Animal Conservation.

Print ISSN 1367-9430

Defaunation and biomass collapse of mammals in the

largest Atlantic forest remnant
M. Galetti1,2, C. R. Brocardo1, R. A. Begotti1, L. Hortenci1, F. Rocha-Mendes1, C. S. S. Bernardo1,
R. S. Bueno1, R. Nobre1, R. S. Bovendorp1, R. M. Marques1, F. Meirelles1, S. K. Gobbo1, G. Beca1,
G. Schmaedecke1 & T. Siqueira1
1 Departamento de Ecologia, Instituto de Biocie^ncias, Universidade Estadual Paulista (UNESP), Rio Claro, Brazil
2 Section for Ecoinformatics and Biodiversity, Department of Bioscience, Aarhus University, Ny Munkegade 114, DK-8000 Aarhus C,
Denmark

Keywords
Brazilian Atlantic forest; hunting; line-transect
method; distance sampling; extinction risk;
protected areas; defaunation; mammalian
communities.
Correspondence
Mauro Galetti, Departamento de Ecologia,
^ncias, Universidade
Instituto de Biocie
Estadual Paulista (UNESP), CP 199, 13506-
900 Rio Claro, SP, Brazil.
Email: mgaletti@rc.unesp.br
Editor: Res Altwegg
Associate Editor: Goncalo Ferraz
Received 08 February 2016; accepted 13
September 2016
doi:10.1111/acv.12311
Abstract
Large continuous rainforests are the main hope for sustaining the population of
large-bodied vertebrates that cannot cope with fragmentation or unsustainable hunt-
ing. The Brazilian Atlantic forest is considered a biodiversity hotspot and although
highly fragmented, it still contains large forest patches that may be important for
the conservation of mammals that require large areas. Here, we estimated species
richness, density and biomass of medium- and large-sized mammals along the lar-
gest remnant of the Atlantic rainforest, Brazil (the Serra do Mar bioregion), an esti-
mated area of 8000 km2. We recorded 44 species based on 4090 km of diurnal
line transects and camera traps, animal tracks and interviews in 11 continental
regions and two large land-bridge islands. We found high levels of similarity in
mammalian composition between pairs of sites in the continental forest sites (0.84
1), but much lower similarity between pairs from the continental forest sites and
the two large land-bridge islands (0.290.74) indicating potential local extinctions
or poor dispersal of continental mammals to these islands. In addition, we found
that the density and biomass varied 16- and 70-fold among sites, respectively.
Mammalian biomass declined by up to 98% in intensively hunted sites and was
53-fold lower than in other Neotropical non-fragmented forests. Although this large
forest remnant is able to maintain a high diversity of medium- and large-bodied
mammal species, their low density and biomass may affect the long-term persis-
tence of these populations and the ecosystem services they provide.

loss because small-bodied species may be favored once

Introduction
Natural habitats worldwide are suffering from animal species
loss and population decline, particularly on large-bodied ver-
tebrates (Galetti et al., 2013; Dirzo et al., 2014). This con-
servation crisis is so pronounced that some authors have
been considered that we are amidst the sixth mass extinction
(Barnosky et al., 2011; Dirzo et al., 2014; Ceballos et al.,
2015). Human occupation on natural environments and con-
sequent land-use change directly reduce the number of spe-
cies (Ceballos & Ehrlich, 2002; Dirzo et al., 2014). In
addition, even relatively pristine habitats have experienced
species losses and populations are declining due to hunting
activities for commercial, subsistence or animal trade (Peres
& Palacios, 2007; Young et al., 2016) with an estimate of 5
ton harvest each year in the Amazon and Afrotropical rain-
forests (Fa, Peres & Meeuwig, 2002). Indeed, the loss of
animal biomass from tropical ecosystems may be more dra-
matic than changes in overall population density and species
large-bodied species disappeared (Peres & Palacios, 2007), a
phenomenon named density compensation (MacArthur, Dia-
mond & Karr, 1972).
Therefore, the use of species richness to evaluate conser-
vation importance of a given area may be a weak measure
of ecosystem health (Gonzalez-Maya et al., 2015) because
many species may have populations so low that their effect
on the ecosystem is marginal (Novaro, Funes & Walker,
2000; McConkey & OFarrill, 2015; Valiente-Banuet et al.,
2015). Thus, it is paramount to understand the effects of
human-made disturbances, such as forest fragmentation
(Rylands & Keuroghlian, 1988; Chiarello, 1999), logging
(Johns, 1986; Meijaard et al., 2007) and exotic plantations
(Barlow et al., 2007; Azhar et al., 2014) on mammal persis-
tence and abundance. Large continuous forests are usually
poorly investigated in terms of the conservation status of
mammals, perhaps because of the false impression that these
areas suffer low human impact and that they are safe from

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Defaunation in the Atlantic forest M. Galetti et al.

major anthropogenic disturbances (Rodrigues et al., 2004;
Beaudrot et al., 2016).
The Atlantic Forest in South America originally extended
from 3 to 31S, and from 35 to 60W, covering more than
150 million ha, extending along the Brazilian coast (92%),
but also reaching into Paraguay and Argentina. The high
levels of endemism of this forest have intrigued scientists for
many years (Leite et al., 2016) which considered a biodiver-
sity hotspot (Myers et al., 2000). The Brazilian part of the
Atlantic forest nowadays covers ~12% of the original area,
distributed in 245 173 forest fragments (Ribeiro et al.,
2009). The largest forest patch is located in the Serra do
Mar subregion, mainly along the coastal mountains of the
states of S~ao Paulo, Parana and Santa Catarina, and
extends into the southern part of the state of Rio de
Janeiro. This single patch contains ~1 109 546 ha of con-
tinuous forests, which represents 7% of what remains
(Ribeiro et al., 2009). This forest patch suffered and con-
tinues suffering from illegal palm harvesting (Galetti &
Fernandez, 1998), hunting (Galetti et al., 2009), human-
made infrastructure (pipeline, roads) and human encroach-
ment that negatively affect animal movement and increase
mortality (Miotto et al., 2012; Bogoni et al., in press). Sev-
eral studies point out that this region as the largest strong-
hold for several endemic species of mammals in critical
conservation status (Duarte et al., 2012; Keuroghlian et al.,
2012; Ingberman, Fusco-Costa & Monteiro-Filho, 2016).
However, we do not have much information on the popula-
tion status of most these species.
Studies on the population density and biomass of med-
ium- and large-sized mammals in the Atlantic forest have
been focused on few isolated forest fragments (Chiarello,
2000; Cullen, Bodmer & Padua, 2000; Bernardo & Galetti,
2004; Bovendorp & Galetti, 2007; Ara ujo, Souza & Ruiz-
Miranda, 2008) or in a few species (Price, Piedade & Wor-
mell, 2002; Passamani, 2008; Norris et al., 2011). Here, we
provide the rst comprehensive study to assess the species
richness, population density, biomass and community compo-
sition of medium and large mammals in the largest Atlantic
forest remnant, the Serra do Mar subregion. We were partic-
ularly interested in understanding spatial variation in species
richness, density and biomass along the largest continuous
Atlantic forest and compare with studies that used similar
methods in the Atlantic forest fragments and continuous
Amazon forests. In addition, we expected to nd higher
composition dissimilarity between pairs of sites located in
the mainland sites versus island sites.
Study areas
We chose 13 sites across 8000 km2 in the Serra do Mar sub-
region (see Ribeiro et al., 2009) for our mammal census
(Fig. 1). This area was divided into three major regions that
differ in human density, historical occupation and hunting
pressure. The Paranapiacaba massif, Serra do Mar massif
and the two largest land-bridge islands that ank the south
and southeast coast of Serra do Mar that were formed by
historical marine incursions due to glaciation events, tectonic
activities and coastal erosion dynamics (Suguio & Martin,
1987). The Paranapiacaba and Serra do Mar differ in the
density of human occupation, which reects in differences in
hunting pressure.

Figure 1 Location of the sampled study areas along the Atlantic forest in southeastern Brazil. In light green the protected parks and in dark
green the areas sampled in this study (IT, Itamambuca-Cunha; PI, Picinguaba; VG, Vargem Grande; IB, Ilhabela; CA, Caraguatatuba; JU, Juru-
par ia; BH, Carlos Botelho-Highland; BL, Carlos Botelho-Lowland; IN, Intervales; PE, Petar; JA, Jacupiranga; IC, Ilha do Cardoso).
a; JR, Jure
All these areas are protected parks.

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M. Galetti et al.
The Paranapiacaba massif consists of ve conservation
protected areas (Parque Estadual Carlos Botelho Highland
(BH) and lowland parts (BL) , Parque Estadual Intervales
(IN), Parque Estadual Jacupiranga (JA), Parque Estadual
Jurupara (JU) and Parque Estadual Turstico do Alto do
Ribeira (JA)), located at 48240 W24180 S, with an area of
460 000 ha. The primary forests occur in step terrains,
whereas secondary forests occur in at areas that have been
used by mining and selective logging in the past. The annual
average temperature is around 24C, but in the highlands
frost is common during the winter. Annual rainfall can reach
up to 4000 mm.
The Serra do Mar massif consists of two conservation
units: Estac~ao Ecol
ogica da Jureia (JR), and Parque Estadual
da Serra do Mar. The Parque Estadual da Serra do Mar is
divided into 10 administrative zones and we sampled four of
them [Caraguatatuba (CA), Itamambuca-Cunha (IT), Picin-
guaba (PI) and Vargem Grande (VG)]. These areas are
located at coordinates between 45250 W and 23350 S to
44500 W and 23220 S.These areas are covered by Atlantic
ombrophilous dense forest, with the annual average tempera-
ture around 1824C, and annual average rainfall of
2200 mm.
In addition, we sampled the two largest land-bridge
islands: Parque Estadual da Ilha do Cardoso (IC) and Par-
que Estadual Ilhabela (IB). IC is located in Cananeia
(48050 W and 25030 S). It has an area of 13 500 ha, of
which 11 000 ha are formed by Atlantic Forest in the strict
sense, and the remainder is composed of mangroves, bea-
ches and sand dunes. The average annual temperature is
21C with annual average rainfall between 1673 and
3014 mm. Ilhabela is the largest and most populated island
in the southeastern Brazilian coast. It is located at Ilha de
S~ao Sebasti~ao (45180 W and 2380 S), and has 33 600 ha
with mean temperature of 22C, and around 1500 mm of
annual rainfall.
Methods
Field efforts
Species richness and composition
We estimated the species richness of each area based on
tracks, occasional sightings and interviews with local resi-
dents and rangers (Supporting Information Table S2). We
included information from the literature, but we were careful
to not include data from management plans because the
quality of the data is usually poor (Supporting Information
Table S2). In addition, we used a series of camera traps
(Reconyx model RC55 RapideFire, www.reconyx.com) to
sample medium- and large-sized mammals (>1 kg, except
Brazilian squirrels and marmosets with ~200 g) in 4 of the
13 sites. We used 18 cameras at Itamambuca-Cunha (IT) 16
at Vargem Grande (VG) 30 at Ilha do Cardoso (IC) and 49
at Carlos Botelho - lowland area (BL) that were distributed
across preexisting transects and trails throughout the areas
including secondary and primary forest habitats, with a
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Defaunation in the Atlantic forest
minimum distance of 200 m between them (Figure 1). Sam-
pling was carried out from September 2011 to January 2012
at IT, September 2011 to June 2012 at VG, August 2010 to
September 2011 at IC and September 2009 to June 2010 at
BL. Cameras operated over 24 h a day and were active for
232 days at IT, 440 days at VG, 528 days at IC and 6
16 days at BH per sampling. The other areas were not sam-
pled due to the lack of protection and safety. We installed
the cameras in trees at a height of c. 40 cm above the
ground with a small angle of inclination. No bait was used.
Population census
Line transects are the most common method to estimate the
population of forest-dwelling mammals (Burnham, Anderson
& Laake, 1980; Peres, 1999). We carried out diurnal line-
transect surveys for mammals >0.20 kg that include from
small-bodied arboreal species (squirrels, marmosets), to mid-
sized (agoutis, pacas) and large-bodied species (monkeys,
peccaries, deer and tapirs).
We established a total of 119 transects (mean = 7.6 tran-
sects per site) that ranged from 0.3 to 14.4 km in length
(mean = 3.53 km) depending on local topography (Support-
ing Information Table S1). All observers were previously
trained and followed the standardized methodology for line-
transect censuses (Peres, 1999). The cumulative distance
sampled in each site varied from 77 to 572 km summing
4090 km (mean = 292.1 km per site). The surveys were
done between 2002 and 2012, and each site was sampled
monthly for at least 1 year, so we do not expect changes
due to potential seasonal variation.
Data analyses
Beta diversity
We estimated pairwise similarity in assemblage composition
by constructing resemblance matrices from the sites-by-spe-
cies dataset based on the Srensen (presenceabsence) coef-
cient. This coefcient incorporates both taxon replacement
and taxon richness differences, and gives equal weight to
both rare and abundant species (Koleff, Gaston & Lennon,
2003). We then plotted values of similarity among all pairs
of sites as a function of geographical distances. This allowed
us to investigate how beta-diversity patterns varied according
to the region a site was located in (Paranapiacaba massif and
Serra do Mar massif vs. the two islands) and to the geo-
graphical distance between pairs of sites.
Density and biomass estimates
The densities of species were estimated using the Distance
6.0 Software (Thomas et al., 2010). We grouped the visual-
ization events of same species in all sites to obtain most pre-
cise effective strip width (ESW), but density was estimated
based on site-specic sampling effort (Peres, 2000). We
pooled all data by sites, not transects, due to the low number
of sightings.
3
 4
Table 1 Density and biomass of eight mammal species in 13 Atlantic forest sites

Density (ind. km2) (biomass kg km2)

Brachyteles Guerlinguetus
Alouatta guariba arachnoides Callithrix aurita Sapajus nigritus Dasyprocta leporina brasiliensis Nasua nasua Tayassu pecari
Ilha do Cardoso NR/NO NO NR
Defaunation in the Atlantic forest

8.91  2.47 4.29  1.62 1.38  0.58 2.64  1.31 13.55  6.25
(50.07  13.88) (18.01  6.80) (0.23  0.09) (13.46  6.68) (474.2  218.7)
Ilhabela NR NR NO 2.49  2.04 NR 6.99  1.99 NR NR
(8.71  7.14) (1.18  0.33)
Carlos Botelho 2.70  0.73 12.15  3.79 NO 8.50  2.15 0.30  0.21 4.26  0.71 2.20  1.39 NR
Highland (15.17  4.10) (130.61  40.74) (29.75  7.52) (1.26  0.88) (0.72  0.12) (11.2  7.08)
Carlos Botelho 1.03  0.53 NR NO 13.94  3.99 NR 4.34  1.27 6.37  4.86 NR
Lowland (5.78  2.97) (48.79  13.96) (0.73  0.21) (32.48  24.78)
Intervales 0.42  0.33 3.04  1.62 NO 2.59  1.09 NR NR NR NR
(2.36  1.85) (32.68  17.41) (9.06  3.81)
Jacupiranga 4.18  2.73 NR NO 1.09  1.11 0.82  0.83 NR 3.38  3.27 NR
(23.49  15.34) (3.81  3.88) (3.44  3.48) (17.23  16.77)
a
Jurupar 0.57  0.48 NR NO 0.90  0.55 0.33  0.28 0.95  0.32 NR NR
(3.20  2.69) (3.15  1.92) (1.38  1.17) (0.16  0.05)
PETAR 0.28  0.25 0.52  0.44 NO 5.51  3.74 NR 0.62  0.39 NR NR
(1.57  1.40) (5.59  4.73) (19.28  13.09) (0.10  0.06)
Caraguatatuba 1.82  0.95 NR NR 7.37  2.39 0.34  0.24 0.16  0.14 NR NR
(10.22  5.33) (25.79  8.36) (1.42  1.00) (0.02  0.02)
Cunha-Itamambuca 0.87  0.43 0.44  0.44 11.45  3.83 2.64  1.30 NR 4.38  1.64 1.19  1.18 3.35  3.09
(4.88  2.41) (4.73  4.73) (4.58  1.53) (9.24  4.55) (0.74  0.27) (6.06  6.01) (117.2  111.6)
eia
Jur 0.98  0.59 1.53  1.65 NO 32.04  7.94 NR 9.42  1.81 NR NR
(5.50  3.31) (16.44  17.73) (112.14  27.79) (1.60  0.30)
Picinguaba NR NR NR NR 1.19  0.79 1.56  0.76 3.45  2.29 NR
(4.99  3.31) (0.26  0.12) (17.59  11.67)
Vargem Grande NR NR 11.06  1.62 2.69  0.54 0.67  0.03 28.74  2.54 2.77  0.13 NR
(4.42  0.64) (9.41  1.89) (2.81  0.12) (4.88  0.43) (14.12  0.66)
ESW 13.9  1.6 ESW 14.9  2.7 ESW 8.1  0.2 ESW 17.7  2.0 ESW 5.9  0.3 ESW 6.3  0.4 ESW 8.6  0.4 ESW 9.2  2.4
m TD 35 m m TD 30 m m TD 16 m m TD 35 m m TD 20 m m TD 15 m m TD 15 m m TD 22 m

NR, not recorded in line transect survey; NO, species does not occur in the area; ESW, effective strip width; TD, truncation distance used in model; PETAR, Parque Estadual Turstico do
Alto do Ribeira.
M. Galetti et al.

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M. Galetti et al.
We used Akaike information criterion for choosing the
best model for ESW denition (truncation distance and ESW
are presented in Table 1). Using density values (D) multi-
plied by average body weight (BW), we calculated the bio-
mass of species (D 9 BW = kg km2). BW was based on
Paglia et al. (2012).
Ecological and human variables
We tested if ecological (forest type: lowland or montane
forest) or human inuence (hunting pressure) explains the
densities and biomass of mammals through Linear Mixed-
Effects Model analysis using the package nlme (Pinheiro
et al., 2007) in R program (R Core Team 2015). To do the
analysis we summed the average density and biomass for
game species only and all mammal sampled per site
(n = 13). We used forest type and hunting pressure as xed
effects and region [Paranapiacaba (n = 6 sites), Islands
(n = 2) and Serra do Mar (n = 5)] as random effects. Forest
type was based on Oliveira-Filho & Fontes (2000). The
hunting pressure was estimated with same parameters
adopted in Galetti et al. (2009), where:
1 Lightmoderate hunting. Forest sites located in areas with
low-to-moderate densities of human residents and weak
evidence of hunting. Usually, these sites used to be pro-
tected by professional rangers who regularly patrolled the
sites.
2 Heavy hunting. Forest sites exhibiting considerable evi-
dence of human disturbances, such as hunting, domestic
dogs and palm harvesting. Usually these areas are easily
accessible by roads and have small residential human pop-
ulations inside the park.
Results
Species richness and composition
We recorded 44 non-volant mammal species in the largest
Atlantic forest remnant based on tracks, indirect sightings,
interviews or literature review that varied from 9 to 40 spe-
cies per site (Supporting Information Table S2). However,
only 19 species were recorded through observations in line-
transect censuses. From these species, we were able to have
a robust density and biomass estimate of only eight species
(Table 1).
Of these 44 mammal species recorded, 2 are classied as
Endangered, 6 as Vulnerable, 7 as Near Threatened, 27 spe-
cies as Least Concern and 1 as Data Decient, according to
the IUCN Red List Status (Supporting Information
Table S2). In addition, two exotic species were recorded (do-
mestic dogs and European hare). At least three species are
typical from open savanna habitats (White-Eared Opossum,
Maned wolf and Giant ant-eater) and may experience an
increase in their distribution. Some species are typical from
semi-deciduous forests (Black-Fronted Titi Monkey, Black
Lion Tamarin, Azaraes Agouti) that occurred in the high-
land ecotone region. The major difference between species
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Defaunation in the Atlantic forest
composition between Paranapiacaba and Serra do Mar is the
occurrence of Buffy-Tufted-Ear Marmoset and Three-Toed
Sloth in Serra do Mar massif.
For the four areas that we used camera traps, we obtained
a total of 416 camera-days at IT (9995 h), 416 camera-days
at VG (9988 h), 555 camera-days at IC (13 320 h) and 497
camera-days at BL (11 749 h). From this effort we identied
9 species at IT, 10 species at VG, 11 species at IC and 13
species at BL (Supporting Information Table S3). The mean
rarefaction curve that estimated species richness per survey-
day did not reach an asymptote in any site (Supporting Infor-
mation Fig. S1), with species continuing to accumulate at a
rate of 0.04 species at IT, 0.06 at VG and IC and 0.09 at BL
after 45 survey days. Based on the rst-order jackknife the
extrapolated species richness was between about 8 and 14
species at IT (estimate  95% CI = 10.96  2.72), 10 and
16 species at VG (estimate  95% CI = 12.93  3.32), 13
and 21 species at CB (estimate  95% CI = 16.93  3.86)
and 10 and 16 species at IC (estimate  95%
CI = 12.96  2.72).
Beta diversity
The community composition reected the location of sites
within the Paranapiacaba massif and Serra do Mar massif
versus the two islands (Fig. 2), but was not related to the
geographical distance between pairs. Pairs of sites located in
the mainland were very similar in terms of species composi-
tion (Srensen similarity values: min = 0.85, max = 1.0,
mean = 0.91, SD = 0.03). Just below those were the pairs
that compare IC and the mainland sites (min = 0.74,
max = 0.84, mean = 0.78, SD = 0.02). Pairs comparing conti-
nental sites versus Ilhabela island were all very dissimilar
(min = 0.29, max = 0.36, mean = 0.32, SD = 0.02).
Figure 2 Mammal (>0.20 kg) species composition similarity,
expressed as Srensen index, between continental forest pairs
(black, green in online), Ilha do Cardoso and other sites (Grey, blue
in online) and Ilhabela and other sites (light grey, red in online) in
relation to their distances (km).
5
Defaunation in the Atlantic forest
Density and biomass estimates
The densities of mammals based on line transects varied 16-
fold among sites, from 2.75 to 45.93 ind. km2, whereas
biomass varied 70-fold from 7.9 to 556 kg km2 (Table 1).
The species with the highest density was capuchin monkey
(Sapajus nigritus) at Jureia with 32.04 ind. km2, and the
lowest density was 0.16 ind. km2 for the Brazilian squirrel
(Guerlinguetus brasiliensis) at Caraguatatuba (Table 1).
Interestingly both sites were in the Serra do Mar massif,
although the area was just 145 km apart from each other.
The greatest density of primates was found at Jureia Eco-
logical Station, but the highest biomass was documented for
CBHighland, due to high density of muriquis, the largest
Figure 3 Average (SD) of density and biomass of all survey species and all game (large-bodied) species in relation to hunting impact in 13
study sites the Brazilian Atlantic forest.
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M. Galetti et al.
Neotropical primate (mean body mass ~12 kg) (Table 1).
The smallest primate species, Callithrix aurita, was present
only in two sites, and although it made a large contribution
to overall density in Cunha-Itamambuca and VG, its contri-
bution to overall biomass is relatively small (Table 1). In
both islands sampled, the density and biomass of primates
was lower than in continental sites. However, in IC we
recorded the highest density and biomass of seed predators
(D. leporina, G. brasiliensis and T. pecari; Table 1).
Ecological and human variables
The average density and especially the average biomass were
higher in sites with lightmoderate hunting pressure.
M. Galetti et al. Defaunation in the Atlantic forest

However, density was not signicantly inuenced by hunting
(F = 0.01; P = 0.92) or forest type, whereas biomass was
affected by hunting (F = 39.09; P < 0.01) and an interaction
between hunting and forest type (F = 27.48, P < 0.01), but
not by forest type alone (F = 2.73, P = 0.14; Fig. 3). When
we analyzed game species apart, the same pattern was
observed. Density was not related to any predictor variable,
whereas biomass was related to hunting pressure and an
interaction between hunting pressure and forest type on bio-
mass (hunting F = 44.68, P < 0.01, hunting 9 forest type
F = 29.5, P < 0.01; Fig. 3, Table 2). Lowland forest with
light hunting pressure presented higher average biomasses
than montane forest with light hunting pressure.
Discussion
Species composition
Our results indicate a high diversity of mammals in the lar-
gest Atlantic forest remnant (from 31 to 38 native species),
with no extinction at the regional level, except in the two
land-bridge islands. However, the exact species richness of
our study areas may be underestimated due to cryptic identi-
ties of some species. For instance, recently a new species of
brocket deer (Mazama bororo) and a small felid (Leopardus
guttulus) were described from the southeastern Atlantic for-
ests (Gonzalez et al., 2009; Trigo et al., 2013).
The local extinction in the islands is intriguing. Ilhabela is
2.3 bigger than IC (3475 km vs. 151 km2, respectively) and
presented the lowest diversity of medium- and large-sized
mammals (eight species). We did not detect even common spe-
cies that usually thrive in highly fragmented forests, such as
raccoon (Procyon cancrivorous) or agoutis (Dasyprocta lepor-
ina). Although we have no historical information on the mam-
malian composition of Ilhabela, it is likely that the extensive
deforestation for sugar cane plantations in the previous cen-
turies, intensive hunting and low immigration from the main-
land explain this low diversity (Olmos, 1996). This is likely the
cause for the lower values of pairwise compositional similarity,
that is, high beta diversity, when one of the pair of sites was
from Ilhabela. Therefore, zoo archeological studies in this
island should be necessary for future wildlife reintroductions.
The second largest island, IC, had at least two species
locally extinct, the tapir and the jaguar (probably around
1960s based on local interviews). The island is too small to
maintain a population of jaguars and they used to reach the
island crossing a shallow channel. Tapirs probably were resi-
dent and we recommend reintroducing this megaherbivore in
the island if hunting and illegal palm harvesting is con-
trolled.
The diversity of mammals that we found in the continen-
tal forests of Serra do Mar and Paranapiacaba is higher than
in other regions of the Atlantic forest. The absence of local
extinction along the continental forests contrasts with other
well-studied regions in the northern Atlantic forest where up
to 80% of the mid and large mammal species have been
extirpated (da Silva & Pontes, 2008; Canale et al., 2012;
Pontes et al., 2016). This resulted in extremely low beta-
diversity values among continental sites and a lack of rela-
tionship between similarity and geographical distance, which
contrasts with previous evidence from tropical areas (e.g.
Condit et al., 2002), especially from tree data. The wide-
spread distribution of most mammal species across the conti-
nental forests of Serra do Mar and Paranapiacaba likely
explains this lack of distance decay relationship.
Species density and biomass
The results of our census showed that the densities of mam-
mals varied strongly within continental Atlantic Forest sites,
from around 3 mammals km2 (Jurupara) to 46 mam-
mals km2 (VG). Surprisingly the two sites with higher
mammalian density have the heaviest hunting pressure (VG
and Jureia). However, the mammalian assemblage of these
areas is composed mostly of small-bodied species (squirrels,
marmosets and capuchin monkeys) that are less affected by
hunting and it is likely that these smaller species are favored
in hunted sites (Peres & Dolman, 2000).
The overall mammalian density recorded in both Paranapi-
acaba and Serra do Mar is 1.53.1 times lower than small
Atlantic forest fragments (Table 3). The high density of pri-
mates and ungulates in Atlantic forest fragments seems to
reect a crowding effect with expected high home range
overlap among individuals or groups.

Table 2 Summarized results of linear mixed-effects model analyses about the influence of forest type (lowland or highland) and hunting
pressure on total density and biomass of all mammals and game mammals

All mammals Game mammals

numDF denDF F-value P-value F-value P-value
Density
Intercept 1 7 14.09 0.007 14.57 0.006
Forest type 1 7 0.01 0.92 0.91 0.37
Hunting pressure 1 7 0.01 0.91 2.42 0.16
Forest type 9 hunting pressure 1 7 0.84 0.38 0.23 0.64
Biomass
Intercept 1 7 41.93 <0.001 38.10 <0.001
Forest type 1 7 2.73 0.14 2.58 0.15
Hunting pressure 1 7 39.09 <0.001 44.68 <0.001
Forest type 9 hunting pressure 1 7 27.48 0.001 29.55 0.001

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2016 The Zoological Society of London 7

Defaunation in the Atlantic forest
Table 3 Comparison between three continuous Atlantic Forest (AF) regions, Atlantic forest fragments and Amazon forest (density:
ind. km2, biomass: kg km2; athis work, bChiarello, 2000; Chiarello & de Melo, 2001; Cullen et al., 2001; Arau
Peres, 2005)
Primates
Region Density Biomass
a
AF Paranapiacaba massif 9.57 55.72
AF Serra do Mar massifa 14.58 41.48
AF Islandsa 5.70 29.40
AF fragments (<2000 ha)b 22.85 65.30
AF fragments (200035 000 ha)b 53.45 196.87
Amazonian terra firmec 122.6 328.9
Amazonian varzeac 202.1 410.23
Our analyses showed the mammal density was not signi-
cantly affected by hunting, whereas the overall crude mam-
malian biomass was, and also by combination of forest type
and hunting pressure. Lowland forests with light hunting
pressure, in average, presented higher biomass than montane
forest with same hunting pressure. These results probably
reect positive effects of forest productivity on mammal bio-
mass, when hunting was limited (Peres, 2000; Galetti et al.,
2009). Similar results were obtained in continuous sites of
Amazonian and fragmented Atlantic forest, where hunting
had no effect on mammalian density, but on biomass (Chiar-
ello, 2000; Peres, 2000). Thus, Neotropical forests exposed
to heavy hunting pressure show more pronounced change in
mammalian biomass than density because density compensa-
tion processes may be occurring (MacArthur et al., 1972).
The low density of ungulates and large rodents in most of
our study areas may be related to hunting preferences of
colonists in the Atlantic forest, who normally do not hunt
primates, but strongly prefer ground-dwelling frugivorous
herbivorous mammals (Chiarello, 2000; Cullen, Bodmer &
Valladares-Padua, 2001; Brocardo et al., 2012) and the pre-
dation by feral dogs that became highly abundant in most
areas (Galetti & Sazima, 2006; Srbek-Araujo & Chiarello,
2008). We were able to obtain robust density estimate for
only one ungulate, the white-lipped peccaries in only two
sites. Our density estimates for one site (Cardoso Island,
13.55 ind. km2) is twice the average density reported for
non-hunted forests elsewhere (Keuroghlian et al., 2012).
Based on tracks and latrines found, tapirs are apparently
common in all continental sites (CB, Intervales, Caraguata-
tuba; Norris et al., 2012), but the method that we used (diur-
nal line transect) is not appropriate to estimate their density.
The low density of primates, especially muriquis, can be
related to historic and current hunting pressure by traditional
populations (Indians, Quilombolas and Caicaras), which do
not have taboo to eat primates (Galetti et al., 2009).
Changes in the Atlantic Forest habitats (due selective log-
ging, palm harvest, roads) coupled with extensive human
density, and consequently high levels of hunting may be the
reason why our sites have low mammalian density and bio-
mass (Galetti et al., 2009; Table 3). For example, the mean
biomass of Paranapiacaba massif is seven times smaller than
some Amazonia terra rme forests. The site with lowest
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2016 The Zoological Society of London
M. Galetti et al.
jo et al., 2008; cHaugaasen &
All medium- and large-
Ungulates sized mammals
Density Biomass Density Biomass
0.00 0.00 13.50 67.18
0.67 23.45 26.02 75.84
6.75 237.12 20.13 282.98
1.12 29.27 41.28 103.31
4.74 178.20 78.84 401.12
5.04 208.38 142.6 596.8
0.16 5.76 211.8 454.8
biomass, Ilhabela, had 53 times smaller than non-hunted
Amazon sites. The absence of white-lipped peccaries popula-
tions from most of our sites (84%) was responsible for the
low biomass in most of our sites, except Itamambuca-Cunha
and IC. White lipped peccaries correspond to 8085% of the
whole mammalian biomass in these sites respectively, but
drops to <34% in slightly hunted Atlantic forest fragments
(Cullen et al., 2001). Based on interview with local rangers,
white-lipped peccaries disappear from Paranapiacaba region
in the late 80s (last seen in 1986), and were not recorded in
our census. This species was recently rediscovered only in
2011 (Beisiegel, Nakano-Oliveira & Jorge, 2014) and hope-
fully the population will recover if hunting and palm har-
vesting is controlled.
Although we could not calculate the densities for all
ungulate species, such as collared peccaries, or deer, the
low encounter rate may represent lower densities too, as the
encounter rates are correlated with density (Hill et al.,
1997). The low density of ungulates may result in a
reduced perturbation of the forest oor by trampling and
seed predation and dispersal (Brocardo et al., 2013), which
may affect plant composition by increasing the dominance
of some species (Dirzo & Miranda, 1991; Wright, Her-
nandez & Condit, 2007; Galetti & Dirzo, 2013). For
instance, the foraging behavior of large herds of white-
lipped peccaries feeding on seeds, trampling seedlings and
rooting of seedling and saplings may have a profound effect
on plant composition (Beck, 2006) and rodent abundance
and diversity (Galetti et al., 2015). In addition, the defauna-
tion of large seed dispersers, such as the primates and
agouties, may also represent a threat for the dispersal of
large-seeded species. These species play a fundamental role
as seed dispersers and their local extirpation may translate
into the lower recruitment and dispersal distances, leading
to long-term declines in plant diversity (Galetti et al., 2006;
Arroyo-Rodrguez et al., 2007; Donatti, Guimaraes &
Galetti, 2009; Stevenson, 2011; Bueno et al., 2013) with
potential consequences for carbon storage (Bello et al.,
2015).
Because most of the Atlantic forest is restricted to small
patches, a lot of effort and resources have been invested to
restore and connect isolated forest patches (Melo et al.,
2013). However, the decline in animal populations is evident
M. Galetti et al.
even in the large forest patches such as the Central Atlantic
Corridor in south Bahia with 50 000 ha of protected area
(Canale et al., 2012), the Misiones Corridor with
412 000 ha (De Angelo, Paviolo & Di Bitetti, 2011) and the
Serra do Mar subregion. It is estimated that 96% of the
entire Atlantic forest biome is likely to be under some
effects of trophic cascades due to mammalian defaunation
(Jorge et al., 2013).
The Serra do Mar and Paranapiacaba region has been
pointed out as the main stronghold for several endemic spe-
cies (Brachyteles arachnoides, Callithrix aurita, Mazama
bororo, Leopardus guttulus) or species that have vanished
from most of the Atlantic forest (Tayassu peccari, Speothos
venaticus, Panthera onca) (Duarte et al., 2012; Keuroghlian
et al., 2012; Galetti et al., 2013; Ingberman et al., 2016).
However, our data show that even in this large forest block
their population size may be too low to ensure their long-
term persistence. Therefore, the main conservation strategies
for these regions are to promote effective conservation by
reducing illegal hunting, palm harvesting and logging. These
strategies also involve hiring and empowering forest guards
to ght against well-structured militias of palm harvesters
and hunters who are becoming common in Serra do Mar.
These war-zones of conservation are usually omitted by
decision makers who ignore that hunting is a widespread
practice in protected areas and by many conservation biolo-
gists who deny the clear global defaunation trend of mam-
mal populations in tropical forests (Beaudrot et al., 2016). In
fact, the ongoing defaunation scenario in the largest Atlantic
forest remnant may be exacerbating due to the recent eco-
nomical crisis in Brazil. For instance, about 30% of all forest
guards (rangers) were dismissed from the protected parks in
S~ao Paulo state in the last 4 years. Therefore, the future of
the mammalian diversity in the largest Atlantic forest rem-
nant may soon mirror the impoverished rainforests world-
wide.
Acknowledgements
This work was supported by the Fundac~ao de Amparo a
Pesquisa do Estado de S~ao Paulo (FAPESP) through the pro-
cess BIOTA FAPESP 2007/03392-6 and 2014/01986-0.
We thank the directors of the protected areas and Fundac~ao
and Instituto Florestal do Estado de S~ao Paulo for allowing
us to carry out this study. We thank S. Nazareth for assis-
tance in the eld. C.R.B., M.C.R. and M.G. receive a CNPq
fellowship (Conselho Nacional para o Desenvolvimento
Cientco e Tecnologico). R.A.F.L. received a CAPES fel-
lowship (Coordenac~ao de Aperfeicoamento de Pessoal de
Nvel Superior). To Paulo Rubim and Carla Stefer for help
in the eld work.
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Supporting information
Additional Supporting Information may be found in the
online version of this article at the publishers web-site:
Figure S1. Mean rarefaction curve showing the upper
bounds of the 95% CI of the expected number of mid-and
large-sized mammals recorded with camera traps in Itamam-
buca (IT) and Vargem Grande (VG), Carlos Botelho (BH)-
Highland, Ilha do Cardoso (IC).
Table S1. Physical attributes and sample size of medium
and large sized mammals in 13 sites long the of Serra do
Mar subregion.
Table S2. Species occurrence of medium and large sized
mammals in each sampling region in the continuous Atlantic
Forest, based on tracks, sightings, interviews and literature
(NR, not recorded in line transect survey; NO, species does
not occur historically; O, species observed; Ex, probably
extinct).
Table S3. Terrestrial mammals recorded by camera trapping
(IT, Itamambuca; VG, Vargem Grande; BH, Carlos Botelho-
Highland; IC, Cardoso Island).
Animal Conservation

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