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17 � Multiple Reintroductions to
Restore Ecological Interactions
in a Defaunated Tropical Forest
MARCELO LOPES RHEINGANTZ,
ALEXANDRA DOS SANTOS PIRES, AND
FERNANDO A. S. FERNANDEZ
17.1 Background
Worldwide, defaunation leads not only to global and local extinctions
but also to the severe loss of ecological interactions (Dirzo et al., 2014).
Reintroductions can be used to restore populations and arealso a main
tool of the rewilding movement, allowing restoration of ecosystem
function (IUCN, 2013). Refaunation (Oliveira-Santos & Fernandez,
2010) and trophic rewilding (Svenning et al., 2016; Seddon, this volume)
have been proposed as the cheapest, safest, and most efficient rewilding
approaches to restore tropical ecosystems (Galetti et al., 2017).
The Atlantic Forest is a biodiversity hotspot and a priority biome for
trophic rewilding (Galetti et al., 2017), prompting the initiation of the
REFAUNA programme (Fernandez et al., 2017). Our first target area is
Tijuca National Park (TNP), a 3,953 ha reserve within Rio de Janeiro
city that suffered extensive deforestation and hunting in the past. In the
nineteenth century forest cover was restored but the fauna remained
impoverished. In the 1970s there was a multi-species reintroduction effort
at TNP (Coimbra-Filho et al., 1973) and at least two species established
populations: boa constrictor Boa constrictor and channel-billed toucan
Ramphastos vitellinus. The isolation of TNP means that it cannot be
naturally recolonised by most missing species but this makes it a good
natural laboratory for studying the benefits and risks of refaunation efforts.
Our goal is to restore TNP as far as possible to pre-colonial conditions
and to achieve self-regulating systems by restoring key missing ecological
interactions. To accomplish this, we needed to identify the missing
species, evaluate the feasibility of reintroductions, translocate individuals,
and monitor their fate and the restoration of ecological interactions.
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17.2 Methods
In 2008, Ivandy Castro Astor, former TNP director, drew co-author
A. S. P.’s attention to the dozens of Joannesia princeps seeds (known as
‘cutieira’ or agouti tree) piled on the ground. They realised that the only
species able to disperse them in the area, the red-rumped agouti
Dasyprocta leporina, was missing. We also noted that other vertebrates
included in the TNP management plan were missing – some of which
have important ecological roles – such as carnivores, peccaries, reptiles,
birds of prey, and primates.
As a response to Ivandy Castro Astor’s observations, red-rumped
agouti reintroduction started in 2010. Following this, Macedo (2017)
plotted mammalian extinctions throughout the Brazilian Atlantic Forest,
helping us to understand better which species were missing. Galetti et al.
(2017) then described trophic rewilding priorities in Neotropical forests.
These ideas were consolidated in a workshop in 2018 to define TNP
reintroduction priorities, involving researchers, environmental agencies,
park managers, and ex situ managers. We used the following criteria:
historical record, ecological role, stock availability, available resources at
TNP, potential hunting/removal pressure, management conditions, and
social support. It was decided to reintroduce generalists of low trophic
level first (agoutis, folivore-frugivore primates, tortoises, and others),
followed by low-level specialists, and then species of higher trophic levels
(native Felidae, Mustelidae, and birds of prey) only when prey abun-
dance could sustain predator populations (Galetti et al., 2017).
17.3 Outcomes
17.3.1 Red-Rumped Agoutis
Red-rumped agoutis (Figure 17.1A) are scatter-hoarding rodents that
disperse large seeds at long distances, equivalent to bigger-sized animals.
Individuals from a semi-captive population were captured and trans-
ported to Rio Zoo facilities. They were examined, quarantined, and
tagged and then transported to TNP acclimatisation pens. Thirty-one
animals were released between 2010 and 2014, using a delayed release
protocol. We monitored individuals by radio tracking (Cid et al., 2014).
In 2014, we started to monitor population trends through the use of
camera trapping (Kenup et al., 2018).
There was a high mortality rate during quarantine and acclimatisation.
However, a population was successfully established in TNP (Kenup
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Figure 17.1 Species released at Tijuca by REFAUNA: (A) red-rumped agouti;
(B) brown howler; (C) yellow-footed tortoise (photos: Marcelo Rheingantz).
(A black and white version of this figure will appear in some formats. For the colour
version, please refer to the plate section.)
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Comp. by: P. Udayasankar Stage: Proof Chapter No.: 17 Title Name: Gaywoodetal
Date:27/7/22 Time:20:53:53 Page Number: 439
et al., 2018). The population was estimated to be around 30–40 individ-
uals in 2018 within the surveyed area, and all individuals present since
2016 have been wild-born (Kenup et al., 2018).
Agoutis interacted with at least 23 plant species, hoarding three
(J. princeps, Astrocaryum aculeatissimum, and Sterculia chicha). They are the
only frugivores able to disperse seeds larger than 30 mm in diameter in
TNP, and the seeds of A. aculeatissimum and J. princeps are only being
buried in areas with agoutis (Zucaratto, 2013; Mittelman et al., 2020).
17.3.2 Brown Howlers
Brown howlers Alouatta guariba (Figure 17.1B) are folivore-frugivores that
have small home ranges for a primate, can disperse seeds, and are charis-
matic. Six adults, three captive-born and three confiscated from the illegal
wildlife trade, were quarantined, health checked, and tagged at Rio de
Janeiro Primatology Center (CPRJ) before being sent to the TNP accli-
matisation pen. These individuals were released using a delayed release
protocol between 2015 and 2017. They have been monitored by radio
tracking and active searching.
Two released males were returned to captivity due to their abnormal
interaction with visitors. One couple formed in the wild and had three
offspring, one each year; they form the single remaining group. A second
female was found dead and the other male has been missing since 2017.
Transmitters led to serious wounds in the ankles of the males (Genes
et al., 2019a). The population remains in the establishment phase and
requires additional releases. Unfortunately, this has not been possible due
to a regional yellow fever outbreak.
Brown howlers interacted with 60 plant species: for several plants, they
became their only disperser in TNP (Genes et al., 2019b). Twenty-one
dung-beetle species interacted with brown howler faeces, most of them
tunnellers, which can act as second dispersers (Genes et al., 2019b).
17.3.3 Yellow-Footed Tortoises
Yellow-footed tortoises Chelonoidis denticulatus (Figure 17.1C) are eco-
system engineers and generalist feeders that can also disperse seeds
over long distances. Adults do not have natural predators at TNP and
they have a long lifespan. Animals were moved from several captive
populations to the Wildlife Screening Center of the Brazilian Institute of
the Environment and Renewable Natural Resources in Rio de Janeiro
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(CETAS-IBAMA-RJ) in 2019, where they were examined and tagged.
Twenty-eight animals were released in 2020 using two different
methods, immediate and six-month delayedrelease, to provide an
experimental evaluation of the two methods. Animals were radio tracked
once a week.
All released tortoises were still alive three months after release. Some
animals dispersed more than 1.3 km from the release area. The monitor-
ing of tortoises was temporarily stopped due to COVID-19. We will
return to track them and release more as soon as possible.
Tortoises consumed parts of at least five native plant species, but only
the restart of the monitoring will allow us to determine their role in
restoring ecological interactions.
17.4 Discussion and Future Recommendations
TNP is a severely defaunated forest; only 10 of the 32 medium and large-
sized mammal species that originally occurred there in pre-colonial times
were present in 2010 (Macedo, 2017). Many other species are also
missing. The REFAUNA programme has achieved promising results,
but so far we have released only three species. Other species will be
reintroduced, with the aim of restoring complementary ecological inter-
actions. The next candidate species include the blue-and-yellow macaw
Ara ararauna, jacutinga Pipile jacutinga, iguana Iguana iguana, red-browed
amazon Amazona rhodocorytha, and lesser grison Galictis cuja. Apart from
the grison, all are low-trophic level generalists with non-redundant
ecological roles. All of them fit the trophic rewilding criteria (Galetti
et al., 2017).
Besides further releases, we will also continue to monitor the species
already reintroduced and their interactions. We need to understand how
to expand the red-rumped agouti distribution within TNP. In 2018, we
started an experiment (delayed versus immediate release, with or without
supplementary feeding) in another sector of TNP to define the best
reintroduction protocol for the species and to establish a new population.
The brown howlers will need population reinforcement, and further
releases are planned.
Rewilding programmes should identify key species missing in an area,
and their ecological roles, in order to assess which reintroductions can be
most effective in restoring function. The refaunation of TNP has been
encouraging; we have evidence that the reintroductions carried out are
recovering lost ecological interactions, even with a limited number of
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released individuals. Populations of all species are still well below their
respective carrying capacities but hopefully, as they increase and occupy
all parts of TNP, they will restore much of the ecosystem functionality in
this impoverished Atlantic Forest reserve. The hope is that more conser-
vation translocations will be used as a tool to mitigate the effects of
defaunation throughout this threatened biome.
17.5 Summary
� Refaunation can be used to restore empty habitat in the Atlantic Forest.
� TNP has suitable habitat for all ongoing reintroductions.
� At TNP, some plants are only dispersed/consumed by reintroduced
species.
� We need to continue monitoring the recovery of ecological inter-
actions and population establishment.
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