Predicting Pollen Transfer Using Plant-Pollinator Interaction Webs

Predicting Pollen Transfer Using Plant-Pollinator Interaction Webs

Karen GoodellDepartment of Evolution, Ecology and Organismal Biology,

The Ohio State Universitywith

Neal Williams and Daniela MitevaDepartment of Biology, Bryn Mawr College

Plant-pollinator webs• Quantitative plant-visitor web

– Use food-web analysis to derive metrics for comparing communities

• Pollen transport webs– Identify potential pollinators of plants– Identify additional resources of pollinators– Extend information about visitors to include historical (short-term) visits

Memmott 1999. Ecol. Let.

Applications of pollinator interaction webs

• Restoration– Compare web structure with intact habitats similar to target

habitat– Compare function of the pollinator community to that in intact

habitat– E.g.: Restoration of British hay meadows (Forup & Memmott,

2005)• Constructed insect visitation and pollen transport webs for intact

and restored meadows• Inferred pollinator function from pollen transport webs

Applications of plant-pollinator webs

• Conservation– Identify important pollinators of rare plants– Identify resources required by these pollinator species– E.g., Gibson et al. 2006

• Identified important pollinators of three rare plant species• Used pollen transport patterns to rank pollinators by their

effectiveness• Identified resources used by these pollinators from pollen transport

webs

• Agriculture– Associate pollinator community structure with pollinator services

to crop plants– Identify important non-crop resources used by pollinators

Relationship to pollination patterns?

• Plant pollinator webs and pollen transport webs consider interactions at the species level

• But patterns of pollination reflect movements and choices of individuals

• Most visitor species are generalists– Average species-level foraging patterns may differ from

individual-level foraging – Floral constancy– Spatially restricted foraging

• Can individual-level data derived from plant-pollinator web contribute to understanding pollination patterns from web data?

Research questions

• Is generality of visitors correlated with patterns of pollen deposition on stigmas across plant species?– More generalized visitor species deposit more

heterospecific pollen• Does consideration of pollen transport web

improve predictions of pollen deposition in a plant community?– Higher diversity of pollen transported means higher

diversity of pollen transferred

Visitation, transport, deposition

• Build visitation web• Examine pollens deposited on stigmas

– Function of visitor diversity– Function of visitor generality

Visitors

Plants

Restored Eastern US Prairie

Pollinator and stigmatic data

• Flower and Pollinator survey– 1 ha plot– Counted all flowers of 8 dominant

plant species– Individually netted and preserved

insect visitors to plants over 1 day– 90 min collection per plant species– Pinned and identified all visitors

• Stigmatic pollen loads– Collected stigmas following 1 day of

open pollination (n = 25 per plant species)

– Counted and identified all grains on stigmas

Flower species surveyed

Carduus acanthoides Heliopsis helianthoides Rudbeckia serotina Nepeta cataria

Monarda fistulosaPhysalis longifoliavar. subglabrataPycnanthemum tenuifolium Solanum carolinense

Pollen transport data

• Dabbed insects with a ca. 25 mm2 cube of glycerin gel stained with fuchsin.

• Melted the gel onto a microscope slide• Counted and identified the pollen using a

reference collection• Constructed a matrix of individuals by

frequencies of pollens on their bodies

Monard

aHeli

opsis

Carduu

sPyc

nanth

emum

Physa

lisRud

beck

iaSola

num

Nepeta

0

1000

2000

3000

4000

5000

6000

Num

ber f

lora

l uni

ts p

er h

a

Plant species

Community structure

Apiform

es

Other H

ym.

Lepid

opter

a

Diptera

0

50

100

150

200

250

300

350

Num

ber o

f ind

ivid

uals

Visitor taxa

67 visitor species 486 visitor specimens

38 bee species 17 wasp species9 Lepidoptera species4 fly species23 Singletons (4.7%)12 Doubletons (2.5%)

8 plant species

Do more generalized visitor species carry higher diversity of pollen?

1 2 3 4 5 6 72.0

2.5

3.0

3.5

4.0

4.5

5.0

5.5

Num

ber o

f pol

len

spec

ies

trans

porte

d

Number of host species

• No • Species-level

foraging patterns poor predictors of individual-level pollen transport

• Shown for subset of species n > 4

0.0 0.5 1.0 1.5 2.0

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1.0

Mea

n pr

opor

tion

corr

ect p

olle

n

H of floral hosts

Hylaeus affinis

Do more generalized visitor species carry less correct pollen?

• No.• n.s. trend for

species with external pollen transport

• Shown for subset of visitor species n > 4)

• H = Shannon-Weiner diversity index

Colletes latitarsus, Physalis specialist

Does low pollen fidelity of visitors mean higher pollen diversity on stigmas?

• No• Marginally significant

negative correlation when Physalisexcluded

• Outlier is Physalis, which has aspecialist pollinator

0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.90.00

0.05

0.10

0.15

0.20

0.25

Mea

n H

of s

tigm

atic

pol

lens

Mean H of bee body pollens

Physalis

Carduus

Heliopsis

Monarda

NepetaPycnanthemum

Rudbeckia

Solanum

• Compare observed diversity of pollen deposited to

– Diversity plants used by visitor species to that plant– Diversity of pollens transported by visitors caught on that plant– Number of pollen grains not considered because not comparable

among plant species

• Compare observed proportion of conspecific pollen deposited to that predicted by three null models

– Species-level visitation fidelity– Species-level pollen transport patterns– Individual-level pollen fidelity

Predicting diversity of stigmatic pollen loads

Visitor fidelity model

Species-level visitor fidelity

Proportion of i pollen on stigma of i =( )( )∑

∑ ×

ji

ijji

NPN

,

,,

Ni,j = number of visitors of species j collected on plant iPj,i = proportion bee species j collected on plant i

Species-level visitor fidelity

Plant

A

B

C

Visitor sp.

1

2

3

Number of visitsA B

10 0

5 5

0 10

1

0.333

0

Percent visits toA B

( )( )∑

∑ ×

ji

ijji

NPN

,

,,

0

0.333

0.5

= (10 x 1) + (5 x 0.3333)/15 = 0.89Proportion of A pollen on stigmas of A

=

=

Assumptions• All pollen on body has equal probability to land on a

stigma– No pollen layering– No grooming– No effects of pollen placement

• Species-level visitation patterns reflect individual foraging patterns– Constancy well-documented in eusocial bees– Spatially restricted foraging likely in small species

• Flowers receive adequate numbers of visits for stigmas to reflect average visitation patterns

• Effects of floral morphology minimal; plant species behave similarly

Pollen fidelity

Individual pollen fidelity model

Proportion of i pollen on stigma of i =

Ni,j = number of visitors of species j collected on plant iBj,i = Mean proportion of pollen i carried on bodies of visitor species j

( )( )∑

∑ ×

ji

ijji

NBN

,

,,

Weights visitors to a focal plant by their pollen fidelity rather than species-level visitation fidelity

Individual pollen fidelity

Plant

A

B

C

Visitor sp.

1

2

3

Number of visitsA B

10 0

5 5

0 10

Proportion pollen carriedA B

1

0.90

0.1

0

0.80

0.75

( )( )∑

∑ ×

ji

ijji

NBN

,

,,Proportion of A pollen on stigmas of A

= = (10 x 1) + (5 x 0.9)/15 = 0.97

If foragers tend to be constant this model will increase the predicted proportion of conspecific pollen on stigmas.

Ni,jBi,j

Assumptions• All pollen on body has equal probability to land on a

stigma• Species-level visitation patterns reflect individual

foraging patterns• Flowers receive adequate numbers of visits for stigmas

to reflect average visitation patterns• Effects of floral morphology minimal; plant species

behave similarly• Pollinator pool limited to those caught on focal plant

Pollen transport

Species-level pollen transport

Proportion of i pollen on stigma of i =( )

( )∑∑

×

××

jij

ijij

NTNDT

,

j,,

Tj,i = Proportion of visitors j transporting pollen iDi,j = Mean proportion pollen i carried on bodies of visitor species jNj = Number of bees of species j in total sample

Related to measure of pollinator importance for a plant speciesPI = Tj,i x Dj,I (Ne’eman, Dafni & Potts 1999)

Considers as potential pollinators all individuals transporting pollen of focal species

Pollen Transport

Plant

A

B

C

Visitor sp.

1

2

3

Number of visitsA B

10 0

5 5

0 10

Prop. pollen carried* Prop indiv. transportingA B A B

1

0.50

0.1

0

0.30

0.45

= [(1 x 1 x 10) + (0.9 x 0.5 x 10) + (0.1 X 0.1 x 10)]/(10 + 9 + 0)= 0.82

Proportion of A pollen on stigmas of A)

=

*Means for all individuals carrying that pollen

( )( )∑

∑×

××

jij

ijij

NTNDT

,

j,,

1.0 0.2

0.9 1.0

0.1 0.6

Tj,iDi,jNj

Assumptions• All pollen on body in fully dynamic pool with equal

probability to land on the stigma• Pollen on body independent of current host• Flowers receive adequate numbers of visits for stigmas

to reflect average visitation patterns• Effects of floral morphology minimal; plant species

behave similarly• Pollinator pool limited to those caught on focal plant

Physa

lisNep

eta

Solanu

mMon

arda

Pycna

nthem

um

Heliop

sis

Rudbe

ckia

Carduu

s

0.00.10.20.30.40.50.60.70.80.91.0

Prop

ortio

n of

con

spec

ific

polle

n on

stig

ma

ObservedSpecies-level visitor fidelityIndividual-level pollen fidelitySepcies-level pollen transport

Pollen deposited on stigmas

• Fit of models tested with log-likelihood G-test for each plant sp.

• No model fit best for all species of plant

• Pollen fidelity model decent fit for 2 of 3 Asteraceae

• Pollen transport model least predictive

***

Individual foraging patterns: pollen on Apis bodies

• 2-d NMS on pollen data

• Apis collected on different hosts group by pollens collected

• MRPP detected significant variation among host-plant groups in pollens carried.

-1.5 -1.0 -0.5 0.0 0.5 1.0-1.5

-1.0

-0.5

0.0

0.5

1.0

1.5

Rud

Car

Mon

Nep

Sol

HelA

xis

2

Axis 1

NepetaCarduusMonardaMean of Apis

21.4% of variation

68.5

% o

f var

iatio

n

-1.5 -1.0 -0.5 0.0 0.5 1.0 1.5-1.5

-1.0

-0.5

0.0

0.5

1.0A

xis

3

Axis 2

Individuals Means Heliopsis Monarda Carduus Nepetaall Augochlorellapollens

Pyc

Monarda

Hel

Rud Solanum

Carduus

Nepeta

Augochlorella aurata pollen on bodies

• 3-d NMS on pollen data

• MRPP indicates significant clustering of visitors by host plant

• Within group variance larger for some species

34.7% of variation

31.2

% o

f var

iatio

n

Heliopsis

CarduusMonarda

Nepeta

Individual foraging patterns differ from species average?

• Apis mellifera Yes• Bombus griseocolis No• Augochlorella aurata Yes• Halictus ligatus No• Lasioglossum admirandum No

Represent species caught on >1 plant species for which n > 4 per plant species

Pollen on B. griseocolis• Similar suites of

pollens collected– Carduus a major

component for all individuals regardless of host plant

– Little Monardatransported

– Monarda primarily a nectar source?

– Complementarity of resources discourages individual specialization

Physalis Rudbeckia Carduus Monarda Solanum Heliopsis0.0

0.2

0.4

0.6

0.8

1.0

Mea

n pr

opor

tion

of p

olle

n on

bod

y

Pollen species

Collected on Carduus Collected on Monarda

Conclusions• Pollen visitation webs poorly predict pollen deposition • Species-level pollen transport patterns add little

predictive power at community level• Individual pollen fidelity shows some promise in

predicting pollen transfer for certain species– Pollen deposition influenced by floral morphology– Simple flowers like Asteraceae work best

• Some evidence for individual differences in foraging choices in some species, but not in others

• Suggest caution in inferring pollinator function from visitation and pollen transport webs

Future directions• Examine spatial patterns of plant species that

could influence constancy– Degree of clumping– Clustering of more than one species

• Compare pollen transport patterns among visitor types– bees of different sizes and social structures– Insect orders

• Investigate predictive power of pollen deposition models within plant species

Acknowledgements

Collaborators: T’ai Roulston, Bob MinckleyStudents: Sarah Letson, Amy Seese

Identification: Sam Droege, John WenzelFunding & logistical support:

Blandy Experimental FarmNSF (REU program)

OSU-Newark (Student assistantship grants)

Structure of the interaction web

Measure Value SD range

Mean # plants/visitor sp. 1.71 1.46 1 - 7

Linkage Density 1.71

Connectance 0.24 = 128/(67 x 8)

Mean # visitor spp./plant sp.

16 7.51 4 - 28

Proportion of plant species’ pollen

transported1.0

Carduus-Carduus Monarda-Monarda Carduus-Monarda0.0

0.5

1.0

1.5

2.0

2.5

3.0

Mea

n pa

irwis

e Eu

clid

ean

dist

ance

Host group comparison

• No significant grouping of B. griseocolis individuals based on host plant

• MRPP based on Euclidean distances (log10) A = 0.036, P>0.05

Bombus griseocolis

n = 55 n = 21 n=77

Pairwise distances betweenpollens carried by individuals

pollen on bodies all bees NMS euclidean logs

Axis 1

Axi

s 2

Host12345678

Explaining pollen transport:species or floral host?

• MRPP of all bees by pollen transported – Significant clustering by species– Clustering by host stronger