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Ecology and Evoluon 2017; 1–6
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1
www.ecolevol.org
Received: 22 November 2016
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Revised: 12 December 2016
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Accepted: 18 December 2016
DOI: 10.1002/ece3.2746
ORIGINAL RESEARCH
Credit of ecological interacons: A new conceptual framework
to support conservaon in a defaunated world
Luísa Genes1 | Bruno Cid1 | Fernando A. S. Fernandez1 | Alexandra S. Pires2
This is an open access arcle under the terms of the Creave Commons Aribuon License, which permits use, distribuon and reproducon in any medium,
provided the original work is properly cited.
© 2017 The Authors. Ecology and Evoluon published by John Wiley & Sons Ltd.
1Departamento de Ecologia, Universidade
Federal do Rio de Janeiro, Rio de Janeiro, RJ,
Brazil
2Departamento de Ciências Ambientais,
Universidade Federal Rural do Rio de Janeiro,
Seropédica, RJ, Brazil
Correspondence
Luísa Genes, Departamento de Ecologia,
Universidade Federal do Rio de Janeiro, Rio de
Janeiro, RJ, Brazil.
Email: genes.luisa@gmail.com
Funding informaon
Coordenação de Aperfeiçoamento Pessoal de
Nível Superior (CAPES); Conselho Nacional
de Pesquisa e Desenvolvimento Cienco e
Tecnológico (CNPq); Fundação de Amparo
à Pesquisa do Estado do Rio de Janeiro
(FAPERJ); Fundação Grupo Bocário de
Proteção à Natureza.
Abstract
As defaunaon spreads through the world, there is an urgent need for restoring eco-
logical interacons, thus assuring ecosystem processes. Here, we dene the new con-
cept of credit of ecological interacons, as the number of interacons that can be
restored in a focal area by species colonizaon or reintroducon. We also dene rewir-
ing me, as the me span unl all the links that build the credit of ecological interac-
ons of a focal area have become funconal again. We expect that the credit will be
gradually cashed following refaunaon in rates that are proporonal to (1) the abun-
dance of the reintroduced species (that is expected to increase in me since release),
(2) the abundance of the local species that interact with them, and (3) the traits of re-
introduced species. We illustrated this approach using a theorecal model and an em-
pirical case study where the credit of ecological interacons was esmated. This new
conceptual framework is useful for seng reintroducon priories and for evaluang
the success of conservaon iniaves that aim to restore ecosystem services.
KEYWORDS
conservaon management, ecological interacons, ecosystem funconing, refaunaon,
reintroducon, rewiring
1 | INTRODUCTION
The pervasive loss of ecological interacons in the Anthropocene
jeopardizes the stability of ecosystems and can cause their collapse.
Defaunaon has been massively wiping out interacons in the last de-
cades (e.g., Dirzo et al., 2014; Gale et al., 2013; Kurten, 2013; Terborgh
et al., 2008). Nowadays, many habitats are in exncon debt of ecolog-
ical interacons (Valiente- Banuet et al., 2015), meaning that large pro-
porons of their remaining interacons are likely to vanish, silently but
inexorably, in the core of ecosystems worldwide. A key factor to mi-
gate this grave conservaon problem is to improve our understanding
on how many and which interacons can sll be rewired. To address this
issue, we propose the concept of credit of ecological interacons.
Unraveling the consequences of defaunaon for ecological pro-
cesses and establishing how to revert them have become a major
and urgent challenge (Iacona et al., 2016; Seddon, Griths, Soorae, &
Armstrong, 2014). Habitat loss, hunng, invasion, and other impacts
wipe out not only species, but also their interacons and funcons. To
shi the conservaon focus from species to a more funconal approach
is likely to be more eecve for the maintenance of ecosystem integ-
rity (Harvey, Gounand, Ward, & Alterma, 2016; Tylianakis, Didham,
Bascompte, & Wardle, 2008). Species reintroducon, ecological re-
placement, refaunaon (reintroducon of enre faunas to localies
where they have been exrpated; Oliveira- Santos & Fernandez, 2010),
and populaon reinforcement (the release of organisms into an exisng
populaon to enhance populaon viability; Seddon et al., 2014) have
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been used to migate defaunaon. Those strategies recover ecological
funcons and interacons (Seddon et al., 2014), restore self- regulang
ecosystems (Svenning et al., 2016), and can be the only way to retain
fundamental ecosystem services well into the Anthropocene.
Ever since the Theory of Island Biogeography (MacArthur &
Wilson, 1967) ecologists have been aware that species exncons
can be delayed aer habitat loss. If the area of an island or island- like
habitat gets smaller, it will tend to achieve a new, lower equilibrium
number of species aer a me span which Diamond (1972) called
relaxaon me. However, it took two further decades unl Tilman,
May, Lehman, & Nowak (1994) coined the related term exncon
debt, which refers to the number or proporon of species expected to
become exnct following habitat disturbance (Kuussaari et al., 2009).
Acknowledging that a given species may persist in spite of habitat
loss merely because insucient me has elapsed (for it to go exnct),
and being able to quanfy the size of this “debt” are key insights for
understanding species richness in recently modied landscapes and
for conservaon planning as well (Jackson & Sax, 2009). Valiente-
Banuet et al. (2015) showed that just as species exncons lag be-
hind habitat loss, interacon loss is delayed aer an environmental
disturbance. They dene exncon debt of ecological interacons as
“any future interacon loss that has to be realized due to a current or
past environmental disturbance” and show that there is a mismatch
between species and interacon exncon curves that aects eco-
logical funcons.
Herein, we propose a new concept that advances our understand-
ing of interacon recovery by shiing the focus from debt to credit.
The number of interacons that can be restored in a focal area follow-
ing species colonizaon or reintroducon can usefully be understood
as that area’s credit of ecological interacons. Just as the exncon debt
may take a long me to be “paid,” there should also be a delay unl
the credit of ecological interacons can be “cashed”—that is, unl the
interacons are fully restored. In early refaunaon or colonizaon,
species with low abundances can sll be considered as exnct from
an ecological or funconal point of view; thus, one would not expect
them to play their full ecological roles immediately aer reintroduc-
on. There should also be a rewiring me, here dened as the me
span unl the credit of ecological interacons of a focal habitat is fully
cashed, that is, all interacons that could be restored have become
funconal again. Just as the relaxaon toward the new equilibrium
number of species in island biogeography, the rewiring process should
be asymptoc, with most interacons being restored much before re-
wiring me.
Ecosystems around the world have disnct amounts of ecological
interacons to be restored. Thus, quanfying the credit of ecological
interacons for dierent areas can be a useful tool for seng conser-
vaon priories, especially in refaunaon. In the following secons,
we explore the idea of credit of ecological interacons and discuss
its applicaons, focusing on species reintroducons in forest ecosys-
tems and on plant–animal interacons. We then present the reintro-
ducon of an important seed disperser in tropical forests, the agou
Dasyprocta leporina in Tijuca Naonal Park (TNP), Brazil, as an empiri-
cal example of the credit of ecological interacons cashing.
2 | FACTORS THAT AFFECT THE CASHING
OF THE CREDIT OF ECOLOGICAL
INTERACTIONS
Cashing the credit of ecological interacons is a result of fullling the
species credit (i.e., the number of species that will potenally recover
due to habitat quality improvement; Jackson & Sax, 2009). The credit is
the number of interacons that is expected to be rewired in a focal area
following species addion. It will be gradually cashed aer reintroduc-
on, at a rate that is inuenced by the following variables: (1) abundance
of the reintroduced species, (2) abundance of the interacng species
(i.e., abundance of the species that are known for interacng with the
reintroduced one), and (3) traits of reintroduced species (such as gener-
alists vs. specialists). We built a simple theorecal model to illustrate our
conceptual development predicons. The model simulates the release
of individuals belonging to a hypothecal animal populaon and its ex-
pansion over an area lled with potenally interacng plant species, as a
proxy of populaon increase through me. A detailed descripon of the
model is given in Appendix S1. The credit of ecological interacons that
can be cashed through a given reintroducon is the number of species
found in the area that are available to interact with the released one.
Thus, interacon richness and the rewiring me can be quaned by
monitoring the reintroduced populaon’s diet, for example.
Populaon size is usually low in the early stages of a reintroducon,
and factors like Allee eects and dependence on supplementary food
may hinder its growth for some me. Thereaer, provided that abun-
dance and occupancy are closely related (Mackenzie et al., 2006), the
populaon would tend to occupy a gradually increasing area, enhancing
its potenal interacon network. In that stage, one would expect the
populaon to rewire interacons at peak rates (Figure 1). Later on, the
pace of rewiring would tend to decrease gradually. At this stage, most
of the interacons with common species would have been rewired al-
ready, and only the ones with the rare species would remain. The curve
would grow asymptocally unl the point when the populaon occu-
pied the whole area, all potenal interacons would have been rewired,
and thus, the credit would have been fully cashed (Figure 1).
Considering species traits, when reintroducing generalist animals
one should expect a high interacon gain per species and per unit of
me due to the higher number of links established (Devictor et al.,
2010). Hence, generalists allow a habitat to cash the credit of ecolog-
ical interacons faster than specialists (Figure 1). On the other hand,
as they link with more species they would take longer than special-
ists to rewire all the potenal interacons (Figure 1). One should also
expect weaker, more redundant interacons as generalist species are
added (Jordano, Bascompte, & Olesen, 2002); however, this can be
benecial in long term because it would increase ecosystem resilience
in face of species loss (García, Marnez, Herrera, & Morales, 2013;
Walker, 1995). A study on the refaunaon of Gorongosa Naonal Park
(Mozambique) exemplies how the addion of generalist seed dispers-
ers can enhance funconal redundancy and why it can be benecial
for the restoraon of ecological processes. Although there was some
overlap on the plant species used by the reintroduced fauna, they
GENES
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3
found a higher richness of dispersed plant species where the animals
were released, when compared to a defaunated adjacent area (Correia
et al., 2016). Thus, placing generalist species rst in a refaunaon se-
quence (Gale, Pires, Brancalion, & Fernandez, 2016) would simul-
taneously provide higher interacon richness for the target area and
increase ecosystem stability through redundancy in funconal roles.
Regarding specialists, one should expect the number of re-
established interacons to be more proporonal to the number of
species added, as they usually build fewer links (Devictor et al., 2010).
The credit of interacons cashed by the addion of specialists is lower
than for generalists, and their overall rate of cashing the credit per
unit of me tends to be slower than for generalists (Figure 1). On the
other hand, they should link with rare species faster and would tend to
establish stronger and less redundant interacons. Even though they
cash a lower credit, specialists should be reintroduced at some point
because they are the only ones able to rewire some key interacons
(McCann, 2000). Specialized interacons can also favor host plant spe-
cies that have keystone roles in forest funconing, as observed for
g–wasp interacons (e.g., Weiblen, 2002).
3 | INTERACTION REWIRING FOLLOWING
AGOUTI REINTRODUCTION IN THE
ATLANTIC FOREST
Consider the reintroducon of agous (D. leporina) to Tijuca Naonal
Park (TNP), an Atlanc Forest reserve within Rio de Janeiro city, Brazil,
as an empirical example of the applicaon of the concept. This was
the rst step of a refaunaon program started in 2010 with the goal
of restoring ecological processes, especially the recruitment of large-
seeded trees. Agous were chosen as the rst species because of
their high ecological benets to the local ecosystem, as these scaer-
hoarding rodents are excellent dispersers of many large- seeded plants
in tropical forests and the only dispersers of some species (e.g., Pires
& Gale, 2012). Reintroduced animals were monitored by radio-
tracking (Cid, Figueira, Mello, Pires, & Fernandez, 2014), and all plant
species they interacted with were recorded. Based on a previous list
of the TNP ora and literature records of the agou’s diet (Table A1),
we esmated how much credit of ecological interacons could be
cashed by their reintroducon to the TNP, that is, the number of plant
species that are known for being used in agou’s diet.
We idened 65 plant species in TNP ora that can be used by
agous. At least 23 of them are large- seeded tree species that rely
on agous for dispersal and recruitment (Table A1). As expected,
the number of interacons increased with the me since release
(Figure 2). Reintroduced agous consumed fruits from at least 23 spe-
cies in the rst 15 months aer release, burying seeds of the large-
seeded trees Astrocaryum aculeassimum (Arecaceae), Sterculia chicha
(Malvaceae), and Joannesia princeps (Euphorbiaceae) (Cid et al., 2014;
Zucarao, 2013). This example illustrates how the credit of ecologi-
cal interacons operates in pracce. As predicted by our theorecal
model (Figure 1), during the rst months the agous interacted with
few species and it took some me for their interacon richness to
increase, thus lowering the remaining credit. As the populaon ex-
panded, agous linked to more plant species. Immediately aer re-
lease, the scaer- hoarding rodents interacted with the most common
FIGURE1 Relationship between number of population
expansions and cumulative rewired ecological interactions.
The circles show interaction richness cumulative increase after
population expansion. The triangles represent the credit of ecological
interactions cashing following population expansion. The shaded area
shows the interaction richness’ range (100% confidence intervals).
White colors indicate specialists, and black colors are the generalist
species. Dotted lines point the population expansion stage in which
each species rewires their maximal contribution to the area’s credit
of ecological interactions (100 species to generalists and 25 to
specialists)
FIGURE2 Rewiring of ecological interactions after the agouti
reintroduction in Tijuca National Park (TNP), Rio de Janeiro, Brazil.
The left vertical axis (interaction richness) shows the number of plant
species known to be part of the agouti’s diet; its highest value shows
the total number of plants in TNP that are known to interact with
agoutis (65), thus representing the credit of ecological interactions
following agouti reintroduction in TNP. The right axis (credit of
ecological interactions) shows the remaining credit, after a part of it
has been cashed by the rewiring already achieved by the agoutis
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GENES
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trees, such as the palm A. aculeassimum, but did not use rare spe-
cies, such as the Lecythidaceae, before 15 months (for details, see
Table A1). Another factor that aects the credit cashing is the plants’
phenology, because several months may pass before a tree starts
to ower and frucfy following its disperser’s release. Furthermore,
capve- born released individuals may be naïve or unaccustomed to
nave plant species, which means they take some me to learn how
to forage; the wild- born generaons should interact faster with more
species. Although the agou reintroducon was not designed to test
the credit of ecological interacons, the paerns found comply well
with our theorecal model (Appendix S1: Fig. A1). To beer evaluate
our framework, future studies should assess the rewiring of ecological
interacons connuously and for a longer period.
4 | PERSPECTIVES FOR APPLYING THE
CONCEPT IN PRACTICE
It should be useful to think about the limitaons of the credit of
ecological interacons approach. If exrpaon of a species also ex-
nguishes all interacons it was involved in, on the other hand one
cannot be sure that reintroducing the same species will rewire all
interacons that existed before exrpaon. Reintroducon usually
takes place decades aer exrpaon, when the ecosystem could have
changed to a new conguraon (e.g., dramac increase in other popu-
laons or a surrogate species that “occupied” the former interacons)
(Gale et al., 2013; Polak & Saltz, 2011). However, the approach
could be useful even in those situaons, as the credit can be esmated
using the number of species sll present in the area that are known to
interact with the reintroduced one.
Another potenal problem, when quanfying the credit of eco-
logical interacons, is that released individuals can fail to develop
expected interacons or develop unexpected ones, especially if they
are naïve capve animals. More generally, ecological interacons can
be hard to predict beforehand. An example is the reintroducon of
wolves in Yellowstone Naonal Park (Bangs & Fris, 1996). Aer 65
years without wolves, their reintroducon in 1995 changed the dy-
namics of several animal and plant species, revealing cascade eects
(Bangs & Fris, 1996; Smith, Peterson, & Houston, 2003). The direct
eect was on elks (Cervus elaphus), which are a primary prey for wolves
(Mech, Smith, Murphy, & MacNulty, 2001; Smith & Bangs, 2009).
Aer wolf exrpaon, elk populaon boomed and their overbrowsing
caused a state change in the riparian plant community (Wolf, Cooper,
& Hobbs, 2007). The reintroduced wolves reduced the elk populaon
(Ripple & Beschta, 2003) and induced elks to select higher places with
more forest cover (Mao et al., 2005). Thus, in the lower open patches,
browsing by elk was lowered and the riparian zone recovered (Ripple
& Beschta, 2003). Nevertheless, the alternave state that had been
established by the wolf exrpaon was resilient and the reintroduc-
on could not return the ecosystem to its original state aer 17 years
(Marshall, Hobbs, & Cooper, 2013).
As an opposite example, the largemouth bass (Micropterus sal-
moides) was exrpated in Lake Michigan in 1978 and reintroduced in
1986 (Mielbach, Turner, Hall, Reg, & Osenberg, 1995). The elimina-
on of the bass caused profound changes in the community under its
inuence, in a top- down eect. In this case, unlike the Yellowstone’s,
the system remained in the new state unl the reintroducon of the
bass, when it predictably turned back to its original state. In either
case, our approach would sll be useful, because it provides an es-
maon of a baseline number of interacons that should maintained, as
much as possible, even when the ecosystem changes.
5 | IMPLICATIONS FOR CONSERVATION
AND MANAGEMENT
The applicaon of the credit of ecological interacons concept can
provide an objecve criterion for management and decision mak-
ing in conservaon. So far, there has been no established method to
evaluate the actual success of reintroducons in restoring ecological
processes (Polak & Saltz, 2011). Using the credit of ecological inter-
acons, on the other hand, the reintroducon would be considered
as successful when all the credit, or an a priori dened proporon of
it, had been cashed. Esmang the credit of interacons can also be
useful for ascertaining how the benets for ecological services (e.g.,
seed dispersal) balance the costs of reintroducon, as compared to
other management opons. For example, when even generalist spe-
cies could cash only a lile credit of ecological interacons in an area,
the best choice would probably be to rst restore the plant com-
munity through reforestaon and then reintroduce animals. On the
other hand, if a rare plant was endangered because its recruitment is
impaired by the loss of frugivores, it would be advantageous to rein-
troduce a more specialist animal that would cash its credit faster, by
means of seed dispersal, in me to prevent exncon. Finally, this
concept is likely to be helpful in adapve management, as dierent
strategies can be applied according to the observed credit cashing and
rewiring me.
Cashing the credit can be useful in areas with a high debt of eco-
logical interacons, to prevent further species exncons and the de-
pleon of ecosystem services. Refaunaon can be an eecve way of
allowing a system to cash its credit of ecological interacons. To prop-
erly restore ecological processes in defaunated natural forest patches,
Gale et al. (2016) propose a species reintroducon sequence for tro-
phic rewilding (Svenning et al., 2016). This logical sequence for species
inseron begins with generalists of lower trophic levels, such as her-
bivores, followed by more specialist species and/or those that occupy
higher trophic posions (Gale et al., 2016). This sequence is relevant
for re- establishing resilient ecosystems, as ecological networks are rel-
avely robust to the loss of specialists, while fragile to the exncon of
generalists (Bascompte & Stouer, 2009). The credit of ecological inter-
acons framework should improve decision making on this sequence
by providing addional informaon on which species would cash its
full credit faster, bringing benets to network structure. Moreover, spe-
cies that bring a higher credit are important for the maintenance and/
or reconstrucon of community structure and can drive ecological and
coevoluonary dynamics (Guimarães Jr, Jordano, & Thompson, 2011).
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Besides, reconstrucng an ecosystem with high interacon diversity
helps in stabilizing ecosystem processes under uctuang environmen-
tal condions (Tylianakis, Laliberté, Nielsen, & Bascompte, 2010), thus
developing higher ecosystem resilience under climate change.
The credit of ecological interacons and its related concepts
provide a useful conceptual framework to understand how ecologi-
cal interacons can be rewired and to help in deciding among man-
agement opons aiming to restore ecological processes. We believe
this framework also provides a fruiul avenue of research, fetching
some important quesons for the coming years. It is sll important
to unravel how the variables that determine the credit of ecological
interacons inuence the rewiring me. Besides, it would be useful to
devise methods incorporang network properes to assess rewiring
in pracce, which could help to relate the number and identy of rein-
troduced species to their eecvity to restore ecological interacons
in the Anthropocene.
ACKNOWLEDGMENTS
We are in debt to Luiza Figueira who kindly provided data for the
empirical example. Personal grants were provided by Coordenação de
Aperfeiçoamento Pessoal de Nível Superior (CAPES) for LG, Conselho
Nacional de Pesquisa e Desenvolvimento Cienco e Tecnológico
(CNPq) for FASF and ASP, and Fundação de Amparo à Pesquisa
do Estado do Rio de Janeiro (FAPERJ) for BC. Fundação Grupo
Bocário de Proteção à Natureza, CNPq, and FAPERJ funded our re-
search. Henrique Zaluar provided TNP’s species list that we used in
our empirical example. We also thank all the people involved in the
REFAUNA- Rio Project for their collaboraon in the reintroducons
and discussions.
CONFLICT OF INTEREST
None declared.
DATA ACCESSIBILITY
All data used are within the paper or in appendix.
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How to cite this arcle: Genes L, Cid B, Fernandez FAS,
Pires AS. Credit of ecological interacons: A new conceptual
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Ecol Evol. 2017;00:1–6. doi: 10.1002/ece3.2746.
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