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As defaunation spreads through the world, there is an urgent need for restoring ecological interactions, thus assuring ecosystem processes. Here, we define the new concept of credit of ecological interactions, as the number of interactions that can be restored in a focal area by species colonization or reintroduction. We also define rewiring time, as the time span until all the links that build the credit of ecological interactions of a focal area have become functional again. We expect that the credit will be gradually cashed following refaunation in rates that are proportional to (1) the abundance of the reintroduced species (that is expected to increase in time since release), (2) the abundance of the local species that interact with them, and (3) the traits of reintroduced species. We illustrated this approach using a theoretical model and an empirical case study where the credit of ecological interactions was estimated. This new conceptual framework is useful for setting reintroduction priorities and for evaluating the success of conservation initiatives that aim to restore ecosystem services.
Ecology and Evoluon 2017; 1–6
Received: 22 November 2016 
  Revised: 12 December 2016 
  Accepted: 18 December 2016
DOI: 10.1002/ece3.2746
Credit of ecological interacons: A new conceptual framework
to support conservaon in a defaunated world
Luísa Genes1| Bruno Cid1| Fernando A. S. Fernandez1| Alexandra S. Pires2
This is an open access arcle under the terms of the Creave Commons Aribuon License, which permits use, distribuon and reproducon in any medium,
provided the original work is properly cited.
© 2017 The Authors. Ecology and Evoluon published by John Wiley & Sons Ltd.
1Departamento de Ecologia, Universidade
Federal do Rio de Janeiro, Rio de Janeiro, RJ,
2Departamento de Ciências Ambientais,
Universidade Federal Rural do Rio de Janeiro,
Seropédica, RJ, Brazil
Luísa Genes, Departamento de Ecologia,
Universidade Federal do Rio de Janeiro, Rio de
Janeiro, RJ, Brazil.
Funding informaon
Coordenação de Aperfeiçoamento Pessoal de
Nível Superior (CAPES); Conselho Nacional
de Pesquisa e Desenvolvimento Cienco e
Tecnológico (CNPq); Fundação de Amparo
à Pesquisa do Estado do Rio de Janeiro
(FAPERJ); Fundação Grupo Bocário de
Proteção à Natureza.
As defaunaon spreads through the world, there is an urgent need for restoring eco-
logical interacons, thus assuring ecosystem processes. Here, we dene the new con-
cept of credit of ecological interacons, as the number of interacons that can be
restored in a focal area by species colonizaon or reintroducon. We also dene rewir-
ing me, as the me span unl all the links that build the credit of ecological interac-
ons of a focal area have become funconal again. We expect that the credit will be
gradually cashed following refaunaon in rates that are proporonal 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 theorecal model and an em-
pirical case study where the credit of ecological interacons was esmated. This new
conceptual framework is useful for seng reintroducon priories and for evaluang
the success of conservaon iniaves that aim to restore ecosystem services.
conservaon management, ecological interacons, ecosystem funconing, refaunaon,
reintroducon, rewiring
The pervasive loss of ecological interacons in the Anthropocene
jeopardizes the stability of ecosystems and can cause their collapse.
Defaunaon has been massively wiping out interacons 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 exncon debt of ecolog-
ical interacons (Valiente- Banuet et al., 2015), meaning that large pro-
porons of their remaining interacons are likely to vanish, silently but
inexorably, in the core of ecosystems worldwide. A key factor to mi-
gate this grave conservaon problem is to improve our understanding
on how many and which interacons can sll be rewired. To address this
issue, we propose the concept of credit of ecological interacons.
Unraveling the consequences of defaunaon for ecological pro-
cesses and establishing how to revert them have become a major
and urgent challenge (Iacona et al., 2016; Seddon, Griths, Soorae, &
Armstrong, 2014). Habitat loss, hunng, invasion, and other impacts
wipe out not only species, but also their interacons and funcons. To
shi the conservaon focus from species to a more funconal approach
is likely to be more eecve for the maintenance of ecosystem integ-
rity (Harvey, Gounand, Ward, & Alterma, 2016; Tylianakis, Didham,
Bascompte, & Wardle, 2008). Species reintroducon, ecological re-
placement, refaunaon (reintroducon of enre faunas to localies
where they have been exrpated; Oliveira- Santos & Fernandez, 2010),
and populaon reinforcement (the release of organisms into an exisng
populaon to enhance populaon viability; Seddon et al., 2014) have
   GT Aal
been used to migate defaunaon. Those strategies recover ecological
funcons and interacons (Seddon et al., 2014), restore self- regulang
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 exncons
can be delayed aer 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 aer a me span which Diamond (1972) called
relaxaon me. However, it took two further decades unl Tilman,
May, Lehman, & Nowak (1994) coined the related term exncon
debt, which refers to the number or proporon of species expected to
become exnct following habitat disturbance (Kuussaari et al., 2009).
Acknowledging that a given species may persist in spite of habitat
loss merely because insucient me has elapsed (for it to go exnct),
and being able to quanfy the size of this “debt” are key insights for
understanding species richness in recently modied landscapes and
for conservaon planning as well (Jackson & Sax, 2009). Valiente-
Banuet et al. (2015) showed that just as species exncons lag be-
hind habitat loss, interacon loss is delayed aer an environmental
disturbance. They dene exncon debt of ecological interacons as
“any future interacon loss that has to be realized due to a current or
past environmental disturbance” and show that there is a mismatch
between species and interacon exncon curves that aects eco-
logical funcons.
Herein, we propose a new concept that advances our understand-
ing of interacon recovery by shiing the focus from debt to credit.
The number of interacons that can be restored in a focal area follow-
ing species colonizaon or reintroducon can usefully be understood
as that area’s credit of ecological interacons. Just as the exncon debt
may take a long me to be “paid,” there should also be a delay unl
the credit of ecological interacons can be “cashed”—that is, unl the
interacons are fully restored. In early refaunaon or colonizaon,
species with low abundances can sll be considered as exnct from
an ecological or funconal point of view; thus, one would not expect
them to play their full ecological roles immediately aer reintroduc-
on. There should also be a rewiring me, here dened as the me
span unl the credit of ecological interacons of a focal habitat is fully
cashed, that is, all interacons that could be restored have become
funconal again. Just as the relaxaon toward the new equilibrium
number of species in island biogeography, the rewiring process should
be asymptoc, with most interacons being restored much before re-
wiring me.
Ecosystems around the world have disnct amounts of ecological
interacons to be restored. Thus, quanfying the credit of ecological
interacons for dierent areas can be a useful tool for seng conser-
vaon priories, especially in refaunaon. In the following secons,
we explore the idea of credit of ecological interacons and discuss
its applicaons, focusing on species reintroducons in forest ecosys-
tems and on plant–animal interacons. We then present the reintro-
ducon of an important seed disperser in tropical forests, the agou
Dasyprocta leporina in Tijuca Naonal Park (TNP), Brazil, as an empiri-
cal example of the credit of ecological interacons cashing.
Cashing the credit of ecological interacons is a result of fullling the
species credit (i.e., the number of species that will potenally recover
due to habitat quality improvement; Jackson & Sax, 2009). The credit is
the number of interacons that is expected to be rewired in a focal area
following species addion. It will be gradually cashed aer reintroduc-
on, at a rate that is inuenced by the following variables: (1) abundance
of the reintroduced species, (2) abundance of the interacng species
(i.e., abundance of the species that are known for interacng with the
reintroduced one), and (3) traits of reintroduced species (such as gener-
alists vs. specialists). We built a simple theorecal model to illustrate our
conceptual development predicons. The model simulates the release
of individuals belonging to a hypothecal animal populaon and its ex-
pansion over an area lled with potenally interacng plant species, as a
proxy of populaon increase through me. A detailed descripon of the
model is given in Appendix S1. The credit of ecological interacons that
can be cashed through a given reintroducon is the number of species
found in the area that are available to interact with the released one.
Thus, interacon richness and the rewiring me can be quaned by
monitoring the reintroduced populaon’s diet, for example.
Populaon size is usually low in the early stages of a reintroducon,
and factors like Allee eects and dependence on supplementary food
may hinder its growth for some me. Thereaer, provided that abun-
dance and occupancy are closely related (Mackenzie et al., 2006), the
populaon would tend to occupy a gradually increasing area, enhancing
its potenal interacon network. In that stage, one would expect the
populaon to rewire interacons at peak rates (Figure 1). Later on, the
pace of rewiring would tend to decrease gradually. At this stage, most
of the interacons with common species would have been rewired al-
ready, and only the ones with the rare species would remain. The curve
would grow asymptocally unl the point when the populaon occu-
pied the whole area, all potenal interacons 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 interacon 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 interacons 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 potenal interacons (Figure 1). One should also
expect weaker, more redundant interacons as generalist species are
added (Jordano, Bascompte, & Olesen, 2002); however, this can be
benecial in long term because it would increase ecosystem resilience
in face of species loss (García, Marnez, Herrera, & Morales, 2013;
Walker, 1995). A study on the refaunaon of Gorongosa Naonal Park
(Mozambique) exemplies how the addion of generalist seed dispers-
ers can enhance funconal redundancy and why it can be benecial
for the restoraon of ecological processes. Although there was some
overlap on the plant species used by the reintroduced fauna, they
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 refaunaon se-
quence (Gale, Pires, Brancalion, & Fernandez, 2016) would simul-
taneously provide higher interacon richness for the target area and
increase ecosystem stability through redundancy in funconal roles.
Regarding specialists, one should expect the number of re-
established interacons to be more proporonal to the number of
species added, as they usually build fewer links (Devictor et al., 2010).
The credit of interacons cashed by the addion 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 interacons. 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 interacons
(McCann, 2000). Specialized interacons can also favor host plant spe-
cies that have keystone roles in forest funconing, as observed for
g–wasp interacons (e.g., Weiblen, 2002).
Consider the reintroducon of agous (D. leporina) to Tijuca Naonal
Park (TNP), an Atlanc Forest reserve within Rio de Janeiro city, Brazil,
as an empirical example of the applicaon of the concept. This was
the rst step of a refaunaon program started in 2010 with the goal
of restoring ecological processes, especially the recruitment of large-
seeded trees. Agous were chosen as the rst species because of
their high ecological benets to the local ecosystem, as these scaer-
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 esmated how much credit of ecological interacons could be
cashed by their reintroducon to the TNP, that is, the number of plant
species that are known for being used in agou’s diet.
We idened 65 plant species in TNP ora that can be used by
agous. At least 23 of them are large- seeded tree species that rely
on agous for dispersal and recruitment (Table A1). As expected,
the number of interacons increased with the me since release
(Figure 2). Reintroduced agous consumed fruits from at least 23 spe-
cies in the rst 15 months aer release, burying seeds of the large-
seeded trees Astrocaryum aculeassimum (Arecaceae), Sterculia chicha
(Malvaceae), and Joannesia princeps (Euphorbiaceae) (Cid et al., 2014;
Zucarao, 2013). This example illustrates how the credit of ecologi-
cal interacons operates in pracce. As predicted by our theorecal
model (Figure 1), during the rst months the agous interacted with
few species and it took some me for their interacon richness to
increase, thus lowering the remaining credit. As the populaon ex-
panded, agous linked to more plant species. Immediately aer re-
lease, the scaer- hoarding rodents interacted with the most common
FIGURE1 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
FIGURE2 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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trees, such as the palm A. aculeassimum, but did not use rare spe-
cies, such as the Lecythidaceae, before 15 months (for details, see
Table A1). Another factor that aects the credit cashing is the plants’
phenology, because several months may pass before a tree starts
to ower and frucfy following its disperser’s release. Furthermore,
capve- born released individuals may be naïve or unaccustomed to
nave plant species, which means they take some me to learn how
to forage; the wild- born generaons should interact faster with more
species. Although the agou reintroducon was not designed to test
the credit of ecological interacons, the paerns found comply well
with our theorecal model (Appendix S1: Fig. A1). To beer evaluate
our framework, future studies should assess the rewiring of ecological
interacons connuously and for a longer period.
It should be useful to think about the limitaons of the credit of
ecological interacons approach. If exrpaon of a species also ex-
nguishes all interacons it was involved in, on the other hand one
cannot be sure that reintroducing the same species will rewire all
interacons that existed before exrpaon. Reintroducon usually
takes place decades aer exrpaon, when the ecosystem could have
changed to a new conguraon (e.g., dramac increase in other popu-
laons or a surrogate species that “occupied” the former interacons)
(Gale et al., 2013; Polak & Saltz, 2011). However, the approach
could be useful even in those situaons, as the credit can be esmated
using the number of species sll present in the area that are known to
interact with the reintroduced one.
Another potenal problem, when quanfying the credit of eco-
logical interacons, is that released individuals can fail to develop
expected interacons or develop unexpected ones, especially if they
are naïve capve animals. More generally, ecological interacons can
be hard to predict beforehand. An example is the reintroducon of
wolves in Yellowstone Naonal Park (Bangs & Fris, 1996). Aer 65
years without wolves, their reintroducon in 1995 changed the dy-
namics of several animal and plant species, revealing cascade eects
(Bangs & Fris, 1996; Smith, Peterson, & Houston, 2003). The direct
eect was on elks (Cervus elaphus), which are a primary prey for wolves
(Mech, Smith, Murphy, & MacNulty, 2001; Smith & Bangs, 2009).
Aer wolf exrpaon, elk populaon boomed and their overbrowsing
caused a state change in the riparian plant community (Wolf, Cooper,
& Hobbs, 2007). The reintroduced wolves reduced the elk populaon
(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 alternave state that had been
established by the wolf exrpaon was resilient and the reintroduc-
on could not return the ecosystem to its original state aer 17 years
(Marshall, Hobbs, & Cooper, 2013).
As an opposite example, the largemouth bass (Micropterus sal-
moides) was exrpated in Lake Michigan in 1978 and reintroduced in
1986 (Mielbach, Turner, Hall, Reg, & Osenberg, 1995). The elimina-
on of the bass caused profound changes in the community under its
inuence, in a top- down eect. In this case, unlike the Yellowstone’s,
the system remained in the new state unl the reintroducon of the
bass, when it predictably turned back to its original state. In either
case, our approach would sll be useful, because it provides an es-
maon of a baseline number of interacons that should maintained, as
much as possible, even when the ecosystem changes.
The applicaon of the credit of ecological interacons concept can
provide an objecve criterion for management and decision mak-
ing in conservaon. So far, there has been no established method to
evaluate the actual success of reintroducons in restoring ecological
processes (Polak & Saltz, 2011). Using the credit of ecological inter-
acons, on the other hand, the reintroducon would be considered
as successful when all the credit, or an a priori dened proporon of
it, had been cashed. Esmang the credit of interacons can also be
useful for ascertaining how the benets for ecological services (e.g.,
seed dispersal) balance the costs of reintroducon, as compared to
other management opons. For example, when even generalist spe-
cies could cash only a lile credit of ecological interacons in an area,
the best choice would probably be to rst restore the plant com-
munity through reforestaon 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 exncon. Finally, this
concept is likely to be helpful in adapve management, as dierent
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 interacons, to prevent further species exncons and the de-
pleon of ecosystem services. Refaunaon can be an eecve way of
allowing a system to cash its credit of ecological interacons. To prop-
erly restore ecological processes in defaunated natural forest patches,
Gale et al. (2016) propose a species reintroducon sequence for tro-
phic rewilding (Svenning et al., 2016). This logical sequence for species
inseron begins with generalists of lower trophic levels, such as her-
bivores, followed by more specialist species and/or those that occupy
higher trophic posions (Gale et al., 2016). This sequence is relevant
for re- establishing resilient ecosystems, as ecological networks are rel-
avely robust to the loss of specialists, while fragile to the exncon of
generalists (Bascompte & Stouer, 2009). The credit of ecological inter-
acons framework should improve decision making on this sequence
by providing addional informaon on which species would cash its
full credit faster, bringing benets to network structure. Moreover, spe-
cies that bring a higher credit are important for the maintenance and/
or reconstrucon of community structure and can drive ecological and
coevoluonary dynamics (Guimarães Jr, Jordano, & Thompson, 2011).
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Besides, reconstrucng an ecosystem with high interacon diversity
helps in stabilizing ecosystem processes under uctuang environmen-
tal condions (Tylianakis, Laliberté, Nielsen, & Bascompte, 2010), thus
developing higher ecosystem resilience under climate change.
The credit of ecological interacons and its related concepts
provide a useful conceptual framework to understand how ecologi-
cal interacons can be rewired and to help in deciding among man-
agement opons aiming to restore ecological processes. We believe
this framework also provides a fruiul avenue of research, fetching
some important quesons for the coming years. It is sll important
to unravel how the variables that determine the credit of ecological
interacons inuence the rewiring me. Besides, it would be useful to
devise methods incorporang network properes to assess rewiring
in pracce, which could help to relate the number and identy of rein-
troduced species to their eecvity to restore ecological interacons
in the Anthropocene.
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 Cienco e Tecnológico
(CNPq) for FASF and ASP, and Fundação de Amparo à Pesquisa
do Estado do Rio de Janeiro (FAPERJ) for BC. Fundação Grupo
Bocário 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 collaboraon in the reintroducons
and discussions.
None declared.
All data used are within the paper or in appendix.
Bangs, E. E., & Fris, S. H. (1996). Reintroducing the gray wolf to cen-
tral Idaho and Yellowstone Naonal Park. Wildlife Society Bullen, 24,
Bascompte, J., & Stouer, D. B. (2009). The assembly and disassembly of
ecological networks. Philosophical Transacons of the Royal Society B:
Biological Sciences, 364, 1781–1787.
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... Resilience metrics are used to evaluate the capacity of a community to recover to its baseline state following alteration, such as how the Gulf of Mexico community might recover following the Deepwater Horizon oil spill (Morzaria-Luna et al. 2018). Resilience might by estimated by how many interactions in a system recover following an extirpated species' reintroduction (referred to as the credit of ecological interactions; Genes et al. 2017), or the expected length of time following species reintroductions until all the links between species are functional (referred to as rewiring time; Genes et al. 2017). This type of analysis can also be used to identify focal points for management actions, facilitating community resilience; this view of resilience measures the amount of external input required for community recovery. ...
... Resilience metrics are used to evaluate the capacity of a community to recover to its baseline state following alteration, such as how the Gulf of Mexico community might recover following the Deepwater Horizon oil spill (Morzaria-Luna et al. 2018). Resilience might by estimated by how many interactions in a system recover following an extirpated species' reintroduction (referred to as the credit of ecological interactions; Genes et al. 2017), or the expected length of time following species reintroductions until all the links between species are functional (referred to as rewiring time; Genes et al. 2017). This type of analysis can also be used to identify focal points for management actions, facilitating community resilience; this view of resilience measures the amount of external input required for community recovery. ...
... The number of interactions expected to be rewired (reconfigured) in a focal area following species reintroduction How many interactions from the original Brazilian forest system will be reestablished with the reintroduction of agoutis (Dasyprocta leporina)? (Genes et al. 2017) Recovery time from a perturbation in a system with a tipping point between stable states How long does it take a forest to recover after harvest or burning in a tropical peat community in which there is a tipping point? (Dieleman et al. 2015) Probability that a community will recover to a reference state after a perturbation Population size below which one or more other species in the network become extinct ...
Community viability analysis (CVA) has been put forth as an analogue for population viability analysis (PVA), an accepted conservation tool for evaluating species-specific threat and management scenarios. The original proposal recommended that CVAs examine resistance-based questions. PVAs, however, are broadly applicable to multiple types of viability questions, suggesting that the original CVA definition may be too narrow. In the present article, we advance an expanded framework in which CVA includes any analysis assessing the status, threats, or management options of an ecological community. We discuss viability questions that can be investigated with CVA. We group those inquiries into categories of resistance, resilience, and persistence, and provide case studies for each. Finally, we broadly present the steps in a CVA.
... However, most reintroductions are focused solely on species conservation, and their effects on ecological and ecosystem functions are seldom evaluated (Polak and Saltz, 2011). One way to evaluate the effect of reintroductions on ecological processes is to estimate the number of restored interactions (Genes et al., 2017). However, two animal species can interact with the same plant species and have different effects on it Lugon et al., 2017). ...
... To evaluate the effect of the reintroduction of howler monkeys (mean female weight: 4.35 kg; mean male weight: 6.73 kg; Smith and Jungers, 1997) in Tijuca, we first selected the mammal and avian species with whose diets the howlers' fruit diet overlapped the most. We determined the howlers' potential diet in Tijuca based on data from a previous study conducted in other localities (Genes et al., 2017). We then used the Atlantic frugivory dataset to compare the howlers' diet to that of the other frugivores in Tijuca. ...
The loss of larger frugivores alters seed dispersal. Species reintroductions have been proposed as a strategy for reversing local disperser extinctions. However, their effects on ecological processes have seldom been assessed. Howler monkeys (Alouatta guariba) have been reintroduced in Tijuca National Park, a defaunated Atlantic Forest fragment. We compared the fate of seeds dispersed by howlers to dispersal by two other frugivores present in the park: capuchin monkeys (Sapajus nigritus) and guans (Penelope superciliaris). Howlers produce clumped defecations that attract dung beetles, which provide secondary dispersal by burying seeds embedded in feces. We expected that seeds dispersed by howlers would have a different fate from those dispersed by capuchins and guans, since their scattered defecations are less attractive to dung beetles. We followed the fate of seeds 3–14 mm in diameter through three processes after seed deposition: secondary dispersal, predation, and seedling emergence. We estimated the probabilities in each step according to the primary disperser and plant species. Dispersal by howlers increased the recruitment of large-seeded plants because of the higher probability of secondary dispersal of the seeds in their feces. Fewer of the seeds dispersed by capuchins or guans were buried, regardless of size, and burial depths were shallower. For 3 mm seeds, the final recruitment probability was similar across frugivores. However, more of the larger seeds reached the seedling stage when dispersed by howlers since they were buried more deeply, which increased their survival without affecting seedling emergence. Reintroductions can thus contribute to restoring ecological processes.
... Likewise, the addition of new species can also change network structure, and thus, network analysis can be used to predict how reintroductions affect ecological communities (Pires 2017). In this sense, we would expect that interaction restoration through species reintroduction would increase ecosystem resilience through the addition of new, and often unique, pairwise interactions (Tylianakis et al. 2010, Genes et al. 2017. ...
... Previous studies had suggested that reintroductions could potentially benefit communities through changes in the network structure (Genes et al. 2017, Pires 2017. However, to our knowledge, this is the first work to show those effects with de facto reintroductions. ...
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Species reintroductions can be used as a conservation strategy to restore ecological interactions and the functionality of impoverished ecosystems. The ecological effects of reintroductions go beyond restoring pairwise interactions, because reintroductions can change how extant species are indirectly linked to each other in an ecological community. These indirect pathways, in turn, may shape a myriad of ecological and evolutionary processes operating in ecological systems. Here, we investigated how reintroductions may affect the direct and indirect pathways connecting species in ecological networks. We modeled the potential effects of the reintroduction of four frugivore species (channel-billed toucans, red-humped agoutis, brown howler monkeys and yellow-footed tortoises) to the local seed dispersal network in an Atlantic Forest site, the Tijuca National Park (Rio de Janeiro, Brazil). We used a seed dispersal interaction dataset together with data on species occurrences in Tijuca to build network models. Then, we calculated how network structure and the total amount of indirect effects varied across simulated networks with and without the reintroduced species. Using random reintroduction simulations, we tested if the observed network changes were expected merely from the increase in species richness. The reintroduction of the frugivore species increased network connectance, nestedness, robustness, number of pathways and total amount of indirect effects in all simulated networks. The increase in number of pathways with the addition of the four reintroduced species was greater than the sum of isolated effects for each species, because some interaction pathways contained several reintroduced species. These changes in network metrics were significantly greater than if a randomly chosen set of four species was reintroduced. Furthermore, our results indicate that multiple reintroductions in the same area, known as refaunation, may have an even greater restoration effect than single species reintroductions through increased indirect connections in the network.
... A possible way to evaluate the effect of reintroductions on ecological processes is to estimate the number of restored interactions (Genes et al. 2017). ...
... Diet overlap was based on data from the Atlantic Frugivory data set , the most complete set of frugivory interactions from the Atlantic Forest so far. The selection of seed species was based on the howler's credit of ecological interactions in the TNP (Genes et al. 2017), that is, the list of TNP's plant species with which the howler has the potential to interact. We chose species of plants whose genera (or species) were also part of the capuchin monkey and guan diet. ...
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The biased loss of large and medium frugivores alters seed dispersal and plant regeneration. Species reintroductions have been proposed as a strategy to reverse the consequences of species loss. However, reintroductions effects on ecological processes are seldom accessed, which hinders the comprehension of reintroductions' potential to reestablish functioning ecosystems. In this study, we investigate the effect of howler monkey Alouatta guariba reintroduction in the plant regeneration of Tijuca National Park (TNP), a highly defaunated Atlantic Forest fragment. Howlers are medium sized folivore-frugivore primates, whose large clumped defecations attract dung beetles. Dung beetles bury seeds present in howlers' feces, a process known as secondary seed dispersal. Thus, we expect that the fate of seeds dispersed by howlers will differ from those dispersed by the other frugivores present in the Park. We followed the fate of seeds between 3 and 14mm in diameter in three steps of the seed dispersal loop, each consisting of a different experiment. First, we estimated secondary seed dispersal and burial depth probabilities according to the frugivores' defecation pattern; then, predation probability in different burial depths and defecation patterns; and, finally, recruitment probability in different burial depths. Considering the final result of the three experiments, the howlers' reintroduction affected positively the regeneration of large seeds. 3mm seeds did not benefit as much because they weren't frequently predated at shallower depths and couldn't recruit when deeply buried. Seeds larger than 3mm reached more frequently the seedling stage when dispersed by howlers than when dispersed by other animals present in the Park. Thus, howler monkey reintroduction in defaunated areas, consisting mainly of smaller frugivores, whose defecation pattern doesn't attract dung beetles as frequently, improves the regeneration of large seeds. We hope that this study will stimulate the resuming of howler reintroduction in TNP, as well as new howler reintroductions in defaunated areas.
... Understanding interspecific interactions is important to assess the specific roles of species in complex ecological networks (Tylianakis & Morris, 2017) and to develop effective strategies for biodiversity conservation (Genes et al., 2017). Recent advances in molecular techniques have significantly improved our knowledge of ecological networks (Evans et al., 2016). ...
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Many species of dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae) are coprophages and possess trophic connections with mammalian dung. Recent studies have shown that the use of genetic information from dung beetle guts (invertebrate‐derived DNA or iDNA) allows for the detection of mammals in a given habitat without intensively surveying the area. However, these studies used live or freshly killed beetles instead of preserved specimens. Here, we assessed the feasibility of extracting and sequencing iDNA from dung beetles that were collected using conventional baited pitfall traps with a mixture of propylene glycol and ethanol. We extracted iDNA from the guts of 18 dung beetles, comprising three species and three functional groups, collected from a seasonal tropical forest in Xishuangbanna, China. Eight mammalian species were detected, including rare species not previously recorded at the same location. Among the three functional groups, paracoprids (tunnelers) yielded the highest number of mammal species. Our study shows that iDNA can be successfully sequenced from preserved specimens, provided they are stored under appropriate conditions. The proposed technique offers a viable alternative to traditional cafeteria experiments for understanding dung beetle‐mammal interactions and can serve as a valuable complementary approach to current mammal survey techniques.
... Hence, restoration strategies should foster the recovery of plant species through the management of natural regeneration or by planting saplings in high diversity. In defaunated landscapes, it might be necessary to reintroduce seed dispersers, in order to enhance plant diversity (Galetti et al., 2017;Genes et al., 2017). ...
... Under this framework, species that would promote a higher number of ecological interactions, or more unique interactions, may be prioritised, and species can be appropriately selected based on restoration goals (Genes et al., 2017;Marjakangas et al., 2018). Adding to this approach an abiotic layer that allows the assessment of the engineering effects of each species on their environment, would allow prioritisation of species with stronger engineering impacts. ...
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Biodiversity is crucial for supporting ecosystem functioning, yet some species play a disproportionate role in maintaining complex ecological processes. Ecosystem engineers are species that directly influence ecosystems by modifying biophysical environments, creating novel habitats, altering biogeochemical cycles, increasing biodiversity and/or modulating ecological processes. Although these species may substantially influence ecosystem functioning, their role is often overlooked and difficult to quantify. Understanding the status, dynamics and trends of ecosystem engineers is essential for mitigating biodiversity loss and maintaining healthy ecosystems. This review reveals the common but underappreciated roles that ecosystem engineers play in ecosystem functioning across many different taxa, biomes and ecological processes. We first synthesise how knowledge of ecosystem engineering improves our understanding of species interactions and the ecological processes underlying both ecosystem functioning and BEF relationships. We provide a conceptual model for addressing the effects of ecosystem engineers in BEF research and ecological dynamics. We provide a ‘how to’ analytical framework for monitoring and quantifying changes in ecosystem engineers and their effects on ecosystem functioning. This framework includes (i) what variables to measure, how and at which scale; (ii) experiments involving species exclusion or removal, introduction and comparative designs when experimental manipulation is not feasible and (iii) statistical, data‐driven and theory‐driven models. We discuss how to leverage ecosystem engineering in the context of current global change and ecosystem restoration efforts. Including ecosystem engineers in conservation and restoration programs, when implemented in the appropriate context and supported by an understanding of ecological mechanisms and processes, may be crucial for sustaining biological diversity and functional ecosystems. Read the free Plain Language Summary for this article on the Journal blog.
... Global change has caused drastic declines in species populations worldwide (Dirzo et al., 2014), impoverishing ecosystems and ecological interactions (Valiente-Banuet et al., 2015;Genes et al., 2017). The dispersal of plant seeds by frugivores is a key biotic interaction (BI), and the disruption of this mutualistic interaction can impede ecosystem functioning. ...
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Biotic interactions are a crucial component of the plant regeneration process, which has been traditionally studied at more local scales, providing the tools for planning and decision-making. Studies showing the signature of species interactions at coarser spatial scales contrasting with animal-plant interactions at fine scales have been scarce. This study aimed at integrating an approach, over both biogeographic and local scales, by testing two endemic species of Mediterranean central Chile: the relict and southernmost threatened Chilean palm Jubaea chilensis (Chilean palm; Molina; Baillón) and the caviomorph scatter-hoarding rodent Octodon degus (Degu; Molina), on which this palm currently relies for seed dispersal. Integrating Geographic Information Systems and Ecological Niche Modeling, the intensity of seed-rodent interactions from a territorial perspective was evaluated in the range of the palm, at a biogeographic scale, identifying areas with greater or lesser potential for seed-rodent interactions; and in local populations, incorporating a variety of environmental factors that might affect palm regeneration. The present results show that the rodent (Octodon degus) may play a role in Chilean palm (Jubaea chilensis) seed dispersal and seed establishment, since; Chilean palm regeneration is higher in areas where both species co-occur. At a local scale, a prominent overlap between palm seedlings and degu burrows was also found, which, allied with other abiotic variables such as altitude and topographic humidity, are crucial for successful palm regeneration. Understanding the full extent of animal-plant interactions and how they are affected by habitat perturbation in a wide range will provide essential information for the design of effective conservation and management strategies, such as rewilding based on plant species.
... Effectively restoring zoochoric plant populations in a changing world is only feasible in combination with conservation or reintroduction of frugivores (Carvalho, 2020). Modeling of interaction credits (Genes et al., 2017) combined with joint species distributions have also shown the high potential of combined habitat restoration and trophic rewilding to restore ecological processes in the Brazilian Atlantic forest (Marjakangas et al., 2018). However, there is a lack of understanding on the effects of antagonistic (herbivory and seed predation) interactions in conservation strategies. ...
Ecosystem restoration is one of the most promising strategies for conservation in the Anthropocene. Within ecosystems, plant-animal interactions are critical to their functioning, biodiversity and to restoration success. However, there is no systematic assessment of such interactions across restoration efforts. We reviewed 127 articles that examined habitat restoration and trophic rewilding to synthesize knowledge on restoration of four key plant-animal interactions: seed dispersal, herbivory, pollination, and seed predation. We conducted a meta-analysis using a subset of 56 studies, which compared restored systems with degraded or reference systems. We addressed four questions: (i) To what extent are interactions recovered in restored sites compared to degraded and reference sites? (ii) Which management practices enhance interaction restoration? (iii) Which interactions and animal taxa were most frequently studied? and (iv) Is interaction restoration being studied in areas deemed critical for conservation? Seed dispersal was the most studied interaction, followed by herbivory, pollination, and seed predation. Mammals were the most studied group, followed by birds, insects, and reptiles. Importantly, occurrence of seed dispersal and pollination was more frequent in restored than degraded sites. While several studies were conducted in critical conservation sites, some biodiversity hotspots, particularly in Southeast Asia, have been understudied. Future research should focus on understudied interactions (e.g., seed predation) and taxa (e.g., insects and reptiles), so this information can be incorporated into practice. Considering the available studies, we find that both habitat restoration and trophic rewilding are effective in bringing seed dispersal and pollination to a better state than in degraded areas.
... The results give powerful insights on the roles of each group participating in this particular ecological process, as well as important information on the potential effect of rein- (White et al. 2015) and indicate areas that would benefit the most with certain species, by simulating the effect of reintroductions in different consumers and resource communities. Genes et al. (2017) proposed a conceptual framework to evaluate the success of reintroductions regarding the reestablishment of ecological processes. ...
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Functional diversity uses response and effect traits to understand how communities are affected by changes in the environment and the consequences of modifications on communities composition to the ecosystem functioning. However, most studies focus on a single taxonomic or functional group, ignoring that many processes result from interspecific interactions. Here we established a multi-trophic trait-based framework to evaluate the consequences of community change for ecological processes. Specifically, we estimate each species’ potential effect taking in account the consumers and resource communities involved on the trophic interaction. Both communities’ functional spaces are incorporated into a single analysis by using resource traits to estimate consumers’ functional space. The framework includes a parameter that allows giving different weights to unique interactions when estimating a species potential effect. We present two modifications for application using abundance and species richness data and two modifications to allow incorporating absent species into the analysis. Our framework can be used to investigate consequences of community changes in different situations, such as species extinctions, invasions and refaunation. To demonstrate the insights derived from our framework we use an exemplary study case of refaunation of an impacted tropical forest. This framework informs on a species contribution to an ecological process according to the uniqueness or redundancy of its interactions and the magnitude of its effect, indicated by the frequency of the resource’s community trait values with which it interacts. Thus, it helps to increase the understanding of the effects of changes in community composition on ecological processes resulting from trophic interactions. It assists practitioners and researches with predictions and evaluations on potential loss and reestablishment of ecological functions resulted from changes in community functional composition.
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Defaunation has a major driver of biodiversity loss in tropical forests. Here we discuss how to reverse defaunation by re-introducing key species in defaunated or restored forests.
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There exists little doubt that the Earth's biodiversity is declining. The Nature Conservancy, for example, has documented that one-third of the plant and animal species in the United States are now at risk of extinction. The problem is a monumental one, and forces us to consider in depth how we expect ecosystems, which ultimately are our life-support systems, to respond to reductions in diversity. This issue — commonly referred to as the diversity–stability debate — is the subject of this review, which synthesizes historical ideas with recent advances. Both theory and empirical evidence agree that we should expect declines in diversity to accelerate the simplification of ecological communities.
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Occupancy Estimation and Modeling: Inferring Patterns and Dynamics of Species Occurrence, Second Edition, provides a synthesis of model-based approaches for analyzing presence-absence data, allowing for imperfect detection. Beginning from the relatively simple case of estimating the proportion of area or sampling units occupied at the time of surveying, the authors describe a wide variety of extensions that have been developed since the early 2000s. This provides an improved insight about species and community ecology, including, detection heterogeneity; correlated detections; spatial autocorrelation; multiple states or classes of occupancy; changes in occupancy over time; species co-occurrence; community-level modeling, and more. Occupancy Estimation and Modeling: Inferring Patterns and Dynamics of Species Occurrence, Second Edition has been greatly expanded and detail is provided regarding the estimation methods and examples of their application are given. Important study design recommendations are also covered to give a well rounded view of modeling.
Current approaches to conservation may be inadequate to maintain ecosystem integrity because they are mostly based on rarity status of organisms rather than functional significance. Alternatively, approaches focusing on the protection of ecological networks lead to more appropriate conservation targets to maintain ecosystem integrity. We propose that a shift in focus from species to interaction networks is necessary to achieve pressing conservation management and restoration ecology goals of conserving biodiversity, ecosystem processes and ultimately landscape‐scale delivery of ecosystem services. Using topical examples from the literature, we discuss historical and conceptual advances, current challenges and ways to move forward. We also propose a road map to ecological network conservation, providing a novel ready to use approach to identify clear conservation targets with flexible data requirements. Synthesis and applications . Integration of how environmental and spatial constraints affect the nature and strength of local interaction networks will improve our ability to predict their response to change and to conserve them. This will better protect species, ecosystem processes, and the resulting ecosystem services we depend on.
De‐extinction technology that brings back extinct species, or variants on extinct species, is becoming a reality with significant implications for biodiversity conservation. If extinction could be reversed there are potential conservation benefits and costs that need to be carefully considered before such action is taken. Here, we use a conservation prioritization framework to identify and discuss some factors that would be important if de‐extinction of species for release into the wild were a viable option within an overall conservation strategy. We particularly focus on how de‐extinction could influence the choices that a management agency would make with regard to the risks and costs of actions, and how these choices influence other extant species that are managed in the same system. We suggest that a decision science approach will allow for choices that are critical to the implementation of a drastic conservation action, such as de‐extinction, to be considered in a deliberate manner while identifying possible perverse consequences. A lay summary is available for this article.
Seed dispersal is a vital step for plant reproduction and long-term vegetation dynamics, and many plants rely on animals for this process. Large animals are disproportionally important dispersers, however they tend to be under a higher extinction risk worldwide. There is compelling evidence that the global biodiversity crisis is leading to the deterioration of several ecosystem functions, including that of seed dispersal. However, there is virtually no information on how large-scale refaunation efforts can reinstate seed dispersal. We evaluated the effectiveness of a 62 km(2) wildlife sanctuary, aimed at recovering large mammals' populations in the Gorongosa National Park (Mozambique), in restoring seed dispersal interactions. The sanctuary provided a unique natural experiment to test the effect of large-mammals' refaunation on this key ecosystem function. The results reveal a higher diversity of dispersers inside the sanctuary that translates into a more diverse, larger and more complex seed-dispersal network. The higher number and diversity of seeds dispersed inside the sanctuary was explained mostly by the greater disperser's abundance, rather than by their identity. Overall, the seed dispersal network inside the sanctuary was less specialized (>H2') and there was a greater overlap on the plant species dispersed by all animals. Both networks were significantly modular and anti-nested. Our findings suggest that conservation efforts aimed at recovering large mammals populations are reinstating not only those target species, but also their functional roles in the ecosystems, specifically restoring seed dispersal networks in Gorongosa. This article is protected by copyright. All rights reserved.
This book had its origin when, about five years ago, an ecologist (MacArthur) and a taxonomist and zoogeographer (Wilson) began a dialogue about common interests in biogeography. The ideas and the language of the two specialties seemed initially so different as to cast doubt on the usefulness of the endeavor. But we had faith in the ultimate unity of population biology, and this book is the result. Now we both call ourselves biogeographers and are unable to see any real distinction between biogeography and ecology.