tree families, but high abun-
dances of palms are also found. Small inselbergs are also
frequent. Sloping areas (N = 9 sites), locally called
mountains despite their modest altitudes (< 840 m asl),
are characterized by higher relief with many slopes. The
dominant forest type is characterized by a high canopy
(35-40 m), high basal-area values and the abundance of
very large trees, with high diversity and much more
infrequent families such as Vochysiaceae, Malvaceae
and Annonaceae being more abundant compared to other
forest types. The multi-convex landscape (N = 3 sites) is
dominated by more or less regular hills with a dense
hydrographic network, and dominance of Lecythidaceae
and Caesalpinioideae. The soil cover is more diversified
mixing clayic ferralsols with more sandy or loamy soils
acrisols. The multi-concave landscape (N = 3 sites) cor-
responds to large peneplains in the south, characterized
by very flat relief, covered by leached and partially in-
undated soils during the wet season, although the water
levels never rise as high as in the Amazonian várzea
forests. The canopy is low (30 m high) and discontinu-
ous, and vegetation is characterized by the dominance of
Burseraceae, Mimosoideae and Myristicaceae with rela-
tively few large trees and dense understorey with few
palms. Finding undisturbed sites was harder in some
landscapes types because of proximity of human settle-
ments (coastal plain) or difficult access (multi-concave
landscape), thus explaining the unbalanced sampling.
Six other broad-scale environmental variables were
also tested: the biogeographical region (Paget 1999), the
vegetation type based on remotely sensed landscape
classes (RSLC) from the VEGETATION sensor of the
SPOT-4 satellite (Gond et al. 2011), annual rainfall
(Meteo France, unpubl. data), the proportion of hydro-
morphic soils, the mean slope and the mean differences
in altitude for the area. The last three variables were
extracted from a digital elevation model computed from
fine-resolution Shuttle Radar Topography Mission imag-
es (SRTM, 30 m resolution). All these data were com-
puted for a circle with a 4-km radius encompassing the
survey transects.
1.2.2 Data analysis
Index of abundance of groups encountered per 10 km
walked (elsewhere referred to as encounter rate, sensu
Buckland et al. 1993) were calculated to control for
overall differences in sampling effort (Peres 1997). Per-
pendicular distances (PD) were recorded, but not enough
observations of each species were made at each site to

Vertebrate communities in rain-forest landscapes —4/12
correctly estimate the detection function for all of them
and hence to calculate densities. However, we assumed
that this index of abundance (hereafter, abundance) of
different species could be compared between sites be-
cause, except for agouti (Dasyprocta leporina), the dis-
tributions of the distances of observation were not statis-
tically different (ANOVA on log(PD), P > 0.5).
The dissimilarity between faunal communities in
different landscape types was first tested by permuta-
tional multivariate analysis of variance on the site
× species tables of raw counts of the 21 most common
species, using chi2 distance matrices. The Adonis test
was selected because it is more robust and less sensitive
to dispersion effects (within-group variation) than some
of its alternatives (ANOSIM, etc.) (Anderson 2001). We
also tested the pertinence of the landscape typology as an
potential explanatory variable in this variation using a
between-class correspondence analysis (BCA), which is
a particular case of correspondence analysis on instru-
mental variable (i.e. canonical correspondence analysis)
with only one categorical variable (Dolédec & Chessel
1989, Dray & Dufour 2007, Dray et al. 2012, Pélissier et
al. 2003). A correspondence analysis was first performed
on the site × species tables of raw counts of the 21 most
common species, and between-class analysis was then
performed on the results (site coordinates), with the
landscape type of each site as categorical variable. From
this analysis, the between-class inertia is the proportion
of total inertia of the table explained by the landscape
variable, while the within-class inertia is the proportion
of total inertia not explained by this variable. The statis-
tical significance of this portion of initial variance cap-
tured by this instrumental variable was tested with Mon-
te Carlo row permutation tests against the null hypothe-
sis of no relation between species assemblage and land-
scape type (Couteron et al. 2003). The same analysis
was made for the six other variables. These analyses
were performed with the ade4 (Dray & Dufour 2007)
and vegan-packages in R.
Diversity of communities and meta-communities –
Crude richness of a study site is the number of species
recorded during the survey, within the fixed maximum
of 37 focal species. We calculated the diversity profile
for each site community, and for each meta-community
created by pooling the sites belonging to the same land-
scape type. The diversity profile plots the value of Hill
numbers (Hill 1973) against the order of diversity q
(Kindt et al. 2006, Patil & Taillie 1982). Hill numbers
are the transformation of Tsallis entropy values into an
effective number of species, i.e. the number of species of
equal frequency that would yield the same diversity as
real data (Jost 2006). Tsallis entropy 𝐻
𝑞 (Tsallis 1988)
generalizes the classical indices of diversity in a parame-
terized measure, where the choice of the parameter gives
more or less importance to rare species: 𝐻
0 is the num-
ber of species minus 1, 𝐻
1 is Shannon’s entropy (Shan-
non 1948) and 𝐻
2 is Simpson’s index (Simpson 1949).
All values of diversity were corrected for estimation bias
(Marcon et al. 2014): the Chao & Shen (2003) estimator
applies to small values of q, that of Grassberger (1988)
to high values.
We tested the relevance of landscape type as a di-
versity predictor. We first pooled sites within one land-
scape type, and then pooled all landscape types together,
allowing the measurement of 𝛽 diversity across both
levels (Marcon et al. 2012). We tested the observed ratio
of 𝛽 diversity between landscapes over 𝛽 diversity with-
in landscapes against its distribution under the null hy-
pothesis of independence between sites and landscapes:
we shuffled sites among landscapes and calculated the
ratio of 𝛽 diversity 1000 times. A result of the test was
considered significant if the actual ratio was in the last
five percentiles of the distribution of the simulated val-
ues, showing that 𝛽 diversity between landscapes was
higher (relative to 𝛽 diversity within landscapes) than
under the null hypothesis. An alternative, more intuitive
test would address the ratio of 𝛽 entropies. Although it is
more similar to a classical analysis of variance (since the
total 𝛽 entropy is the sum of within and between land-
scape 𝛽 entropies), it suffers from the drawbacks dis-
cussed by Jost (2008). 𝛽 entropy is constrained by the
value of 𝛼 entropy, thereby invalidating the test. Diversi-
ty estimates and comparison were made with R package
entropart (Marcon & Hérault 2015).
Finally, we looked for species-landscape associa-
tions using the set of indices initially proposed by Du-
frêne & Legendre (1997) to study species assemblages
and habitat types. Our aim here focused on the relative
abundance of the 21 most common species occurring in
most sites rather than that of rare or indicative species.
Following De Caceres & Legendre (2009), we thus se-
lected the point-biserial correlation coefficient (rpb),
which is the Pearson correlation computed between a
quantitative vector (i.e. the vector containing the species
abundance values at the various sites) and a binary vec-
tor (i.e. the vector of site membership values) rather than
the better known indicator value index (IndVal). To
account for the unequal number of sites in the different
landscape types, we used the corrected group-equalized
index (rgpb), (De Caceres & Legendre 2009). The signifi-
cance of these associations was tested by Monte Carlo
permutation tests. We also tested the difference in spe-
cies abundance in sites belonging to one particular land-
scape compared to sites located in different landscapes
by permutation tests, after Sidak's correction for multiple
testing. We then considered whether combining basic
landscape types would better match species preferences
(De Caceres et al. 2010). It may also happen that a par-
ticular site group has no indicator or associated species
even if its sites have a community composition that is
clearly distinct from the sites of other site groups (De
Caceres et al. 2012). In these cases, the joint occurrence
of two or more species has a higher positive predictive
value for the site group than the two species taken inde-
pendently, so we also explored correlation values for
combinations of species (De Caceres et al. 2012). All
analyses mentioned in this section were computed with
the R package indicspecies.

Vertebrate communities in rain-forest landscapes —5/12
Table 1: Index of abundance (number of observations per 10 km) recorded for 21 species in 25 undisturbed sites in French
Guiana, and according to the different landscape types (MCV: multi-concave; MCX: multi-convex; PLA: plateau; PLN:
coastal plains; SLO: sloping areas). Abundance significantly higher or lower compared to all other sites: **: P ≤ 0.05;
abundance significantly higher or lower compared to other landscapes: ††: P ≤ 0.05 (permutation test, corrected P-value
for multiple comparisons).
General mean
± SD
Landscape
MCV
MCX
PLA
PLN
SLO
Primates
Alouatta macconnelli
(Linnaeus, 1976)
0.56 ± 0.30
0.71
0.42
0.61
0.45
0.52
Ateles paniscus
(Linnaeus, 1758)
1.19 ± 0.76
0.81
1.31
0.96
0.36
††1.66**
Cebus apella
(Linnaeus, 1758)
0.85 ± 0.46
0.96
1.04
0.61
1.69**
0.79
Cebus olivaceus
(Schomburgk, 1848)
0.24 ± 0.24
0.19
0.45
0.21
††0.00**
0.25
Pithecia pithecia
(Linnaeus, 1766)
0.06 ± 0.08
0.16
0.00
0.06
0.07
0.04
Saguinus midas
(Linnaeus, 1758)
0.41 ± 0.31
0.53
0.55
0.32
0.92
0.30
Saimiri sciureus
(Linnaeus, 1758)
0.04 ± 0.09
0.15
0.00
0.00
0.10
0.03
Ungulates
Mazama americana
(Erxleben, 1777)
0.43 ± 0.29
0.33
0.32
0.53
0.30
0.43
Mazama nemorivaga
(F.Cuvier, 1817)
0.44 ± 0.29
0.39
0.34
0.51
0.59
0.39
Pecari tajacu
(Linné, 1758)
0.29 ± 0.20
0.34
0.07
0.41
0.41
0.22
Tayassu pecari
(Link, 1795)
0.03 ± 0.06
0.02
0.00
0.02
0.00
0.05
Tapirus terrestris
(Linnaeus, 1758)
0.05 ± 0.07
0.00
0.06
0.04
0.07
0.06
Rodents
Dasyprocta leporina
(Linné, 1758)
1.48 ± 0.75
1.66
2.26
1.27
2.50
††1.11
Myoprocta acouchy
(Erxleben, 1777)
0.57 ± 0.33
0.72
0.50
0.52
0.65
0.57
Birds
Crax alector
(Linnaeus, 1776)
0.57 ± 0.33
0.33
0.48
0.60
0.49
0.66
Odontophorus gujanensis
(J.F. Gmelin, 1789)
0.31 ± 0.31
0.54
0.04
0.42
0.00
0.30
Ortalis motmot
(Linnaeus, 1766)
0.02 ± 0.07
0.13
0.02
0.01
0.00
0.00
Penelope marail
(S. Müller, 1776)
0.33 ± 0.17
††0.59**
0.11**
0.32
0.42
0.31
Psophia crepitans
(Linnaeus, 1758)
1.05 ± 0.66
1.44
0.87
0.97
1.29
1.01
Tinamidae
2.20 ± 0.89
3.33**
2.11
2.12
2.29
1.92
Reptile
Chelonoidis denticulata
(Linnaeus, 1766)
0.19 ± 0.17
0.45**
0.20
0.12
0.24
0.16

Vertebrate communities in rain-forest landscapes —6/12
Table 2: Analysis of variance between the communities of medium- to large-bodied vertebrates in 25 study sites in French
Guiana, according to seven environmental variables. Partial R-square from permutational multivariate analysis of variance
(Adonis test), tested with permutation test with pseudo-F. Between-class inertia from of a principal component analysis
with respect to the instrumental variable (PCAIV) performed on the coordinates of a correspondence analysis, tested by
Monte Carlo test. *: P < 0.05; **: P < 0.01; ***: P < 0.001
Landscape
Vegetation
type
Biogeography
% hydromorphic
soil
Mean
Slope
Difference
in altitude
Annual
rainfall
Partial R2
(Adonis test)
0.24**
0.17
0.15**
0.16***
0.14**
0.13*
0.12*
% between-
class inertia
0.24**
0.20*
0.15***
0.15**
0.14*
0.13*
0.13*
2 Results
Abundances of common species varied greatly across
French Guiana, even in areas with no strong or recent
human influence of hunting, logging or gold mining
(Table 1). Nine out of 21 species were present in each of
the 25 sites, 15 were present in at least 90% of sites
(more than 21) and 12 showed a null kilometric index
abundance at least once. These 12 species may be totally
absent from the site or present in densities that were too
low to be detected with our sampling protocol.
2.1 Structure of animal communities
in various landscapes
The permutational multivariate analysis of variance
(Adonis test) on animal communities according to the
various environmental variables showed that the propor-
tion of variance explained by the landscape variable was
the highest (R2 = 0.24), and significant according to
permutation test (Table 2). The between-class analysis
also revealed that 24.3% of the total inertia of the data
was explained by the instrumental variable of landscape
typology.
The Monte-Carlo row permutation test for this
unique environmental variable was significant (P
= 0.007). Moreover, the graphic representation of the
results of this between-class analysis showed that multi-
convex and multi-concave landscapes presented the most
distinct vertebrate assemblages, while plateau and moun-
tain communities were less clearly distinguished (Fig-
ure 2). The main structuring species are shown on the
graph, and their affinities with the various landscapes
were tested subsequently with the correlation index. All
the other environmental variables tested explained a
smaller proportion of total inertia with both analyses
(Table 2).
2.1.1 Diversity of landscape communities
For each individual site community, Simpson diversity
varied from eight to 16 effective species, and richness (q
= 0) estimated with Chao and Shen’s bias correction
(approximately equal to the Jackknife 1 or Chao 1 esti-
mators) was between 18 and 31 (Table 3). With a few
exceptions, the highest richness values corresponded to
sites in multi-concave landscapes and the lowest richness
values to sites in multi-convex ones, with values for
plains and mountainous sites between the two. Consider-
ing Simpson diversity, however, mountain sites were
among the lowest values.
Figure 2: Between-class analysis of the communities of medi-
um- to large-bodied vertebrates in 25 study sites in five land-
scapes types in terra firme forests of French Guiana. The ellip-
ses graphically sum up each landscape type (MCX = multi-
convex; MCV = multi-concave; PLA = plateau; SLO = sloping
areas; PLN = coastal plain) by covering 67% of the sites be-
longing to the landscape type; the centre of each ellipse is the
centre of gravity of these sites. Main structuring species are
indicated (Omo: Ortalis motmot, Ssc: Saimiri sciureus, Ppi :
Pithecia pithecia, Pma: Penelope marail, Pta Pecari tajacu,
Mam: Mazama americana, Cal: Crax alector, Apa: Ateles
paniscus, Col: Cebus olivaceus, Smi: Saguinus midas, Dle:
Dasyprocta leporina).
The beta diversity between landscape meta-communities
was significantly different (P < 0.05) from the beta di-
versity between random meta-communities for q values
of between 0.2 and 1.9. Common species were more
evenly distributed in the various landscapes, and were

Vertebrate communities in rain-forest landscapes —7/12
present everywhere: less common species made the
difference between landscapes; ignoring them (choosing
high values of q) made the test inconclusive. For small
values of q, a lack of power of the test was involved:
bias correction was more important, and so was the vari-
ance of the estimator of diversity.
Table 3: Main diversity indices, corresponding to three entropy
values (q), for the medium- to large-bodied vertebrate commu-
nities in 25 study sites in terra firme forests of French Guiana,
according to their landscape type. Values correspond to effec-
tive number of species. Landscape types: MCV = multi-
concave, 3 sites; MCX = multi-convex, 3 sites; PLA = plateau,
8 sites; PLN = coastal plains, 2 sites; SLO = sloping areas, 9
sites.
Diversity index
Site
Richness
(q = 0)
Shannon
(q = 1)
Simpson
(q = 2)
MCV.1
31.3
18.1
14.1
MCV.2
21.7
13.8
11.0
MCV.3
26.3
18.2
15.3
MCX.1
22.4
13.6
10.1
MCX.2
22.6
11.9
09.0
MCX.3
23.5
14.1
11.1
PLA.1
20.9
14.9
12.3
PLA.2
25.7
16.5
12.7
PLA.3
22.6
14.2
11.3
PLA.4
23.7
15.5
12.3
PLA.5
22.0
15.0
13.1
PLA.6
24.0
17.6
15.4
PLA.7
26.6
19.0
16.3
PLA.8
18.9
13.8
10.8
PLN.1
23.3
12.8
08.6
PLN.2
17.8
14.6
12.2
SLO.1
23.3
12.2
07.9
SLO.2
19.7
13.9
11.5
SLO.3
23.8
13.8
09.3
SLO.4
23.7
15.2
12.4
SLO.5
23.3
13.5
09.5
SLO.6
24.6
16.2
13.7
SLO.7
22.9
16.9
14.6
SLO.8
20.2
14.7
13.0
SLO.9
23.6
15.1
11.6
The diversity profiles of the five meta-communities
(𝛾 diversity) corresponding to the five landscape types
differed, whatever the order of entropy considered (0 ≤ q
≤ 2, i.e. from the number of species to Simpson diversi-
ty, Figure 3). The most diverse meta-community is en-
countered in the multi-concave landscape, despite the
small sample size in this category, and the least diverse
in the plain and multi-convex landscapes. Plateaux and
mountainous areas were intermediate in terms of diversi-
ty, the steeper-sloped areas were more diverse than plat-
eaux when rare species were considered (q = 0), and the
reverse when only common species were considered (q
= 2).
Figure 3: Gamma diversity profiles of the communities of
medium- to large-bodied vertebrates in the five landscape types
(MCX = multi-convex; MCV = multi-concave; PLA = plateau;
SLO = sloping areas; PLN = coastal plain), as estimated by
diurnal line-transects conducted in 25 non-disturbed study sites
in terra firme forest in French Guiana.
2.1.2 Characterization of landscape communi-
ties
The multi-concave landscape was positively associated
with the largest number of species (Table 4). Six species
had a correlation coefficient rgpb ≥ 0.5 for this landscape
category. Penelope marail, Ortalis motmot, Tinamidae
and the tortoise Chelonoidis denticulata were the most
characteristic species, and Saimiri sciureus and Pithecia
pithecia were the most typically associated primates.
Moreover, despite lower scores and no statistical signifi-
cance, four more species had their maximum correlation
coefficient in multi-concave landscapes (Alouatta mac-
connelli, Psophia crepitans, Odontophorus guyanensis
and Myoprocta acouchi). These results on association
tendencies between species and landscapes are con-
firmed by comparisons of abundance. The abundance of
S. sciureus, O. guyanensis, O. motmot, P. marail, C.
denticulata and tinamidae were significantly higher in
multi-concave landscapes than in other landscapes
and/or other sites combined (Table 1). In contrast, two
species had negative rgpb in these areas: Tapirus ter-
restris and Crax alector (rgpb = -0.4 and -0.3 respective-
ly) (Table 4). Finally, two of the three top-ranked sites in
terms of crude richness were also located in a multi-
concave landscape, and they also belonged to the three
top-ranked sites regarding total abundance (total abun-
dance, all species combined).

Vertebrate communities in rain-forest landscapes —8/12
Table 4: Association of 21 medium- to large-bodied vertebrate
species with five landscape types in French Guianan pristine
rainforest, as estimated by point-biserial correlation coefficient,
corrected for unequal sampling in different landscapes (rgpb).
MCV: Multi-concave; MCX: Multi-convex; PLA: Plateau;
PLN: Coastal plains; SLO: sloping area. Monte Carlo Permuta-
tion test: **: P ≤ 0.05; ***: P≤ 0.01
Landscape
MCV
MCX
PLA
PLN
SLO
Primates
Alouatta macconnelli
0.3
-0.2
0.1
-0.2
0
Ateles paniscus
-0.2
0.2
0
-0.5
0.5
Cebus apella
-0.1
0
-0.4
0.7
***
-0.2
Cebus olivaceus
-0.1
0.5
0
-0.5
0.1
Pithecia pithecia
0.5
-0.3
0
0
-0.1
Saguinus midas
0
0
-0.3
0.5
-0.3
Saimiri sciureus
0.5
-0.3
-0.3
0.2
-0.1
Ungulates
Mazama americana
-0.1
-0.1
0.3
-0.2
0.1
Mazama nemorivaga
-0.1
-0.2
0.1
0.3
-0.1
Pecari tajacu
0.1
-0.6
0.3
0.3
-0.2
Tayassu pecari
0
-0.2
0
-0.2
0.4
Tapirus terrestris
-0.4
0.1
0
0.2
0.1
Rodents
Dasyprocta leporina
-0.1
0.3
-0.3
0.4
-0.4
Myoprocta acouchy
0.2
-0.1
-0.1
0.1
0
Bird
Crax alector
-0.3
-0.1
0.2
-0.1
0.3
Odontophorus guyanensis
0.4
-0.3
0.2
-0.4
0.1
Ortalis motmot
0.6
-0.1
-0.1
-0.2
-0.2
Penelope marail
0.6
**
-0.6
-0.1
0.2
-0.1
Psophia crepitans
0.3
-0.2
-0.1
0.1
-0.1
Tinamidae
0.5
-0.1
-0.1
0
-0.2
Reptiles
Chelonoidis denticulata
0.6
-0.1
-0.3
0
-0.2
Cebus apella was clearly associated with coastal
plains (rgpb = 0.7, P < 0.05, Table 4). The abundance of
this species was significantly higher there than at all the
other sites combined, (Table 1) (P < 0.05). Saguinus
midas also reached its maximum levels in this plain
landscape. In contrast, Ateles paniscus and Cebus oliva-
ceus had their lowest and negative coefficient there (rgpb
= -0.5), and the abundance of C. olivaceus was signifi-
cantly lower than in other landscape types.
The associations between all species and the multi-
convex, mountainous or plateau landscapes were all
weaker, (rgpb ≤ 0.5), and none was statistically signifi-
cant. Cebus olivaceus was the only species showing
some association with multi-convex areas (rgpb = 0.5)
and a higher abundance than in other landscapes, while
nine species showed a negative association with this
landscape, among which most conspicuously Pecari
tajacu and Penelope marail (rgpb = -0.6) (Table 1). Ateles
paniscus tended to show a maximum association with
the mountainous landscape (rgpb = 0.5; abundance signif-
icantly higher than in other landscapes and other sites (P
< 0.05)), whereas Dasyprocta leporina and the small
primate Saguinus midas showed their minimum and
negative values in this landscape type (Table 1). The
abundance of D. leporina was significantly lower in
mountainous landscapes than in other landscapes (P
< 0.05) (Table 1). Mazama americana was the species
most associated with plateaux (rgpb = 0.3, and Cebus
apella the least (rgpb = - 0.4, Table 4).
Another analysis considered if combining land-
scapes matched species preferences better. Whereas
several species remained more strongly associated with a
single landscape type, some species turned out to be
more strongly associated with a combination of land-
scapes. Penelope marail and Saimiri sciureus appeared
to be associated with the combination of smoothed land-
scapes, i.e. multi-concave + plain (rgpb = 0.7, P < 0.05
and rgpb = 0.6, P < 0.1 respectively), Ateles paniscus
tended to be associated with the most hilly landscapes,
i.e. mountain + multi-convex (rgpb = 0.5) and Dasyprocta
leporina with the most northern landscapes, i.e. multi-
convex+ plain (rgpb = 0.6, P = 0.1).
Finally, another analysis looked for associations
between combinations of two or more species and vari-
ous landscapes. Multi-concave landscape appeared to be
characterized by a large multi-species community, main-
ly comprising birds (Odontophorus guyanensis, Penelo-
pe marail, Ortalis motmot, Tinamidae), the small pri-
mate Saimiri sciureus and the tortoise Chelonoidis den-
ticulata; the plateau landscape by the simultaneous
abundance of Pecari tajacu and Mazama americana, and
the multi-convex landscape by the combined high abun-
dance of Cebus olivaceus and Dasyprocta leporina.
3 Discussion
We found that the geomorphological typology of land-
scapes is a non-negligible factor driving the structure and
the beta-diversity patterns of medium- to large-bodied
vertebrate communities in terra firme forests in French
Guiana. The geomorphological landscapes combine
effects of geology, climate, relief and history in one
descriptive variable. As previously found for tree beta-
diversity patterns, this integrated parameter better ex-
plains the differences between animal communities than
some simple environmental parameters separately.
Habitat preference results in the disproportionate
use of some resources and/or conditions over others.
Habitat selection can be considered at various scales,
previously defined as four selection orders (Johnson
1980). At small spatial and temporal scales, animals
select different local resources or conditions. As both

Vertebrate communities in rain-forest landscapes —9/12
scales increase, these individual behavioural decisions
result in survival and reproductive performances at the
levels of individuals and populations. Over evolutionary
time, these habitat choices contribute to the species’
environmental niche or functional habitat (Gaillard et al.
2010). In the same way, De Caceres & Legendre (2009)
stated that the rgpb value, computed from relative abun-
dance, indicates the degree of preference of species for a
target landscape compared to the other landscapes, and
that ‘negative correlation values tell us when a species
‘‘avoids’’ the target site group’ (also referred to as ‘neg-
ative fidelity’ by phytosociologists). Following these
assumptions, we interpreted the higher abundance of
species in a particular habitat as a preference of this
species for this habitat, resulting in higher abundance.
Some species, as the howler monkey Alouatta ma-
connelli, appeared to be generalists or ubiquitous, and
were not associated with any particular landscapes. This
is consistent with other studies generally considering
howler monkey as a generalist plastic species, with a
varied diet (Julliot & Sabatier 1993, Simmen et al. 2001)
and few particular requirements (Lehman 2004,
Schwarzkopf & Rylands 1989). Some other species
appear to have more restricted distribution: Saimiri sciu-
reus were only detected in three study sites and Pithecia
pithecia in 12. This may be related to very special habi-
tat requirements leading to a true patchy distribution, or
to very low densities in the other sites, in both cases
denoting some habitat preferences although no signifi-
cant results were highlighted in this study. In contrast,
Cebus apella is a very common species encountered all
over the country, but our results showed a clear prefer-
ence for plain landscape type, in which they are particu-
larly abundant. Among birds, the smallest species are
characteristic of the low-altitude southern area, while
Penelope marail is more generally associated with all the
flat relief areas (northern plains and southern multi-
concave area). On the other hand, Crax alector appears
to favour steeper areas. In French Guiana, the distribu-
tion of Crax alector in various habitats and with respect
to environmental parameters has been analyzed more
precisely, showing a clear positive relationship between
C. alector densities and the mean slope of the prospected
site (Denis 2012).
Few species appeared really specialized, but alt-
hough most species taken separately do not demonstrat-
ed strong habitat preferences, their assemblages pro-
duced typical communities in the various landscapes
types.
3.1 Landscape communities charac-
teristics
The multi-concave forest type appears to be the preferred
habitat of a large set of species. These relatively low-
elevation forests also host higher diversities of both rare
and common species. We hypothesize that the lower and
fragmented canopy provides a better-lit environment,
with vertical strata and a greater diversity of niches. The
flat environment at lower elevations can also be consid-
ered as less constraining. However one site appears to be
quite different from the others with respect to most of the
parameters considered, in particular for its much lower
diversity. However, this site (the Waki basin) is also
considered to be a very particular forest habitat type, and
should probably be considered and characterized sepa-
rately (Guitet et al. 2013, 2015).
In contrast, the other landscapes were the preferred
habitat of only one or two species, and the 𝛼 diversities
of these sites were also lower. For example, the correla-
tion coefficients of all animal species with montane
environments were generally low, and very often nega-
tive, and only two species tended to be associated (Ateles
paniscus and Crax alector). The 𝛼 richness (q = 0) of
each mountainous site was rather low (20-24), even if
the estimated richness of the meta-community of whole
mountainous landscape (𝛾 diversity) was among the
highest, and was similar to that of the multi-concave
meta-community (32.8). These two results may indicate
that our mountain sample is rather heterogeneous (great-
er turnover), or that many less abundant species are
present in these environments, but were difficult to de-
tect and hence only randomly detected by our sampling
method. However, the larger number of study sites in
this category may also explain this higher 𝛾 diversity.
Cebus olivaceus and Dasyprocta leporina were the only
species to be positively associated with multi-convex
landscapes. These areas are generally characterized by
high abundance of the tree families Lecythidaceae and
Caesalpinioideae, and of several species of palm tree
(> 200 ha-1), which could explain the high abundance of
this rodent (Cid et al. 2013). As for mountainous or
multi-convex areas, few animal species clearly showed
preference for plateaux, but the combined abundance of
red brocket deer Mazama americana and the collared
peccary Pecari tajacu is nevertheless characteristic of
these environments. Like for mountainous areas, the
mean 𝛼 diversity was relatively low whereas the global 𝛾
diversity was higher (for q = 0), which could also be
linked with the large sample size in this category. More-
over, the definition of ‘plateau’ used in this study was
probably too broad, and combined habitats that were too
dissimilar. A finer-scale landscape typology identified
three different types of plateaux (Guitet et al. 2013), but
we lacked sufficient replicates to analyze the potential
differences in the vertebrate community in these subcat-
egories. In the same way, the two study sites considered
in this study in the ‘plain’ category are in fact quite dif-
ferent and belonged to different types in the finer typol-
ogy (Guitet et al. 2013). The coastal plain is the most
extensively inhabited and consequently hunted area (de
Thoisy et al. 2010), so finding replicates in undisturbed
localities is challenging.
In all cases, it should be kept in mind that the di-
versity values estimated here depend on the methodolo-
gy used, which mainly concerns the large diurnal species
potentially detected during line transects. Some taxa may

Vertebrate communities in rain-forest landscapes —10/12
be underrepresented by this method, particularly noctur-
nal species and felids.
3.2 Relevance of the landscape typol-
ogy for communities of medium-
to large-bodied vertebrates
Our results highlight the influence of broad habitat cate-
gories on medium- to large-sized vertebrate communities
in upland terra firme forests of French Guiana. An inte-
grative parameter, the geomorphological landscapes
proposed by Guitet et al. (2013), explains this heteroge-
neity better than most of the single parameters related to
it. This is congruent with the conclusions drawn by Pal-
minteri et al. (2011) that each environmental variable
examined appeared to contribute to some component of
the heterogeneity in primate communities in Peru, none
of them being an outstanding contributor. In some cases,
however, the geographical scale inherent to this classifi-
cation (and used in this study) may not match field reali-
ty. For example, a medium-sized valley within a larger
sloping environment was included in the mountain land-
scape category, whereas its faunal community was not
characteristic of this landscape type (low to medium
abundances of Ateles and Crax, for example). However,
the overall floristic composition of this particular site
matched the expected one better, according to the classi-
fication, than the faunal community (Guitet et al. 2015).
It is likely that the temporal and geographical scales of
these two biodiversity components differ. The vegetation
reflects long-term climatic and geomorphologic influ-
ences, whereas the large-fauna community should react
more rapidly to local conditions and present filter-
effects. On the other hand, some species presented affini-
ties with two different landscapes, which for them, prob-
ably share key environmental features. For example,
Penelope marail and Saimiri sciureus were associated
with both the multi-concave landscapes located in the
southern part of French Guiana and with the plains lo-
cated in the northern part. The common pertinent param-
eter may be flat relief and low elevations, independently
of other parameters. The landscape classification used
here permitted sufficient replicates within each type. A
finer classification exists, identifying 12 different land-
scape types instead of five (Guitet et al. 2013), including
three different forms of plateau, and three types of forest
in the coastal plains, but additional sampling is needed to
correctly analyze vertebrate assemblages at this finer
scale.
A priori classifications of structural habitats do not
focus on the meaning of the species distributions, with
respect to active habitat selection or to environmental
parameter selection by the different species. However, it
corresponds to the approach used when designing legis-
lation or policy to manage species in geographical space.
Although still rough, our results may help guide territo-
rial management of highly sensitive species, and help
analyze the impacts of hunting while accounting for
natural variation in abundance in various environments.
More generally, the geomorphological-based typology of
landscapes could be used in other countries and/or re-
gions to characterize and predict animal community
distribution throughout their territory. Coblentz & Riiter
(2004) already pointed out that topography plays a pri-
mary role in regional to continental-scale biodiversity,
and the landscape level is becoming more and more
popular in analysis and/or resource management (Ar-
royo-Rodriguez & Fahrig 2014, Bonnot et al. 2013,
Clark & Clark 2000, Hawes et al. 2012, Melo et al.
2013, Mockrin et al. 2011, Priego-Santander et al.
2013). The terra firme forests are generally known as
oligotrophic forests typically sustaining low biomass
densities of primates and other medium-sized to large-
sized vertebrates (Emmons 1984, Haugaasen & Peres
2005a, Palacios & Peres 2005). However, they represent
approximately 95%, of the Amazon basin (Palacios &
Peres 2005), so it is a major challenge to be able to char-
acterize their heterogeneity, including the faunal assem-
blages with which they are associated.
Acknowledgements
Funding was provided for many years by ONCFS,
and came from other external sources including Europe-
an Funds “HABITAT” and “CHASSE” programs,
French Overseas Ministry, French Ministry of environ-
ment (ECOTROP program), Parc Amazonien de Guyane
PAG, ONF Office National des Forêts, CNRS
Nouragues funds. EM and GJ and TD were supported by
an "Investissement d’Avenir" grant managed by Agence
Nationale de la Recherche (CEBA, ref. ANR-10-LABX-
0025). We are very grateful to all participants in transect
surveys, including ONCFS and PAG staff and some
hard-working and passionate volunteers.
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