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Primate seed dispersal is a vital, but complex, ecological process that involves many interacting agents and plays important roles in the maintenance of old-growth forest, as well as in the development of regenerating forest. Focusing primarily on African examples, in this article we briefly review the ecological process of primate seed dispersal, highlighting understudied and contentious topics, and then we discuss how our knowledge on primate seed dispersal can promote both forest restoration and primate conservation. Though it is frequently claimed that primates are critically important for the maintenance of diverse tropical forest ecosystems, we believe that more empirical evidence is needed to support this claim. Confounding factors can often be difficult to rule out and long-term studies extending beyond the seedling or sapling stage are very rare. In addition, though primates are critical for initial seed dispersal of many tree species, spatial and temporal variation in post-deposition processes, such as secondary seed dispersal and predation by rodents, can dramatically alter the initial patterns generated by primates. However, given the need for immediate conservation action to prevent further primate extinctions, we advocate that the knowledge about primate seed dispersal be used in formulating informed conservation plans. One prominent area where this knowledge will prove extremely valuable is in forest restoration efforts. To aid in the development of such efforts, we pose five questions, the answers to which will help facilitate forest restoration becoming a useful tool in strategies designed to conserve primates. © 2018 Springer Science+Business Media, LLC, part of Springer Nature
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Primate Seed Dispersal and Forest Restoration:
An African Perspective for a Brighter Future
Colin A. Chapman
1,2,3
&Amy E. Dunham
4
Received: 1 November 2017 / Accepted: 22 June 2018
#Springer Science+Business Media, LLC, part of Springer Nature 2018
Abstract Primate seed dispersal is a vital, but complex, ecological process that
involves many interacting agents and plays important roles in the maintenance of
old-growth forest, as well as in the development of regenerating forest. Focusing
primarily on African examples, in this article we briefly review the ecological process
of primate seed dispersal, highlighting understudied and contentious topics, and then
we discuss how our knowledge on primate seed dispersal can promote both forest
restoration and primate conservation. Though it is frequently claimed that primates are
critically important for the maintenance of diverse tropical forest ecosystems, we
believe that more empirical evidence is needed to support this claim. Confounding
factors can often be difficult to rule out and long-term studies extending beyond the
seedling or sapling stage are very rare. In addition, though primates are critical for
initial seed dispersal of many tree species, spatial and temporal variation in post-
deposition processes, such as secondary seed dispersal and predation by rodents, can
dramatically alter the initial patterns generated by primates. However, given the need
for immediate conservation action to prevent further primate extinctions, we advocate
that the knowledge about primate seed dispersal be used in formulating informed
conservation plans. One prominent area where this knowledge will prove extremely
valuable is in forest restoration efforts. To aid in the development of such efforts, we
Int J Primatol
https://doi.org/10.1007/s10764-018-0049-3
Handling Editor: Yamato Tsuji
*Colin A. Chapman
Colin.Chapman@McGill.ca
1
Department of Anthropology and McGill School of Environment, McGill University, Montréal,
Québec H3A 2T7, Canada
2
Wildlife Conservation Society, Bronx, NY 10460, USA
3
Section of Social Systems Evolution, Primate Research Institute, Kyoto University, Inuyama,
Aichi 4840094, Japan
4
Department of Biosciences, Rice University, Houston, TX 77005, USA
pose five questions, the answers to which will help facilitate forest restoration becom-
ing a useful tool in strategies designed to conserve primates.
Keywords Primate conservation .Reforestation .Regeneration .Seed fate .Tropical
forest
Introduction
The pace of biodiversity loss is increasing, with current extinction rates ca. 1000 times
higher than background rates (Pimm et al. 2014). Recent estimates suggest that at least
322 vertebrate species have gone extinct since 1500 and that surviving vertebrate
species have declined in abundance by 25% since 1970 (Dirzo et al. 2014). Overall,
60% of all primate species are currently threatened with extinction (Estrada et al. 2017),
and though it remains to be confirmed, it seems almost a certainty that with the
disappearance of Miss Waldronsredcolobus(Procolobus badius waldroni)wehave
lost the first primate to extinction in the twenty-first century (McGraw 2005). The slow
life histories and high infant mortality rates of primates makes them especially suscep-
tible to anthropogenic impacts and increasing environmental variability (Van Allen
et al. 2012).
Humans are clearly responsible for the current decline of primate populations.
Between 2000 and 2012, 2.3 million km
2
of forest was lost globally, and in the
tropics, forest loss increased each year (Hansen et al. 2013). To put this in perspective,
this area is approximately the size of Mexico. Another action leading to the decline in
primate numbers is bushmeat hunting. Global estimates of the extent of wildlife
overexploitation are very poor; however, in Africa, 4 million metric tons of bushmeat
are extracted each year from the Congo basin alone (equivalent to ca. 4.5 million cows,
or 80 million small (5 kg) monkeys; of course not all bushmeat is primate (Fa and
Brown 2009)). Primates are also threatened by a changing climate. Temperatures are
predicted to increase by 1.5 °C by the end of the twenty-first century (IPCC 2014), and
researchers have projected that by 2100 75% of all tropical forests present in 2000 will
experience temperatures that are higher than the temperatures presently supporting
closed canopy forests (Peres et al. 2016; Wright et al. 2009). As forests change,
primate populations of many species may decline precipitously. Even if temperature
changes were to be somewhat buffered in tropical forests, there is a general agreement
that rainfall regimes are already changing and will continue to change over large areas
of the tropics (Feng et al. 2013;Fu2015). Altered rainfall patterns are likely to have
distressing consequences for the functioning of these diverse ecosystems and the
survival of primates.
For endangered primates it is very difficult to predict the combined and potentially
synergistic impacts of different dynamic factors on a particular population without
long-term data, of which there are unfortunately little available (Chapman et al. 2017).
For example, a demographic study of a Madagascar lemur, Propithecus edwardsi,
quantified that hunting and deforestation were (not surprisingly) the most significant
threats to this species (Dunham et al. 2008). However, the study also revealed that a
continued intensification of the El Niño effect and extreme weather events caused by
climate change would lead to further declines in the speciespopulations (Dunham
Chapman C.A., Dunham A.E.
et al. 2008,2011). Such multiple threats create feedbacks that may make the extinction
risk faced by primates more severe than currently recognized.
Tropical ecosystems are not just losing biodiversity; they are losing ecological
processes (Chapman and Peres 2001; Peres and Dolman 2000). One of the processes
in which primates play a very significant role is seed dispersal. Primates constitute
between 25 and 40% of the frugivore biomass in tropical forests and they defecate or
spit out a large number of seeds (Chapman 1995; Lambert and Garber 1998;
Wrangham et al. 1994). As up to 75% of tropical tree species produce fruits adapted
for dispersal by frugivores (Frankie et al. 1974; Howe and Smallwood 1982), how
forest ecosystems will operate without primate seed dispersal, or with their populations
much reduced, is unclear.
Our objectives in this article are to 1) briefly review the ecological process of
primate seed dispersal, highlighting areas we view have not received sufficient attention
or where there is confusion, focusing on African examples; 2) take what has already
been learned about primate seed dispersal and evaluate how this knowledge can support
primate conservation efforts, focusing on the role that primates play in forest restora-
tion; and 3) explore what knowledge about seed dispersal will be needed in the future to
promote and facilitate restoration efforts. We address these three points based on our
years of professional experience in field at sites with very different primate species, and
based on our thoughts regarding results found in the literature.
The Ecological Process of Primate Seed Dispersal
When one first considers seed dispersal, it seems to be a deceptively simple, yet vital,
ecological process. This process allows seeds to escape the density- and distance-
dependent mortality that occurs under or very near the parent tree (Connell 1971;
Janzen 1970) and reach new sites for colonization. Thus, the nature of seed dispersal
influences plant demography, genetics, plant spatial distribution, and future vegetation
composition (Howe and Miriti 2004; Lambert and Garber 1998;Leveyet al. 2008),
which in turn influences primate abundance (Chapman et al. 2018). However, though
seed dispersal is a vital process, it is not simple. Claims of the importance of primate
seed dispersal for plant populations and communities abound (Andresen 2000;Kaplin
and Lambert 2002), yet quantitative evidence of this has proven very difficult to obtain
(Russo and Chapman 2011), and rarely is the evidence free of confounding factors or
involves assessment beyond the seedling stage. In fact, most claims of the importance
of primates are often simply based on the number of seeds that a specific primate
handles. For example, a single group of gibbons (Hylobates mulleri × agilis)disperses
a minimum of 16,400 seeds per km
2
each year from 160 plant species (McConkey et al.
2002), Geoffroys woolly monkey (Lagothrix cana) disperses nearly 1 million
Manilkara bidentata seeds per km
2
every fruiting season (Levi and Peres 2013), and
redtail monkeys (Cercopithecus ascanius) disperse 24,492 fruits/ km
2
each day
(Lambert 1999).
Though moving such a large number of seeds is an important aspect of seed
dispersal, it does not necessarily mean these animals are playing an important role in
seedling establishment or subsequent stages of the plants life history. Other consider-
ations must be taken into account when evaluating the role of primate seed dispersers.
Primate Seed Dispersal and Forest Restoration: An African...
For example, tropical trees often produce hundreds of thousands of seeds during their
adult life spans. To be successful, an individual tree has to make one a similarly
successful adult, and thus the importance of primates will depend, not just on the
quantity of seeds dispersed, but also on the quality of the dispersal service (Schupp
1993; Schupp et al. 2010). Almost universally, fleshy fruited tree species have their
seeds dispersed by a variety of animal species (cf. Chapman et al. 1992). For example,
during only 61.5 h of watching fruit removal from Trichilia gilgiana in Gabon, 22
species, including two ruminants, nine rodents, ten birds, and two monkey species, ate
this speciesfruit (Gautier-Hion et al. 1985). Such observations contributed to the
proposal of the term diffuse coevolutionto describe the evolutionary relationship
between plants and frugivores (Herrera 1985) and later to the refinement of this idea
into the concept of coevolving multispecies interaction networks (Guimarães et al.
2017;Thompson2009). If many nonprimate frugivores are dispersing a speciesseeds,
the relative importance of primates may be low because other frugivores, such as birds,
rodents, and ruminants, can play important roles by moving many seeds to high-quality
sites for germination and seedling establishment.
Another consideration is that the spatial and temporal variation in the fate of the
dispersed seeds can be so large as to obscure the initial seed deposition patterns
(Schupp 1993;Schuppet al. 2010). Thus, while the extinction of one or a few frugivores
may alter the number of seeds dispersed and the location where they are deposited
(Chapman and Chapman 1996; Gross-Camp and Kaplin 2011; Razafindratsima and
Dunham 2015), variation in seed fate may make the demographic consequences of seed
dispersal difficult to estimate. For example, in Costa Rica, 98% of the seeds placed at
experimental stations were removed or killed within 70 days (Chapman 1989). In Peru,
99% of the Virola calophylla seeds naturally dispersed by spider monkeys (Ateles
paniscus) or ones that had fallen below the parent tree were preyed upon within 15 months
(Russo 2003). In Uganda, a detailed study on Monodora myristica illustrated how
postdispersal processes can overwhelm the patterns of primate seed dispersal for plant
populations (Balcomb and Chapman 2003).M.myristicahas large (16 cm in diameter)
thick husked (1.8 cm) fruits, such that primates and elephants are the only animals known
to open the fruits and, not surprisingly, primates dispersed >85% of the seeds. Despite this,
of the six sites studied, the ones with higher abundance of primate frugivores had lower
than expected seedling recruitment and lower sapling and pole abundances. Thus, while
primates are critical for the initial dispersal in this system, spatial and temporal variation in
postdispersal processes overwhelmed the patterns of dispersal and changed the predict-
ability of frugivore effects on recruitment. These postdispersal processes include seed
predation and secondary seed dispersal by rodents, disease from bacteria and fungi,
herbivory on seedlings and saplings, and competition from other seedlings and previously
established plants (Forget et al. 1994;Howe1990; Jansen and Forget 2001;Schupp1988;
Visser et al. 2011).
Apart from studies claiming that primates are important seed dispersers based on the
number of seeds they process, the majority of the studies available to evaluate the
importance of primates as seed dispersers involve investigations done in areas with
reduced primate numbers, either in forests that are fragmented or where primate numbers
are diminished by hunting (Chapman and Onderdonk 1998;Poulsenet al. 2011). How-
ever, in disturbed forests there are many confounding factors that change (e.g., light and
soil moisture levels) and these need to be simultaneously studied alongside of the number
Chapman C.A., Dunham A.E.
of seeds primates disperse and when comparing hunted and unhunted forests the situation
is complex (Poulsen et al. 2011). Studies of hunting indicate that primates are important in
maintaining substantial populations of large-seeded tree species in tropical forests
(Pacheco and Simonetti 2000;Effiomet al. 2013;Vanthommeet al. 2010;Wrightet al.
2007). African forests are of particular concern given the high human population density
(Chapman et al. 2006) and the heavy levels of hunting of animals that have a seed
dispersal role (Abernethy et al. 2013;Campbellet al. 2011; Covey and McGraw 2014).
Though these studies are suggestive of the importance of primates, we encourage
researchers to evaluate potential confounding factors, such as changes in microhabitat,
seed predators, and other natural enemies. Also, the impacts of hunted or defaunated
fragments on primate dispersed trees are likely to be context dependent. Some studies have
shown that nonprimate frugivores can expand their niche to fill the role of the primates that
cannot survive in forest fragments or in heavily exploited areas (Chapman and Onderdonk
1998; Peres and Dolman 2000;Wright2003), while in some situations they may be unable
to do so (Chaves et al. 2015). In Madagascar it was found that a lack of primate dispersers
in forest fragments did not hurt recruitment of an animal-dispersed trees species. Instead
recruitment was enhanced because of a concomitant decline of seed predators and because
the lack of primate frugivores allowed an expanded role of ants that delivered high-quality
seed dispersal (Dausmann et al. 2008).
When evaluating the importance of primate seed dispersers, the ecological processes
that are in play between seed dispersal and the establishment of an adult in the next
generation play out over hundreds of years. Thus, most trees whose fruits are currently
being fed on by primates come from seeds that were dispersed by frugivores dating back
20100 generations (Herrera 1985). Many canopy-level fruiting trees are shade-tolerant
species and often slowly build their way to the canopy (Grubb 1996). For example,
seedlings and saplings of Chrysophyllum sp. grow extremely slowly in the shaded
understory; their mean height only doubling every 27 years (Connell and Green 2000).
With this growth rate, a 20-cm seedling could take almost 70 years to reach a meter in
height. Similarly, life history modeling has suggested that the population growth rates of
several tropical species are relatively insensitive to changes in the transition probabilities
of seeds to seedlings, but it is later stages that determine if a population grows or not
(Pinero et al. 1984). Thus, for such species changing the number of seeds dispersed, by, for
example, extensive bushmeat hunting, will have little or no effect on the subsequent
population size (Myster 2017).
The extinctions of important seed dispersers that occurred before modern times
(Guimarães et al. 2008; Janzen and Martin 1982;Pireset al. 2014) illustrate that many
ecological interactions must be viewed from a long-term perspective. Madagascar lemurs
represent a particularly sad and poignant example (Dew and Wright 1998; Overdorff and
Strait 1998). After the intensification of human activity on Madagascar roughly 1700 years
ago, at least 17 species of lemurs went extinct (Perez et al. 2005). Many of these lemurs
lived in or near forest and relied on fruit and thus were dispersing seeds (Burney et al.
2003). Recently, Federman et al. (2016) demonstrated that the extinction of large-bodied
lemurs resulted in a significant reduction in the frugivore communitys seed dispersal
ability. Despite these frugivore extinctions on Madagascar, and similar ones in North and
South America (i.e., gomphothere extinctions), there does not seem to have been large
extinctions of tree species; rather other animals have taken over the seed dispersal role.
Federman et al. (2016 pers. comm.) suggest that the persistence of these fruiting species,
Primate Seed Dispersal and Forest Restoration: An African...
despite the absence of their dispersing megafauna, was due to their long generation times
and secondary dispersal agents, such as the introduced Rattus rattus or strong winds
during cyclones. Combining all of these lines of evidence suggests that thus far there is
little long-term empirical data available to evaluate the impact of hunting on forest
communities (Poulsen et al. 2011; Stoner et al. 2007). This means that while it is
appropriate to advocate for the protection of primates on moral/ethical grounds or on
ecological grounds owing to the many biotic interactions in which they are involved,
advocating for primate conservation because their decline will cause the extinction of tree
species is currently ungrounded.
Use of Knowledge of Seed Dispersal to Support Primate Conservation
and Forest Restoration
The seed dispersal interaction network in which primates are involved in is a complex and
dynamic system involving many plants and animals, whose connections vary over even
short spatial and temporal scales. Causing this ecological network to break down will have
cascading, unforeseen, effects. Though extinctions will likely not occur, there may be very
negative consequences (Valiente-Banuet et al. 2015). Thus maintaining the process of
seed dispersal by primates should be a priority. This means maintaining relatively
undisturbed intact tropical forests, which calls for effective national parksan urgent call
that is repeatedly made around the world (Laurance et al. 2012;Watsonet al. 2018). Most
seed dispersal research makes connections to conservation by stating that maintaining the
ecological process of seed dispersal is needed to prevent negative cascading conse-
quences. However, seed dispersal is also essential for the re-creation of tropical for-
estsforest restoration (Chazdon and Guariguata 2016; Duncan and Chapman 1999;
Guariguata and Ostertag 2001; Guevara et al. 1986;HollandAide2011; Kaplin and
Lambert 2002). Large areas of tropical forests have been converted to agriculture, but with
rapid urbanization rates and changing demographics in some countries many lands have
been abandoned and left to recover natural forests, creating opportunities for primate
conservation (Hansen et al. 2013;Jacobet al. 2008,2016). In contrast to the extensive
body of research on the relative role of primate seed dispersal in old growth forest, the role
of natural seed dispersal for large scale restoration has received little attention, and the role
that primates play in this process has largely been overlooked. Conservation projects can
involve active restoration, where people plant seedlings or sow seeds into areas, or passive
restoration, where the land is allowed to regenerate on its own accord. Typically, the
actions of primates aid in both types of restoration projects. To help future efforts and give
moreattentiontotheroleprimatescanplayin restoration, we consider in this section the
significance that forest restoration could play in conservation strategies for primates. Then,
in the next section, we outline what knowledge about seed dispersal by primates must be
available to reach this goal.
Potential for Forest Restoration to Aid in Primate Conservation
It is clear that in the tropics large areas have been deforested through logging and
agricultural expansion and deforestation is increasing at an accelerating rate (Felton
Chapman C.A., Dunham A.E.
et al. 2013;Hansenet al. 2013). However, these areas do not always remain deforested
and estimates suggest secondary forests have replaced at least one of each 6 ha of
relatively undisturbed forest deforested in the 1990s (Jacob et al. 2008; Wright and
Muller-Landau 2006). Furthermore, 2 billion ha in forest and forest/savanna biomes
have been identified as opportunities for forest restoration (Chazdon and Guariguata
2016;Laestadiuset al. 2011); this is an area twice the size of Canada. Estimates of the
area covered by regenerating forests range from 500 to 850 million ha (Lamb et al.
2005;Panet al. 2011); the upper estimate is the size of Brazil. Moreover, current global
trends indicate that the area of regenerating forest is increasing and a great deal of this
increase is caused by agricultural land being abandoned as people move to the cities
(Wright and Muller-Landau 2006). As of 2008, more people lived in cities than in rural
settings. This urbanization trend is increasing, and the UN Population Division esti-
mates that 90% of the worlds population growth between 2000 and 2030 will occur in
cities of the developing world (United Nations Population Division 2008).
The movement of people from a rural to urban setting offers great conservation
opportunities as these abandoned or devalued lands can be restored. But for this
opportunity to be grasped to its fullest many questions remain that need to be answered
such as the following: 1) What will be the future of lands abandonedby rural
farmers? Will they become lands of large agricultural industry, such as palm oil (Linder
2013), or be turned into agroecosystems where primate conservation is possible to
varying degrees (Estrada et al. 2012), or become regenerating natural forest, thereby
expanding protected areas or acting as corridors? 2) How does the conservation
community illustrate to local and national governments the value of restoring land?
Is the carbon value of these lands something that will convince these groups? How do
we collect evidence of the carbon value of regenerating forests to convince carbon
buyers (Wheeler et al. 2016)? Can farmers be convinced of the value of reforested lands
by showing them that they increase the abundance and diversity of pollinators coming
to their crops? As clean water becomes a scarce resource in many countries, can the fact
that forests maintain watersheds and purify polluted waters be used to convince people
of their value? How can the aesthetic value of forests and the animals they support be
promoted? 3) Can primates be used as Flagshipor Guardian Angelspecies to
promote the value of restoring these lands to a native forest (Bicca-Marques and de
Freitas 2010; Simberloff 1998)? The term Guardian Angel has been used by UNESCO
to mean that a decline in this species or group of species signals a negative impact for
humankind. For example, howlers in Southern Brazil are being called the Guardian
Angel of local communities, as they get yellow fever before it erupts in the human
population, so they signal that preventative action must be put in place to prevent
yellow fever from breaking out in the local communities (Bicca-Marques et al.2017).
4) Finally, can regenerating vegetation be primate habitat? There are only a handful of
studies that suggest that forests, and the primate communities they support, can rebound
rapidly when left to recover or encouraged to recover. For example, a survey of a site in
Korup National Park, Cameroon that was abandoned 78 years previously, found
populations of all eight species of diurnal primates that occur in the region; in addition,
sighting frequency in this recovering area was not significantly different from other
sectors of the park (Baya and Storch 2010;Linder2008). In Kibale National Park,
Uganda, 7 years after an area of grassland was replanted with trees as part of a carbon
offset program (Omeja et al. 2012), all species of diurnal primates were present in high
Primate Seed Dispersal and Forest Restoration: An African...
numbers, including the endangered red colobus (Piliocolobus tephrosceles) and chim-
panzee (Pan troglodytes)(Chapmanet al. 2018). Similarly, 16 years post logging of a
pine plantation in Kibale, all primate species except one were present in high numbers
(Fig. 1)(Chapmanet al. 2018). Such studies give hope for the future.
What Knowledge about Seed Dispersal Is Needed to Promote Forest
Restoration?
Seed dispersal is a stepwise process: primates eat fruits and ingest the seed; they
move away from the parent tree; defecate or spit out the seed; the seed on the ground
is or is not destroyed, the seed germinates or does not; the seedling survives or does
not; and so on. This progression of steps can be used to formulate a set of questions
that can guide the procurement of information needed to construct informed conser-
vation and restoration plans. Using this stepwise progression, we propose five
questions, the answers to which, we believe, will be important in understanding the
role primates play in forest restoration programs:
1) What primate species use deforested lands and why?
It is important to know which of the primate species in a community will leave
the protection of the forest to venture into deforested lands and which will not, as
only those species that leave the old-growth forest will bring seeds into deforested
lands to promote tree regeneration. Deforested lands are often a dangerous
0.00
0.10
0.20
0.30
0.40
0.50
0.60
0.70
123456
Groups per km walked
Species
Fig. 1 The number of groups per km walked for the following species (1 = red colobus [Piliocolobus
tephrosceles], 2 = black-and-white colobus [Colobus guereza], 3 = redtail monkey [Cercopithecus ascanius],
4 = blue monkey [Cercopithecus mitis], 5 = mangabey [Lophocebus albigena], 6 = baboon [Papio Anubis])
monitored in the old-growth forest of Kanyawara, Kibale National Park, Uganda in 2005, 2014 (white and
black bars) and the adjoining regenerating forest block (Nyakatojo, 2014, gray bar) that was a pine plantation
before being logged starting in 1993. Further information on this research can be found in Chapman et al.
(2018).
Chapman C.A., Dunham A.E.
environment for primates largely because of the presence of dogs (Farris et al.
2017;Pozo-Montuyet al. 2013). Terrestrial or semiterrestrial species, such as
baboons, vervets, and ring-tailed lemurs will likely readily use these deforested
habitats as they naturally cross and forage in grasslands, but for other species it
may be difficult to predict if they use deforested habitats or not. For example, blue
monkeys in southwestern Uganda are not found along forest edges or in fragments
(Worman and Chapman 2006), while in South Africa they are common in frag-
ments and frequently move among fragments (Lawes 2004).
All too often conservation strategies developed for a given context are applied
to other contexts worldwide without considering their suitability for those other
contexts (e.g., extractive reserve concepts developed for areas with low human
densities are often applied without modification to areas with high human densi-
ties). This leads to inefficiencies, unsatisfied local communities, and project failure.
Thus, it is important that this is not done when applying a conservation strategy of
promoting primates as agents of reforestation. As a result, it will be important to
consider the pool of local primate seed dispersers and this will vary by region. For
example, Victor Arroyo-Rodriguez (unpubl. data) made a detailed study of the
species using deforested areas (the matrix among fragments) and found that Africa
had on average 3 times the percentage of the communitys species that used the
matrix when compared to Madagascar, which was the lowest of any region. The
Neotropics and Asia were intermediate. This shows the importance of the conti-
nental scale, but the local scale is also important. For example, in Kibale vervets
are absent from the north of the park, as were baboons until recently, while to the
south both species are abundant. Thus it seems likely that because both of these
species are often found in grasslands and very young regenerating forests, the rate
of regeneration would differ between the north and the south of the park.
2) How can primates be encouragedto use deforested lands?
To increase the rate of natural restoration or to improve the tree diversity in
areas in which seedlings have been planted, research is needed into ways to
encourage seeds from old-growth forest to be dispersed to deforested lands and
primates can play a major role in this process (Chazdon et al. 2009; Omeja et al.
2016). In general, we have a poor understanding of how seed dispersal services can
be positively affected (McConkey and OFarrill 2016); however, there are likely to
be many ways that this can be naturally done. One simple and well-tested means is
to leave abandoned structures where primates can seek refuge from predators or
leave introduced tree species in which the animals can feed (Duncan and Chapman
1999). Often when land is being restored buildings are levelled; crops are cleared;
and nonnative trees, such as fruit or timber trees, are cut to allow the land to return
to its natural state. However, leaving such structures and trees in place for a time
will encourage primates to leave the forest (Jacob et al. 2016). More research on
conditions under which primates move across open matrices would improve our
view of the relative importance of primates in the regeneration of fallow fields and
pastures.
Primate Seed Dispersal and Forest Restoration: An African...
3) What seeds are dispersed into deforested lands by primates and what is their fate?
The most valuable type of seed disperser to use deforested lands would be one
that brought a diversity of seeds into degraded lands and deposited them in a
fashion that they germinated and survived. Thus, to provide scientific support for
the idea that primates can be important in restoration efforts, knowledge of what
plant species they are dispersing into these areas and the fates of these seeds is
important. The diversity of fruits eaten by most primates (Chapman and Rothman
2009) make them potentially important for restoring a diverse forest community.
However, typically the disappearance/mortality rate of seeds in primate dung is
very high (ca. 75100%), making determining the fate to the seedling stage
difficult and requiring large sample sizes, particularly when seeds that disappear
cannot be monitored. Such high seed mortality rates also mean that monitoring a
suitable sample of seedlings to determine seedling survivorship will require ger-
minating seeds in a greenhouse setting, allowing the seedlings to grow, and
transplanting them to the deforested area to evaluate seedling fate.
Research into the role of primates in aiding restoration of deforested lands is in
the pioneering stages, as there are few existing studies. Yet, the conservation/
management community needs general information now. This is a dilemma for the
research community as recommendations must be made based on very limited
data. To facilitate generalization from one area to the next, it would help if tree
species are categorized into regeneration niches (i.e., early successional to old-
growth species) (Grubb 1977). Thus, for researchers attempting to make general-
izations, rather than trying to compare species or genera, they can evaluate that in
one location some percentage of a specific regeneration niche did well, while in
another location it did not, and explore reasons for such differences. However,
defining a species regeneration niche is often a difficult task (Zanne and Chapman
2005). Despite this difficulty, it is our opinion that conducting analysis on regen-
eration niches is the right course of action.
4) What is the fate of seedlings that establish?
Most research on primate seed dispersal only follows the process of seed
dispersal to seed deposition (Chapman 1989; Lambert 2001; cf. Andresen 1999);
however, with respect to conservation and management needs, this is clearly
insufficient. Wherever possible, it would be desirable to follow seedlings to
determine their fate. Though difficult, it is possible to germinate seeds that have
been defecated by primates, grow them to the seedling stage, and determine their
fate through the seedling to sapling stage (Balcomb and Chapman 2003), and we
suggestthatsuchanapproachshouldbeconsideredinfutureresearchefforts.
One particularly important element affecting seed and seedling fate in many
systems is fire. Evidence from a variety of sites clearly indicates that if fire is not
controlled, regeneration of seedlings will not progress (Buechner and Dawkins
1961;Omeja et al. 2012; Struhsaker 2002; Vargas et al. 2008). While controlling
fire seems like an obviously necessary management practice, other practices that
seem logical may have unanticipated results. For example, in a system where the
deforested lands are dominated by aggressive grasses that can grow to 3 m in
Chapman C.A., Dunham A.E.
height, a management practice that would be apparently useful would be to weed
around a seedling to remove competition with the grasses and allow the seedling to
receive more sunlight. However, in an experimental examination of such a strategy
Omeja et al. (2009) discovered that such weeding led to the desiccation and death
of many seedlings in the dry season. This example illustrates the need for careful
evaluation of management practices before they are broadly applied.
5) What happens at later stages of succession?
Financial and logistic constraints make long-term research very difficult, but of
course the longer the research, the more useful it is for providing accurate
information for conservation/management plans. With respect to regeneration, it
is well documented that the rates of biomass accumulation subsequent to distur-
bance is highly variable (Omeja et al. 2012;Uhlet al. 1982); thus whenever
possible it will be useful to place a study done at one site into a more general
framework and attempt to understand factors affecting the recovery. This is needed
to compare sites where primates are thought to contribute to the initial forest
regeneration to different degrees. For example, variation among pioneer species
between regions may be very important to explain decadal patterns of regeneration.
Although the structure of trees that become established after disturbance can be
variable (Grubb and Metcalfe 1996), Richards (1996) and others have noted the
existence of a guild of large-leafed, fast-growing, widely dispersed pioneer species
typically with umbrella-like crowns (e.g., Cecropia [Neotropics], Musanga [Afri-
ca], and some Macaranga [Africa, Asia, and Australia]). In the course of succes-
sion, these pioneers establish a canopy beneath which less light-tolerant species
can establish and prosper. However, in some regions these large-leafed, fast-
growing pioneer species are rare or absent and thus while initial regeneration in
such regions can be rapid, once the smaller-leafed pioneers age and die, regener-
ation can be slow as shade-tolerant species have to establish (Chapman et al.
1999). Understanding such patterns will greatly advance the accuracy with which
managers can predict the recovery of the plant and animal communities.
In conclusion, our article illustrates that primate seed dispersal is a complex
process that plays a crucial role in plant regeneration, both in conserved and
disturbed forests. Furthermore, while claims of the importance of primates in
shaping the long-term future of forest ecosystems abound, providing quantitative
evidence of their importance has proven difficult and rarely is the evidence
independent of confounding factors or involves examinations beyond the seedling
stage. We have demonstrated that while primates move many seeds away from the
parent trees, spatial and temporal variation in post-deposition processes, such as
seed dispersal and predation by rodents, can change the initial patterns generated
by the frugivoresactions. Such complexity is intriguing, demonstrates the need to
maintain all of the interactants in the process to prevent unanticipated negative
cascading events, and calls for careful science that makes cautious claims of
conservation significance until systems are well studied. However, the habitats in
which primates live are all affected by anthropogenic change; thus the role that
primates as seed dispersers needs to be reinvestigated with a fresh eye.
Primate Seed Dispersal and Forest Restoration: An African...
Acknowledgments We thank Michael Huffman and Andrew MacIntosh for helpful discussion while
writing; Onja Razafindratsima, Laurence Culot, Hiroki Sato, and Yamato Tsuji for inviting us to participate
in this special issue on primate seed dispersal; and Yamato Tsuji, Marilyn Norconk, and two anonymous
reviewers for very useful comments on the submitted manuscript.
Funding Information Funding for the research in Kibale National Park and during writing this
manuscript was provided by the IDRC grant Climate change and increasing humanwildlife conflict:
How to conserve wildlife in the face of increasing conflicts with landowners; the Canada Research
Chairs Program; Natural Science and Engineering Research Council of Canada; and Kyoto University.
Compliance with Ethical Standards
Ethical Note: The nature of the paper does not involve direct the use of animals, rather we rely on published
literature and the synthesis of ideas.
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Chapman C.A., Dunham A.E.
... While primates are typically among the most important taxonomic group or arboreal seed dispersers in tropical forests (Bufalo et al., 2016;Chapman & Dunham, 2018;Clark et al., 2001), we found that white-fronted capuchins (one of four primate species in the region) appear to use Pleodendron fruits as medicine rather than food. There is a growing body of evidence documenting the selective use of medicinal plants by animals-known as zoopharmacognosy animals (Campbell, 2000;Huffman & Pebsworth, 2018;Laska et al., 2007;Morrogh-Bernard, 2008). ...
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Background and Research aims The extinction of relict and rare tree species is accelerated by habitat loss and climate change. Pleodendron costaricense is a critically endangered tree, with only four mature individuals known in Southern Pacific Costa Rica. With the discovery of three additional trees, we set out to learn more about P. costaricense’s natural history and attempt the first successful germination. Methods We collected fruits from two trees and carried out preliminary germination trials in a nursery at the study site. We also used camera traps in one of the fruiting mother-trees to understand natural dispersal mechanisms of the species. Results Although plagued by excessive levels of invertebrate predation, we were able to germinate and produce 59 saplings ready for restoration planting. Five mammal species were detected on the camera traps feeding on the fruits, along with one primate potentially using the fruits as a topical medicine. Conclusion P. costaricense can be propagated ex-situ, potentially with greater success using stimulating hormones. To improve production rates, future efforts should focus on the protection of germinating seeds and saplings from seed predators. We also identified numerous potential natural mammalian seed dispersers, mostly in the family Procyonidae. Implications for Conservation Given the propagation knowledge we have developed, the active restoration efforts of the saplings by Osa Conservation to help increase population numbers, and the strict protection of the two fruiting mother trees, there is now the possibility to attain a positive conservation outcome for this critically endangered species.
... Eulemur rubriventer was mostly studied in pristine habitats such as Ranomafana National Park and its demography is poorly known in degraded and fragmented habitat. A deeper knowledge of these lemurs' occurrence in disturbed habitats is crucial because they are seed dispersers (Razafindratsima et al., 2014), and therefore, they potentially play a major role in reforestation (Manjaribe et al., 2013;Chapman and Dunham, 2018). The main goal of this study is to provide preliminary data about the presence, abundance, density, and group size of red-bellied lemurs in a degraded and fragmented area in the southern part of this species' geographic range, in the nearby of the Ranomafana National Park. ...
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Habitat fragmentation and degradation are serious threats to biodiversity. Knowledge on rare species' demography in disturbed habitat is relevant for conservation plans. In Madagascar, habitat alteration is known to affect both lemur density and distribution. We conducted a 40-day daylight census of an endangered lemur species, the red-bellied lemur (Eulemur rubriventer), in a fragmented and degraded forest in the southern part of its geographic range. With this preliminary study, we report that this species occurs in small fragments and populates a mosaic area east of the Ranomafana National Park, in southeastern Madagascar. Using a total count method, we estimated a minimum population of 30 individuals, a density of 1.05 individuals/km2, and a mean group size of 3.3 individuals. Slash-and-burn agriculture, logging, and the presence of free-ranging dogs appear as the major threats to lemur survival and likely contributed to the disappearance of three species (Eulemur rufifrons, Propithecus edwardsi, Varecia variegata). In the future, management strategies based on field data will be crucial to the survival of the lemur population in the Ranomafana area, which is likely home to the largest population of red-bellied lemurs.
... Population size and population trajectories over time are key parameters for understanding the ecology of animal communities and guiding species-specific conservation efforts. In many habitats, particularly in tropical forests, primate species constitute a major component of animal communities and provide multiple ecosystem services as folivores, frugivores, seed dispersers, seed predators, pollinators, and as prey and predators [1,2]. ...
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Estimating population density and population dynamics is essential for understanding primate ecology and relies on robust methods. While distance sampling theory provides a robust framework for estimating animal abundance, implementing a constrained, non-systematic transect design could bias density estimates. Here, we assessed potential bias associated with line distance sampling surveys along roads based on a case study with olive baboons (Papio anubis) in Lake Manyara National Park (Tanzania). This was achieved by comparing density estimates of olive baboons derived from road transect surveys with density estimates derived from estimating the maximum number of social groups (via sleeping site counts) and multiplying this metric with the estimated average size of social groups. From 2011 to 2019, we counted olive baboons along road transects, estimated survey-specific densities in a distance sampling framework, and assessed temporal population trends. Based on the fitted half-normal detection function, the mean density was 132.5 baboons km-2 (95% CI: 110.4-159.2), however, detection models did not fit well due to heaping of sight-ings on and near the transects. Density estimates were associated with relatively wide confidence intervals that were mostly caused by encounter rate variance. Based on a generalized additive model, baboon densities were greater during the rainy seasons compared to the dry seasons but did not show marked annual trends. Compared to estimates derived from the alternative method (sleeping site survey), distance sampling along road transects overestimated the abundance of baboons more than threefold. Possibly, this over-estimation was caused by the preferred use of roads by baboons. While being a frequently used technique (due to its relative ease of implementation compared to spatially randomized survey techniques), inferring population density of baboons (and possibly other species) based on road transects should be treated with caution. Beyond these methodological PLOS ONE PLOS ONE | https://doi.org/10.1371/journal.pone.
... When present in restored habitats, primates contributed with most of the dispersed seeds in regenerating sites (Silva et al., 2020, but see Martinez and Razafindratsima, 2014). Still, despite the importance of primates that persist in anthropogenic landscapes, their role in restored habitats has been largely overlooked hitherto (Andresen et al., 2018;Chapman and Dunham, 2018). ...
Article
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.
... Long-term monitoring studies are therefore critical to detect population-level changes, especially among species with limited dispersal capacity, providing an early warning signal to conservationists. Furthermore, the ecological roles that primates such as lemurs play in maintaining ecosystem function underscore the importance of their survival in threatened forests (Bollen et al., 2004;Chapman, 1995;Chapman & Dunham, 2018;Chapman & Onderdonk, 1998;Ramananjato et al., 2020). ...
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Habitat loss and fragmentation pose a significant threat to many primate species worldwide, yet community-level responses are complex and nuanced. Despite repeated calls from primatologists and the wider conservation community to increase monitoring initiatives that assess long-term population dynamics, such studies remain rare. Here we summarize results from a longitudinal study set in the littoral forests of southeast Madagascar. Littoral forests are a useful model for monitoring lemur population dynamics, as they are relatively well studied and their highly fragmented nature enables the effect of forest size and anthropogenic impacts to be examined. This study focuses on three Endangered nocturnal lemur species—Avahi meridionalis, Cheirogaleus thomasi, and Microcebus tanosi—across three forest fragments of different size and with different usage histories. Between 2011 and 2018, we walked 285 km of line transect and recorded 1968 lemur observations. Based on distance sampling analysis our results indicate that nocturnal lemurs respond to forest patch size and to levels of forest degradation in species-specific ways. The largest species, A. meridionalis, declined in density and encounter rate over time across the three study forests. C. thomasi populations appeared stable in all three fragments, with densities increasing in the most degraded forest. M. tanosi encounter rates were extremely low across all study fragments but were lowest in the most heavily degraded forest fragment. Our results emphasize the importance of localized pressures and species-specific responses on population dynamics. Monitoring population trends can provide an early warning signal of species loss and species-specific responses can inform crucial intervention strategies.
... If seed supply is limiting for forest edge communities, management of large-seeded species may need to be considered in some areas. For example, encouraging key seed dispersers to frequent the edge habitats could be useful for conserving rare, large-seeded species and increasing plant diversity in these areas (Couvreur et al., 2004;Cosyns et al., 2005;Chapman and Dunham, 2018). Generalist seed dispersers could increase the odds of many species reaching and establishing in these areas, thereby increasing local species richness (Myers and Harms, 2009;McConkey et al., 2012;Carlo and Morales, 2016). ...
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Edge effects, driven by human modification of landscapes, can have critical impacts on ecological processes such as species interactions, with cascading impacts on biodiversity as a whole. Characterizing how edges affect vital biotic interactions such as seed dispersal by frugivores is important for better understanding potential mechanisms that drive species coexistence and diversity within a plant community. Here, we investigated how differences between frugivore communities at the forest edge and interior habitats of a diverse tropical rainforest relate to patterns of animal-mediated seed dispersal and early seedling recruitment. We found that the lemur communities across the forest edge-interior gradient in this system showed the highest species richness and variability in body sizes at intermediate distances; the community of birds showed the opposite pattern for species richness. Three large-bodied frugivores, known to be effective dispersers of large seeds, tended to avoid the forest edge. As result, the forest edges received a lower rate of animal-mediated seed dispersal compared to the interior habitats. In addition, we also found that the seeds that were actively dispersed by animals in forest edge habitats were smaller in size than seeds dispersed in the forest interior. This pattern was found despite a similarity in seed size of seasonally fruiting adult trees and shrubs between the two habitats. Despite these differences in dispersal patterns, we did not observe any differences in the rates of seedling recruitment or seed-size distribution of successful recruit species. Our results suggest that a small number of frugivores may act as a potential biotic filter, acting on seed size, for the arrival of certain plant species to edge habitats, but other factors may be more important for driving recruitment patterns, at least in the short term. Further research is needed to better understand the potential long-term impacts of altered dispersal regimes relative to other environmental factors on the successional dynamics of edge communities. Our findings are important for understanding potential ecological drivers of tree community changes in forest edges and have implications for conservation management and restoration of large-seeded tree species in disturbed habitats.
... Additionally, it has supplemented documentation about differences in microhabitat preference in small-bodied primate species, which are often ecologically flexible (Estrada et al. 2012;Knoop et al. 2018). Such knowledge is particularly important in the tropics for conservation purposes as forests undergo permanent land transformations, and primates can act as seed dispersers and pollinators for many plant species (Chapman 1995;Chapman and Dunham 2018). Prioritizing habitat conservation in a landscape context could effectively promote species persistence and sustain long-term ecological restoration Estrada et al. 2012). ...
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Microhabitat preference among primates, which provides them with the niche they need to survive, often conditions primate diversity, abundance, and coexistence. Vegetation alteration and recovery have built heterogeneous forest landscapes that may influence primates’ microhabitat preference. We compared the diversity and size of trees/shrubs and the presence of lianas in 132 sites where we captured the rufous mouse lemur (Microcebus rufus), with that of 240 sites where we did not capture this species, to investigate the aspects of microhabitat structure they prefer. We then examined how this structural preference varies across a heterogeneous landscape of forests with different disturbance levels. Overall, microhabitats used by M. rufus differed significantly from unused ones in densities of small size, understory, and midstory plants. Microcebus rufus frequented microhabitats with significantly denser small- and medium-size (DBH 2.5-10 cm) trees/shrubs without lianas in the primary forest and small-size plants (DBH 2.5-4.9 cm) with one liana in other forest types. Compared to the microhabitats they used in the primary forest, the microhabitats in other forest types had lower densities of trees/shrubs with lianas. Additionally, the secondary forests and forest fragments also had significantly lower DBH. Although this variation in microhabitat use may represent an opportunity for M. rufus to live in disturbed habitats, it may expose them to additional threats, affecting their long-term survival. These findings emphasize the need to examine potential changes in microhabitat use among primates living in anthropogenic landscapes, which could help optimize long-term conservation and management of threatened primate species in heterogeneous landscapes.
... The effect of such biomic transformations is expected to propagate widely across the vertebrate fauna (Redford, 1992;Chapman and Dunham, 2018), including small to medium-sized mammalian carnivores (Michalski and Peres, 2005;Gerber et al., 2012). Indeed, the temporal dynamics of taxic codetection suggests substantial disintegration and ecological reassembly of the Washakie vertebrate fauna between the late Bridgerian and early Uintan (Fig. 46). ...
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The middle Eocene Washakie Formation of Wyoming, USA, provides a rare window, within a single depositional basin, into the faunal transition that followed the early Eocene warming events. Based on extensive examination, we report a minimum of 27 species of carnivorous mammals from this formation, more than doubling the previous taxic count. Included in this revised list are a new species of carnivoraform, Neovulpavus mccarrolli n. sp., and up to ten other possibly new taxa. Our cladistic analysis of early Carnivoraformes incorporating new data clarified the array of middle Eocene taxa that are closely related to crown-group Carnivora. These anatomically relatively derived carnivoraforms collectively had an intercontinental distribution in North America and east Asia, exhibiting notable variations in body size and dental adaptation. This time period also saw parallel trends of increase in body size and dental sectoriality in distantly related lineages of carnivores spanning a wide range of body sizes. A new, model-based Bayesian analysis of diversity dynamics accounting for imperfect detection revealed a high probability of substantial loss of carnivore species between the late Bridgerian and early Uintan North American Land Mammal ‘Ages’, coinciding with the disappearance of formerly common mammals such as hyopsodontids and adapiform primates. Concomitant with this decline in carnivore diversity, the Washakie vertebrate fauna underwent significant disintegration, as measured by patterns of coordinated detection of taxa at the locality level. These observations are consistent with a major biomic transition in the region in response to climatically induced opening-up of forested habitats. UUID: http://zoobank.org/9162f1a6-a12c-4d55-ba1d-dc66e8cda261
... In the Atlantic Forest, primates interact with all seed sizes (Bufalo et al. 2016), have a generally positive effect on seed germination (Fuzessy et al. 2016) and disperse seeds to long distances (Fuzessy et al. 2017). Nevertheless, there are still many gaps in the knowledge of their role on plant regeneration (Chapman and Dunham 2018). ...
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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.
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Apart from frugivory, we have limited knowledge of the ecological consequences of primate herbivory. We aimed to ascertain the effects of spring folivory and winter bark/bud herbivory by Japanese macaques (Macaca fuscata) on tree species and succession patterns of cool-temperate forests with heavy snow. To evaluate the impact of herbivory on individual trees, we assessed the growth and mortality of trees consumed by simulating herbivory on nine tree species over 4 years. Additionally, we assessed the cumulative impacts of bark/bud herbivory observed at the tree community level by monitoring the patterns of natural herbivory for almost a decade and evaluating the structure of tree assemblages in places with different cumulative impacts of herbivory. The results of simulated herbivory showed that the mortality caused by both spring and winter herbivory was limited (<20%) for almost all tree species monitored; however, the simulated folivory led to delayed tree growth and/or weakening of tree architecture. In contrast, the simulated bark/bud herbivory sometimes resulted in overcompensation of the tree consumed. The multiyear monitoring of natural herbivory demonstrated that, while bark/bud herbivory did not reduced the diversity and biomass of tree assemblages, the cumulative impacts of natural herbivory could have affected the tree succession pattern, resulting in increasing the availability of bark/buds preferably fed by macaques. The key cause for this feedback effect of herbivory on available foods of macaques might be heavy snow conditions, which could physically and physiologically restrain the excessive bark/buds herbivory by macaques.
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As the terrestrial human footprint continues to expand, the amount of native forest that is free from significant damaging human activities is in precipitous decline. There is emerging evidence that the remaining intact forest supports an exceptional confluence of globally significant environmental values relative to degraded forests, including imperilled biodiversity, carbon sequestration and storage, water provision, indigenous culture and the maintenance of human health. Here we argue that maintaining and, where possible, restoring the integrity of dwindling intact forests is an urgent priority for current global efforts to halt the ongoing biodiversity crisis, slow rapid climate change and achieve sustainability goals. Retaining the integrity of intact forest ecosystems should be a central component of proactive global and national environmental strategies, alongside current efforts aimed at halting deforestation and promoting reforestation.
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The rapid disappearance of tropical forests, the potential impacts of climate change, and the increasing threats of bushmeat hunting to wildlife, makes it imperative that we understand wildlife population dynamics. With long-lived animals this requires extensive, long-term data, but such data is often lacking. Here we present longitudinal data documenting changes in primate abundance over 45 years at eight sites in Kibale National Park, Uganda. Complex patterns of change in primate abundance were dependent on site, sampling year, and species, but all species, except blue monkeys, colonized regenerating forest, indicating that park-wide populations are increasing. At two paired sites, we found that while the primate populations in the regenerating forests had increased from nothing to a substantial size, there was little evidence of a decline in the source populations in old-growth forest, with the possible exception of mangabeys at one of the paired sites. Censuses conducted in logged forest since 1970 demonstrated that for all species, except black-and-white colobus, the encounter rate was higher in the old-growth and lightly-logged forest than in heavily-logged forest. Black-and-white colobus generally showed the opposite trend and were most common in the heavily-logged forest in all but the first year of monitoring after logging, when they were most common in the lightly-logged forest. Overall, except for blue monkey populations which are declining, primate populations in Kibale National Park are growing; in fact the endangered red colobus populations have an annual growth rate of 3%. These finding present a positive conservation message and indicate that the Uganda Wildlife Authority is being effective in managing its biodiversity; however, with constant poaching pressure and changes such as the exponential growth of elephant populations that could cause forest degradation, continued monitoring and modification of conservation plans are needed.
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Ecological interactions have been acknowledged to play a key role in shaping biodiversity. Yet a major challenge for evolutionary biology is to understand the role of ecological interactions in shaping trait evolution when progressing from pairs of interacting species to multispecies interaction networks. Here we introduce an approach that integrates coevolutionary dynamics and network structure. Our results show that non-interacting species can be as important as directly interacting species in shaping coevolution within mutualistic assemblages. The contribution of indirect effects differs among types of mutualism. Indirect effects are more likely to predominate in nested, species-rich networks formed by multiple-partner mutualisms, such as pollination or seed dispersal by animals, than in small and modular networks formed by intimate mutualisms, such as those between host plants and their protective ants. Coevolutionary pathways of indirect effects favour ongoing trait evolution by promoting slow but continuous reorganization of the adaptive landscape of mutualistic partners under changing environments. Our results show that coevolution can be a major process shaping species traits throughout ecological networks. These findings expand our understanding of how evolution driven by interactions occurs through the interplay of selection pressures moving along multiple direct and indirect pathways.
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Emerging infectious diseases were cited as a cause of population decline of wild nonhuman primates (NHPs) by A. Estrada and collaborators in their review “Impending extinction crisis of the world’s primates” (Science Advances, 18 January, e1600946). Concurrent with the publication of this review, an epidemic of jungle yellow fever (YF) in the Atlantic Forest region of southeastern Brazil is affecting humans and NHPs alike, challenging health and wildlife conservation authorities and professionals. From December 2016 to 18 May 2017, YF has killed 264 people (42 additional deaths are under investigation) and caused, at least, 5,000 NHP deaths (1). Our field estimates sum many thousands of NHP deaths. Humans have access to an effective vaccine and about 85% of infected unvaccinated people are asymptomatic or develop a mild form of YF (2). Despite this resistance, there are 758 confirmed human cases and a further 622 cases under investigation, about 63% of them in regions of recommended vaccination prior to the current epidemic.
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The role of the seed rain in affecting recruitment, regeneration, and plant community dynamics continues to be debated. Studies show that seed limitation for recruitment is more likely as ecosystems become colder and more species-poor, as in boreal forests, and for species that have large seeds and short-lived seed banks. Even if there is a limiting effect of the seed rain for recruitment, however, clumping seen for mature trees and other evidence suggests that its effect diminishes with time. I posit that the dynamics of plant communities are largely determined where the seed rain is abundant and not limiting—in local spaces close to dispersing plants. Putting all the evidence together, I conclude that it is what happens to seeds after dispersal—such as loss to predation and pathogenic attack, or germination success resulting from environmental tolerances—that has a greater effect on recruitment, regeneration and plant community dynamics. And thus the variation in the workings of seed fate mechanisms and environmental tolerances, deserve more research attention. The importance of the seed rain in affecting recruitment of individual plants, regeneration of individual plants, and plant community dynamics has been over-emphasized in plant modeling and theory.
Chapter
This book provides information on the historical and theoretical perspectives of biodiversity and ecology in tropical forests, plant and animal behaviour towards seed dispersal and plant-animal interactions within forest communities, consequences of seed dispersal, and conservation, biodiversity and management.
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Simian primates (monkeys and apes) are typically long-lived animals with slow life histories. They also have varying social organization and can slowly impact their environment by either being seed dispersers or by overbrowsing their food trees. As a result, short-term studies and those focusing on just 1 location only provide a snapshot of simian life under a specific set of ecological conditions that typically do not represent the complete spatial and temporal picture. Long-term field studies are needed to obtain a true understanding of their behavior, life history, ecology, and the selective pressures acting on them. Fortunately, there have been many long-term studies of simians, so a great deal is known about many species. Here, we consider examples of long-term studies that have operated continuously for approximately a decade or more. We review studies that deal with ecophysiology, social organization, population and community ecology, or conservation. The information emerging from these sites is particularly helpful in the construction of informed conservation plans, which are desperately needed given the severity of threats to simians and the fact that responses do not occur over the duration of a Ph.D. or granting cycle (typically 1–3 years).
Article
Protected areas (PA) aim to eliminate many of the threats that species face on the greater landscape. In the last three decades, PA's have expanded considerably; however, quantitative assessments of how well they have mitigated threats to habitat and biodiversity are very limited. Habitat bordering PA's and the wildlife that use it are threatened by a wide-range of anthropogenic pressures (e.g., edge effects, fragmentation, and introduced predators) and this situation is particularly acute for low-density, poorly studied carnivore communities. From 2010 to 2015, we photographically sampled within (contiguous forest) and bordering (degraded, fragmented forest) a UNESCO World Heritage rainforest PA in Madagascar - Ranomafana National Park (RNP). We investigated the effects of invasive predators, local people presence, and habitat quality on the endemic rainforest carnivore community using static, dynamic, and co-occurrence models. We found native carnivores to be absent or have a low probability of occurrence in degraded forest bordering the PA, while local people and dogs (Canis familiaris) had high occurrence. Madagascar's largest endemic carnivore, the fosa (Cryptoprocta ferox) and the much smaller ring-tailed vontsira (Galidia elegans), occurrence in RNP declined rapidly over six years; their strong co-occurrence with dogs suggests interspecific competition, direct aggression/mortality, or disease as the cause. We highlight the dangers posed to biodiversity, particularly carnivores, from anthropogenic pressures bordering PA's and present recommendations to address increased human and dog activity, including programs to control dogs and their impact on biodiversity.