Ants in their plants: Pseudomyrmex ants reduce
primate, parrot and squirrel predation on Macrolobium
acaciifolium (Fabaceae) seeds in Amazonian Brazil
ADRIAN A. BARNETT
1,2*, THAIS ALMEIDA
3, RICHELLY ANDRADE
4, SARAH BOYLE
5,
MARCELO GONÇALVES DE LIMA
6, ANN MACLARNON
1, CAROLINE ROSS
1,
WELMA SOUSA SILVA
7, WILSON R. SPIRONELLO
2and BEATRIZ RONCHI-TELES
21Centre for Research in Evolutionary and Environmental Anthropology, University of Roehampton,
London SW15 4JD, UK
2Coordenação de Biodiversidade, Instituto Nacional de Pesquisas da Amazônia, Manaus, AM
69067-375, Brazil
3Lab. de Herpetologia, Univ. Federal do Mato Grosso, Boa Esperança, MT 68060-900, Brazil
4Dept. de Química, Univ. Federal do Amazonas, Manaus, AM 69077-000, Brazil
5Dept. of Biology, Rhodes College, Memphis, TN 38112-1690, USA
6Protected Areas Programme, United Nations Environment Program, World Conservation Monitoring
Centre, 219c Huntingdon Rd., Cambridge CB3 0DL, UK
7Instituto de Ciências Exatas e Tecnologia, Univ. Federal do Amazonas, Itacoatiara, AM 69100-000,
Brazil
Received 12 July 2014; revised 30 September 2014; accepted for publication 30 September 2014
Although plant-inhabiting ants are known to act as effective deterrents to a variety of vertebrate and invertebrate herbivores, this has been reported only once before for primates, a group better known for their predation of ants. In the present study, we investigated the effects that colonies of Pseudomyrmex viduus ants living in individual Macrolobium acaciifolium (Fabaceae) trees have on the rates of visitation and fruit removal by four taxa of seed-predating vertebrates: the primate Cacajao melanocephalus ouakary; macaws (Ara spp.); large parrots (Amazona spp.); and the Northern Amazonian red squirrel (Sciurus igniventris). We found that ant presence significantly reduced both rates of visitation and of fruit removal by C. m. ouakary. The same pattern of reduced fruit removal was also observed for other seed predators (parrots, macaws, and squirrels) but not for visitation rates (although this may be a result of the small sample size). This appears to be only the second-known demonstration
of the repellent effect of ants on primates and, indeed, the first for squirrels and psittacine birds. © 2014 The
Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114, 260–273.
ADDITIONAL KEYWORDS: Amazona – Ara – Cacajao – Formicidae – plant defence – Sciurus.
INTRODUCTION
Documentation of defensive associations between ants and plants is extensive (Janzen, 1966, 1969; Fiala et al., 1989; DeVries, 1991; Huxley & Cutler,
1991). These associations occur in a variety of forms (Lev-Yadun & Inbar, 2002; Heil & McKey, 2003; Vázquez, Chacoff & Cagnolo, 2009) and may vary in interaction intensity depending on environmental conditions (Davidson & Fisher, 1991; Fiala, 1994; Palmer et al., 2010; Yu, 2001), although they are often mutualistic, with ants gaining either suste-nance, shelter or both, and the plants gaining protec-tion from herbivores predaprotec-tion on leaves and/or stems (Bronstein, 1998). Such associations have been reported to effectively deter a variety of both *Corresponding author.
E-mail: [email protected]
This paper is a tribute to the memory of Donald Petrie (1958–2013), a dedicated birder.
Biological Journal of the Linnean Society, 2015, 114, 260–273. With 3 figures
vertebrate and invertebrate herbivores (Beattie, 1985; Fiala, 1994; Dejean, Djiéto-Lordon & Orivel, 2008). However, studies have concentrated on defence of leaves and shoots, and mutualistic ant defence against potential seed predators has rarely been con-sidered (Inouye & Taylor, 1979; Schemske, 1980; Horovitz & Schemske, 1984).
In the present study, we report on the association between Pseudomyrmex viduus ants and the Neo-tropical leguminous tree Macrolobium acaciifolium (Fabaceae: Faboideae), as well as the impact of ant presence on predation of M. acaciifolium seed by
a primate (the golden-backed uacari, Cacajao
melanocephalus ouakary, Pitheciidae), a squirrel (Sciurus igniventris, Sciuridae), and six species from the parrot family (Psittacidae: three large parrots, Amazona spp., and three macaws, Ara spp.). To our knowledge, effective defence of plants by ants against primates has previously been reported only once in the literature (McKey, 1974). Other reports of primate/ant interactions concern active predation of ants by pri-mates (Cebus capuchinus: Freese, 1976; Erythrocebus patas: Isbell & Young, 2007; Pan troglodytes: Schöning et al., 2007; Lophocebus albigena: Struhsaker, 1979) or of primates eating insects disturbed by army ants (Saguinus: Rylands, de Cruz & Ferrari, 1989) or anting (Longino, 1984). Similarly, other than a report of how forest-floor ants may secondarily disperse fruit that had fallen to the ground as a result of parrot foraging activity (Galetti, 1993), we know of no papers that refer specifically to interactions between ants and psittacines. Anting behaviour appears to be the only reported ant–squirrel interaction (Hauser, 1964).
A variety of fruit characteristics are known to influ-ence diet composition of seed-predating vertebrates (including hardness: Kinzey & Norconk, 1990; size: Muñoz & Bonal, 2008; spatial distribution: Notman, Gorchov & Cornejo, 1996; toxins: Cipollini & Levey, 1997; weight: Jensen, 1985; Madej & Clay, 1991; topic review: Bodmer, 1991). The observations reported in the present study expand the repertoire of potential influences because the additional factor of defensive ant presence may explain the absence or low repre-sentation of the seeds of some plant species in the diet of seed-predating vertebrates.
SPECIES STUDIED
The tree: Macrolobium acaciifolium (Benth.) Benth (Fabaceae: Faboideae) is a widespread tree in northern South America. Reaching up to 40 m in height, M. acaciifolium occurs in a variety of habitats includ-ing seasonally flooded riparian forests (várzea and igapó, sensu Prance, 1979) and never-flooded (terra firme) forest (Cowan, 1953). For plants in flooded forests, such as those in the present study, new shoots
and foliage are produced in a concentrated pulse as annual floodwaters rise (Ferreira & Parolin, 2007). Flowers are produced at this time, and occur as small inflorescences in the axil of each leaf on the new shoot. The white, bee-pollinated, flowers in each inflorescence open near-simultaneously, as do the inflorescences on each shoot (Rech & Absy, 2011) (Fig. 1). Consequently, as they mature, the fruits are very similar in size and age. Fruits, which are single seeded indehiscent woody pods, are hydrochorous (water-dispersed) and can ger-minate after floating for up to 36 days (Kubitzki & Ziburski, 1994). Some fish dispersal (ichthiochory) also occurs (Correa et al., 2007).
The ant: Pseudomyrmex viduus (Smith 1858) is the ant species associated with M. acaciifolium (Ward, 1991, 1999). It lives in the central hollows of older stems of the tree. On M. acaciifolium, P. viduus workers patrol leaves and stems, and summon others to any area to which a threat is perceived, presum-ably, as in other members of the genus (Morgan, 2008), by a combination of pheromonal and vibra-tional communication. Such ants are known in
Brazilian Amazonia as taxi (pron. ‘tah-shee’).
Pseudomyrmex are highly aggressive, and vigorously defend their host plant from perceived intruders (Janzen, 1966; Hölldobler & Wilson, 1990). So
effec-tive are taxi ants at repelling intruders that
two species of hummingbirds (Anthracothorax pre-vostii: Calderón-F., 2005; Anthracothorax nigricollis: Greeney & Merino-M., 2006) preferentially nest in
Figure 1. Macrolobium acaciifolium in flower. Because
inflorescences open near-simultaneously, and flowering time is short, fruit development is near-synchronous and size variation is small.
Macrolobium trees containing their colonies: although it is not known why the hummingbirds themselves are tolerated by the ants.
Pseudomyrmex ants are commonly associated with species of Fabaceae (Ward, 1999), where they raise pseudococcids and coccids (Hemioptera: Coccoidea) in hollow stems. As is common in such relations, sugary secretions from the hemiopterans form much of the colony energy budget (Fonseca, 1993; Gaume, McKey & Terrin, 1998; Pringle, Dirzo & Gordon, 2011). Although often defending the host tree against folivores and perceived dangers, ant colonies (or more correctly their hemiopteran commensals) may act as a substantial energetic sink for the trees that possess them (Letourneau & Choe, 1987; Stadler & Dixon, 1998) and many studies have shown this can lower seed crop weight per unit of canopy (Addicott, 1985; Beattie, 1985; Keeler, 1985; Bronstein, 1988; for a review of the topic, see Herms & Mattson, 1992). If fruit- or seed-size is negatively affected, this may produce a potentially confounding variable in the Macrolobium-Pseudomyrmex-seed predator system being investigated in the present study because seeds in fruits on plants with ants may be smaller (and therefore less attractive to seed predators).
The primate: The golden-backed uacari, Cacajao melanocephalus ouakary, is a medium-sized Neotropical primate (Hershkovitz, 1987). Unripe seeds from hard-husked fruits dominate its diet and it primarily inhabits flooded forest on the margins of blackwater rivers (Barnett et al., 2013). In common with other members of their clade (Pithecia and Chiropotes), primates of the genus Cacajao have a suite of morphological adaptations to hard-husked seed predation, including robust splayed canines (used as awls to open fruits, especially along their sutures) and hypertrophied, spatulate, incisors to gouge out seeds once the hardened husk is opened (Kay, Meldrum & Takai, 2013). Uacari damage pat-terns are very characteristic (Fig. 2A). Unripe seeds of M. acaciifolium are an important component of the C. m. ouakary diet, ranked 17th out of 148 species by number of annual diet records (Barnett, 2010), rising to fourth position when recalibrated for just those specific months when the species was in fruit.
The squirrel: The Northern Amazon red squirrel (S. igniventris) is considered a specialist on seeds of large hard fruit (Emmons, 1984), although its diet does not appear to have been recorded systematically. Tooth marks on fruits (Fig. 2B) allowed us to distinguish squirrel predation on Macrolobium seeds from that of parrots, macaws, and uacaris. Other arboreal rodent genera in Jaú, the central Amazonian site studied
here, include Coendou, Echimys, Makalata, and Rhipidomys. The bite marks of each of these species can be separated from those of S. igniventris by their width, curve and thickness (A. A. Barnett, unpubl. data).
The parrots: There are 23 psittacine species known from Jaú National Park (Borges et al., 2001). Of these, six are large and sufficiently powerful to effectively process M. acaciifolium fruit (the parrots Amazona amazonica, Amazona farinosa, and Amazona festiva; the macaws Ara ararauna, Ara chloroptera, and Ara macao). The physical pattern of psittacine seed predation on a fruit is highly dis-tinctive (Fig. 2C), with the distal portion of the gnathothecal tomia being used to gouge open the fruit and access the seed (Fig. 2D).
A system in which some individuals of a plant species have aggressive host-defending mutualistic ants and others do not is clearly heterogeneous from the perspective of a herbivore or seed-predator. Within a local population individual plants may vary not only in the level of defence, but also in the size and nutrient-content of seeds and leaves. These may be bigger or smaller in plants with ants, depending
on the energy-balance between plant and ant
mutualists (Frederickson & Gordon, 2009). Such between-individual variation has also been recorded
for mutualisms insects and carnivorous plants
(Scharmann et al., 2013). As a result, in a system with defensive ant mutualists, the simple predictions of optimal foraging (i.e. that seed predators will always choose larger fruit: Leighton, 1993; Russo, 2003) may be confounded by defensive effects because it is pos-sible to imagine a ranked preference (depending on the pain of interacting with the ants and the size difference between the fruits) of:
1. Fewer ants/larger fruits> more ants/larger fruits > fewer ants/smaller fruits> more ants/smaller fruits
Or:
2. Fewer ants/larger fruits> fewer ants/smaller fruits > more ants/larger fruits> more ants/smaller fruits.
HYPOTHESES TESTED AND THEIR PREDICTIONS We tested the following two null hypotheses:
1. In the flooded forest of central Amazonia, the presence of P. viduus ant colonies in M. acaciifolium trees does not deter seed predators
2. In the M. acaciifolium–P. viduus system in the flooded forest of central Amazonia, the presence of ant colonies does not produce a detectable impact on growth in stems, leaves or fruit.
Predictions:
(a) From hypothesis (1), we predict that none of the three types of vertebrate seed predators studied will show dif-ferences in rates of feeding visits or seed predation between M. acaciifolium trees that have or did not have P. viduus ant colonies.
(b) From hypothesis (2), we predict that there will be no difference in canopy surface area, seed weight m−2
(referred to as ‘seed crop weight’), fruit size or percentage of fruit weight contributed by the seed between M. acaciifolium trees that have P. viduus ant colonies and trees that do not have these ant colonies.
MATERIAL AND METHODS SITE
We conducted the investigation in Jaú National Park, a protected area in Amazonas State, Brazil (Barnett,
2010). Jaú is located on the southern bank of the Rio Negro, some 220 km upstream from the state capital Manaus. The vegetation is approximately 80% never-flooded lowland tropical forest (terra firme), 12% seasonally-inundated river-margin forest (igapó), 4% white sand vegetation (campina), and 3% palm and aroid swamps (buritizal and aningal, respectively; Borges et al., 2004). The remaining 1% is made up of land being actively used for subsistence farming and minor vegetation types, such as beach scrub and mist forest. The study site was located between the first major set of rapids on the Jaú River (Cachoeira do
Jaú: 01°53.21″S, 61°40.43″W) and the community of
Patauá (01°53.16″S, 61°44.31″W).
STUDY HABITAT
Igapó is a seasonally flooded forest habitat that occurs in narrow ribbons along the margins of
sediment-Figure 2. The fruit of Macrolobium acaciifolium, a single-seeded pod, showing damage patterns characteristic of a variety
of predators and indicating how such predators can be distinguished. Damage is evident by primate Cacajao melanocephalus
ouakary (A), rodent Sciurus igniventris (B), and parrot Amazona amazonica (C). Example of parrot A. amazonica using the
distal portion of the gnathothecal tomia as a gouge open a M. acaciifolium fruit and access the seed (D).
poor, black- and clear-water rivers in Amazonia (Junk et al., 2011). Inundation may last for up to 9 months and water levels may exceed 12 m (Ferreira & Stohlgren, 1999). Plants of some species may be totally submerged for up to 6 months (Parolin, 2009). The majority of plant species in igapó are either water-dispersed or fish-dispersed (Correa et al., 2007), and fruit production coincides with the peak of inun-dation (Ferreira & Parolin, 2007). Igapó community composition is structured by inundation duration and tolerance, with zones of distinct botanical composition occurring in bands parallel to, and progressively further away from, the river bank (Ferreira, 1997; Ferreira & Stohlgren, 1999).
FIELD DATA COLLECTION
During 2007, we made observations on Macrolobium– ant–seed predator interactions. These occurred in igapó for 15 days each month, during the part of the year (June to September) when igapó was flooded and M. acaciiflolium trees were producing their floating fruits. The project was part of a broader study of the diet and ecology of the golden-backed uacari (Barnett, 2010).
We paddled wooden canoes along two flooded transects of igapó, each approximately 2 km long and 200 m wide (total, approximately 80 ha), and also criss-crossed within a 78-ha flooded mid-river island of pure igapó. During these times, we recorded all visual observations of feeding by uacaris, parrots, macaws, and squirrels, including those on Macrolobium trees. The duration of all feeding events was recorded, although only the duration of those
where animals were encountered just entering
M. acaciifolium canopies was used in this analysis. If multiple individual of a seed predator species were in the same canopy at the same time, their individual occupancy times were recorded and then summed.
We marked all trees in which feeding occurred, including repeat visits by the same species and those used by multiple seed predator species. A ‘feeding visit’ was operationally defined as ‘animals paused in a M. acaciifolium tree and were observed processing or ingesting M. acaciifolium fruit or involved in activities that led to ingesting such fruit’. Roosting, resting, brief pauses, and the use of M. acaciifolium trees as means of passage from the canopy of one tree to another were thus excluded. We also surveyed all M. acaciifolium trees within the three areas surveyed by canoe (the two transects and the igapó island), including both those trees that predators had been seen to visit and those they had not visited. We assayed for ant occupancy by lightly shaking and tapping with a stick the canopy of each plant (the canopy rarely being more than 1 m above the water level of the flooded forest).
Daily, during the 15 observation days per month, we also hand-netted and removed all M. acaciifolium fruits found floating under individual M. acaciifolium trees, recording any damage patterns on them,
including the characteristic marks from uacari
canines and incisors, rodent bite marks and psittacine gouges (Fig. 2).
Macrolobium acaciifolium do not grow in clumps, and flow rates of surface water are very slow within
the forest (less than 0.2 m h−1; A. A. Barnett, unpubl.
data). Flow rates increase briefly with heavy precipi-tation, and so seeds were not collected on the day after a large storm. These facts and precautions, plus a daily seed collection-and-removal regimen, meant that the intrusion of seeds from elsewhere was minimal, and so we are confident that most (if not all) seeds analyzed and counted came from the tree under which they were collected. Because seeds were float-ing, post-fall seed removal by forest floor rodents (Terborgh et al., 1993) was precluded, although loss to frugivorous-granivorous fish (such as Collosoma spp., Characidae: Correa et al., 2007) could not be discounted.
We measured the weight of fruit per m2of canopy of
each sampled M. acaciifolium tree, noting whether it had P. viduus ants. To estimate seed crop weight, we counted the number of fruits in the canopy and weighed 15 randomly selected fruits (and their seeds) from each study tree.
When calculating crop size per unit area we used
the number of seeds m−2 (and not m−3), because
M. acaciifolium infrutescences occur exclusively on the outer surface of the canopy. Canopy surface area was calculated by assuming each canopy to be a half-sphere (the shape most closely approximating that of a M. acaciifolium canopy), measuring the width and greatest height, and applying the formula
2πr2 (with half the width of the canopy being used
to give r, the radius). We weighed and measured
fruits at the late immature stage (≥ 4 cm long,
peri-carp brown, and sclerotized, pedicular attachment
extant) before excision and dispersal because
this was the stage when the study animals fed on them.
We measured all collected fruits along their great-est length with SPI 2000 callipers (Fig. 3). To avoid double counting fruits retrieved from beneath trees and showing evidence of predation, we only meas-ured fruits when both valves of the pod were retrieved. Because of small sample sizes from other species (Table 1), comparison of lengths of eaten-and on-tree pods involved only fruits eaten by C. m. ouakary.
We collected ants from each tree, storing them separately. Under the supervision of Beatriz Ronches-Teles, Itanna Oliveira Fernandes (Department of
Entomology, Instituto Nacional de Pesquisas da Amazônia) identified the ant specimens.
STATISTICAL ANALYSIS
To investigate Prediction 1 (i.e. that ant presence has no effect on seed predation), we tested for differences in number of visits to trees with ants versus visits to trees without ants using a chi-squared test for data on Amazona spp. and Ara spp. (data combined), C. m. ouakary, and the combined totals from both taxa (there were not enough visits by S. igniventris to conduct this test). We also tested for differences in the number of fruits freshly eaten and encountered beneath trees with ants versus trees without ants using a chi-squared test for data on Amazona spp. and Ara spp. (data combined), C. m. ouakary, S. igniventris, and the combined totals from all taxa. To investigate Prediction 2 (i.e. that ant presence has no effect on canopy surface area, seed crop weight, fruit size, or percentage of fruit weight con-tributed by the seed), and so to test for the potentially confounding variable of negative impacts of ant pres-ence on tree or fruit size or seed weight, we tested for
relationships between canopy surface area (m2) and
number of fruits, fruit weight (g), and seed weight (g) for trees with ants and trees without ants using Spearman’s rank correlation and linear regression analysis. We compared mean seed crop weight, mean number of fruit per tree, mean fruit length, mean fruit weight, and mean seed weight per fruit for M. acaciifolium plants with and without ants using
Mann–Whitney U-tests. P< 0.05 was considered
sta-tistically significant for all tests.
Figure 3. Fruit of Macrolobium acaciifolium showing
how maximum longitudinal length was measured.
T able 1. Comparisons of seed predator visits to Macrolobium trees with versus without ants, and consumption of fresh fruits T axon Feeding visits to trees Fruits freshly eaten by taxon and encountered beneath trees T otal visits Observed (and expected): with ants Observed (and expected): without ants χ 2 test results (d.f. = 1) T otal fruits Observed (and expected): with ants Observed (and expected): without ants χ 2 test results (d.f. = 1) Pitheciine (Cacajao ) 36 2 (22.4) 34 (13.6) 49.18, P < 0.0001 168 4 (104.7) 164 (63.3) 257.05, P < 0.0001 Psittacine (Amazona and Ara combined) 13 6 (8.1) 7 (4.9) 1.60, P = 0.21 69 25 (42.9) 44 (26.1) 19.75, P < 0.0001 Sciuridae (Sciurus ) 0 0 0 – 1 1 2 (6.9) 9 (4.1) 9.34, P = 0.002 T otals 49 8 (30.5) 41 (18.5) 43.97, P < 0.0001 248 31 (146.4) 217 (88.6) 280.37, P < 0.0001
RESULTS
Data were obtained from 42 trees of M. acaciifolium, of which 16 lacked ants and 26 had ants present. Overall, we observed 513% more feeding visits by seed-predating vertebrates to ant-less M. acaciifolium trees than to those where ants were present (N = 41 versus 8), and found 506% more fruits predated under ant-less M. acaciifolium trees than under those possessing ants (N = 217 versus 31) (Table 1).
This occurred even though only 16/42 (38%)
M. acaciifolium trees in the study area lacked ants. This is statistically significant (Table 1). Individuals of C. m. ouakary were also seen to visit ant-less trees significantly more often than those with ants (34 versus 2), and significantly more seeds eaten by these primates were found beneath ant-less trees (164 versus 4).
For psittacines, a similar pattern to that observed for C. m. ouakary was found for seed predation data (44 versus 25). The number of feeding visits did not differ (6 versus 7), although the sample size is very small.
For rodents, no fruits were found bearing teeth
marks of Coendou, Echimys, Malakomys, and
Rhipidomys. Although no S. igniventris visits were actually observed, 11 fruits bearing Sciurus sp. teeth marks were found under the study trees.
Overall, when all 42 trees were considered, there was a positive correlation between tree canopy surface area and crop size, as measured by number of
fruits (ρ = 0.70, N = 43, P = 0.001), although there
was no relationship between canopy surface area and
the tree’s mean fruit weight (ρ = −0.25, N = 43,
P = 0.1) or the tree’s mean seed weight (ρ = −0.23, N = 43, P = 0.14). When trees were examined sepa-rately based on whether or not ants were present, trees with ants had a positive correlation between
canopy surface area and crop size (ρ = 0.92, N = 27,
P< 0.001), although there was no correlation with
either fruit weight (ρ = 0.07, N = 27, P = 0.72) or seed
weight (ρ = 0.05, N = 27, P = 0.79).
Trees without ants, however, had a positive corre-lation between canopy surface area and crop size
(ρ = 0.80, N = 16, P < 0.001) but a negative
correla-tion between surface canopy area and fruit weight
(ρ = −0.74, N = 16, P = 0.001) and seed weight
(ρ = −0.75, N = 16, P = 0.001). These results
invali-dates null hypothesis 2 and reject the prediction: neither the presence, nor absence of ants appear to promote growth of trees or their fruits. Where greater removal of fruits occurs, it is because of the absence of ants, with trees otherwise being identical with respect to fruit density and fruit size and weight.
We found no difference between the canopy
surface area of trees with and without ants (Table 2).
However, there was a significant difference between the numbers and weights of fruits observed on trees with and without ants (Table 2), with trees without ants having a mean seed crop 63% smaller than those
recorded on those with ants (1.5 m−2versus 4.05 m−2).
Fruits on trees with ants were 13.6% heavier (mean ± SD of 11.0 ± 2.4 g versus 9.5 ± 2.9 g on trees without ants) and had seeds that were 21.3% heavier (6.1 versus 4.8 g) (Table 2). These differences were statistically significant (Table 2), again allowing null Hypothesis 2 to be rejected.
For fruits found floating under trees without ants, mean length of eaten fruits was 17.5% larger than those of the same developmental stage remaining on the trees with ants (8 versus 6.6 cm) (Table 2), which is a statistically significant difference (Table 2). Com-bined, the mean lengths of fruits removed from trees with no ants were 2.3% smaller than those collected from trees with ants, which is a nonsignificant difference (Table 2). Thus, Hypothesis 2 is partially rejected.
The duration of single feeding bouts was generally short (Tables 3, 4), with a mean ± SD of 46.9 ± 27.04 s (N = 34) and 13 ± 1.4 s (N = 2), for C. m. ouakary vis-iting, respectively, trees with and without ants, with 104 ± 88.4 s (N = 3) and 84 ± 38.6 s (N = 3) for Ara spp. and 83.3 ± 45.1 s (N = 3) and 47.3 ± 48.3 s (N = 3)
for Amazona spp. Statistical tests (χ2) aiming to
deter-mine whether significant differences in visitation times existed between trees with and without ants could not be conducted because of the small sample size from trees with ants (C. m. ouakary) and in general for the psittascines.
DISCUSSION
The data obtained in the present study show that M. acaciifolium trees with ants are visited less often by vertebrate seed predators than trees lacking ants. Such animals also eat fewer seeds from trees with ants. This apparent preference cannot be a result of differences in the size of trees with or without ants because the two samples do not differ statistically for canopy surface area. Neither is it a result of the size of the individual fruits because the mean values do not differ significantly between tree classes. However, trees with ants had both larger seed crop weights and larger heavier fruits, whereas trees without ants had larger fruits floating below them than were on the trees (Table 2). Thus, the potentially confounding variables relating to smaller size of fruit in trees with ant colonies appears not to be in operation, and we therefore attribute the differences solely to the pres-ence of P. viduus ants. Differpres-ences in size and weight of seeds remaining on trees appear to a result of the seed predators themselves, which (in Cacajao m.
T able 2. T ree, fruit, and seed comparisons between trees with ants and trees without ants V ariable Mean ± SD (range; N ) Statistical result Interpretation Canopy size (m 2) W ith ants 136.9 ± 38.6 (55–240; 27) P = 0.87, Z = 0.163, U = 231.0 Not significantly dif ferent: trees with ants and without ants had the same range of canopy sizes W ithout ants 132.1 ± 45.9 (58–213; 16) Number of fruits per tree W ith ants 571.6 ± 227.8 (1 10–1008; 27) P < 0.001, Z = 2.284, U = 655.0 Significantly dif ferent: trees with ants had more fruit per tree than trees without ants W ithout ants 205.4 ± 136.2 (24–535; 16) Number of fruits per m 2(canopy) W ith ants 4.0 ± 1.0 (1.4–5.7; 27) P < 0.001, Z = 4.940, U = 62040.5 Significantly dif ferent: trees with ants had more fruits on them than those without ants W ithout ants 1.4 ± 0.6 (0.2–2.5; 16) Length (cm) of fruits (1) On trees, with ants 7.5 ± 1.2 (4.6–10.3; 82) (1) versus (4): P = 0.06, Z = 1.533, U = 4326.0 (2) versus (4): P < 0.001, Z = 6.520, U = 3932.5 (1) versus (2): P < 0.001, Z = 6.520, U = 3932.5 (1) versus (2) + (4): P = 0.15, Z = 1.010, U = 6381.5 (1) versus (4): not significantly dif ferent: where foraging was painful to do, uacaris just quickly grabbed what they could before leaving. They were not selective (2) versus (4): significantly dif ferent: uacari monkeys were taking a very specific part of the fruit crop (just the larger fruits) (1) versus (2): significantly dif ferent: the trees with ants (less visited by monkeys) still had a lot of large fruits. The larger fruits had already been removed from trees with no ants (1) versus (2) + (4): not significantly dif ferent: trees with and without ants each started of f with a fruit crop that has the same amount of variation in fruit length (2) On trees, without ants 6.6 ± 1.1 (4.4–9.6; 51) (3) Under trees with Cacajao tooth marks, with ants 8.4 ± 1.6 (6.4–10.0; 4) (4) Under trees with Cacajao tooth marks, without ants 7.8 ± 0.8 (5.4–8.9; 93)
ouakary at least) selectively consume larger fruits. If the data for psittacine and rodents are excluded because of a small sample size, the primate results are still sufficiently robust to reject null Hypothesis 1 and invalidate the prediction that significant differ-ences exist in visitation rates and seed predation rates between M. acaciifolium trees that have and do not have P. viduus ants.
Our analysis of seed predation patterns within the guild of vertebrate predators of hard seeds at Jaú showed that M. acaciifolium seeds were eaten by large parrots (A. amazonica, A. farinosa, and A. festiva), macaws (Ar. ararauna, Ar. chloroptera, and Ar. macao), a squirrel (S. igniventris), and C. m. ouakary (Barnett et al., 2005; Barnett, 2010). Although samples for the nonprimate predators are
Table 3. Frequency and duration (in seconds) of visits to seven Macrolobium acaciifolium trees with ants by Cacajao,
Amazona, and Ara*
Macrolobium acaciifolium tree sample number†
3 9 11 13 15 20 21 Cacajao‡ Number of visits 1 1 Duration (s)§ 14 12 Amazona Number of visits 1 1 1 Duration (s)§ 23 103 17 Ara Number of visits 1 1 1 Duration (s)§ 121 87 44 Totals (N = 8) 1 1 2 1 1 1 1
*There were no direct observations made of Sciurus feeding on trees without ants. †There were no recorded visits by seed predators to trees # 1, 4, 8, and 12.
‡All observations of Cacajao melanocephalus ouakary were of single animals. One animal per tree is the most frequent foraging pattern in Cacajao (for Cacajao calvus calvus, see Ayres, 1986; for C. m. ouakary, see Barnett, 2010). §There were no records of primates and psittacines feeding simultaneously in a tree.
Table 4. Frequency and duration of visits to Macrolobium acaciifolium trees without ants by Cacajao, Amazona, and
Ara*
Macrolobium acaciifolium tree sample number†
2 3 5 6 7 9 10 11 13 14 15 16 17 Cacajao‡ Number of visits 2 3 6 1 1 4 2 1 2 5 3 4 Duration (s)§ 21, 70 09, 38, 67 18, 43, 44, 57, 67, 81 27 40 34, 36, 78, 99 15, 31 17 19, 28 11, 28, 35, 67, 89 34, 56, 94 24, 44, 74, 104 Amazona Number of visits 1 1 1 Duration (s)§ 83 201 28 Ara Number of visits 1 2 1 Duration (s)§ 45 72 133 Totals (N = 41) 2 3 7 2 1 4 2 1 4 6 4 1 4
*There were no direct observations made of Sciurus feeding on trees without ants. †There were no recorded visits by seed predators to trees # 1, 4, 8, and 12.
‡All observations of Cacajao melanocephalus ouakary were of single animals. One animal per tree is the most frequent foraging pattern in Cacajao (for Cacajao calvus calvus, see Ayres, 1986; for C. m. ouakary, see Barnett, 2010). §There were no records of primates and psittacines feeding simultaneously in a tree.
small, we consider that observed significant difference in surviving fruit numbers between the two classes of M. acaciifolium trees (Table 1) are a result of the cumulative deterrent effect of ants’ defence against the trees’ multiple vertebrate seed predators.
Fruit size and seed weight were very similar for trees attacked by seed predators and those they did not attack. We consider this notable for two reasons. First, it shows the seed predators are not choosing one set of trees over another by virtue of some aspect of the fruit (as might be predicted from optimal for-aging if either ant or no-ant trees had larger fruit: Leighton, 1993; Russo, 2003). Second, it indicates that the trees likely had the same initial crop sizes (because, when two plants of similar size are matur-ing fruits, the one with the lower number of fruits may end up producing larger individual fruits; e.g. Myers et al., 2002). Thus, observed selectivity is based either largely or solely on the presence/absence of the mutualistic P. viduus ants. This emphasizes the effec-tiveness of the defensive capacity of these very aggressive insects.
The results of the present study provide novel data on the interactions between seed predators, the plants on which they feed, and the ants that are mutualistic with those plants. To the best of our knowledge, this represents only the second time that
such defensive effects have been demonstrated
against a primate (McKey, 1974), and the first against a seed-predating primate. It also appears to be the first time that such effects have been demonstrated for the parrot family and for squirrels. A similar effect was reported by Thomas (1988) for trees of Ficus capensis (Moraceae), where the presence of O. longinoda weaver ants reduced fruit removal by fruit bats (Megachiroptera: Pteropteridae), although, in this case, the defensive interaction may disrupt normal dispersal of the fig’s chiropterochoerous fruits. Given how effective P. viduus ant colonies appear to be as a seed-predator deterrent, one obvious question is ‘why do approximately one-third of M. acaciifolium trees lack ants?’ This, we consider, is explained by the stochastic nature of mutualistic and commensal ant colony foundation and survivorship (Vasconcelos, 1991, 1993), a process that must be even more fraught in a seasonally flooded habitat such as igapó. Mutualistic ants commonly use honeydew as a major food source (Herms & Mattson, 1992). Derived from phloem via pseudococcid and coccid Hemioptera, the drain on the energy budget of the host plant is fre-quently sufficient to reduce growth and fruit crop size (Buckley, 1983; Bronstein, 1988; Huxley & Cutler, 1991). Given the near-ubiquity of this response, why do M. acaciifolium plants not show this same pattern? Ant colony faeces and debris are often important sources of nutrients for the epiphytic myrmecophytes
in arboreal ant-gardens (Davidson, 1988; Dejean et al., 2000), and we therefore suggest that the nutri-ent supplemnutri-ent from this additional input is sufficinutri-ent to offset the honeydew-based energy drain in M. acaciifolium. This may be because white-sand soils on which they grow are particularly poor in nutrients (Furch, 1997) and plants in such habitats are espe-cially effective at scouring nutrients (Piedade et al,, 2010; Scarano, 2010).
In addition to their ecological interest, we consider the results to be important for a methodological reason: studies of diet selectivity in seed-eating or fruit-eating animals are often based on Ivlev ratios, where the attractiveness of a species is calculated by the ratio of individuals eaten versus number available (Jacobs, 1974). This metric considers all individuals of a species to be equally attractive to a foraging animal whether or not the species has separate male and female plants or hermaphrodite ones. For plants with separate sexes, this approach underestimates the selection ratio for seed predators because a proportion of the population cannot bear seeds (Barnett, 2010). As shown here, for plant species where some indi-viduals host mutualistic ants, this metric may be less accurate still, with failure to correct for the propor-tion of individuals unavailable-by-virtue-of-defence, leading to an inevitable underestimation of a plant species’ importance in the diet of the foraging animal under study.
The presence of ant-defended plants in igapó could have profound effect on foraging success by the habi-tat’s herbivores and granivores. Whether mutualistic associations between ants and igapó trees are common appears unknown. However, we observed ant associations at the base of Tabebuia flowers and of the fruits of two species of Caraipa (Clusiaceae). Eschweilera tenuifolia (Lecythidaceae) seeds are eaten by psittacines, squirrels, and uacaris (Barnett et al., 2005), and are an important diet component (Barnett, 2010). This species also has ants associated with its fruits, and we observed that (but did not quantify) individual E. tenuifolia with ant colo-nies retained fruits for longer than those without them, and uacaris appeared to eat flowers only from Tabebuia and seeds from Caraipa trees that
lacked ants. In addition, Tachigali (Fabaceae:
Caesalpinioideae) and Triplaris (Polygonaceae) are common igapó plants at Jaú, although their seeds were never recorded being eaten by any of the taxa investigated in the present study. Both genera are renowned for the ferocity of their mutualistic Pseudomyrmex and Azteca ants (Ward, 1999), and, at Jaú, all individuals encountered possessed such ants. Taken together, these observations indicate that
situations similar to that recorded here with
M. acaciifolium may also exist for other Amazonian
forest plants, including those in igapó. Therefore, studies of diet selectivity may have been skewed by the presence of individuals that were unavailable for eating because the trees concerned were inhabited by defensive mutualistic ants. A pertinent example comes from the terra firme of Amazonian Peru (E. Heymann, pers.comm.) where Saguinus nigrifrons tamarins have frequently been seen jumping out of Duroia hirsuta (Rubiaceae) trees after having plucked a fruit, then heavily scratching and shaking their bodies to get rid of the aggressive Azteca ants that associate mutualistically with this tree (Frederickson & Gordon, 2009). This situation is in contrast to that recorded for Codonanthe crassifolia (Gesneriaceae), a small creeping vine common on trunks and branches of igapó trees (present on 81 of 100 randomly selected
trees≥ 25 cm diameter at breast height: Barnett,
2010). Members of the ant genus Crematogaster asso-ciate with Codonanthe species, building a carton nest among the roots and defending the plants against herbivores (Kleinfeld, 1978). Cacajao m. ouakary eats both the leaves and flowers of C. crassifolia but does so by nipping off a short trailing section of the vine and then quickly removing to an ant-free perch to process it (Barnett, 2010). Thus, presence of mutualistic ants does not guarantee a plant defence against primates.
Given the potentially underestimated role of ants as deterrents and their influence in making certain foods unavailable, a specific study is recommended that, in accordance with the methods of Stevenson, Link & Ramírez (2005), involves focal sampling on trees with and without ants, and records such vari-ables as the visitation rates of each type of seed predator, the time spent foraging, and seed removal rates.
ACKNOWLEDGEMENTS
The study was undertaken under CNPq-IBAMA Pro-tected Area Study License 138/2006 issued to WRS.
IBAMA-Manaus issued monthly park research
permits to AAB. Funding was generously provided by the American Society of Primatologists, Colum-bus Zoo Conservation Fund, Sophie Danforth
Con-servation Fund, LSB Leakey Foundation (US),
Leakey Fund (UK), Laurie Shapley, Margot Marsh Foundation, Oregon Zoo Conservation Fund, Percy
Sladen Memorial Fund, Pittsburgh Zoo and
Aquarium Conservation Fund, Primate Action Fund, Primate Conservation Inc., Roehampton University, and Wildlife Conservation Society. Technical assis-tance and advice were provided by Fundação Vitória Amazônica, Manaus. At Jaú, we thank Eliana dos Santos Andrade, Eduardo de Souza, Maria do Bom Jesus, Roberto Moreira, and the staff at the IBAMA
base. We thank Itanna Oliveira Fernandes (Instituto Nacional de Pesquisas da Amazônia Ant Laboratory)
for identifying the Pseudomyrmex; Luis Fabio
Silveira (ornithology curator at the Zoological
Museum at the University of São Paulo) for access to the psittacine collection; the staff of the Mammal Section, Natural History Museum London, for access to rodent skulls in their collection; and Eliana dos Santos Andrade for picture research. We thank Eckhard Heymann for sharing unpublished observa-tions. This is Contribution 20 from the Igapó Study Project and contribution no. 2 from the Amazon Mammal Research Group. We thank the journal editors and three anonymous reviewers whose com-ments greatly improved the manuscript.
REFERENCES
Addicott JF. 1985. Competition in mutualistic systems. In:
Boucher DH, ed. The biology of mutualism: ecology and evolution. Oxford: Oxford University Press, 217–247.
Ayres MJ. 1986. White uakaris and the Amazon flooded
forests. PhD Thesis, University of Cambridge.
Barnett AA. 2010. Diet, habitat use and conservation ecology
of the golden-backed uacari (Cacajao melanocephalus ouakary) in Jaú National park, Amazonian Brazil. DPhil Thesis, Roehampton University.
Barnett AA, Bowler M, Bezerra BM, Defler TR. 2013.
Ecology and behaviour of uacaris (genus Cacajao). In: Veiga LM, Barnett AA, Ferrari SF, Norconk M, eds. Evolutionary biology and conservation of titis, sakis and uacaris. Cam-bridge: Cambridge University Press, 151–172.
Barnett AA, de Castilho CV, Shapley R, Anicácio A. 2005. Diet, habitat selection, and natural history of the
golden-backed uacari, Cacajao melanocephalus ouakary, in Jaú National Park, Brazil. International Journal of Primatology 26: 949–961.
Beattie AJ. 1985. The evolutionary ecology of ant–plant
mutualisms. Cambridge: Cambridge University Press.
Bodmer RE. 1991. Strategies of seed dispersal and seed
predation in Amazonian ungulates. Biotropica 23: 255– 261.
Borges SH, Cohn-Haft M, Carvalhaes AMP, Henriques LM, Pacheco JF, Whittaker A. 2001. Birds of Jaú
National Park, Brazilian Amazon: species check-list, bioge-ography and conservation. Ornitologia Neotropical 12: 109– 140.
Borges SH, Iwanaga S, Durigan CC, Pinheiro MR. 2004.
Janelas para a biodiversidade no Parque Nacional do Jau: uma estratégia para o estúdio da biodiversidade na Amazônia. Manaus: WWWF-FVA-IBAMA.
Bronstein JL. 1988. Limits to fruit production in a
monoecious fig: consequences of an obligate mutualism. Ecology 69: 207–214.
Bronstein JL. 1998. The contribution of ant–plant protection
studies to our understanding of mutualism. Biotropica 30: 150–161.
Buckley R. 1983. Interaction between ants and membracid
bugs decreases growth and seed set of host plant bearing extrafloral nectaries. Oecologia 58: 132–136.
Calderón-F D. 2005. Notas acerca de um nido del mango perchiverde Anthracothorax prevostii hendersonii (Trochilidae) en la islã de San Andrés em el Caribe Colombiano. Ornitologia Colombiana 3: 92–96.
Cipollini ML, Levey DJ. 1997. Why are some fruits toxic?
Glycoalkaloids in Solanum and fruit choice by vertebrates. Ecology 78: 782–798.
Correa SB, Winemiller KO, Lopez-Fernandez H, Galetti M. 2007. Evolutionary perspectives on seed consumption
and dispersal by fishes. BioScience 57: 748–756.
Cowan RS. 1953. A taxonomic revision of the genus
Macrolobium (Leguminosae-Caesalpinioideae). Memoires of the New York Botanical Gardens 8: 257–342.
Davidson DW. 1988. Ecological studies of neotropical ant
gardens. Ecology 69: 1138–1152.
Davidson DW, Fisher BL. 1991. Symbiosis of ants with
Cercropia as a function of light regime. In: Huxley CR, Cutler DF, eds. Ant–plant interactions. Oxford: Oxford Uni-versity Press, 289–308.
Dejean A, Corbara B, Orivel J, Snelling RR, Delabie JHC, Belin-Depoux M. 2000. The importance of ant
gardens in the pioneer vegetal formations of French Guiana (Hymenoptera: Formicidae). Sociobiology 35: 425–439.
Dejean A, Djiéto-Lordon C, Orivel J. 2008. The plant ant
Tetraponera aethiops (Pseudomyrmecinae) protects its host myrmecophyte Barteria fistulosa (Passifloraceae) through aggressiveness and predation. Biological Journal of the Linnean Society 93: 63–69.
DeVries PJ. 1991. Mutualism between Thisbe irenea
butter-flies and ants, and the role of ant ecology in the evolution of larval–ant associations. Biological Journal of the Linnean Society 43: 179–195.
Emmons LH. 1984. Geographic variations in densities and
diversities of non-flying mammals in Amazonia. Biotropica
16: 210–222.
Ferreira LV. 1997. Effects of the duration of flooding
on species richness and floristic composition in three hec-tares in the Jaú National Park in floodplain forests in central Amazonia. Biodiversity and Conservation 6: 1353– 1363.
Ferreira LV, Parolin P. 2007. Tree phenology in central
Amazonian floodplain forests: effects of water level fluctua-tion and precipitafluctua-tion at community and populafluctua-tion level. Pesquisas Botânica 58: 139–156.
Ferreira LV, Stohlgren TJ. 1999. Effects of river level
fluctuation on plant species richness, diversity, and distri-bution in a floodplain forest in Central Amazonia. Oecologia
120: 582–597.
Fiala B. 1994. Diversity of ant–plant interactions: protective
efficacy in Macaranga species with different degrees of ant association. Oecologia 97: 186–192.
Fiala B, Maschwitz U, Pong TY, Helbig AJ. 1989. Studies
of a South East Asian ant–plant association: protection of Macaranga trees by Crematogaster borneensis. Oecologia
79: 463–470.
Fonseca CR. 1993. Nesting space limits colony size of the
plant-ant Pseudomyrmex concolor. Oikos 67: 473–482.
Frederickson ME, Gordon DM. 2009. The intertwined
population biology of two Amazonian myrmecophytes and their symbiotic ants. Ecology 90: 1595–1607.
Freese CH. 1976. Predation on swollen-thorn acacia ants by
white-faced monkeys Cebus capucinus. Biotropica 8: 278– 281.
Furch K. 1997. Chemistry of várzea and igapó soils and
nutrient inventory of their floodplain forests. In: Junk WJ, ed. The Central Amazon Floodplain: ecology of a pulsing system. Berlin: Springer, 47–67.
Galetti M. 1993. Diet of the scaly-headed parrot (Pionus
maximiliani) in a semideciduous forest in southeastern Brazil. Biotropica 25: 419–425.
Gaume L, McKey D, Terrin S. 1998. Ant–plant–homopteran
mutualism: how the third partner affects the interaction between a plant-specialist ant and its myrmecophyte host. Proceedings of the Royal Society of London Series B, Bio-logical Sciences 265: 569–575.
Greeney HF, Merino-M PA. 2006. Notes on breeding birds
from the Cuyabeno Faunistic Reserve in north eastern Ecuador. Boletin da Sociedade Antioquenˇ a de Ornitologia
16: 46–54.
Hauser DC. 1964. Anting by gray squirrels. Journal of
Mammalogy 45: 136–138.
Heil M, McKey D. 2003. Protective ant–plant interactions as
model systems in ecological and evolutionary research. Annual Review of Ecology, Evolution and Systematics 34: 425–453.
Herms DA, Mattson WJ. 1992. The dilemma of plants: to
grow or defend. Quarterly Review of Biology 67: 283–335.
Hershkovitz P. 1987. Uacaris. New World monkeys of the
genus Cacajao (Cebidae, Platyrrhini): a preliminary taxo-nomic review with a description of a new sub-species. American Journal of Primatology 12: 1–53.
Hölldobler B, Wilson EO. 1990. The ants. Cambridge:
Harvard University Press.
Horovitz CC, Schemske DM. 1984. Effects of ants and an
ant-tended herbivore on seed production of a Neotropical herb. Ecology 65: 1369–1378.
Huxley CR, Cutler DF. 1991. Ant–plant interactions.
Oxford: Oxford University Press.
Inouye DW, Taylor OR. 1979. A temperate region
plant-ant-seed predator system: consequences of extra floral nectar secretion by Helianthella quinquenervis. Ecology 60: 1–7.
Isbell LA, Young TP. 2007. Interspecific and temporal
vari-ation of ant species within Acacia drepanolobium ant domatia, a staple food of patas monkeys (Erythrocebus patas) in Laikipia, Kenya. American Journal of Primatology
69: 1387–1398.
Jacobs J. 1974. Quantitative measurement of food selection.
Oecologia 14: 413–417.
Janzen DH. 1966. Coevolution of mutualism between ants
and acacias in Central America. Evolution 3: 249–275.
Janzen DH. 1969. Birds and the Ant × Acacia interaction
in Central America, with notes on birds and other myrmecophytes. The Condor 71: 240–256.
Jensen TS. 1985. Seed-seed predator interactions of European beech, Fagus silvatica and forest rodents, Clethrionomys glareolus and Apodemus flavicollis. Oikos 44: 149–156.
Junk WJ, Piedade MTF, Schöngart J, Cohn-Haft M, Adeney JM, Wittmann F. 2011. A classification of major
naturally-occurring Amazonian lowland wetlands. Wetlands
31: 623–640.
Kay RF, Meldrum J, Takai M. 2013. Pitheciidae and other
platyrrhine seed predators. In: Veiga LM, Barnett AA, Ferrari SF, Norconk M, eds. Evolutionary biology and con-servation of titis, sakis and uacaris. Cambridge: Cambridge University Press, 3–12.
Keeler KH. 1985. Cost–benefit models of mutualism. In:
Boucher DH, ed. The biology of mutualism: ecology and evolution. Oxford: Oxford University Press, 100–127.
Kinzey WG, Norconk MA. 1990. Hardness as a basis of fruit
choice in two sympatric primates. American Journal of Physical Anthropology 81: 5–15.
Kleinfeld SE. 1978. Ant-gardens: the interaction of Codonanthe crassifolia (Gesneriaceae) and Crematogaster longispina (Formicidae). Ecology 59: 449–456.
Kubitzki K, Ziburski A. 1994. Seed dispersal in flood plain
forests of Amazonia. Biotropica 26: 30–43.
Leighton M. 1993. Modeling dietary selectivity by Bornean
orangutans: evidence for integration of multiple criteria in fruit selection. International Journal of Primatology 14: 257–313.
Letourneau DK, Choe JC. 1987. Homopteran attendance by
wasps and ants: the stochastic nature of interactions. Psyche 94: 81–92.
Lev-Yadun S, Inbar M. 2002. Defensive ant, aphid and
caterpillar mimicry in plants? Biological Journal of the Linnean Society 77: 393–398.
Longino JT. 1984. True anting by the capuchin, Cebus
capucinus. Primates 25: 243–245.
Madej CW, Clay K. 1991. Avian seed preference and weight
loss experiments: the effect of fungal endophyte-infected tall fescue seeds. Oecologia 88: 296–302.
McKey D. 1974. Ant–plants: selective eating of an unoccupied
Barteria by a Colobus monkey. Biotropica 6: 269–270.
Morgan ED. 2008. Chemical sorcery for sociality: exocrine
secretions of ants (Hymenoptera: Formicidae). Myrmecology News 11: 79–90.
Muñoz A, Bonal R. 2008. Are you strong enough to carry
that seed? Seed size/body size ratios influence seed choices by rodents. Animal Behaviour 76: 709–715.
Myers SC, Savelle AT, Tustin DS, Byers RE. 2002. Partial
flower thinning increase shoot growth, fruit size and sub-sequent flower formation of peach. HortScience 37: 647–650.
Notman E, Gorchov DL, Cornejo F. 1996. Effect of
dis-tance, aggregation, and habitat on levels of seed predation for two mammal – dispersed neotropical rain forest tree species. Oecologia 106: 221–227.
Palmer TM, Doak DF, Stanton ML, Bronstein JL, Kiers ET, Young TP, Goheen JR, Pringle RM. 2010. Synergy
of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism. Proceedings of the
National Academy of Sciences of the United States of America 107: 17234–17239.
Parolin P. 2009. Submerged in darkness: adaptations to
prolonged submergence by woody species of the Amazonian floodplains. Annals of Botany 103: 359–376.
Piedade MTF, Junk W, D’Ângelo SA, Wittmann F, Schöngart J, Barbosa KMDN, Lopes A. 2010. Aquatic
herbaceous plants of the Amazon floodplains: state of the art and research needed. Acta Limnologica Brasiliensia 22: 165–178.
Prance GT. 1979. Notes on the vegetation types of Amazonia
III – the terminology of Amazonian forest types subject to inundation. Brittonia 31: 26–38.
Pringle EG, Dirzo R, Gordon DM. 2011. Indirect benefits of
symbiotic coccoids for an ant-defended myrmecophytic tree. Ecology 92: 37–46.
Rech AR, Absy ML. 2011. Pollen storage in the nests of
bees of the genera Partamona, Scaura and Trigona (Hymenoptera, Apidae). Revista Brasiliera de Entomologia
55: 361–372.
Russo SE. 2003. Responses of dispersal agents to tree and
fruit traits in Virola calophylla (Myristicaceae): implications for selection. Oecologia 136: 80–87.
Rylands AB, da Cruz MAOM, Ferrari SF. 1989. An
asso-ciation between marmosets and army ants in Brazil. Journal of Tropical Ecology 5: 113–116.
Scarano FR. 2010. A comparison of dispersal, germination
and establishment of woody plants subjected to distinct flooding regimes in Brazilian flood-prone forests and estua-rine vegetation. Oecologia Australis 4: 177–193.
Scharmann M, Thornham DG, Grafe TU, Federle W. 2013. A novel type of nutritional ant–plant interaction:
ant partners of carnivorous pitcher plants prevent nutrient export by dipteran pitcher infauna. PLoS ONE 8: e63556.
Schemske DW. 1980. The evolutionary significance of
extrafloral nectar production by Costus woodsonii (Zingiberaceae): an experimental analysis of ant protection. Journal of Ecology 68: 959–967.
Schöning C, Ellis D, Fowler A, Sommer V. 2007. Army
ant prey availability and consumption by chimpanzees (Pan troglodytes vellerosus) at Gashaka (Nigeria). Journal of Zoology (London) 271: 125–133.
Stadler B, Dixon AFG. 1998. Costs of ant attendance for
aphids. Journal of Animal Ecology 67: 454–459.
Stevenson PR, Link A, Ramírez BH. 2005. Frugivory and
seed fate in Bursera inversa at Tinigua Park, Colombia: implications for primate conservation. Biotropica 37: 431– 438.
Terborgh J, Losos EM, Riley P, Riley MB. 1993. Predation
by vertebrates and invertebrates on the seeds of five canopy tree species of an Amazonian forest. Vegetatio 107/108: 375–386.
Thomas DW. 1988. The influence of aggressive ants on fruit
removal in the tropical tree, Ficus capensis (Moraceae). Biotropica 20: 49–53.
Vasconcelos HL. 1991. Mutualism between Maieta guianensis Aubl., a myrmecophytic melastome, and one of
its ant inhabitants: ant protection against insect herbivores. Oecologia 87: 295–298.
Vasconcelos HL. 1993. Ant colonization of Maieta guianensus
seedlings, an Amazon ant–plant. Oecologia 93: 439–443.
Vázquez DP, Chacoff NP, Cagnolo L. 2009. Evaluating
multiple determinants of the structure of plant–animal mutualistic networks. Ecology 90: 2039–2046.
Ward PS. 1991. Phylogenetic analysis of pseudomyrmecine
ants associated with domatia-bearing plants. In: Huxley
CR, Cutler DF, eds. Ant–plant interactions. Oxford: Oxford University Press, 335–352.
Ward PS. 1999. Systematics, biogeography and host-plant
associations of the Pseudomyrmex viduus (Hymenoptera: Formicidae) – Triplaris and Tachigali-inhabiting ants. Zoological Journal of the Linnean Society 126: 451– 540.
Yu DW. 2001. Parasites of mutualisms. Biological Journal of
the Linnean Society 72: 529–546.
SHARED DATA
Raw data for all reported numerical results are available on Figshare (http://figshare.com).
