Keywords

1 Introduction

More than 60 % and up to 94 % of woody plant species in tropical forests have their seeds dispersed through endozoochory by frugivorous animals. Hence, studying the interactions between frugivores and plants is critical for understanding the dynamics of these ecosystems (Jordano 2000). Frugivory and the consequent dispersal of seeds constitute a key ecological interaction that is mostly mutualistic, and that has important ecological, evolutionary, and conservation implications for both the animal and plant species involved, as well as for the ecosystems in which they occur (Herrera 2002; Schupp et al. 2010).

From a plant’s perspective, seed dispersal has three main, non-mutually exclusive, advantages (Howe and Smallwood 1982): (1) escape from areas of high mortality; (2) colonization of suitable sites which occur at random locations; and (3) directed dispersal to suitable sites. The ‘escape hypothesis’, which was derived from the mechanistic part of the Janzen–Connell hypothesis (Janzen 1970; Connell 1971), predicts that seed/seedling mortality will be higher under the parent plant, due to predators and/or pathogens that act in a density- and/or distance-dependent fashion, resulting in greater recruitment with increasing distance from the parent plant. In turn, according to the ‘colonization hypothesis’, widespread dispersal of seeds may be critical for some species, because it allows the arrival of at least some seeds into favorable sites, whose occurrence is unpredictable in space and time. Finally, according to the ‘directed dispersal hypothesis’, some dispersal vectors, and in particular animal vectors, can promote the arrival of seeds into specific non-random habitats (or microsites), where survival of seeds/seedlings will be predictably higher.

As mentioned above, these and other advantages of seed dispersal are not mutually exclusive, and the relative importance of each is species- and context-dependent (Andresen 2000; Vulinec and Lambert 2009; Chaves et al. 2011). In this regard, the theoretical framework most extensively used to assess the contribution of seed dispersal agents to plant fitness is the ‘Seed Dispersal Effectiveness’ framework (Schupp 1993; Schupp et al. 2010). Dispersal effectiveness is defined in terms of the contribution that dispersal agents make to the reproduction of a given plant species (Schupp et al. 2010). However, seed dispersal not only affects plant demography or the number of saplings present in a given area (e.g., recruitment); it can also play an important role in determining the spatial distribution of individuals in a given population, and it can have important consequences at the plant community level (Schupp et al. 2010; Russo and Chapman 2011). Regarding the latter, seed dispersal not only plays a role in determining the species composition of local plant communities through its effect on individual species, but it will also affect emerging properties such as community structure and diversity (Schupp et al. 2010; Russo and Chapman 2011).

In tropical forests, the most prominent taxa of seed-dispersing frugivores are birds, bats, and primates (Fleming and Kress 2011). While the former two have been the focus of seed dispersal studies for many decades, it has only been during the last two decades that primates have been recognized as important seed dispersers, with an increasing number of evidences from species within the Strepsirrhini and Haplorrhini suborders of primates (Chapman 1995; Lambert and Garber 1998; Koné et al. 2008; Chaves et al. 2011; Russo and Chapman 2011; Stevenson 2011; González-Zamora et al. 2014). This may reflect the fact that although many primates act as seed dispersers, they also act as seed predators. Seed consumption is reported in a large number of primate taxa including Lagothrix, Ateles, and Alouatta (Stevenson et al. 2002). In addition, since larger bodied primates tend to disperse many seeds together in a large fecal clump (Chapman 1989; Russo et al. 2006; González-Zamora et al. 2012, 2014), which may attract fungal pathogens or other seed predators (rodents), post-dispersal survivorship of voided seeds can be low (Howe and Smallwood 1982).

Frugivorous primates can disperse viable seeds of many plant species. However, evidence shows that the effects of seed dispersal on plant populations and communities can be highly variable among and within primate species (see Russo and Chapman 2011 for a thorough review). Primate species also differ in their vulnerability to disturbances such as hunting or habitat loss. While some primate species are highly sensitive, others are known to be particularly resilient (e.g. howler monkeys in the Neotropics; Arroyo-Rodríguez and Dias 2010; Estrada 2014), becoming the main or only seed dispersal agent for many plant species in areas where other frugivores have disappeared (Andresen 2000).

This chapter focuses on seed dispersal by howler monkeys (Alouatta spp.) throughout their geographical range. As is the case with primates in general, studies of seed dispersal by howler monkeys have focused on one or a few aspects of the seed dispersal process (e.g., frugivory, seed-handling, gut-passage effects, seed deposition patterns, post-dispersal seed fate, among others; Table 5.1). Thus, clearly establishing the effects of howler monkey seed dispersal on plant populations (demography, spatial distribution), and on plant communities (composition, structure, diversity), has been difficult.

Table 5.1 Aspects of seed dispersal by howler monkeys (Alouatta spp.) studied throughout their geographic range in both continuous forest (CF) and forest fragments (FF). References are indicated inside parentheses
Full size table

As an attempt to fill these gaps of information, we first assess the effects of seed dispersal by howler monkey on plant populations. To do so, we follow the seed dispersal effectiveness framework by identifying general patterns of the two primary components of effectiveness, i.e., quantity and quality of dispersal. Then, we discuss how seed dispersal by howler monkeys also can affect the spatial distribution of plant individuals in a population. At present, however, we know very little regarding the degree to which seeds dispersed by howlers actually survive the seedling, sapling, and pole stages of development and live to become fruiting and reproductive adults. In the second section, we evaluate the impact that howler monkey seed dispersal may have on plant community properties. Finally, in the last section we draw some conclusions on the roles that howler monkeys may play in forest conservation and restoration. Although this genus represents a radiation of some 12 species (Cortés-Ortiz et al. 2014), this review is focused on 6 howler monkey species due to the lack of data on the remaining species (Table 5.1).

2 Implications of Howler Monkey Seed Dispersal for Plant Populations

2.1 Seed Dispersal Effectiveness and its Effects on Demography

Seed dispersal effectiveness depends on both the quantity and the quality of seed dispersal (Schupp 1993). Dispersal quantity is simply given by the number of seeds that are dispersed. In turn, the number of dispersed seeds depends on the number of visits to the plant by a disperser and the number of seeds swallowed per visit. The quality component is given by the probability that a dispersed seed germinates and the developing sapling survives to become a reproductive adult. The quality of seed dispersal is determined by two sub-components: the quality of the treatment given to the seed in the animal’s mouth/gut, and the quality of seed deposition (Schupp 1993). This latter is influenced by primary dispersal, as well as in many cases secondary dispersal.

2.1.1 Quantity of Seed Dispersal

Considering that the number of visits to a particular feeding site is directly related to the abundance of the dispersers, their dietary preferences, and the reliability of visitation (Schupp 1993), howler monkeys can contribute notably to this component of seed dispersal effectiveness. First, because of their high population densities (densities vary widely, but values of up to 283 ind/km2 have been reported) (reviewed in IUCN 2012), howler monkeys constitute one of the most common vertebrate species in many Neotropical forests (Peres 1997; Garber et al. 2006). Second, although howler monkeys have been typically considered the most folivorous of Neotropical primates, they spend approximately half of their feeding time consuming ripe fruits when this resource is available (reviewed by Bicca-Marques 2003; Cristóbal-Azkarate and Arroyo-Rodríguez 2007; see also Dias and Rangel-Negrin 2014), generally being ‘as frugivorous as possible and as folivorous as necessary’ (Silver et al. 1998). Finally, howler monkeys spend most of their time feeding on the fruits of a small number of plant families (e.g. Moreaceae, Fabaceae, Lauraceae and Sapotaceae; Bicca-Marques 2003; Cristóbal-Azkarate and Arroyo-Rodríguez 2007; Dias and Rangel-Negrin 2014). These species are consistently used year after year (e.g. Estrada and Coates-Estrada 1984), such that howler monkeys can be considered highly reliable seed dispersers for these plant taxa. Therefore, these evidences indicate that howlers are able to disperse very large quantities of seeds.

The number of seeds dispersed per visit depends on the number of seeds handled and swallowed per visit and the probability of dispersing a handled seed (Schupp 1993). In general, howler monkeys disperse, through defecation, most of the seeds they handle. Also, there is a trend showing that, in general, the larger the frugivorous animal, the higher the amount of fruits (and seeds) it can handle, and the larger the size of fruits/seeds it is able to swallow (e.g., Cramer et al. 2007). However, some important exceptions have been published (e.g., tamarin monkeys: Lambert and Garber 1998).

Studies indicate that howlers disperse large numbers of seeds from both small-seeded species and from large-seeded (>10 mm) plant species (Tables 5.2 and 5.3). For example, Andresen (2002a) found that up to 560 seeds >3 mm long can be found in a defecation sample of A. macconnelli in Brazil, although 20 % of the defecation samples with seeds had less than 30 seeds. Similarly, Giraldo et al. (2007) analyzed 60 fecal samples of A. seniculus in Colombia, finding 290,174 seeds (1–33 mm long), of which 99.9 % belonged to three small-seeded light-demanding tree species (Ficus spp., Cecropia telealba, and Miconia acuminifera). Martins (2006) assessed seeds larger than 2 mm in length and reported an average of 18 seeds (range: 1–97 seeds) per fecal sample (from 1 or 2 tree species) in 147 fecal samples of A. guariba in a semideciduous forest in Brazil. In Argentina, one A. caraya group can remove up to 1,070 fruits from a tree of Ocotea diospyrifolia (Lauraceae) in a day (Bravo 2012a). Ocotea diospyrifolia seeds are 13.2 mm long (7 mm in diameter) and the howlers were reported to swallow 100 % of removed seeds.

Table 5.2 Ranging pattern and gut passage time (GPT) of howler monkeys (Alouatta spp.), and characteristics of seeds in monkeys’ feces
Full size table
Table 5.3 Plant taxa dispersed by howler monkeys (Alouatta spp.) throughout their geographic rangea
Full size table

The ability to swallow large seeds (up to 4.6 cm length; Table 5.2) that are unlikely to be swallowed by smaller frugivorous animals makes the dispersal services offered by howler monkeys particularly relevant for large-seeded plants (Julliot 1996a; Andresen 2002a; Bravo 2009; Anzures-Dadda et al. 2011). For example, 83 % of the large-seeded fruit species (i.e., 5–25 mm in length) in the Paraná flooded forest (e.g., Lauraceae species) are dispersed by A. caraya (Bravo 2009). Also, genera such as Garcinia and Inga and many Sapotaceae species have seeds >3 cm long and are commonly found in howler monkeys’ defecations (Table 5.3). Ramos-Obregon (2007) found that howler monkeys disperse a larger biomass of seeds >4 mm (in width) than the smaller sympatric brown capuchins, and that the mass of seeds dispersed per fecal sample was also higher (12.1 g vs. 1.3 g). In addition, she found that adult howler monkeys defecated a larger biomass of seeds than juveniles (mean adult female: 15 g/sample, adult male: 12, and juvenile: 7), consistent with the idea that body size can limit seed dispersal abilities within a primate species (Stevenson et al. 2005). Given that juveniles, in general, eat the same species with the adults, this difference between age classes can be explained by higher seed spitting rates in juveniles than in adults.

Plant species with indehiscent hard-husked fruits also tend to have a limited assemblage of dispersers. This is due to the fact that small bats and avian frugivores have limited handling abilities to open protected fruits in comparison with primates and other mammals (Janson 1983). For such plant species, howler monkeys and non-flying mammals with biting and manipulative abilities will likely play a very important role in seed dispersal (Andresen 2000). This is again the case for most species in the Sapotaceae family, which are very diverse and dominant in the forests of the Guiana Shield and in Central Amazonia and are frequently dispersed by Guianan red howler monkeys (A. macconnelli; Julliot 1996b; Andresen 2002a). For example, during a 2-years period A. macconnelli in Brazil defecated seeds from 47 species of Sapotaceae with large seeds (average size ± SD: 19.6 ± 0.7 mm in length, and 11.2 ± 0.4 mm width; Andresen 2002a). Other species with hard indehiscent husks and for which howler monkeys provide important dispersal services include Dialium guianense, Inga spp., Genipa americana, and Gustavia hexapetala (Table 5.3).

The number of seeds dispersed per visit also depends on the length of a visit, and howler monkeys tend to have long feeding bouts. For instance, the time fruit feeding in a single tree by a group of A. palliata in Los Tuxtlas, Mexico, can reach 40 min (mean ± SD, 19.0 ± 7.0 min; Dunn et al. 2012), whereas A. caraya in Argentina can spend up to 2 h feeding on fruit in a single laurel tree (Ocotea diospyrifolia; Bravo 2012a). In fact, A. seniculus in Colombia spends on average 14 min (±15.6, SD) per tree feeding on fruits, which represent longer feeding bouts than those reported for three other sympatric primates (mean bout length: Cebus apella: 8.4 ± 10.3 min, Lagothrix lagothricha: 7.8 ± 9.3 min, and Ateles belzebuth: 6.9 ± 9.0 min; Stevenson et al. 1998). As argued by these authors, the stronger group cohesion in howler monkeys compared to Ateles and Lagothrix results in larger feeding subgroup sizes and longer feeding bouts (more fruits consumed per group feeding bout). This stable grouping pattern can result in howlers exploiting larger food patches (to accommodate all group members; group size in A. seniculus in Colombia averaged 9.3 ± 0.9 individuals), allowing individuals to spend more time feeding on each food patch (Stevenson et al. 1998) and minimizing thus the energy cost related to traveling between food patches.

2.1.2 Quality of Seed Dispersal

Seed treatment in the mouth and gut determines both the proportion of seeds destroyed (due to mastication and/or digestion) and the germination ability (percentage of seeds that are not destroyed) (Schupp 1993; Schupp et al. 2010). In general, researchers have considered howler monkeys as high quality seed dispersers because, despite a long transit time (18–35 h), seeds remain viable after passing through their gut (e.g., Milton 1980; Estrada and Coates-Estrada 1984; de Figueiredo 1993; Julliot 1996a; Santamaría 1999; Gonzalez-Di Pierro et al. 2011). Howler monkeys generally swallow seeds and rarely chew or spit out seeds (e.g., A. caraya: Bravo 2009; A. palliata: Wehncke et al. 2004). Occasionally, however, howler monkeys include unripe fruits in their diet, and in these cases they act as seed predators by selecting seeds before they are fully mature and capable of germination. In some cases these seeds are digested in the gut (Giraldo et al. 2007). However, several studies of howlers indicate that individuals show a marked preference for consuming mature fruits (80–90 % of fruit feeding time: Estrada and Coates-Estrada 1984, 1991; Giraldo et al. 2007; Amato and Estrada 2010), which implies a reduced likelihood of seed predation.

Gut passage can also positively affect germination and early seedling establishment through at least two mechanisms (Traveset et al. 2007): (1) scarification (i.e., removal or thinning of the seed coat); and (2) deinhibition (i.e., separation of the seeds from the pulp). The scarification process increases the permeability of seeds, allowing the exchange of gases and water, which in turn triggers germination in many seed species (Traveset et al. 2007). It has been reported that gut passage in howler monkeys can have a positive, neutral, or negative effect on germination (Table 5.4). On the other hand, the impact of deinhibition has not been assessed for seeds dispersed by howler monkeys, and studies focusing on how howlers treat, process, and void seeds are needed to gain a better understanding of all possible implications of gut passage on seed germination. It is important to note that deinhibition occurs not only for defecated seeds, but also for seeds that are spat or dropped. Therefore, although howler monkeys disperse most seeds through defecation, in future studies it would be very useful to analyze the effect of pulp removal on seed fate, not only for defecated seeds, but also for spat and dropped seeds.

Table 5.4 Gut passage net effect on seed germination rates (i.e., percentage of defecated vs. control seeds that germinated in trials) and latency period of seedsa
Full size table

Another positive effect of gut passage on seed survival and germination is the control of insect larvae present in the ingested fruits/seeds. For example, the passage of seeds through the gut of howler monkeys can kill insect larvae that infest seeds of Ocotea diospyrifolia (Lauraceae), increasing the probability of seed survival and germination (Bravo 2008). In other cases, larvae are not killed, and seed dispersal by monkeys actually favors insect dispersal (Hernández 2011). Both phenomena are probably widespread, but have so far received little attention. Finally, gut passage may also have effects beyond germination, i.e., on seedling survival and growth; however, the available evidence on this topic is very limited (e.g., Gonzalez-Di Pierro et al. 2011; Table 5.1).

While the quality of seed treatment is relatively easy to quantify and has thus received more attention (Tables 5.1 and 5.4), the quality of seed deposition is much harder to evaluate, as it requires an assessment of seed and seedling fate through the primary and secondary post-dispersal and post-germination phases (Schupp et al. 2010). Seed deposition quality can be affected by many variables. Some of these can be directly linked to characteristics of the primary disperser (e.g., howlers), while others cannot. Variables affecting deposition quality, which can be directly associated to the primary disperser, include movement, foraging, and defecation patterns (whether seeds are voided singly or in large clumps), diet, social structure, and frugivore gut size and food passage rates (Schupp 1993). These aspects of animal behavior will determine many specific circumstances of seed deposition which are known to affect seed fate, such as: (1) presence/absence of dung surrounding the seeds; (2) amount and type of dung surrounding the seeds; (3) amount of seeds and number of seed species dispersed together; and (4) dispersal distance with respect to conspecific fruiting trees (Andresen 1999). Most of these variables will affect seed/seedling fate indirectly, i.e., through the effect they have on the behavior of secondary seed dispersers and/or predators and fungal pathogens, which in turn will determine what happens to a seed or seedling. These biotic post-dispersal agents will be discussed separately in the next section.

In terms of dispersal distances, howler monkeys are able to disperse seeds far from the parent plant due to their high daily travel distances (mean = 497 m, range = 50–1,564 m: Bicca-Marques 2003; also see Table 5.2) and long retention times (up to 35 h; Table 5.2). Evidence indicates that seeds dispersed by howler monkeys are deposited at distances of up to 1,000 m or more from the parent plant (Table 5.2). Nevertheless, howler monkeys may also defecate or drop fruits underneath conspecific fruiting trees; a reason why some authors have considered these primates as low-quality dispersers (e.g., Howe 1980).

In fact, due to their cohesive social structure, and their digestive physiology, howler monkeys spend most of their time resting in large sleeping trees [mean = 64.2 %, range = 8–97 %; from Cristóbal-Azkarate and Arroyo-Rodríguez (2007) and Bicca-Marques (2003) reviews]. After the resting period, and before moving to another tree, all or most of the individuals in the group usually defecate simultaneously (this occurs 2–4 times in a 24 h period; A. palliata: Wehncke et al. 2004; A. s. puruensis: Andresen 1999; A. seniculus: Giraldo et al. 2007). This behavior results in high amounts of feces and seeds being deposited in latrines located under the sleeping trees (e.g., Chapman 1989; Julliot 1996a, 1997; Andresen 2002a; Wehncke et al. 2004; Pouvelle et al. 2009, Table 5.2). For example, Wehncke et al. (2004) report that 67 % of A. palliata feces in a tropical dry forest in Costa Rica are deposited under sleeping trees. Similar percentages have been reported for A. caraya in Argentina (65 %, Bravo 2009). Larger percentages have been reported, but these are usually related to howler monkeys living in smaller habitat patches (e.g., 90 % of A. caraya feces are deposited in latrines in a small tropical dry forest patch in Argentina; Bravo and Zunino 2000).

Despite this large aggregation of feces and seeds under sleeping trees and/or underneath conspecific fruiting trees, howler monkeys can also disperse a substantial fraction (33–35 %) of seeds in individual scats distributed across the forest (e.g., scattered pattern; Wehncke et al. 2004; Bravo 2009). Furthermore, during periods in which howler monkeys are eating large amounts of leaves, relative to fruits, seeds are reported to be dispersed in low densities (Andresen 2002a). Therefore, seed deposition patterns produced by howler monkeys can be considered mixed, i.e., a fraction clumped and another one scattered. However, given that clumped fecal deposits generally contain many more seeds than scatted fecal deposits, and there exist very few studies on the seedling survivorship of seeds voided by howlers, the specific impact of howler monkeys as seed dispersers relative to other fruit eating tropical vertebrates remains unclear (Russo and Chapman 2011).

The clumped defecation and seed deposition pattern produced by howler monkeys may be important in terms of soil nutrient enrichment. Evidence indicates that latrines are enriched in nutrients (e.g., N, P, and several minerals) compared to surrounding areas (Feeley 2005; Pouvelle et al. 2008; Neves et al. 2010), and may have positive effects on establishment, growth, and survival of seedlings arising from howler-dispersed seeds. For example, Bravo (2012b) found that the per capita survival of saplings taller than 1 m was higher in latrines than in control sites. This result is unlikely to be solely related to a higher rate of seed arrival and the possible saturation of biotic mortality agents, but is probably also affected by the higher nutrient availability in latrines (Russo and Augspurger 2004; Bravo 2012b). Thus, consistent with the ‘directed dispersal hypothesis’ (Howe and Smallwood 1982), howler monkeys may be depositing a large proportion of seeds in specific non-random habitats (i.e., latrines), where survival of seeds/seedlings could be relatively high. In fact, Bravo (2012b) also reports four times more saplings (and from more species) in latrines of A. caraya than in randomly selected areas within the forest, and that saplings >1 m tall of three tree species (Ocotea diopyrifolia, Nectandra megapotamica, and Eugenia punicifolia) have higher densities in latrines than below parent trees. Nevertheless, available evidence on this topic is very scarce and needs to be investigated more deeply.

2.1.3 Post-dispersal Seed Fate: Seed Predation and Secondary Seed Dispersal

Seed predation and secondary seed dispersal are considered key processes in the seed dispersal cycle (Wang and Smith 2002). These processes can greatly alter the initial seed shadow created by the primary seed dispersal agent, thus affecting the patterns of seedling recruitment (Forget et al. 2005; Russo and Chapman 2011). The behavior of seed predators and secondary dispersers is often directly affected by the particular characteristics of the seed deposition patterns produced by the primary seed dispersal agent. For howler monkeys in particular, seed density and the presence/amount of dung in individual dung piles, as well as the overall seed/dung density produced by scatter vs. clumped defecation patterns, are known to affect post-dispersal seed fate (Chapman 1989; Andresen 2002a, b; Wehncke et al. 2004; Santos-Heredia et al. 2010).

Rodents, ants, and dung beetles are known to be attracted to howler monkey defecations and to affect, positively or negatively, the fate of the seeds in them (e.g., Chapman 1989; Estrada and Coates-Estrada 1991; Andresen 1999, 2001; Martínez-Mota et al. 2004; Wehncke et al. 2004). While granivorous rodents and ants may act both as seed predators and secondary seed dispersers by actively searching for seeds in defecations, dung beetles act solely as secondary seed dispersers, as they search and use the fecal material, and move and bury accidentally seeds imbedded in it (Andresen and Feer 2005).

In general, rodents are known to be highly efficient in locating seeds dispersed by monkeys, and removal rates of 90 % or more are not uncommon (Chapman 1989; Estrada and Coates-Estrada 1991; Andresen 1999). Moreover, seeds embedded in relatively large quantities of feces have a higher probability of removal by rodents than seeds in small quantities or without feces (Chapman 1989; Andresen 1999, 2002a; Wehncke et al. 2004). Seed density can be another factor affecting seed removal by rodents, but much variation exists among microhabitats, seed species, and/or seasons/years (see Hulme 2002 and references therein). Although seed removal by rodents has been traditionally considered equivalent to seed predation, it is clear now that not all seeds removed by rodents are consumed. Depending on the rodent species, the seed species, and the overall fruit availability in a given moment, the probability of secondary seed dispersal by rodents, rather than predation, can be quite high (Forget et al. 1998; Feer and Forget 2002).

Secondary seed dispersal by dung beetles is characterized by burial and/or small horizontal movements (generally <1 m, Andresen and Feer 2005; Vulinec and Lambert 2009) of the seeds imbedded in the fecal material. In general, Neotropical dung beetles bury small and large seeds (up to approximately 3 cm), but there is a negative relationship between seed size and the percentage of seeds buried (Estrada and Coates-Estrada 1991; Feer 1999; Andresen and Feer 2005). Burial depth also varies greatly, but in general, most seeds are buried <5 cm (e.g., Andresen and Feer 2005). Seed burial by dung beetles greatly increases the probability of seed survival (Estrada and Coates-Estrada 1991; Andresen 1999, 2001, 2002b; Santos-Heredia et al. 2010) and, while seed burial may in some cases hinder seedling emergence (Feer 1999), it has been shown to have a significant net positive effect on seedling establishment of large-seeded species (Andresen 2001; Andresen and Levey 2004). In particular, twice as many seedlings emerged from seeds buried by beetles compared to defecated seeds that remained on the surface (Andresen and Levey 2004).

As with rodents, seeds surrounded by larger amounts of dung (as is often the case with seeds defecated by howler monkeys compared to seeds defecated by other frugivorous mammals including some other primates such as tamarins; Garber 1986) also have a higher probability of being removed by dung beetles (Andresen and Feer 2005). However, seed density per fecal clump does not seem to affect the probability of seed burial by dung beetles (Andresen 2002a; Culot et al. 2009). Regarding the influence of defecation patterns (clumped vs. scattered), results are not conclusive. Some studies report no significant effect of the defecation pattern on seed burial by dung beetles (Andresen 2002a; Ponce et al. 2006), but one study has reported increased seed burial rates for the clumped defecation pattern, but only for spider monkey dung, and not so for howler monkey dung (Santos-Heredia et al. 2010).

Although less studied, ants are likely to play very important roles as both predators and secondary dispersers of seeds defecated by howler monkeys, in particular of small seed species (<3 mm). A very extensive literature exists on seed predation and seed dispersal by ants in many different ecosystems. These studies illustrate how important these insects can be in plant–animal interactions (see Beattie and Hughes 2002 and references therein). For seeds defecated by howler monkeys, one study has shown that ants transport seeds to moist sites, rich in organic material, such as cracks in bark, ant gardens, and tunnel-like nests (Martínez-Mota et al. 2004). As argued by Martínez-Mota et al. (2004), these microsites may favor germination of some important epiphytic fig trees (Ficus spp.) and may thus constitute an example of directed seed dispersal.

Finally, post-dispersal seed fate is not only affected by rodents, dung beetles, and ants. Other biotic factors, such as pathogens (e.g., fungi) and other insect predators (e.g., bruchid beetles) also are responsible for the death of many dispersed seeds (Jones 1994). For example, Lambert (2002a, b) demonstrated that red-tailed guenons (Cercopithecus ascanius schmidti) consume fruits and spit out cleaned seeds of the tree Strychnos mitis, and that these seeds are significantly less likely to be attacked by seed predators and fungus than the unprocessed seeds. Further studies are needed to assess the impact of insect predators and fungus on post-dispersal fate of seeds dispersed by howler monkeys.

2.2 Effects on the Spatial Distribution of Individuals in a Plant Population

The implications of primary seed dispersal at the level of plant populations go beyond determining the number of seeds that are dispersed and affecting the probability those seeds have on producing a reproductive adult. While effective dispersal is necessary for the successful recruitment of new individuals, dispersal will also play an important role in determining the spatial distributions of those recruits, and possibly the spatial structuring of reproductive adults in a population or metapopulation. The spatial distribution of dispersed seeds is generally assessed by describing the seed shadow (number of seeds at different distances from the parent plant) and/or estimating the seed dispersal kernel (probability distribution of dispersed seeds relative to distance). Although the shape and size of seed shadows are recognized as having profound implications for population/metapopulation dynamics and community structure (see below), accurately estimating seed shadows, particularly for vertebrate-dispersed trees, remains an important challenge (Russo et al. 2006).

One of the main difficulties researchers face is how to incorporate complex animal behavior and their spatially explicit movement patterns, when estimating seed dispersal shadows (Russo and Augspurger 2004). Yet, the behaviors and movements of dispersers are known to create highly structured seed deposition patterns, often with no distance relationship to the parent plant (Schupp et al. 2002). Studies on tamarins, spider monkeys, and tapirs show evidence of how these animals, through their behavior and movement patterns, are responsible for the spatial distribution of individuals for some of the plant species they disperse (Garber 1986; Fragoso et al. 2003; Russo and Augspurger 2004).

No study has yet explicitly assessed the seed shadows created by howler monkeys for particular plant species, and only one has focused on the possible implications (Bravo 2012b). However, the potential impact that howler monkeys are having through their seed dispersal on the spatial distribution of local plants is repeatedly mentioned by authors. Indeed, since the seminal study by Milton (1980), it has been suggested that seed dispersal by howler monkeys could create a patchy spatial distribution of preferred fruit-tree species. Studies reporting ranging and defecation patterns for these primates (e.g., Julliot 1996a; Andresen 2002a; Bravo 2009), together with studies quantifying seedling abundance in howler latrines (e.g., Julliot 1997; Anzures-Dadda et al. 2011; Bravo 2012b), suggest that seed dispersal by howler monkeys may have strong effects on the spatial distribution of howler-preferred plants. This constitutes a very important avenue for future research, in particular for those plant species for which howler monkeys constitute the only or main seed dispersal agent.

3 Implications of Howler Monkey Seed Dispersal for Plant Communities

At the plant community level, howler monkeys are considered important seed dispersers because they can disperse the seeds of many plant species from different life forms (e.g., trees, lianas, palms, and epiphytes; Tables 5.2 and 5.3). Although most studies have reported fruit diets consisting of less than 40 species (Bicca-Marques 2003), studies of A. macconnelli indicate that in some areas howler monkeys are able to disperse the seeds of more than 100 plant species (110 species, French Guiana: Julliot and Sabatier 1993; Julliot 1996a; 137 species, Central Amazonia: Andresen 2002a). In general, howler monkeys can feed and disperse a fewer number of plant species than other primates in pristine habitats. For instance, in Tinigua Park, during the same year of observations, red howlers fed on 52 species, while capuchins fed on 106, woolly monkeys on 137, and spider monkeys on 97 (Stevenson et al. 2000, 2002). However, the number of species dispersed depends, in part, on local tree diversity and, hence, in forests with fewer tree species or due to their smaller home range howler monkeys may disperse seeds of a small number of fruit species (Ramos-Obregon 2007). The length of the study can also affect the number of species reported in the diet of primates. Many plant species fruit every two years, while most primate research studies last one year or less. Not surprisingly, the studies reporting >100 fruit species in howler monkey diet had a duration of two years.

As already mentioned, howler monkeys, as well as other arboreal mammals and a few large birds species such as toucans, may serve as the main dispersers of large-seeded plants (>10 mm, seed length) and/or plants with hard indehiscent husks. These plants may constitute a large proportion of the total tree species richness and stem density (e.g., Sapotaceae in Central Amazonia and the Guiana Shield); therefore, by dispersing seeds of these species, howler monkeys may affect the abundance and distribution of structurally important tropical plant populations, directly impacting the structure of plant communities and forest dynamics.

Seed dispersal by howler monkeys also may have important implications for the maintenance of high tree species diversity in tropical forests. For other primate species, in particular highly frugivorous atelines, it has been shown that primate density is positively associated with the diversity of regenerating plants (Stevenson 2011). Although the effect of less frugivorous primates, such as howler monkeys, is probably less strong, the effect of these primates still remains positive in models that predict the diversity of regenerating plants (Stevenson 2011).

Howler monkeys and other primates may promote species diversity not only through effective seed dispersal, but also through the highly structured seed shadow they produce (see above). Due to their behavior and ranging patterns, the seed shadow created by howler monkeys is characterized by areas of very high seed density in latrines, which are used repeatedly over time (Julliot 1997; Bravo 2009). It has been argued that such patterns of seed dispersal will create dissemination limitation for other potential plant recruitment sites, and consequently recruitment limitation, which is defined as the failure to establish seedlings in a suitable site (Schupp et al. 2002). In turn, recruitment limitation is one of the main mechanisms that are assumed to prevent competitive exclusion by superior competitors, and thus favoring the coexistence of many plant species (see Schupp et al. 2002 and references therein). Nevertheless, much research is still needed to clearly establish the relative importance of different aspects of recruitment limitation (Terborgh et al. 2011), as well as to ascertain its role in the maintenance of high plant species richness.

4 Implications of Howler Monkey Seed Dispersal for Conservation and Restoration

Large-bodied, seed-dispersers have been shown to be particularly vulnerable to hunting pressure and habitat destruction, with potentially severe cascading effects for plant regeneration (Peres and Palacios 2007; Stoner et al. 2007; Wilkie et al. 2011). Studies increasingly show that such disturbances disrupt plant-animal dispersal systems, causing changes in plant recruitment, and potentially changing forest composition and structure in sites without primates and/or with lower primate population sizes (Chapman and Onderdonk 1998; Stevenson and Aldana 2008; Gonzalez-Di Pierro et al. 2011; Stevenson 2011). In this sense, understanding the long-term effects that primate disappearance and/or population declines could have on the composition and structure of plant communities represents an important challenge for ecologists, primatologists, and conservation biologists (Chapman 1989; Russo and Chapman 2011; Stevenson 2011).

In this chapter we have shown that howler monkeys can have negative effects on seed dispersal. For example, they can deposit a large number of seeds in clumps, which can result in high seed and seedling mortality. Also, in some cases, howler monkeys can act as seed predators. Nevertheless, the positive effects are more frequently reported, indicating that they play an important role in Neotropical forest regeneration due to a combination of factors: (1) they are one of the most abundant frugivorous arboreal mammals; (2) they can spend ca. 50 % of their monthly or yearly feeding time consuming fruits, swallowing most of the seeds they handle, and defecating them undamaged; (3) gut passage rarely has a negative effect on germination and often has a positive one; (4) their behavior and ranging patterns create a highly structured seed shadow, i.e., a spatially heterogeneous distribution of seeds, that may enhance plant species diversity; (5) they disperse seeds of many plant species from different life forms, including trees, lianas, palms, and epiphytes; (6) they are likely to be the main seed dispersers of certain tree species (e.g., large-seeded species and/or with indehiscent hard-husked fruits), especially in small forest fragments in which other primates are absent; and (7) their dung enriches the soil (that is commonly poor in many tropical forests), and attracts secondary seed dispersers that move the seeds to microsites with higher probability of survival and seedling establishment.

Howler monkeys not only play an important role as seed dispersers in conserved habitats, but they can also be playing a crucial role in disturbed habitats. Unlike most large Neotropical mammal species, howler monkeys are highly resilient to disturbance, being able to maintain populations in disturbed habitats, such as forest fragments, secondary forests, and some types of agroecosystems (Vulinec et al. 2006; Williams-Guillén et al. 2006; Arroyo-Rodríguez and Dias 2010; Zárate et al. 2014). For example, in a small fragment in the Orinoco basin in Colombia without other large atelines, howler monkeys were estimated to disperse approximately 40,900 g of dry weight of seeds per km2 in 4 months (Ramos-Obregon 2007), equivalent to the dispersal rate of more frugivorous ateline primates at other sites (Stevenson 2007). Thus, it has been increasingly recognized that howler monkeys play a key role for local plant regeneration in disturbed habitats (e.g. Gonzalez-Di Pierro et al. 2011). However, in smaller and/or disturbed habitat patches, howler monkeys tend to spend a lower percentage of time feeding on fruits (Dias and Rangel-Negrin 2014) and exploit a smaller number of plant species (Bicca-Marques 2003; Cristóbal-Azkarate and Arroyo-Rodríguez 2007). This has also been found for other frugivorous primate species (e.g. Ateles geoffroyi; González-Zamora et al. 2009). Thus, in terms of the quantity of seeds dispersed, as well as the number of species dispersed, the role played by howler monkeys as seed dispersers at both the plant population and the plant community level appears to be lower in highly disturbed habitats. Nevertheless, the role played by these primates in such habitats will depend on the extent to which their populations are able to compensate for lost dispersal services due to the local extinction of other seed-dispersing animals and may thus be proportionally large. Such compensatory role, however, still remains to be assessed in future studies.

Howler monkeys can transport seeds among different forest types and conditions (e.g., continuous and fragmented forests, old-growth and secondary forests), contributing to secondary succession and thus aiding in the restoration of degraded habitats (e.g., Giraldo et al. 2007). Particularly relevant for forest restoration in degraded habitats is the fact that howler monkeys disperse seeds of both pioneer and old-growth forest species. Abundant dispersal of light-demanding and pioneer tree species, such as Ficus, Cecropia, Inga, and many liana species (Julliot 1996a; Cristóbal-Azkarate and Arroyo-Rodríguez 2007; Pouvelle et al. 2009) could favor rapid recruitment of vegetation in open areas. At the same time, dispersal of long-lived pioneer and old-growth forest species could favor the incorporation of such species in the seed and seedling bank, allowing for the continuation of succession.

Finally, soil nutrient enrichment through defecation is an important factor that may affect forest regeneration, particularly in degraded areas. Only three studies are available on this topic (Feeley 2005; Pouvelle et al. 2008; Neves et al. 2010), and all agree that howler monkeys’ dung contributes considerably to the horizontal and vertical redistribution of nutrients. For example, the clumped defecation pattern of howler monkeys can enrich the soil in nutrients such as phosphorus and nitrogenous, which are important for vegetation growth (Feeley 2005). Also the physical characteristics of the soil are improved due to increased activity of the soil microbial and microfaunal communities (Neves et al. 2010). Whether the improvement of soil characteristics in defecation sites actually translates into positive effects for plants (seedling survival, establishment, growth), either in conserved or disturbed habitats, is still unknown. This is a highly promising avenue for future research.

5 New Directions for Future Research

Overall, we found that several aspects of seed dispersal by howler monkeys (Alouatta spp.) have been studied throughout their geographic range (Table 5.1), but there are some important questions that need to be addressed to improve our understanding on the importance of howler monkeys as seed dispersers. First, we found that current evidence comes exclusively from studies of eight of 14–18 howler monkey species, and therefore studies of other species are needed to accurately determine (e.g., through meta-analyses) whether there are inter-specific differences in their contribution as seed dispersers. This is likely given differences in diet found across the genus Alouatta (see Dias and Rangel-Negrin 2014). Second, most studies have so far focused on well-conserved forests. Thus, more research is needed in fragmented/degraded forests in order to assess, for example, if seed dispersal effectiveness can be lower in these habitats, if primate disappearance and/or population declines can negatively affect forest regeneration, and the potential compensatory role of howlers in sites lacking other dispersal agents. Third, while the quantity component of seed dispersal has received much attention, some aspects of the quality component require further research (Table 5.1). These include: (1) the effect of pulp removal (deinhibition) on seed fate, not only for defecated seeds, but also for spat and dropped seeds; (2) the effect of gut passage on the control of insect larvae present in the ingested fruits/seeds; and (3) the impact of gut passage on seedling survival and growth.

Regarding the impact of howler monkeys on the spatial distribution of plants, no study to date has yet explicitly assessed the seed shadows created by howler monkeys for particular plant species. Also, the post-dispersal seed fate is not well understood. Studies are needed to fully assess the importance of ants, dung beetles, rodents, insect predators, and fungal pathogens in determining the fate of small-seeded species dispersed by howler monkeys and other primates. Finally, more investigation is also needed to assess the differences between clumped (e.g., in latrines) and scattered seed deposition patterns on seeds/seedlings survival and plant recruitment. Also, an interesting hypothesis that needs to be tested in future research is whether seed dispersal by howler monkeys creates a patchy spatial distribution of preferred fruit-tree species, creating food gardens within the forests (Milton 1980). This is possible if seeds deposited in latrines regenerate in greater density than seeds deposited in other areas, but evidence on this topic is scarce, and it is still unclear whether the improvement of soil characteristics in latrines actually translates into positive effects for plants (seedling survival, establishment, growth).