Ecology, 85(6), 2004, pp. 1503±1511 ᭧ 2004 by the Ecological Society of America

THE DUAL ROLE OF FLORAL TRAITS: POLLINATOR ATTRACTION AND PLANT DEFENSE

REBECCA E. IRWIN,1,2,5 LYNN S. ADLER,3 AND ALISON K. BRODY2,4 1Institute of Ecology, University of Georgia, Athens, Georgia 30602 USA 2Rocky Mountain Biological Laboratory, Crested Butte, Colorado 81224 USA 3Department of Biology, Virginia Tech, Blacksburg, Virginia 24060 USA 4Department of Biology, University of Vermont, Burlington, Vermont 05405 USA

Abstract. Plants are under siege from a diversity of enemies that consume both leaf and ¯oral parts. Plants resist damage to leaves in a variety of ways, and we now have a rich literature documenting how plants defend themselves against attack. In con- trast, the mechanisms by which plants resist enemies that consume ¯oral parts or resources are much less known, even though damage to ¯oral tissue usually has tighter links to plant ®tness than damage to leaf tissue. Many plants experience nectar robbing, whereby ¯oral visitors remove nectar from ¯owers, often without pollinating. Nectar robbers can reduce plant ®tness to degrees comparable to, or even surpassing, reduction by . How- ever, because nectar attracts both pollinators and nectar robbers, plants face a dilemma in defending against nectar robbers without also deterring pollinators. Here, we extend the conceptual framework of resistance to herbivores to include resistance to nectar robbers, focusing on nectar traits. We review published data and ®nd that an array of nectar traits may deter robbers without deterring pollinators. Although resistance traits against robbers have been broadly identi®ed, the costs and bene®ts of these traits in terms of plant ®tness remain poorly understood. We present data showing that a nectar trait (dilute nectar) might Feature Special directly, as well as indirectly, bene®t plant ®tness by deterring nectar-robbing bumble bees of Ipomopsis aggregata without deterring pollinators. However, the magni- tude of any plant ®tness bene®t will depend on the degree to which plants are - vs. resource-limited in a given year. The results of our work offer both conceptual and empirical insight into how plants cope with attack by nonpollinating ¯oral visitors through a relatively unexplored trait, nectar. Key words: Bombus occidentalis; bumble bee; herbivory; Ipomopsis aggregata; nectar concen- tration; nectar robbing; plant defense; ; resistance.

INTRODUCTION to resist enemy attack may be more dif®cult when mu- Plants are attacked by a variety of organisms that tualists and antagonists use the same resource, such as feed in different ways and on different types of tissue. nectar. Organisms that feed on nectar without providing At any given time, a plant may face damage by her- pollination service in return (henceforth referred to as bivores feeding on leaves or ¯owers, while others feed ``nectar robbers'' or ``nectar thieves'') can have sub- on roots, and still others consume sap, phloem, or xy- stantial effects on male and female plant ®tness (re- lem. The defenses deployed against such enemies can viewed in Irwin et al. 2001). A meta-analysis of ex- be constitutive or induced (Bryant et al. 1988, Karban isting studies suggests that ¯oral larceny has an overall and Meyers 1989). The defenses can be quite general detrimental effect on female plant reproduction (Irwin and effective against many organisms (Krischik et al. et al. 2001), although individual studies ®nd that nectar 1991, Omer et al. 2001), or highly speci®c and effective robbing can have a continuum of effects on plant re- against a single type or species of herbivore (Agrawal production, from positive to neutral to negative (Ma- and Karban 2000). By mounting defenses against en- loof and Inouye 2000). Nectar robbers can reduce plant emies, plants increase their resistance to further feeding ®tness to degrees comparable to, or even surpassing, and, presumably, minimize the ®tness costs of damage ®tness reduction by herbivores (Juenger and Bergelson (Karban and Myers 1989). 1997, Irwin and Brody 2000). Damage to ¯oral tissue Resistance is the ability of plants to decrease the can have stronger links to plant ®tness than does dam- frequency of attack (Painter 1958). The ability of plants age to leaf tissue (reviewed in Strauss et al. 2003); nectar robbing can reduce female ®tness by 50% (e.g., Manuscript received 9 June 2003; revised 2 September 2003; Irwin and Brody 2000, Lara and Ornelas 2001) and accepted 8 September 2003. Corresponding Editor: A. A. Agra- estimates of male ®tness by up to 80% (Irwin and Bro- wal. For reprints of this Special Feature, see footnote 1, p. 1477. dy 1999). Yet, the mechanisms by which plants resist 5 Address for correspondence: Institute of Ecology, Ecol- ogy Building, University of Georgia, Athens, Georgia 30602 nectar robbers are less well known than mechanisms USA. E-mail: [email protected] associated with resistance to herbivores. This lack of 1503 Special Feature r n edpeaos(err 92 ioln and Cipollini 1982, (Herrera 1997). predators Levey seed dispers- seed and with an- ers interactions and plant which mutualists as such in attracting tagonists, in interactions trade-offs plant±animal face functionally plants other and to applicable are similar is presented work predictions results this the robbers, and Although nectar ®eld. to resistance this on future focused in suggest research and of data new areas and present herbivores then We to robbers. resistance impor- between but subtle similarities the tant re- highlighting on robbers, literature to to the sistance review herbivores We robbers. to nectar resistance include of framework conceptual robbers? nectar attract at- avoiding plants the while in might pollinators how and in Thus, 1991) robbers. both (Pyke nectar costly, tracting invested be resources of can amount pollinators attracting payment the However, for 1998). al. et Kearns in plants (reviewed ¯owering of majority the mu- the of to for success reproductive critical reward is a attraction Pollinator this as pollinators. nectar of tualist providing nature in The lies herbivores. quandary leaf-feeding preventing by in attack experienced not conundrum a with plants plant affect negatively robbers which be ®tness. in can rob- cases nectar resistance in with of cope bers plants concept how understand the to that applied likely seems (e.g., it taxa Bro 1999, across al. theory et Agrawal unifying pre- a as providing an- such dation, 2000). other herbivory, to Brody besides applied interactions and been tagonistic have Irwin resistance 1996, of al. Concepts et be- as (Strauss pollinator well in havior as changes 2001), as such al. mechanisms, et indirect Adler 1983, reproduc- include (Galen ¯oral These organs to tive damage herbivores. as of such mechanisms, those direct to analogous ®tness are plant affect the robbers Moreover, nectar which larceny. by spurs ¯oral mechanisms nectar of with form ¯owers some or experience spe- corollas plant tubular Most with 2002). cies Maloof and (Irwin reasons. plants ¯ow- of ering among common number extremely is a robbing nectar for First, surprising is understanding 1504 sdb eiiaepliaosbtd o otc the contact not do opening but ¯oral pollinators the legitimate through by nectar used remove through Nec- pollinating. thieves nectar without tar often remove ¯owers, that in bitten organisms holes those rob- nectar as de®ne bers without we larcenists Hereafter, ¯oral pollinators. to deterring resistance these of confer Some can phys- resistance. traits (4) indirect space, (5) in and escape barriers, deter- (3) ical time, chemical in and escape (2) (1) rents, involve can nec- robbers to resistance tar herbivores, with As resistance robbers. and nectar to herbivores to resistance with associated h i fti otiuini oetn h existing the extend to is contribution this of aim The presents however, robbing, nectar to Resistance hr r tiigsmlrte ewe mechanisms between similarities striking are There R SSAC TO ESISTANCE nake l 99.Therefore, 1999). al. et Ènmark N ECTAR R OBBING EEC .IWNE AL. ET IRWIN E. REBECCA we rista ofrrssac ohrioe and herbivores to robbers. nectar resistance be- to effects confer resistance pleiotropic that re¯ect traits also tween may Many traits interactions. these different of very been other, have into that inter- herbivores) co-opted and or plants pollinators between and actions most plants robbers between interactions to of set (interactions one resistance in involved confer traits represent that likely robbers, Traits by selection se. to response per in evolve not did and that 1997) thus (Armbruster robbers exaptations many, against are that traits describe will resistance likely we the is of it most, not robbers, if nectar deter that traits nec- to applicable thieves. only tar scenarios describe we cases which in in except robber'' ``nectar and term robbers the nectar under (both thieves) larcenists ¯oral all simplicity, include For we 1980). (Inouye ¯owers of organs sexual euetefeunyo etrrbig In robbing. nectar may of nectar frequency toxic the that reduce suggest examples (Ad- few debated a are 2000), nectar'' ler ``toxic of Al- 2000). bene®ts Adler the 1977, though (Baker nectar ¯oral in surprisingly common are toxins) or compounds (secondary tance olntr Sehno 91 92.In bee 1982). legitimate 1981, deter (Stephenson not did pollinators but nectar-thieving loafc h rqec fnca obn.Frex- For robbing. of nectar ¯owers of the frequency ample, the affect also pol- ®tness. affect also plant toxins ultimately, the and, which de- linators to will degree nectar the toxic on of pend deter bene®ts the may however, compounds robbers; secondary that demonstrate stud- the These ies tested. explicitly protect been al- never has ants, to this nectar-thieving though serve or Secondary nectar-robbing may nectar. from plants the released into thus tissue compounds com- secondary from a release on can pounds species ants tropical by of damage variety corolla-tube that suggest Fiedler (1981) and Guerrant 1996). Baldwin and (Euler pounds oto eue iiainb eiiaebepolli- Irwin, bee E. legitimate R. and by Adler visitation S. (L. reduced nators of at cost but bees, a carpenter nectar-robbing deterred nectar in lhuhoemgtacieaatv ucinto function adaptive ascribe might one Although aa rvc es.Lwsgrcnetaini nectar in concentration sugar Low versa. deter vice pollinator could or some taxa, luring composition while taxa nectar pref- nectar-robbing some that in variation implies such erence unexplored, acid Gillman Although amino and 2002). (Gardener speci®c concentrations with or nectar components nectar- prefer deter visitors to ¯oral (Pry hypothesized ants is thieving bumble but to pollinators tolerable dissolved of bee is presence ammonia the to Dissolved due ammonia. pH high a with nectar uscript ciosa sempervirens ln opud soitdwt ebvr resis- herbivore with associated compounds Plant ua n te oemnrnca opnnsmay components nectar minor more other and Sugar etrcnann rdi lcsdsdeterred glycosides iridoid containing nectar , .Ptltsu a locnanscnaycom- secondary contain also can tissue Petal ). oisadceia deterrents chemical and Toxins xeietlmnplto falkaloids of manipulation experimental , sJnsadWlmr19) Some 1992). Willmer and Ãs-Jones ahaaclandestina Lathraea clg,Vl 5 o 6 No. 85, Vol. Ecology, nulse man- unpublished aap spe- Catalpa Gelsemium produce June 2004 COMMUNITY AND EVOLUTIONARY NECTAR ECOLOGY 1505 may deter nectar-robbing bees without deterring some Ornelas 2001). Bract liquid that can create a ``moat'' pollinators. Bolten and Feinsinger (1978) argue that around ¯owers may prevent nectar-robbing ants from dilute nectar does not yield net energy pro®ts for some gaining access to nectar (Wootton and Sun 1989). Fi- nectar-robbing bees. However, dilute nectar with low nally, the toughness of the corolla or calyx may make viscosity might not deter some legitimate pollinators, it dif®cult for robbers to chew holes. For example, in such as , that feed by capillary action central Panama, it takes solitary workers of the bee (Baker and Baker 1982; but see Pyke and Waser 1981, Trigona ferricauda Ն30 min to chew a hole 2±4 mm MartõÂnez del Rio et al. 2001). As far as we know, this in diameter through the calyces of Pavonia dasypetala hypothesis has never been explicitly tested. from which it steals nectar (Roubik 1982). Escape in time Indirect resistance Just as plants can escape herbivore damage by lea®ng Predators of nectar robbers may also serve to protect out when herbivores are absent or rare (Feeny 1970), plants. For example, some plants produce extra¯oral plants can avoid damage from nectar robbers by vary- nectaries (nectar-secreting tissues located on leaves, ing their timing of nectar production or ¯owering (Ir- stems, or external calyces of ¯owers) that attract ants win et al. 2001). For example, if nectar robbers and that deter herbivores. Keeler (1977) found that ants pollinators are active at different times of day, plants attracted to the extra¯oral nectaries of Ipomoea carnea may bene®t by producing nectar on a diel rhythm that also deterred carpenter bees from robbing ¯owers. Ad- coincides with peak pollinator activity and relative in- ditional bene®ts of extra¯oral nectaries are reviewed activity of robbers. Hummingbird pollinators forage in detail in Rudgers and Gardener (2004, this Special most actively in the morning and late afternoon on Feature). Castilleja linariaefolia, times when nectar-robbing car- penter bees are relatively inactive due to cool temper- RESISTANCE TRAITS AND PLANT DEFENSE atures (Carpenter 1979). Although C. linariaefolia pro- Although traits that might confer resistance to nectar duces nectar all day, peak rates of nectar production robbers have been identi®ed, little is known about Feature Special occur in the morning and late afternoon, coinciding whether these traits actually defend plants against nec- with peak pollinator visitation and low nectar-robber tar robbers. Using Karban and Myers' (1989) classi- visitation (Carpenter 1979). ®cation, a defense trait not only must decrease the pref- erence (or performance) of nectar robbers but also must Escape in space increase plant ®tness in the presence of robbers. Plants may also escape nectar robbers by growing It might seem intuitive that traits that decrease nectar next to host plants that are more preferable to robbers, robbing should increase plant ®tness; however, this loosely analogous to associational resistance to her- need not be the case. For example, constitutive traits bivores (Tahvanainen and Root 1972). The most com- that provide a fairly constant and effective deterrence pelling evidence thus far for associational resistance to against robbers might incur both allocation costs (re- robbers comes from Ipomopsis aggregata (scarlet gi- source-based trade-offs between resistance and ®tness) lia), which is robbed by Bombus occidentalis (Irwin and ecological costs (trade-offs between resistance and Brody 1998). Where I. aggregata co-occurs with traits and interactions with other organisms, such as Linaria vulgaris, a species introduced to the Colorado mutualists; Strauss et al. 2002). Moreover, plants may Rocky Mountains over 100 years ago, robbing rates to be able to compensate for damage to ¯oral reproductive I. aggregata are 68% lower than in areas where L. structures or loss of nectar by producing more ¯owers vulgaris does not occur. Bombus occidentalis prefers or by increasing nectar production rate (analogous to L. vulgaris, which receives 60% more robbing than I. tolerance to herbivores; Strauss and Agrawal 1999). In aggregata where the two species grow together. Thus, cases in which robbers do not damage plant reproduc- L. vulgaris provides associational resistance to I. ag- tive structures and pollinators are unaffected by the gregata by luring away robbers, resulting in decreased reduction of nectar due to robbing, a plant may gain robbing and increased seed set of I. aggregata where no bene®t in deterring robbers. Finally, recent theo- the two species co-occur (Irwin et al. 2001). retical studies suggest that mutualisms, such as those between plants and pollinators, can persist even in the Physical barriers presence of cheaters that have negative consequences Physical barriers, such as thick leaves, thorns, and on the (Morris et al. 2003). trichomes, are effective at deterring herbivores. Simi- Although traits conferring resistance to herbivores larly, a variety of physical traits may confer resistance have been linked to plant ®tness (reviewed in Marquis to nectar robbers without deterring pollinators. Tightly 1992), evidence that resistance to nectar robbers affects packed ¯owers may physically deny nectar robbers ac- plant ®tness is largely lacking. Only one study, to our cess to nectar spurs or the sides of corolla tubes (Proc- knowledge, has measured the ®tness consequences of tor et al. 1996). Short corolla tubes may decrease the a resistance trait to robbers. L. S. Adler and R. E. Irwin frequency of robbing by some hummingbirds (Lara and (unpublished manuscript) experimentally manipulated Special Feature laod ntenca of nectar the in alkaloids 1506 utn nicesdfml tesi pollen-limited a in ®tness plant. re- female (1978), increased Feinsinger in and sulting Bolten by pollina- proposed as hummingbird tors, deterring without bees nectar- deter robbing would nectar nectar). dilute dilute concen- whether as examined to sugar We referred low (hereafter nectar associated trait, in bene®ts resistance tration ®tness putative the one examining with by address to gap attempt we as this Here traits, costs. potential these their of as most well the with of associated ignorant bene®ts relatively ®tness remain we robbers, nectar to arti®cial of example, For tissue nectar. ¯oral in to or plant damage a ¯oral on all in on tissue chemicals tissue secondary to induce may Damage ¯ower 1996). one Baldwin and within in- (Euler can hours same tissue those to petal compounds in to secondary Damage duce production nectar. chemical or tissues secondary ¯oral increased responses, by plant as of tissue variety such a ¯oral induce to may robbers in Damage Huth nectar examined robbers. and been with not Pellmyr association has (e.g., induction However, mutualisms in 1994). exploitation of against kinds responses ev- other is induced there for and 1997), idence Baldwin are and lower damage (Karban might herbivore common plants to responses which Induced in costs. way such resistance one is of damage induction upon costs, ecological or allocation ntepeec frbes osuishv tackled have studies robbers. No nectar to robbers. responses of induced presence ®tness plant the increase must in and robbers nectar by attack subsequent reduce must response the however, favored, because parts. thieves ¯oral nectar damage not to do applicable mechanism they a not Such is nectar. or probably petals second- in of compounds production Thus, the ary ¯orivores. induce could by robbers produced nectar indis- that probably is from damage tinguishable their nectar, obtain to tissue D cation aae otos(.C McCall, C. un- subsequent to (A. compared controls for plants damaged damaged ¯orivores on of produced ¯owers preference the creased obr opat®ns r eddbfr n gener- any before made. needed be are can alizations ®tness plant against to traits resistance robbers relating nectar studies as More well robbers. as pollinators be- deterred nectar success toxic reproductive cause male decreased nectar Toxic aggregata O esuidtemnaeprnilherb perennial montane the studied We resistance confer might traits of variety a Although high carry robbers nectar against traits resistance If o nue epne gis etrrbest be to robbers nectar against responses induced For R ESISTANCE NDUCED .Bcuenca obr hwtruh¯oral through chew robbers nectar Because ). I Plmnaee,goigna h Rocky the near growing (Polemoniaceae), P R LANTS SOSSTO ESPONSES T RAITS ?AC Methods A GAINST esmu sempervirens Gelsemium ASE eohl menziesii Nemophila N ECTAR S TUDY esnlcommuni- personal R OBBERS R OBBERS EEC .IWNE AL. ET IRWIN E. REBECCA Ipomopsis B ENEFIT de- . 80m nteEkMutiso eta Colorado, central of Mountains RMBL, Elk the Around the USA. in elevation m, (RMBL), 2800 Laboratory Biological Mountain pmpi aggregata Ipomopsis Ͻ iaos(ri n rd 1998). Brody and pol- (Irwin hummingbird by linators ¯owers and 50% plants avoid- to robbed by due of effect ance reproduction indirect an plant 2000), Brody and female (Irwin and male reduce spat®ns) edpouto n fsrn re- offspring and for production correlated positively to Seed are referred cruitment ®tness). (hereafter plant plant per as produced ceased seeds num- of total plants the ber as ®tness When female estimated we concentration. blooming, whole-plant estimate reliable a of provided probably plant per ¯owers obrhlso ahpat(si ri n Maloof and Irwin in in knowledge, (as our plant To each 2002). the on with counting ¯owers holes of by number robber the week and ¯owers per open of times number two estimated robbing we season, nectar ¯owering each the of km Throughout 2 other. within were and species ¯owering curring tto w ie e ekuigsim olnloads pollen stigma In using indices. week as per times two itation Ͼ ig h esnihrpliaetepatnrdamage Irwin, E. nor structures (R. nectar-producing plant or the reproductive rob- plants' pollinate While the neither visit. single bees a the re- in they bing, nectar which available through corolla all the move of side the through hntevrac nnca ocnrto mn plants ( among concentration (6.25%) nectar in lower variance con- signi®cantly the nectar is than in (2.88%) plants variance peak within The at centration plant. days each sunny for on ¯owering midday with at and sampled concentration only daily sugar we 1983), vary (Pleasants conditions can weather Be- concentration USA). nectar York, IFT40, New cause per (Leica Buffalo, ¯owers refractometer Microsystems, unrobbed hand-held Leica bagged, a two using nectar of plant of average equivalents) an sucrose on of (mea- percentage and concentration in (Engel sugar sured measured receipt We pollen 2003). increased Irwin in results tation ( bee, rmrl nBodtie ( Broad-tailed on The primarily rely ¯owers. and self-incompatible, trumpet-shaped hermaphroditic, are ¯owers red, numerous ducing ino ln a emaue noe¯wrn season. ¯owering one in measured be dies can plant and reproduc- a lifetime of once, tion Therefore, ¯owers 1989). Price years, and 2±7 (Waser for rosette etative raim omnyselnca hog h holes the through by nectar made steal commonly organisms ffu ie,ec cuidby occupied each sites, four of n uosHmigid ( Hummingbirds Rufous and data gregata n19,w admycoe10 chose randomly we 1998, In 0 faalbe¯wr obd r omnand common are robbed) ¯owers available of 80% .1 .E ri n .K Brody, K. A. and Irwin E. R. 0.01; h oesof ¯owers The .Teeoe esrn ua ocnrto ntwo in concentration sugar measuring Therefore, ). obsoccidentalis Bombus lns l ie a iia lp n co-oc- and slope similar had sites All plants. .occidentalis B. F S ϭ nulse data unpublished .aggregata I. .7 df 2.17, .aggregata I. oesfor ¯owers eetmtdpliao vis- pollinator estimated We . ϭ .aggregata I. h esce hole a chew bees The . nrae olntrvisi- pollinator increased , ,254, 1, eapou platycercus Selasphorus .rufus S. .Hg eeso robbing of levels High ). r obdb bumble a by robbed are .aggregata I. Ͼ clg,Vl 5 o 6 No. 85, Vol. Ecology, 0 ¯owering 200 .aggregata I. ϳ N o pollination. for ) ± ek,pro- weeks, 4±8 ϭ .aggregata I. rw saveg- a as grows 5 plants, 256 unpublished oother no , neach in .ag- I. (N. P ) June 2004 COMMUNITY AND EVOLUTIONARY NECTAR ECOLOGY 1507 pca Feature Special

FIG. 1. Four competing path diagrams testing the direct and indirect effects of sugar concentration of nectar (nectar conc.) on pollinator visitation (estimated as pollen receipt to stigmas), nectar robbing, and plant ®tness (estimated as seed set). In all models, there is unexplained variation [(1 Ϫ R2)0.5] associated with the measurement of pollinator visitation, nectar robbing, and seed set. See Methods for explanation of the models.

M. Waser, M. V. Price, A. K. Brody, and D. R. Camp- Model A (Fig. 1), dilute nectar directly affects plant bell, unpublished data). ®tness and indirectly affects plant ®tness through To examine whether dilute nectar deters robbing bees changes in robber and pollinator behavior. Al- without deterring pollinating hummingbirds, we used though the physiology of nectar production in I. ag- path analysis combined with structural equation mod- gregata is unknown, to our knowledge, plants could eling (SEM; for a review see Mitchell [1993]) to com- produce dilute nectar by putting more water in the nec- pare four competing a priori hypotheses (Fig. 1). In all tar or by putting less sugar in the nectar. Thus, the models, nectar concentration affects hummingbird and direct effect of producing dilute nectar on plant ®tness bumble bee preference, given that both birds and bees could be negative if plants are water limited, or positive forage selectively on sugar rewards (reviewed in Proc- if sugar is costly. In Model B, all paths remain identical tor et al. 1996), and pollinator visitation directly affects to those of Model A except that the path between dilute female plant ®tness (Campbell and Halama 1993). In nectar and ®tness is constrained to zero, assuming that Special Feature cosstsuigPO ICI,option DISCRIM, PROC P using variables the of sites POOL homo- structure for covariance across tested the we of hypothesis), geneity relevant between (the within individuals correlations sites among than of rather sites, across in¯uence traits avoid confounding To 2002). al. the likelihood et other (Strauss with the traits correlated resistance minimized spuriously putative thus was nectar and dilute sites that in of plants variety with worked a we compensate, To crosses. mono- plant. long-lived experimental carpic a with of possible not series was this a However, using was by concentration expressed nectar which in background genetic plant enhanced and resulting visitation ®tness. nectar, that pollinator dilute increased expect with in we plants avoid robbers, will nectar robbers to nectar dilute resistance If zero. confers to dilute constrained between identical is path ®tness the remain and that nectar except paths C all Model of D, those to Model (Car- limited In are 1979). resources penter a nectar selective at when less resource plants become limited among pollinators a and is plants, scale nectar robbed landscape if avoid occur not could do which C pollinators Model behavior. that pollinator effect assumes through indirect no ®tness have plant those robbers to on that identical except remain A paths Model to all of bene®t C, or Model cost In allocation direct plants. no has nectar dilute 1508 et h to h orlto arxo lentv path alternative of matrix correlation the of ®t the tests ooeet ftecvrac tutr ( of structure hypothesis covariance null the the of reject to homogeneity evidence no found We icnl rmteosre data. observed the from ni®cantly Model ABLE T Signi®cant ² )uigsrcua qainmdln (SEM). modeling equation structural using 1) dal,i hssuyw ol aecnrle the controlled have would we study this in Ideally, ϭ ocmaetefu oes eue E,which SEM, used we models, four the compare To kiesIfrainCriterion. Information Akaike's ³ D C B A .8;teeoe epoe h aaars sites. across data the pooled we therefore, 0.18); ϭ .Acmaio fatraiept igas(Fig. diagrams path alternative of comparison A 2. ET(A eso ;SSIsiue2001). Institute SAS 8; Version (SAS TEST 20.58 17.83 3.11 0.36 ␹ 2 ®tness Plant robbing Nectar visitation Pollinator concentration Nectar ␹ ABLE 2 siaesim-olnla o olntrvstto;22.52 visitation; pollinator for load stigma-pollen estimate o etrrbig 487.17 robbing; nectar for Note: urs qiaet o etrcnetain 92.61 concentration; nectar for equivalents sucrose ausidct httemdl eit sig- deviate models the that indicate values T obrvstto,adpat®tness. plant and visitation, robber Variables .Osre orltos( correlations Observed 1. ausfrec aibe(mean variable each for Values 3 2 2 1 df 0.0001 0.0001 0.2111 0.5490 P AIC³ ² Ϯ 14 5±40 ed/ln o ln ®tness. plant for seeds/plant (52±1400) 61.42 concentration EEC .IWNE AL. ET IRWIN E. REBECCA ␹ Nectar 2 r Ϫ Ϫ Ϫ Ϫ ϭ 14.58 13.83 mn ua ocnrto nnca,pliao n nectar- and pollinator nectar, in concentration sugar among ) 0.30 0.45 0.08 0.89 1.64 36.64, Ϯ 1 SE Tbe1 sn odeso-tsaitcta a an has that statistic data goodness-of-®t the approximate a of using matrix 1) correlation (Table observed the to models n ag)ae23.21 are range) and Pollinator icn ifrnebtenMdl n ( B nonsig- and A a Models found between We difference took ni®cant 1993). we (Mitchell freedom de- B, and of and statistics grees further goodness-of-®t A their To Models in data. difference of the ®t the relative to the ®ts compare both reliable that suggesting provided 2), models (Table data observed the from iiainNca obn ln ®tness Plant robbing Nectar visitation S(A eso ;SSIsiue2001). Institute SAS 8; Version CAL- PROC (SAS in IS conducted were levels. analyses signi®cance statistical All and regression effects, cal- partial indirect we data, (standardized coef®cients), diagram observed effects path the direct to the ®t culated For best data. the the provided that to ®t reasonable most tesin ®tness (Martõ se dilute for per preference nectar, pollinator not avoidance and pollinator plants through robbed of mediated nectar be dilute to of likely bene®ts are any Therefore, 2). robbed (Fig. avoided plants strongly pollinators However, 2). (Fig. signi®cant statistically not a but visitation, was and hummingbird concentration There nectar robbers. between relationship nectar positive to resistance nectar confer dilute may that suggesting robbing, less signi®cantly A Model retained 2). we Fig. B, 2, Model (Table than value AIC lower iie sntucmo.Ple eep osimsin stigmas to receipt pollen Pollen are Among- uncommon. plants 2). not which (Fig. is to 1998 degree limited in the in set variation seed year in variation the of little relatively explained visitation pollinator increased nication l ihmr aaees(.. e feto adding of Institute, effect SAS net paths; a and (i.e., variables parameters more mod- with Akai- penalizes report els AIC also (AIC). We Criterion data. Information the ke's to pro- ®t observed model reasonable the the a that vides from suggesting data, signi®cantly the in differ di- correlations path not the do in correlations agram expected the that indicates df ete oe o oe ifrdsigni®cantly differed B Model nor A Model Neither lhuhpliao iiainuulylmt female limits usually visitation pollinator Although experienced nectar dilute with plants A, Model In Ϫ ϭ Ϯ 0.21 0.61 1, .1(216 olngan/tgato grains/stigma pollen (22±196) 7.21 Ϯ .Temdlta iiie I rvdsthe provides AIC minimizes that model The ). P .3 010)o oesrobbed ¯owers of (0±100%) 6.93% .aggregata I. ϭ ␹ 2 .) eas oe a slightly a had A Model Because 0.1). itiuin nonsigni®cant A distribution. Ϫ Ϯ 0.18 nzdlRoe l 2001). al. et Rio del Ânez .3 (15.00±30.83%) 0.63% Cmbl n aaa1993), Halama and (Campbell Results clg,Vl 5 o 6 No. 85, Vol. Ecology, esnlcommu- personal ␹ 2 ␹ ϭ 2 value 2.75, June 2004 COMMUNITY AND EVOLUTIONARY NECTAR ECOLOGY 1509

FIG. 2. Path diagram that provided the best ®t to the observed correlation matrix (Table 1), identi®ed using SEM (Table 2). Positive effects are indicated by solid lines, and negative effects by dashed lines. The widths of the arrows indicate the magnitude of the standardized path coef®cients. Pathways signi®cant at P Ͻ 0.05 are denoted by an asterisk. The residual variables for pollinator visitation (U1), nectar robbing (U2), and seed set (U3) indicate unmeasured factors.

1998 was Ͼ20% higher than in 2001, another year in set, suggesting that nectar may play a dual role of re- which we measured this response variable (F1,72 ϭ 4.42, ward and defense in some years. P ϭ 0.039; Engel and Irwin 2003), suggesting that seed A variety of questions must be addressed before we set was not limited by pollen receipt in 1998, and/or can fully understand the degree to which nectar traits Feature Special that resources also limited seed production in the year defend plants against nectar robbers. We list three in- of study (R. E. Irwin, unpublished data). Because the triguing and challenging questions. link between pollinator visitation and female ®tness (1) Are there allocation and/or ecological costs as- was weak, robbing had only a marginally negative ef- sociated with resistance to nectar robbers?ÐTheories fect on plant ®tness mediated indirectly through the of plant defense rely on the assumption that plants ex- avoidance of robbed plants by pollinators. perience costs associated with resistance traits (McKey Dilute nectar had a weak, nonsigni®cant direct ®tness 1974). Otherwise, we would expect plants to be max- bene®t to plants (Fig. 2). The marginal direct bene®ts imally resistant. Plants do incur both allocation and of dilute nectar to plant ®tness outweighed the indirect ecological costs associated with resistance to herbi- bene®ts through decreased robbing and increased pol- vores (recently reviewed in Strauss et al. 2002). How- lination, probably because plants were only weakly pol- ever, almost nothing is known about costs of resistance len limited. In years with strong pollen limitation of to nectar robbing. Robbing levels vary widely both seed set, the indirect bene®ts of dilute nectar on resis- geographically and temporally (Irwin and Maloof tance to robbing might outweigh the direct bene®ts. 2002), and variability in robbing may constrain selec- This might be the case because of the strong links tion for resistance traits that are costly to produce. Giv- between robber avoidance of dilute nectar and polli- en the crucial importance of both pollinators (Dodd et nator avoidance of robbed plants. To further test this al. 1999, Grimaldi 1999) and herbivores (Becerra 1997, hypothesis, we need to experimentally manipulate nec- Farrell 1998) in shaping plant evolution and speciation, tar concentration in combination with resource avail- it is essential to integrate robbers, which could in¯u- ability and pollen limitation, measure subsequent levels ence both plant secondary compounds and ¯oral traits, of robbing, and assess male and female plant ®tness. into our conceptual framework of plant±animal inter- actions. CONCLUSIONS AND AVENUES (2) Can plants tolerate the negative effects of nectar FOR FUTURE RESEARCH robbers?ÐResistance represents just one strategy that Nectar serves as an important reward, mediating in- plants use to cope with attack. Plants may also be able teractions between plants and pollinators. Here we to tolerate the negative effects of robbing, incurring show that particular nectar traits may also confer re- few, if any, ®tness consequences as a result of damage. sistance against nectar robbers. To understand the evo- The negative effects of robbers may be tolerable if, for lutionary ecology of nectar traits that provide resis- example, plants can produce enough nectar to feed all tance, we need to quantify their costs and bene®ts. For ¯oral visitors. Tolerance to herbivory is common Ipomopsis aggregata, dilute nectar deters nectar-rob- (Strauss and Agrawal 1999) and may represent an al- bing bumble bees. Dilute nectar may also increase plant ternative or additional defensive mechanism to resis- ®tness in years of strong pollinator limitation of seed tance (Fineblum and Rausher 1995, Mauricio et al. Special Feature ae,H . n .Bkr 92 hmclcnttet of constituents Chemical 1982. Baker. I. and G., H. Baker, nectar. of constituents chemical Non-sugar 1977. G. H. Baker, plant± of evolution link Exaptations 1997. S. W. Armbruster, Trans- 1999. Tollrian. R. and Laforsch, C. A., A. Agrawal, consti- of Speci®city 2000. Karban. R. and A., A. Agrawal, de,L . .Kra,adS .Srus 01 ietand Direct 2001. Strauss. Y. S. and Karban, R. S., L. Adler, nectar. toxic of signi®cance ecological The 2000. S. L. Adler, negative the mitigates robbing. tolerance of addressed which effects have to knowledge, degree our the to studies, No 1997). 1510 ygat rmteNtoa cec onain(DEB- Foundation Georgia. from Science of funds University by National the and the DEB-0211480) DEB-0089643, from 9806501, supported was grants co-authors the by among collaboration and for work travel laboratory a and provided Field environment. Laboratory work Biological Ecol- stimulating Nectar Mountain Agrawal on Rocky A. Feature The Special and ogy. this manuscript, organizing with the help on for reviewer comments anonymous one valuable and for Rudgers, J. McCall, A. Burkle, epneo lnst iutnosatc ymultiple by attack simultaneous enemies? to plants of evolutionary response the impact traits resistance herbivore and ret hc lnscnceov ihayoeenemy. one any with coevolve de- can the plants have which affecting may to ®tness, gree plant plant host on same effects the non-additive share nat- Moreover, that agent. enemies selective ural one any to plants respond which to can degree and the herbivores constrain may against robbers nectar correla- traits Genetic resistance 2001). between Ber- Cuba and tions and Juenger Galen (e.g., infancy 1998, its gelson in still in- is multiple-species been teractions of long outcomes evolutionary has ecolog- and the ical plants of understanding host our however, shared among recognized; their interactions and indirect and enemies direct The of predators. complexity seed and ¯orivores, in- herbivores, antagonists, cluding other includes that framework broader Bro hummingbird do Why 1978. Feinsinger. P. and B., A. 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