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From dropping to dropping: The contribution of a small primate to seed dispersal in Atlantic Forest
Acta Oecologica 100 (2019) 103464
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From dropping to dropping: The contribution of a small primate to seed dispersal in Atlantic Forest
T
Carla Cristina Gestich∗,1, Mariana B. Nagy-Reis2, Christini Barbosa Caselli3 Departamento de Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas, Rua Monteiro Lobato 255, Caixa Postal: 6109, CEP: 13083–862, Campinas, SP, Brazil
A R T I C LE I N FO
A B S T R A C T
Keywords: Callicebus nigrifrons Frugivory Seed germination Seed handling Titi monkey
The dynamic interaction between animals and plants through frugivory and seed dispersal is one of several ecological processes that modulates tropical biodiversity. Here we evaluated the potential role of a highlyfrugivorous Neotropical primate, the black-fronted titi monkey (Callicebus nigrifrons), as seed disperser. We studied two titi monkey groups in semideciduous Atlantic Forest remnants. Each group fed on over 49 zoochorous plant species in about one year and ingested seeds from nearly a half of them, especially those with small seeds (< 0.5 cm). The groups of titi monkeys defecated a large number of seeds, reaching over 300 seeds per day (1–305). More than half of the total deposited seeds and seed species germinated after gut passage, however gut passage reduced germination success in three of five evaluated species. Feces were deposited in small clumps distributed across groups’ home range. We suggest that the observed distribution pattern of feces may enhance plant reproductive fitness by increasing the probability of seeds being deposited far from parent plants, in novel and favorable sites. We concluded that the seed handling and deposition behavior of black-fronted titi monkey make this primate an important agent for Atlantic forest regeneration.
1. Introduction The dynamic interaction between zoochorous plants and animals through frugivory has important implications for animal and plant fitness (Howe and Smallwood, 1982; Jordano, 2000) and on ecosystem integrity (Mcconkey et al., 2012). Frugivores may act as seed dispersers by transporting unharmed seeds far away from parent plant (Norconk et al., 1998; Jordano, 2000), but also as seed predators, by destroying them and disrupting seed dispersal process (Peres, 1991; Stoner et al., 2007). Seed predation occurs when frugivorous animals chew and destroy the seeds in the mouth while consuming it or the fleshy pulp of fruits, or when they ingest entire seed but their digestive tract inhibits seed germination (Norconk et al., 1998; Jordano, 2000). However, rather than a dichotomy between seed predation and dispersal, there is a continuum between them that varies according to frugivore-plant interactions (Heleno et al., 2011). Consequently, the reproductive success of zoochorous plant species relies on the seed dispersal effectiveness of
the pool of frugivorous species that consume their fruits (Garber and Lambert, 1998; Calviño-Cancela, 2002; Stoner et al., 2007). The main components to evaluate the effectiveness of seed dispersal by frugivores are the quantity of seeds dispersed and the quality of the dispersal itself (Schupp, 1993). The first aspect is a function of the number of visits of a disperser to a plant and the number of seeds removed and deposited away from it (Schupp, 1993; Schupp et al., 2010). This aspect, in turns, depends on the animals' diet and feeding behaviour (Schupp, 1993; Jordano, 2000; Russo et al., 2006). The qualitative aspect is related to the probability of producing a new adult plant after seeds being manipulated and/or consumed by the disperser, which may include the passage of seeds through the animals' gut (Schupp, 1993; Stoner et al., 2007). In this sense, seed germination capability may be used as a proxy of qualitatively effectiveness when overall process cannot be measured. Animals’ manipulation and ingestion may have a negative or positive effect on seed germination success: it is negative when seeds are destroyed or the germination is inhibited,
∗
Corresponding author. E-mail address: [email protected] (C.C. Gestich). 1 Present address: Departamento de Genética e Evolução, Centro de Ciências Biológicas e da Saúde, Universidade Federal de São Carlos, Rodovia Washington Luís km 235, São Carlos, SP, Brazil, CEP: 13565-905. 2 Present address: Department of Biological Sciences, University of Alberta, 116 St. and 85 Ave, Edmonton, Canada, T6G 2R3. 3 Present address: Departamento de Biologia, Universidade Federal Rural de Pernambuco, Rua Dom Manoel de Medeiros, s/n, Dois Irmãos, Recife, PE, Brazil, CEP: 52171-90. https://doi.org/10.1016/j.actao.2019.103464 Received 13 March 2019; Received in revised form 8 August 2019; Accepted 25 August 2019 1146-609X/ © 2019 Elsevier Masson SAS. All rights reserved.
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monkeys’ feces and tested if titi monkeys improve seed germination success. We expect that overall germination performance of seeds (the proportion that germinates and the latency to germinate) will be enhanced in seeds from feces compared to seeds from fresh fruits.
whereas it is positive when increases the speed of seed germination (Lieberman and Lieberman, 1986; Schupp, 1993). This last process may also enhance seedling survival by reducing the time of seed exposure to predators and diseases (Schupp, 1993). Another key aspect of the qualitative component of the seed dispersal effectiveness is the spatial pattern of seed deposition (Schupp, 1993; Wehncke et al., 2004). Seed dispersal effectiveness is favored by seed deposition at sites with adequate conditions for germination and under reduced competition pressure, such as far from the parent plant, and in novel sites not yet colonized (Augspurger, 1984; Chapman and Russo, 2006; Bueno et al., 2013). The spatial pattern of seed deposition by frugivores is a consequence of gut passage time and the ranging behavior of the species. For instance, frugivorous species that travel long distances daily and have a longer interval between defecations may disperse seeds further from parent plants and in a less clumped pattern (Chapman and Russo, 2006; Russo et al., 2006; Stoner et al., 2007). In this context, the feces deposited in a scattered pattern is supposed to favor the survival of dispersed seeds (Howe and Miriti, 2004; Wehncke et al., 2004). Frugivorous animals contribute differently to plant reproduction fitness due to their variable diet, feeding behaviour, seed processing, and feces deposition (Wehncke et al., 2004; Chapman and Russo, 2006; Stoner et al., 2007; Fuzessy et al., 2018). In tropical forests, primates are a key group of seed dispersers because they represent a prominent percentage of the frugivore biomass and most species heavily rely on fruits (Chapman, 1995; Lambert and Garber, 1998; Chapman and Russo, 2006). However, primates face a worrisome threat of extinction, and their absence may represent an imbalance in ecosystem health (Nuñez-Iturri et al., 2008; Chapman et al., 2013; Estrada et al., 2017, 2018). Therefore, understanding the potential role of different primate species in dispersing seeds is essential to comprehend primates’ role as forest maintainer and to help elucidate what and how conservation efforts should be directed (Chapman and Onderdonk, 1998). Here we evaluated the potential role of a highly-frugivorous Neotropical primate, the black-fronted titi monkey (Callicebus nigrifrons, Spix 1823, Pitheciidae), as a seed disperser in the Atlantic Forest. In this study, we evaluated some aspects of seed dispersal effectiveness by titi monkeys, as a first approach about their contribution to forest regeneration. Despite a recent increasing number of publications on seed dispersal (Razafindratsima et al., 2018), data on the role of primates is available only for a few Neotropical species, none of which from Callicebinae species (reviewed by Fuzessy et al., 2018). Titi monkeys are small primates (1–2 kg, Bicca-Marques and Heymann, 2013), with a great potential for seed dispersal, as they are predominantly frugivorous (Caselli and Setz, 2011; Boyle et al., 2016; Nagy-Reis and Setz, 2017), a characteristic associated with increased probability of ingesting seeds and dispersing zoochorous species (Fuzessy et al., 2016, 2018). Different from other pitheciid species, titi monkeys present lesser degree of morphological adaptations to forage on mechanically resistant foods, such as seeds (Kinzey, 1992), and their frugivorous diet relies mainly on fruit pulp (Caselli and Setz, 2011; Nagy-Reis and Setz, 2017). Nonetheless, titi monkeys' position in the seed dispersal-predation gradient is still poorly investigated. Uncovering the role of titi monkeys as seed disperser is especially important in endangered biomes such as the Atlantic Forest, subjected to high fragmentation rate (Ribeiro et al., 2009). This landscape changing is leading to the disappearance of mammal frugivore species (Canale et al., 2012), but titi monkeys seem to persist (São Bernardo and Galetti, 2004; Gestich et al., 2019). In this context, we described titi monkeys' feeding behaviour on fruits, registering the zoochorous species ingested, their seed handling and seed size. Then, we characterized some aspects of both the quantitative and qualitative components of seed dispersal effectiveness of titi monkeys. To characterize one of the aspects of the quantitative component, we quantified the number of seeds in their feces as a proxy of the amount of seeds removed from parent plants. Regarding the qualitative component, we evaluated the distribution pattern of titi
2. Methods 2.1. Monitored groups and study sites We studied two habituated free-ranging groups of black-fronted titi monkey (Callicebus nigrifrons) at two protected areas of Atlantic Forest in São Paulo State, Southeast Brazil. One group (5–6 individuals) was monitored in a 350-km2 forest remnant (Serra do Japi: 23°14′S, 46°56′W) and the second (3–5 individuals) was monitored in a 2.45km2 forest remnant (Ribeirão Cachoeira: 22°49′S, 46°55′W). Both areas are characterized by semideciduous secondary Atlantic Forest and seasonal climate, with mean annual temperature about 19 °C (Japi group study site) and 22 °C (RC group study site), and total annual rainfall about 1400 mm (Cepagri, 2011, Ciiagro, 2011). Like other Neotropical rainforests, Atlantic Forest integrity depends on the presence of frugivores since most plant species have zoochorous dispersal syndromes (Almeida-Neto et al., 2008; Jordano, 2000). In our study areas, for instance, about 60–70% of wood plants species have zoochorous dispersal syndrome (Morellato and Leitão-Filho, 1992; Garcia et al., 2014). At both study sites, titi monkeys co-occur with other less frugivorous species, such as coati (Nasua nasua) and porcupine (Coendou prehensilis), and also with other less frugivorous primates, such as marmosets (Callithrix aurita) at Serra do Japi and howler monkeys (Alouatta guariba clamitans) and marmosets (Callithrix spp.) at Ribeirão Cachoeira. These species were observed feeding on fruits of some of the same plant species as titi monkeys. 2.2. Data collection 2.2.1. Feeding behavior and seed handling Data collection on Japi group was done over 11 months (N = 40 days, from August 2010 to June 2011) and on RC group over 12 months (N = 52 days, from June 2010 to May 2011), during three to five days per month. This study is part of a longer monitoring study of a total of 20 and 13 months, respectively (Caselli, 2013; Gestich, 2012; NagyReis, 2012). Both groups were monitored from dawn to dusk (i.e., complete days) or from the moment they were found until the moment they were lost (i.e., partial days with at least 6 h of monitoring). We recorded animals' behavior through scan sampling every 5 min (Altmann, 1974), and the central spatial position of the group every 10 min with a GPS receiver. Based on these scan samples we calculated the proportion of recordings invested in feeding activity. Additionally, at each feeding scan, we recorded the type of item and the plant species that animals consumed and estimate the contribution of each plant species (trees or vines) with zoochorous syndrome of dispersion to titi monkeys' pulp fruit diet. We calculated the relative importance of each zoochorous species in titi monkeys’ diet as a percent of feeding records from the scan sampling. We then determined the most consumed zoochorous plant species for pulp fruit as those species with a cumulative contribution of 75% in the feeding records, considering the entire period of the study. For those species only, we determined how titi monkeys handled their seeds (preyed, spat out, or swallowed) based on ad libitum records. Taxonomic specialists (see acknowledgements) identified the plant species, and when the identification was not possible, we used the morphospecies as a surrogate for taxonomic species. 2.2.2. Characterization of seeds We collected the feces immediately after defecation. We washed each sample in running water, using a 1-mm mesh sieve. We then separated and counted all seeds using a stereomicroscope and identified 2
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germination time (number of days until the emergence of the radicle) between control and treatment, testing each plant species individually. For that, we performed a time-to-event analysis with the Kaplan–Meier estimator to compare treatment groups for potential differences in temporal patterns of germination, which consider the joint influence of time and percentage of seed germination (MacNair et al., 2012). We adopted the non-parametrical approach with exact data (continuous observation), using Peto-Peto weight function, implemented by function “survdiff” in package “survival” (Therneau, 2015). We considered each seed of each specie and treatment as a replicate. We performed the analyses in R software version 3.5.2 (R Development Core Team, 2018).
seed species (or morphospecies). We determined the seed size by measuring the longest dimension of seeds from feces samples. We classified each seed species as small- (≤0.5 cm), medium- (> 0.5 and ≤2.0 cm), and large-seed (> 2 cm) (following Wrangham et al., 1994). In addition, we determined seed size from those zoochorous species not found in titi monkeys’ feces but present in the list of the most consumed species, either by directly measuring seeds from fresh fruits or obtaining this information from literature (Lorenzi and Matos, 2002). 2.2.3. Seed germination trials We performed germination trials for all seeds obtained from Japi group's feces. We separated the seeds from feces and incubated all them on wet filter paper in Petri-dishes. We placed the seeds at distances of 3–5 seeds from each other, limiting the number of seeds in each Petridish according to seed size. We kept the seeds under the natural regime of light in a natural illuminated laboratory at the study site and we wet the seeds whenever necessary to keep them constantly moist. We checked the seeds daily until the emergence of the radicle or obvious death of the seeds (following Lieberman and Lieberman, 1986). Then, we calculated the cumulative proportion of seeds per species that germinated, and the mean time elapsed until germination. We also compared the germination success of seeds present in the feces (i.e., treatment) with those from fresh fruits (i.e., control). Given the probability of being dispersed increases with dispersers’ feeding rate of fruits from a species (Schupp, 1993; Jordano and Schupp, 2000), we selected for controlled germination trials only the zoochorous species present among the most consumed species by Japi group (Table 1). For the control, we used seeds from mature intact fruits without a bitten sign and insect infestation collected under the plants in which we observed Japi group foraging. We collected seeds from different fruits and from different plant individuals of each tested species on which titi monkeys foraged. We removed the seeds from fruit pulp and washed them following the same procedure used to clean seeds from feces. Control and treatment were kept under the same conditions and comprised the same amount of seeds, except when the number of seeds from fresh fruits was limited (see Table 2). We compared germination frequency (number of seeds) and
2.2.4. Spatial distribution of feces We recorded the position of each defecation with a GPS receiver (Japi group N = 326; RC group N = 470). We estimated the feces spatial distribution pattern with a 100% Kernels using the “kernelUD” function from the “adehabitatHR” package (Calenge, 2017), assuming a bivariate normal distribution, with the smoothing parameter as a fixed radius of 25 m (same radius adopted in our previous study; Caselli et al., 2017). The UD (Utilization Distribution) map describes the intensity of defecation records by calculating the probability of new feces being deposited at each site according to the number of feces within the fixed radius value. We plotted the Kernel map of feces over the groups' home range, calculated with the minimum convex polygon (MCP; Hayne, 1949) using 100% of the recorded locations of groups during monitoring (adehabitatHR package, Calenge, 2017). To aid our interpretation of feces distribution pattern, we also georeferenced all sleeping sites where all group members spent the night together, since sleeping sites distribution is recognized as important influence on seed shadow for several primate species (Chapman and Russo, 2006; Russo et al., 2006). We plotted the sleeping site locations in the map using the “layer” function from the “latticeExtra” package (Sarkar and Andrews, 2016). In addition, we superimposed a virtual grid of 25 × 25 m over each group home range and counted the number of defecation records in each quadrant. Then, we used a Chi-square test to investigate whether the deposition of feces was higher near to sleeping sites than expected by chance. To do this, we compared the number of defecation records close to sleeping sites (in cells with sleeping sites plus cells with a shared side or corner with these cells) with the number of records not close to sleeping sites. To calculate the values expected by chance we considered the proportional contribution of these two types of cells (with sleeping sites or close to one and without sleeping sites) to groups’ total home range. Finally, to describe the distances traveled by titi monkey groups, we calculated the daily path length of the Japi group based on the 10 min samplings of group's spatial position, using “adehabitatLT” package (Calange, 2006). This data has already been obtained for the RC group (Nagy-Reis and Setz, 2017). All spatial analyses were performed in R software (R Development Core Team, 2018).
Table 1 Percentage contribution and seed size of the most consumed (sum > 75%) zoochorous plant species by Callicebus nigrifrons. Seed size: ≤0.5 cm is small, > 0.5 and ≤ 2.0 cm is medium, > 2.0 cm is large. The species indicated by an asterisk are those also found in the feces. Titi monkey groups
Plant species
Records of consumption (%)
Seed size
Japi
Miconia cinnamomifolia * Ocotea puberula * Maytenus robusta Non-identified vine I * Eugenia uvalha Myrcia rostrata Struthanthus complexus Non-identified tree * Ficus luschnathiana * Non-identified vine II
34.0
small
8.5 8.0 5.8 4.8 3.6 3.5 3.2 3.2 2.5 ∑ 77.1
medium medium medium medium medium small small small medium
17.4 17.3 9.3 9.1 8.2 5.3 4.8 4.0 ∑ 75.4
small medium medium small large medium medium medium
RC
Ixora gardneriana* Calycorectes acutatus Neomitranthes glomerata Pereskia aculeata* Syagrus romanzoffiana Diclidanthera sp.* Eugenia glazioviana Alchornea glandulosa
3. Results 3.1. Feeding behaviour and seed handling About half of the titi monkeys' feeding records came from events in which they fed on flesh pulp of fruits from zoochorous species (Japi group = 62% of feeding records, N = 3,648; RC group = 47%, N = 3,071). In lower proportion, seeds was the second (RC group = 22% seeds, 19% vegetative plant parts, 10% invertebrates, 2% other, see in Nagy-Reis and Setz, 2017) and the third (Japi group = 11.5% vegetative plant parts, 11.3% seeds, 10.5% invertebrates, 4.7% other) consumed food item. All seeds consumed by Japi group was from non-zoochorous species (411 feeding records from 12 species), and the most consumed species for seeds (Croton floribundus, an autochorous species) represented only 6.2% of total diet. Titi monkeys consumed fleshy pulp of fruits from 66 to 49 zoochorous 3
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Table 2 Temporal pattern of seed germination of five species consumed by Callicebus nigrifrons (Japi group). Total germination (percentage) and mean latency to germinate (in number of days) of ingested (feces) and fresh (control) seeds. Species
Chi-squared test with the Kaplan–Meier estimator
Treatment
Replicates (N)
Germination (%)
Latency (days ± SD)
Miconia cinnamomifolia*
X2 = 289
Feces Control
478 414
56 90
33 ± 13 21 ± 11
Ocotea puberula*
X2 = 16.1
Feces Control
21 20
29 95
41 ± 27 39 ± 27
Non-identified vine I
X2 = 0.6
Feces Control
25 25
84 96
14 ± 5 14 ± 7
Non-identified tree
X2 = 0.5
Feces Control
82 17
62 82
24 ± 56 69 ± 35
Ficus luschnathiana*
X2 = 110
Feces Control
361 201
83 97
35 ± 22 22 ± 9
*p < 0.001.
concentrated close to sleeping sites (Group 1: X2 = 104.38, df = 1, p < 0.001; Group 2: X2 = 11.35, df = 1, p < 0.001).
species, in which ten and eight species (Japi group and RC group, respectively) represent a cumulative contribution of 75% to their total feeding time (herein the most consumed species; Table 1). Considering the most consumed species, they swallowed the seeds (together with the pulp) of all species with small-sized seeds, except one (Struthanthus complexus). Although they typically spat out all medium and large seeds, we occasionally found intact medium-sized seeds of Ocotea puberula (Japi group), Diclidanthera sp. (RC group), and an unidentified vine (Japi group) in titi monkeys’ feces. None of these larger seeds were found destroyed in the feces.
4. Discussion Black-fronted titi monkeys invest a substantial proportion of feeding time on consuming pulp of fruits from zoochorous plant species and ingested the seeds of about half of them, depositing a large quantity of seeds in their feces, mostly small-sized seeds. Germination success was similar or inferior to that of seeds retrieved from fresh fruits, contrary to what we expected. However, although not in a uniform pattern, titi monkeys' feces were spread broadly across the groups’ home range. Therefore, given the high number of seeds deposited from diverse zoochorous species (a quantitative component of seed dispersal effectiveness) and the broad distribution pattern of feces (a qualitative component), we cannot discard the potential of titi monkeys to enhance plant reproductive fitness by spreading their seeds throughout their home range. Titi monkeys feed mainly on fruit pulp and occasionally on unripe seeds of non-zoochorous species (Caselli and Setz, 2011; Souza-Alves et al., 2011; Nagy-Reis and Setz, 2017, present study). Different from other seed predator Pitheciidae species, Callicebiin species have less specialized dentition to forage on mechanically resistant foods (Kinzey, 1992), reducing their potential as seed predators. By ingesting seeds while consuming fruit pulp of zoochorous species, titi monkeys may have an important role on forest regeneration, as already reported to other Atlantic Forest primate species (Bufalo et al., 2016). The amount of seeds defecated by titi monkey groups may reach a minimum of 300 seeds per day. Considering that our sampling did not include all feces deposited, this is an underestimation of feces deposition, and so seed deposition may reach even higher values per day. The quantitative potential of titi monkeys as seed disperser is skewed to plant species with small-sized seeds (< 0.5 cm) since they consistently swallowed a high amount of these seeds with fruit pulp and often discarded larger seeds. Plant species with the reproductive strategy of producing a large amount of fruits with small seeds attract a wide range of seed disperser species, including small mammals and birds (Jordano, 2000; Stoner et al., 2007). In this case, the complementarity of seed dispersers can increase plant fitness due to differences in their seed handling and deposition pattern. Small seeds generally are ingested with the fruit pulp and are less likely to be chewed or destroyed by chewing (Norconk et al., 1998; Fuzessy et al., 2018). In fact, we barely found destroyed (i.e., broken) seeds in titi monkeys' feces. In addition, although the ingested seeds are primarily from plant species with small seed size, some medium-sized seeds were also sporadically swallowed and deposited intact with titi monkeys’
3.2. Characteristics of deposited seeds We found an average of 45 ± SD 59 seeds (Japi group: range = 1–305 seeds, N = 40) and 24 ± SD 45 seeds (RC group: range = 1–263, N = 51) from feces collected per day. We found seeds in titi monkeys' feces from nearly a half of the zoochorous species that they consumed during the study period (Japi group: 42%, N = 66 plant species; RC group: 55%, N = 49 plant species). Seeds of most plant species found in titi monkeys' feces had small size (Japi group: 58%, N = 28; RC group: 68%, N = 27). In addition, more than 90% of the total seeds found in titi monkeys’ feces, irrespective of the species, were smaller than 0.5 cm (Japi group = 93%, N = 1,307 seeds; RC group = 94%, N = 339 seeds). Less than 1% of seeds found in their feces, all them from small size, was damaged or broken. 3.3. Seed germination trials More than half of the seeds (56%, N = 1,307 seeds) and seed species (54%, N = 28 species) found in Japi group's feces germinated. But germination success was not improved in any case of controlled experiments, contrary to the expected pattern. The temporal pattern of seed germination was the same between control and treatment for two of the five tested species and higher in the control for the other three (Table 2). 3.4. Feces spatial deposition Titi monkeys traveled about 1 km per day (Japi group:1.07 ± SD 0.15 km, N = 40 days; RC group: see Nagy-Reis and Setz, 2017). We registered 2–19 defecations per day (Japi group: 7.3 ± SD 3.4 feces, N = 40 days; RC group: 8.9 ± SD 4.5, N = 52 days). Defecation activity was not conspicuously synchronized among individuals throughout the day, except early in the morning when they leave the sleeping sites. Feces were distributed throughout the entire home ranges of the groups with a few denser nuclei of defecation (Fig. 1) 4
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and S. mystax, Muñoz Lazo et al., 2011) and other mammal (e.g., duikers, Feer, 1995) and bird species (e.g., cassowary, Mack, 1995). In addition, titi monkeys travel along ca. 1 km daily (present study and data available for RC group in Nagy-Reis and Setz, 2017) and rarely returned to the same place in the same day (pers. obs.). This information together with the long-estimated gut transit time, ranging from about three to over 4.5 h (Baião et al., 2015), suggest that seeds consumed in an individual tree are probably defecated far from it. Yet, considering that none of plant species used as sleeping site are feeding trees (Caselli et al., 2017), the observed distribution pattern of feces has the potential to enhance plant reproductive fitness by increasing the probability of seeds being deposited far from parent plants, in novel and favorable sites. The seed ingestion and deposition patterns by titi monkeys suggest that this small Neotropical primate mainly favors the reproductive fitness of small-seeded plant species. Even though their disperser role may be less efficient for some species, titi monkeys' overall contribution to forest regeneration may be essential in the current degraded scenario of Atlantic Forest. Further studies, encompassing the whole seed dispersal effectiveness framework will be essential to fully comprehend titi monkeys' contribution to plant fitness. The occasional dispersal of medium-sized seeds also may have special importance to plant fitness where larger frugivores are extinct or scarce. Since frugivores affect differently seed fate due to their specific fruit handling and seed processing (Lugon et al., 2017), a high diversity of potential dispersers may guarantee the complementarity of seed dispersal function (Bueno et al., 2013; Chapman et al., 2013). The complementary role of seed dispersers, including titi monkeys, is especially important to the Brazilian Forest Atlantic biome, which currently have only about 12% of its original covers (Ribeiro et al., 2009), and is increasingly defaunated and losing ecological services, such as seed dispersal (Jorge et al., 2013; Dirzo et al., 2014). Considering titi monkeys’ high persistence in small fragments (São Bernardo and Galetti, 2004; Bufalo et al., 2016; Gestich et al., 2019), this Neotropical primate may be a key species for forest regeneration, sowing the forest from dropping to dropping.
Fig. 1. Titi monkeys' feces distribution within Japi (a) and RC (b) groups' home range (black polygon MCP considering 100% of registers: Japi group = 32 ha, RC group = 18 ha) according to kernel utilization distribution (UD) estimates. The colour intensity represents an index that indicates probability of new feces being deposited at each site, Δ indicates sleeping sites.
Author contributions
feces. This eventual swallowing may exert a relevant contribution to the parent plant reproductive success when their fruits are consumed in a great proportion by a frugivorous species (Lambert and Garber, 1998; Jordano and Schupp, 2000; Chapman and Russo, 2006). Titi monkeys do not seem to improve seed germination, either proportion or latency time of germination. In fact, they reduced germination success of three from five tested species. However, given that at least half of all swallowed seeds (54%) survived and germinated after gut passage, and that these seeds are spread over a larger area being most probably deposited away from a parent tree, we cannot discard the potential benefit of titi monkeys to overall plant fitness. Even for those species in which titi monkeys reduced their germination success, seed deposition far from parent plant can also contribute to the overall recruitment success (i.e., seed to adult survival), likely greater than if they were deposited under the parent plants. Although titi monkeys’ feces were also deposited in some denser nuclear areas (Fig. 1), which could represent an increased competition among seedlings (Harms et al., 2000; Wehncke et al., 2004), they defecated across their entire home range, not only in restricted clumps, enhancing the probability of seeds being deposited in favorable microsites (Rogers et al., 1998; Howe and Miriti, 2004). The clumped pattern of feces deposition by primates is commonly related to the concentration of feces near sleeping sites (Chapman and Russo, 2006, Link and Di Fiori, 2006; Russo et al., 2006). In the case of titi monkeys, the early morning defecation bouts explain the increased density of feces near some sleeping sites (Fig. 1). The same aggregated pattern is also observed for other repeatedly used sites, such resting sites of tamarins (Saguinus fuscicolis
All authors conceived the ideas of the study, collected the data in the field and contributed to the writing of the manuscript. C.C.G. conducted the analyses and led the writing of the manuscript. All authors gave their final approval for submission.
Declarations of interest None.
Acknowledgements We are grateful to the Jundiaí City Hall and Colinas do Atibaia gated community for permission to conduct this research at Serra do Japi Municipal Reserve and Ribeirão Cachoeira, respectively. We thank J.Y. Tamashiro (Botanical Department, UNICAMP), L. Garcia, J. A. Gomes and G. Shimizu for plant species identification. We also thank Cássia A. Gestich for helping in the germination monitoring. The species assessed in this study was registered according to new Brazilian legislation on access to the biodiversity (Law 13,123/15 and Decree 8772/16) under the SisGen License AEB363E. This work was supported by FAPESP, Brazil (CBC: Process #2008/05127-0; CCG: process #2010/04034-9; MBNR: Process #2009/12124-0) and received equipment from Idea Wild, USA. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brasil (CAPES) -Finance Code 001. 5
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From dropping to dropping: The contribution of a small primate to seed dispersal in Atlantic Forest
T
Carla Cristina Gestich∗,1, Mariana B. Nagy-Reis2, Christini Barbosa Caselli3 Departamento de Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas, Rua Monteiro Lobato 255, Caixa Postal: 6109, CEP: 13083–862, Campinas, SP, Brazil
A R T I C LE I N FO
A B S T R A C T
Keywords: Callicebus nigrifrons Frugivory Seed germination Seed handling Titi monkey
The dynamic interaction between animals and plants through frugivory and seed dispersal is one of several ecological processes that modulates tropical biodiversity. Here we evaluated the potential role of a highlyfrugivorous Neotropical primate, the black-fronted titi monkey (Callicebus nigrifrons), as seed disperser. We studied two titi monkey groups in semideciduous Atlantic Forest remnants. Each group fed on over 49 zoochorous plant species in about one year and ingested seeds from nearly a half of them, especially those with small seeds (< 0.5 cm). The groups of titi monkeys defecated a large number of seeds, reaching over 300 seeds per day (1–305). More than half of the total deposited seeds and seed species germinated after gut passage, however gut passage reduced germination success in three of five evaluated species. Feces were deposited in small clumps distributed across groups’ home range. We suggest that the observed distribution pattern of feces may enhance plant reproductive fitness by increasing the probability of seeds being deposited far from parent plants, in novel and favorable sites. We concluded that the seed handling and deposition behavior of black-fronted titi monkey make this primate an important agent for Atlantic forest regeneration.
1. Introduction The dynamic interaction between zoochorous plants and animals through frugivory has important implications for animal and plant fitness (Howe and Smallwood, 1982; Jordano, 2000) and on ecosystem integrity (Mcconkey et al., 2012). Frugivores may act as seed dispersers by transporting unharmed seeds far away from parent plant (Norconk et al., 1998; Jordano, 2000), but also as seed predators, by destroying them and disrupting seed dispersal process (Peres, 1991; Stoner et al., 2007). Seed predation occurs when frugivorous animals chew and destroy the seeds in the mouth while consuming it or the fleshy pulp of fruits, or when they ingest entire seed but their digestive tract inhibits seed germination (Norconk et al., 1998; Jordano, 2000). However, rather than a dichotomy between seed predation and dispersal, there is a continuum between them that varies according to frugivore-plant interactions (Heleno et al., 2011). Consequently, the reproductive success of zoochorous plant species relies on the seed dispersal effectiveness of
the pool of frugivorous species that consume their fruits (Garber and Lambert, 1998; Calviño-Cancela, 2002; Stoner et al., 2007). The main components to evaluate the effectiveness of seed dispersal by frugivores are the quantity of seeds dispersed and the quality of the dispersal itself (Schupp, 1993). The first aspect is a function of the number of visits of a disperser to a plant and the number of seeds removed and deposited away from it (Schupp, 1993; Schupp et al., 2010). This aspect, in turns, depends on the animals' diet and feeding behaviour (Schupp, 1993; Jordano, 2000; Russo et al., 2006). The qualitative aspect is related to the probability of producing a new adult plant after seeds being manipulated and/or consumed by the disperser, which may include the passage of seeds through the animals' gut (Schupp, 1993; Stoner et al., 2007). In this sense, seed germination capability may be used as a proxy of qualitatively effectiveness when overall process cannot be measured. Animals’ manipulation and ingestion may have a negative or positive effect on seed germination success: it is negative when seeds are destroyed or the germination is inhibited,
∗
Corresponding author. E-mail address: [email protected] (C.C. Gestich). 1 Present address: Departamento de Genética e Evolução, Centro de Ciências Biológicas e da Saúde, Universidade Federal de São Carlos, Rodovia Washington Luís km 235, São Carlos, SP, Brazil, CEP: 13565-905. 2 Present address: Department of Biological Sciences, University of Alberta, 116 St. and 85 Ave, Edmonton, Canada, T6G 2R3. 3 Present address: Departamento de Biologia, Universidade Federal Rural de Pernambuco, Rua Dom Manoel de Medeiros, s/n, Dois Irmãos, Recife, PE, Brazil, CEP: 52171-90. https://doi.org/10.1016/j.actao.2019.103464 Received 13 March 2019; Received in revised form 8 August 2019; Accepted 25 August 2019 1146-609X/ © 2019 Elsevier Masson SAS. All rights reserved.
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monkeys’ feces and tested if titi monkeys improve seed germination success. We expect that overall germination performance of seeds (the proportion that germinates and the latency to germinate) will be enhanced in seeds from feces compared to seeds from fresh fruits.
whereas it is positive when increases the speed of seed germination (Lieberman and Lieberman, 1986; Schupp, 1993). This last process may also enhance seedling survival by reducing the time of seed exposure to predators and diseases (Schupp, 1993). Another key aspect of the qualitative component of the seed dispersal effectiveness is the spatial pattern of seed deposition (Schupp, 1993; Wehncke et al., 2004). Seed dispersal effectiveness is favored by seed deposition at sites with adequate conditions for germination and under reduced competition pressure, such as far from the parent plant, and in novel sites not yet colonized (Augspurger, 1984; Chapman and Russo, 2006; Bueno et al., 2013). The spatial pattern of seed deposition by frugivores is a consequence of gut passage time and the ranging behavior of the species. For instance, frugivorous species that travel long distances daily and have a longer interval between defecations may disperse seeds further from parent plants and in a less clumped pattern (Chapman and Russo, 2006; Russo et al., 2006; Stoner et al., 2007). In this context, the feces deposited in a scattered pattern is supposed to favor the survival of dispersed seeds (Howe and Miriti, 2004; Wehncke et al., 2004). Frugivorous animals contribute differently to plant reproduction fitness due to their variable diet, feeding behaviour, seed processing, and feces deposition (Wehncke et al., 2004; Chapman and Russo, 2006; Stoner et al., 2007; Fuzessy et al., 2018). In tropical forests, primates are a key group of seed dispersers because they represent a prominent percentage of the frugivore biomass and most species heavily rely on fruits (Chapman, 1995; Lambert and Garber, 1998; Chapman and Russo, 2006). However, primates face a worrisome threat of extinction, and their absence may represent an imbalance in ecosystem health (Nuñez-Iturri et al., 2008; Chapman et al., 2013; Estrada et al., 2017, 2018). Therefore, understanding the potential role of different primate species in dispersing seeds is essential to comprehend primates’ role as forest maintainer and to help elucidate what and how conservation efforts should be directed (Chapman and Onderdonk, 1998). Here we evaluated the potential role of a highly-frugivorous Neotropical primate, the black-fronted titi monkey (Callicebus nigrifrons, Spix 1823, Pitheciidae), as a seed disperser in the Atlantic Forest. In this study, we evaluated some aspects of seed dispersal effectiveness by titi monkeys, as a first approach about their contribution to forest regeneration. Despite a recent increasing number of publications on seed dispersal (Razafindratsima et al., 2018), data on the role of primates is available only for a few Neotropical species, none of which from Callicebinae species (reviewed by Fuzessy et al., 2018). Titi monkeys are small primates (1–2 kg, Bicca-Marques and Heymann, 2013), with a great potential for seed dispersal, as they are predominantly frugivorous (Caselli and Setz, 2011; Boyle et al., 2016; Nagy-Reis and Setz, 2017), a characteristic associated with increased probability of ingesting seeds and dispersing zoochorous species (Fuzessy et al., 2016, 2018). Different from other pitheciid species, titi monkeys present lesser degree of morphological adaptations to forage on mechanically resistant foods, such as seeds (Kinzey, 1992), and their frugivorous diet relies mainly on fruit pulp (Caselli and Setz, 2011; Nagy-Reis and Setz, 2017). Nonetheless, titi monkeys' position in the seed dispersal-predation gradient is still poorly investigated. Uncovering the role of titi monkeys as seed disperser is especially important in endangered biomes such as the Atlantic Forest, subjected to high fragmentation rate (Ribeiro et al., 2009). This landscape changing is leading to the disappearance of mammal frugivore species (Canale et al., 2012), but titi monkeys seem to persist (São Bernardo and Galetti, 2004; Gestich et al., 2019). In this context, we described titi monkeys' feeding behaviour on fruits, registering the zoochorous species ingested, their seed handling and seed size. Then, we characterized some aspects of both the quantitative and qualitative components of seed dispersal effectiveness of titi monkeys. To characterize one of the aspects of the quantitative component, we quantified the number of seeds in their feces as a proxy of the amount of seeds removed from parent plants. Regarding the qualitative component, we evaluated the distribution pattern of titi
2. Methods 2.1. Monitored groups and study sites We studied two habituated free-ranging groups of black-fronted titi monkey (Callicebus nigrifrons) at two protected areas of Atlantic Forest in São Paulo State, Southeast Brazil. One group (5–6 individuals) was monitored in a 350-km2 forest remnant (Serra do Japi: 23°14′S, 46°56′W) and the second (3–5 individuals) was monitored in a 2.45km2 forest remnant (Ribeirão Cachoeira: 22°49′S, 46°55′W). Both areas are characterized by semideciduous secondary Atlantic Forest and seasonal climate, with mean annual temperature about 19 °C (Japi group study site) and 22 °C (RC group study site), and total annual rainfall about 1400 mm (Cepagri, 2011, Ciiagro, 2011). Like other Neotropical rainforests, Atlantic Forest integrity depends on the presence of frugivores since most plant species have zoochorous dispersal syndromes (Almeida-Neto et al., 2008; Jordano, 2000). In our study areas, for instance, about 60–70% of wood plants species have zoochorous dispersal syndrome (Morellato and Leitão-Filho, 1992; Garcia et al., 2014). At both study sites, titi monkeys co-occur with other less frugivorous species, such as coati (Nasua nasua) and porcupine (Coendou prehensilis), and also with other less frugivorous primates, such as marmosets (Callithrix aurita) at Serra do Japi and howler monkeys (Alouatta guariba clamitans) and marmosets (Callithrix spp.) at Ribeirão Cachoeira. These species were observed feeding on fruits of some of the same plant species as titi monkeys. 2.2. Data collection 2.2.1. Feeding behavior and seed handling Data collection on Japi group was done over 11 months (N = 40 days, from August 2010 to June 2011) and on RC group over 12 months (N = 52 days, from June 2010 to May 2011), during three to five days per month. This study is part of a longer monitoring study of a total of 20 and 13 months, respectively (Caselli, 2013; Gestich, 2012; NagyReis, 2012). Both groups were monitored from dawn to dusk (i.e., complete days) or from the moment they were found until the moment they were lost (i.e., partial days with at least 6 h of monitoring). We recorded animals' behavior through scan sampling every 5 min (Altmann, 1974), and the central spatial position of the group every 10 min with a GPS receiver. Based on these scan samples we calculated the proportion of recordings invested in feeding activity. Additionally, at each feeding scan, we recorded the type of item and the plant species that animals consumed and estimate the contribution of each plant species (trees or vines) with zoochorous syndrome of dispersion to titi monkeys' pulp fruit diet. We calculated the relative importance of each zoochorous species in titi monkeys’ diet as a percent of feeding records from the scan sampling. We then determined the most consumed zoochorous plant species for pulp fruit as those species with a cumulative contribution of 75% in the feeding records, considering the entire period of the study. For those species only, we determined how titi monkeys handled their seeds (preyed, spat out, or swallowed) based on ad libitum records. Taxonomic specialists (see acknowledgements) identified the plant species, and when the identification was not possible, we used the morphospecies as a surrogate for taxonomic species. 2.2.2. Characterization of seeds We collected the feces immediately after defecation. We washed each sample in running water, using a 1-mm mesh sieve. We then separated and counted all seeds using a stereomicroscope and identified 2
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germination time (number of days until the emergence of the radicle) between control and treatment, testing each plant species individually. For that, we performed a time-to-event analysis with the Kaplan–Meier estimator to compare treatment groups for potential differences in temporal patterns of germination, which consider the joint influence of time and percentage of seed germination (MacNair et al., 2012). We adopted the non-parametrical approach with exact data (continuous observation), using Peto-Peto weight function, implemented by function “survdiff” in package “survival” (Therneau, 2015). We considered each seed of each specie and treatment as a replicate. We performed the analyses in R software version 3.5.2 (R Development Core Team, 2018).
seed species (or morphospecies). We determined the seed size by measuring the longest dimension of seeds from feces samples. We classified each seed species as small- (≤0.5 cm), medium- (> 0.5 and ≤2.0 cm), and large-seed (> 2 cm) (following Wrangham et al., 1994). In addition, we determined seed size from those zoochorous species not found in titi monkeys’ feces but present in the list of the most consumed species, either by directly measuring seeds from fresh fruits or obtaining this information from literature (Lorenzi and Matos, 2002). 2.2.3. Seed germination trials We performed germination trials for all seeds obtained from Japi group's feces. We separated the seeds from feces and incubated all them on wet filter paper in Petri-dishes. We placed the seeds at distances of 3–5 seeds from each other, limiting the number of seeds in each Petridish according to seed size. We kept the seeds under the natural regime of light in a natural illuminated laboratory at the study site and we wet the seeds whenever necessary to keep them constantly moist. We checked the seeds daily until the emergence of the radicle or obvious death of the seeds (following Lieberman and Lieberman, 1986). Then, we calculated the cumulative proportion of seeds per species that germinated, and the mean time elapsed until germination. We also compared the germination success of seeds present in the feces (i.e., treatment) with those from fresh fruits (i.e., control). Given the probability of being dispersed increases with dispersers’ feeding rate of fruits from a species (Schupp, 1993; Jordano and Schupp, 2000), we selected for controlled germination trials only the zoochorous species present among the most consumed species by Japi group (Table 1). For the control, we used seeds from mature intact fruits without a bitten sign and insect infestation collected under the plants in which we observed Japi group foraging. We collected seeds from different fruits and from different plant individuals of each tested species on which titi monkeys foraged. We removed the seeds from fruit pulp and washed them following the same procedure used to clean seeds from feces. Control and treatment were kept under the same conditions and comprised the same amount of seeds, except when the number of seeds from fresh fruits was limited (see Table 2). We compared germination frequency (number of seeds) and
2.2.4. Spatial distribution of feces We recorded the position of each defecation with a GPS receiver (Japi group N = 326; RC group N = 470). We estimated the feces spatial distribution pattern with a 100% Kernels using the “kernelUD” function from the “adehabitatHR” package (Calenge, 2017), assuming a bivariate normal distribution, with the smoothing parameter as a fixed radius of 25 m (same radius adopted in our previous study; Caselli et al., 2017). The UD (Utilization Distribution) map describes the intensity of defecation records by calculating the probability of new feces being deposited at each site according to the number of feces within the fixed radius value. We plotted the Kernel map of feces over the groups' home range, calculated with the minimum convex polygon (MCP; Hayne, 1949) using 100% of the recorded locations of groups during monitoring (adehabitatHR package, Calenge, 2017). To aid our interpretation of feces distribution pattern, we also georeferenced all sleeping sites where all group members spent the night together, since sleeping sites distribution is recognized as important influence on seed shadow for several primate species (Chapman and Russo, 2006; Russo et al., 2006). We plotted the sleeping site locations in the map using the “layer” function from the “latticeExtra” package (Sarkar and Andrews, 2016). In addition, we superimposed a virtual grid of 25 × 25 m over each group home range and counted the number of defecation records in each quadrant. Then, we used a Chi-square test to investigate whether the deposition of feces was higher near to sleeping sites than expected by chance. To do this, we compared the number of defecation records close to sleeping sites (in cells with sleeping sites plus cells with a shared side or corner with these cells) with the number of records not close to sleeping sites. To calculate the values expected by chance we considered the proportional contribution of these two types of cells (with sleeping sites or close to one and without sleeping sites) to groups’ total home range. Finally, to describe the distances traveled by titi monkey groups, we calculated the daily path length of the Japi group based on the 10 min samplings of group's spatial position, using “adehabitatLT” package (Calange, 2006). This data has already been obtained for the RC group (Nagy-Reis and Setz, 2017). All spatial analyses were performed in R software (R Development Core Team, 2018).
Table 1 Percentage contribution and seed size of the most consumed (sum > 75%) zoochorous plant species by Callicebus nigrifrons. Seed size: ≤0.5 cm is small, > 0.5 and ≤ 2.0 cm is medium, > 2.0 cm is large. The species indicated by an asterisk are those also found in the feces. Titi monkey groups
Plant species
Records of consumption (%)
Seed size
Japi
Miconia cinnamomifolia * Ocotea puberula * Maytenus robusta Non-identified vine I * Eugenia uvalha Myrcia rostrata Struthanthus complexus Non-identified tree * Ficus luschnathiana * Non-identified vine II
34.0
small
8.5 8.0 5.8 4.8 3.6 3.5 3.2 3.2 2.5 ∑ 77.1
medium medium medium medium medium small small small medium
17.4 17.3 9.3 9.1 8.2 5.3 4.8 4.0 ∑ 75.4
small medium medium small large medium medium medium
RC
Ixora gardneriana* Calycorectes acutatus Neomitranthes glomerata Pereskia aculeata* Syagrus romanzoffiana Diclidanthera sp.* Eugenia glazioviana Alchornea glandulosa
3. Results 3.1. Feeding behaviour and seed handling About half of the titi monkeys' feeding records came from events in which they fed on flesh pulp of fruits from zoochorous species (Japi group = 62% of feeding records, N = 3,648; RC group = 47%, N = 3,071). In lower proportion, seeds was the second (RC group = 22% seeds, 19% vegetative plant parts, 10% invertebrates, 2% other, see in Nagy-Reis and Setz, 2017) and the third (Japi group = 11.5% vegetative plant parts, 11.3% seeds, 10.5% invertebrates, 4.7% other) consumed food item. All seeds consumed by Japi group was from non-zoochorous species (411 feeding records from 12 species), and the most consumed species for seeds (Croton floribundus, an autochorous species) represented only 6.2% of total diet. Titi monkeys consumed fleshy pulp of fruits from 66 to 49 zoochorous 3
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Table 2 Temporal pattern of seed germination of five species consumed by Callicebus nigrifrons (Japi group). Total germination (percentage) and mean latency to germinate (in number of days) of ingested (feces) and fresh (control) seeds. Species
Chi-squared test with the Kaplan–Meier estimator
Treatment
Replicates (N)
Germination (%)
Latency (days ± SD)
Miconia cinnamomifolia*
X2 = 289
Feces Control
478 414
56 90
33 ± 13 21 ± 11
Ocotea puberula*
X2 = 16.1
Feces Control
21 20
29 95
41 ± 27 39 ± 27
Non-identified vine I
X2 = 0.6
Feces Control
25 25
84 96
14 ± 5 14 ± 7
Non-identified tree
X2 = 0.5
Feces Control
82 17
62 82
24 ± 56 69 ± 35
Ficus luschnathiana*
X2 = 110
Feces Control
361 201
83 97
35 ± 22 22 ± 9
*p < 0.001.
concentrated close to sleeping sites (Group 1: X2 = 104.38, df = 1, p < 0.001; Group 2: X2 = 11.35, df = 1, p < 0.001).
species, in which ten and eight species (Japi group and RC group, respectively) represent a cumulative contribution of 75% to their total feeding time (herein the most consumed species; Table 1). Considering the most consumed species, they swallowed the seeds (together with the pulp) of all species with small-sized seeds, except one (Struthanthus complexus). Although they typically spat out all medium and large seeds, we occasionally found intact medium-sized seeds of Ocotea puberula (Japi group), Diclidanthera sp. (RC group), and an unidentified vine (Japi group) in titi monkeys’ feces. None of these larger seeds were found destroyed in the feces.
4. Discussion Black-fronted titi monkeys invest a substantial proportion of feeding time on consuming pulp of fruits from zoochorous plant species and ingested the seeds of about half of them, depositing a large quantity of seeds in their feces, mostly small-sized seeds. Germination success was similar or inferior to that of seeds retrieved from fresh fruits, contrary to what we expected. However, although not in a uniform pattern, titi monkeys' feces were spread broadly across the groups’ home range. Therefore, given the high number of seeds deposited from diverse zoochorous species (a quantitative component of seed dispersal effectiveness) and the broad distribution pattern of feces (a qualitative component), we cannot discard the potential of titi monkeys to enhance plant reproductive fitness by spreading their seeds throughout their home range. Titi monkeys feed mainly on fruit pulp and occasionally on unripe seeds of non-zoochorous species (Caselli and Setz, 2011; Souza-Alves et al., 2011; Nagy-Reis and Setz, 2017, present study). Different from other seed predator Pitheciidae species, Callicebiin species have less specialized dentition to forage on mechanically resistant foods (Kinzey, 1992), reducing their potential as seed predators. By ingesting seeds while consuming fruit pulp of zoochorous species, titi monkeys may have an important role on forest regeneration, as already reported to other Atlantic Forest primate species (Bufalo et al., 2016). The amount of seeds defecated by titi monkey groups may reach a minimum of 300 seeds per day. Considering that our sampling did not include all feces deposited, this is an underestimation of feces deposition, and so seed deposition may reach even higher values per day. The quantitative potential of titi monkeys as seed disperser is skewed to plant species with small-sized seeds (< 0.5 cm) since they consistently swallowed a high amount of these seeds with fruit pulp and often discarded larger seeds. Plant species with the reproductive strategy of producing a large amount of fruits with small seeds attract a wide range of seed disperser species, including small mammals and birds (Jordano, 2000; Stoner et al., 2007). In this case, the complementarity of seed dispersers can increase plant fitness due to differences in their seed handling and deposition pattern. Small seeds generally are ingested with the fruit pulp and are less likely to be chewed or destroyed by chewing (Norconk et al., 1998; Fuzessy et al., 2018). In fact, we barely found destroyed (i.e., broken) seeds in titi monkeys' feces. In addition, although the ingested seeds are primarily from plant species with small seed size, some medium-sized seeds were also sporadically swallowed and deposited intact with titi monkeys’
3.2. Characteristics of deposited seeds We found an average of 45 ± SD 59 seeds (Japi group: range = 1–305 seeds, N = 40) and 24 ± SD 45 seeds (RC group: range = 1–263, N = 51) from feces collected per day. We found seeds in titi monkeys' feces from nearly a half of the zoochorous species that they consumed during the study period (Japi group: 42%, N = 66 plant species; RC group: 55%, N = 49 plant species). Seeds of most plant species found in titi monkeys' feces had small size (Japi group: 58%, N = 28; RC group: 68%, N = 27). In addition, more than 90% of the total seeds found in titi monkeys’ feces, irrespective of the species, were smaller than 0.5 cm (Japi group = 93%, N = 1,307 seeds; RC group = 94%, N = 339 seeds). Less than 1% of seeds found in their feces, all them from small size, was damaged or broken. 3.3. Seed germination trials More than half of the seeds (56%, N = 1,307 seeds) and seed species (54%, N = 28 species) found in Japi group's feces germinated. But germination success was not improved in any case of controlled experiments, contrary to the expected pattern. The temporal pattern of seed germination was the same between control and treatment for two of the five tested species and higher in the control for the other three (Table 2). 3.4. Feces spatial deposition Titi monkeys traveled about 1 km per day (Japi group:1.07 ± SD 0.15 km, N = 40 days; RC group: see Nagy-Reis and Setz, 2017). We registered 2–19 defecations per day (Japi group: 7.3 ± SD 3.4 feces, N = 40 days; RC group: 8.9 ± SD 4.5, N = 52 days). Defecation activity was not conspicuously synchronized among individuals throughout the day, except early in the morning when they leave the sleeping sites. Feces were distributed throughout the entire home ranges of the groups with a few denser nuclei of defecation (Fig. 1) 4
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and S. mystax, Muñoz Lazo et al., 2011) and other mammal (e.g., duikers, Feer, 1995) and bird species (e.g., cassowary, Mack, 1995). In addition, titi monkeys travel along ca. 1 km daily (present study and data available for RC group in Nagy-Reis and Setz, 2017) and rarely returned to the same place in the same day (pers. obs.). This information together with the long-estimated gut transit time, ranging from about three to over 4.5 h (Baião et al., 2015), suggest that seeds consumed in an individual tree are probably defecated far from it. Yet, considering that none of plant species used as sleeping site are feeding trees (Caselli et al., 2017), the observed distribution pattern of feces has the potential to enhance plant reproductive fitness by increasing the probability of seeds being deposited far from parent plants, in novel and favorable sites. The seed ingestion and deposition patterns by titi monkeys suggest that this small Neotropical primate mainly favors the reproductive fitness of small-seeded plant species. Even though their disperser role may be less efficient for some species, titi monkeys' overall contribution to forest regeneration may be essential in the current degraded scenario of Atlantic Forest. Further studies, encompassing the whole seed dispersal effectiveness framework will be essential to fully comprehend titi monkeys' contribution to plant fitness. The occasional dispersal of medium-sized seeds also may have special importance to plant fitness where larger frugivores are extinct or scarce. Since frugivores affect differently seed fate due to their specific fruit handling and seed processing (Lugon et al., 2017), a high diversity of potential dispersers may guarantee the complementarity of seed dispersal function (Bueno et al., 2013; Chapman et al., 2013). The complementary role of seed dispersers, including titi monkeys, is especially important to the Brazilian Forest Atlantic biome, which currently have only about 12% of its original covers (Ribeiro et al., 2009), and is increasingly defaunated and losing ecological services, such as seed dispersal (Jorge et al., 2013; Dirzo et al., 2014). Considering titi monkeys’ high persistence in small fragments (São Bernardo and Galetti, 2004; Bufalo et al., 2016; Gestich et al., 2019), this Neotropical primate may be a key species for forest regeneration, sowing the forest from dropping to dropping.
Fig. 1. Titi monkeys' feces distribution within Japi (a) and RC (b) groups' home range (black polygon MCP considering 100% of registers: Japi group = 32 ha, RC group = 18 ha) according to kernel utilization distribution (UD) estimates. The colour intensity represents an index that indicates probability of new feces being deposited at each site, Δ indicates sleeping sites.
Author contributions
feces. This eventual swallowing may exert a relevant contribution to the parent plant reproductive success when their fruits are consumed in a great proportion by a frugivorous species (Lambert and Garber, 1998; Jordano and Schupp, 2000; Chapman and Russo, 2006). Titi monkeys do not seem to improve seed germination, either proportion or latency time of germination. In fact, they reduced germination success of three from five tested species. However, given that at least half of all swallowed seeds (54%) survived and germinated after gut passage, and that these seeds are spread over a larger area being most probably deposited away from a parent tree, we cannot discard the potential benefit of titi monkeys to overall plant fitness. Even for those species in which titi monkeys reduced their germination success, seed deposition far from parent plant can also contribute to the overall recruitment success (i.e., seed to adult survival), likely greater than if they were deposited under the parent plants. Although titi monkeys’ feces were also deposited in some denser nuclear areas (Fig. 1), which could represent an increased competition among seedlings (Harms et al., 2000; Wehncke et al., 2004), they defecated across their entire home range, not only in restricted clumps, enhancing the probability of seeds being deposited in favorable microsites (Rogers et al., 1998; Howe and Miriti, 2004). The clumped pattern of feces deposition by primates is commonly related to the concentration of feces near sleeping sites (Chapman and Russo, 2006, Link and Di Fiori, 2006; Russo et al., 2006). In the case of titi monkeys, the early morning defecation bouts explain the increased density of feces near some sleeping sites (Fig. 1). The same aggregated pattern is also observed for other repeatedly used sites, such resting sites of tamarins (Saguinus fuscicolis
All authors conceived the ideas of the study, collected the data in the field and contributed to the writing of the manuscript. C.C.G. conducted the analyses and led the writing of the manuscript. All authors gave their final approval for submission.
Declarations of interest None.
Acknowledgements We are grateful to the Jundiaí City Hall and Colinas do Atibaia gated community for permission to conduct this research at Serra do Japi Municipal Reserve and Ribeirão Cachoeira, respectively. We thank J.Y. Tamashiro (Botanical Department, UNICAMP), L. Garcia, J. A. Gomes and G. Shimizu for plant species identification. We also thank Cássia A. Gestich for helping in the germination monitoring. The species assessed in this study was registered according to new Brazilian legislation on access to the biodiversity (Law 13,123/15 and Decree 8772/16) under the SisGen License AEB363E. This work was supported by FAPESP, Brazil (CBC: Process #2008/05127-0; CCG: process #2010/04034-9; MBNR: Process #2009/12124-0) and received equipment from Idea Wild, USA. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brasil (CAPES) -Finance Code 001. 5
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