Ants as flower visitors and their effects on pollinator

Ants as flower visitors and their effects on pollinator behavior

and plant reproduction

by

Adam Richard Cembrowski

A thesis submitted in conformity with the requirements

for the degree of Masters of Science

Ecology and Evolutionary Biology

University of Toronto

copy Copyright by Adam Cembrowski 2013

ii

Ants as flower visitors and their effects on pollinator behavior and plant

reproduction

Adam Cembrowski

Masters of Science



2013

Abstract

Ants regularly visit flowers but they may decrease plant reproductive success by competing with

pollinators or damaging reproductive structures However how ants may exert these costs needs

further clarification In Chapter 1 I review the literature finding that flower-visiting ants often

have neutral effects on plant fitness In Chapter 2 using artificial flowers with male and female

function I investigate how interference competition between flower-visiting Myrmica rubra ants

and Bombus impatiens bumblebees changes pollen analogue movement patterns Ant presence

and scent significantly reduced pollen analogue donation and reception because bees avoided

flowers with ant cues In Chapter 3 to assess the frequency of palynivory among ants I

conducted an acetolysis survey of 75 neo- and paleo-tropical ant species Ants consistently

contained low numbers of pollen grains suggesting opportunistic pollen consumption may be

widespread Altogether ant visitation may be costly but the mechanism depends on the plant

pollinator and ant identities

iii

Acknowledgments

Science is never an individual undertaking Numerous people made the completion of this thesis

possible First and foremost Megan Frederickson gave me the freedom to pursue research

outside of her realm of expertise was extremely patient my ever-changing interests and

supported the decisions I made in my degree My committee also deserves strong thanks James

Thomson was instrumental in my studies giving me lab space supplies and most importantly

time and guidance when I had questions about anything pollination bee or flower related Ben

Gilbert gave statistics help and was helpful with coding questions As well thank you to my

examination committee Spencer Barrett and Helen Rodd

The Frederickson and Thomson lab groups helped me immeasurably giving encouragement

guidance and reality checks when I went too far off track Thank you to Kyle Turner Lina

Arcila Hernandez Kirsten Prior Jane Ogilvie Alison Parker Eric Youngerman and Rebecca

Batstone Kyle especially helped me in all regards both inside and outside of school and was

without question the best field roommate and officemate I could have had Several volunteers

work study students and our lab tech fed ants washed artificial flowers and counted tiny objects

saving me countless hours particularly Harry Rusnock Shannon Meadley Dunphy Margaret

Thompson and Jackie Day I would also like to highlight Marcus Guorui Tan in particular for

his work collaborating with me and running trials when I was in out of town and being

unwaveringly positive about our research Our experiment would not have been nearly as

successful without him

Several people in the department and associated with the lab provided feedback jokes and

friendship without which grad school would have been a depressing place So thank you Natalie

Jones Rachel Germaine Kelly Carscadden Alex de Serrano Jordan Pleet Aaron Hall Susana

Wadgymar Emily Austen Eddie Ho Amanda Gorton Dorina Szuroczki Jenn Coughlan Jon

Sanders and Gabe Miller

People not in the department and both inside and outside of ecology made my time here possible

and more enjoyable than otherwise Thanks to the Tuner family for taking me in during holidays

Maureen Murray and Matt Mazowita for everything and my old supervisor Colleen Cassady St

Clair for helping me get where I am

iv

Lastly my family did an astounding amount for me in letting me cultivate my love of biology

buying me books letting me keep strange animals and getting me outdoors So thank you to my

brothers John and Mark my dad George and my mom Kay And to my partner Katherine for

her unbelievable patience both in regards to my academic life and in her willingness to adapt

hers for mine thank you This could not have happened without you

ldquoVor Allem sind aus der Reihe der fluumlgellosen Insecten die weitverbreiteten fluumlgellosen Ameisen

sehr unwillkommene Gaumlste der Bluumlthen Und dennoch sind gerade sie nach dem Nectar der

Bluumlthen in hohem Grade luumlsternhelliprdquo

ldquoOf all the wingless insects it is the widely dispersed ants that are the most unwelcome guests to

flowers And yet they are the very ones which have the greatest longing for nectarhelliprdquo

A Kerner 1878 Flowers and their Unbidden Guests

v

Table of Contents

Acknowledgments iii

List of Tables vii

List of Figures viii

Chapter 1 Ants as flower visitors and their effects on pollinator behavior and plant

reproduction 1

Abstract 1

Introduction 2

1 Ant interactions with flowers and floral visitors 3

2 Ants as pollinators 12

3 Floral defenses against ants 14

4 Future directions 20

References 24

Tables 39

Chapter 2 Ants and ant scent reduce bumblebee pollination of artificial flowers 54

Abstract 54

Introduction 55

Methods 57

Results 62

Discussion 63

Acknowledgements 66

References 68

Figures 73

Chapter 3 Not just for the bees pollen consumption is common among tropical ants 75

vi

Abstract 75

Introduction 75

Methods 77

Results 78

Discussion 79

Acknowledgements 82

References 83

Tables 86

Figures 91

Concluding Remarks 93

Copyright Acknowledgments 96

vii

List of Tables

Table 11 List of studies of flower-visiting ants that consumed floral rewards or interacted with

pollinators and included a measure of fitness39

Table 12 List of studies that have either demonstrated ant pollination through exclusion

experiments or whose results strongly suggest it48

Table 31 Numbers of adult worker and larval ants examined for each species collected in Peru

and numbers of pollen grains found87

Table 32 Numbers of adult worker and larval ants examined for each species collected in Papua

New Guinea and numbers of pollen grains found90

viii

List of Figures

Figure 21 Photograph of artificial flower lids with anther and stigma74

Figure 22 Dye transferred (mean plusmn 1SE) by B impatiens a) in the presence and absence of M

rubra ants and b) with or without M rubra scent75

Figure 31 Photographs of pollen grains found inside ants92

Figure 32 Relationship between trophic level and pollen presence for neotropical

ant species93

1


reproduction

Cembrowski AR and Frederickson ME

Planned submission to a journal such as Oikos or Insectes Sociaux

ARC wrote the manuscript with input from MEF

Abstract

Ants often provide a range of benefits to flowering plants particularly by reducing herbivory

However when ants visit flowers they can deter pollinators or damage floral structures

Currently it is unclear how often and in what direction flower-visiting ants affect plant

reproductive success A review of the literature shows that ants can help or hinder pollination

processes but overall flower-visiting ants most commonly have a non-significant net effect on

plant fitness Although ants may directly harm flowers or indirectly affect pollination by

consuming floral nectar or harassing pollinators they can also benefit plants by attacking

florivores or predators of pollinators Ants occasionally act as pollinators themselves though ant

secretions often kill pollen grains There is growing evidence that many plants have traits that

allow them to avoid or minimize the negative effects of flower-visiting ants More research is

needed to determine if these traits provide fitness benefits to plants by preventing ant visitation

or if they function as generalized repellents of floral antagonists

2

Introduction

Ants and angiosperms share a long evolutionary history Ant diversification closely followed that

of flowering plants as ants took advantage of the large prey numbers that angiosperms supported

and the new habitats they provided (Moreau 2006) Subsequently numerous angiosperm

lineages evolved intimate associations with ants that function as an indirect or biotic form of

plant defense Food rewards such as extrafloral nectar or pearl bodies or housing in the form of

domatia attract ants to plants where they reduce herbivory and increase plant fitness (reviewed

in Rosumek et al 2009) However the traits that make ants good plant defenders particularly

their abundance attraction to sugar sources and aggressiveness can also cause problems for

plant reproduction Ants attracted by floral nectar can compete with pollinators for resources

and defend flowers potentially reducing plant fitness (Ness 2006 Junker et al 2007) That ants

negatively affect plant reproduction is an old and pervasive hypothesis Kerner (1878) called ants

ldquomost unwelcome guestsrdquo on flowers and more recent authors have similarly expressed that ant

visitation to flowers reduces plant reproductive success (Ness 2006 Lach 2007 Willmer et al

2009)

Nonetheless studies assessing the impact of flower-visiting ants on plant reproductive

success have produced mixed results Ants can have negative impacts on pollination and flower

function (Galen 1983 Puterbaugh 1998 Ness 2006 Hansen and Muumlller 2009) However other

studies have found no effect or even strong benefits of ant visits to flowers (Rico-Gray and

Thien 1989 Altshuler 1999 Schuumlrch 2000 Ashman and King 2005) This discrepancy between

ants being ldquounwelcome guestsrdquo and their actual effects on plant reproduction requires

clarification Our goal here is to highlight the ways that flower-visiting ants may affect plant

reproduction both positively and negatively and to discern through a review of the literature

3

what impacts ants have on plant reproductive success First we discuss mechanisms by which

flower-visiting ants can directly and indirectly impact plant reproduction both through floral

damage and by mediating changes in pollinator or florivore behavior We end this section by

evaluating published research that collectively shows that flower-visiting ants have

predominantly neutral effects on plant fitness measures Next we discuss pollination by ants

focusing on the ldquoantibiotic hypothesisrdquo before describing how plants may prevent ants from

visiting flowers Lastly we discuss promising new avenues of research and highlight work that

still needs to be performed to give a more complete understanding of ants as flower visitors

1 Ant interactions with flowers and floral visitors

i) Damage to flowers

Ants can directly disrupt plant reproduction by damaging floral structures preventing either the

fertilization of ovules or the presentation of pollen Rarely ants forage on floral tissue itself for

example Puterbaugh (1998) found that Formica neorufibarbus ants chewed through the coronal

ring of Eritrichium aretiodes flowers to get lipids More often but still not commonly foraging

ants chew through reproductive tissue to access floral nectar This can cause sterilization of

whole flowers (Echium plantagineum Kirk 1984) or affect female function only if just styles are

damaged effectively creating male flowers (Polemonium viscosum Galen 1983) Antibiotic

secretions on ant integuments may also directly damage pollen grains but the fitness effects of

this are unclear (see 2 below)

Several species of Crematogaster and Allomerus ants sterilize their host plants by

attacking floral buds (Yu and Pierce 1998 Stanton et al 1999 Gaume et al 2005 Maleacute et al

2012 Table 11) These ants nest in ldquoant-plantsrdquo or ldquomyrmecophytesrdquomdashie plants that host ant

4

colonies in specialized structures (domatia) The sterilizing ants do not appear to consume floral

tissues (Yu and Pierce 1998) and two hypotheses may explain why ants destroy floral buds First

ant colony size is often limited by domatia availability on their host plant By destroying floral

buds ants can cause plants to divert resources from reproductive to vegetative growth increasing

domatia number and allowing for larger ant colonies (Yu amp Pierce 1998 Frederickson 2009)

Second when plant-ants must defend their colony from takeovers by other colonies they may

benefit from limiting access to their host plant By destroying buds that could develop into

flowers branches or leaves ants can prevent their host plant from contacting nearby plants

occupied by enemy ant colonies (Stanton et al 1999)

The impact of sterilization on lifetime plant fitness is unclear Ants may destroy all of

their host plantrsquos floral buds (Yu and Pierce 1998) completely preventing reproduction or only a

portion of them (Maleacute et al 2012) allowing some seed set However counter-intuitively this

sterilization behavior may provide long-term fitness benefits to plants (Frederickson 2009

Palmer et al 2010) Ant-plants often host several different ant species over their lifetimes some

of which are non-sterilizing If hosting a sterilizing species at a certain life stage increases

survival or growth relative to hosting a non-sterilizing species at that life stage plants may

increase lifetime fitness by largely forgoing current reproduction in favor of increasing future

reproduction (Palmer et al 2010) Why plants invest resources in producing flowers that are

quickly destroyed by ants is not known but the timing of flower destruction may be important If

ants attack flowers after anthers dehisce plants may still realize some male fitness via pollen

donation (Yu and Pierce 1998) Additionally if the cost of flower production is relatively minor

and ants sometimes ldquomissrdquo flowers (Edwards and Yu 2008) attempting limited reproduction

may be a better strategy than forgoing it entirely

5

ii) Competition with pollinators

Ant activity on flowers can dramatically alter pollinator behavior Ants can reduce the species

diversity frequency or duration of pollinator visits to flowers (Norment 1988 Tsuji et al 2004

Ness 2006 Junker et al 2007 Lach 2007 2008b Romero et al 2011 and see Chapter 2) These

changes are largely due to either exploitative competition (ie consumption of shared resources)

or interference competition (ie direct aggression) between ants and pollinators

a) Exploitative competition

Pollinators and ants frequently compete for floral nectar Flower-visiting ants are often classified

as nectar thieves (sensu Inouye 1980) because they typically enter flowers through the

ldquolegitimaterdquo opening and consume nectar but transfer no pollen (Wyatt 1980 Ness 2006

Chamberlain and Holland 2008) Ants can also act as primary nectar robbers chewing holes

through corollas to reach nectaries (Willmer and Corbet 1981 Koopowitz and Marchant 1998)

although they are more commonly secondary nectar robbers and use holes made by previous

robbers (Newman and Thomson 2005)

Like other flower visitors foraging ants will often leave nectar behind in flowers This

amount can be less (Bleil et al 2011) more (Fritz and Morse 1982) or similar to (Lach 2008a)

amounts left by other visitors Often ants are morphologically constrained from fully exploiting

nectar Unlike bees and butterflies ants do not have proboscises and must get close to nectar to

consume it Narrow corollas or nectar spurs can prevent ant access to some or all floral nectar

(Schemske 1980 Galen and Cuba 2001 and see below) Smaller ants may be better able to

6

access nectar (Newman and Thomson 2005 Agarwal and Rastogi 2007) but can be limited by

their crop size in the amount of nectar they can remove (Lach 2005) If foraging ants leave

enough nectar behind for a pollinator to recover the cost of visiting a flower ants may have

minimal effects on plant reproductive success (Maloof and Inouye 2000 Turner et al 2012)

Differences among ant species in behavior and diet also affect their consumption of floral

nectar Species vary in how many flowers they visit per inflorescence or per plant and in how

many ants will visit a flower simultaneously (Lach 2005 Junker et al 2007 Lach 2013)

Invasive antsmdashthought to be better at exploiting and defending resources than native ants

(Holway et al 2002)mdashoften recruit to flowers in large numbers sometimes several dozen or

more (Visser et al 1999 Hansen and Muumlller 2009) Overall many factors may influence how

heavily ants exploit floral nectar on plants including ant density plant height the spatial or

temporal distribution of floral nectar and the availability of alternative food resources for ants

(Cushman and Addicott 1991 Lach 2013)

Rarely ants and pollinators may compete for pollen We know of only a few studies that

have recorded ants harvesting pollen directly from anthers (Horskins and Turner 1999 Ness

2006 Byk and Del-Claro 2010) Other studies have found pollen grains in ants (eg Baroni

Urbani and de Andrade 1997 and see Chapter 3) but this may not indicate competition with

pollinators ants sometimes collect stray pollen grains from the environment (Creighton 1967)

One New World genus Cephalotes might be specially adapted for pollen consumption They

possess ldquoproventricular shieldsrdquo structures that may restrict solid food to the crop allowing

nestmates to exchange pollen grains via trophallaxis It is unclear if this structure evolved for this

purpose but Cephalotes are the most frequently documented palynivorous ants (eg Creighton

1967 Baroni Urbani and de Andrade 1997 Byk and Del-Claro 2010) How efficiently ants

7

digest pollen and whether ants like bees feed it to larvae as a protein source is unknown At

least two studies have found that ant larvae consume pollen providing some support for this idea

(Wheeler and Bailey 1920 and Chapter 3)

b) Interference competition

Ants are relatively unique among flower visitors in defending floral resources from competitors

(but see Willmer and Corbett 1981 Roubik 1982) This defense ranges from chance encounters

with ants attacking visitors when flower occupancy overlaps (Ashman and King 2005 Junker et

al 2007) to actively patrolling inflorescences or constructing protective galleries around

nectaries (Horvitz and Schemske 1984 Gaume et al 2005 Hansen and Muumlller 2009)

Interference competition even in the absence of exploitative competition is sufficient to alter

pollinator behavior (Chapter 2)

The strength and outcome of interference competition depends on the identities of the ant

and the pollinator Pollinators might not alter their visitation patterns in response to non-

aggressive ants (Junker et al 2007) but more antagonistic ants may elicit avoidance behavior

before or soon after the visitor lands (Willmer and Corbet 1982 Altshuler 1999 Schuumlrch et al

2000 Table 11) Pollinator size may help predict their reaction to ants because ants may deter

only small-bodied pollinators (Gonzaacutelvez et al 2012) It is not clear whether flower visitors view

ants as aggressive competitors or as potential predators rarely ants prey on pollinators (Schatz

and Wcislo 1999) but in most cases ants merely cause pollinators to relocate

How well pollinators recognize and avoid ant-visited flowers is unresolved Collectively

pollinators have lower visitation rates to flowers visited by ants (Romero et al 2011) This is

8

dependent on pollinator identity however dipterans do not appear to discriminate between ant-

visited and ant-free flowers while bees can identify and avoid ant-visited flowers Bees likely

use a combination of visual and olfactory cues to recognize ant-visited flowers They can

identify previous conspecific and some heterospecific insect visitors by the hydrocarbon

ldquofootprintsrdquo they leave during foraging (Stout and Goulson 2001) Bumblebees can detect ant

hydrocarbons although this has been shown only in the laboratory (Ballantyne and Willmer

2012 Chapter 2) No study has yet examined if bees can use sight alone to detect ants but

several suggest it (Junker et al 2007 Gonzaacutelvez et al 2012) Some bees may discriminate

between ant species when visiting flowers (eg Lach 2008b) which follows if not all ant-

pollinator interactions are equally costly The ability of bees to do so will affect how generalized

their avoidance behaviors will be If they can discriminate between species bees may avoid

specific flowers visited by more ldquocostlyrdquo ants However if they cannot bees might either avoid

all ant-visited flowers or none depending on how negative the average interaction with an ant is

iii) Interactions with flower and pollinator antagonists

Ants can defend the flowers they visit Numerous plant species have circumfloral or bracteal

nectaries (ie extrafloral nectaries around flowers) and ants attracted to these nectaries can

reduce bud ovule or flower predation increasing plant fitness (Inouye and Taylor 1979 Rico-

Gray and Thien 1989 Sugiura et al 2006) Although the presence of EFNs (extrafloral nectaries)

so close to floral nectaries (sometimes less than 1 cm Ness 2006) might increase discovery and

exploitation of floral nectar by ants only one study has investigated this hypothesis finding no

relationship between the proximity of EFNs to floral nectaries and antsrsquo use of floral nectar

(Galen 2005) Holes made by nectar robbers are functionally analogous to circumfloral nectaries

9

and can also attract ants that defend flowers (Newman and Thomson 2005) and nectar-thieving

ants can similarly prevent florivory in some systems (Lach 2007 Bleil et al 2011)

Ants can also reduce the abundance of flower-dwelling predators or parasites of

pollinators Ambush predators such as crab spiders often forage at flowers where they may

reduce pollinator visitation rates and plant fitness (Dukas 2001 Gonccedilalvez-Souza et al 2008)

Ants can decrease spider abundance and richness on plants (Rudgers 2004 Renault et al 2005

Nahas et al 2012) and some evidence suggests that they can do the same on flowers (Lach

2008) In select cases ants may also reduce the abundance of pollinator parasitoids (Holland et

al 2011) Whether ants increase plant reproductive success by removing pollinator antagonists

has not yet been examined but should be If ants create lsquoenemy-freersquo flowers pollinators might

prefer to land on flowers with ants

iv) Net effects

Table 11 compiles studies in which the authors recorded ants consuming floral rewards or

interacting with pollinators and measured some aspect of plant fitness (eg fruit or seed set

pollen deposition) We included only a single study per plant species unless subsequent studies

found conflicting results or measured the fitness of another plant sex Records of ant pollination

are included in a separate table (Table 12)

Table 11 reveals relatively few examples of flower-visiting ants negatively affecting

plant fitness given how costly ant visitation is assumed to be The net effect of ants on plant

reproductive success is actually quite variable with similar numbers of studies finding positive

negative or neutral effects of ant presence Surprisingly when ants do have negative effects it is

10

usually because they directly damage floral structures and not because they prevent pollinators

from visiting flowers and successfully transferring pollen Why are ants not more often negative

for plant reproduction when this is commonly assumed to be true

First ants may compensate for reducing pollinator visitation rates by improving

pollination quality As pollinators move between flowers on a plant they often deposit self-

pollen on stigmas (ie geitonogamy) In some plants with late-acting self-incompatibility ovules

fertilized by self-pollen are subsequently aborted reducing the number of seeds that can be

produced (Barrett 2002 and references therein) Geitonogamy can also reduce offspring viability

or vigor (de Jong et al 1993) and cause pollen discounting a reduction in the amount of pollen

available for outcrossing because of self-pollination (Barrett 2002) By competing with

pollinators ants might decrease rates of geitonogamous pollination if pollinators then visit fewer

sequential flowers within a plant Ants might also cause pollinators to fly further between plants

potentially increasing the genetic diversity of pollen arriving at stigmas Although such effects

have been reported for other floral larcenists (Maloof 2001 Irwin 2003) to our knowledge these

hypotheses have not been investigated in relation to ants

Second ants and pollinators do not always forage for the same resources possibly

allowing them to partition floral rewards If ants forage for nectar but not pollen and flowers can

be pollinated efficiently by visitors looking to gather mostly pollen and little or no nectar then

plant reproduction will not be affected by ants consuming floral nectar Junker et al (2010a)

found that honeybees foraged for both pollen and nectar in the absence of ants but reduced their

foraging on nectar but not pollen when ants could access flowers resulting in no difference in

fruit set between treatments Whether pollinators commonly adjust their foraging behaviors in

response to ants warrants further research

11

Third ants are somewhat unique among floral larcenists in that they often provide direct

benefits to the plants they visit In the studies listed in Table 11 ants sometimes decreased

herbivory on plants (Chamberlain and Holland 2008 Bleil et al 2011) or otherwise aided the

plant (eg ant presence repelling smaller less effective pollinators Gonzaacutelvez et al 2012) If the

positive effects of ants cancel or outweigh the negative effects of flower-visiting ants on

pollinators then ant visitation may be neutral or even positive for plant fitness

Fourth ants may impose fitness costs to plants not captured in the studies in Table 11

Nectar robbers have stronger negative effects when plants are pollen-limited (Burkle et al 2007)

but only one study in Table 11 assessed whether flowers would set more seed if they received

more pollen finding no evidence of pollen limitation (Lach 2008a Table 11) Even if ants

decrease pollinator visitation rates there is limited scope for ants to decrease plant reproductive

success when plants are not pollen-limited Furthermore nearly all the studies in Table 11

measured only female fitness Only three quantified aspects of male fitness (Wyatt 1980 Fritz

and Morse 1981 Galen and Geib 2007) and we know of only one other study in a system in

which ants occasionally pollinate that has also measured male fitness (Ashman 2000) All four

studies measured pollen or pollinia removal rates and none found any effect of flower-visiting

ants on male fitness However whether other measures of male fitness (eg seeds sired pollen

deposition patterns) would reveal similar or different effects needs investigation

Finally although floral defenses against ants (see 3 below) may prevent us from

observing the negative effects of ants on plant reproductive success we consider this unlikely

Several studies have examined interactions between ants and plants that share little or no

coevolutionary history usually in the context of ant invasions Although invasive ants often

recruit to flowers in larger numbers than native ants they do not appear to reduce plant

12

reproductive success (Blancafort and Goacutemez 2005 Lach 2007 Lach 2008a but see Hansen and

Muumlller 2009) And in Hawaii where angiosperms evolved for millions of years in the absence of

ants and are thought to have secondarily lost floral defenses against ants (Junker et al 2011a)

there is no evidence that the preponderance of recently introduced flower-visiting ants negatively

affects plant fitness (Junker et al 2010a Bleil et al 2011)

2 Ants as pollinators

Ants may directly benefit plant reproduction by acting as pollinators but this is a relatively rare

occurrence Ants have long been considered poor pollinators (Kerner 1878) Initially this was

based on morphological and behavioral differences between ants and recognized pollinators

Worker ants are wingless and often relatively hairless making them poor pollen dispersers As

well because many ants exhibit Ortstreue (literally ldquoplace fidelityrdquo) ants were thought to return

to the same branch or flower repeatedly effecting no cross pollination (Houmllldobler and Wilson

1990) Though largely true these traits do not necessarily preclude ants from acting as

pollinators (Table 12) Although they commonly have restricted foraging ranges (Houmllldobler and

Wilson 1990) some ants can effect outcrossing (eg Ashman and King 2005 Carvalheiro 2008)

and many ants are as hairy if not hairier than their pollinating counterparts

In the late 1970s the ldquoantibiotic hypothesisrdquo was put forward to explain the rarity of ant

pollination Ants use antibiotic secretions to protect themselves against the fungal and bacterial

pathogens common in their nests and environs Iwanami and Iwadare (1978) found that one of

these compounds myrmicacin also greatly reduces pollen germination rates Subsequently

Beattie et al (1984 1985) found that short periods of contact (le 30 minutes) with an antrsquos

integument caused pollen grains to fail to germinate Some of these pollen-killing compounds

13

were traced back to the ant metapleural gland which produces hygienic secretions (Houmllldobler

and Wilson 1990) although contact with ants lacking metapleural glands can also reduce pollen

viability (Beattie et al 1985 Dutton and Frederickson 2012) Ant mandibular or anal gland

secretions and potentially ant venom may likewise defend ants against pathogens and have

similar effects on pollen germination (Beattie et al 1985 Graystock and Hughes 2011)

Nonetheless ant pollination has been documented repeatedly There are at least 18 cases

in which ant pollination has been shown experimentally and five others in which observations

strongly suggest it (Table 12) The majority of these plants fit the ldquoant pollination syndromerdquo

originally proposed by Hickman (1974) dense stands of short plants with small flowers and

easily accessible nectaries Typically ant-pollinated plants are associated with hot and dry

climates (principally in the Mediterranean) but dry alpine environments may also favor the

evolution of ant pollination (eg Svensson 1985 Puterbaugh 1998 Schiestl and Glaser 2011) In

most cases ants appear to be the sole or major pollinator of the plant in question (Hickman 1974

Peakall et al 1990 de Vega et al 2009) although ants sometimes make only supplementary

contributions to pollination (Schuumlrch et al 2000 Ashman and King 2005) This suggests that co-

evolution between ants and plants may not be necessary for ants to be useful pollinatorsmdashwhich

is surprising given the potential negative effects of ants on plant reproduction

Ant-pollinated plants cope with ant secretions in a variety of ways Several plant species

may simply tolerate pollen damage (Gόmez and Zamora 1992 de Vega et al 2009) apparently

possessing no overt adaptations to prevent it These plants might receive enough pollen to

overcome reduced pollen viability Other plants may place pollen on ant body parts thought to

have fewer secretions thereby potentially escaping damage (eg on ant legs Ramsey 1995) or

attach pollen to ants with specialized structures avoiding direct contact with the ant integument

14

(Peakall et al 1990) It is not known whether pollen evolves resistance to ant secretions or

whether plants deposit pollen on ants which have less disruptive secretions although these

possibilities have been suggested elsewhere (eg Garciacutea et al 1995 Ramsey 1995)

One key question regarding the effects of ant secretions on pollen grains urgently needs

to be resolved Several studies have suggested that the pollen-killing secretions of ants may have

contributed to the evolution of floral defenses against ants (eg Wagner 2000 Galen and Geib

2007) For this to be true ants must decrease male fitness by damaging pollen grains before they

leave flowers and are deposited on receptive stigmas Only two studies have investigated the

effects of ant secretions on pollen still in anthers (Wagner 2000 Galen and Butchard 2003) and

both constrained ants unnaturally to flowers for significantly longer than ants would normally

stay on flowers Although these studies found strong reductions in pollen vigor it is unclear if

ant secretions decrease male fitness under natural ant visitation conditions

3 Floral defenses against ants

Plants are not passive recipients of flower visitors and have some ability to ldquochooserdquo which

organisms can access floral rewards Flowers resist ants using both structural and chemical traits

More thorough investigation is needed to determine whether these traits evolved to prevent or

minimize the negative effects of ants on plant reproductive success (ie whether these traits can

truly be considered defenses against ants see 4ia below) It is unlikely however that ants

experience reciprocal selection to circumvent floral resistance traits because the fitness benefits

to ants of accessing flowers are probably small Thus there may be little scope for

coevolutionary arms races between floral defenses against ants and ant counter-adaptations

15

i) Structural resistance traits

a) Restricting ant access

Numerous plant species have physical structures preventing ant access to flowers Thin pedicels

can limit antsrsquo gripping abilities and make ants easier to dislodge when flowers are moved by

wind (Gaume et al 2005) and waxy secretions can render stems too slippery for ants to climb

(Harley 1991) Structures surrounding flowers such as water moats or dense hairs may similarly

keep ants from accessing floral rewards (Willmer et al 2009) Many such traits function as broad

filters and prevent not only ants but most crawling insects from reaching flowers Thus it is

difficult to determine whether ants florivores or both acted as selective agents favoring the

evolution of physical barriers to flowers

Flower shape may also reduce ant-pollinator conflict Long narrow corollas or nectar

spurs can prevent all but the smallest ants from accessing floral nectaries (Bluumlthgen et al 2004

Agarwal and Rastogi 2007) while still allowing long-tongued pollinators access to rewards

Selection to exclude nectar-thieving ants in such a manner however may be counteracted by

pollinator preferences for wider corollas that allow easier flower handling (Galen and Cuba

2001) Additionally these types of flowers may be more prone to robbery (Irwin and Maloof

2002) limiting their usefulness in preventing nectar larceny

b) Separation in space or time

Plants may separate floral rewards and ants temporally or spatially to minimize ant impacts on

plant reproduction Several authors have proposed that myrmecophytes have adapted to the

16

sterilization or otherwise detrimental activities of ants by locating domatia or food rewards on

different branches than flowers (Izzo and Vasconcelos 2002 Raine et al 2002 Edwards and Yu

2008) Temporal separation of ant and pollinator activities could likewise reduce conflict though

evidence is limited Some acacia flowers dehisce during periods of low ant activity (Willmer and

Stone 1997 Nicklen and Wagner 2006) but it is unclear if this is in response to ants

temperature or pollinator activity Timing of nectar secretion may similarly reduce ant-pollinator

competition If ants are active prior to pollinators they may deplete floral nectar and reduce

pollinator visitation rates (Schaffer et al 1984) However if nectar is secreted when ants are

inactive pollination may occur unimpeded (Norment 1988) This temporal separation could

favor pollinators that are active when ants are not (eg Wyatt and Morse 1981) but this is

poorly documented Further studies particularly focusing on flowers with the potential for

nocturnal and diurnal pollination may provide more examples

c) Extrafloral nectaries (EFNs)

One hypothesis put forward to explain the evolution of EFNs proposes that EFNs ldquodistractrdquo ants

from consuming floral nectar (Kerner 1878 Wagner and Kay 2002) Wagner and Kay (2002)

tested this hypothesis by constructing model plants using artificial nectaries assigned at random

to represent either floral or extrafloral nectaries They found that the presence of EFNs could

reduce ant exploitation of floral nectar However as highlighted by Galen (2005) this design is

closer to a plant making a surplus of flowers some of which will avoid ant visitation if visitation

rates increase sublinearly with increasing flower number Producing extra flowers to escape ant

visitation appears to be a viable strategy in some systems (Ashman and King 2005 Galen 2005)

However Galen (2005) found that applying honey (simulating extrafloral nectar) to P viscosum

17

leaves had the opposite effect and increased ant visits to flowers Only two studies both in

Pachycereus schottii have found evidence for the distraction hypothesis under field conditions

(Chamberlain and Holland 2008 Holland et al 2011)

There is limited empirical support for the distraction hypothesis but abundant evidence

that EFNs attract ants that defend plants against herbivores (reviewed in Rosumek et al 2009)

To function as attractants the presence of EFNs must increase ant abundance on plants

However because of the increased numbers attracted EFNs would not be expected to reduce the

abundance of ants on nectar rewards or be able to satiate the ants recruited Only if ant

abundance stops increasing at a reward density much lower than that available on the plant

would EFNs serve to distract ants In this case the amount of rewards may overwhelm ants

leaving some flowers underexploited However even in P schottii ants still visited flowers

(Chamberlain and Holland 2008) In cases where ant abundance would continue to increase with

additional rewards it is unlikely that EFNs function as distractions

ii) Chemical resistance traits

a) Toxic nectar

One of the earliest proposed floral defenses against ants was toxic nectar (Janzen 1977)

However studies testing Janzenrsquos (1977) hypothesis uncovered only a very few isolated

examples (eg Catalpa speciosa Stephenson 1981 Crinum erubescens Guerrant and Fiedler

1981) in short most floral nectar is not toxic or repellent to ants (Baker and Baker 1978

Schubart and Anderson 1978) In fact ants sometimes prefer floral nectar over solutions with

equivalent sugar concentrations (Koptur and Truong 1998)

18

In contrast floral nectar can repel other flower visitors (eg birds Johnson et al 2006

lepidopterans Kessler and Baldwin 2007) Repellency is often caused by plant secondary

metabolites which may occur in nectar as a by-product of their production elsewhere in the

plant where they function as defenses against herbivory (Adler 2001) Alternatively toxic or

repellent nectar may be adaptive repellent nectar may promote effective pollination by reducing

the amount of reward any one pollinator takes spreading nectar over several pollinator visits

(Kessler and Baldwin 2007) or it may function as a filter selecting for specific pollinators

(Johnson et al 2006) The latter may explain why repellent nectar is not more common

legitimate pollinators in addition to floral larcenists may be deterred from visiting flowers with

repellent nectar This may be particularly true of nectars that would repel ants which are closely

related to bees nectar distasteful to ants may often also be distasteful to bees and those nectars

acting as a filter for bees may still be palatable to ants For example Prŷs-Jones and Willmer

(1992) found that the ammonia-containing nectar of Lathraea clandestina is readily consumed

by both bees and ants even though it deters birds that act as nectar thieves Although floral

nectar itself rarely repels ants Guerrant and Fielder (1981) found that the presence of macerated

petals within nectar can often keep ants away Alkaloids in petals may be responsible and might

explain why ants seldom act as primary nectar robbers these secondary compounds may prevent

ants from chewing through corollas

b) Floral volatiles

Repellent floral volatiles appear to be a more widespread form of chemical resistance against

ants These were reviewed recently by Willmer et al (2009) and will be discussed here only

briefly Numerous plant taxa produce floral scents repellent to ants including myrmecophilous

19

myrmecophytic and non-ant associated plants in both temperate and tropical ecosystems

(Willmer et al 2009 Junker et al 2011a Ballantyne and Willmer 2012) In three large studies

floral volatiles that repel ants were detected in about a third of all plants tested (Willmer et al

2009 Junker et al 2011a Ballantyne and Willmer 2012) Pollen is often the source of ant-

repellent volatile compounds (Willmer et al 2009 Ballantyne and Willmer 2012) but they can

be emitted from other floral parts including petals That pollen is often the source of repellence

could suggest that preventing ant visitation may be more important in protecting male than

female function Additionally because repellence would decrease as pollen is removed from

anthers ants may return and defend flowers more quickly than if repellent chemicals were in

longer-lasting structures (eg petals) In some cases floral volatiles are thought to mimic ant

alarm pheromones (Willmer et al 2009) However floral scents elicit inconsistent reactions

across ant species ranging from repellence to attraction (Agarwal and Rastogi 2007 Ballantyne

and Willmer 2012)

Producing structural or chemical resistance traits may be costly for plants Native

Hawaiian plants which have little recent coevolutionary history with ants appear to have

secondarily lost floral ant repellents (Junker et al 2011a) Both Willmer et al (2009) and Junker

et al (2011a) found that highly chemical repellent flowers did not have strong physical defenses

and vice versa suggesting trade-offs between the two (but see Ballantyne and Willmer 2012)

Like toxic nectar floral ant repellents might sometimes deter both pollinators and ants For

example Galen et al (2011) found that 2-phenylethanol in P viscosum floral scent repels both

flower-damaging F neorufibarbis ants and the plantrsquos main pollinator Bombus kirbyellus

Interestingly four recent studies have found that floral scents can also attract ants

(Agarwal and Rastogi 2007 Edwards and Yu 2008 Schiestl and Glaser 2011 Gonzaacutelvez et al

20

2012) One study (Schiestl and Glaser 2011) has shown that floral scents attract ants to a

potentially ant-pollinated plant and such systems may provide many more examples

4 Future directions

We have highlighted areas in need of further investigation throughout the review Here we focus

on several questions we consider high priorities for future research

i) Floral defenses against ants

a) Do floral resistance traits increase plant fitness

The existence ant-repellent floral traits is often taken as evidence that ants negatively affect plant

reproductive success However despite the abundance and variety of mechanisms excluding ants

from flowers few studies show that ants reduce plant fitness when they visit flowers (Table 11)

This absence is particularly apparent with repellent floral volatiles which may be the most

widespread floral resistance trait (Willmer et al 2009 Junker et al 2011a Ballantyne and

Willmer 2012) To our knowledge only one study has shown that floral ant repellents benefit

plants with repellent P viscosum flowers avoiding damaging ant visits (Galen et al 2011)

Research is urgently needed to investigate if these traits increase plant fitness by excluding ants

or if ant visitation is inconsequential More studies taking advantage of standing variation in

traits (Galen et al 2011) or creating it artificially (eg Junker et al 2010b) will allow us to

distinguish between the two

21

b) If ant visitation is often not costly what caused the evolution of repellent traits and

what maintains them Similarly are these repellent traits truly defenses against ant

visitation or are they generalized defenses against a range of floral antagonists

Ant-repellent floral traits are widespread and their production may be costly (Willmer et al

2009 Junker et al 2011a) The studies in Table 11 however indicate that flower-visiting ants

often do not disrupt plant reproduction particularly outside of myrmecophytes What then

selected for these traits One possibility is that these repellents are not directed solely at ants

Instead a community of antagonistic flower visitors may exert diffuse selection on plants

thereby selecting for and maintaining these traits Structural modifications may repel crawling

insects while chemical repellents such as floral volatiles may repel both flying and non-flying

insects (Junker et al 2011b) How much overlap there is in floral volatiles that repel both ants and

other antagonists needs investigation Until we examine how specific these defenses are to ants

we risk overstating the importance of ants in their evolution

ii) Do ants alter pollen movement patterns or reduce male fitness

We are aware of only four studies that have measured if ant visitation impacts male fitness

(Wyatt 1980 Fritz and Morse 1981 Ashman 2000 Galen and Geib 2007) While none of these

studies found an effect all measured only amounts of pollen or pollinia removed However this

measure does not adequately encompass male fitness alterations to pollen movement patterns

and eventual deposition location may be more important to male function than changes in

removal rates If as suggested by some studies (Altshuler 1999 Lach 2007) ants increase

pollinator relocation rates they may decrease pollen discounting increasing male fitness

However if this increased relocation reduces overall pollen export rates ant competition with

22

pollinators may depress male function Studies using pollen-tracking methods such as fluorescent

dyes will allow us to see how ants change pollen movement patterns and methods like paternity

analysis will reveal how competition between ants and pollinators alters male fitness

iii) Coevolution between ants and plants do myrmecophytes exhibit stronger more

specific defenses against ants

The floral traits of myrmecophytes are most likely to coevolve with ants because all plant

reproduction occurs in the presence of ants Their floral defenses would thus be expected to be

both stronger and more specific to their resident ants than those other plants visited by an array

of more opportunistic ant species Some evidence supports this Willmer et al (2009) found that

resident ants of acacias were repelled by flowers with more aggressive ant species showing

stronger repellence than less aggressive ants Additionally ants not normally associated with

acacias did not respond to acacia floral volatiles More studies are needed in other systems and

should take advantage of phylogenetic approaches examining floral traits in closely related

myrmecophytic and non-myrmecophytic plant species to determine whether ants commonly

select for floral defenses against ants in myrmecophytes

Acknowledgements

For comments and discussion we thank the Frederickson lab particularly Eric Youngerman

Lina Arcila Hernandez and Kyle Turner as well as Alison Parker and Jordan Pleet MEF

acknowledges financial support from an NSERC Discovery Grant a Connaught New Researcher

23

Award an Ontario Ministry of Economic Development and Innovation Early Researcher Award

and the University of Toronto ARC was supported by an Ontario Graduate Scholarship and

Sigma Xi

24

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constricta (Fabaceae) American Journal of Botany 87711ndash715

Wagner D and A Kay 2002 Do extrafloral nectaries distract ants from visiting flowers An

experimental test of an overlooked hypothesis Evolutionary Ecology Research 4293ndash305

Wang C Y Luo Y Tai D An and Y Kou 2008 Ants pollinate Neottia listeroides

(Orchidaceae) in Sichuan China 46836ndash846

Wyatt R 1980 The impact of nectar-robbing ants on the pollination system of Asclepias

curassavica Bulletin of the Torrey Botanical Club 10724ndash28

Wheeler WM and IW Bailey 1920 The feeding habits of Pseudomymine and other ants

Transactions of the American Philosophical Society 22235-279

38

Willmer P G and S A Corbet 1981 Temporal and microclimatic partitioning of the floral

resources of Justicia aurea amongst a concourse of pollen vectors and nectar robbers


Willmer P G and G N Stone 1997 How aggressive ant-guards assist seed-set in Acacia

flowers Nature 388165ndash167

Willmer P G C V Nuttman N E Raine G N Stone J G Pattrick K Henson P Stillman

et al 2009 Floral volatiles controlling ant behaviour Functional Ecology 23888ndash900

Young T P C H Stubblefield and L a Isbell 1997 Ants on swollen-thorn acacias species

coexistence in a simple system Oecologia 10998ndash107

Yu D W and N E Pierce 1998 A castration parasite of an ant-plant mutualism Proceedings

of the Royal Society B Biological Sciences 265375ndash382

39

Tables

Table 11 Studies of ant-flower or ant-pollinator interactions that included a measure of plant fitness Each study system is listed only

once except when results varied between years or when different studies examined male and female fitness Significant effects of ants on

plant fitness are either lsquopositiversquo or lsquonegativersquo non-significant effects are lsquoneutralrsquo When ants significantly affected only one fitness

component but several were measured (eg fruit set and seed production) we still consider the result significant

Plant species Ant species Fitness measure Direction of effect Proposed mechanism Reference

Acacia

drepanolobium

Crematogaster

nigriceps

Proportion

fruiting

Negative Destruction of floral buds Young et al 1997

Asclepias exaltata Several Pollinia inserted

removed

Negative for pollinia

insertion neutral for

pollinia removal

Exploitative competition Wyatt 1980 T

40


Asclepias syriaca Several

Fruit set pollinia

removed

Negative for fruit

set neutral for

pollinia removal

Exploitative competition Fritz and Morse

1981 T

Cordia nodosa Allomerus cf

demerarae

Fruit set Negative Destruction of floral buds Yu and Pierce

1998

Costus woodsonii Wasmannia

auropunctata

Seed set Positive Unknown ant pollination

suggested (but unlikely)

Schemske 1980

Eritrichum aretioides F neorufibarbis

gelida

Seed set Negative Ants damaged flowers Puterbaugh 1998

41


Euphorbia characias Several Seed set Neutral Plants in Argentine ant-

invaded area set less seed

than those in un-invaded

sites but an ant-exclusion

experiment did not produce

significant results

Blancafort and

Gόmez 2005

Ferocactus wislizeni Solenopsis xyloni

and others

Seed set Unknown negative Interference and exploitative

competition S xyloni

reduced seed set relative to

other ants but the study did

not include a no-ant control

Ness 2006

42


Frasera speciosa F neorufibarbis

and Formica sp

Seed set Neutral Nocturnal pollination

occurring when ants were

less active may have

compensated for reduced

diurnal pollinator visitation

Norment 1988

Gypsophila struthium Several Seeds per

inflorescence

Neutral No effect despite large

numbers of ants on flowers

Gόmez et al

1996

Hirtella physophora Allomerus

decemarticulatus

Fruit set Negative Destruction of flowers Orivel et al

2011

Humboldtia brunonis Crematogaster

dohrni

Fruit set Negative Destruction of flowers Gaume et al

2005

43


Lepidium subulatum Several Percentage of

ovules setting

seed

Positive Unknown Gόmez et al

1996

Leucospermum

conocarpodendron

Several Seed set Neutral Site not pollen limited Lach 2008

Linaria vulgaris Several ldquoFemale fitness

indexrdquo

(combination of

number of seeds

fruits flowers

and seed weight)

Positive Reduction in florivory and

seed predation nectar

robbing holes increased ant

visitation

Newman and

Thomson 2005

44


Melastoma

malabathricum

Oecophylla

smaragdina

Seed set Positive Ants deterred less efficient

pollinators increasing

visitation by the more

efficient pollinator

Gonzaacutelvez et al

2012

Metrosideros

polymorpha

Several Fruit set Neutral Ants reduced nectar

collection rates by foraging

bees but had no effect on

pollen collection rates or

fruit set

Junker et al

2010a

Orexis alpine F neorufibarbis

gelida

Seed set Neutral Autogamy or not pollen

limited

Puterbaugh 1988

45


Ouratea spectabilis Cephalotes

pusillus and others

Seeds per fruit Neutral positive C pusillus had no effect on

seed number but other ants

collectively increased seed

set

Byk and Del

Claro 2010

Pachycereus schottii Several Seed set Neutral positive In one year ants showed a

positive effect (seed

number 2008) but no effect

with increased sample sizes

Chamberlain and

Holland 2008

Polemonium

viscosum

F neorufibarbis

gelida

Seed set Negative Ants damaged styles Galen 1983

46


Polemonium

viscosum

F neorufibarbis

gelida

Pollen removal Neutral Ants did not affect pollen

removal even at high ant

densities

Galen and Geib

2007 T

Protea nitida Linepithema

humile and others

Seed set Neutral positive L humile had no effect on

P nitida seed set but native

ants increased it in one year

ants may cause pollinators

to relocate

Lach 2007

Psychotria

limonensis

Ectatomma spp Fruit set Positive Suggested increased

pollinator relocation

Altshuler 1999

47


Roussea simplex Technomyrmex

albipes

Seed set Negative Interference and exploitative

competition

Hansen and

Muumlller 2009

Tristerix aphyllus Several Fruit set Neutral Nectar robbing ants

minimally reduced nectar

levels and had no effect on

hummingbird visitation

Caballero et al

2013

Vaccinium

reticulatum

Several Fruit set Neutral Ants reduced florivory but

did not affect fruit set

Bleil et al 2011

T Study measured male fitness

Study of sterilizing ants showed short-term decrease in female fitness long-term effects are unclear (see text)

48

Table 12 Studies demonstrating either i) ant pollination through an exclusion experiment or ii) that ants transfer pollen (or pollen

analogue) between flowers strongly suggesting ant pollination

Plant species Ant species Ant pollination Evidence Reference

Alyssum purpureum Several Yes Exclusion experiment Gόmez et al 1996

Arenaria tetraquetra Several Yes Exclusion experiment Gόmez et al 1996

Balanophora kuroiwai Leptothorax sp Suggested Exclusion experiment and

observed pollen transfer

and pollen tube formation

but did not see if plants set

seed

Kawakita and Kato 2002

Blandfordia grandiflora Iridomyrmex sp Yes Exclusion experiment Ramsey 1995

Borderea pyrenaica Several Yes Exclusion experiment Garciacutea et al 1995

49


Cytinus hypocistis Several Yes Exclusion experiment de Vega et al 2009

Epipactis thunbergii Camponotus

japonicas

Suggested Observed transfer of

pollinia from ants to

orchids

Sugiura et al 2006

Euphorbia cyparissias Several Yes Exclusion experiment Schuumlrch et al 2000

Fragaria virginiana Several Very likely Ant-only treatments set

comparable seed to flying

pollinator-only treatment

seed set increased with

increasing ant visitation

Ashman and King 2005

Frasera speciosa Several Yes Exclusion experiment Norment 1988

Frankenia thymifolia Several Yes Exclusion experiment Gόmez et al 1996

50


Hormathophylla spinosa Proformica

longiseta

Yes Exclusion experiment Gόmez and Zamora 1992

Jatropha curcas

Several

Tapinoma

melanocephalum

most common

Yes Exclusion experiment Luo et al 2012

Leporella fimbriata Myrmecia urens Yes Observed pollinia transfer

and subsequently

confirmed as ant

pollination

Peakall et al 1987

51


Lobularia maritima Several

Camponotus

micans most

common

Yes Exclusion experiment Gόmez 2000

Microtis parviflora

Iridomyrmex

gracilis

Yes Observation used

laboratory colonies to

replicate observations

Peakall and Beattie 1989

Naufraga balearica

Several

especially

Plagiolepis

pygmaea and

Lasius grandis

Suggested Observation over three

years of study only ants

were observed visiting

ants carried pollen

Cursach and Rita 2011

52


Neottia listeroides Leptothoras sp

Paratrechina sp



orchids

Wang et al 2008

Paronychia pulvinata Formica

neorufibarbis

gelida

Yes Exclusion experiment Puterbaugh 1998

Polygonum cascadense Formica argentea

Very likely Grew plants in greenhouse

open to flying visitors with

minimal seed set only

plants with access to ants

set significant seed

Hickman 1974

53


Retama sphaerocarpa Several Yes Exclusion experiment Gόmez et al 1996

Scleranthus perennis

Several

especially

Formica

rufibarbis

Suggested Ants transferred pollen

analogue to stigmas and

carried pollen on bodies

Svensson 1985

Sedum anglicum Proformica

longiseta

Yes Exclusion experiment Gόmez et al 1996

Trinia glauca Several Yes Exclusion experiment Carvalheiro et al 2008

54

Chapter 2 Ants and ant scent reduce bumblebee pollination of artificial flowers

Cembrowski AR Tan MG Thomson JD and Frederickson ME

In press The American Naturalist

All authors designed the experiment ARC and MGT performed the experiment ARC and MEF

performed statistical analyse

s and ARC wrote the manuscript with input from all authors

Abstract

Ants on flowers can disrupt pollination by consuming rewards or harassing pollinators but it is

difficult to disentangle the effects of these exploitative and interference forms of competition on

pollinator behavior Using highly rewarding and quickly replenishing artificial flowers that

simulate male or female function we allowed bumblebees (Bombus impatiens) to forage (1) on

flowers with or without ants (Myrmica rubra) and (2) on flowers with or without ant scent cues

Bumblebees transferred significantly more pollen analogue both to and from ant free flowers

demonstrating that interference competition with ants is sufficient to modify pollinator foraging

behavior Bees also removed significantly less pollen analogue from ant scented flowers than

from controls making this the first study to show that bees can use ant scent to avoid harassment

at flowers Ant effects on pollinator behavior possibly in addition to their effects on pollen

viability may contribute to the evolution of floral traits minimizing ant visitation

55

Introduction

Trait-mediated indirect interactions arise when a focal species causes phenotypic changes

including behavioral modifications in a second species and these effects cascade to still other

species (Werner and Peacor 2003) Although trait-mediated indirect interactions are often studied

in food webs (eg Werner and Peacor 2003 Preisser et al 2005) they are not limited to trophic

interactions For example the threat of predation can change the behavior of a mutualist thus

affecting its partners (Suttle 2003) In animal-pollinated plants predators can disrupt pollination

directly through density-mediated indirect interactions (Dukas 2005) or via trait-mediated

indirect interactions by changing pollinator behavior When predators are present pollinators

may switch to visiting less rewarding flowers or they may avoid flowers altogether potentially

reducing the amount of pollen donated or received by a flower and thus decreasing plant fitness

(Gonccedilalves-Souza 2008 Ings and Chittka 2009) Similarly competition for floral rewards with

other flower visitors may cause behavioral changes in pollinators (Maloof and Inouye 2000

Ohashi et al 2008) Previous research has shown that bees may spend less time visiting flowers

depleted of rewards (Thomson 1986) and may avoid flowers bearing scent marks that indicate

recent visits by other individuals of the same or different bee species as these flowers are likely

to be depleted (Stout and Goulson 2002)

Whereas competition between pollinators may not be particularly costly for the plant

because both competitors are likely to provide pollination services competition between

pollinators and organisms that do not usually provide a pollination service such as ants has a

greater potential to reduce plant fitness Ants are common floral visitors they are attracted to

flowers for nectar (Lach 2007) and in some cases pollen (Byk and Del Claro 2010) and will

often defend these resources against other flower visitors (Altshuler 1999) However ants rarely

56

contribute much useful pollination antibiotic secretions present on their cuticles kill pollen

grains (Beattie et al 1985 Dutton and Frederickson 2012) and when foraging in flowers ants

sometimes impede female function by damaging stigmas (Galen and Cuba 2001) We will

henceforth consider ants to be non-pollinators and will contrast them to animals like bees that

are pollinators Ants are capable of competing with pollinators in two ways (1) by consuming

floral rewards and reducing their availability to pollinators (ie exploitative competition) and (2)

by directly antagonizing and excluding pollinators from flowers (ie interference competition)

Many plants benefit from the presence of ants numerous plant species recruit ants using

extrafloral nectar food bodies or domatia because ants provide protection against folivores (Heil

and McKey 2003) Similarly some plants have extrafloral nectaries on or near reproductive

tissues that recruit ants that deter florivores (eg Inouye and Taylor 1979) However plants

may incur reproductive costs as a result of their association with ants Some ant species that nest

in myrmecophytes sterilize flowers to shunt plant resources from reproduction to vegetative

growth allowing for greater ant colony growth (Frederickson 2009) Also ants visiting

extrafloral nectaries may be attracted to floral nectaries where they can harass pollinators (Ness

2006) There is growing evidence that many angiosperms have evolved floral traits that prevent

ants from accessing flowers during anthesis (Willmer and Stone 1997 Ballantyne and Willmer

2012) The effects of flower-visiting ants can be substantial Ants can decrease the frequency

duration or species diversity of pollinator visits to flowers (Lach 2008 Hansen and Muumlller 2009

Junker et al 2010 Gonzaacutelvez et al 2012) all of which potentially impact pollen donation and

receipt In some studies changes to pollinator behavior induced by ants have also been linked to

seed set

It is difficult however to disentangle the intertwined effects of exploitative and

interference competition in nature If ants disrupt pollination plants may often evolve traits to

57

deter ants from flowers (Willmer et al 2009) From a practical standpoint this would then limit

our ability to study the effects of ants on pollinator visitation because ants would not visit

flowers Here we used artificial flowers to explore ant-bee interactions in the absence of floral

defenses against ants We used highly rewarding quickly replenishing artificial flowers to

examine how direct harassment (ie interference competition expressed through behavior)

changes bee foraging behavior and how this affects donation and receipt of a pollen analogue

(powdered food dye) while minimizing the effects of exploitative competition We predicted

that flowers visited by ants would both donate and receive less pollen analogue than flowers

without ants because bees would avoid flowers with ants or leave them sooner Because scent

plays a large role in bumblebee communication and flower choice (Stout and Goulson 2002) we

also tested whether the presence or absence of ant scent on artificial flowers would affect pollen

analogue donation because of changes in the foraging behavior of bumblebees

Methods

i) Subjects

Myrmica rubra is an invasive ant in eastern North America with a range and habitat preferences

overlapping that of Bombus impatiens a common bumblebee Because M rubra visits flowers

(A Cembrowski pers obs) the two species likely interact in nature We collected 12 M rubra

colonies in the fall of 2011 and 2012 from Toronto Ontario Canada and the surrounding area

and maintained them in environmental chambers on artificial diet (Dussutour and Simpson 2009)

and a 1410 LD schedule (light 600-2200) We used these colonies as sources of M rubra

workers for experiments

58

Workers from commercially supplied colonies of Bombus impatiens (Biobest Canada

Ltd) foraged on artificial flowers in flight cages (either 24 x 24 x 21 m or 79 x 34 x 20m) at

the University of Toronto We tested a total of five bee colonies four colonies were used in the

ant presence trials and two of these and one additional colony were used in the ant scent trials

Flight cages had overhead fluorescent lights attached to timers In contrast to most previous

studies in which bees have been trained and tested individually the entire worker force of a bee

colony was free to forage at will in our experiments Colonies were trained to forage on artificial

flowers for at least four days before being used in trials After being used for a trial the colony

was not used for at least two days to reduce dye carryover between trials Between trials

bumblebees were fed pollen and given sugar water

ii) Artificial flowers

The flowers (Fig 1 Thomson et al 2012 see also Makino 2008) consisted of glass jars filled

with 30 WV sucrose solution Sugar water travelled by capillary action up a sewing-thread

wick to a hole in a blue-painted lid accumulating in a knot that acts as a nectary Flowers

depleted by visitors were quickly replenished via capillary action and were non-rewarding only

very briefly after visits taking less than a minute to accumulate 05 microl note that bumblebee

visits to a single flower are often separated by several minutes or more (A Cembrowski

unpublished data)

Unlike most previous artificial flower designs these flowers allow for estimation of male

and female fitness because we can measure both the amount and type of dye received by female

flowers (see (d) Dye quantification below) In order to access nectar on a ldquomalerdquo flower a bee

must crawl through a circular ldquoantherrdquo of brush-like weather stripping material dusted in a

59

consistent manner with our pollen analogue powdered food dye (FDampC 5 or 6) which is

transferred to the bee in the process On a ldquofemalerdquo flower a bee crawls through a sticky plastic

reinforcement that functions as a ldquostigmardquo receiving dye from the beersquos body Male flowers

dispensed dye particles over multiple bee visits and could still dispense dye at the end of trials

They resemble many real flowers or flower heads in that pollen is dispensed gradually over time

but less dye is available for transfer with each subsequent bee visit (Harder and Thomson 1989)

iii) Flight cage trials

We conducted 6 ant scent trials between 22 March and 4 June 2012 and the remaining trials (16

ant presence trials and 9 ant scent trials) between 9 November 2012 and 6 January 2013 Ant

presence trials lasted for eight hours and ant scent trials lasted for four hours Artificial flowers

were prepared and placed individually in small plastic containers treated with Fluon (Insect-a-

Slip BioQuip Products Inc) to prevent ants from escaping In ant presence trials we used 32

flowers (16 male and 16 female flowers) arranged in an eight-by-four array with flowers spaced

45 cm apart between rows and 30 cm within rows Ant scent trials used 20 flowers (10 male and

10 female flowers) in a four-by-five array with flowers spaced 30 cm apart between and within

rows In all of the ant presence trials and 9 of the ant scent trials we counted the number of bees

actively foraging after one hour to get a measure of colony activity

a) Ant presence trials

We examined the effects of ants on the amount of dye donated by male flowers and received by

female flowers in sixteen trials testing four bee colonies four times each The containers of eight

randomly chosen male flowers and eight randomly chosen female flowers received 15 M rubra

60

workers each the other 16 flowers remained free of ants Isolated from their colonies M rubra

workers have nowhere to deposit sugar water they collect and therefore may become sated

nonetheless a force of 15 ant workers was enough to maintain visitation to the nectaries where

bees foraged while still rarely having more than one or two ants visit the nectary at any time As

ants attacked bees bees would occasionally carry or throw attacking ants off flowers but despite

this some ants maintained their presence at the nectary throughout the trials Because ants the

size of M rubra consume liquids slowly (~017 ndash 024 microlmin Davidson et al 2004) flowers

replenished nectar more quickly than ants consumed it We used two colors of dye (FDampC 5 and

FDampC 6) to differentiate male flowers with and without ants In two trials for each bee colony

anthers of male flowers with ants were coated with FDampC 5 dye while brushes of male flowers

lacking ants were coated with FDampC 6 dye In the other two trials we reversed dye colors to

control for effects of dye type and color Dye color was assigned in a random order Artificial

flowers were placed in randomly assigned positions in the array before we opened the colony

and allowed the bees to begin foraging

b) Scent trials

We explored the effect of ant scent on dye donation in fifteen trials testing three bee colonies in

six five and four trials each Bees were first exposed to ants by allowing the bees to forage for

eight hours on twenty flowers (ten male and ten female) of which five male flowers had 15 ants

and all others had none No dye was used during this ldquoexposurerdquo day We then collected all but

the five ant-free male flowers in the flight cage leaving these flowers to keep bees foraging

Next we individually stored five new male lids in Fluon-treated containers with ten M rubra

workers Five control male lids were put in identical containers lacking ants The following

61

morning we removed the remaining flowers and set out ten new male and female flowers in a

random spatial arrangement using the lids having or lacking ant scent Thus the ant-scented

flowers were not in the same positions as the ant-visited flowers on which the bees were trained

Only five male flowers had ant scent and the other 15 flowers (five male and ten female) did not

We used the same two dye colors as in i) to differentiate male flowers with and without ant

scent and randomized which color was used for ant-scented flowers between trials We collected

and replaced stigmas from female flowers after one hour and collected the stigmas again after

four hours In the first trial performed we also collected stigmas after two hours but due to the

small amount of dye transferred this was not repeated

iv) Dye quantification

After each trial we quantified the amount of dye transferred to female flowers using a

spectrophotometer We removed the stigmas from female flowers placed them in test tubes

added 51 mL of distilled water to each tube and vortexed each tube thoroughly to ensure the

dye was evenly diluted These were diluted further as needed if the absorbance exceeded the

sensitivity range of the spectrophotometer In the first six scent trials each stigma was analyzed

separately and the dye amounts were summed to obtain a total amount of each dye color

transferred to female flowers in each trial In all the ant presence trials and the other nine scent

trials we opted to treat the experiment as the unit of replication Therefore we combined stigmas

from each treatment type (ant-visited or ant-free) in a test tube and measured the total amount of

each dye color transferred in each treatment in each trial

Because we put different dye colors on male flowers with and without ants we could use

the amount of each dye color donated to all female flowers to measure the reproductive success

62

of ant-visited and ant-free male flowers The total amount of dye (of both colors) received by

female flowers with and without ants was our measure of female reproductive success We

calculated the amount of each dye color in the sample by measuring absorbance at 428 or 486

nm and converting absorbance to micrograms following computational methods for overlapping

spectra (Blanco et al 1989)

v) Statistical analyses

In two trials (one ant presence and one ant scent) most female flowers received no dye because

of low bee activity so we excluded these trials from analyses Because dye reception and

donation values were non-normally distributed we square-root transformed the data before

examining the effects of ant presence or ant scent on dye transfer in ANCOVAs For ant

presence trials we included ant presence on male and female flowers and their interaction as

main effects and the total amount of dye transferred in each trial as a covariate to account for

the large variation in overall dye transfer among trials For ant scent trials we included ant scent

as the main effect time (one or four hours) as a repeated measure the interaction between scent

and time and the total amount of dye transferred as a covariate Covariate by treatment (ant

presence or ant scent) interactions were never significant and so were excluded in final analyses

All analyses were conducted in JMP (v 1000)

Results

Bees usually started foraging within minutes of the beginning of the trial and continued until

flowers were collected from the flight cage or the lights were extinguished An average of 34 plusmn

012 and 40 plusmn 015 (mean plusmn SE) bees were foraging after an hour in the ant presence and ant

63

scent trials respectively Male flowers with ants donated significantly less dye than male flowers

lacking ants (Fig 22a F155 = 4019 p lt 00001) Similarly female flowers with ants received

significantly less dye than female flowers lacking ants (Fig 22a F155 = 461 p = 0036) There

was no significant interaction between ant presence on male flowers and ant presence on female

flowers (F155 = 118 p = 028) Flowers with ant scent donated significantly less dye than

flowers without ant scent (Fig 22b F125 = 11216 p lt 00001) There was no significant effect

of time (F125 = 121 p = 028) or interaction between time and scent (F125 = 111 p = 030) in

the model

Discussion

In this study ants altered bumblebee pollination behavior and exhibited trait-mediated indirect

interactions with (artificial) flowers Through interference competition M rubra workers

significantly affected the pattern of dye transfer by B impatiens causing a preferential flow of

dye from male flowers lacking ants to female flowers lacking ants If manifested in nature such

effects would reduce the reproductive success of plants visited by ants through both male and

female function

Ants could have changed the attractiveness of artificial flowers in at least two ways First

as ants interrupted or altogether prevented bumblebees from foraging at nectaries bumblebees

may have learned to avoid flowers with ants due to the relative inefficiency of foraging at these

flowers something bumblebees take into account (Heinrich 2004) Second bees attempt to

minimize their risk of being attacked during foraging bouts which ants did to visiting bees Ants

often attacked or harassed bees by biting grasping and appearing to sting visiting bees

preventing them from accessing the nectary or reducing their time on flowers (see online video

64

1) and bees sometimes avoided ant-tended flowers entirely This harassment was sometimes

physically traumatic (online video 1) and bees often appeared to have trouble flying after being

attacked by ants Previous research has demonstrated that bumblebees leave or avoid flowers

where they have been harassed (Jones and Dornhaus 2011) and avoid foraging where there is

visual or olfactory evidence of a predator or predation event (Abbott 2006 Goodale and Nieh

2012) Though it is unclear if bumblebees viewed ants as competitors or predators they

responded similarly to flowers having ants as they do to flowers housing predators (Gonccedilalves-

Souza et al 2008)

To avoid artificial flowers with ants bees likely used a combination of visual and

olfactory cues Previous research has shown that bees respond to conspicuous predators or

predator ldquodummiesrdquo on flowers (Suttle 2003 Gonccedilalves-Souza et al 2008) decreasing the

frequency and duration of their visits to these flowers Thus bees may have been able to avoid

flowers harboring ants by sight alone However even in the absence of ants bees still

preferentially visited flowers lacking ant scents (Fig 22b) suggesting that they had learned to

associate ant scent with harassment Bees are adept at associative learning (Wright and Schiestl

2009) and can learn to recognize unique scents left behind by both conspecific and heterospecific

flower visitors (Stout et al 1998) Bees can use these various scents often arising from tarsal

gland deposits (Stout et al 1998) to recognize recently visited flowers that are less likely to be

profitable (Stout and Goulson 2002) Recently Ballantyne and Willmer (2012) demonstrated that

bees learn to associate ant scents with unrewarding artificial flowers and decrease their visitation

to these flowers Our results complement their findings by showing that bees can associate ant

scent with harassment at otherwise rewarding flowers

In our study ant scent caused bees to adjust their foraging strategy and decreased the

amount of pollen analogue that was donated by ant-scented flowers Thus the effects of

65

interference competition with ants on flowers can extend beyond immediate interactions and may

have fitness consequences for plants even when ants are absent Like other olfactory cues these

effects are likely transitory (Stout et al 1998) Although more dye was still donated by male

flowers lacking ant scent than those with ant scent the ratio of dye donated was on average

closer to equality in hours 2-4 than in the first hour (Fig 22b) This effect may be partially

driven by dye depletion of male flowers without ant scent but the lack of a strong corresponding

decrease in flowers with ant scent suggests that visitation patterns became more similar We did

not test whether B impatiensrsquo avoidance of ant scent was an innate or a learned behavior but

previous work has shown that Bombus terrestris does not innately avoid flowers with ant scent

(Ballantyne and Willmer 2012)

Ants may be necessary for plant survival and growth but can be costly for plant

reproduction The evolution of ant attractants such as extrafloral nectaries in some plant lineages

suggests that the costs of ants can be outweighed by their protective abilities However in this

study flowers visited by ants received and donated significantly less dye although they did

retain some sexual function The net benefit of having ants depends on whether ants increase

plant fitness by reducing herbivory more than they decrease plant fitness by disrupting

pollination Alternatively plants may actually benefit from the costs of ants to plant

reproduction ants that castrate flowers may be better defenders increasing plant survival or

vegetative growth when plants are young allowing for increased reproduction later in life when

the plant is colonized by less aggressive non-castrating ants (Frederickson 2009 Palmer et al

2010) In some plant species pollinator harassment by ants may even be beneficial Altshuler

(1999) reported that Ectatomma ants greatly increased fruit set of Psychotria limonensis despite

reductions in pollinator visitation rates presumably due to increases in the rate of pollen

outcrossing Similarly Gonzaacutelvez et al (2012) found that the presence of Oecophylla

66

smaragdina ants on Melastoma malabathricum flowers reduced visitation by less effective

pollinators and increased visitation by more effective Xylocopa bees increasing plant fitness

Cases of ants being beneficial to flowers appear to be the minority and many plant

species have traits that limit ant access to flowers Several studies have detailed floral volatiles

that are thought to mimic ant alarm pheromones and thus repel ants (Junker and Bluumlthgen 2008

Willmer et al 2009) Other plants use structural modifications such as narrow corollas or

slippery stems to limit ant access to flowers (reviewed in Willmer et al 2009) Exploitative

competition between ants and pollinators (Lach 2005 Ballantyne and Willmer 2012) as well as

the lethal effects of ant antibiotic secretions on pollen grains (Beattie et al 1985 Dutton and

Frederickson 2012) may have resulted in selection on plants to reduce ant visits to flowers Our

results suggest that trait-mediated indirect interactions resulting from interference competition

between ants and bees may favor plants that defend their flowers and their pollinators against

ants

Acknowledgements

We thank H Rusnock and S Meadley-Dunphy for assistance J Dix for help with flight cage

construction and Biobest for bumblebee colonies We are grateful to the Thomson and

Frederickson labs for guidance particularly T Makino funded by JSPS for helping to refine

artificial flowers J Ogilvie for help with bees K Prior for M rubra colony collections and K

Turner for study design suggestions The comments of the editor and two anonymous reviewers

prompted improvements in the article especially with regards to study design MEF and JDT

acknowledge NSERC Discovery Grant funding The University of Torontorsquos Faculty of Arts and

Science supported MGRTrsquos participation

67

68

References

Abbott K R 2006 Bumblebees avoid flowers containing evidence of past predation events

Canadian Journal of Zoology 841240-1247


consumers in a tropical forest Oecologia 119600-606

Ballantyne G and Willmer P 2012 Floral visitors and ant scent marks noticed but not used


Beattie A J Turnbull C Knox R B and Williams E G 1984 Ant inhibition of pollen


71421-426

Blanco M Runiaga H Maspoch S and Tarin P 1989 A simple method for

spectrophotometric determination of two-components with overlapped spectra Journal of

Chemical Education 66178-180

Byk J amp Del Claro K 2010 Nectar- and pollen-gathering Cephalotes ants provide no


capabilities Acta Ethologica 1333-38

Davidson D W S C Cook and R R Snelling 2004 Liquid-feeding performances of ants

(Formicidae) ecological and evolutionary implications Oecologia 139255ndash66

Dukas R 2005 Bumble bee predators reduce pollinator density and plant fitness Ecology

861401-1406

Dussutour A and Simpson S J 2009 Communal nutrition in ants Current Biology 19740-

744

69

Dutton E M and Frederickson M E 2012 Why ant pollination is rare new evidence and

implications of the antibiotic hypothesis Arthropod-Plant Interactions 6561-569

Frederickson ME 2009 Conflict over reproduction in an ant-plant symbiosis why Allomerus

octoarticulatus ants sterilize Cordia nodosa trees American Naturalist 173675-681

Galen C and Cuba J 2001 Down the tube pollinators predators and the evolution of flower


Gonccedilalves-Souza T Omena P M Souza J C and Romero G Q 2008 Trait-mediated

effects on flowers artificial spiders deceive pollinators and decrease plant fitness Ecology

892407-2413

Gonzaacutelvez F G Santamariacutea L Corlett R T and Rodriacuteguez-Gironeacutes M A 2012 Flowers


Goodale E and Nieh JC 2012 Public use of olfactory information associated with predation

in two species of social bees Animal Behaviour 84919-924

Harder LD and Thomson JD 1989 Evolutionary options for maximizing pollen dispersal of

animal-pollinated plants American Naturalist 133323-344

Heil M and McKey D 2003 Protective ant-plant interactions as model systems in ecological

and evolutionary research Annual Review of Ecology Evolution and Systematics 34425-

453

Heinrich B 2004 Bumblebee economics 2nd

edn Harvard University Press Cambridge

Ings T C and Chittka L 2009 Predator crypsis enhances behaviourally mediated indirect

effects on plants by altering bumblebee foraging preferences Proceedings of the Royal

Society B 2762031-2036

70

Inouye D W and Taylor O R Jr 1979 A temperate region plant-ant-seed predator system

consequences of extra floral nectar secretion by Helianthella quinquenervis Ecology 601-

7

Junker R R and Bluumlthgen N 2008 Floral scents repel potentially nectar-thieving ants

Evolutionary Ecology Research 10295ndash308

Junker R R Bleil R Daehler C C and Bluumlthgen N 2010 Intra-floral resource partitioning



Jones E I and Dornhaus A 2011 Predation risk makes bees reject rewarding flowers and

reduce foraging activity Behavioral Ecology and Sociobiology 651505-1511

Lach L 2005 Interference and exploitative competition of three nectar-thieving invasive ant

species Insect Sociaux 52257-262


Argentine ants Ecology 881994-2004

Lach L 2008 Argentine ants displace floral arthropods in a biodiversity hotspot Diversity and

Distributions 14281-290

Makino T T and Sakai S 2007Experience changes pollinator responses to floral display size

from size-based to reward-based foraging Functional Ecology 21854863

Maloof J E and Inouye D W 2000 Are nectar robbers cheaters or mutualists  Ecology

812651ndash2661

Ness J H 2006 A mutualismrsquos indirect costs the most aggressive plant bodyguards also deter

pollinators Oikos 113506-514

Ohashi K Leslie A and Thomson JD 2008 Trapline foraging by bumble bees V Effects of

experience and priority on competitive performance Behavioral Ecology 19936-948

71

Palmer T M Doak D F Stanton M L Bronstein J L Kiers E T Young T P Goheen

J R and Pringle R M 2010 Synergy of multiple partners including freeloaders

increases host fitness in a multispecies mutualism Proceedings of the National Academy

of Sciences 10717234-17239

Preisser E L Bolnick D I and Benard M E 2005 Scared to death The effects of

intimidation and consumption in predator-prey interactions Ecology 86501-509

Stout J C Goulson D and Allen J A 1998 Repellent scent-marking of flowers by a guild of

foraging bumblebees (Bombus spp) Behavioral Ecology and Sociobiology 43317-326

Stout J and Goulson D 2002 The influence of nectar secretion rates on the responses of

bumblebees (Bombus spp) to previously visited flowers Behavioral Ecology and

Sociobiology 52239-246

Suttle K B 2003 Pollinators as mediators of top-down effects on plants Ecology Letters

6688-694

Thomson JD 1986 Pollen transport and deposition by bumble bees in Erythronium influences

of floral nectar and bee grooming Journal of Ecology 74329-341

Thomson JD Ogilvie J E Makino T T Arisz A Raju S Rojas-Luengas V and Tan M

G R 2012 Estimating pollination success with novel artificial flowers effects of nectar

concentration Journal of Pollination Ecology 9108-114

Tsuji K Hasyim A and Nakamura K 2004 Asian weaver ants Oecophylla smaragdina and

their repelling of pollinators Ecological Research 19669-673

Ulrich S and Bertsch A 1990 Do foraging bumblebees scent-mark food sources and does it

matter Oecologia 82137-144

Werner E E and Peacor S D 2003 A review of trait-mediated indirect interactions in

ecological communities Ecology 841083-1100

72

Willmer P G Nuttman C V Raine N E Stone G N Pattrick J G Henson K Stillman

P McIlroy L Potts S G and Knudsen J T 2009 Floral volatiles controlling ant

behaviour Functional Ecology 23888-900

Wright G A and Schiestl F P 2009 The evolution of floral scent the influence of olfactory

learning by insect pollinators on the honest signaling of floral rewards Functional Ecology

23841-851

73

Figures

Figure 21 Photograph of artificial flower lids A = anther L = lid N = nectary R = region

where anther or stigma is placed S = stigma T = thread W = weight

74

Figure 22 Dye transferred (mean plusmn 1SE) per trial by B impatiens workers A) from artificial

male and to artificial female flowers in the presence (unfilled circles) or absence (filled circles)

of Myrmica rubra workers and B) from artificial male flowers with (unfilled circles) or without

(filled circles) M rubra scent to ant-free female flowers in the 1st or the 2

nd to 4

th hours of the

trials

75

Chapter 3 Not just for the bees pollen consumption is common among tropical

ants

Cembrowski AR Reurink G and Frederickson ME

Planned submission to Biotropica

ARC and MEF designed the study ARC and GR did laboratory work ARC performed statistical

analyses and wrote the manuscript with input from other authors

Abstract

Although palynivory or pollen consumption is widespread among other hymenopterans there

are few accounts of palynivory in ants To quantify how often ants consume pollen we subjected

adult workers and larvae from 75 species of neo- and paleo-tropical ants to acetolysis a process

that destroys most organic material but leaves behind pollen grains In over half of the species

we examined ants contained a few pollen grains (lt 5) and ants of several Camponotus species

contained abundant pollen grains (gt50) We tested for an association between trophic level and

palynivory using stable nitrogen isotope ratios (δ15

N) but we did not find a significant

correlation we found pollen grains in lsquoherbivorousrsquo omnivorous and carnivorous ants We

suggest that our results indicate sporadic opportunistic pollen consumption by ants in tropical

forests

Introduction

For those organisms that can digest it efficiently pollen can be an excellent food source

Depending on the plant species pollen can contain up to 60 protein as well as lipids

76

carbohydrates and numerous trace nutrients (Roulston and Cane 2000) Pollen feeding

(palynivory) occurs in many taxa including birds mammals and arthropods (Roulston and Cane

2000) but it is best known among the Hymenoptera particularly bees Although adult bees feed

mainly on plant exudates (ie nectar) nearly all bee species rely on pollen as the chief protein

source for developing larvae (Willmer 2011) Closely related to bees ants have similar

nutritional requirements adult workers need carbohydrates whereas larvae are fed a diet rich in

protein (Dussutour and Simpson 2009) Ants also exploit nectar heavily and regularly visit

flowers (eg Herrera et al 1984 Bluumlthgen et al 2004) but unlike bees are not believed to

widely consume pollen Instead ants are thought to receive most of the protein in their diet from

predation or scavenging (eg Floren et al 2002)

However ants may not be as reliant on animal protein sources as commonly assumed In

tropical forests arboreal ants can have similar δ15

N ratios a measure of trophic level as

herbivores suggesting limited carnivory and substantial feeding on plant-derived protein sources

(Davidson et al 2003) One potential protein source is pollen This idea is supported by scattered

accounts of pollen consumption by ants from other ecosystems including deserts (Ness 2006)

boreal forests (Czechowski et al 2009) and tropical savannas (Byk and Del Claro 2010) One

ant genus Cephalotes is widely recognized to consume pollen (Creighton 1967 Baroni Urbani

and de Andrade 1997 Byk and Del Claro 2010) However beyond this genus our knowledge of

pollen consumption by ants has largely been limited to direct observations (but see Czechowski

et al 2011) and it is unknown if palynivory is truly rare among ants or simply under-reported

We borrowed a technique commonly used in palynology acetolysis to assess the frequency of

pollen consumption by ants in 75 neo- and paleo-tropical ant species This technique allowed us

to examine many more ant species than we could have observed directly

77

Methods

Adult worker ants were collected by hand at baits or from leaf litter using Winkler extractors

while larvae along with adults were collected by hand from nests Collections were made by L

Arcila Hernandez and J Sanders in the primary tropical rainforest surrounding the Centro de

Investigaciόn y Capacitaciόn Rio Los Amigos (CICRA 12deg34rsquoS 70deg05rsquoW) in Peru in 2010-

2011 and by E Youngerman from lowland primary and secondary rainforests in Madang

Province Papua New Guinea (PNG) in 2011-2012 We sorted ant samples to morphospecies and

then identified them to genus and when possible to species using existing keys which were

unavailable for PNG ants Ant samples used for acetolysis were whole adult workers guts from

adult workers and whole larvae

We used acetolysis to look for pollen grains inside ants In acetolysis organic material is

dissolved in acetic anhydride and sulfuric acid leaving behind stained pollen exines When

possible we used adult and larval ants of the same species from different colonies or bait

locations in an attempt to sample more representatively We prepared samples by first washing

them in 70 ethanol to remove any pollen present on the samplersquos outer surface before placing

them individually in micro-centrifuge tubes with ~05mL of a 91 mixture of acetic anhydride

sulfuric acid We then heated each sample at 95degC for 20min allowing tissues to dissolve Next

we centrifuged samples at 1000 RPM for 5min and decanted the liquid supernatant before

adding ~05mL of glacial acetic acid to the precipitate centrifuging again as above We decanted

the samples and added a drop of distilled water

78

We examined a 150μL sub-sample of this solution for pollen grains under a light

microscope Larvae gave less than 150μL of solution following acetolysis so we sampled the

entire amount We identified pollen grains by their staining and their surface architecture For

most species we examined at least three adult workers and three larvae but for some species

fewer than three adult workers or larvae were available (Tables 31 and 32)

We investigated the relationship between trophic level as measured by δ15

N ratios and

pollen consumption by ants Stable isotope (SI) data was available for some (n =23) of the

Peruvian species from a separate project in which collections overlapped Samples were stored in

EtOH and dried at 50degC overnight We used heads legs and thoraxes (but not gasters) of ants

for SI analysis Often single individuals did not provide enough material for analysis and we

combined multiple individuals to achieve necessary weights up to 10 for small ant species

Samples were analyzed at the Boston University Stable Isotope Laboratory using a Finnigan

Delta-S analyzer For other Peruvian species for which we had samples but not corresponding

stable isotope data (n =25) we took the median δ15

N ratio value of that speciesrsquo genus and

assigned it to the species in question Using pollen presenceabsence data for these 48 species

we used logistic regression to correlate pollen presence and δ15

N ratio using R (v 2151)

Results

We found pollen grains in 37 of the 197 adult workers 20 of the 102 larvae and 38 of the 75 ant

species we examined (Tables 31 and 32) The proportion of individuals containing pollen did

not differ significantly between larvae and adults (χ2

1 = 002 p = 088) The number of pollen

grains found was often low (median = 3) but highly variable (range 1-468) Also pollen

79

presence was inconsistent among conspecific ant samples of species that contained pollen 31

had pollen in only one of the larvae or adults examined In only three species (two Cephalotes

and one Myrmelachista) did all examined adults contain pollen

Highly lsquoherbivorousrsquo carnivorous and omnivorous ants contained pollen grains (Fig

31) There was no correlation between δ15

N ratio and pollen presence (χ2 = 150 df = 1 p =

022) In fact several carnivorous species contained pollen grains (eg Odontomachus sp 1

Pachycondola sp1)

Discussion

Pollen consumption by ants appears to be more common than suspected The majority of species

(51) had at least one individual that had consumed pollen and in 20 multiple individuals

contained pollen Numbers of grains found tended to be low however with most individuals

containing only a few grains Ants may use pollen as only a small portion of their diet exploiting

a host of other protein-containing foods more heavily including other low- δ15

N foods (eg

honeydew epiphylls Houmllldobler and Wilson 1990 Davidson et al 2003)

There are a few reasons why pollen may not be heavily exploited by ants Pollen requires

much post-consumption processing to extract its nutrients These nutrients are located in the

pollenrsquos cytoplasm which is protected from direct digestion by the exines and intines of the

grains Organisms must either break through these layers or cause the pollen grains to germinate

or pseudo-germinate to access and digest the cytoplasm (Roulston and Cane 2000) This can be

achieved by consuming a sugar-containing solution (such as nectar) along with pollen However

animals that are not adapted to feed on pollen may not be very efficient at this process only

80

extracting nutrients from some of the grains (Herrera and Martiacutenez del Rio 1998) Thus while

ants can likely get some nutrients from pollen other forms of more easily processed protein may

be more attractive

Pollen may also pose handling difficulties for ants Despite the large number of studies

that have recorded ants visiting flowers (Chapter 1) only a few papers detail ants harvesting

pollen directly from anthers Byk and Del Claro (2010) reported that Cephalotes pusillus ants

removed almost all of the available pollen from Ouratea spectabilis flowers and at least two

other studies describe ants consuming pollen along with nectar from flowers (Horskins and

Turner 1999 Ness 2006) Unlike bees which possess both morphological (eg specialized hairs

for holding pollen) and behavioral adaptations (eg stereotyped pollen-packing motions) ants

have no apparent mechanisms to increase the amount of pollen harvested and are likely limited

by the number of grains they can ingest or carry Rather than collect pollen directly from flowers

it appears more likely that ants collect it haphazardly in the environment leading to a smaller

number of pollen grains consumed at any one time It is known that at least Cephalotes ants

engage in such behavior Creighton (1967) observed Cephalotes texanus collecting pollen grains

trapped by Citrus x paradisi leaf hairs

There is a chance that the small numbers of pollen grains we observed came from

secondary pollen consumption (ie consuming a palynivorous organism) or consumption of

liquid containing pollen While we cannot rule this out we believe our results represent actual

targeted pollen consumption by ants Cephalotes ants known palynivores (Creighton 1967

Baroni Urbani and de Andrade 1997) contained similar numbers of pollen grains as many of the

pollen-containing ant species that we examined As well in at least once instance ants that we

found containing pollen grains were in the process of preying on non-pollen consuming

81

organisms (eg a Pachycondola species that was carrying a termite in its mandibles) or were

attracted by sugar baits

Contrary to our expectations there was no relationship between an ant speciesrsquo δ15

N ratio

and whether it had consumed pollen (Fig 32) We expected palynivory to be more common in

herbivorous ants because pollen presents a widespread source of protein a potentially limiting

resource The lack of pattern might reflect how available pollen grains are in the environment

While other forms of food may be preferable ants tend to be opportunistic foragers (Carroll and

Janzen 1973) and there is likely little cost associated with the consumption of scattered pollen

grains during foraging trips beyond the volume they occupy in the gut Some genera were found

to consistently consume pollen In support of previous observations (Baroni Urbani and de

Andrade 1997 Byk and Del Claro 2010) Cephalotes species were among the most common

pollen consumers Camponotus species also consistently contained pollen grains of the eight

species examined five contained pollen and pollen was found in species from both Peru and

PNG Camponotus species also contained the two largest numbers of pollen grains found (468

and 271) Taken together these results suggest that they may be another as yet unrecognized

commonly palynivorous genus

In general larvae did not contain large numbers of pollen grains (ranging from 1-38

grains) This is counter to what is seen in bees where larvae are the main recipients of pollen

(Willmer 2011) This difference may be because ant larvae are continually fed via trophallaxis

by adults throughout their development whereas bee larval cells are provisioned with pollen and

then sealed while larvae complete their development If both adults and larvae are able to extract

nutrients from pollen we would expect to see a preferential flow of nutrients from pollen to

larvae but not necessarily the grains themselves

82

Unlike palynivory by organisms that also provide pollination services pollen

consumption by ants is unlikely to benefit plants Ants rarely act as pollinators (Beattie et al

2004) They have pollen-killing antibiotic secretions on their cuticles (Dutton and Frederickson

2012) and they can compete with other flower visitors reducing flower visitation rates (Ness

2006) The negative impacts of flower-visiting ants are thought to have led to the evolution of

ant-repellent floral volatiles (reviewed in Willmer 2009) These volatiles can pre-empt

competition between ants and pollinators and may often be located within the pollen itself

(Willmer 2009) If floral volatiles truly are a defense against ant visitation our results suggest an

additional evolutionary pressure to not only prevent ant-pollinator interactions but to also

protect plant gametes from occasional consumption by a non-pollinating visitor

Acknowledgements

We would like to thank Jon Sanders Lina Arcila Hernandez and Eric Youngerman for providing

samples the Thomson lab for use of supplies the Pierce lab for funding support during JSrsquo and

EYrsquos collections and the staff of CICRA and the New Guinea Binatang Research Center for

logistical support The Peruvian Ministry of Agriculture provided permits (Nos 394-2009-AG-

DGFFS-DGEFFS and 299-2011-AG-DGFFS-DGEFFS) MEF acknowledges financial support

from an NSERC Discovery Grant a Connaught New Researcher Award an Ontario Ministry of

Economic Development and Innovation Early Researcher Award and the University of Toronto

ARC was supported by an Ontario Graduate Scholarship and Sigma Xi

83

References




function a possible reason why ant pollination is rare American Journal of Botany 71421ndash

426



29418ndash429




Carroll C R and D H Janzen 1973 Ecology of foraging ants Annual Review of Ecology and

Systematics 4231ndash257



Czechowski W B Markό and A Radchenko 2009 Rubbish dumps reveal the diet of ant

colonies Myrmica schencki Em and Myrmica rubra (L) (Hymenoptera Formicidae) as

facultative pollen-eaters Polish Journal of Ecology 56737ndash741

Czechowski WB Markoacute K Erős and E Csata 2011 Pollenivory in ants (Hymenoptera

Formicidae) seems to be much more common than it was thought Annales Zoologici

61519ndash525

84

Dussutour A and S J Simpson 2009 Communal nutrition in ants Current Biology 19740ndash4



Floren A A Biun and K E Linsenmair 2002 Arboreal ants as key predators in tropical

lowland rainforest trees Oecologia 131137ndash144

Grant B R 1996 Pollen digestion by Darwinrsquos finches and its importance for early breeding

Ecology 77489-499

Herrera L G and C Martiacutenez del Rio 1998 Pollen digestion by new world bats effects of

processing time and feeding habits Ecology 792828ndash2838


Cambridge

Horskins K and Turner V B 1999 Resource use and foraging patterns of honeybees Apis


Ecology 24221-227



Roulston T H I and J H Cane 2000 Pollen nutritional content and digestibility for animals

Plant Systematics 222187ndash209

Van Tets I G 1997 Extraction of nutrients from Protea pollen by African rodents Belgian

Journal of Zoology 12759-65

Willmer P G 2011 Pollination and Floral Ecology 1st Edition Princeton University Press

New Jersey

85



86

Tables


Numbers of pollen grains found in individual samples are given in parentheses after the sample

size when there were no grains no numbers are given

Genus Species Number of adults analyzed

(numbers of grains found)

Number of larvae analyzed


Dolichoderinae

Azteca sp 1 3 0

sp 2 2 0

sp 3 0 2

sp 4 3 (1) 0

sp 5 3 (2) 0

Dolichoderus decollatus 3 (66) 0

sp 1 3 0

sp 2 3 1 (2)

sp 3 3 3

sp 4 0 2

Ecitoninae

Labidus sp 1 3 0

Formicinae

Camponotus sp 1 3 3

sp 2 3 (82) 1 (2)

sp 3 3 (3) 0

sp 4 0 2

87

sp 5 8 (11) 0

sp 6 4 (7 16 468) 0

sp 7 5 (12) 0

sp 8 2 (1) 0

Paratrechina sp 1 4 (11) 0

Myrmelachista sp 1 3 (5 11 18) 0

sp 2 0 3

Trachymyrmex sp 1 3 (21) 0

sp 2 3 0

Myrmicinae

Atta sp 1 3 0

Cephalotes atratus 3 (2 2 21) 0

placidus 3 (1 4 21) 0

sp 1 3 0

sp 2 1 0

sp 3 2 0

Crematogaster sp 1 3 1

sp 2 3 (35) 0

sp 3 9 (7) 0

sp 4 2 0

Megalomyrmex sp 1 3 0

sp 2 0 2

sp 3 4 (7) 0

sp 4 3 0

Monomorium sp 1 0 3 (2)

88

Pheidole sp 1 0 3

sp 2 3 0

sp 3 0 3

Procryptocerus sp 1 3 0

Solenopsis sp 1 0 3

sp 2 3 (3 5) 0

Wasmannia sp 1 3 0

Ponerinae

Pachycondola sp 1 3 (3) 0

Odontomachus sp 1 3 (34) 0

Pseudomyrmicinae

Pseudomyrmex sp 1 3 0

sp 2 3 0

sp 3 3 (9) 0

sp 4 0 3

sp 5 0 3

89


New Guinea Numbers of pollen grains found in individual samples are given in parentheses

after the sample size when there were no grains no numbers are given

Genus Species Number adults analyzed

(grains found)

Number larvae analyzed

(grains found)

Aenictinae

Aenictus sp 1 3 3 (1 1)

Dolichoderinae

Philidris sp 1 3 1 (4)

Tapinoma sp 1 2 3 (38)

Technomyrmex sp 1 0 3 (12 12)

Ectatomminae

Rhytidoponera sp 1 1 3 (2)

Formicinae

Acropyga sp 1 3 3 (2)

sp 2 3 3

sp 3 3 3

Anoplolepsis sp 1 3 (1) 3 (1)

Calomyrmex sp 1 3 3 (1)

Camponotus sp 1 3 (1 271) 3

sp 2 1 3

sp 3 2 0

Nylanderia sp 1 3 3

Opisthopsis sp 1 3 3

Polyrachis sp 1 1 3 (4)

90

Myrmicinae


sp 2 3 (32) 3

Monomorium sp 1 3 (1) 3 (1)

sp 2 3 3 (1 1 1)

Pheidole sp 1 3 3

Pristomyrmex sp 1 3 3 (11)

Pyramica sp 1 3 0

Ponerinae

Odontomachus sp 1 3 3 (4)

91

Figures

Figure 31 Photographs of pollen grains found in two ant species a) Dolichoderus sp 2 and b)

Camponotus sp 6 Scale bars = 50 microm

92

Figure 32 Relationship between trophic level as measured by δ15

N ratio and pollen presence

for 48 neotropical ant species 1 Atta sp 5 Azteca spp 8 Camponotus spp 5 Cephalotes spp 4

Crematogaster spp 5 Dolichoderus spp 1 Labidus sp 3 Megalomyrmex spp 1 Monomorium

sp 2 Myrmelachista spp 1 Odontomachus sp 1 Pachycondola sp 1 Paratrechina sp 3

Pheidole sp 4 Pseudomyrmex spp 2 Solenopsis spp and 1 Wasmannia sp

93

Concluding Remarks

Ants have traditionally been considered to be unwelcome flower visitors they consume floral

rewards ostensibly meant for pollinators while rarely providing pollination services themselves

In this thesis I investigate the validity of this assumption and use an experimental study and an

observational study to examine two ways that ants may impact plant reproduction

In the first chapter I review the literature on ants as flower visitors I show that the common

assumption of ants always being categorically negative for plant reproduction is incorrect while

ants may reduce floral attractiveness to pollinators the net effect of ants on plant fitness

measures is variable ranging from positive to negative to neutral I also discuss ants as

pollinators and ways that plants may minimize ant visitation to flowers before finishing with a

section highlighting questions that still need investigation

In the second chapter I explore how interference competition with ants can structure bumblebee

foraging behavior and how this may alter pollen movement patterns Using artificial flowers with

male or female function I allowed Bombus impatiens bumblebees to forage on flowers that

either did or did not have Myrmica rubra ants on them Ant presence significantly reduced the

amount of pollen analogue donated and received by flowers Building on these results I found

that the presence of ant scent alone elicited similar changes to bumblebee behavior reducing the

amount of pollen analogue donated by male flowers My results show that interference

competition is sufficient to alter bumblebee foraging behavior and that the effects of ants on

pollinators may extend after ant visitation to flowers Further study is needed to determine if bees

are able to differentiate between ant species by visual or olfactory cues Their ability to do so

94

could affect how generalized their response to ant presence is and may help to better predict how

ants will affect plant reproduction

In the final chapter I investigate how common palynivory is amongst tropical ant species I used

acetolysis and light microscopy to examine whole ants larvae and ant guts from Papua New

Guinea and Peru I found that tropical ants consistently contain pollen grains albeit often in

small numbers (lt5) However some genera notably Camponotus and Cephalotes consistently

contained higher numbers providing the first evidence that Camponotus may be a palynivorous

genus The small numbers of pollen grains present may indicate that ants preferentially exploit

other more easily digestible high-protein foods over pollen Future studies should investigate

exactly what role pollen plays in ant diets by supplementing the diet of captive ant colonies with

pollen This would allow us to examine how pollen consumption affects colony demography as

well as how efficiently ants digest pollen and whether ants exhibit pollen preferences

I bring up several pressing and unanswered questions within this thesis and highlight three here

First numerous plant species possess chemical or physical traits assumed to increase plant

fitness by reducing ant visitation However this has rarely been tested and instead research has

focused predominately on documenting ant repellence We should move away from this and

begin examining plant fitness in the presence or absence of these repellent traits to see how

beneficial these traits truly are Second how flower visiting ants impact male fitness has been

almost completely ignored in favor of female fitness Future studies should investigate how ant

visitation affects both pollen donation and pollen movement patterns Lastly research involving

antibiotics present on ant cuticles and their effect on pollen viability has been too small in scope

often limited to demonstrating the pollen killing effects of ant secretions Investigation into

95

whether plants have evolved any resistance to the secretions of the local ant community or why

some plants appear unaffected by their ant partners may yield exciting results

In conclusion ants have the capacity to strongly affect plant reproduction both positively and

negatively The fact that these diametrically opposing forces exist means we cannot approach

flower-visiting ants as either positive or negative a priori Instead we should strive to work

towards a better understanding of what is occurring in the system of interest and what role ants

play within it

96

Copyright Acknowledgments

Chapter 2 ldquoAnts and ant scent reduce bumblebee pollination of artificial flowersrdquo is current in

press in The American Naturalist Request for its inclusion here was sought and approved

ii

Ants as flower visitors and their effects on pollinator behavior and plant

reproduction

Adam Cembrowski

Masters of Science



2013

Abstract

Ants regularly visit flowers but they may decrease plant reproductive success by competing with

pollinators or damaging reproductive structures However how ants may exert these costs needs

further clarification In Chapter 1 I review the literature finding that flower-visiting ants often

have neutral effects on plant fitness In Chapter 2 using artificial flowers with male and female

function I investigate how interference competition between flower-visiting Myrmica rubra ants

and Bombus impatiens bumblebees changes pollen analogue movement patterns Ant presence

and scent significantly reduced pollen analogue donation and reception because bees avoided

flowers with ant cues In Chapter 3 to assess the frequency of palynivory among ants I

conducted an acetolysis survey of 75 neo- and paleo-tropical ant species Ants consistently

contained low numbers of pollen grains suggesting opportunistic pollen consumption may be

widespread Altogether ant visitation may be costly but the mechanism depends on the plant

pollinator and ant identities

iii

Acknowledgments





























iv












v

Table of Contents

Acknowledgments iii

List of Tables vii



reproduction 1

Abstract 1

Introduction 2





References 24

Tables 39


Abstract 54

Introduction 55

Methods 57

Results 62

Discussion 63

Acknowledgements 66

References 68

Figures 73


vi

Abstract 75

Introduction 75

Methods 77

Results 78

Discussion 79

Acknowledgements 82

References 83

Tables 86

Figures 91



vii

List of Tables









viii

List of Figures






ant species93

1


reproduction




Abstract













2

Introduction














2009)









3























4
























5





















6
























7






















8























9












iv) Net effects










10
























11
























12























13
























14






















15





















16























17















a) Toxic nectar







18



















b) Floral volatiles




19













and Willmer 2012)











20



4 Future directions
















21























22
















Acknowledgements




23



Sigma Xi

24

References




65















25



71421ndash426












29418ndash429







26













298581ndash596







Botany 4517ndash8

27


333









319







528



28






272



27





652319ndash2327







29



892407ndash2413














Cambridge



30



Ecology 24221-227






7












31



22665ndash670











371323ndash31








32




54















411163ndash1168

33






812651ndash2661













34







10717234ndash9











45373-388



3096

35


Oikos 74265ndash272

















36






68959ndash967















37





















38












39

Tables






Acacia

drepanolobium

Crematogaster

nigriceps

Proportion

fruiting



removed



pollinia removal


40



Fruit set pollinia

removed

Negative for fruit

set neutral for

pollinia removal


1981 T


demerarae


1998


auropunctata



Schemske 1980


gelida


41







significant results

Blancafort and

Gόmez 2005


and others






Ness 2006

42



and Formica sp






Norment 1988


inflorescence



Gόmez et al

1996


decemarticulatus


2011


dohrni


2005

43



ovules setting

seed


1996

Leucospermum

conocarpodendron



indexrdquo

(combination of

number of seeds

fruits flowers

and seed weight)




visitation

Newman and

Thomson 2005

44


Melastoma

malabathricum

Oecophylla

smaragdina






2012

Metrosideros

polymorpha





fruit set

Junker et al

2010a


gelida


limited

Puterbaugh 1988

45



pusillus and others




set

Byk and Del

Claro 2010





Chamberlain and

Holland 2008

Polemonium

viscosum

F neorufibarbis

gelida


46


Polemonium

viscosum

F neorufibarbis

gelida



densities

Galen and Geib

2007 T


humile and others





to relocate

Lach 2007

Psychotria

limonensis



Altshuler 1999

47



albipes


competition

Hansen and

Muumlller 2009





Caballero et al

2013

Vaccinium

reticulatum



Bleil et al 2011



48










seed




49




japonicas



orchids

Sugiura et al 2006










50



longiseta


Jatropha curcas

Several

Tapinoma

melanocephalum

most common



and subsequently

confirmed as ant

pollination

Peakall et al 1987

51



Camponotus

micans most

common


Microtis parviflora

Iridomyrmex

gracilis





Naufraga balearica

Several

especially

Plagiolepis

pygmaea and

Lasius grandis




ants carried pollen


52



Paratrechina sp



orchids

Wang et al 2008


neorufibarbis

gelida








Hickman 1974

53




Several

especially

Formica

rufibarbis




Svensson 1985


longiseta



54







Abstract












55

Introduction























56






















seed set



57













Methods

i) Subjects








58


















unpublished data)





59






















60















b) Scent trials








61























62


















Results




63








the model

Discussion






female function








64








Souza et al 2008)

















65

























66













ants

Acknowledgements









67

68

References









71421-426










861401-1406


744

69









892407-2413









453





Society B 2762031-2036

70



7

















812651ndash2661





71




of Sciences 10717234-17239









6688-694












72






23841-851

73

Figures



74





nd to 4

th hours of the

trials

75


ants





Abstract











forests

Introduction



76

























77

Methods




















78







N ratios and













Results






79








Pachycondola sp1)

Discussion






N foods (eg









80



be more attractive





















81




N ratio





















82











Acknowledgements









83

References





426



29418ndash429













61519ndash525

84







Ecology 77489-499




Cambridge



Ecology 24221-227








New Jersey

85



86

Tables








Dolichoderinae

Azteca sp 1 3 0

sp 2 2 0

sp 3 0 2

sp 4 3 (1) 0

sp 5 3 (2) 0


sp 1 3 0

sp 2 3 1 (2)

sp 3 3 3

sp 4 0 2

Ecitoninae

Labidus sp 1 3 0

Formicinae

Camponotus sp 1 3 3

sp 2 3 (82) 1 (2)

sp 3 3 (3) 0

sp 4 0 2

87

sp 5 8 (11) 0

sp 6 4 (7 16 468) 0

sp 7 5 (12) 0

sp 8 2 (1) 0



sp 2 0 3


sp 2 3 0

Myrmicinae

Atta sp 1 3 0


placidus 3 (1 4 21) 0

sp 1 3 0

sp 2 1 0

sp 3 2 0


sp 2 3 (35) 0

sp 3 9 (7) 0

sp 4 2 0


sp 2 0 2

sp 3 4 (7) 0

sp 4 3 0


88

Pheidole sp 1 0 3

sp 2 3 0

sp 3 0 3


Solenopsis sp 1 0 3

sp 2 3 (3 5) 0

Wasmannia sp 1 3 0

Ponerinae



Pseudomyrmicinae


sp 2 3 0

sp 3 3 (9) 0

sp 4 0 3

sp 5 0 3

89





(grains found)


(grains found)

Aenictinae


Dolichoderinae




Ectatomminae


Formicinae


sp 2 3 3

sp 3 3 3




sp 2 1 3

sp 3 2 0

Nylanderia sp 1 3 3



90

Myrmicinae


sp 2 3 (32) 3


sp 2 3 3 (1 1 1)

Pheidole sp 1 3 3


Pyramica sp 1 3 0

Ponerinae


91

Figures



92







93

Concluding Remarks





















94























95







play within it

96




iii

Acknowledgments





























iv












v

Table of Contents

Acknowledgments iii

List of Tables vii



reproduction 1

Abstract 1

Introduction 2





References 24

Tables 39


Abstract 54

Introduction 55

Methods 57

Results 62

Discussion 63

Acknowledgements 66

References 68

Figures 73


vi

Abstract 75

Introduction 75

Methods 77

Results 78

Discussion 79

Acknowledgements 82

References 83

Tables 86

Figures 91



vii

List of Tables









viii

List of Figures






ant species93

1


reproduction




Abstract













2

Introduction














2009)









3























4
























5





















6
























7






















8























9












iv) Net effects










10
























11
























12























13
























14






















15





















16























17















a) Toxic nectar







18



















b) Floral volatiles




19













and Willmer 2012)











20



4 Future directions
















21























22
















Acknowledgements




23



Sigma Xi

24

References




65















25



71421ndash426












29418ndash429







26













298581ndash596







Botany 4517ndash8

27


333









319







528



28






272



27





652319ndash2327







29



892407ndash2413














Cambridge



30



Ecology 24221-227






7












31



22665ndash670











371323ndash31








32




54















411163ndash1168

33






812651ndash2661













34







10717234ndash9











45373-388



3096

35


Oikos 74265ndash272

















36






68959ndash967















37





















38












39

Tables






Acacia

drepanolobium

Crematogaster

nigriceps

Proportion

fruiting



removed



pollinia removal


40



Fruit set pollinia

removed

Negative for fruit

set neutral for

pollinia removal


1981 T


demerarae


1998


auropunctata



Schemske 1980


gelida


41







significant results

Blancafort and

Gόmez 2005


and others






Ness 2006

42



and Formica sp






Norment 1988


inflorescence



Gόmez et al

1996


decemarticulatus


2011


dohrni


2005

43



ovules setting

seed


1996

Leucospermum

conocarpodendron



indexrdquo

(combination of

number of seeds

fruits flowers

and seed weight)




visitation

Newman and

Thomson 2005

44


Melastoma

malabathricum

Oecophylla

smaragdina






2012

Metrosideros

polymorpha





fruit set

Junker et al

2010a


gelida


limited

Puterbaugh 1988

45



pusillus and others




set

Byk and Del

Claro 2010





Chamberlain and

Holland 2008

Polemonium

viscosum

F neorufibarbis

gelida


46


Polemonium

viscosum

F neorufibarbis

gelida



densities

Galen and Geib

2007 T


humile and others





to relocate

Lach 2007

Psychotria

limonensis



Altshuler 1999

47



albipes


competition

Hansen and

Muumlller 2009





Caballero et al

2013

Vaccinium

reticulatum



Bleil et al 2011



48










seed




49




japonicas



orchids

Sugiura et al 2006










50



longiseta


Jatropha curcas

Several

Tapinoma

melanocephalum

most common



and subsequently

confirmed as ant

pollination

Peakall et al 1987

51



Camponotus

micans most

common


Microtis parviflora

Iridomyrmex

gracilis





Naufraga balearica

Several

especially

Plagiolepis

pygmaea and

Lasius grandis




ants carried pollen


52



Paratrechina sp



orchids

Wang et al 2008


neorufibarbis

gelida








Hickman 1974

53




Several

especially

Formica

rufibarbis




Svensson 1985


longiseta



54







Abstract












55

Introduction























56






















seed set



57













Methods

i) Subjects








58


















unpublished data)





59






















60















b) Scent trials








61























62


















Results




63








the model

Discussion






female function








64








Souza et al 2008)

















65

























66













ants

Acknowledgements









67

68

References









71421-426










861401-1406


744

69









892407-2413









453





Society B 2762031-2036

70



7

















812651ndash2661





71




of Sciences 10717234-17239









6688-694












72






23841-851

73

Figures



74





nd to 4

th hours of the

trials

75


ants





Abstract











forests

Introduction



76

























77

Methods




















78







N ratios and













Results






79








Pachycondola sp1)

Discussion






N foods (eg









80



be more attractive





















81




N ratio





















82











Acknowledgements









83

References





426



29418ndash429













61519ndash525

84







Ecology 77489-499




Cambridge



Ecology 24221-227








New Jersey

85



86

Tables








Dolichoderinae

Azteca sp 1 3 0

sp 2 2 0

sp 3 0 2

sp 4 3 (1) 0

sp 5 3 (2) 0


sp 1 3 0

sp 2 3 1 (2)

sp 3 3 3

sp 4 0 2

Ecitoninae

Labidus sp 1 3 0

Formicinae

Camponotus sp 1 3 3

sp 2 3 (82) 1 (2)

sp 3 3 (3) 0

sp 4 0 2

87

sp 5 8 (11) 0

sp 6 4 (7 16 468) 0

sp 7 5 (12) 0

sp 8 2 (1) 0



sp 2 0 3


sp 2 3 0

Myrmicinae

Atta sp 1 3 0


placidus 3 (1 4 21) 0

sp 1 3 0

sp 2 1 0

sp 3 2 0


sp 2 3 (35) 0

sp 3 9 (7) 0

sp 4 2 0


sp 2 0 2

sp 3 4 (7) 0

sp 4 3 0


88

Pheidole sp 1 0 3

sp 2 3 0

sp 3 0 3


Solenopsis sp 1 0 3

sp 2 3 (3 5) 0

Wasmannia sp 1 3 0

Ponerinae



Pseudomyrmicinae


sp 2 3 0

sp 3 3 (9) 0

sp 4 0 3

sp 5 0 3

89





(grains found)


(grains found)

Aenictinae


Dolichoderinae




Ectatomminae


Formicinae


sp 2 3 3

sp 3 3 3




sp 2 1 3

sp 3 2 0

Nylanderia sp 1 3 3



90

Myrmicinae


sp 2 3 (32) 3


sp 2 3 3 (1 1 1)

Pheidole sp 1 3 3


Pyramica sp 1 3 0

Ponerinae


91

Figures



92







93

Concluding Remarks





















94























95







play within it

96




iv












v

Table of Contents

Acknowledgments iii

List of Tables vii



reproduction 1

Abstract 1

Introduction 2





References 24

Tables 39


Abstract 54

Introduction 55

Methods 57

Results 62

Discussion 63

Acknowledgements 66

References 68

Figures 73


vi

Abstract 75

Introduction 75

Methods 77

Results 78

Discussion 79

Acknowledgements 82

References 83

Tables 86

Figures 91



vii

List of Tables









viii

List of Figures






ant species93

1


reproduction




Abstract













2

Introduction














2009)









3























4
























5





















6
























7






















8























9












iv) Net effects










10
























11
























12























13
























14






















15





















16























17















a) Toxic nectar







18



















b) Floral volatiles




19













and Willmer 2012)











20



4 Future directions
















21























22
















Acknowledgements




23



Sigma Xi

24

References




65















25



71421ndash426












29418ndash429







26













298581ndash596







Botany 4517ndash8

27


333









319







528



28






272



27





652319ndash2327







29



892407ndash2413














Cambridge



30



Ecology 24221-227






7












31



22665ndash670











371323ndash31








32




54















411163ndash1168

33






812651ndash2661













34







10717234ndash9











45373-388



3096

35


Oikos 74265ndash272

















36






68959ndash967















37





















38












39

Tables






Acacia

drepanolobium

Crematogaster

nigriceps

Proportion

fruiting



removed



pollinia removal


40



Fruit set pollinia

removed

Negative for fruit

set neutral for

pollinia removal


1981 T


demerarae


1998


auropunctata



Schemske 1980


gelida


41







significant results

Blancafort and

Gόmez 2005


and others






Ness 2006

42



and Formica sp






Norment 1988


inflorescence



Gόmez et al

1996


decemarticulatus


2011


dohrni


2005

43



ovules setting

seed


1996

Leucospermum

conocarpodendron



indexrdquo

(combination of

number of seeds

fruits flowers

and seed weight)




visitation

Newman and

Thomson 2005

44


Melastoma

malabathricum

Oecophylla

smaragdina






2012

Metrosideros

polymorpha





fruit set

Junker et al

2010a


gelida


limited

Puterbaugh 1988

45



pusillus and others




set

Byk and Del

Claro 2010





Chamberlain and

Holland 2008

Polemonium

viscosum

F neorufibarbis

gelida


46


Polemonium

viscosum

F neorufibarbis

gelida



densities

Galen and Geib

2007 T


humile and others





to relocate

Lach 2007

Psychotria

limonensis



Altshuler 1999

47



albipes


competition

Hansen and

Muumlller 2009





Caballero et al

2013

Vaccinium

reticulatum



Bleil et al 2011



48










seed




49




japonicas



orchids

Sugiura et al 2006










50



longiseta


Jatropha curcas

Several

Tapinoma

melanocephalum

most common



and subsequently

confirmed as ant

pollination

Peakall et al 1987

51



Camponotus

micans most

common


Microtis parviflora

Iridomyrmex

gracilis





Naufraga balearica

Several

especially

Plagiolepis

pygmaea and

Lasius grandis




ants carried pollen


52



Paratrechina sp



orchids

Wang et al 2008


neorufibarbis

gelida








Hickman 1974

53




Several

especially

Formica

rufibarbis




Svensson 1985


longiseta



54







Abstract












55

Introduction























56






















seed set



57













Methods

i) Subjects








58


















unpublished data)





59






















60















b) Scent trials








61























62


















Results




63








the model

Discussion






female function








64








Souza et al 2008)

















65

























66













ants

Acknowledgements









67

68

References









71421-426










861401-1406


744

69









892407-2413









453





Society B 2762031-2036

70



7

















812651ndash2661





71




of Sciences 10717234-17239









6688-694












72






23841-851

73

Figures



74





nd to 4

th hours of the

trials

75


ants





Abstract











forests

Introduction



76

























77

Methods




















78







N ratios and













Results






79








Pachycondola sp1)

Discussion






N foods (eg









80



be more attractive





















81




N ratio





















82











Acknowledgements









83

References





426



29418ndash429













61519ndash525

84







Ecology 77489-499




Cambridge



Ecology 24221-227








New Jersey

85



86

Tables








Dolichoderinae

Azteca sp 1 3 0

sp 2 2 0

sp 3 0 2

sp 4 3 (1) 0

sp 5 3 (2) 0


sp 1 3 0

sp 2 3 1 (2)

sp 3 3 3

sp 4 0 2

Ecitoninae

Labidus sp 1 3 0

Formicinae

Camponotus sp 1 3 3

sp 2 3 (82) 1 (2)

sp 3 3 (3) 0

sp 4 0 2

87

sp 5 8 (11) 0

sp 6 4 (7 16 468) 0

sp 7 5 (12) 0

sp 8 2 (1) 0



sp 2 0 3


sp 2 3 0

Myrmicinae

Atta sp 1 3 0


placidus 3 (1 4 21) 0

sp 1 3 0

sp 2 1 0

sp 3 2 0


sp 2 3 (35) 0

sp 3 9 (7) 0

sp 4 2 0


sp 2 0 2

sp 3 4 (7) 0

sp 4 3 0


88

Pheidole sp 1 0 3

sp 2 3 0

sp 3 0 3


Solenopsis sp 1 0 3

sp 2 3 (3 5) 0

Wasmannia sp 1 3 0

Ponerinae



Pseudomyrmicinae


sp 2 3 0

sp 3 3 (9) 0

sp 4 0 3

sp 5 0 3

89





(grains found)


(grains found)

Aenictinae


Dolichoderinae




Ectatomminae


Formicinae


sp 2 3 3

sp 3 3 3




sp 2 1 3

sp 3 2 0

Nylanderia sp 1 3 3



90

Myrmicinae


sp 2 3 (32) 3


sp 2 3 3 (1 1 1)

Pheidole sp 1 3 3


Pyramica sp 1 3 0

Ponerinae


91

Figures



92







93

Concluding Remarks





















94























95







play within it

96




v

Table of Contents

Acknowledgments iii

List of Tables vii



reproduction 1

Abstract 1

Introduction 2





References 24

Tables 39


Abstract 54

Introduction 55

Methods 57

Results 62

Discussion 63

Acknowledgements 66

References 68

Figures 73


vi

Abstract 75

Introduction 75

Methods 77

Results 78

Discussion 79

Acknowledgements 82

References 83

Tables 86

Figures 91



vii

List of Tables









viii

List of Figures






ant species93

1


reproduction




Abstract













2

Introduction














2009)









3























4
























5





















6
























7






















8























9












iv) Net effects










10
























11
























12























13
























14






















15





















16























17















a) Toxic nectar







18



















b) Floral volatiles




19













and Willmer 2012)











20



4 Future directions
















21























22
















Acknowledgements




23



Sigma Xi

24

References




65















25



71421ndash426












29418ndash429







26













298581ndash596







Botany 4517ndash8

27


333









319







528



28






272



27





652319ndash2327







29



892407ndash2413














Cambridge



30



Ecology 24221-227






7












31



22665ndash670











371323ndash31








32




54















411163ndash1168

33






812651ndash2661













34







10717234ndash9











45373-388



3096

35


Oikos 74265ndash272

















36






68959ndash967















37





















38












39

Tables






Acacia

drepanolobium

Crematogaster

nigriceps

Proportion

fruiting



removed



pollinia removal


40



Fruit set pollinia

removed

Negative for fruit

set neutral for

pollinia removal


1981 T


demerarae


1998


auropunctata



Schemske 1980


gelida


41







significant results

Blancafort and

Gόmez 2005


and others






Ness 2006

42



and Formica sp






Norment 1988


inflorescence



Gόmez et al

1996


decemarticulatus


2011


dohrni


2005

43



ovules setting

seed


1996

Leucospermum

conocarpodendron



indexrdquo

(combination of

number of seeds

fruits flowers

and seed weight)




visitation

Newman and

Thomson 2005

44


Melastoma

malabathricum

Oecophylla

smaragdina






2012

Metrosideros

polymorpha





fruit set

Junker et al

2010a


gelida


limited

Puterbaugh 1988

45



pusillus and others




set

Byk and Del

Claro 2010





Chamberlain and

Holland 2008

Polemonium

viscosum

F neorufibarbis

gelida


46


Polemonium

viscosum

F neorufibarbis

gelida



densities

Galen and Geib

2007 T


humile and others





to relocate

Lach 2007

Psychotria

limonensis



Altshuler 1999

47



albipes


competition

Hansen and

Muumlller 2009





Caballero et al

2013

Vaccinium

reticulatum



Bleil et al 2011



48










seed




49




japonicas



orchids

Sugiura et al 2006










50



longiseta


Jatropha curcas

Several

Tapinoma

melanocephalum

most common



and subsequently

confirmed as ant

pollination

Peakall et al 1987

51



Camponotus

micans most

common


Microtis parviflora

Iridomyrmex

gracilis





Naufraga balearica

Several

especially

Plagiolepis

pygmaea and

Lasius grandis




ants carried pollen


52



Paratrechina sp



orchids

Wang et al 2008


neorufibarbis

gelida








Hickman 1974

53




Several

especially

Formica

rufibarbis




Svensson 1985


longiseta



54







Abstract












55

Introduction























56






















seed set



57













Methods

i) Subjects








58


















unpublished data)





59






















60















b) Scent trials








61























62


















Results




63








the model

Discussion






female function








64








Souza et al 2008)

















65

























66













ants

Acknowledgements









67

68

References









71421-426










861401-1406


744

69









892407-2413









453





Society B 2762031-2036

70



7

















812651ndash2661





71




of Sciences 10717234-17239









6688-694












72






23841-851

73

Figures



74





nd to 4

th hours of the

trials

75


ants





Abstract











forests

Introduction



76

























77

Methods




















78







N ratios and













Results






79








Pachycondola sp1)

Discussion






N foods (eg









80



be more attractive





















81




N ratio





















82











Acknowledgements









83

References





426



29418ndash429













61519ndash525

84







Ecology 77489-499




Cambridge



Ecology 24221-227








New Jersey

85



86

Tables








Dolichoderinae

Azteca sp 1 3 0

sp 2 2 0

sp 3 0 2

sp 4 3 (1) 0

sp 5 3 (2) 0


sp 1 3 0

sp 2 3 1 (2)

sp 3 3 3

sp 4 0 2

Ecitoninae

Labidus sp 1 3 0

Formicinae

Camponotus sp 1 3 3

sp 2 3 (82) 1 (2)

sp 3 3 (3) 0

sp 4 0 2

87

sp 5 8 (11) 0

sp 6 4 (7 16 468) 0

sp 7 5 (12) 0

sp 8 2 (1) 0



sp 2 0 3


sp 2 3 0

Myrmicinae

Atta sp 1 3 0


placidus 3 (1 4 21) 0

sp 1 3 0

sp 2 1 0

sp 3 2 0


sp 2 3 (35) 0

sp 3 9 (7) 0

sp 4 2 0


sp 2 0 2

sp 3 4 (7) 0

sp 4 3 0


88

Pheidole sp 1 0 3

sp 2 3 0

sp 3 0 3


Solenopsis sp 1 0 3

sp 2 3 (3 5) 0

Wasmannia sp 1 3 0

Ponerinae



Pseudomyrmicinae


sp 2 3 0

sp 3 3 (9) 0

sp 4 0 3

sp 5 0 3

89





(grains found)


(grains found)

Aenictinae


Dolichoderinae




Ectatomminae


Formicinae


sp 2 3 3

sp 3 3 3




sp 2 1 3

sp 3 2 0

Nylanderia sp 1 3 3



90

Myrmicinae


sp 2 3 (32) 3


sp 2 3 3 (1 1 1)

Pheidole sp 1 3 3


Pyramica sp 1 3 0

Ponerinae


91

Figures



92







93

Concluding Remarks





















94























95







play within it

96




vi

Abstract 75

Introduction 75

Methods 77

Results 78

Discussion 79

Acknowledgements 82

References 83

Tables 86

Figures 91



vii

List of Tables









viii

List of Figures






ant species93

1


reproduction




Abstract













2

Introduction














2009)









3























4
























5





















6
























7






















8























9












iv) Net effects










10
























11
























12























13
























14






















15





















16























17















a) Toxic nectar







18



















b) Floral volatiles




19













and Willmer 2012)











20



4 Future directions
















21























22
















Acknowledgements




23



Sigma Xi

24

References




65















25



71421ndash426












29418ndash429







26













298581ndash596







Botany 4517ndash8

27


333









319







528



28






272



27





652319ndash2327







29



892407ndash2413














Cambridge



30



Ecology 24221-227






7












31



22665ndash670











371323ndash31








32




54















411163ndash1168

33






812651ndash2661













34







10717234ndash9











45373-388



3096

35


Oikos 74265ndash272

















36






68959ndash967















37





















38












39

Tables






Acacia

drepanolobium

Crematogaster

nigriceps

Proportion

fruiting



removed



pollinia removal


40



Fruit set pollinia

removed

Negative for fruit

set neutral for

pollinia removal


1981 T


demerarae


1998


auropunctata



Schemske 1980


gelida


41







significant results

Blancafort and

Gόmez 2005


and others






Ness 2006

42



and Formica sp






Norment 1988


inflorescence



Gόmez et al

1996


decemarticulatus


2011


dohrni


2005

43



ovules setting

seed


1996

Leucospermum

conocarpodendron



indexrdquo

(combination of

number of seeds

fruits flowers

and seed weight)




visitation

Newman and

Thomson 2005

44


Melastoma

malabathricum

Oecophylla

smaragdina






2012

Metrosideros

polymorpha





fruit set

Junker et al

2010a


gelida


limited

Puterbaugh 1988

45



pusillus and others




set

Byk and Del

Claro 2010





Chamberlain and

Holland 2008

Polemonium

viscosum

F neorufibarbis

gelida


46


Polemonium

viscosum

F neorufibarbis

gelida



densities

Galen and Geib

2007 T


humile and others





to relocate

Lach 2007

Psychotria

limonensis



Altshuler 1999

47



albipes


competition

Hansen and

Muumlller 2009





Caballero et al

2013

Vaccinium

reticulatum



Bleil et al 2011



48










seed




49




japonicas



orchids

Sugiura et al 2006










50



longiseta


Jatropha curcas

Several

Tapinoma

melanocephalum

most common



and subsequently

confirmed as ant

pollination

Peakall et al 1987

51



Camponotus

micans most

common


Microtis parviflora

Iridomyrmex

gracilis





Naufraga balearica

Several

especially

Plagiolepis

pygmaea and

Lasius grandis




ants carried pollen


52



Paratrechina sp



orchids

Wang et al 2008


neorufibarbis

gelida








Hickman 1974

53




Several

especially

Formica

rufibarbis




Svensson 1985


longiseta



54







Abstract












55

Introduction























56






















seed set



57













Methods

i) Subjects








58


















unpublished data)





59






















60















b) Scent trials








61























62


















Results




63








the model

Discussion






female function








64








Souza et al 2008)

















65

























66













ants

Acknowledgements









67

68

References









71421-426










861401-1406


744

69









892407-2413









453





Society B 2762031-2036

70



7

















812651ndash2661





71




of Sciences 10717234-17239









6688-694












72






23841-851

73

Figures



74





nd to 4

th hours of the

trials

75


ants





Abstract











forests

Introduction



76

























77

Methods




















78







N ratios and













Results






79








Pachycondola sp1)

Discussion






N foods (eg









80



be more attractive





















81




N ratio





















82











Acknowledgements









83

References





426



29418ndash429













61519ndash525

84







Ecology 77489-499




Cambridge



Ecology 24221-227








New Jersey

85



86

Tables








Dolichoderinae

Azteca sp 1 3 0

sp 2 2 0

sp 3 0 2

sp 4 3 (1) 0

sp 5 3 (2) 0


sp 1 3 0

sp 2 3 1 (2)

sp 3 3 3

sp 4 0 2

Ecitoninae

Labidus sp 1 3 0

Formicinae

Camponotus sp 1 3 3

sp 2 3 (82) 1 (2)

sp 3 3 (3) 0

sp 4 0 2

87

sp 5 8 (11) 0

sp 6 4 (7 16 468) 0

sp 7 5 (12) 0

sp 8 2 (1) 0



sp 2 0 3


sp 2 3 0

Myrmicinae

Atta sp 1 3 0


placidus 3 (1 4 21) 0

sp 1 3 0

sp 2 1 0

sp 3 2 0


sp 2 3 (35) 0

sp 3 9 (7) 0

sp 4 2 0


sp 2 0 2

sp 3 4 (7) 0

sp 4 3 0


88

Pheidole sp 1 0 3

sp 2 3 0

sp 3 0 3


Solenopsis sp 1 0 3

sp 2 3 (3 5) 0

Wasmannia sp 1 3 0

Ponerinae



Pseudomyrmicinae


sp 2 3 0

sp 3 3 (9) 0

sp 4 0 3

sp 5 0 3

89





(grains found)


(grains found)

Aenictinae


Dolichoderinae




Ectatomminae


Formicinae


sp 2 3 3

sp 3 3 3




sp 2 1 3

sp 3 2 0

Nylanderia sp 1 3 3



90

Myrmicinae


sp 2 3 (32) 3


sp 2 3 3 (1 1 1)

Pheidole sp 1 3 3


Pyramica sp 1 3 0

Ponerinae


91

Figures



92







93

Concluding Remarks





















94























95







play within it

96




vii

List of Tables









viii

List of Figures






ant species93

1


reproduction




Abstract













2

Introduction














2009)









3























4
























5





















6
























7






















8























9












iv) Net effects










10
























11
























12























13
























14






















15





















16























17















a) Toxic nectar







18



















b) Floral volatiles




19













and Willmer 2012)











20



4 Future directions
















21























22
















Acknowledgements




23



Sigma Xi

24

References




65















25



71421ndash426












29418ndash429







26













298581ndash596







Botany 4517ndash8

27


333









319







528



28






272



27





652319ndash2327







29



892407ndash2413














Cambridge



30



Ecology 24221-227






7












31



22665ndash670











371323ndash31








32




54















411163ndash1168

33






812651ndash2661













34







10717234ndash9











45373-388



3096

35


Oikos 74265ndash272

















36






68959ndash967















37





















38












39

Tables






Acacia

drepanolobium

Crematogaster

nigriceps

Proportion

fruiting



removed



pollinia removal


40



Fruit set pollinia

removed

Negative for fruit

set neutral for

pollinia removal


1981 T


demerarae


1998


auropunctata



Schemske 1980


gelida


41







significant results

Blancafort and

Gόmez 2005


and others






Ness 2006

42



and Formica sp






Norment 1988


inflorescence



Gόmez et al

1996


decemarticulatus


2011


dohrni


2005

43



ovules setting

seed


1996

Leucospermum

conocarpodendron



indexrdquo

(combination of

number of seeds

fruits flowers

and seed weight)




visitation

Newman and

Thomson 2005

44


Melastoma

malabathricum

Oecophylla

smaragdina






2012

Metrosideros

polymorpha





fruit set

Junker et al

2010a


gelida


limited

Puterbaugh 1988

45



pusillus and others




set

Byk and Del

Claro 2010





Chamberlain and

Holland 2008

Polemonium

viscosum

F neorufibarbis

gelida


46


Polemonium

viscosum

F neorufibarbis

gelida



densities

Galen and Geib

2007 T


humile and others





to relocate

Lach 2007

Psychotria

limonensis



Altshuler 1999

47



albipes


competition

Hansen and

Muumlller 2009





Caballero et al

2013

Vaccinium

reticulatum



Bleil et al 2011



48










seed




49




japonicas



orchids

Sugiura et al 2006










50



longiseta


Jatropha curcas

Several

Tapinoma

melanocephalum

most common



and subsequently

confirmed as ant

pollination

Peakall et al 1987

51



Camponotus

micans most

common


Microtis parviflora

Iridomyrmex

gracilis





Naufraga balearica

Several

especially

Plagiolepis

pygmaea and

Lasius grandis




ants carried pollen


52



Paratrechina sp



orchids

Wang et al 2008


neorufibarbis

gelida








Hickman 1974

53




Several

especially

Formica

rufibarbis




Svensson 1985


longiseta



54







Abstract












55

Introduction























56






















seed set



57













Methods

i) Subjects








58


















unpublished data)





59






















60















b) Scent trials








61























62


















Results




63








the model

Discussion






female function








64








Souza et al 2008)

















65

























66













ants

Acknowledgements









67

68

References









71421-426










861401-1406


744

69









892407-2413









453





Society B 2762031-2036

70



7

















812651ndash2661





71




of Sciences 10717234-17239









6688-694












72






23841-851

73

Figures



74





nd to 4

th hours of the

trials

75


ants





Abstract











forests

Introduction



76

























77

Methods




















78







N ratios and













Results






79








Pachycondola sp1)

Discussion






N foods (eg









80



be more attractive





















81




N ratio





















82











Acknowledgements









83

References





426



29418ndash429













61519ndash525

84







Ecology 77489-499




Cambridge



Ecology 24221-227








New Jersey

85



86

Tables








Dolichoderinae

Azteca sp 1 3 0

sp 2 2 0

sp 3 0 2

sp 4 3 (1) 0

sp 5 3 (2) 0


sp 1 3 0

sp 2 3 1 (2)

sp 3 3 3

sp 4 0 2

Ecitoninae

Labidus sp 1 3 0

Formicinae

Camponotus sp 1 3 3

sp 2 3 (82) 1 (2)

sp 3 3 (3) 0

sp 4 0 2

87

sp 5 8 (11) 0

sp 6 4 (7 16 468) 0

sp 7 5 (12) 0

sp 8 2 (1) 0



sp 2 0 3


sp 2 3 0

Myrmicinae

Atta sp 1 3 0


placidus 3 (1 4 21) 0

sp 1 3 0

sp 2 1 0

sp 3 2 0


sp 2 3 (35) 0

sp 3 9 (7) 0

sp 4 2 0


sp 2 0 2

sp 3 4 (7) 0

sp 4 3 0


88

Pheidole sp 1 0 3

sp 2 3 0

sp 3 0 3


Solenopsis sp 1 0 3

sp 2 3 (3 5) 0

Wasmannia sp 1 3 0

Ponerinae



Pseudomyrmicinae


sp 2 3 0

sp 3 3 (9) 0

sp 4 0 3

sp 5 0 3

89





(grains found)


(grains found)

Aenictinae


Dolichoderinae




Ectatomminae


Formicinae


sp 2 3 3

sp 3 3 3




sp 2 1 3

sp 3 2 0

Nylanderia sp 1 3 3



90

Myrmicinae


sp 2 3 (32) 3


sp 2 3 3 (1 1 1)

Pheidole sp 1 3 3


Pyramica sp 1 3 0

Ponerinae


91

Figures



92







93

Concluding Remarks





















94























95







play within it

96




viii

List of Figures






ant species93

1


reproduction




Abstract













2

Introduction














2009)









3























4
























5





















6
























7






















8























9












iv) Net effects










10
























11
























12























13
























14






















15





















16























17















a) Toxic nectar







18



















b) Floral volatiles




19













and Willmer 2012)











20



4 Future directions
















21























22
















Acknowledgements




23



Sigma Xi

24

References




65















25



71421ndash426












29418ndash429







26













298581ndash596







Botany 4517ndash8

27


333









319







528



28






272



27





652319ndash2327







29



892407ndash2413














Cambridge



30



Ecology 24221-227






7












31



22665ndash670











371323ndash31








32




54















411163ndash1168

33






812651ndash2661













34







10717234ndash9











45373-388



3096

35


Oikos 74265ndash272

















36






68959ndash967















37





















38












39

Tables






Acacia

drepanolobium

Crematogaster

nigriceps

Proportion

fruiting



removed



pollinia removal


40



Fruit set pollinia

removed

Negative for fruit

set neutral for

pollinia removal


1981 T


demerarae


1998


auropunctata



Schemske 1980


gelida


41







significant results

Blancafort and

Gόmez 2005


and others






Ness 2006

42



and Formica sp






Norment 1988


inflorescence



Gόmez et al

1996


decemarticulatus


2011


dohrni


2005

43



ovules setting

seed


1996

Leucospermum

conocarpodendron



indexrdquo

(combination of

number of seeds

fruits flowers

and seed weight)




visitation

Newman and

Thomson 2005

44


Melastoma

malabathricum

Oecophylla

smaragdina






2012

Metrosideros

polymorpha





fruit set

Junker et al

2010a


gelida


limited

Puterbaugh 1988

45



pusillus and others




set

Byk and Del

Claro 2010





Chamberlain and

Holland 2008

Polemonium

viscosum

F neorufibarbis

gelida


46


Polemonium

viscosum

F neorufibarbis

gelida



densities

Galen and Geib

2007 T


humile and others





to relocate

Lach 2007

Psychotria

limonensis



Altshuler 1999

47



albipes


competition

Hansen and

Muumlller 2009





Caballero et al

2013

Vaccinium

reticulatum



Bleil et al 2011



48










seed




49




japonicas



orchids

Sugiura et al 2006










50



longiseta


Jatropha curcas

Several

Tapinoma

melanocephalum

most common



and subsequently

confirmed as ant

pollination

Peakall et al 1987

51



Camponotus

micans most

common


Microtis parviflora

Iridomyrmex

gracilis





Naufraga balearica

Several

especially

Plagiolepis

pygmaea and

Lasius grandis




ants carried pollen


52



Paratrechina sp



orchids

Wang et al 2008


neorufibarbis

gelida








Hickman 1974

53




Several

especially

Formica

rufibarbis




Svensson 1985


longiseta



54







Abstract












55

Introduction























56






















seed set



57













Methods

i) Subjects








58


















unpublished data)





59






















60















b) Scent trials








61























62


















Results




63








the model

Discussion






female function








64








Souza et al 2008)

















65

























66













ants

Acknowledgements









67

68

References









71421-426










861401-1406


744

69









892407-2413









453





Society B 2762031-2036

70



7

















812651ndash2661





71




of Sciences 10717234-17239









6688-694












72






23841-851

73

Figures



74





nd to 4

th hours of the

trials

75


ants





Abstract











forests

Introduction



76

























77

Methods




















78







N ratios and













Results






79








Pachycondola sp1)

Discussion






N foods (eg









80



be more attractive





















81




N ratio





















82











Acknowledgements









83

References





426



29418ndash429













61519ndash525

84







Ecology 77489-499




Cambridge



Ecology 24221-227








New Jersey

85



86

Tables








Dolichoderinae

Azteca sp 1 3 0

sp 2 2 0

sp 3 0 2

sp 4 3 (1) 0

sp 5 3 (2) 0


sp 1 3 0

sp 2 3 1 (2)

sp 3 3 3

sp 4 0 2

Ecitoninae

Labidus sp 1 3 0

Formicinae

Camponotus sp 1 3 3

sp 2 3 (82) 1 (2)

sp 3 3 (3) 0

sp 4 0 2

87

sp 5 8 (11) 0

sp 6 4 (7 16 468) 0

sp 7 5 (12) 0

sp 8 2 (1) 0



sp 2 0 3


sp 2 3 0

Myrmicinae

Atta sp 1 3 0


placidus 3 (1 4 21) 0

sp 1 3 0

sp 2 1 0

sp 3 2 0


sp 2 3 (35) 0

sp 3 9 (7) 0

sp 4 2 0


sp 2 0 2

sp 3 4 (7) 0

sp 4 3 0


88

Pheidole sp 1 0 3

sp 2 3 0

sp 3 0 3


Solenopsis sp 1 0 3

sp 2 3 (3 5) 0

Wasmannia sp 1 3 0

Ponerinae



Pseudomyrmicinae


sp 2 3 0

sp 3 3 (9) 0

sp 4 0 3

sp 5 0 3

89





(grains found)


(grains found)

Aenictinae


Dolichoderinae




Ectatomminae


Formicinae


sp 2 3 3

sp 3 3 3




sp 2 1 3

sp 3 2 0

Nylanderia sp 1 3 3



90

Myrmicinae


sp 2 3 (32) 3


sp 2 3 3 (1 1 1)

Pheidole sp 1 3 3


Pyramica sp 1 3 0

Ponerinae


91

Figures



92







93

Concluding Remarks





















94























95







play within it

96




1


reproduction




Abstract













2

Introduction














2009)









3























4
























5





















6
























7






















8























9












iv) Net effects










10
























11
























12























13
























14






















15





















16























17















a) Toxic nectar







18



















b) Floral volatiles




19













and Willmer 2012)











20



4 Future directions
















21























22
















Acknowledgements




23



Sigma Xi

24

References




65















25



71421ndash426












29418ndash429







26













298581ndash596







Botany 4517ndash8

27


333









319







528



28






272



27





652319ndash2327







29



892407ndash2413














Cambridge



30



Ecology 24221-227






7












31



22665ndash670











371323ndash31








32




54















411163ndash1168

33






812651ndash2661













34







10717234ndash9











45373-388



3096

35


Oikos 74265ndash272

















36






68959ndash967















37





















38












39

Tables






Acacia

drepanolobium

Crematogaster

nigriceps

Proportion

fruiting



removed



pollinia removal


40



Fruit set pollinia

removed

Negative for fruit

set neutral for

pollinia removal


1981 T


demerarae


1998


auropunctata



Schemske 1980


gelida


41







significant results

Blancafort and

Gόmez 2005


and others






Ness 2006

42



and Formica sp






Norment 1988


inflorescence



Gόmez et al

1996


decemarticulatus


2011


dohrni


2005

43



ovules setting

seed


1996

Leucospermum

conocarpodendron



indexrdquo

(combination of

number of seeds

fruits flowers

and seed weight)




visitation

Newman and

Thomson 2005

44


Melastoma

malabathricum

Oecophylla

smaragdina






2012

Metrosideros

polymorpha





fruit set

Junker et al

2010a


gelida


limited

Puterbaugh 1988

45



pusillus and others




set

Byk and Del

Claro 2010





Chamberlain and

Holland 2008

Polemonium

viscosum

F neorufibarbis

gelida


46


Polemonium

viscosum

F neorufibarbis

gelida



densities

Galen and Geib

2007 T


humile and others





to relocate

Lach 2007

Psychotria

limonensis



Altshuler 1999

47



albipes


competition

Hansen and

Muumlller 2009





Caballero et al

2013

Vaccinium

reticulatum



Bleil et al 2011



48










seed




49




japonicas



orchids

Sugiura et al 2006










50



longiseta


Jatropha curcas

Several

Tapinoma

melanocephalum

most common



and subsequently

confirmed as ant

pollination

Peakall et al 1987

51



Camponotus

micans most

common


Microtis parviflora

Iridomyrmex

gracilis





Naufraga balearica

Several

especially

Plagiolepis

pygmaea and

Lasius grandis




ants carried pollen


52



Paratrechina sp



orchids

Wang et al 2008


neorufibarbis

gelida








Hickman 1974

53




Several

especially

Formica

rufibarbis




Svensson 1985


longiseta



54







Abstract












55

Introduction























56






















seed set



57













Methods

i) Subjects








58


















unpublished data)





59






















60















b) Scent trials








61























62


















Results




63








the model

Discussion






female function








64








Souza et al 2008)

















65

























66













ants

Acknowledgements









67

68

References









71421-426










861401-1406


744

69









892407-2413









453





Society B 2762031-2036

70



7

















812651ndash2661





71




of Sciences 10717234-17239









6688-694












72






23841-851

73

Figures



74





nd to 4

th hours of the

trials

75


ants





Abstract











forests

Introduction



76

























77

Methods




















78







N ratios and













Results






79








Pachycondola sp1)

Discussion






N foods (eg









80



be more attractive





















81




N ratio





















82











Acknowledgements









83

References





426



29418ndash429













61519ndash525

84







Ecology 77489-499




Cambridge



Ecology 24221-227








New Jersey

85



86

Tables








Dolichoderinae

Azteca sp 1 3 0

sp 2 2 0

sp 3 0 2

sp 4 3 (1) 0

sp 5 3 (2) 0


sp 1 3 0

sp 2 3 1 (2)

sp 3 3 3

sp 4 0 2

Ecitoninae

Labidus sp 1 3 0

Formicinae

Camponotus sp 1 3 3

sp 2 3 (82) 1 (2)

sp 3 3 (3) 0

sp 4 0 2

87

sp 5 8 (11) 0

sp 6 4 (7 16 468) 0

sp 7 5 (12) 0

sp 8 2 (1) 0



sp 2 0 3


sp 2 3 0

Myrmicinae

Atta sp 1 3 0


placidus 3 (1 4 21) 0

sp 1 3 0

sp 2 1 0

sp 3 2 0


sp 2 3 (35) 0

sp 3 9 (7) 0

sp 4 2 0


sp 2 0 2

sp 3 4 (7) 0

sp 4 3 0


88

Pheidole sp 1 0 3

sp 2 3 0

sp 3 0 3


Solenopsis sp 1 0 3

sp 2 3 (3 5) 0

Wasmannia sp 1 3 0

Ponerinae



Pseudomyrmicinae


sp 2 3 0

sp 3 3 (9) 0

sp 4 0 3

sp 5 0 3

89





(grains found)


(grains found)

Aenictinae


Dolichoderinae




Ectatomminae


Formicinae


sp 2 3 3

sp 3 3 3




sp 2 1 3

sp 3 2 0

Nylanderia sp 1 3 3



90

Myrmicinae


sp 2 3 (32) 3


sp 2 3 3 (1 1 1)

Pheidole sp 1 3 3


Pyramica sp 1 3 0

Ponerinae


91

Figures



92







93

Concluding Remarks





















94























95







play within it

96




2

Introduction














2009)









3























4
























5





















6
























7






















8























9












iv) Net effects










10
























11
























12























13
























14






















15





















16























17















a) Toxic nectar







18



















b) Floral volatiles




19













and Willmer 2012)











20



4 Future directions
















21























22
















Acknowledgements




23



Sigma Xi

24

References




65















25



71421ndash426












29418ndash429







26













298581ndash596







Botany 4517ndash8

27


333









319







528



28






272



27





652319ndash2327







29



892407ndash2413














Cambridge



30



Ecology 24221-227






7












31



22665ndash670











371323ndash31








32




54















411163ndash1168

33






812651ndash2661













34







10717234ndash9











45373-388



3096

35


Oikos 74265ndash272

















36






68959ndash967















37





















38












39

Tables






Acacia

drepanolobium

Crematogaster

nigriceps

Proportion

fruiting



removed



pollinia removal


40



Fruit set pollinia

removed

Negative for fruit

set neutral for

pollinia removal


1981 T


demerarae


1998


auropunctata



Schemske 1980


gelida


41







significant results

Blancafort and

Gόmez 2005


and others






Ness 2006

42



and Formica sp






Norment 1988


inflorescence



Gόmez et al

1996


decemarticulatus


2011


dohrni


2005

43



ovules setting

seed


1996

Leucospermum

conocarpodendron



indexrdquo

(combination of

number of seeds

fruits flowers

and seed weight)




visitation

Newman and

Thomson 2005

44


Melastoma

malabathricum

Oecophylla

smaragdina






2012

Metrosideros

polymorpha





fruit set

Junker et al

2010a


gelida


limited

Puterbaugh 1988

45



pusillus and others




set

Byk and Del

Claro 2010





Chamberlain and

Holland 2008

Polemonium

viscosum

F neorufibarbis

gelida


46


Polemonium

viscosum

F neorufibarbis

gelida



densities

Galen and Geib

2007 T


humile and others





to relocate

Lach 2007

Psychotria

limonensis



Altshuler 1999

47



albipes


competition

Hansen and

Muumlller 2009





Caballero et al

2013

Vaccinium

reticulatum



Bleil et al 2011



48










seed




49




japonicas



orchids

Sugiura et al 2006










50



longiseta


Jatropha curcas

Several

Tapinoma

melanocephalum

most common



and subsequently

confirmed as ant

pollination

Peakall et al 1987

51



Camponotus

micans most

common


Microtis parviflora

Iridomyrmex

gracilis





Naufraga balearica

Several

especially

Plagiolepis

pygmaea and

Lasius grandis




ants carried pollen


52



Paratrechina sp



orchids

Wang et al 2008


neorufibarbis

gelida








Hickman 1974

53




Several

especially

Formica

rufibarbis




Svensson 1985


longiseta



54







Abstract












55

Introduction























56






















seed set



57













Methods

i) Subjects








58


















unpublished data)





59






















60















b) Scent trials








61























62


















Results




63








the model

Discussion






female function








64








Souza et al 2008)

















65

























66













ants

Acknowledgements









67

68

References









71421-426










861401-1406


744

69









892407-2413









453





Society B 2762031-2036

70



7

















812651ndash2661





71




of Sciences 10717234-17239









6688-694












72






23841-851

73

Figures



74





nd to 4

th hours of the

trials

75


ants





Abstract











forests

Introduction



76

























77

Methods




















78







N ratios and













Results






79








Pachycondola sp1)

Discussion






N foods (eg









80



be more attractive





















81




N ratio





















82











Acknowledgements









83

References





426



29418ndash429













61519ndash525

84







Ecology 77489-499




Cambridge



Ecology 24221-227








New Jersey

85



86

Tables








Dolichoderinae

Azteca sp 1 3 0

sp 2 2 0

sp 3 0 2

sp 4 3 (1) 0

sp 5 3 (2) 0


sp 1 3 0

sp 2 3 1 (2)

sp 3 3 3

sp 4 0 2

Ecitoninae

Labidus sp 1 3 0

Formicinae

Camponotus sp 1 3 3

sp 2 3 (82) 1 (2)

sp 3 3 (3) 0

sp 4 0 2

87

sp 5 8 (11) 0

sp 6 4 (7 16 468) 0

sp 7 5 (12) 0

sp 8 2 (1) 0



sp 2 0 3


sp 2 3 0

Myrmicinae

Atta sp 1 3 0


placidus 3 (1 4 21) 0

sp 1 3 0

sp 2 1 0

sp 3 2 0


sp 2 3 (35) 0

sp 3 9 (7) 0

sp 4 2 0


sp 2 0 2

sp 3 4 (7) 0

sp 4 3 0


88

Pheidole sp 1 0 3

sp 2 3 0

sp 3 0 3


Solenopsis sp 1 0 3

sp 2 3 (3 5) 0

Wasmannia sp 1 3 0

Ponerinae



Pseudomyrmicinae


sp 2 3 0

sp 3 3 (9) 0

sp 4 0 3

sp 5 0 3

89





(grains found)


(grains found)

Aenictinae


Dolichoderinae




Ectatomminae


Formicinae


sp 2 3 3

sp 3 3 3




sp 2 1 3

sp 3 2 0

Nylanderia sp 1 3 3



90

Myrmicinae


sp 2 3 (32) 3


sp 2 3 3 (1 1 1)

Pheidole sp 1 3 3


Pyramica sp 1 3 0

Ponerinae


91

Figures



92







93

Concluding Remarks





















94























95







play within it

96




3























4
























5





















6
























7






















8























9












iv) Net effects










10
























11
























12























13
























14






















15





















16























17















a) Toxic nectar







18



















b) Floral volatiles




19













and Willmer 2012)











20



4 Future directions
















21























22
















Acknowledgements




23



Sigma Xi

24

References




65















25



71421ndash426












29418ndash429







26













298581ndash596







Botany 4517ndash8

27


333









319







528



28






272



27





652319ndash2327







29



892407ndash2413














Cambridge



30



Ecology 24221-227






7












31



22665ndash670











371323ndash31








32




54















411163ndash1168

33






812651ndash2661













34







10717234ndash9











45373-388



3096

35


Oikos 74265ndash272

















36






68959ndash967















37





















38












39

Tables






Acacia

drepanolobium

Crematogaster

nigriceps

Proportion

fruiting



removed



pollinia removal


40



Fruit set pollinia

removed

Negative for fruit

set neutral for

pollinia removal


1981 T


demerarae


1998


auropunctata



Schemske 1980


gelida


41







significant results

Blancafort and

Gόmez 2005


and others






Ness 2006

42



and Formica sp






Norment 1988


inflorescence



Gόmez et al

1996


decemarticulatus


2011


dohrni


2005

43



ovules setting

seed


1996

Leucospermum

conocarpodendron



indexrdquo

(combination of

number of seeds

fruits flowers

and seed weight)




visitation

Newman and

Thomson 2005

44


Melastoma

malabathricum

Oecophylla

smaragdina






2012

Metrosideros

polymorpha





fruit set

Junker et al

2010a


gelida


limited

Puterbaugh 1988

45



pusillus and others




set

Byk and Del

Claro 2010





Chamberlain and

Holland 2008

Polemonium

viscosum

F neorufibarbis

gelida


46


Polemonium

viscosum

F neorufibarbis

gelida



densities

Galen and Geib

2007 T


humile and others





to relocate

Lach 2007

Psychotria

limonensis



Altshuler 1999

47



albipes


competition

Hansen and

Muumlller 2009





Caballero et al

2013

Vaccinium

reticulatum



Bleil et al 2011



48










seed




49




japonicas



orchids

Sugiura et al 2006










50



longiseta


Jatropha curcas

Several

Tapinoma

melanocephalum

most common



and subsequently

confirmed as ant

pollination

Peakall et al 1987

51



Camponotus

micans most

common


Microtis parviflora

Iridomyrmex

gracilis





Naufraga balearica

Several

especially

Plagiolepis

pygmaea and

Lasius grandis




ants carried pollen


52



Paratrechina sp



orchids

Wang et al 2008


neorufibarbis

gelida








Hickman 1974

53




Several

especially

Formica

rufibarbis




Svensson 1985


longiseta



54







Abstract












55

Introduction























56






















seed set



57













Methods

i) Subjects








58


















unpublished data)





59






















60















b) Scent trials








61























62


















Results




63








the model

Discussion






female function








64








Souza et al 2008)

















65

























66













ants

Acknowledgements









67

68

References









71421-426










861401-1406


744

69









892407-2413









453





Society B 2762031-2036

70



7

















812651ndash2661





71




of Sciences 10717234-17239









6688-694












72






23841-851

73

Figures



74





nd to 4

th hours of the

trials

75


ants





Abstract











forests

Introduction



76

























77

Methods




















78







N ratios and













Results






79








Pachycondola sp1)

Discussion






N foods (eg









80



be more attractive





















81




N ratio





















82











Acknowledgements









83

References





426



29418ndash429













61519ndash525

84







Ecology 77489-499




Cambridge



Ecology 24221-227








New Jersey

85



86

Tables








Dolichoderinae

Azteca sp 1 3 0

sp 2 2 0

sp 3 0 2

sp 4 3 (1) 0

sp 5 3 (2) 0


sp 1 3 0

sp 2 3 1 (2)

sp 3 3 3

sp 4 0 2

Ecitoninae

Labidus sp 1 3 0

Formicinae

Camponotus sp 1 3 3

sp 2 3 (82) 1 (2)

sp 3 3 (3) 0

sp 4 0 2

87

sp 5 8 (11) 0

sp 6 4 (7 16 468) 0

sp 7 5 (12) 0

sp 8 2 (1) 0



sp 2 0 3


sp 2 3 0

Myrmicinae

Atta sp 1 3 0


placidus 3 (1 4 21) 0

sp 1 3 0

sp 2 1 0

sp 3 2 0


sp 2 3 (35) 0

sp 3 9 (7) 0

sp 4 2 0


sp 2 0 2

sp 3 4 (7) 0

sp 4 3 0


88

Pheidole sp 1 0 3

sp 2 3 0

sp 3 0 3


Solenopsis sp 1 0 3

sp 2 3 (3 5) 0

Wasmannia sp 1 3 0

Ponerinae



Pseudomyrmicinae


sp 2 3 0

sp 3 3 (9) 0

sp 4 0 3

sp 5 0 3

89





(grains found)


(grains found)

Aenictinae


Dolichoderinae




Ectatomminae


Formicinae


sp 2 3 3

sp 3 3 3




sp 2 1 3

sp 3 2 0

Nylanderia sp 1 3 3



90

Myrmicinae


sp 2 3 (32) 3


sp 2 3 3 (1 1 1)

Pheidole sp 1 3 3


Pyramica sp 1 3 0

Ponerinae


91

Figures



92







93

Concluding Remarks





















94























95







play within it

96




4
























5





















6
























7






















8























9












iv) Net effects










10
























11
























12























13
























14






















15





















16























17















a) Toxic nectar







18



















b) Floral volatiles




19













and Willmer 2012)











20



4 Future directions
















21























22
















Acknowledgements




23



Sigma Xi

24

References




65















25



71421ndash426












29418ndash429







26













298581ndash596







Botany 4517ndash8

27


333









319







528



28






272



27





652319ndash2327







29



892407ndash2413














Cambridge



30



Ecology 24221-227






7












31



22665ndash670











371323ndash31








32




54















411163ndash1168

33






812651ndash2661













34







10717234ndash9











45373-388



3096

35


Oikos 74265ndash272

















36






68959ndash967















37





















38












39

Tables






Acacia

drepanolobium

Crematogaster

nigriceps

Proportion

fruiting



removed



pollinia removal


40



Fruit set pollinia

removed

Negative for fruit

set neutral for

pollinia removal


1981 T


demerarae


1998


auropunctata



Schemske 1980


gelida


41







significant results

Blancafort and

Gόmez 2005


and others






Ness 2006

42



and Formica sp






Norment 1988


inflorescence



Gόmez et al

1996


decemarticulatus


2011


dohrni


2005

43



ovules setting

seed


1996

Leucospermum

conocarpodendron



indexrdquo

(combination of

number of seeds

fruits flowers

and seed weight)




visitation

Newman and

Thomson 2005

44


Melastoma

malabathricum

Oecophylla

smaragdina






2012

Metrosideros

polymorpha





fruit set

Junker et al

2010a


gelida


limited

Puterbaugh 1988

45



pusillus and others




set

Byk and Del

Claro 2010





Chamberlain and

Holland 2008

Polemonium

viscosum

F neorufibarbis

gelida


46


Polemonium

viscosum

F neorufibarbis

gelida



densities

Galen and Geib

2007 T


humile and others





to relocate

Lach 2007

Psychotria

limonensis



Altshuler 1999

47



albipes


competition

Hansen and

Muumlller 2009





Caballero et al

2013

Vaccinium

reticulatum



Bleil et al 2011



48










seed




49




japonicas



orchids

Sugiura et al 2006










50



longiseta


Jatropha curcas

Several

Tapinoma

melanocephalum

most common



and subsequently

confirmed as ant

pollination

Peakall et al 1987

51



Camponotus

micans most

common


Microtis parviflora

Iridomyrmex

gracilis





Naufraga balearica

Several

especially

Plagiolepis

pygmaea and

Lasius grandis




ants carried pollen


52



Paratrechina sp



orchids

Wang et al 2008


neorufibarbis

gelida








Hickman 1974

53




Several

especially

Formica

rufibarbis




Svensson 1985


longiseta



54







Abstract












55

Introduction























56






















seed set



57













Methods

i) Subjects








58


















unpublished data)





59






















60















b) Scent trials








61























62


















Results




63








the model

Discussion






female function








64








Souza et al 2008)

















65

























66













ants

Acknowledgements









67

68

References









71421-426










861401-1406


744

69









892407-2413









453





Society B 2762031-2036

70



7

















812651ndash2661





71




of Sciences 10717234-17239









6688-694












72






23841-851

73

Figures



74





nd to 4

th hours of the

trials

75


ants





Abstract











forests

Introduction



76

























77

Methods




















78







N ratios and













Results






79








Pachycondola sp1)

Discussion






N foods (eg









80



be more attractive





















81




N ratio





















82











Acknowledgements









83

References





426



29418ndash429













61519ndash525

84







Ecology 77489-499




Cambridge



Ecology 24221-227








New Jersey

85



86

Tables








Dolichoderinae

Azteca sp 1 3 0

sp 2 2 0

sp 3 0 2

sp 4 3 (1) 0

sp 5 3 (2) 0


sp 1 3 0

sp 2 3 1 (2)

sp 3 3 3

sp 4 0 2

Ecitoninae

Labidus sp 1 3 0

Formicinae

Camponotus sp 1 3 3

sp 2 3 (82) 1 (2)

sp 3 3 (3) 0

sp 4 0 2

87

sp 5 8 (11) 0

sp 6 4 (7 16 468) 0

sp 7 5 (12) 0

sp 8 2 (1) 0



sp 2 0 3


sp 2 3 0

Myrmicinae

Atta sp 1 3 0


placidus 3 (1 4 21) 0

sp 1 3 0

sp 2 1 0

sp 3 2 0


sp 2 3 (35) 0

sp 3 9 (7) 0

sp 4 2 0


sp 2 0 2

sp 3 4 (7) 0

sp 4 3 0


88

Pheidole sp 1 0 3

sp 2 3 0

sp 3 0 3


Solenopsis sp 1 0 3

sp 2 3 (3 5) 0

Wasmannia sp 1 3 0

Ponerinae



Pseudomyrmicinae


sp 2 3 0

sp 3 3 (9) 0

sp 4 0 3

sp 5 0 3

89





(grains found)


(grains found)

Aenictinae


Dolichoderinae




Ectatomminae


Formicinae


sp 2 3 3

sp 3 3 3




sp 2 1 3

sp 3 2 0

Nylanderia sp 1 3 3



90

Myrmicinae


sp 2 3 (32) 3


sp 2 3 3 (1 1 1)

Pheidole sp 1 3 3


Pyramica sp 1 3 0

Ponerinae


91

Figures



92







93

Concluding Remarks





















94























95







play within it

96




5





















6
























7






















8























9












iv) Net effects










10
























11
























12























13
























14






















15





















16























17















a) Toxic nectar







18



















b) Floral volatiles




19













and Willmer 2012)











20



4 Future directions
















21























22
















Acknowledgements




23



Sigma Xi

24

References




65















25



71421ndash426












29418ndash429







26













298581ndash596







Botany 4517ndash8

27


333









319







528



28






272



27





652319ndash2327







29



892407ndash2413














Cambridge



30



Ecology 24221-227






7












31



22665ndash670











371323ndash31








32




54















411163ndash1168

33






812651ndash2661













34







10717234ndash9











45373-388



3096

35


Oikos 74265ndash272

















36






68959ndash967















37





















38












39

Tables






Acacia

drepanolobium

Crematogaster

nigriceps

Proportion

fruiting



removed



pollinia removal


40



Fruit set pollinia

removed

Negative for fruit

set neutral for

pollinia removal


1981 T


demerarae


1998


auropunctata



Schemske 1980


gelida


41







significant results

Blancafort and

Gόmez 2005


and others






Ness 2006

42



and Formica sp






Norment 1988


inflorescence



Gόmez et al

1996


decemarticulatus


2011


dohrni


2005

43



ovules setting

seed


1996

Leucospermum

conocarpodendron



indexrdquo

(combination of

number of seeds

fruits flowers

and seed weight)




visitation

Newman and

Thomson 2005

44


Melastoma

malabathricum

Oecophylla

smaragdina






2012

Metrosideros

polymorpha





fruit set

Junker et al

2010a


gelida


limited

Puterbaugh 1988

45



pusillus and others




set

Byk and Del

Claro 2010





Chamberlain and

Holland 2008

Polemonium

viscosum

F neorufibarbis

gelida


46


Polemonium

viscosum

F neorufibarbis

gelida



densities

Galen and Geib

2007 T


humile and others





to relocate

Lach 2007

Psychotria

limonensis



Altshuler 1999

47



albipes


competition

Hansen and

Muumlller 2009





Caballero et al

2013

Vaccinium

reticulatum



Bleil et al 2011



48










seed




49




japonicas



orchids

Sugiura et al 2006










50



longiseta


Jatropha curcas

Several

Tapinoma

melanocephalum

most common



and subsequently

confirmed as ant

pollination

Peakall et al 1987

51



Camponotus

micans most

common


Microtis parviflora

Iridomyrmex

gracilis





Naufraga balearica

Several

especially

Plagiolepis

pygmaea and

Lasius grandis




ants carried pollen


52



Paratrechina sp



orchids

Wang et al 2008


neorufibarbis

gelida








Hickman 1974

53




Several

especially

Formica

rufibarbis




Svensson 1985


longiseta



54







Abstract












55

Introduction























56






















seed set



57













Methods

i) Subjects








58


















unpublished data)





59






















60















b) Scent trials








61























62


















Results




63








the model

Discussion






female function








64








Souza et al 2008)

















65

























66













ants

Acknowledgements









67

68

References









71421-426










861401-1406


744

69









892407-2413









453





Society B 2762031-2036

70



7

















812651ndash2661





71




of Sciences 10717234-17239









6688-694












72






23841-851

73

Figures



74





nd to 4

th hours of the

trials

75


ants





Abstract











forests

Introduction



76

























77

Methods




















78







N ratios and













Results






79








Pachycondola sp1)

Discussion






N foods (eg









80



be more attractive





















81




N ratio





















82











Acknowledgements









83

References





426



29418ndash429













61519ndash525

84







Ecology 77489-499




Cambridge



Ecology 24221-227








New Jersey

85



86

Tables








Dolichoderinae

Azteca sp 1 3 0

sp 2 2 0

sp 3 0 2

sp 4 3 (1) 0

sp 5 3 (2) 0


sp 1 3 0

sp 2 3 1 (2)

sp 3 3 3

sp 4 0 2

Ecitoninae

Labidus sp 1 3 0

Formicinae

Camponotus sp 1 3 3

sp 2 3 (82) 1 (2)

sp 3 3 (3) 0

sp 4 0 2

87

sp 5 8 (11) 0

sp 6 4 (7 16 468) 0

sp 7 5 (12) 0

sp 8 2 (1) 0



sp 2 0 3


sp 2 3 0

Myrmicinae

Atta sp 1 3 0


placidus 3 (1 4 21) 0

sp 1 3 0

sp 2 1 0

sp 3 2 0


sp 2 3 (35) 0

sp 3 9 (7) 0

sp 4 2 0


sp 2 0 2

sp 3 4 (7) 0

sp 4 3 0


88

Pheidole sp 1 0 3

sp 2 3 0

sp 3 0 3


Solenopsis sp 1 0 3

sp 2 3 (3 5) 0

Wasmannia sp 1 3 0

Ponerinae



Pseudomyrmicinae


sp 2 3 0

sp 3 3 (9) 0

sp 4 0 3

sp 5 0 3

89





(grains found)


(grains found)

Aenictinae


Dolichoderinae




Ectatomminae


Formicinae


sp 2 3 3

sp 3 3 3




sp 2 1 3

sp 3 2 0

Nylanderia sp 1 3 3



90

Myrmicinae


sp 2 3 (32) 3


sp 2 3 3 (1 1 1)

Pheidole sp 1 3 3


Pyramica sp 1 3 0

Ponerinae


91

Figures



92







93

Concluding Remarks





















94























95







play within it

96




6
























7






















8























9












iv) Net effects










10
























11
























12























13
























14






















15





















16























17















a) Toxic nectar







18



















b) Floral volatiles




19













and Willmer 2012)











20



4 Future directions
















21























22
















Acknowledgements




23



Sigma Xi

24

References




65















25



71421ndash426












29418ndash429







26













298581ndash596







Botany 4517ndash8

27


333









319







528



28






272



27





652319ndash2327







29



892407ndash2413














Cambridge



30



Ecology 24221-227






7












31



22665ndash670











371323ndash31








32




54















411163ndash1168

33






812651ndash2661













34







10717234ndash9











45373-388



3096

35


Oikos 74265ndash272

















36






68959ndash967















37





















38












39

Tables






Acacia

drepanolobium

Crematogaster

nigriceps

Proportion

fruiting



removed



pollinia removal


40



Fruit set pollinia

removed

Negative for fruit

set neutral for

pollinia removal


1981 T


demerarae


1998


auropunctata



Schemske 1980


gelida


41







significant results

Blancafort and

Gόmez 2005


and others






Ness 2006

42



and Formica sp






Norment 1988


inflorescence



Gόmez et al

1996


decemarticulatus


2011


dohrni


2005

43



ovules setting

seed


1996

Leucospermum

conocarpodendron



indexrdquo

(combination of

number of seeds

fruits flowers

and seed weight)




visitation

Newman and

Thomson 2005

44


Melastoma

malabathricum

Oecophylla

smaragdina






2012

Metrosideros

polymorpha





fruit set

Junker et al

2010a


gelida


limited

Puterbaugh 1988

45



pusillus and others




set

Byk and Del

Claro 2010





Chamberlain and

Holland 2008

Polemonium

viscosum

F neorufibarbis

gelida


46


Polemonium

viscosum

F neorufibarbis

gelida



densities

Galen and Geib

2007 T


humile and others





to relocate

Lach 2007

Psychotria

limonensis



Altshuler 1999

47



albipes


competition

Hansen and

Muumlller 2009





Caballero et al

2013

Vaccinium

reticulatum



Bleil et al 2011



48










seed




49




japonicas



orchids

Sugiura et al 2006










50



longiseta


Jatropha curcas

Several

Tapinoma

melanocephalum

most common



and subsequently

confirmed as ant

pollination

Peakall et al 1987

51



Camponotus

micans most

common


Microtis parviflora

Iridomyrmex

gracilis





Naufraga balearica

Several

especially

Plagiolepis

pygmaea and

Lasius grandis




ants carried pollen


52



Paratrechina sp



orchids

Wang et al 2008


neorufibarbis

gelida








Hickman 1974

53




Several

especially

Formica

rufibarbis




Svensson 1985


longiseta



54







Abstract












55

Introduction























56






















seed set



57













Methods

i) Subjects








58


















unpublished data)





59






















60















b) Scent trials








61























62


















Results




63








the model

Discussion






female function








64








Souza et al 2008)

















65

























66













ants

Acknowledgements









67

68

References









71421-426










861401-1406


744

69









892407-2413









453





Society B 2762031-2036

70



7

















812651ndash2661





71




of Sciences 10717234-17239









6688-694












72






23841-851

73

Figures



74





nd to 4

th hours of the

trials

75


ants





Abstract











forests

Introduction



76

























77

Methods




















78







N ratios and













Results






79








Pachycondola sp1)

Discussion






N foods (eg









80



be more attractive





















81




N ratio





















82











Acknowledgements









83

References





426



29418ndash429













61519ndash525

84







Ecology 77489-499




Cambridge



Ecology 24221-227








New Jersey

85



86

Tables








Dolichoderinae

Azteca sp 1 3 0

sp 2 2 0

sp 3 0 2

sp 4 3 (1) 0

sp 5 3 (2) 0


sp 1 3 0

sp 2 3 1 (2)

sp 3 3 3

sp 4 0 2

Ecitoninae

Labidus sp 1 3 0

Formicinae

Camponotus sp 1 3 3

sp 2 3 (82) 1 (2)

sp 3 3 (3) 0

sp 4 0 2

87

sp 5 8 (11) 0

sp 6 4 (7 16 468) 0

sp 7 5 (12) 0

sp 8 2 (1) 0



sp 2 0 3


sp 2 3 0

Myrmicinae

Atta sp 1 3 0


placidus 3 (1 4 21) 0

sp 1 3 0

sp 2 1 0

sp 3 2 0


sp 2 3 (35) 0

sp 3 9 (7) 0

sp 4 2 0


sp 2 0 2

sp 3 4 (7) 0

sp 4 3 0


88

Pheidole sp 1 0 3

sp 2 3 0

sp 3 0 3


Solenopsis sp 1 0 3

sp 2 3 (3 5) 0

Wasmannia sp 1 3 0

Ponerinae



Pseudomyrmicinae


sp 2 3 0

sp 3 3 (9) 0

sp 4 0 3

sp 5 0 3

89





(grains found)


(grains found)

Aenictinae


Dolichoderinae




Ectatomminae


Formicinae


sp 2 3 3

sp 3 3 3




sp 2 1 3

sp 3 2 0

Nylanderia sp 1 3 3



90

Myrmicinae


sp 2 3 (32) 3


sp 2 3 3 (1 1 1)

Pheidole sp 1 3 3


Pyramica sp 1 3 0

Ponerinae


91

Figures



92







93

Concluding Remarks





















94























95







play within it

96




7






















8























9












iv) Net effects










10
























11
























12























13
























14






















15





















16























17















a) Toxic nectar







18



















b) Floral volatiles




19













and Willmer 2012)











20



4 Future directions
















21























22
















Acknowledgements




23



Sigma Xi

24

References




65















25



71421ndash426












29418ndash429







26













298581ndash596







Botany 4517ndash8

27


333









319







528



28






272



27





652319ndash2327







29



892407ndash2413














Cambridge



30



Ecology 24221-227






7












31



22665ndash670











371323ndash31








32




54















411163ndash1168

33






812651ndash2661













34







10717234ndash9











45373-388



3096

35


Oikos 74265ndash272

















36






68959ndash967















37





















38












39

Tables






Acacia

drepanolobium

Crematogaster

nigriceps

Proportion

fruiting



removed



pollinia removal


40



Fruit set pollinia

removed

Negative for fruit

set neutral for

pollinia removal


1981 T


demerarae


1998


auropunctata



Schemske 1980


gelida


41







significant results

Blancafort and

Gόmez 2005


and others






Ness 2006

42



and Formica sp






Norment 1988


inflorescence



Gόmez et al

1996


decemarticulatus


2011


dohrni


2005

43



ovules setting

seed


1996

Leucospermum

conocarpodendron



indexrdquo

(combination of

number of seeds

fruits flowers

and seed weight)




visitation

Newman and

Thomson 2005

44


Melastoma

malabathricum

Oecophylla

smaragdina






2012

Metrosideros

polymorpha





fruit set

Junker et al

2010a


gelida


limited

Puterbaugh 1988

45



pusillus and others




set

Byk and Del

Claro 2010





Chamberlain and

Holland 2008

Polemonium

viscosum

F neorufibarbis

gelida


46


Polemonium

viscosum

F neorufibarbis

gelida



densities

Galen and Geib

2007 T


humile and others





to relocate

Lach 2007

Psychotria

limonensis



Altshuler 1999

47



albipes


competition

Hansen and

Muumlller 2009





Caballero et al

2013

Vaccinium

reticulatum



Bleil et al 2011



48










seed




49




japonicas



orchids

Sugiura et al 2006










50



longiseta


Jatropha curcas

Several

Tapinoma

melanocephalum

most common



and subsequently

confirmed as ant

pollination

Peakall et al 1987

51



Camponotus

micans most

common


Microtis parviflora

Iridomyrmex

gracilis





Naufraga balearica

Several

especially

Plagiolepis

pygmaea and

Lasius grandis




ants carried pollen


52



Paratrechina sp



orchids

Wang et al 2008


neorufibarbis

gelida








Hickman 1974

53




Several

especially

Formica

rufibarbis




Svensson 1985


longiseta



54







Abstract












55

Introduction























56






















seed set



57













Methods

i) Subjects








58


















unpublished data)





59






















60















b) Scent trials








61























62


















Results




63








the model

Discussion






female function








64








Souza et al 2008)

















65

























66













ants

Acknowledgements









67

68

References









71421-426










861401-1406


744

69









892407-2413









453





Society B 2762031-2036

70



7

















812651ndash2661





71




of Sciences 10717234-17239









6688-694












72






23841-851

73

Figures



74





nd to 4

th hours of the

trials

75


ants





Abstract











forests

Introduction



76

























77

Methods




















78







N ratios and













Results






79








Pachycondola sp1)

Discussion






N foods (eg









80



be more attractive





















81




N ratio





















82











Acknowledgements









83

References





426



29418ndash429













61519ndash525

84







Ecology 77489-499




Cambridge



Ecology 24221-227








New Jersey

85



86

Tables








Dolichoderinae

Azteca sp 1 3 0

sp 2 2 0

sp 3 0 2

sp 4 3 (1) 0

sp 5 3 (2) 0


sp 1 3 0

sp 2 3 1 (2)

sp 3 3 3

sp 4 0 2

Ecitoninae

Labidus sp 1 3 0

Formicinae

Camponotus sp 1 3 3

sp 2 3 (82) 1 (2)

sp 3 3 (3) 0

sp 4 0 2

87

sp 5 8 (11) 0

sp 6 4 (7 16 468) 0

sp 7 5 (12) 0

sp 8 2 (1) 0



sp 2 0 3


sp 2 3 0

Myrmicinae

Atta sp 1 3 0


placidus 3 (1 4 21) 0

sp 1 3 0

sp 2 1 0

sp 3 2 0


sp 2 3 (35) 0

sp 3 9 (7) 0

sp 4 2 0


sp 2 0 2

sp 3 4 (7) 0

sp 4 3 0


88

Pheidole sp 1 0 3

sp 2 3 0

sp 3 0 3


Solenopsis sp 1 0 3

sp 2 3 (3 5) 0

Wasmannia sp 1 3 0

Ponerinae



Pseudomyrmicinae


sp 2 3 0

sp 3 3 (9) 0

sp 4 0 3

sp 5 0 3

89





(grains found)


(grains found)

Aenictinae


Dolichoderinae




Ectatomminae


Formicinae


sp 2 3 3

sp 3 3 3




sp 2 1 3

sp 3 2 0

Nylanderia sp 1 3 3



90

Myrmicinae


sp 2 3 (32) 3


sp 2 3 3 (1 1 1)

Pheidole sp 1 3 3


Pyramica sp 1 3 0

Ponerinae


91

Figures



92







93

Concluding Remarks





















94























95







play within it

96




Documents

Ants as flower visitors and their effects on pollinator