Important pollinator species for conserving rare plant species endemic to San Clemente Island, California
Keywords:California Channel Islands, Endangered species, pollination, conservation
Much effort has been spent on the conservation of rare, threatened, and endangered plants in the biodiversity hotspot of the California Floristic Province, however little is known about the identity of their pollinators. In this study we provide the first formal study on the identity of the invertebrate pollinators of five rare endemic island plant species from San Clemente Island, the southernmost of the California Channel Islands: Delphinium variegatum ssp kinkiense, Lithophragma maximum, Malacothamnus clementinus, Malva assurgentiflora ssp glabra, and Sibara filifolia. We surveyed plant-pollinator interactions at populations of each focal plant species using timed sweep-netting. We used pollinator capture data to compile bipartite interaction networks for each plant population, and calculated centrality indices (degree, betweenness centrality, and closeness centrality) of pollinators to identify species important to network stability. We found a significant effect of pollinator taxonomic group (fly, bee, wasp, or Lepidopteran) on some indices of pollinator centrality in interaction networks, and variation in pollinator centrality between different locations. Hoverflies, moths, and butterflies were important generalists with higher network centrality across all plant populations, while bees tended to be more specialists within their networks, except for the Malva assurgentiflora ssp glabra network, where bees were on average of higher centrality than flies. We recommend targeted restoration practices for future study that could support pollination both directly and indirectly to focal rare plant species of conservation interest across plant populations. These practices could augment general pollinator conservation best practices such as reducing pesticide use and planting native plant species to provide increased pollination to endangered plants.
Antoine CM, Forrest JR (2021) Nesting habitat of ground‐nesting bees: a review. Ecological Entomology 46:143-159. https://doi.org/10.1111/een.12986
Badenes-Pérez FR (2022) Benefits of insect pollination in Brassicaceae: A meta-analysis of self-compatible and self-Incompatible crop species. Agriculture 12:446. https://doi.org/10.3390/agriculture12040446
Barton K (2022). MuMIn: Multi-model inference R package version 1.4.60. URL: https://CRANR-projectorg/package=MuMIn.
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67:1-48. https://doi.org/10.18637/jss.v067.i01
Bischoff M, Campbell DR, Lord JM, Robertson AW (2013) The relative importance of solitary bees and syrphid flies as pollinators of two outcrossing plant species in the New Zealand alpine. Austral Ecology 38:169-176. https://doi.org/10.1111/j.1442-9993.2012.02389.x
Byrd BF, Raab LM (2007) Prehistory of the southern bight: Models for a new millennium. In: Jones TL, Klar K (eds) California prehistory: Colonization, culture, and complexity. Altamira Inc., DC, pp 215-227.
California Native Plant Society (2022) Rare Plant Inventory. [online] URL: https://www.cnps.org/rare-plants/cnps-inventory-of-rare-plants (accessed 29 December 2022).
Cayenne Engel E, Irwin RE (2003) Linking pollinator visitation rate and pollen receipt. American Journal of Botany 90:1612-1618. https://doi.org/10.3732/ajb.90.11.1612
Celorio-Mancera MDLP, Wheat CW, Huss M, Vezzi F, Neethiraj R, Reimegård J, Nylin S, Janz N (2016) Evolutionary history of host use, rather than plant phylogeny, determines gene expression in a generalist butterfly. BMC Evolutionary Biology 16:1-10. https://doi.org/10.1186/s12862-016-0627-y
Courtney SP, Hill CJ, Westerman A (1982) Pollen carried for long periods by butterflies. Oikos 38:260-263. https://doi.org/10.2307/3544030
Crespo A, Aguilar JM, Pintado K, Tinoco BA (2022) Key plant species to restore plant–hummingbird pollinator communities in the southern Andes of Ecuador. Restoration Ecology 30:e13557. https://doi.org/10.1111/rec.13557
Fernandez de Castro AG, Moreno‐Saiz JC, Fuertes‐Aguilar J (2017) Ornithophily for the nonspecialist: Differential pollination efficiency of the Macaronesian island paleoendemic Navaea phoenicea (Malvaceae) by generalist passerines. American Journal of Botany 104:1556-1568. https://doi.org/10.3732/ajb.1700204
Friberg M, Schwind C, Raguso RA, Thompson JN (2013) Extreme divergence in floral scent among woodland-star species (Lithophragma spp) pollinated by floral parasites. Annals of Botany 111:539-550. https://doi.org/10.1093/aob/mct007
Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347:1255957. https://doi.org/10.1126/science.1255957
Jauker F, Speckmann M, Wolters V (2016) Intra-specific body size determines pollination effectiveness. Basic and Applied Ecology 17:714-719. https://doi.org/10.1016/j.baae.2016.07.004
Junak SA, Wilken DH (1998) Sensitive plant status survey Naval Auxiliary Landing Field, San Clemente Island, California. Santa Barbara Botanic Garden, Santa Barbara.
Kearns CA (2001) North American Dipteran pollinators: assessing their value and conservation status. Conservation Ecology 5:1-9. https://doi.org/10.5751/ES-00262-050105
Kellogg EM, JL Kellogg (1994) San Clemente Island vegetation condition and trend. Southwest Division Naval Facilities Engineering Command, San Diego.
Mawdsley JR (2003) The importance of species of Dasytinae (Coleoptera: Melyridae) as pollinators in western North America. The Coleopterists Bulletin 57:154-160. https://doi.org/10.1649/541
McEachern K, Atwater T, Collins PW, Faulkner K, Richards DV (2016) Managed island ecosystems. In: Mooney H, Zavaleta E (eds) Ecosystems of California. University of California Press, Berkeley pp 755-778.
McGlaughlin ME, Riley L, Brandsrud M, Archibal E, Helenurm M, Helenurm K (2015) How much is enough? Minimum sampling intensity required to capture extant genetic diversity in ex situ seed collections: examples from the endangered plant Sibara filifolia (Brassicaceae). Conservation Genetics 16:253-266. https://doi.org/10.1007/s10592-014-0655-3
Memmott J, Waser NM, Price MV (2004) Tolerance of pollination networks to species extinctions. Proceedings of the Royal Society of London. Series B: Biological Sciences 271:2605-2611. https://doi.org/10.1098/rspb.2004.2909
Michener (2007) The bees of the world (2nd ed.). Johns Hopkins University Press. https://doi.org/10.56021/9780801885730
Mittermeier, R. A., Turner, W. R., Larsen, F. W., Brooks, T. M., & Gascon, C. (2011). Global biodiversity conservation: the critical role of hotspots. In Biodiversity hotspots: distribution and protection of conservation priority areas (pp. 3-22). Berlin, Heidelberg: Springer Berlin Heidelberg. https://doi.org/10.1007/978-3-642-20992-5_1
Olesen JM, Bascompte J, Dupont YL, Elberling H, Rasmussen C, Jordano P (2011) Missing and forbidden links in mutualistic networks. Proceedings of the Royal Society B: Biological Sciences 278:725-732. https://doi.org/10.1098/rspb.2010.1371
Opsahl T (2009) Structure and evolution of weighted networks. University of London. [online] URL: https://toreopsahl.com/publications/thesis/ (accessed December 2022).
R Core Team (2023) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, URL https://www.R-project.org/
Ramírez-Rodríguez R, Amich F (2017) Effects of local abundance on pollination and reproduction in Delphinium fissum ssp sordidum (Ranunculaceae). Botany Letters 164:371-383. https://doi.org/10.1080/23818107.2017.1383307
Sahli HF, Conner JK (2007) Visitation, effectiveness, and efficiency of 15 genera of visitors to wild radish, Raphanus raphanistrum (Brassicaceae). American Journal of Botany 94:203-209. https://doi.org/10.3732/ajb.94.2.203
Sazima C, Guimarães Jr PR, Dos Reis SF, Sazima I (2010) What makes a species central in a cleaning mutualism network? Oikos 119:1319-1325. https://doi.org/10.1111/j.1600-0706.2009.18222.x
Severns PM (2004) Creating bare ground increases presence of native pollinators in Kincaid’s lupine seeding plots. Ecological Restoration 22:234-235.
Sihag RC (1986) Insect pollination increases seed production in cruciferous and umbelliferous crops. Journal of Apicultural Research 25:121-126. https://doi.org/10.1080/00218839.1986.11100704
Taylor (1965) The genus Lithophragma (Saxifragaceae). University of California Publications in Botany 37:1-89.
Thompson JN (1997) Evaluating the dynamics of coevolution among geographically structured populations. Ecology 78:1619-1623. https://doi.org/10.1890/0012-9658(1997)078[1619:ETDOCA]2.0.CO;2
U. S. Fish & Wildlife Service (2007) Malacothamnus clementinus (San Clemente Island bush mallow) 5-year review: Summary and evaluation. United States Fish and Wildlife Service, Carlsbad.
U. S. Fish & Wildlife Service (2008) Delphinium variegatum ssp kinkiense (San Clemente Island Larkspur) 5-year review: Summary and evaluation. United States Fish and Wildlife Service, Carlsbad.
U. S. Fish & Wildlife Service (2020a) Lithophragma maximum (Island woodland-star) 5-year review: Summary and evaluation United States Fish and Wildlife Service, Carlsbad.
U. S. Fish & Wildlife Service (2020b) Sibara filifolia (Santa Cruz Island rock-cress) 5-year review: Summary and evaluation. United States Fish and Wildlife Service, Carlsbad.
U. S. Fish & Wildlife Service (2021) Draft post-delisting monitoring plan for five San Clemente Island taxa. United States Fish and Wildlife Service, Carlsbad.
Valverde, J., Gómez, J. M., & Perfectti, F. (2016). The temporal dimension in individual‐based plant pollination networks. Oikos, 125(4), 468-479. https://doi.org/10.1111/oik.02661
Wallace LE, Furches MS, Helenurm K (2006) Polymorphic microsatellite loci in Lithophragma maximum (Saxifragaceae), an endemic plant of San Clemente Island. Molecular Ecology Notes 6:459-461. https://doi.org/10.1111/j.1471-8286.2006.01272.x
Waser NM, Price MV (1989) Optimal outcrossing in Ipomopsis aggregata: Seed set and offspring fitness. Evolution 43:1097-1109. https://doi.org/10.1111/j.1558-5646.1989.tb02554.x
Waser NM, Price MV (1991) Outcrossing distance effects in Delphinium nelsonii: pollen loads, pollen tubes, and seed set. Ecology 72:171-179. https://doi.org/10.2307/1938912
Willcox BK, Aizen MA, Cunningham SA, Mayfield MM, Rader R (2017) Deconstructing pollinator community effectiveness. Current Opinion in Insect Science 21:98-104. https://doi.org/10.1016/j.cois.2017.05.012
Williams CF, Ruvinsky J, Scott PE, Hews DK (2001) Pollination, breeding system, and genetic structure in two sympatric Delphinium (Ranunculaceae) species. American Journal of Botany 88:1623-1633. https://doi.org/10.2307/3558407
Willmer P, Finlayson K (2014) Big bees do a better job: intraspecific size variation influences pollination effectiveness. Journal of Pollination Ecology 14:244-254. https://doi.org/10.26786/1920-7603(2014)22
Wratten SD, Gillespie M, Decourtye A, Mader E, Desneux N (2012) Pollinator habitat enhancement: benefits to other ecosystem services. Agriculture, Ecosystems & Environment 159:112-122. https://doi.org/10.1016/j.agee.2012.06.020
Yoshida Y, Nikkeshi A, Chishiki A (2021) Identification of effective pollinators of Primula sieboldii E. Morren in a wild habitat in Hiroshima, Japan. Plant Species Biology 36:157-169. https://doi.org/10.1111/1442-1984.12302
How to Cite
Copyright (c) 2023 Jenny Hazlehurst, Stephanie Calloway, Denise Knapp
This work is licensed under a Creative Commons Attribution 4.0 International License.
JPE is an open access journal which means that all content is freely available without charge to the user or his/her institution.
Authors who publish with this journal agree to the following terms:
1) Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
2) Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
3) Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
To assure a broader targeted audience, content will be included into databases (such as EBSCO) and directories (such as DOAJ).