Ecology, 85(6), 2004, pp. 1495±1502 ᭧ 2004 by the Ecological Society of America

EXTRAFLORAL NECTAR AS A RESOURCE MEDIATING MULTISPECIES INTERACTIONS

JENNIFER A. RUDGERS1,3 AND MARK C. GARDENER2,4 1Center for Population Biology, One Shields Avenue, University of California, Davis, California 95616 USA 2Ecology and Evolution Research Group, Department of Biological Sciences, The Open University, Walton Hall, Milton Keynes, MK7 6AA UK

Abstract. Extra¯oral (EF) nectar resources can affect the dynamics of inter- actions at the community scale. Furthermore, selection acting on EF nectary traits may extend beyond simple mutualisms between and the enemies of herbivores to involve other community members that use EF nectar. We examine how EF nectaries in¯uence and are in¯uenced by interactions with multiple species, highlighting our review with original data from the association between ants and wild cotton ( thurberi). Our survey of the literature suggested that EF nectar attracts a diverse assemblage of arthropods and may enhance the diversity and abundance of arthropod assemblages. However, experimental evidence on the importance of EF nectar to terrestrial food webs was equivocal. Exploring potential avenues for selection, we uncovered several costs and bene®ts of EF nectary traits that have received little empirical attention. These include a constraint faced by plants when attracting both pollinators and protectors via nectar, as well as an ecological cost of nectar when herbivores consume EF nectar as adults. Finally, we discuss how geographic variation in multispecies interactions may affect selection on EF nectary traits. In wild cotton, variation among populations in EF nectar composition was consistent with the bene®ts afforded by attracting ants; however, non-ant species may also mediate spatially Feature Special variable selection on EF nectaries. Our synthesis underscores a need for studies that ma- nipulate EF resources at the community level and investigate selection on EF nectaries in a multispecies and geographic context. Key words: extra¯oral nector; geographic variation; Gossypium thurberi; indirect effects; mul- tispecies interactions; nectar chemistry; species diversity; wild cotton.

INTRODUCTION ditionally, ants have been viewed as the most important Extra¯oral (EF) nectaries occur in more than 90 agents of selection on EF nectary traits; however, sev- families and 330 genera (Koptur 1992a). These secre- eral other taxa may in¯uence the evolution of EF nec- tory structures are thought to function primarily in pro- taries, including pollinators and herbivores. Selective tection mutualisms, most commonly involving ants that regimes will depend on a balance between the costs reduce herbivory in exchange for nectar (Bentley 1977, and bene®ts of EF nectar. This balance is likely to shift Koptur 1992a). However, carbohydrate-rich, EF nectar with the local ecological context because interactions rewards are also consumed by insect herbivores, par- involving EF nectar are characteristically variable in asitoids, spiders, and even birds (Adjei-Maafo and Wil- space and time (Bronstein 1998). son 1983, Hespenheide 1985, Vanstone and Paton We explore multispecies interactions mediated by EF 1988, Taylor and Foster 1996, Cuautle and Rico-Gray nectar from both ecological and evolutionary perspec- 2003). Although few studies have directly investigated tives. First, we ask, what are the community-level ef- fects of EF nectar resources? We evaluate the potential the effects of EF nectar on communities, current evi- for EF nectar to affect entire assemblages of arthro- dence suggests that EF nectar may in¯uence species pods, examine methods to assess the contribution of composition, abundance, and interactions at the com- EF nectar to terrestrial food webs, and suggest a role munity scale (Keeler 1978, Rico-Gray et al. 1998). for EF nectar in mediating plant±plant interactions. In turn, the evolution of EF nectary traits should be Second, given the potential for many species to interact affected by a broad array of community members. Tra- with EF nectar, we ask how multispecies interactions might shape the evolution of EF nectary traits. To this Manuscript received 9 June 2003; revised 3 September 2003; accepted 10 September 2003; ®nal version received 20 October end, we examine costs as well as nondefensive bene®ts 2003. Corresponding Editor (ad hoc): L. S. Adler. For reprints of EF nectar. Finally, we ask, how does geographic of this Special Feature, see footnote 1, p. 1477. variation in multispecies interactions affect the evo- 3 Present address: Department of Biology, Indiana Uni- lution of EF nectaries? We include examples from the versity, Bloomington, Indiana 47405 USA. E-mail: jrudg- [email protected] current literature and emphasize our published and new 4 Present address: Department of Botany, University of work on ants and the EF nectary-bearing wild cotton Hawaii, 3190 Maile Way, Honolulu, Hawaii 96822 USA. (Gossypium thurberi). Throughout the paper, our goal 1495 Special Feature r motn oftr eerho Fnectar-mediated EF feel on we interactions. research that future areas to highlight important to are examples these use to is 1496 n eemndama f11.7 records of published mean of a determined survey and a conducted We plants. to omnt-ee fet fE etri iie.How- ( similar limited. cotton cultivated is in for ever, nectar EF aphids Evidence of effects 1996). without community-level Whitham conspeci®cs and to cot- (Dickson on compared arthropods of tonwood abundance and richness species aaie n olntrtx na es 0arthropod 10 least at 1992 in (Koptur taxa orders herbivore, diverse pollinator including and arthropods, documented, parasite, non-ant been of have survey visitors al- similar to a insuf®cient are low records current Although Rico-Gray 1993). also than (see ants rather of diverse, assemblages hosts homogeneous, often nectar EF that suggests rnDsr fAioaadMxc,idct htEF that indicate Mexico, and Arizona of Desert oran hoosta etr-espat.A nlgu ex- ( ar- analogous aphids gall-forming of An from abundance comes plants. ample or nectary-less diversity than greater thropods a support may ospu thurberi Gossypium neatosaogpat htmysaeo compete or visitors. share nectary may for that of plants chain among food interactions facilitating tri-trophic by speci®cally inter- simple plants±herbivores±enemies, species the mediate we beyond may Finally, actions nectaries vs. webs. EF nectar food that EF terrestrial propose of to contribution resources ways relative other novel the suggest explore then to We that hypothesis. data this new address present of abundance also We or assemblages. diversity the arthropod affect to sub- are enough rewards con- stantial nectar a EF whether provide assessing to evidence the potential summarize We the resource. community-level has siderable Blu nectar Oliveira- 1991, EF and Feener 2000), and (Oliveira Schupp regions 1991, some Filho in reach per- can 30% nectaries the EF nearly bearing As species plant nectar animals. of EF centage nectar-feeding of importance provisioning the in of indication some vides e Fncaybaigpatseis(ag ±7ant 1±27 (range species species, plant nectary-bearing EF per ( Wilson and Adjei-Maafo 1977, lines al. 1983). nectary-less et related) (or (Henneberry near-isogenic com- nectaries non-ant to EF with pared and plants on parasitoids, found were predators herbivores, of abundances tae Fnca a trc ies sebaeo visitors of assemblage diverse a attract can nectar EF ypoiigcroyrts lnswt Fnectar EF with plants carbohydrates, providing By ,wihpoiehnye n hrb nraethe increase thereby and honeydew provide which ), h rvlneo Fncaybaigpat pro- plants nectary-bearing EF of prevalence The ncnrs,nwdt rmawl otnspecies cotton wild a from data new contrast, In W fet fE etro rhoo diversity arthropod on nectar EF of Effects HAT n ϭ A ETHE RE 5patseis pedx.Ti result This Appendix). species; plant 35 FN EF OF n abundance and a C avca) aiet h Son- the to native ), , ECTAR ). OMMUNITY ospu hirsutum Gossypium R ENFRA UGR N AKC GARDENER C. MARK AND RUDGERS A. JENNIFER ESOURCES Ϯ . (1 6.5 -L EVEL SD epiu be- Pemphigus ? E tgne al. et Èthgen n species ant ) FFECTS ,greater ), oswr one nwl otnpat nAu Cal- Agua (31 in USA plants Arizona, cotton Canyon, wild iente arthro- on all counted 2000, were September pods abundance 8±10 arthropod During promote diversity. or always not may nectar ant, ϩ com- treatment access four ant of one binations: to exposed were Plants W). Ϯ ϭ f1.61 of uig n-eddahd ( aphids ant-tended ducing, rvn igeatrpdfo oooiigtere- the monopolizing from arthropod could single communities a in nectar prevent EF of distribution spatial lnsi ersa(elr18)adi lrd,USA Florida, in and 1992 (Koptur 1980) (Keeler per- Nebraska nectary-bearing in the EF plants of with composed correlated vegetation of positively centage was spe- ant richness Similarly, nectar. EF cies more more or attack with nectar, sites (e.g., EF in behavior moths) greater their with alter para- may areas more parasitoids in 1996); occur Lee may in and sitoids sites (Pemberton forest across Korea nectaries South EF with plants of dance hno-enrdvriyidxo 1.26 of index diversity Shannon-Weiner rhoosta lnswt nsecue (ant, excluded non-ant ants of with diversity plants lower than a arthropods supported ants to access A Fnectar, EF VA: a,atexclusion ant tar, clso in®atyrdcdvstto yants Shannon- for the index by affect diversity not Weiner did visitation nectar EF 2004), reduced (Rudgers signi®cantly exper- nectar EF additional occlusion Although 2004). (for Rudgers bridges see details, ant imental plus controls barrier and the (Tanglefoot), Tangleguard had of band a over spread bar- USA) sticky Michigan, Rapids, a Grand (Tanglefoot, with cov- rier excluded not were but near, Ants placed nectaries. ering, glue had controls Califor- nec- USA); Buellton, (Aleene's, covering nia, glue by reduced nontoxic was with nectar taries Beginning EF respectively). 2000, treatment, July per in plants 28 26, est.Freape aaiimo ys oh ( moths di- gypsy and of density parasitism arthropod example, high For versity. of islands However, create nectar arthropods. EF may supplying on habitats that effects indicate to observations atten- respect less with even tion received have plants nectary-bearing are abundances ant when or low. ants by com- exclusion resist can petitive arthropods of these availability in when the resources nectar with nectar increase EF will ar- of diversity that thropod predict role We the assemblages. and arthropod assess ad- structuring cotton for that need native studies a highlight ditional vs. cottonwood on cultivated aphids among in con- results These 2001). trasting Whitham and (Wimp mutualism the without trees on conspeci®c to abundance compared trees and cottonwood richness species arthropod reduced ati dispar mantria 1 eue Fnca,atexclusion ant nectar, EF reduced 12.33, oprdt igepatseis sebae fEF of assemblages species, plant single to Compared SE F ,108 1, ;pat ihatecuinhdadvriyindex diversity a had exclusion ant with plants ]; Ϯ P ϭ .6.I iia xml,honeydew-pro- example, similar a In 0.06). ϭ 0.06, b u e elr17) ocial,the Conceivably, 1979). Keeler see but , nrae agnlywt h abun- the with marginally increased ) .07 lnswt n ceshda had access ant with plants 0.0007; F ,108 1, ϩ P ϭ eue Fnca ( nectar EF reduced ϩ ϭ .1.I diin lnswith plants addition, In 0.81). min Fnca,ataccess ant nectar, EF ambient 1.54, non-ant hiohrspopulicola Chaitophorus P Њ ϭ 41 clg,Vl 5 o 6 No. 85, Vol. Ecology, ϩ Ј .2 Fnectar EF 0.22; rhoos(ANO- arthropods 32 min Fnec- EF ambient Љ ,110 N, Ϯ n .8[mean 0.08 ϭ Њ 8 30, 28, 57 F Ј ,108 1, Ly- 23 ϫ ) Љ June 2004 COMMUNITY AND EVOLUTIONARY NECTAR ECOLOGY 1497 source and thus promote species coexistence (BluÈthgen EF nectaries. Identifying and quantifying the costs and et al. 2000). bene®ts of EF nectary traits will enhance our under- Experiments manipulating EF nectar resources at the standing of selection on these characters; however, few community level have not been performed outside of studies have examined EF nectary traits in a cost±ben- agricultural systems (e.g., EF nectary and nectary-less e®t framework. Costs of EF nectar may be expressed cotton cultivars). Plantings of nectary-bearing plants physiologically (direct costs) or ecologically via inter- with crops lacking nectaries have successfully recruited actions involving other species (ecological costs) biological control agents to agroecosystems (Atsatt and (Strauss et al. 2002). For example, EF nectaries that O'Dowd 1976), but are EF nectaries as attractive to attract ants to deter generalist herbivores may also lure arthropods in more complex, natural food webs? Ma- specialized, ant-tended herbivores, exacting an ecolog- nipulations of EF nectar (independently of plant spe- ical cost when specialized herbivores are abundant cies) could determine whether this resource affects the (Buckley 1983). Bene®ts of EF nectaries may include diversity or abundance of arthropods. If strong effects both the commonly studied protective bene®ts as well are found, a next step is to examine how variation in as other, nondefensive bene®ts, such as the attraction EF nectary traits (volume, composition, volatiles) af- of pollinators or seed dispersers. fects arthropods. How these traits mediate interactions is not well resolved, even for the most common species Costs of ants (Lanza et al. 1993, Heil et al. 2001), because Physiological costs.ÐEF nectar typically contains most studies exclude ants but do not manipulate EF carbohydrates with dilute concentrations of amino ac- nectar (see Rudgers 2004). ids (Baker et al. 1978). Although EF nectar production is presumed to be inexpensive, this assumption has Contribution of EF nectar to food web dynamics rarely been tested. The best estimate of which we are In communities rich with EF nectary-bearing plants, aware indicates that EF nectar is relatively cheap, equal nectar may be a vital resource in food webs. Currently, to ϳ1% of the total energy invested per leaf (O'Dowd few data are available to address this hypothesis. Fisher 1979). Comparing the ®tness of plants for which nectar Feature Special et al. (1990) used stable-isotope analyses to determine is repeatedly removed to controls without removals that the contribution of EF nectar to the diets of 11 could estimate the physiological cost of EF nectar pro- orchid-associated ant species ranged from 11% to 48%. duction (see Pyke 1991). Furthermore, the cost of nec- Although ants were con®ned to plants in that study tary structures might be determined by growing iso- (potentially in¯ating the dietary contribution of nectar), genic lines of nectaried and nectary-less plants in the stable-isotope analyses of natural diets could provide absence of arthropods. Because physiological costs (if a useful metric for assessing the bene®ts of nectar to they occur) may vary depending on local resources, arthropods. Such analyses would be especially infor- experiments altering nutrient and water availability mative in seasonal systems in which EF nectar is may also be informative. ephemeral relative to arthropod activity (see Rico-Gray Phenotypic plasticity.ÐFollowing leaf damage, sev- and Sternberg 1991). Future work that evaluates the eral species, including cultivated cotton, increase pro- relative contribution of EF nectar vs. other resources duction of EF nectar (Agrawal and Rutter 1998, Heil (insect prey, ¯oral nectar, homopteran honeydew) will et al. 2001, WaÈckers et al. 2001, Ness 2003). This help to discern the importance of EF nectar in subsi- induced response to damage may indicate that consti- dizing food webs (Rico-Gray 1993, Rico-Gray et al. tutively high levels of nectar are costly to maintain. 1998). Similarly, EF nectar ¯ow stops or slows in some plants when nectar is allowed to accumulate (Heil et al. 2000, Effects of EF nectar on plant±plant interactions but see Torres-HernaÂndez et al. 2000), although nec- Just as Homoptera can compete for the defense con- taries may simply become clogged, rather than being ferred by tending ants (Fischer et al. 2001), plant spe- regulated. These data suggest that plants may moderate cies may compete for the protection provided by ants the physiological costs of EF nectar via plasticity in and other arthropods (e.g., Apple and Feener 2001). nectar production; however, direct evidence for the ge- Alternatively, co-occurring plant species may bene®t netic basis and the adaptive signi®cance of this plas- from associational resistance gained by sharing her- ticity is lacking. bivores' enemies (Leius 1967, Atsatt and O'Dowd Allocation trade-offs and pleiotropy.ÐAs plants 1976). Experiments are needed that determine the con- possess ®nite resources, allocation to one plant function ditions under which plants compete for mutualists or (e.g., indirect defense via EF nectar production) may pro®t from sharing them. diminish the availability of resources for other plant functions, a physiologically-based allocation trade-off HOW DO MULTISPECIES INTERACTIONS SHAPE (Mole 1994). For example, plants that invest in EF THE EVOLUTION OF EF NECTARIES? nectar-mediated defense may express reduced invest- The diversity of EF nectar consumers just described ment in other resistance traits (e.g., toxic secondary suggests that multiple species may exert selection on compounds; Heil et al. 2002; Rudgers et al. 2004). In Special Feature nulse manuscript unpublished J. and Gardener C. (M. nectar Rudgers, EF A. of phe- volume negative nectar the ¯oral a of and volume showed the cotton between correlation wild notypic from prelim- example, data For inary nectar. EF via pro- arthropods attract attract to tective available to resources nectar limit ¯oral may in pollinators investment manner, similar a ϭ ϭ Sub-bracteal 1498 Fnca a xeietlyrdcd(.A Rudgers, A. (J. experienced reduced experimentally site was when than nectar one nectar EF EF had at they when plants damage Similarly, leaf greater composition. cotton nectar wild EF ant-free on in¯u- selection could nectar therefore ence among and 1987), preferences (Ramaswamy of sugars exhibits one least herbivores At al. 1983). these et Wilson (Henneberry and adults Adjei-Maafo as 1977, nectar some on because feed results re- cost herbivores this than lines; herbivores nectary-less EF more lated with attract cultivars tilling, commonly and nectaries pesticides by ants of low more abundance kept received the is where have ®elds, nectar cotton In EF attention. of costs ecological the ugs htsm ye fpatcnuesmyselect may consumers plant of types some that ants suggest of absence the in nectar (Torres-Herna EF (e.g., utilize consumers also plant may other fungi) herbivores, to addition In nectar. EF cotton wild consume herbivores lepidopteran utpemtait aentbe netgtdi other in investigated supporting systems. been not from have derived mutualists multiple To constraints nectar). EF knowledge, and ¯oral sim- our of (e.g., composition occur the corre- also in positive may ilarities traits then reward linked, among closely lations are through or interact traits pleiotropy extra¯oral and ¯oral underlying ordc yeIerror. I Type reduce to ABLE ypopulation² by oioBasin Molino Canyon Florida Caliente Agua Notes: (mean clgclcosts Ecological 8.91, 46.28, etr type Nectary Population T nteudrie flae.Frec etr yesprtl,wti oun ifrn etr niaesgicn differences signi®cant indicate letters different no column, a had within but at separately, Caliente, populations type Agua nectary three at each the For production between leaves. seed of Basin. reduced undersides Molino and the at on damage effect Basin. to no increased Molino led had to or treatment but led Canyon, exclusion Canyon ants Florida ant Florida of and The at Caliente presence population. effect Agua the of both in effect at reduction signi®cant production seed Nectar a reduced showed and which damage MANOVA, increased by preceded were ANOVAs Foliar u-rcelncaisocrblwtebat urudn erdcietsus oirncaisocraogtemidvein the along occur nectaries Foliar tissues. reproductive surrounding bracts the below occur nectaries Sub-bracteal ² oioBasin Molino Canyon Florida Caliente Agua .Athrioecnet o he otenAioawl otnppltoswt orsodn aito ntraits in variation corresponding with populations cotton wild Arizona southern three for contexts Ant±herbivore 1. P Ϯ NV eut r sflos o cuuae ouencay Population volume/nectary, accumulated for follows: as are results ANOVA P Ͻ F Ͻ 1 2,35 .0;Nectary 0.001; SE nulse data unpublished .0,Population 0.001, ne ta.20) nsm hs examples these sum, In 2000). al. et Ândez ϭ o w xr¯rlncaytps u-rceladfoliar. and sub-bracteal types, nectary extra¯oral two for ) 0.66, Ðncnrs opyilgclcosts, physiological to contrast .ÐIn cuuae volume Accumulated P .A ncliae otn adult cotton, cultivated in As ). Ͼ 0.201 0.021 0.015 0.059 e nectary per 0.285 ( F .5 Nectary 0.05; 1,46 ␮ 0.036 /4h) L/24 ab ENFRA UGR N AKC GARDENER C. MARK AND RUDGERS A. JENNIFER ϫ b b a a a .Atraiey fgenes if Alternatively, ). P ϭ Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ Nectary Ͻ 0.19, 0.005 0.006 0.004 0.013 0.093 0.025 .1 sdtrie yps o ue' s et.A lh ee f00 a chosen was 0.01 of level alpha An tests. hsd Tukey's hoc post by determined as 0.01, P F Ͼ F 1,35 2,29 .5 Population 0.05, ϭ ϭ 27.97, 0.35, oc ftotal of Conc. carbohydrates 845.8 716.1 522.0 632.1 444.6 344.0 ( P ␮ P ab ab g/ b b a a Ͼ Ͻ Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ ␮ .5 o ocnrto fttlcroyrts Population carbohydrates, total of concentration for 0.05; .0,Population 0.001, L) etpliaosfo aasetb ants. by pro- harassment may from and pollinators 2001) tect (Ghazoul that ¯owers signal from chemical ants a repels In- release 1999). plants plant some Altshuler other terestingly, dispersers, deter at- seed ants, are as (e.g., that such mutualists nectaries, species thievery, EF when to to arise tracted addition may In costs undertaken. thievery ecological been nectar yet EF not of Hes- has assessment have 1978, an (Keeler plants 1985), nectaries to penheide EF protection at confer documented many not been Although reduce do displays. can that robbers ¯oral visitors nectar of that attractiveness arthro- way the bene®cial same the to in re- plants pods could of attractiveness thievery the Such duce plant. the bene®ting wide- nectar be without EF taking may arthropods thievery nonprotective ex- with nectar on spread, EF occur surfaces, commonly leaf nectaries posed EF Because ways. low. are enemies other or the ants when of particularly nectar, abundances EF in investment against 137.4 208.3 78.1 82.0 60.9 29.9 ahgn,o aaie Bnly17,Kpu 1992 Koptur 1977, (Bentley herbivores, parasites reduce or that pathogens, arthropods attracting by plants ϫ clgclcssmyas rs hog te path- other through arise also may costs Ecological ap)aemc edd nadto,svrlstudies several addition, predaceous In needed. (e.g., much are arthropods wasps) bene®cial other of Cuautle potentially exclusions see selective and (but as- 2003), protection Rico-Gray to of and ants bene®ts excluded ®tness have the date sess to studies Most pathogen and attack. herbivory than attention robbing less ¯oral although received has 1979), deter O'Dowd that (e.g., arthropods robbers lure nectar also can nectaries EF ovninlwso od htE etre bene®t nectaries EF that holds wisdom Conventional Nectary F 2,46 0.458 0.436 0.412 0.569 0.477 0.460 ϭ ϫ rcoeSucrose Fructose 1.54, Nectary ab b a a a a Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ F rprino sugars of Proportion P 0.035 0.017 0.024 0.052 0.011 0.005 2,29 Bene®ts Ͼ F ϭ .5 n o oa mn acids, amino total for and 0.05; 2,35 7.29, ϭ 0.58, P clg,Vl 5 o 6 No. 85, Vol. Ecology, Ͻ 0.178 0.159 0.127 0.117 0.030 0.029 P .1 Nectary 0.01; Ͼ ab ab .5 Protected 0.05. b b a a Ϯ Ϯ Ϯ Ϯ Ϯ Ϯ 0.017 0.053 0.022 0.017 0.009 0.006 F F a 2,46 1,29 ). June 2004 COMMUNITY AND EVOLUTIONARY NECTAR ECOLOGY 1499

TABLE 1. Extended.

Proportion of sugars Total amino acid Aspargine Glucose Inositol conc. (pmol/␮L) proportion

0.363a Ϯ 0.007 0.007a Ϯ 0.002 6017a Ϯ 641 0.026a Ϯ 0.006 0.387a Ϯ 0.010 0.017ab Ϯ 0.012 5775a Ϯ 800 0.010a Ϯ 0.004 0.339a Ϯ 0.063 0.151b Ϯ 0.120 4697a Ϯ 1598 0.027a Ϯ 0.015

0.316a Ϯ 0.019 0.059a Ϯ 0.015 17287a Ϯ 1912 0.061a Ϯ 0.013 0.329a Ϯ 0.024 0.132ab Ϯ 0.054 15730a Ϯ 3067 0.045ab Ϯ 0.021 0.232a Ϯ 0.025 0.169b Ϯ 0.032 18969a Ϯ 2078 0.129b Ϯ 0.021

indicate that EF nectaries bene®t plants through alter- 1998). If the outcomes of interactions vary among pop- native pathways. ulations, then species in local populations are likely to Alteration of ant behavior.ÐSome of these bene®ts experience different patterns of selection, with recip- originate by averting ant behaviors that are harmful to rocal selection between ants and plants occurring only plants. For example, EF nectar may create a diversion in some locations (``Geographic mosaic theory of co- from ¯owers where ants could disturb pollinators, steal evolution''; Thompson 1999). Geographically struc- nectar, or reduce pollen germination via their antimi- tured coevolution is expected to result in differences crobial integuments (Beattie et al. 1984, Wagner and among populations in the traits shaped by coevolu- Kay 2002). In a similar manner, EF nectaries may dis- tionary interactions (Thompson 1999). For example, tract ants from tending Homoptera that reduce plant we may expect populations that vary in the bene®ts Feature Special ®tness (Becerra and Venable 1989). However, evidence gained from ants to differ in investment in EF nectar. thus far is equivocal; EF nectar reduces tending be- This prediction has seldom been tested, because most havior in some cases (Offenberg 2001) and encourages studies do not manipulate or measure EF nectary traits tending ants in others (Buckley 1983, Del-Claro and in multiple populations (but see Inouye and Inouye Oliveira 1993). The net bene®t of EF nectar to plants 1980, Daehler et al. 1999). In addition, gene ¯ow, ge- may depend on the local abundance of both ants and netic drift, and metapopulation dynamics may also in- tended herbivores, in addition to other nectar visitors. ¯uence the EF nectary evolution (Thompson 1999), yet Attraction of alternative mutualists.ÐEF nectaries these factors have not been considered in prior studies. may also attract alternative mutualists that could select Little is currently known about how variation in the for nectary traits. For example, EF nectaries in some outcomes of multispecies interactions affects the evo- acacias (located near the nectarless in¯orescences) at- lution of EF nectary traits. tract avian pollinators (Vanstone and Paton 1988); pol- We explored the spatial component of variable se- len is distributed when the bird's plumage contacts the lection on EF nectaries by examining multiple popu- ¯owers. Honeybees are common visitors to EF nectar- lations of wild cotton. Prior work with wild cotton has ies on cotton (Eiskowitch and Loper 1984), although revealed signi®cant spatial variation in the strength and abundant EF nectar could reduce ¯oral visitation by outcome of interactions with ants (Rudgers 2002, 2004; distracting these pollinators from ¯owers. EF nectar J. A. Rudgers, unpublished manuscript). Speci®cally, may also attract seed dispersers, as in Acacia ligulata, experiments reducing ants (via sticky barriers) and EF where EF nectar feeds ants that disperse the plants' nectar (via gluing) revealed variation among popula- arillate seeds (Whitney 2002; K. D. Whitney, personal tions in both the importance of EF nectar in attracting communication). Finally, because ant colonies accu- ants and the importance of ants to plant ®tness (Table mulate nutrient-rich debris, plants may also derive re- 1). We used these results to predict how populations source bene®ts if ants preferentially nest near (or inside might differ in EF nectary traits. To do so, we assumed of) plants that exude copious nectar (Wagner 1997). that ants (by reducing herbivory) were the primary agents of selection and that interactions varied more HOW DOES GEOGRAPHIC VARIATION AFFECT in space than in time. We based this assumption on the THE EVOLUTION OF EF NECTARIES? temporal consistency of ant±wild cotton interactions When selection on EF nectary traits is in¯uenced by during 2±3 years of ®eld experiments in three popu- multiple species, the evolution of EF nectar traits may lations. Speci®cally, we predicted that where ants en- strongly depend on local ecological conditions. Studies hanced plant ®tness and where ants responded to the often demonstrate that the net outcome of ecological availability of EF nectar (Agua Caliente Canyon, south- interactions between ants and plants (positive, nega- ern Santa Rita Mountains, Arizona, USA), plants would tive, or neutral) varies in space or time (Bronstein invest signi®cantly in EF nectar. Where ants protected Special Feature ihnrnol eetdpat ( plants selected from popu- random randomly at cotton within selected wild were three branches Single among lations. nectar EF of position predictions our re¯ect to 1999). fail (Thompson may and their traits for nectary time, mismatched EF over is ecologically variable populations be exceedingly may among is to populations ¯ow selection important gene if is if or It high that predictions. mind nectary these in docu- of keep EF data light new in in present traits variation we among-population Here, nectar. menting alloca- EF minimal to Moun- anticipated tion we Catalina USA), Santa Arizona, Basin, not tains, did (Molino that plants visitors infrequent protect Fi- were traits. ants Moun- nectary where EF nally, Rita intermediate Santa expected we northern tains), Canyon, avail- (Florida nectar EF ability of regardless cotton wild bene®ted and 1500 ie oefla etradnal ortmsmore times four two nearly and produced nectar Caliente foliar In Agua more sugars. times other from over plants sucrose addition, prefer in ants may that system prediction the this to leads com- variation The Basin. positional in Molino at inositol highest were and nectaries fructose foliar of proportions However, from bene®ts ants. no than received Caliente plants Agua where Basin, at Molino greater at times ®ve sucrose than of more was comprised of carbohydrates 1). (Table concentration of volume proportion highest nectar The high the as well found as responsive we carbohydrates most nectar, in and population, EF bene®cial Caliente to most Agua were the ants In which wild ants. between interactions and geographic of cotton with outcome the corresponded in nectar variation EF of position residuals. the homosce- con- and of distribution total dasticity the the square-root improve arcsine to to was sugar transformed and or calculated acid was amino centration each contri- proportional of The bution 2000). pop- within Institute nested (SAS effect ulation random a plant, see and sub-bracteal, 1), or Table (foliar of type effects nectary the EF including population, ANOVA) per and examined (MANOVA mod- els nectaries linear general per 2±10 employed analysis calculated with Statistical plant. were plant Means per 1994). following nectary Hendrix Wei L. and D. (by Hendrix sugars for Gill- and liquid and 2001) (Gardener (high-pressure man acids HPLC amino for via samples chromatography) analyzed Nectar then microcapillaries. were glass nectar assessed with we h, volume 24 in After identically. treated only we collections and interested populations, were among differences may we relative physiology, cuttings altered Although nectary have accumulation. to of laboratory nectar abundance the permit in and maintained be- climate were probably Cuttings arid collection, visitors. the of of time lacked the cause Nectaries at 2001). nectar September visible (2±5 tubes water- to ®lled immediately transferred and cut, population), easse aito ntepouto n com- and production the in variation assessed We ouaindfeecsi h rdcinadcom- and production the in differences Population ENFRA UGR N AKC GARDENER C. MARK AND RUDGERS A. JENNIFER n ϭ 63 plants/ 16±32 aldt eosrt tesefc frdcdEF reduced of Rudgers, A. effect (J. ®tness production a nectar Canyon Florida demonstrate at to experiments of failed years the three despite investment, that nectar fact did EF in canyons differ Florida strongly not and Caliente Basin. Agua Molino from Surprisingly, plants did than nectar sub-bracteal hti¯ec rhoo iest n bnac,as abundance, and diversity factors arthropod the arthropod in¯uence diverse understand and that to large attempts a Thus, by total assemblage. visited the are of and fraction considerable ¯ora a nec- to EF contribute bearing taries plants of systems, dynamics some and In composition communities. the affect can resources nsaesaoa,bcuewl otntpclypro- December. to typically July cotton from wild leaves because duces seasonal, to bene®ts are (5) ants and pollinators, with thereby interactions and ¯oral re¯ect nectar EF in on investment selection constrain (4) may EF possibly nectar; nectar of some aphids, bene®ts tend (3) the also limiting 2002); the species negate (Rudgers ant may nectar nectar-visiting and EF nectar of EF bene®ts reduces covers that surfaces parasite algal leaf dominant an po- (2) a a cost; representing ecological of nectar, tential EF moths to attracted adult are (1) herbivore cotton context, example, wild the for community In system, broader complex. a more con- become in we predictions When nectaries traits. alternative EF nectary examine EF sider of that bene®ts studies and costs future (ants), envision nectaries EF to on we assumed selection ants. of is agent with what primary on the interactions be here the focused have of we view Although inadequate giv- an have would en population single wild a In examining nectaries. EF cotton, on nectar. selection understanding crit- EF to be ical may by populations fac- multiple mediated in in explorations are common Thus, be that will mutualisms traits among-population ultative nectary that EF predict in is We variation that ants. selection by con- variable mediated manner geographically a in with traits sistent nectary EF in vary populations al. et (Baker nectar EF of component asparagine 1978). typical 1); a Table not Basin, EF is Molino foliar in at asparagine (highest of only nectar proportion The the for 1978). was amino acids al. other individual of pro®les to et the in compared (Baker difference signi®cant high examined is nectars value found EF This not were samples. in some all acids although in amino nectar, 21 EF popu- found cotton we among wild total, vary In 1). not (Table did lations concentration acid amino de- other be to or termined. remains selection, operating are historical interactions represents ecological nectar investment high EF Canyon, in Florida at selection swamps script h vdnepeetdhr ugssta Fnectar EF that suggests here presented evidence The ecncnld rmteerslsta idcotton wild that results these from conclude can We carbohydrates, and volume in differences of spite In .Wehrgn o rmohrpopulations other from ¯ow gene Whether ). C ONCLUSION clg,Vl 5 o 6 No. 85, Vol. Ecology, nulse manu- unpublished June 2004 COMMUNITY AND EVOLUTIONARY NECTAR ECOLOGY 1501 well as analyses of terrestrial food web dynamics, could Acacia koa in the Hawaiian Islands. International Journal bene®t from considering EF nectar resources. In ad- of Plant Sciences 160:767±773. Del-Claro, K., and P. S. Oliveira. 1993. Ant±homoptera in- dition, because of the myriad species that forage for teraction: do alternative sugar sources distract tending ants? EF nectar, natural selection on EF nectary traits is likely Oikos 68:202±206. to re¯ect interactions beyond the protective services Dickson, L. L., and T. G. Whitham. 1996. Genetically-based offered by herbivores' enemies, such as ants. Finally, plant resistance traits affect arthropods, fungi, and birds. the widespread occurrence of spatial and temporal var- Oecologia 106:400±406. Eisikowitch, D., and G. M. Loper. 1984. Some aspects of iation in the outcomes of EF nectar-mediated interac- ¯ower biology and bee activity on hybrid cotton in Arizona, tions calls for an expansion of our investigations from USA. Journal of Apicultural Research 23:243±248. those focused on local dynamics to those that encom- Fischer, M. K., K. H. Hoffmann, and W. Voelkl. 2001. Com- pass geographic mosaics of selection. petition for mutualists in an ant±homopteran interaction mediated by hierarchies of ant attendance. Oikos 92:531± ACKNOWLEDGMENTS 541. Thanks to L. Adler, K. Clay, R. Irwin, R. Marquis, A. Fisher, B. L., L. da Silveira Lobo Sternberg, and D. Price. Packer, S. Richardson, K. Whitney, and two anonymous re- 1990. Variation in the use of orchid extra¯oral nectar by viewers for helping us to clarify our ideas about the com- ants. Oecologia 83:262±266. munity-level effects of EF nectar. D. Hendrix kindly analyzed Gardener, M. C., and M. P. Gillman. 2001. The effects of nectar sugar composition. 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York, Fernandes, New temperate W. and G. in and tropical ecology evolutionary Lewinsohn, interactions: Plant±animal M. editors. T. Benson, W. W. virescens auttv soitoswt ns saalbei S' lcrncDt Archive: Data Electronic ESA's in available is ants) with associations facultative fetaoa etre nwoy¯r ftoia com- tropical of 163±175 ¯ora Pages Brazil. woody Western in in munities nectaries extra¯oral of Sociobiology 310. and Ecology Behavioral aphids. and ees hoy iehsoyprpcie Oikos perspective. life-history a theory: defense Entomologist Canadian moth. 99 codling and caterpillars tent Environmental Entomology nectars. extra¯oral of components sugar and al hwn h oa ubro n pce eoddvstn lnswt xr¯rlncais(o lnsta have that plants (for nectaries extra¯oral with plants visiting recorded species ant of number total the showing table A :444±446. Lpdpea otia)t tmlto ihsug- with stimulation to Noctuidae) (Lepidoptera: 134 140 :210±218. 25 aap bignonioides Catalpa 22 350 :301±315. :411±417. :21±26. :58±59. 23 crm pyramidale Ochroma :93±95. oe Friia)i Yucatan, in (Formicidae) Roger 83 ENFRA UGR N AKC GARDENER C. MARK AND RUDGERS A. JENNIFER :1187±1194. 33 :755±760. lesetaoa nec- extra¯oral alters Oecologia . in .W Price, W. P. Lasius Heliothis 49 71 :304± :3±12. ants 43 APPENDIX : ugr,J .20.Eeiso ebvrscnsaeplant shape can herbivores of Enemies 2004. A. J. Rudgers, ugr,J . .Y tas,adJ .Wne.20.Re- 2004. Wendel. F. J. and Strauss, Y. S. A., J. Rudgers, cup .W,adD .Fee.19.Pyoey lifeform, Phylogeny, 1991. Feener. H. D. Cary, and W., Institute, E. SAS Schupp, 8.1. version SAS 2000. Institute. SAS ris eeto nafclaieatpatmtaim Ecol- mutualism. ant±plant ogy facultative a in selection traits: nihsfo ospee(avca) mrcnJournal Botany, American of (Malvaceae). traits: from resistance insights anti-herbivore in trade-offs and dundancy Torres-Herna geographic the on hypotheses Speci®c nectarivory. 1999. Spider N. J. 1996. Thompson, Foster. Irwin. A. W. E. and R. M., and R. Taylor, Lau, A. J. Rudgers, A. J. Y., S. Strauss, anr .19.Tei¯ec fatnsson nests ant of in¯uence The 1997. D. Wagner, Wa ip .M,adT .Wihm 01 idvriycon- Biodiversity 2001. Whitham. G. T. and M., G. Wimp, asoe .A,adD .Ptn 98 xr¯rlnectaries Extra¯oral 1988. Paton. C. D. and A., V. Vanstone, hte,K .20.Dseslfrdistance? for Dispersal 2002. D. K. Whitney, dis- nectaries extra¯oral Do 2002. Kay. A. and D., Wagner, ed n etants meat and seeds n aia eedneo n-eeddpat naPana- a 175±197 in Pages plants forest. ant-defended manian of dependence habitat and USA. Carolina, North .A egr.20.Efc fnca-oaigat and ants nectar-foraging of of ®tness Effect reproductive the on 2000. wasps Vergara. A. J. Naturalist American coevolution. of mosaic Entomologist American herbiv- Evolution to and resistance Ecology of in costs Trends ecological ory. and Direct 2002. UK. University Oxford, Oxford Press, interactions. Ant±plant editors. Cutler, ffla etrpouto ncto n atr nasof Annals castor. and cotton (London) dynamics in spatial Botany production and nectar temporal foliar on of herbivory of effect The rla ora fBotany of Journal tralian ces .L,D ue,R udri,adF elr 2001. Keller. F. and Wunderlin, R. Zuber, D. L., F. Èckers, eune fpeainadhs ln yrdzto nan on hybridization Ecology plant mutualism. host aphid±ant and predation of sequences Ecology eaee nacatlsn uei eio caZoologica Serie Acta Mexico. Nueva in Mexicana dune sand coastal a in neraceae) n olnto of pollination and rdcin ebvr n olntins ora fEcol- of Journal nutrients. ogy soil and herbivory production, rc nsfo iiig¯wr?A xeietlts of test Research experimental Ecology 4 An Evolutionary hypothesis. ¯owers? overlooked visiting an from ants tract 85 :293±305. :195±205. 85 :83±93. 27 ne,L,V ioGa,C atloGeaa and Castillo-Guevara, C. Rico-Gray, V. L., Ândez, npress in :589±595. clgclArchives Ecological ccapycnantha Acacia 87 . :365±370. rdmre viridiaeneus Iridomyrmex 81 42 36 :13±21. :82±86. :519±531. in 82 .R ulyadD F. D. and Huxley R. C. :440±452. clg,Vl 5 o 6 No. 85, Vol. Ecology, unr ulmifolia Turnera et.b id.Aus- birds. by Benth. E085-040-A1. 17 :278±285. ccaligulata Acacia 153 Acacia :S1±S14. Austral . (Tur- seed