DOI: 10.5061/dryad.gqnk98sj0
title: Experimental shifts in exotic flowering phenology produce strong indirect effects on native plant reproductive success

description: By causing phenological shifts that vary among species, climate change is
 altering time envelopes for species interactions, often with unexpected
 demographic consequences. Indirect interactions, like apparent competition
 and apparent facilitation, are especially likely to change in duration
 because they involve multiple interactors, increasing the likelihood of
 asynchronous phenological shifts by at least one interactor. Thus, we
 might observe ecological surprises if intermediaries of indirectly
 interacting species change their mediating behavior. We explored this
 possibility in a plant-pollinator community that is likely to experience
 asynchronous phenological shifts. We advanced and delayed the flowering
 phenology of two ubiquitous exotic plants of western Washington prairies,
 Hypochaeris radicata and Cytisus scoparius, relative to seven native
 perennial forb species whose phenologies remained unmanipulated. These
 species interact indirectly through shared pollinators, whose foraging
 behavior influences plant reproductive success. We quantified impacts of
 experimental phenological shifts on seedset, pollinator visitation rates,
 and visiting pollinator composition relative to an unmanipulated control.
 We first verified that unmanipulated indirect interactions between native
 and exotic plants were strong, ranging from facilitative to competitive.
 Seedset of native plants was strongly affected by changes in exotic
 flowering phenology, but the magnitude and direction of effects were not
 predicted by the nature of the original indirect interaction (facilitative
 vs. neutral vs. competitive) or the change in interaction duration. The
 relationship between pollinator visitation and seedset changed for most
 species, though changes in pollinator visitation rate and pollinator
 composition were not as widespread as effects on native seedset.
 Synthesis. Changes in pollinator foraging behavior in response to changes
 in available floral resources are probably responsible for the unexpected
 effects we observed. Asynchronous phenological shifts have the potential
 to produce large and unexpected effects on reproductive success via
 indirect interactions.
description: Three datasets here include flowering phenology, pollinator
 visitation, and seed production data for prairie forbs native to western
 Washington, USA. Data were collected at Glacial Heritage Prairie in
 Littlerock, WA from July-August 2011. We experimentally altered flowering
 phenology for two exotic species (Cytisus scoparius and Hypochaeris
 radicata) and looked at effects on seedset of seven neighboring native
 forbs (Ranunculus occidentalis, Camassia quamash, Microseris laciniata,
 Lupinus lepidus, Eriophyllum lanatum, Prunella vulgaris, Campanula
 rotundifolia). We established 48 5x5 m plots in a
 randomized block design, with eight blocks each containing one plot for
 each of six phenology treatments. Within blocks, plots were randomly
 located, with the constraint that they must contain at least 6 naturally
 occurring individuals of each of the native species. While other forb
 species were present in plots, they never occurred at high densities
 relative to focal species. Naturally occurring <i>C.
 scoparius</i> was absent from all plots, and naturally occurring
 <i>H. radicata</i> was present in all plots. We established
 plots to be at least 10 - 16 meters apart; plots are not separated by
 enough distance to represent non-overlapping pollinator
 communities.             Control plots were
 unmanipulated, while flowering greenhouse-grown potted exotic plants were
 placed in experimental plots. Management actions had largely removed
 <i>C. scoparius </i> from the surrounding plant community, so
 the potted plants represented a “reinvasion” for <i>C. scoparius,
 </i>while for <i>H. radicata</i>, treatments amplified
 an existing invasion. Pots were placed with the desired timing (‘Ambient’,
 ‘Advanced’ and ‘Delayed’), to impose phenological treatments (1 potted
 <i>C. scoparius</i> shrub = 152 ± 23 flowers added, or 4 pots
 of large <i>H. </i>radicata = 56 ± 4 capitulas added). There
 were thus two kinds of controls: exotic absent, and exotic present with
 “ambient” timing. The
 appropriate control is different depending on the species pair: for native
 species that had no initial flowering overlap with the neighboring exotic,
 the appropriate comparison is exotic absent (control) vs. ‘Advanced’ or
 ‘Delayed’ exotic phenology. By contrast, the appropriate comparison for
 plants that already overlapped with the exotic (before manipulation of
 exotic phenology) would be ‘Ambient’ exotic phenology vs. ‘Advanced’ or
 ‘Delayed’ exotic phenology. Using potted plants allowed us to
 isolate pollinator-mediated effects from direct competitive/facilitative
 effects that occur belowground. Pots were typically at least ~0.75m away
 from focal native individuals, so shading was minimal. We altered exotic
 phenology by adding pots at the onset of the species’ natural flowering at
 nearby sites for Ambient treatments, ~3 weeks before ambient flowering for
 Advanced treatments, or ~3 weeks later than ambient flowering for Delayed
 treatments. We were unable to delay flowering of <i>C.
 scoparius</i>, so the Delayed treatments were used only for
 <i>H. radicata</i>. Note that in addition to manipulating
 presence/absence and timing of flowering, these treatments also affect the
 total floral density of the neighborhood.
 <i>Measurements</i> We quantified seedset of 3
 individuals of each focal native species within plots, representing three
 phenological stages to capture phenological spread in the native
 population: Early (first individuals of the species to bloom in plot),
 Peak (blooming during maximum conspecific floral density), and Late
 blooming (site-wide, &gt;80% of conspecifics with mostly senescing
 flowers). We selected only plants that were estimated to be in “full
 bloom” (<i>i.e., </i>bearing multiple flowers/inflorescences),
 haphazardly chose one newly opening inflorescence on each of these
 individuals, and bagged the inflorescence when it had senesced to ensure
 seed capture. To quantify pollinator dependence, we also excluded
 pollinators on one additional individual of each native species using a
 breathable bag, and collected seed after senescence.  When counting seed
 from pollinator-excluded and naturally pollinated flowers, we also
 recorded evidence of predispersal seed predator activity that might reduce
 seed counts (insect presence or seed residues). We observed pollinator visitation
 to each focal native species 3 times per plot per plant species during the
 bloom season: early, mid, and late. Observations were performed for
 fifteen minutes on sunny days &gt; 15.5°C. Visiting
 insects were netted in sites once a week for three weeks and preserved in
 reference collections; specimens were classified into visually
 recognizable morphospecies, and further observations used these
 morphospecies designations without collecting specimens. We counted visits
 to the focal native individuals, identified each visitor, and recorded the
 number of conspecific floral units (flowers or inflorescences) within the
 1x1m subplot where the focal plants were located to quantify floral patch
 size. Visits were counted only if there was contact between the visitor
 and flower stigmas or anthers. We surveyed floral richness and abundance
 biweekly in all plots as a covariate, by counting open inflorescences in 6
 randomly chosen 1x1m subplots per 5x5m plot.
description: For all the .csv files: phentrt=phenology
 treatment. NAT=control plot without any exotic forb added, ECYT=potted C.
 scoparius placed in plots ~2 weeks in advance of typical flowering peak,
 RCYT=potted C. scoparius placed in plots at typical flowering peak,
 EHYP=potted H. radicata placed in plots ~2 weeks in advance of typical
 flowering peak, RHYP=potted H. radicata placed in plots around typical
 flowering peak, LHYP=potted H. radicata placed in plots ~2 weeks later
 than typical flowering peak block=randomized block.
 Site was divided into 8 blocks, A-H plot=a 5x5 m plot;
 1-7 species=six-letter codons representing the 7 native
 western Washington prairie forbs listed above: ACHMIL=<em>Achillea
 millefolium; </em>BROELE=<em>Brodiaea elegans;</em>
 CAMQUA=<em>Camassia quamash;</em> CAMROT=<em>Campanula
 rotundifolia;</em> DODHEN=<em>Dodecatheon
 hendersonii;</em> EMPTY=no species flowering in plot;
 ERILAN=<em>Eriophyllum lanatum;</em> FRAVIR=<em>Fragaria
 virginiana; </em>FRIAFF=<em>Fritillaria affinis;</em>
 HIECYN=<em>Hieracium cynoglossoides;
 </em>HYPPER=<em>Hypericum perforatum;</em>
 HYPRAD=<em>Hypochaeris radicata;
 </em>LEUVUL=<em>Leucanthemum vulgare;</em>
 LOMUTR=<em>Lomatium utriculatum; </em>LOTMIC=<em>Lotus
 micranthus; </em>LUPLEP=<em>Lupinus lepidus;
 </em>MICLAC=<em>Microseris laciniata;</em>
 PARVIS=<em>Parentucellia viscosa;</em>
 PRUVUL=<em>Prunella vulgaris; </em>RANOCC=<em>Ranunculus
 occidentalis;</em> SOLSPA=<em>Solidago spathulata;
 </em>TAROFF=<em>Taraxacum officinale;</em>
 TEENUD=<em>Teesdalia nudicaulis;
 </em>TRIDUB=<em>Trifolium dubium;
 </em>VICSAT=<em>Vicia sativa;</em>
 VIOADU=<em>Viola adunca;</em> ZIGVEN=<em>Zigadenus
 venenosus.</em> phenstg=a qualitative category
 for when the focal native forb individual flowered relative to others in
 the population: EARLY, PEAK, LATE, or LL ("latelate").
   For seed data:
 polltrt=pollination treatnent imposed: either SELF (pollinators
 excluded with bag) or OPEN (no manipulation, pollinators have access to
 inflorescence) totheads=total number of
 seedheads/pods/capitulas on plant filledheads=number
 with filled seeds FILLEDseednum=number of seeds filled
 (i.e., successfully pollinated) in the seedhead counted
 UNFILLEDseednum=number of seeds unfilled in the seedhead
 counted FILLEDseedwt=weight of filled seeds in the
 seedhead counted UNFILLEDseedwt=weight of unfilled
 seeds in the seedhead counted plwt=aboveground dry
 biomass of plant from which seed was harvested and counted
 infested=evidence of seed predation (insect frass, seed
 fragments): binary variable seedperhead=number of
 filled seeds counted   For
 phenology data: phenobsdate=date flowering
 phenology was observed phenobsjulianday=julian date
 flowering phenology was observed obsperiod=segment of
 season during which observations took place 1-7
 square=1-25. One of 25 1x1m squares making up the 5x5m
 plot. species_counted= a six-letter codon representing
 the identity of forb species flowering in the plot at the time of
 survey blooms=# flowering stems counted for that
 species   For pollinator visitation
 data: patch_size: number of flowering units of the
 focal native forb species present in a 1x1m square chosen for
 observation pollobsdate: date of observation for
 pollinator visitation pollobsjuliandate: julian date of
 observation for pollinator visitation species_watched:
 focal native forb species observed for visitation
 rhsp=<em>Rhamphomyia</em> sp.
 drsp2=<em>Drymeia</em> sp. 2
 anthsp1=<em>Anthomyiid</em> sp.
 unfly1=k=unknown fly 1
 drsp1=<em>Drymeia</em> sp. 1
 erhi=<em>Erystalis hirsuta</em>
 boca=<em>Bombus californicus</em>
 bovo=<em>Bombus vosnesenskii</em>
 ossp1=<em>Osmia</em> sp.
 bomi=<em>Bombus mixtus</em>
 hese=<em>Hemihalictus</em> series
 hasp=<em>Halictid</em> sp.
 andsp1=<em>Andrenid</em> sp.
 apme=<em>Apis mellifera</em>
 nomsp1=<em>Nomada</em> sp.
 duca=<em>Dufourea campanulae</em>
 unfly2=unknown fly 2 unbee1=unknown bee
 1 unwasp1=unknown wasp 1
 beetle1=unknown beetle 1 boma=<em>Bombus
 melanopygus</em> snakefly=unknown
 snakefly unbee2=unknown bee 2 other=
 other taxon not identified, e.g. true bug, earwig, etc.