Fo Pee Re iew
In e ac ion equency and pe in e ac ion e ec s as
p edic o s o o al e ec s in plan -pollina o mu ualisms: a
case s udy wi h he sel -incompa ible he b Lina ia lilacina.
Jou nal:
Oecologia
Manusc ip ID:
OEC-KG-2010-0548.R3
Manusc ip Type:
o iginal esea ch pape
Da e Submi ed by he
Au ho :
n/a
Comple e Lis o Au ho s:
Sanchez-La uen e, Al onso; Uni e sidad de Se illa, Biologia Vege al
y Ecologia
Rod iguez-Gi ones, Miguel Angel; Es acion Expe imen al de Zonas
A idas (CSIC)
Pa a, Raquel; Uni e sidad de Se illa, Biologia Vege al y Ecologia
Keywo ds:
mu ualis ic ne wo ks, plan -pollina o in e ac ions, isi a ion a e,
bou leng h, pollen deposi ion
Oecologia
Fo Pee Re iew
Sánchez-La uen e e al. In e ac ion equency and o al e ec s in Lina ia - 1
In e ac ion equency and pe in e ac ion e ec s as p edic o s o
o al e ec s in plan -pollina o mu ualisms: a case s udy wi h he
sel -incompa ible he b Lina ia lilacina.
Sho i le: In e ac ion equency and o al e ec s in Lina ia
Al onso M. Sánchez-La uen e1, *, Miguel A. Rod íguez-Gi onés2 and Raquel Pa a1
1Depa amen o de Biología Vege al y Ecología, Facul ad de Biología, Uni e sidad de Se illa, A d. Reina
Me cedes 9, 41012 Se illa, Spain
2Es ación Expe imen al de Zonas A idas (EEZA-CSIC), C a. de Sac amen o s/n, La Cañada de San U bano,
04120 Alme ía, Spain
*Co esponding au ho
email: al onso@sla uen e.es
Fax: +34-953-294570
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Abs ac
I is widely ecognized ha pollina o s a y in hei e ec i eness in pollina ion mu ualisms, due bo h o
di e ences in lowe -pollina o mo phological i as well as pollina o beha iou . Howe e , pollina ion webs
ypically ea all in e ac ions as equal, and we con end ha his me hod may p o ide misleading esul s. Using
empi ical and heo e ical da a, we p esen he case s udy o a sel -incompa ible he b in which he numbe o
lowe s isi ed by a pollina o canno be used as a su oga e o he o al e ec o a pollina o on a plan due o
di e ences in pe - isi e ec i eness a p oducing seeds. In sel incompa ible species, he ela ionship be ween
in e ac ion equency and pe -in e ac ion e ec may be inc easingly nega i e as mo e lowe s pe plan a e
isi ed due o gei onogamous pollen ans e . We ound ha pollina o s making longe bou s (i.e. isi ing mo e
lowe s pe plan isi ) had an o e all highe pollina ion success pe bou . Howe e , pe -in e ac ion e ec s
ended o dec ease as he bou p og essed, pa icula ly o pollina o s ha cause highe pollen deposi ion. Since
he same in e ac ion equency may esul om di e en combina ions o numbe o bou s (plan isi s) and bou
leng h ( lowe s isi ed/bou ), pollina o s making epea edly sho e bou s may con ibu e mo e o plan
ep oduc ion o he same numbe o lowe s isi ed. Consequen ly, he magni ude o he di e ences in numbe
o in e ac ions o di e en insec ypes may be o e idden by he magni ude o he di e ences in e ec i eness as
pollina o s, e en i he same pollina o s consis en ly in e ac mo e equen ly. We discuss wo p edic ions
ega ding he alidi y o using in e ac ion equency as a su oga e o plan seed p oduc ion (as a measu e o
o al e ec ) depending o he deg ee o sel -compa ibili y, plan size and lo al display. We sugges ha he ole
o in e ac ion equency mus be es ed o di e en species, en i onmen s, and ac oss wide scales o alida e i s
use as su oga e o o al e ec in plan -pollina o ne wo ks.
Key wo ds: mu ualis ic ne wo ks, plan -pollina o in e ac ion, isi a ion a e, bou leng h, pollen
deposi ion.
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In oduc ion
In o de o p edic he e ec s o bio ic in e ac ions be ween species, i is impo an o ake in o accoun
he quali a i e and quan i a i e componen s o he in e ac ion. The quali a i e componen accoun s o
di e ences in he ai s o he in e ac ing indi iduals (e.g., ana omical o beha iou al, inna e o lea ned). The
quan i a i e componen accoun s o di e ences in he in ensi y o he in e ac ion (e.g., equency and/o
s eng h; see Be low e al. 2004; Vázquez e al. 2005). In plan -pollina o mu ualis ic in e ac ions, bo h
componen s may ha e a signi ican in luence on ou come o plan -pollina o in e ac ion in e ms o ep oduc i e
o demog aphic success o he in e ac ing species (e.g., He e a 1987, 1989; Colling e al. 2004; Aizen and
Ha de 2007). The need o ake in o accoun bo h he quali a i e and quan i a i e componen s o plan -pollina o
in e ac ions was al eady acknowledged in he well known 'Mos E ec i e Pollina o P inciple' (S ebbins 1970),
which emphasised he ole o pollina o s as de e minan o he e olu ion o lowe specializa ion, p oposing ha
he mos abundan and e ec i e agen s o pollen ans e be ween indi idual plan s we e he mos likely ones o
de e mine hei e olu iona y pa hways. He e we a gue ha quali a i e and quan i a i e componen s o species
in e ac ions also need o be aken in o accoun when analysing webs o in e ac ions be ween plan s and
pollina o s.
An inc easing numbe o s udies analyse whole plan -pollina o in e ac ions ne wo ks (Olesen and
Jo dano 2002, Jo dano e al. 2003; Vázquez and Aizen 2004). These in e ac ion ne wo ks a e gene ally
cha ac e ised by bina y ma ices, whe e each ow ep esen s a plan species and each column a pollina o
species, and he cell a he in e ac ion be ween a ow (plan ) and column (pollina o ) is se equal o ze o (i he
co esponding plan and pollina o species a e no known o in e ac ), o one (i he plan and pollina o a e
obse ed o in e ac ). In his app oach no in o ma ion is gi en abou he quali a i e and quan i a i e componen s
ha ac ually occu be ween in e ac o s. This bina y app oach, howe e , may be insu icien o p ope ly de ine
he opology o an in e ac ion ne wo k, because no all ealized in e ac ions a e equally impo an , which has
been pinpoin ed as one o he mos ecu en p oblems o pollina ion ne wo k s udies (e.g., Paine 1988, 1992,
Memmo 1999, Blü hgen e al. 2006). A numbe o ecen pape s emphasize he need o include a sui able
ep esen a ion o he quan i a i e componen o species in e ac ions (Jo dano 1987, Memmo 1999, Vázquez e
al. 2005; see also Goldbe g e al. 1999), o assess he p ope ies o in e ac ion ne wo ks beyond hose add essed
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Sánchez-La uen e e al. In e ac ion equency and o al e ec s in Lina ia - 4
solely om bina y ma ices. Se e al app oaches ha e been ecen ly used o include a sou ce o a ia ion in
quan i a i e componen s when cha ac e izing in e ac ion ne wo ks, anging om di e si y indexes o a e ac ion
me hods (e.g., Vázquez and Simbe lo 2002, He e a 2005).
In plan -animal mu ualis ic ne wo ks, i has ecen ly been sugges ed ha one quan i a i e componen ,
he in e ac ion equency (de ined as he numbe o in e ac ion e en s pe ime uni ), may be used as a su oga e
o he o al in e ac ion e ec (de ined as he pe -capi a ep oduc i e o seed dispe sal pe o mance o a plan
species), when he pe -in e ac ion e ec is in a ian (Vázquez e al. 2005). The use o in e ac ion equency as a
quan i a i e es ima e o o al in e ac ion e ec ha e been p oposed no only o plan -pollina o mu ualis ic
ne wo ks bu also o o he in e ac ion ne wo ks, including plan -seed dispe se s (Jo dano and Schupp 2000),
plan -an p o ec ion (Ness e al. 2006), and hos -pa asi e (Poulin e al. 2008). Howe e , a numbe o s udies ha e
shown ha he mos abundan animal mu ualis s (i.e. hose who p esumably in e ac mo e equen ly) a e no
necessa ily he mos e ec i e ones on a pe - isi basis (e.g., He e a 1987, 1989; Schupp 1993; May ield e al.
2001). Fo plan -pollina o in e ac ions, subs an ial a iabili y in pe in e ac ion e ec s may a ise because o (1)
a ying abili ies o di e en pollina o g oups o pick up pollen om an he s and deli e i o s igma ( ela ed o
hei beha iou , size, mechanical i , e c.; e.g., Wilson and Thomson 1991, Wilson 1995, Robe son e al. 2005);
and (2) he composi ion o he pollen mix u e deli e ed by hose pollina o g oups (mos ele an in sel -
incompa ible species, o in sel -compa ible ones wi h high le els o inb eeding dep ession; e.g., I ey e al. 2003,
Colling e al. 2004; Williams 2007). This a ia ion in pe in e ac ion e ec is he esul o pollina o o aging
s a egies and a e s ongly a ec ed by he pollina ion en i onmen (i.e., he bio ic and abio ic condi ions in
which he plan -pollina o in e ac ion akes place; see Rod íguez-Gi onés and San ama ía 2010). In u n, he
pollina ion en i onmen may also a ec he in e ac ion equency, o example h ough he numbe o lowe s
ha indi idual pollina o s isi pe plan (he ea e e e ed o as bou leng h; e.g. Robe son and Macnai 1995,
G indeland e al. 2005, Williams 2007; see also Iwasa e al. 1995). Consequen ly, he pe in e ac ion e ec is no
necessa ily an in a ian , inhe en , pa ame e o a gi en plan -pollina o pai , and dis ega ding i s in luence may
limi he alidi y o using in e ac ion equency as he main p edic o o o al e ec .
In his pape , we p esen empi ical da a o a case s udy illus a ing how he a ia ion in pe in e ac ion
e ec may limi he p edic i e alue o in e ac ion equency as a su oga e o o al e ec s (plan seed se ) in
plan -pollina o in e ac ions. We used he plan Lina ia lilacina (Plan aginaceae) and i s pollina o assemblage.
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L. lilacina is a sel -incompa ible he b; hus, only ou c ossed pollen is sui able o seed si ing. L. lilacina is
isi ed ac oss i s ange by se e al bee species ha di e in abundance, beha iou , body size and o he
mo phological ai s, which could a ec hei pe isi e ec i eness. We also de elop a gene al model o sel -
incompa ible plan species aimed a calcula ing he ela i e con ibu ion o di e en pollina o s o seed
p oduc ion as a unc ion o a iable bou leng h and pollen deposi ion abili y.
Me hods
S udy sys em and si es
Lina ia lilacina Lange (Plan aginaceae) is a pe ennial he b endemic o moun ains in Sou h-eas e n
Spain (Valdés 1970; Sáez and C espo 2005). This s udy was ca ied ou in 2005-2006 in he Jaén moun ains, in
wo L. lilacina popula ions (Sillón del Rey [SR] and O iña [OT]) sepa a ed by ca. 3 km ( u he de ails can be
consul ed in Sánchez-La uen e 2007). In hese popula ions plan s sp ou e e y season in mid win e and p oduce
se e al o many simple o b anched s ems ( ange 5-156; mean±SE s ems/plan : 38.21±26.66; n= 195) o ca. 22
cm. in leng h, some o which may p oduce a a iable numbe o zygomo phic lowe s clumped a hei op
( ange 20-285; mean±SE lowe s/plan : 102.49±52.18; n= 146). Mo phologically, lowe s consis o an
occluded, ubula co olla, wi h uppe and lowe whi ish lips, and colou ed nec a guides (blue o yellow,
depending on he popula ion; Sánchez-La uen e and Alcán a a, unpub. da a). A spu is p esen o collec nec a
p oduced by a nec a y loca ed unde he o a y inside he co olla. Func ionally, lowe s a e he maph odi ic and
sel -incompa ible. F ui s a e a 2-locule capsule, dehiscing by al es. A e success ul pollina ion, he capsule
de elops, con aining nume ous small b own, la ened, winged seeds ( ange 8-87; mean±SE seeds/ ui :
68.22±23.24; n= 2541). F ui ma u a ion akes be ween 18-24 days. In 2005, 15 plan s we e andomly selec ed in
SR and 14 in OT. In 2006, he same plan s we e used in bo h popula ions, excep o 2 plan s los in OT and ha
we e no subs i u ed.
Composi ion, beha iou and e ec i eness o he pollina o assemblage
In each season, we used he ea lies 2-3 ep oduc i e in lo escences o each agged plan du ing a week
o p elimina y insec obse a ions, aimed o de ec he composi ion and abundance o he isi o assemblage,
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and o analyse hei beha iou while isi ing plan s. O e all, we de ec ed 7 insec species, o which 4 we e
analysed in u he de ail (see Resul s o a jus i ica ion). F om hese p elimina y obse a ions he expe imen al
p ocedu e p oceeded as ollows.
The emaining ep oduc i e in lo escences o he agged plan s we e co e ed wi h bags be o e lowe ing
s a ed o a oid uncon olled lowe isi a ion by insec s while plan s we e no obse ed and o de e lo al
he bi o es ha may damage co ollas be o e abscission (Sánchez-La uen e 2007). When he in lo escences
s a ed o lowe , we emo ed bags on each census day and obse ed each plan in a andom o de wice a day in
20-minu es shi s du ing he ime o maximum pollina o ac i i y (12-18 h CET). Plan s in bo h popula ions we e
obse ed be ween 1-8 hou s each season, depending on hei lowe ing phenology. O e all, pollina o censuses
ex ended o 18 days in 2005 and 25 days in 2006, wi h 144 and 200 hou s o obse a ion espec i ely (bo h
popula ions pooled). Du ing each shi , we eco ded he ac i i y o all insec s isi ing lowe s. Fo each plan
isi (i.e., each bou , he ea e de ined as he pe iod in which an insec was isi ing lowe s on he ocal plan ),
we iden i ied he insec species and he lowe s i isi ed (i.e., he bou leng h). In o de o acili a e obse a ions,
only one insec was allowed a a ime. Thus, when a plan was being isi ed by an insec , any o he insec
in e es ed in ha plan was gen ly wa ed away.
A e each bou , we pu a combina ion o colou ed wi es a ound he pedicel o all i gin lowe s isi ed,
di e en o each isi o and acco ding o he o de in which hey we e isi ed. We conside ed he o de in which
lowe s we e isi ed as a cue o assess he composi ion o he pollen mix u e deposi ed on s igmas. We assumed
ha he i s lowe isi ed would ecei e he highes p opo ion o xenogamous pollen, while in subsequen
lowe s isi ed on he same plan (i.e. gei onogamous isi a ions) he pollen mix u e deposi ed would be
composed o an inc easingly highe p opo ion o au ogamous pollen (Ka on e al. 2009). Using his me hod,
we could iden i y he lowe s isi ed in each bou , he o de in which hey we e isi ed, he isi o species and i s
ela i e abundance, based on isi a ion a es. As we only allowed one isi pe i gin lowe , all lowe s isi ed
once we e immedia ely closed by pu ing a small anspa en glue d op o obs uc he opening o he co olla
ape u e. A he end o each shi , he ep oduc i e in lo escences we e bagged again. When all lowe s in an
in lo escence had been isi ed, he pollina o bag was no emo ed again un il co olla abscission.
Pollina o e ec i eness was es ima ed om he numbe o seeds p oduced pe ui . All lowe s we e
su eyed e e y hi d day o check o o a y enla gemen . F ui s we e collec ed be o e dehiscence, and he
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numbe o seeds coun ed. Plan size, measu ed as o al lowe p oduc ion, was eco ded a he end o he season.
De eloping ui s a e used by Gymnae on sp. (Cu culionidae, Coleop e a) wee ils o o oposi ion; hus we
sp ayed all in lo escences wi h Syngen a Ka a e King ® (a lambda-cyhalo h in-based insec icide) when lowe s
we e no longe unc ional o pollina ion. Sp ay was applied e e y hi d day. P e ious obse a ions
demons a ed ha his p oduc is well ole a ed by bees when dilu ed and applied acco ding o he manu ac u e 's
ins uc ions, and i is easonably e ec i e a p e en ing wee il a ack (Sánchez-La uen e 2007).
Da a analyses
Gene al linea mixed models we e used o es di e ences among pollina o g oups in (1) bou leng h,
(2) seed p oduc ion pe plan in ela ion o he numbe o isi s pe plan , and (3) pe isi e ec i eness (seeds
p oduced pe lowe ) in ela ion o lowe isi a ion o de in each bou . In he la e analysis, and since Apis
made signi ican ly longe bou s han he o he pollina o g oups ( ange 1-9 lowe s/bou s. 1-4 lowe s/bou ; see
Resul s), bou leng h was conside ed a con inuous a iable, a he han a ac o , o analyse he ull ange
exhibi ed by Apis. All dependen a iables we e modelled as no mal. Pollina o g oup, season and popula ion
we e included as ixed ac o s, while plan s we e conside ed as andom blocks. Plan lo al display (when es ing
o di e ences among lowe o plan isi s) o o al lowe p oduc ion (when es ing o di e ences among
whole plan s) we e used as co a ia es.
All s a is ical analyses we e conduc ed using R 2.11.1. (R De elopmen Co e Team, 2010) and he nlme
(Pinhei o e al. 2009) package.
Model o pe in e ac ion e ec s
Acco ding o Vázquez e al. (2005), he o al e ec (T) o a pollina o ype on a isi ed plan (in e ms o
ep oduc i e pe o mance; e.g. seed p oduc ion) may be de ined as he p oduc o i s in e ac ion equency (I,
numbe o lowe s isi ed du ing a imed obse a ion pe iod) and i s pe in e ac ion e ec (P, pe in e ac ion
con ibu ion o seed p oduc ion): T= IP. In he da a-se ha Vázquez e al. (2005) analysed, T was co ela ed
wi h I, and he e was no co ela ion be ween I and P, hus hey concluded ha he in e ac ion equency, I, can be
used as a su oga e o he o al in e ac ion e ec s, T, ega dless o di e ences in e ec i eness among
in e ac ions, P. Wi h he same p emises we de elop a model add essing he e ec o a ia ion in pe in e ac ion
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e ec s, and i s e en ual nega i e ela ionship wi h in e ac ion equency, wi h impac s on o al e ec s.
Using a de e minis ic exp ession, i a pollina o ype i di e s in e ec i eness a seed p oduc ion among
he di e en lowe s isi ed in each plan isi (i.e., in pe in e ac ion e ec ), he o al numbe o seeds (Ni)
p oduced by pollina o ype i a e each bou may be calcula ed as:
Ni=∑
=1
b
Pi,
(Eq. 1),
whe e b is he bou leng h (i.e., numbe o lowe s isi ed/bou ) o pollina o ype i, and
Pi,
is he numbe o
seeds p oduced by he - h lowe isi ed on he plan .
Wi h a mo e gene al pe spec i e, we can calcula e Ni using a modi ied e sion o he model p oposed by
de Jong e al. (1992) o e alua e he likelihood o seed p oduc ion by sel ing. As ou s udy species is sel -
incompa ible, we ha e modelled he p oduc ion o seeds by c ossing as a measu e o he pe in e ac ion e ec ,
assuming a linea ela ionship be ween xenogamous pollen deposi ion and seed se . While he ela ionship
be ween pollen deposi ion and seed se mus sa u a e when he e is enough pollen o e ilise all o ules, he
linea ela ionship cons i u es a good app oxima ion when pollen is a limi ing esul , as was he case in ou
expe imen (we only allowed a single isi pe lowe ) Fu he mo e, unlike de Jong e al. (1992), we ha e also
assumed ha ans e o au ogamous pollen om an he s o s igmas wi hin he same lowe is likely om he
e y i s lowe isi ed on a plan as a esul o he lowe handling by he isi o and gi en he close p oximi y
o hese ep oduc i e s uc u es in ou s udy species.
We i s conside ed a plan ha p oduces one seed pe lowe . When a pollina o a i es o he plan , i
ca ies a ce ain amoun o xenogamous pollen om p e iously isi ed plan s (E), and i may also emo e a
ac ion (k2) o he o al au ogamous pollen (A) p oduced by he cu en ly isi ed lowe . In hese calcula ions,
we igno e any pollen ha is added o he bee’s “pollen baske ” and hence emo ed om he pollina ion ci cui .
Because bo h E and k2A a e a ailable o deposi ion, he p opo ion o xenogamous pollen deposi ed is E/(E +
k2A). This is also he p obabili y ha a xenogamous pollen g ain eaches and e ilises he o ule o he lowe . I ,
in each lowe , he pollina o deposi s a ac ion k1 o he pollen i ca ies, and he pollina o goes on o isi a
second lowe on he same plan , upon a i al o ha lowe i will ca y amoun s (1- k1) E and (1- k1) k2 A o
xenogamous and au ogamous pollen, espec i ely. A his second lowe , he pollina o will collec k2 A new
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plan (e.g., S ickle and Vinson 2000, Ka on e al. 2009; see also Rode e al. 1998), seed se o lowe isi
n+1 is lowe han seed se o lowe isi n. The e o e, a e age pollina o e ec i eness is a dec easing unc ion
o he numbe o lowe s isi ed pe plan . Thus, he h ee pollina o g oups seemed o be unc ionally equi alen
in he i s lowe isi ed in each bou (Kendall and Smi h 1975, 1976; Die inge 1992), while e ec i eness
p og essi ely dec eased in subsequen lowe s isi ed. The a e a which e ec i eness dec eases depends on he
p opo ion o ca yo e pollen deposi ed a each lowe : he highe he p opo ion o pollen deposi ed a each
isi , he as e he p opo ion o xenogamous pollen app oaches ze o and he as e pollina o e ec i eness
dec eases. In ou sys em, pollina o e ec i eness dec eased as e o Apis han o An hopho a and Bombus. As
we only allowed one isi pe pollina o g oup pe i gin lowe , and he e a e no di e ences in he amoun o
o al pollen deposi ed among lowe s o each pollina o g oup (Sánchez-La uen e and Pa a, unpub. da a), he
mos likely explana ion o his esul is ha Apis deposi s a highe ac ion o au ogamous pollen on each lowe
(e.g., Rode e al. 1998; I ey e al. 2003; bu see Chambe lain and Schlising 2008) han Bombus and An hopho a,
mos likely as a esul o he ways in which i handles lowe s, spending mo e ime pe isi , and pene a ing he
lowe deepe , han Bombus and An hopho a (Sánchez-La uen e 2007, Sánchez-La uen e and Pa a, unpub. da a;
see also Ha de 1990, Thos esen and Olesen 1996).
A heo e ical model allows us o p edic how pe lowe seed se changes wi h he numbe o lowe s
al eady isi ed on a plan , and wi h he pollen deposi ion abili y o he pollina o s. Con olling o bou leng h,
pollina o s wi h highe capabili ies o pollen deposi ion (la ge k1; including bo h ou c ossed and au ogamous
pollen) ha e lowe no malised cumula i e seed se s pe bou , since he cumula i e seed se app oached i s
asymp o ic alue a e he i s 3-4 lowe s isi ed/bou (e.g. Ka on e al. 2009). In con as , lowe deposi ion
abili ies lead o highe asymp o ic cumula i e seed se , which is app oached a e a g ea e numbe o isi s. Fo
example, he ela ionship be ween bou leng h and no malised cumula i e seed se is almos linea o bou
leng hs o up o 9 isi s (Fig. 3), and he a e age pollina o e ec i eness is li le a ec ed by bou leng h.
Compa ing model p edic ions wi h da a on seed se pe lowe , we can also es ima e he p opo ion o
a ailable pollen ha bees deposi a each lowe . When pollen deposi ion abili y (k1) is la ge, he e ec o bou
leng h on pollina o e ec i eness can be su icien ly high o b eak he ypical posi i e co ela ion be ween
in e ac ion equency and o al e ec . Fo example, i ing ou model o he seed p oduc ion da a in Fig. 1 leads
o alues o pollen deposi ion o 0.12, 0.16 and 0.31 o Bombus, An hopho a and Apis, espec i ely. Wi h hese
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alues o pollen deposi ion we ound ha , while he in e ac ion equency o Apis was he highes among all he
isi o g oups, a less abundan pollina o (An hopho a), making sho e bou s, con ibu ed mo e o seed
p oduc ion. Al hough Bombus also made sho e bou s han Apis, and he e o e had highe a e age pe
in e ac ion pollina ion e ec i eness, he e ec was no su icien ly s ong o compensa e o he much lowe
in e ac ion equency o Bombus, which consequen ly had he lowes o al e ec o he h ee g oups. Simila
esul s ha e been ound o ano he sel -incompa ible plan species in which pollina o e ec i eness has been
s udied. May ield e al. (2001) compa ed he e ec i eness a seed p oduc ion and pollen expo in he sel -
incompa ible Ipomopsis agg ega a (Polemoniaceae) o Bombus apposi us and se e al hummingbi d species o
which his plan species was supposedly adap ed. They ound ha B. apposi us isi ed ewe lowe s pe plan
han hummingbi ds. Howe e , hey we e 4.04 imes mo e e ec i e a seed p oduc ion, and 2.75 imes mo e
e ec i e a pollen expo pe lowe isi , han he bi ds. Consequen ly, al hough hei o e all isi a ion
equency could be be ween a hi d and a qua e ha o hummingbi ds in some seasons, B. apposi us had a
highe o al e ec on plan ep oduc i e success.
Di e ences among pollina o g oups in bou leng h and pollen deposi ion abili y may in luence pe
in e ac ion e ec independen ly o each o he . In u n, a ia ion in pollina o abundance may be ela ed o he
o al numbe o in e ac ions o each pollina o g oup. The ou come in e ms o he measu ed o al e ec may
esul om a combina ion o hese h ee pa ame e s. Fo ins ance, in Fig. 5 he o al e ec o a pollina o wi h a
bou leng h (b) o 4 lowe s pe plan isi and a pollen deposi ion abili y (k1) o 0.47 is ac ually compa able o
ha o a pollina o wi h b= 8 and k1= 0.02, despi e he la ge di e ences in bo h pa ame e s. Bu , di e ences in
pollen deposi ion abili y may e en ually be mo e impo an han di e ences in bou leng h o gene a e a ia ion
in pe in e ac ion e ec s. Thus, while we would no expec lo al display and/o plan size o se a limi on he
pollen deposi ion abili y o a gi en pollina o g oup when isi ing plan s o he same species, hose pa ame e s
may se a limi on he a ia ion in bou leng h (e.g., Wase and P ice 1991; Di Pasquale and Jacobi 1998,
S ickle and Vinson 2000; G indeland e al. 2005; Ka on e al 2009). Fo example, Pellmy and Thompson
(1996) ound di e ences in numbe o in e ac ions and e ec i eness among se e al insec g oups isi ing he
sel -incompa ible he b Li hoph agma pa i lo um (Saxi agaceae). Howe e , because no di e ences occu ed
among insec ypes in hei bou leng h, gi en he small lo al display exhibi ed by he s udy species a any one
ime, no a ia ion in pe in e ac ion e ec , associa ed wi h a ia ion in bou leng h would be expec ed. Thus,
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only he numbe o bou s pe plan (bu no he bou leng h) was esponsible o he a ia ion in in e ac ion
equency among pollina o g oups, and he o al e ec could be accu a ely p edic ed om he in e ac ion
equency alone.
Many ecological p ocesses ela ed o ep oduc i e success, demog aphy o na u al selec ion (among
o he s) in wild popula ions a e con ex -dependen . This implies he occu ence o a numbe o a iable ou comes
depending on he pa icula condi ions in which hese p ocesses ake place (e.g., Rey e al., 2006; Alonso e al.
2007; see also Thompson 1994, 2005). Unde s anding he ela ionship be ween pollina o e ec i eness and bou
leng h is also impo an i we a e o explain a iabili y in ep oduc i e success be ween plan s, popula ions and
yea s. The heo e ical model can be applied no only o assess seed p oduc ion o sel -incompa ible plan species,
bu also o es ima e he p opo ion o sel ed and ou c ossed seeds p oduced in sel -compa ible species. In he
p esence o la e -ac ing inb eeding dep ession, hese es ima es a e essen ial o quan i y pollina o e ec i eness,
as ou c ossed seeds a e mo e aluable han sel ed ones. By measu ing seed se o a andom sample o lowe s
isi ed by a single pollina o o a gi en plan species, we can ob ain an unbiased es ima e o his species'
pollina ion e ec i eness. Bu plan s and en i onmen al ai s, such as lo al display and plan densi y, may a ec
bou leng h (e.g. Oha a and Higashi 1994, I ey e al. 2003). The es ima e pe in e ac ion e ec ob ained in one
popula ion will obscu e he ac ha he same pollina o species has di e en pollina o e ec i eness o plan s
o di e en sizes, and i will be impossible o ex apola e om one popula ion measu ed one yea , o o he
popula ions o yea s. Fo example, we ound ha bou leng h was di ec ly ela ed o lo al display (see also
Robe son and Macnai 1995, G indeland e al. 2005, Williams 2007), while plan isi a ion was no .
Consequen ly, di e ences in lowe ing phenology o synch ony among plan popula ions o he same plan
species, o igina ing by en i onmen al o bio ic ac o s, o by di e ences among plan s sizes, may di ec ly be
esponsible o he a ia ion in bou leng h and numbe o bou s o he same pollina o species (e.g. S ickle and
Vinson 2000), wi h p esumed in luences in he among- lowe a ia ion in seed numbe and/o quali y (e.g.
Ka on e al. 2009).
A leas wo complemen a y and es able p edic ions o plan -pollina o in e ac ions may a ise om ou
esul s. Fi s , we p edic ha in e ac ion equency will be a wo se p edic o o o al e ec in sel -incompa ible
han in sel -compa ible species, while in sel -compa ible species he p edic i e alue o he in e ac ion equency
as a su oga e o o al e ec s will dec ease as he le el o inb eeding dep ession inc eases. In bo h cases, a
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lowe mean pe in e ac ion e ec may be expec ed as mo e lowe s a e isi ed pe bou , because he amoun o
au ogamous pollen will inc ease wi h bou leng h. Second, because bou leng h is o in e es o de ine he
a ia ion in pe in e ac ion e ec s, and hence i s in luence on o al e ec s, he alidi y o he in e ac ion
equency as a p edic o o o al e ec s in such plan species may be educed as plan size and/o lo al display
inc ease, as a la ge numbe o lowe s open a any one ime may allow pollina o s o inc ease hei bou leng h.
These p edic ions could also a ise om he da ase used by Vázquez e al. (2005), e en hough hey combined
sel -compa ible and sel -incompa ible species. Thus, al hough mos o he 22 species included in he da ase used
we e sel -compa ible (ca. 70%), he co ela ion be ween in e ac ion equency and pe in e ac ion e ec s was
nega i e o mos o he sel -incompa ible ones. In cases o a posi i e co ela ion, his could be due o he
absence o di e ences among pollina o s in bou leng h, as sugges ed abo e. Howe e , he co ela ion be ween
in e ac ion equency and o al e ec was posi i e in all cases, and Vázquez e al. (2005) concluded ha pe
in e ac ion e ec s could be dis ega ded o explain o al e ec s. Howe e , as shown in Fig. 2 om ou empi ical
da a, a posi i e co ela ion be ween in e ac ion equency and o al e ec does no gua an ee ha he pollina o
wi h he highes equency would also con ibu e he mos o o al e ec s. A c i ical pa ame e o e alua e
whe he a pollina o g oup may con ibu e mo e han o he o seed p oduc ion may be he a io o mean pe isi
e ec i eness (i.e., he mean pe in e ac ion e ec ). The a io o mean pe in e ac ion e ec s o An hopho a and
Apis is 2.66. Fo any gi en in e ac ion equency, Apis would be mo e aluable han An hopho a a seed
p oduc ion i i isi s mo e han 2.66 imes as many lowe s as he la e . Howe e , unde his c i ical alue,
An hopho a would be o g ea e alue, despi e Apis s ill ha ing a highe in e ac ion equency. As he a io o he
di e ence in numbe o lowe s isi ed by hese pollina o g oups was below he c i ical alue in bo h seasons
(in 2005: 237 lowe s isi ed by Apis / 151 lowe s isi ed by An hopho a = 1.57; in 2006: 227 lowe s isi ed
by Apis / 155 lowe s isi ed by An hopho a = 1.46), An hopho a consis en ly con ibu ed mo e o seed
p oduc ion han Apis, despi e he la e isi ing mo e lowe s. Howe e , i we compa e Bombus o Apis, we ind
a c i ical alue o 1.78. As he a io o he di e ence in numbe o lowe s isi ed by hese pollina o g oups is
always abo e his c i ical alue (in 2005: 237 lowe s isi ed by Apis / 63 lowe s isi ed by Bombus = 3.76; in
2006: 227 lowe s isi ed by Apis / 80 lowe s isi ed by Bombus = 2.84), he pollina o making mo e isi s
(Apis) is, in his case, mo e aluable a seed p oduc ion. Thus, as in Vázquez e al. (2005), we also ound posi i e
co ela ions be ween in e ac ion equency and o al e ec o all he pollina o g oups es ed, bu i was he a io
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be ween pe in e ac ion e ec s wha inally de e mined wha pollina o con ibu ed he mos o o al e ec s.
O e all, because di e ences in in e ac ion equency may be o e idden by di e ences o igina ing om
a ia ion in bou leng h and/o pollen deposi ion abili y, i is clea ha beha iou (He e a 1987; Rod íguez-
Gi onés and San ama ía 2010) may explain pollina o con ibu ion o plan ep oduc ion be e han he numbe
o in e ac ions. Ou esul s sugges ha , a leas o sel -incompa ible plan species, he p edic i e alue o he
in e ac ion equency in plan -pollina o in e ac ions may be a “mo ing a ge ” because i is con ex dependen .
In o he wo ds, we do no expec he same dis ibu ion o all i s componen s unde di e en en i onmen al
condi ions, e en when he same pa icipan s a e in ol ed. Fo simplici y, ou model assumes a linea
ela ionship be ween pollen deposi ion and seed p oduc ion. Tha is, i i s species wi h pos -zygo ic mechanisms
o sel -incompa ibili y, while in cases o p e-zygo ic mechanisms, he esul s may be app oxima e. Howe e ,
e en in hese cases he ela ionship be ween pollen deposi ion and seed se may s ill be linea (depending on
each pa icula sys em) and he model may accu a ely p edic he o al e ec s, as obse ed o ou example
species.
Ou s udy assess he impo ance o di e en insec ypes as pollina o s based upon hei e ec i eness a
seed p oduc ion a plan le el, as measu ed h ough beha iou al and mo phological ea u es. Howe e , ou s udy
does no add ess he syne gis ic e ec o each insec ype in p esence/absence o he es o he insec ypes. In
o he wo ds, we ha e no es ed how in e ac ions among di e en insec ypes may in luence hei alue as
pollina o s, as sugges ed by Aigne (2001). Because plan s a e pollina ed by a numbe o insec ypes
cons i u ing an assemblage, hese in e ac ions may be impo an o de ine unc ional g oups, a he han
indi idual pollina o ypes, as aluable con ibu o s o plan i ness (see Fens e 2004). A p econdi ion o he
de ini ion o a unc ional g oup o pollina o s is ha all pollina o s in such g oup should ha e addi i e e ec s on
plan i ness, and his can only be es ed by a ying he p esence/absence o abundance o di e en insec ypes,
and analysing he i ness consequences o such a ia ion. Consequen ly, we sugges ha he ole o he
in e ac ion equency, as a sui able p edic o o o al e ec s, mus be es ed o di e en pollina ion sys ems, in
di e en pollina ion en i onmen s, o di e en pollina o assemblages, and ac oss wide scales, o alida e i s
gene alised use as a quan i a i e measu e in plan -pollina o in e ac ion ne wo ks.
Acknowledgemen s
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We hank Rebecca E. I win, James C esswell, Diego Vázquez, Je Olle on and wo anonymous
e iewe s o hei aluable sugges ions o imp o e ea lie e sions o he MS. This wo k was suppo ed by he
Spanish Minis e io de Educación y Ciencia (g an s BOS2003-00292 o AMSL and CGL2006-02860 o RP) and
by Minis e io de Ciencia e Inno ación / FEDER (g an CGL2007-63223/BOS) and Jun a de Andalucía / FEDER
(g an RNM-340) o MARG.
Re e ences
Aigne P (2001) Op imali y modeling and i ness ade-o s: when should plan s become pollina o
specialis s ? Oikos 95: 177-184.
Aizen MA, Ha de LD (2007) Expanding he limi s o he pollen-limi a ion concep : e ec s o pollen
quan i y and quali y. Ecology 88: 271–281.
Alonso C, Mu ikainen P, He e a CM (2007) Ecological con ex o b eeding sys em a ia ion: sex, size
and pollina ion in a (p edominan ly) gynodioecious sh ub. Annals o Bo any 100: 1547-1556.
Be low EL, Neu el AM, Cohen JE, De Rui e PC, Ebenman B, Emme son M, Fox JW, Jansen VAA,
Iwan Jones J, Kokko is GD, Logo e DO, Mckane AJ, Mon oya JM, Pe chey O (2004).
In e ac ion s eng hs in ood webs: issues and oppo uni ies. Jou nal o Animal Ecology 73: 585-
598.
Blü hgen N, Menzel F, Blü hgen N (2006) Measu ing specializa ion in species in e ac ion ne wo ks.
BMC Ecology 6: 9. doi:10.1186/1472-6785-6-9
Chambe lain SA, Schlising RA (2008) Role o honey bees (Hymenop e a: Apidae) in he pollina ion
biology o a Cali o nia na i e plan , T i eleia laxa (Aspa agales: Themidaceae). En i onmen al
En omology 37: 808-816.
Colling G, Reckinge C, Ma hies D (2004) E ec s o pollen quan i y and quali y on ep oduc ion and
o sp ing igo in he a e plan Sco zone a humilis (As e aceae). Ame ican Jou nal o Bo any
91: 1774-1782.
De Jong TJ, Klinkhame PGL, S aalduinen MJ (1992) The consequences o pollina ion biology o
selec ion o mass o ex ended blooming. Func ional Ecology 6: 606-615.
500
501
502
503
504
505
506
507
508
509
510
511
512
513
514
515
516
517
518
519
520
521
522
523
524
525
526
20
Page 20 o 35Oecologia

Fo Pee Re iew
Sánchez-La uen e e al. In e ac ion equency and o al e ec s in Lina ia - 21
Die inge G (1992) Pollina o e ec i eness and seed se in popula ions o Agalinis s ic i olia
(Sc ophula iaceae). Ame ican Jou nal o Bo any 79: 1018–1023.
Di Pasquale C, Jacobi CM (1998) Dynamics o pollina ion: a model o insec -media ed pollen ans e in
sel -incompa ible plan s. Ecological Modelling 109: 25–34.
Fens e CB, A mb us e WS, Wilson P, Dudash MR, Thomson JD (2004). Pollina ion synd omes and
lo al specializa ion. Annual Re iew o Ecology, E olu ion and Sys ema ics 35: 375-403. doi:
10.1146/annu e .ecolsys.34.011802.132347
Goldbe g DE, Rajaniemi T, Gu e i ch J, S ewa -Oa en A (1999). Empi ical app oaches o quan i ying
in e ac ion in ensi y: compe i ion and acili a ion along p oduc i i y g adien s. Ecology 80: 1118-
1131.
G indeland JM, Sle old N, Ims RA (2005) E ec s o lo al display size and plan densi y on pollina o
isi a ion a e in a na u al popula ion o Digi alis pu pu ea. Func ional. Ecology 19: 383–390.
doi: 10.1111/j.1365-2435.2005.00988.x
Ha de LD (1990) Pollen emo al by bumble bees and i s implica ions o pollen dispe sal. Ecology 71:
1110-1125.
He e a CM (1987) Componen s o pollina o quali y: compa a i e analysis o a di e se pollina o
assemblage. Oikos 50: 79-90.
He e a CM (1989) Pollina o abundance, mo phology, and lowe isi a ion a e: analysis o he
'quan i y' componen in a plan -pollina o sys em. Oecologia 80, 241-248.
He e a CM (2005) Plan gene aliza ion on pollina o s: species p ope y o local phenomenon ?.
Ame ican Jou nal o Bo any 92: 13-20.
He e a CM, Ce dá X, Ga cía MB, Gui ián J, Med ano M, Rey PJ, Sánchez-La uen e AM (2002) Flo al
in eg a ion, pheno ypic co a iance s uc u e and pollina o a ia ion in bumblebee-pollina ed
Hellebo us oe idus. Jou nal o E olu iona y Biology 15: 108-121.
I ey CT, Ma inez P, Wya R (2003) Va ia ion in pollina o e ec i eness in swamp milkweed Asclepias
inca na a (Apocynaceae). Ame ican Jou nal o Bo any 90: 214-225.
Iwasa Y, De Jong TJ, Klinkhame PGL (1995) Why pollina o s isi only a ac ion o eh open lowe s on
a plan : he plan 's poin o iew. Jou nal o E olu iona y Biology 8: 439-453.
527
528
529
530
531
532
533
534
535
536
537
538
539
540
541
542
543
544
545
546
547
548
549
550
551
552
553
554
21
Page 21 o 35 Oecologia
Fo Pee Re iew
Sánchez-La uen e e al. In e ac ion equency and o al e ec s in Lina ia - 22
Jo dano P (1987) Pa e ns o mu ualis ic in e ac ions in pollina ion and seed dispe sal: connec ance,
dependence asymme ies, and coe olu ion. The Ame ican Na u alis 129: 657-677.
Jo dano P, Schupp EW (2000) Seed dispe se e ec i eness: he quan i y componen and pa e ns o seed
ain o P unus mahaleb. Ecological Monog aphs 70: 591- 615.
Jo dano P, Bascomp e J, Olesen JM (2003) In a ian p ope ies in coe olu iona y ne wo ks o plan -
animal in e ac ions. Ecology Le e s 6: 69-81.
Ka on JD, Holmquis KG, Flanagan RJ, Mi chel RJ (2009) Pollina o isi a ion pa e ns s ongly
in luence among- lowe a ia ion in sel ing a e. Annals o Bo any 103: 1379–1383.
doi:10.1093/aob/mcp030
Kendall DA, Smi h BD (1975) The pollina ing e iciency o honeybee and bumblebee isi s o ield bean
lowe s (Vicia aba L.). Jou nal o Applied Ecology 12: 709-717.
Kendall DA, Smi h BD (1976) The pollina ing e iciency o honeybee and bumblebee isi s o lowe s o
he unne bean bean Phaseolus coccineus. Jou nal o Applied Ecology 13: 749-752.
May ield MM, Wase NM, P ice MV (2001) Explo ing he `Mos E ec i e pollina o p inciple' wi h
complex lowe s: bumblebees and Ipomopsis agg ega a. Annals o Bo any 88: 591-596.
doi:10.1006/anbo.2001.1500
Memmo J (1999) The s uc u e o a plan -pollina o ood web. Ecology Le e s 2: 276-280.
Ness JH, Mo is WF, B ons ein JL (2006). In eg a ing quali y and quan i y o mu ualis ic se ice o
con as an species p o ec ing Fe ocac us wislizeni. Ecology 87: 912-921.
Oha a M, Higashi S (1994) E ec s o in lo escence size on isi s om pollina o s and seed se o
Co ydalis ambigua (Papa e aceae). Oecologia 98: 25-30.
Olesen JM, Jo dano P (2002) Geog aphic pa e ns in plan -pollina o mu ualis ic ne wo ks. Ecology 83:
2416-2424.
Paine RT (1988). Food-webs: oad maps o in e ac ions o g is o heo e ical de elopmen ? Ecology 69:
1648-1654.
Paine RT (1992). Food-web analysis h ough field measu emen o pe capi a in e ac ion s eng h. Na u e,
355: 73-75.
Pellmy P, Thompson JN (1996). Sou ces o a ia ion in pollina o con ibu ion wi hin a guild: he e ec s
555
556
557
558
559
560
561
562
563
564
565
566
567
568
569
570
571
572
573
574
575
576
577
578
579
580
581
582
22
Page 22 o 35Oecologia
Fo Pee Re iew
Sánchez-La uen e e al. In e ac ion equency and o al e ec s in Lina ia - 23
o plan and pollina o ac o s. Oecologia 107: 595–604.
Pinhei o J, Ba es D, DebRoy S, Sa ka D and he R Co e eam (2009). nlme: Linea and Nonlinea Mixed
E ec s Models. R package e sion 3.1-96.
Poulin R, K asno BR, Shenb o GI (2008) In e ac ion equency ac oss he geog aphical ange as a
de e minan o hos specialisa ion in gene alis fleas. In e na ional Jou nal o Pa asi ology 38:
989-997. doi:10.1016/j.ijpa a.2008.01.001
R De elopmen Co e Team. 2010. R: A language and en i onmen o s a is ical compu ing. R
Founda ion o S a is ical Compu ing, Vienna, Aus ia. ISBN 3-900051-07-0, URL:
h p://www.R-p ojec .o g.
Rey PJ, He e a CM, Gui ián J, Ce dá X, Sánchez-La uen e AM, Med ano M, Ga ido, JL (2006) The
geog aphic mosaic in p e-dispe sal in e ac ions and selec ion on Hellebo us oe idus
(Ranunculaceae). Jou nal o E olu iona y Biology 19: 21-34.
Robe son AW, Macnai MR (1995) The e ec s o lo al display size on pollina o se ice o indi idual
lowe s o Myoso is and Mimulus. Oikos 72: 106-114.
Robe son AW, Ladley JJ, Kelly D (2005) E ec i eness o sho - ongued bees as pollina o s o
appa en ly o ni hophilous New Zealand mis le oes. Aus al Ecology 30: 298-309.
Rode G, Vaissie e BE, B e aul T, To e G ossa JP (1998). S a us o sel -pollen in bee pollina ion
e iciency o whi e clo e (T i olium epens L.). Oecologia 114: 93–99.
Rod íguez-Gi onés MA, San ama ía L (2010) How o aging beha iou and esou ce pa i ioning can
d i e he e olu ion o lowe s and he s uc u e o pollina ion ne wo ks. Open Ecology Jou nal 3:
1-11.
Sáez L, C espo MB (2005) A axonomic e ision o he Lina ia e icilla a g oup (An i hineae,
Sc ophula iaceae). Bo anical Jou nal o he Linnean Socie y 148: 229-244.
Sánchez-La uen e AM (2007) Co olla he bi o y, pollina ion success and ui p eda ion in complex
lowe s: an expe imen al s udy wi h Lina ia lilacina (Sc ophula iaceae). Annals o Bo any 99:
355-364. doi:10.1093/aob/mcl267
Schemske DW, B adshaw HD (1999) Pollina o p e e ence and he e olu ion o lo al ai s in monkey
lowe s (Mimulus). P oceedings o he Na ional Academy o Sciences 96: 11910-11915.
583
584
585
586
587
588
589
590
591
592
593
594
595
596
597
598
599
600
601
602
603
604
605
606
607
608
609
610
23
Page 23 o 35 Oecologia
Fo Pee Re iew
Sánchez-La uen e e al. In e ac ion equency and o al e ec s in Lina ia - 24
Schupp EW (1993) Quan i y, quali y and he e ec i eness o seed dispe sal by animals. Vege a io 107-
108: 15–29.
S ebbins GL (1970) Adap i e adia ion o ep oduc i e cha ac e is ics in Angiospe ms, I: Pollina ion
mechanism. Annual Re iew o Ecology and Sys ema ics 1: 307-326.
S ickle K, Vinson JW (2000) Simula ion o he e ec o pollina o mo emen on al al a seed se .
En i onmen al En omology 9: 907–918.
Thompson JN (1994) The coe olu iona y p ocess. The Uni e si y o Chicago P ess. London.
Thompson JN (2005) The geog aphic mosaic o coe olu ion. The Uni e si y o Chicago P ess. London.
Thos esen AM, Olesen JM (1996) Pollen emo al and deposi ion by specialis and gene alis bumblebees
in Aconi um sep en ionale. Oikos 77: 77–84.
Valdés B (1970) Re isión de las especies eu opeas de Lina ia con semillas aladas. Anales de la
Uni e sidad Hispalense nº 7, Uni e sidad de Se illa.
Va gas P, O nosa C, O iz-Sanchez FJ, A oyo J (2010) Is he occluded co olla o An i hinum bee-
specialized? Jou nal o Na u al His o y 44: 1427-1443.
Vázquez DP, Simbe lo D (2002) Ecological specializa ion and suscep ibili y o dis u bance: conjec u es
and e u a ions. The Ame ican Na u alis 159: 606-623.
Vázquez DP, Aizen MA (2004) Asymme ic specializa ion: a pe asi e ea u e o plan -pollina o
in e ac ions. Ecology 85: 1251-1257.
Vázquez DP, Mo is WF, Jo dano P (2005) In e ac ion equency as a su oga e o he o al e ec o
animal mu ualis s on plan s. Ecology Le e s 8: 1088-1094. doi: 10.1111/j.1461-
0248.2005.00810.x
Wase NM, P ice MV (1991) Rep oduc i e cos s o sel pollina ion in Ipomopsis agg ega a: a e o ules
usu ped ?. Ame ican Jou nal o Bo any 78: 1036-1043.
Wase NM, Chi ka L, P ice MV, Williams NM, Olle on J (1996) Gene aliza ion in pollina ion sys ems,
and why i ma e s. Ecology 77: 1043-1060.
Williams CF (2007) E ec s o lo al display size and bipa en al inb eeding on ou c ossing a es in
Delphinium ba beyi (Ranunculaceae). Ame ican Jou nal o Bo any 94: 1696-1705.
Wilson P (1995) Selec ion o pollina ion success and he mechanical i o Impa iens lowe s a ound
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