Ants in their plants: Pseudomyrmex ants reduce primate, parrot and squirrel predation on Macrolobium...

Ants in their plants: Pseudomyrmex ants reduceprimate, parrot and squirrel predation on Macrolobiumacaciifolium (Fabaceae) seeds in Amazonian Brazil

ADRIAN A. BARNETT1,2*, THAIS ALMEIDA3, RICHELLY ANDRADE4, SARAH BOYLE5,MARCELO GONÇALVES DE LIMA6, ANN MACLARNON1, CAROLINE ROSS1,WELMA SOUSA SILVA7, WILSON R. SPIRONELLO2 and BEATRIZ RONCHI-TELES2

1Centre for Research in Evolutionary and Environmental Anthropology, University of Roehampton,London SW15 4JD, UK2Coordenação de Biodiversidade, Instituto Nacional de Pesquisas da Amazônia, Manaus, AM69067-375, Brazil3Lab. de Herpetologia, Univ. Federal do Mato Grosso, Boa Esperança, MT 68060-900, Brazil4Dept. de Química, Univ. Federal do Amazonas, Manaus, AM 69077-000, Brazil5Dept. of Biology, Rhodes College, Memphis, TN 38112-1690, USA6Protected Areas Programme, United Nations Environment Program, World Conservation MonitoringCentre, 219c Huntingdon Rd., Cambridge CB3 0DL, UK7Instituto 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 invertebrateherbivores, 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 individualMacrolobium acaciifolium (Fabaceae) trees have on the rates of visitation and fruit removal by four taxa ofseed-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 presencesignificantly reduced both rates of visitation and of fruit removal by C. m. ouakary. The same pattern of reduced fruitremoval 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 demonstrationof the repellent effect of ants on primates and, indeed, the first for squirrels and psittacine birds. © 2014 TheLinnean Society of London, Biological Journal of the Linnean Society, 2014, ••, ••–••.

ADDITIONAL KEYWORDS: Amazona – Ara – Cacajao – Formicidae – plant defence – Sciurus.

INTRODUCTION

Documentation of defensive associations betweenants 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 ininteraction intensity depending on environmentalconditions (Davidson & Fisher, 1991; Fiala, 1994;Palmer et al., 2010; Yu, 2001), although they areoften mutualistic, with ants gaining either suste-nance, shelter or both, and the plants gaining protec-tion from herbivores predation on leaves and/orstems (Bronstein, 1998). Such associations havebeen reported to effectively deter a variety of both

*Corresponding author.E-mail: [email protected] paper is a tribute to the memory of Donald Petrie(1958–2013), a dedicated birder.

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Biological Journal of the Linnean Society, 2014, ••, ••–••. With 3 figures

© 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, ••, ••–•• 1

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vertebrate and invertebrate herbivores (Beattie,1985; Fiala, 1994; Dejean, Djiéto-Lordon & Orivel,2008). However, studies have concentrated on defenceof leaves and shoots, and mutualistic ant defenceagainst potential seed predators has rarely been con-sidered (Inouye & Taylor, 1979; Schemske, 1980;Horovitz & Schemske, 1984).

In the present study, we report on the associationbetween Pseudomyrmex viduus ants and the Neo-tropical leguminous tree Macrolobium acaciifolium(Fabaceae: Faboideae), as well as the impact of antpresence on predation of M. acaciifolium seed bya primate (the golden-backed uacari, Cacajaomelanocephalus ouakary, Pitheciidae), a squirrel(Sciurus igniventris, Sciuridae), and six species fromthe parrot family (Psittacidae: three large parrots,Amazona spp., and three macaws, Ara spp.). To ourknowledge, effective defence of plants by ants againstprimates has previously been reported only once in theliterature (McKey, 1974). Other reports of primate/antinteractions concern active predation of ants by pri-mates (Cebus capuchinus: Freese, 1976; Erythrocebuspatas: Isbell & Young, 2007; Pan troglodytes: Schöninget al., 2007; Lophocebus albigena: Struhsaker, 1979) orof primates eating insects disturbed by army ants(Saguinus: Rylands, de Cruz & Ferrari, 1989) or anting(Longino, 1984). Similarly, other than a report of howforest-floor ants may secondarily disperse fruit thathad fallen to the ground as a result of parrot foragingactivity (Galetti, 1993), we know of no papers thatrefer specifically to interactions between ants andpsittacines. Anting behaviour appears to be the onlyreported 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; topicreview: Bodmer, 1991). The observations reported inthe present study expand the repertoire of potentialinfluences because the additional factor of defensiveant presence may explain the absence or low repre-sentation of the seeds of some plant species in the dietof seed-predating vertebrates.

SPECIES STUDIED

The tree: Macrolobium acaciifolium (Benth.) Benth(Fabaceae: Faboideae) is a widespread tree in northernSouth America. Reaching up to 40 m in height,M. acaciifolium occurs in a variety of habitats includ-ing seasonally flooded riparian forests (várzea andigapó, sensu Prance, 1979) and never-flooded (terrafirme) forest (Cowan, 1953). For plants in floodedforests, such as those in the present study, new shoots

and foliage are produced in a concentrated pulse asannual floodwaters rise (Ferreira & Parolin, 2007).Flowers are produced at this time, and occur as smallinflorescences in the axil of each leaf on the new shoot.The white, bee-pollinated, flowers in each inflorescenceopen near-simultaneously, as do the inflorescences oneach shoot (Rech & Absy, 2011) (Fig. 1). Consequently,as they mature, the fruits are very similar in size andage. Fruits, which are single seeded indehiscent woodypods, are hydrochorous (water-dispersed) and can ger-minate after floating for up to 36 days (Kubitzki &Ziburski, 1994). Some fish dispersal (ichthiochory) alsooccurs (Correa et al., 2007).

The ant: Pseudomyrmex viduus (Smith 1858) is theant species associated with M. acaciifolium (Ward,1991, 1999). It lives in the central hollows of olderstems of the tree. On M. acaciifolium, P. viduusworkers patrol leaves and stems, and summon othersto 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 inBrazilian Amazonia as taxi (pron. ‘tah-shee’).Pseudomyrmex are highly aggressive, and vigorouslydefend their host plant from perceived intruders(Janzen, 1966; Hölldobler & Wilson, 1990). So effec-tive are taxi ants at repelling intruders thattwo species of hummingbirds (Anthracothorax pre-vostii: Calderón-F., 2005; Anthracothorax nigricollis:Greeney & Merino-M., 2006) preferentially nest in

Figure 1. Macrolobium acaciifolium in flower. Becauseinflorescences open near-simultaneously, and floweringtime is short, fruit development is near-synchronous andsize variation is small.

2 A. A. BARNETT ET AL.

© 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, ••, ••–••

Macrolobium trees containing their colonies: althoughit is not known why the hummingbirds themselvesare tolerated by the ants.

Pseudomyrmex ants are commonly associated withspecies of Fabaceae (Ward, 1999), where they raisepseudococcids and coccids (Hemioptera: Coccoidea) inhollow stems. As is common in such relations, sugarysecretions from the hemiopterans form much of thecolony energy budget (Fonseca, 1993; Gaume, McKey& Terrin, 1998; Pringle, Dirzo & Gordon, 2011).Although often defending the host tree againstfolivores and perceived dangers, ant colonies (or morecorrectly their hemiopteran commensals) may act as asubstantial energetic sink for the trees that possessthem (Letourneau & Choe, 1987; Stadler & Dixon,1998) and many studies have shown this can lowerseed crop weight per unit of canopy (Addicott, 1985;Beattie, 1985; Keeler, 1985; Bronstein, 1988; for areview of the topic, see Herms & Mattson, 1992). Iffruit- or seed-size is negatively affected, this mayproduce a potentially confounding variable in theMacrolobium-Pseudomyrmex-seed predator systembeing investigated in the present study because seedsin fruits on plants with ants may be smaller (andtherefore less attractive to seed predators).

The primate: The golden-backed uacari, Cacajaomelanocephalus ouakary, is a medium-sizedNeotropical primate (Hershkovitz, 1987). Unripeseeds from hard-husked fruits dominate its diet andit primarily inhabits flooded forest on the margins ofblackwater rivers (Barnett et al., 2013). In commonwith other members of their clade (Pithecia andChiropotes), primates of the genus Cacajao have asuite of morphological adaptations to hard-huskedseed predation, including robust splayed canines(used as awls to open fruits, especially along theirsutures) and hypertrophied, spatulate, incisors togouge out seeds once the hardened husk is opened(Kay, Meldrum & Takai, 2013). Uacari damage pat-terns are very characteristic (Fig. 2A). Unripe seedsof M. acaciifolium are an important component ofthe C. m. ouakary diet, ranked 17th out of 148species by number of annual diet records (Barnett,2010), rising to fourth position when recalibrated forjust those specific months when the species was infruit.

The squirrel: The Northern Amazon red squirrel(S. igniventris) is considered a specialist on seeds oflarge hard fruit (Emmons, 1984), although its diet doesnot appear to have been recorded systematically. Toothmarks on fruits (Fig. 2B) allowed us to distinguishsquirrel predation on Macrolobium seeds from that ofparrots, macaws, and uacaris. Other arboreal rodentgenera in Jaú, the central Amazonian site studied

here, include Coendou, Echimys, Makalata, andRhipidomys. The bite marks of each of these speciescan be separated from those of S. igniventris by theirwidth, curve and thickness (A. A. Barnett, unpubl.data).

The parrots: There are 23 psittacine species knownfrom Jaú National Park (Borges et al., 2001). Ofthese, six are large and sufficiently powerful toeffectively process M. acaciifolium fruit (the parrotsAmazona amazonica, Amazona farinosa, andAmazona festiva; the macaws Ara ararauna, Arachloroptera, and Ara macao). The physical patternof psittacine seed predation on a fruit is highly dis-tinctive (Fig. 2C), with the distal portion of thegnathothecal tomia being used to gouge open the fruitand access the seed (Fig. 2D).

A system in which some individuals of a plantspecies have aggressive host-defending mutualisticants and others do not is clearly heterogeneousfrom the perspective of a herbivore or seed-predator.Within a local population individual plants may varynot only in the level of defence, but also in the sizeand nutrient-content of seeds and leaves. These maybe bigger or smaller in plants with ants, dependingon the energy-balance between plant and antmutualists (Frederickson & Gordon, 2009). Suchbetween-individual variation has also been recordedfor mutualisms insects and carnivorous plants(Scharmann et al., 2013). As a result, in a system withdefensive ant mutualists, the simple predictions ofoptimal foraging (i.e. that seed predators will alwayschoose larger fruit: Leighton, 1993; Russo, 2003) maybe confounded by defensive effects because it is pos-sible to imagine a ranked preference (depending onthe pain of interacting with the ants and the sizedifference between the fruits) of:

1. Fewer ants/larger fruits > more ants/larger fruits > fewerants/smaller fruits > more ants/smaller fruits

Or:

2. Fewer ants/larger fruits > fewer ants/smaller fruits > moreants/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 ofP. viduus ant colonies in M. acaciifolium trees does notdeter seed predators

2. In the M. acaciifolium–P. viduus system in the floodedforest of central Amazonia, the presence of ant coloniesdoes not produce a detectable impact on growth in stems,leaves or fruit.

ANT DEFENCE AGAINST SEED PREDATORS 3


Predictions:

(a) From hypothesis (1), we predict that none of the threetypes of vertebrate seed predators studied will show dif-ferences in rates of feeding visits or seed predationbetween M. acaciifolium trees that have or did not haveP. viduus ant colonies.

(b) From hypothesis (2), we predict that there will beno difference in canopy surface area, seed weight m−2

(referred to as ‘seed crop weight’), fruit size or percentageof fruit weight contributed by the seed betweenM. acaciifolium trees that have P. viduus ant colonies andtrees that do not have these ant colonies.

MATERIAL AND METHODSSITE

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 RioNegro, some 220 km upstream from the state capitalManaus. 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 andaroid swamps (buritizal and aningal, respectively;Borges et al., 2004). The remaining 1% is made up ofland being actively used for subsistence farming andminor vegetation types, such as beach scrub and mistforest. The study site was located between the firstmajor set of rapids on the Jaú River (Cachoeira doJaú: 01°53.21″S, 61°40.43″W) and the community ofPatauá (01°53.16″S, 61°44.31″W).

STUDY HABITAT

Igapó is a seasonally flooded forest habitat that occursin narrow ribbons along the margins of sediment-

Figure 2. The fruit of Macrolobium acaciifolium, a single-seeded pod, showing damage patterns characteristic of a varietyof predators and indicating how such predators can be distinguished. Damage is evident by primate Cacajao melanocephalusouakary (A), rodent Sciurus igniventris (B), and parrot Amazona amazonica (C). Example of parrot A. amazonica using thedistal 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 (Junket al., 2011). Inundation may last for up to 9 monthsand water levels may exceed 12 m (Ferreira &Stohlgren, 1999). Plants of some species may betotally submerged for up to 6 months (Parolin, 2009).The majority of plant species in igapó are eitherwater-dispersed or fish-dispersed (Correa et al., 2007),and fruit production coincides with the peak of inun-dation (Ferreira & Parolin, 2007). Igapó communitycomposition is structured by inundation duration andtolerance, with zones of distinct botanical compositionoccurring in bands parallel to, and progressivelyfurther 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 inigapó for 15 days each month, during the part of theyear (June to September) when igapó was flooded andM. acaciiflolium trees were producing their floatingfruits. The project was part of a broader study of thediet and ecology of the golden-backed uacari (Barnett,2010).

We paddled wooden canoes along two floodedtransects of igapó, each approximately 2 km longand 200 m wide (total, approximately 80 ha), andalso criss-crossed within a 78-ha flooded mid-riverisland of pure igapó. During these times, werecorded all visual observations of feeding by uacaris,parrots, macaws, and squirrels, including those onMacrolobium trees. The duration of all feeding eventswas recorded, although only the duration of thosewhere animals were encountered just enteringM. acaciifolium canopies was used in this analysis. Ifmultiple individual of a seed predator species were inthe same canopy at the same time, their individualoccupancy times were recorded and then summed.

We marked all trees in which feeding occurred,including repeat visits by the same species and thoseused by multiple seed predator species. A ‘feedingvisit’ was operationally defined as ‘animals paused ina M. acaciifolium tree and were observed processingor ingesting M. acaciifolium fruit or involved inactivities that led to ingesting such fruit’. Roosting,resting, brief pauses, and the use of M. acaciifoliumtrees as means of passage from the canopy of one treeto another were thus excluded. We also surveyed allM. acaciifolium trees within the three areas surveyedby canoe (the two transects and the igapó island),including both those trees that predators had beenseen to visit and those they had not visited. Weassayed for ant occupancy by lightly shaking andtapping with a stick the canopy of each plant (thecanopy rarely being more than 1 m above the waterlevel of the flooded forest).

Daily, during the 15 observation days per month,we also hand-netted and removed all M. acaciifoliumfruits found floating under individual M. acaciifoliumtrees, recording any damage patterns on them,including the characteristic marks from uacaricanines and incisors, rodent bite marks and psittacinegouges (Fig. 2).

Macrolobium acaciifolium do not grow in clumps,and flow rates of surface water are very slow withinthe 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 dayafter a large storm. These facts and precautions, plusa daily seed collection-and-removal regimen, meantthat the intrusion of seeds from elsewhere wasminimal, and so we are confident that most (if not all)seeds analyzed and counted came from the tree underwhich they were collected. Because seeds were float-ing, post-fall seed removal by forest floor rodents(Terborgh et al., 1993) was precluded, although lossto frugivorous-granivorous fish (such as Collosomaspp., Characidae: Correa et al., 2007) could not bediscounted.

We measured the weight of fruit per m2 of canopy ofeach sampled M. acaciifolium tree, noting whether ithad P. viduus ants. To estimate seed crop weight, wecounted the number of fruits in the canopy andweighed 15 randomly selected fruits (and their seeds)from each study tree.

When calculating crop size per unit area we usedthe number of seeds m−2 (and not m−3), becauseM. acaciifolium infrutescences occur exclusively onthe outer surface of the canopy. Canopy surface areawas calculated by assuming each canopy to be ahalf-sphere (the shape most closely approximatingthat of a M. acaciifolium canopy), measuring thewidth and greatest height, and applying the formula2πr2 (with half the width of the canopy being usedto give r, the radius). We weighed and measuredfruits at the late immature stage (≥ 4 cm long, peri-carp brown, and sclerotized, pedicular attachmentextant) before excision and dispersal becausethis was the stage when the study animals fed onthem.

We measured all collected fruits along their great-est length with SPI 2000 callipers (Fig. 3). To avoiddouble counting fruits retrieved from beneath treesand showing evidence of predation, we only meas-ured fruits when both valves of the pod wereretrieved. Because of small sample sizes from otherspecies (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 themseparately. Under the supervision of Beatriz Ronches-Teles, Itanna Oliveira Fernandes (Department of



Entomology, Instituto Nacional de Pesquisas daAmazônia) identified the ant specimens.

STATISTICAL ANALYSIS

To investigate Prediction 1 (i.e. that ant presence hasno effect on seed predation), we tested for differencesin number of visits to trees with ants versus visits totrees without ants using a chi-squared test for dataon 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 toconduct this test). We also tested for differences inthe number of fruits freshly eaten and encounteredbeneath trees with ants versus trees without antsusing a chi-squared test for data on Amazonaspp. 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 presencehas no effect on canopy surface area, seed cropweight, fruit size, or percentage of fruit weight con-tributed by the seed), and so to test for the potentiallyconfounding variable of negative impacts of ant pres-ence on tree or fruit size or seed weight, we tested forrelationships between canopy surface area (m2) andnumber of fruits, fruit weight (g), and seed weight (g)for trees with ants and trees without ants usingSpearman’s rank correlation and linear regressionanalysis. We compared mean seed crop weight, meannumber of fruit per tree, mean fruit length, meanfruit weight, and mean seed weight per fruit forM. acaciifolium plants with and without ants usingMann–Whitney U-tests. P < 0.05 was considered sta-tistically significant for all tests.

Figure 3. Fruit of Macrolobium acaciifolium showinghow maximum longitudinal length was measured.

Tab

le1.

Com

pari

son

sof

seed

pred

ator

visi

tsto

Mac

rolo

biu

mtr

ees

wit

hve

rsu

sw

ith

out

ants

,an

dco

nsu

mpt

ion

offr

esh

fru

its

Taxo

n

Fee

din

gvi

sits

totr

ees

Fru

its

fres

hly

eate

nby

taxo

nan

den

cou

nte

red

ben

eath

tree

s

Tota

lvi

sits

Obs

erve

d(a

nd

expe

cted

):w

ith

ants

Obs

erve

d(a

nd

expe

cted

):w

ith

out

ants

χ2te

stre

sult

s(d

.f.=

1)To

tal

fru

its

Obs

erve

d(a

nd

expe

cted

):w

ith

ants

Obs

erve

d(a

nd

expe

cted

):w

ith

out

ants

χ2te

stre

sult

s(d

.f.=

1)

Pit

hec

iin

e(C

acaj

ao)

362

(22.

4)34

(13.

6)49

.18,

P<

0.00

0116

84

(104

.7)

164

(63.

3)25

7.05

,P

<0.

0001

Psi

ttac

ine

(Am

azon

aan

dA

raco

mbi

ned

)13

6(8

.1)

7(4

.9)

1.60

,P

=0.

2169

25(4

2.9)

44(2

6.1)

19.7

5,P

<0.

0001

Sci

uri

dae

(Sci

uru

s)0

00

–11

2(6

.9)

9(4

.1)

9.34

,P

=0.

002

Tota

ls49

8(3

0.5)

41(1

8.5)

43.9

7,P

<0.

0001

248

31(1

46.4

)21

7(8

8.6)

280.

37,

P<

0.00

01



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 byseed-predating vertebrates to ant-less M. acaciifoliumtrees than to those where ants were present (N = 41versus 8), and found 506% more fruits predatedunder ant-less M. acaciifolium trees than underthose 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). Individualsof C. m. ouakary were also seen to visit ant-less treessignificantly more often than those with ants (34versus 2), and significantly more seeds eaten by theseprimates were found beneath ant-less trees (164versus 4).

For psittacines, a similar pattern to that observedfor C. m. ouakary was found for seed predation data(44 versus 25). The number of feeding visits did notdiffer (6 versus 7), although the sample size is verysmall.

For rodents, no fruits were found bearing teethmarks of Coendou, Echimys, Malakomys, andRhipidomys. Although no S. igniventris visits wereactually observed, 11 fruits bearing Sciurus sp. teethmarks were found under the study trees.

Overall, when all 42 trees were considered, therewas a positive correlation between tree canopysurface area and crop size, as measured by number offruits (ρ = 0.70, N = 43, P = 0.001), although therewas no relationship between canopy surface area andthe 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 betweencanopy surface area and crop size (ρ = 0.92, N = 27,P < 0.001), although there was no correlation witheither fruit weight (ρ = 0.07, N = 27, P = 0.72) or seedweight (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 topromote growth of trees or their fruits. Where greaterremoval of fruits occurs, it is because of the absenceof ants, with trees otherwise being identical withrespect to fruit density and fruit size and weight.

We found no difference between the canopysurface area of trees with and without ants (Table 2).

However, there was a significant difference betweenthe numbers and weights of fruits observed on treeswith and without ants (Table 2), with trees withoutants having a mean seed crop 63% smaller than thoserecorded on those with ants (1.5 m−2 versus 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 treeswithout ants) and had seeds that were 21.3% heavier(6.1 versus 4.8 g) (Table 2). These differences werestatistically significant (Table 2), again allowing nullHypothesis 2 to be rejected.

For fruits found floating under trees without ants,mean length of eaten fruits was 17.5% larger thanthose of the same developmental stage remaining onthe trees with ants (8 versus 6.6 cm) (Table 2), whichis a statistically significant difference (Table 2). Com-bined, the mean lengths of fruits removed from treeswith no ants were 2.3% smaller than those collectedfrom trees with ants, which is a nonsignificantdifference (Table 2). Thus, Hypothesis 2 is partiallyrejected.

The duration of single feeding bouts was generallyshort (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, with104 ± 88.4 s (N = 3) and 84 ± 38.6 s (N = 3) for Araspp. 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 visitationtimes existed between trees with and without antscould not be conducted because of the small samplesize from trees with ants (C. m. ouakary) and ingeneral for the psittascines.

DISCUSSION

The data obtained in the present study show thatM. acaciifolium trees with ants are visited less oftenby vertebrate seed predators than trees lacking ants.Such animals also eat fewer seeds from trees withants. This apparent preference cannot be a result ofdifferences in the size of trees with or without antsbecause the two samples do not differ statistically forcanopy surface area. Neither is it a result of the sizeof the individual fruits because the mean values donot differ significantly between tree classes. However,trees with ants had both larger seed crop weights andlarger heavier fruits, whereas trees without ants hadlarger fruits floating below them than were on thetrees (Table 2). Thus, the potentially confoundingvariables relating to smaller size of fruit in trees withant colonies appears not to be in operation, and wetherefore attribute the differences solely to the pres-ence of P. viduus ants. Differences in size and weightof seeds remaining on trees appear to a result of theseed predators themselves, which (in Cacajao m.



Tab

le2.

Tree

,fr

uit

,an

dse

edco

mpa

riso

ns

betw

een

tree

sw

ith

ants

and

tree

sw

ith

out

ants

Var

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ean

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D(r

ange

;N

)S

tati

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alre

sult

Inte

rpre

tati

on

Can

opy

size

(m2 )

Wit

han

ts13

6.9

±38

.6(5

5–24

0;27

)P

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ouakary at least) selectively consume larger fruits. Ifthe data for psittacine and rodents are excludedbecause of a small sample size, the primate resultsare still sufficiently robust to reject null Hypothesis 1and invalidate the prediction that significant differ-ences exist in visitation rates and seed predationrates between M. acaciifolium trees that have and donot have P. viduus ants.

Our analysis of seed predation patterns withinthe guild of vertebrate predators of hard seeds atJaú showed that M. acaciifolium seeds were eatenby large parrots (A. amazonica, A. farinosa, andA. 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 1Duration (s)§ 14 12

AmazonaNumber of visits 1 1 1Duration (s)§ 23 103 17

AraNumber of visits 1 1 1Duration (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 frequentforaging 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, andAra*

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 4Duration (s)§ 21,

7009,38, 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

AmazonaNumber of visits 1 1 1Duration (s)§ 83 201 28

AraNumber of visits 1 2 1Duration (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 frequentforaging 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 differencein surviving fruit numbers between the two classes ofM. acaciifolium trees (Table 1) are a result of thecumulative deterrent effect of ants’ defence againstthe trees’ multiple vertebrate seed predators.

Fruit size and seed weight were very similar fortrees attacked by seed predators and those they didnot attack. We consider this notable for two reasons.First, it shows the seed predators are not choosingone set of trees over another by virtue of some aspectof 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 indicatesthat 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 fruitsmay end up producing larger individual fruits; e.g.Myers et al., 2002). Thus, observed selectivity is basedeither largely or solely on the presence/absence of themutualistic P. viduus ants. This emphasizes the effec-tiveness of the defensive capacity of these veryaggressive insects.

The results of the present study provide novel dataon the interactions between seed predators, theplants on which they feed, and the ants that aremutualistic with those plants. To the best of ourknowledge, this represents only the second time thatsuch defensive effects have been demonstratedagainst a primate (McKey, 1974), and the first againsta seed-predating primate. It also appears to be thefirst time that such effects have been demonstratedfor the parrot family and for squirrels. A similareffect was reported by Thomas (1988) for trees ofFicus capensis (Moraceae), where the presence ofO. longinoda weaver ants reduced fruit removal byfruit bats (Megachiroptera: Pteropteridae), although,in this case, the defensive interaction may disruptnormal dispersal of the fig’s chiropterochoerous fruits.

Given how effective P. viduus ant colonies appear tobe as a seed-predator deterrent, one obvious questionis ‘why do approximately one-third of M. acaciifoliumtrees lack ants?’ This, we consider, is explained bythe stochastic nature of mutualistic and commensalant colony foundation and survivorship (Vasconcelos,1991, 1993), a process that must be even morefraught in a seasonally flooded habitat such as igapó.Mutualistic ants commonly use honeydew as a majorfood source (Herms & Mattson, 1992). Derived fromphloem via pseudococcid and coccid Hemioptera, thedrain 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, whydo M. acaciifolium plants not show this same pattern?Ant colony faeces and debris are often importantsources of nutrients for the epiphytic myrmecophytes

in arboreal ant-gardens (Davidson, 1988; Dejeanet al., 2000), and we therefore suggest that the nutri-ent supplement from this additional input is sufficientto offset the honeydew-based energy drain in M.acaciifolium. This may be because white-sand soils onwhich 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 considerthe results to be important for a methodologicalreason: studies of diet selectivity in seed-eating orfruit-eating animals are often based on Ivlev ratios,where the attractiveness of a species is calculated bythe ratio of individuals eaten versus number available(Jacobs, 1974). This metric considers all individuals ofa species to be equally attractive to a foraging animalwhether or not the species has separate male andfemale plants or hermaphrodite ones. For plants withseparate sexes, this approach underestimates theselection ratio for seed predators because a proportionof the population cannot bear seeds (Barnett, 2010).As shown here, for plant species where some indi-viduals host mutualistic ants, this metric may be lessaccurate still, with failure to correct for the propor-tion of individuals unavailable-by-virtue-of-defence,leading to an inevitable underestimation of a plantspecies’ importance in the diet of the foraging animalunder study.

The presence of ant-defended plants in igapó couldhave profound effect on foraging success by the habi-tat’s herbivores and granivores. Whether mutualisticassociations between ants and igapó trees arecommon appears unknown. However, we observed antassociations at the base of Tabebuia flowers and ofthe fruits of two species of Caraipa (Clusiaceae).Eschweilera tenuifolia (Lecythidaceae) seeds areeaten by psittacines, squirrels, and uacaris (Barnettet al., 2005), and are an important diet component(Barnett, 2010). This species also has ants associatedwith its fruits, and we observed that (but didnot quantify) individual E. tenuifolia with ant colo-nies retained fruits for longer than those withoutthem, and uacaris appeared to eat flowers onlyfrom Tabebuia and seeds from Caraipa trees thatlacked ants. In addition, Tachigali (Fabaceae:Caesalpinioideae) and Triplaris (Polygonaceae) arecommon igapó plants at Jaú, although their seedswere never recorded being eaten by any of the taxainvestigated in the present study. Both generaare renowned for the ferocity of their mutualisticPseudomyrmex and Azteca ants (Ward, 1999), and, atJaú, all individuals encountered possessed such ants.

Taken together, these observations indicate thatsituations similar to that recorded here withM. acaciifolium may also exist for other Amazonian



forest plants, including those in igapó. Therefore,studies of diet selectivity may have been skewed bythe presence of individuals that were unavailablefor eating because the trees concerned were inhabitedby defensive mutualistic ants. A pertinent examplecomes from the terra firme of Amazonian Peru(E. Heymann, pers.comm.) where Saguinus nigrifronstamarins have frequently been seen jumping out ofDuroia hirsuta (Rubiaceae) trees after having pluckeda fruit, then heavily scratching and shaking theirbodies to get rid of the aggressive Azteca ants thatassociate mutualistically with this tree (Frederickson& Gordon, 2009). This situation is in contrast to thatrecorded for Codonanthe crassifolia (Gesneriaceae), asmall creeping vine common on trunks and branchesof igapó trees (present on 81 of 100 randomly selectedtrees ≥ 25 cm diameter at breast height: Barnett,2010). Members of the ant genus Crematogaster asso-ciate with Codonanthe species, building a carton nestamong the roots and defending the plants againstherbivores (Kleinfeld, 1978). Cacajao m. ouakary eatsboth the leaves and flowers of C. crassifolia but doesso by nipping off a short trailing section of the vineand then quickly removing to an ant-free perchto process it (Barnett, 2010). Thus, presence ofmutualistic ants does not guarantee a plant defenceagainst primates.

Given the potentially underestimated role of antsas deterrents and their influence in making certainfoods unavailable, a specific study is recommendedthat, in accordance with the methods of Stevenson,Link & Ramírez (2005), involves focal sampling ontrees with and without ants, and records such vari-ables as the visitation rates of each type of seedpredator, the time spent foraging, and seed removalrates.

ACKNOWLEDGEMENTS

The study was undertaken under CNPq-IBAMA Pro-tected Area Study License 138/2006 issued to WRS.IBAMA-Manaus issued monthly park researchpermits to AAB. Funding was generously providedby 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 MarshFoundation, Oregon Zoo Conservation Fund, PercySladen Memorial Fund, Pittsburgh Zoo andAquarium Conservation Fund, Primate Action Fund,Primate Conservation Inc., Roehampton University,and Wildlife Conservation Society. Technical assis-tance and advice were provided by Fundação VitóriaAmazônica, Manaus. At Jaú, we thank Eliana dosSantos Andrade, Eduardo de Souza, Maria do BomJesus, Roberto Moreira, and the staff at the IBAMA

base. We thank Itanna Oliveira Fernandes (InstitutoNacional de Pesquisas da Amazônia Ant Laboratory)for identifying the Pseudomyrmex; Luis FabioSilveira (ornithology curator at the ZoologicalMuseum at the University of São Paulo) for accessto the psittacine collection; the staff of the MammalSection, Natural History Museum London, for accessto rodent skulls in their collection; and Eliana dosSantos Andrade for picture research. We thankEckhard Heymann for sharing unpublished observa-tions. This is Contribution 20 from the Igapó StudyProject and contribution no. 2 from the AmazonMammal Research Group. We thank the journaleditors and three anonymous reviewers whose com-ments greatly improved the manuscript.

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SHARED DATA

Raw data for all reported numerical results are available on Figshare (http://figshare.com).



http://figshare.com

Ants in their plants: Pseudomyrmex ants reduce primate, parrot and squirrel predation on Macrolobium...

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