Abstract
Distance between habitats may impact the composition and corresponding interactions between trophic levels. Mutualistic networks, such as those of plants and pollinators tend to have a core set of properties that often relate to the resilience of the community, or the ability of the community to retain function and structure after a disturbance. Furthermore, network structure is highly dependent on the number of specialists and generalists; however, it is unclear how different groups of species with various life-history strategies influence network structure. In this study, we evaluated how the composition of plants and pollinators within 16 oak-savanna sites changed across a latitudinal gradient. In addition, we evaluated how the abundance of different groups of plants and pollinators affected network metrics related to resilience. We found that the composition of plants and pollinators varied between ecoregions, while pollinator composition further varied with habitat characteristics. Network metrics displayed no spatial pattern but were related to the abundance of several pollinator groups. Above-ground nesting insects had a positive relationship with nestedness and a negative relationship with modularity, while predatory larvae had a negative relationship with modularity. Thus, above-ground nesting insects and predatory larvae could be expected to increase network resilience. This study emphasizes how spatial scales can influence species compositions, which in turn affects the structure of interactions in the community with implications for resilience.
Similar content being viewed by others
References
Almeida-Neto M, Ulrich W (2011) A straightforward computational approach for measuring nestedness using quantitative matrices. Environ Model Softw 26:173–178. https://doi.org/10.1016/j.envsoft.2010.08.003
Altman B, Stephens JL (2012) Land manager guide to bird habitat and populations in oak ecosystems of the Pacific Northwest. American Bird Conservancy and Klamath Bird Observatory, pp 82
Baldwin BG (2014) Origins of plant diversity in the California Floristic Province. Annu Rev Ecol Evol Syst 45:347–369. https://doi.org/10.1146/annurev-ecolsys-110512-135847
Bargen H, Saudhof K, Poehling HM (1998) Prey finding by larvae and adult females of Episyrphus balteatus. Entomol Exp Appl 87:245–254. https://doi.org/10.1023/A:1003213421253
Bartomeus I, Bosch J (2018) Pérdida de polinizadores: evidencias, causas y consecuencias. Rev Ecol y Medio Ambient 27:1–2. https://doi.org/10.7818/ECOS.1542
Bascompte J, Jordano P (2007) Plant–animal mutualistic networks: the architecture of biodiversity. Annu Rev Ecol Evol Syst 38:567–593. https://doi.org/10.1146/annurev.ecolsys.38.091206.095818
Bascompte J, Jordano P, Melián CJ, Olesen JM (2003) The nested assembly of plant-animal mutualistic networks. Proc Natl Acad Sci USA 100:9383–9387. https://doi.org/10.1073/pnas.1633576100
Beckett SJ (2016) Improved community detection in weighted bipartite networks. R Soc open sci 3:140536. https://doi.org/10.1098/rsos.140536
Blüthgen N, Menzel F, Blüthgen N (2006) Measuring specialization in species interaction networks. BMC Ecol 6:1–12. https://doi.org/10.1186/1472-6785-6-9
Blüthgen N, Fründ J, Vázquez DP, Menzel F (2008) What do interaction network metrics tell us about specialization and biological traits. Ecology 89:3387–3399. https://doi.org/10.1890/07-2121.1
Cane JH, Minckley RL, Kervin LJ, Roulston TH, Williams NM (2006) Complex responses within a desert bee guild (Hymenoptera: Apiformes) to urban habitat fragmentation published by: Ecological Society of America. Ecol Appl 16:632–644. https://doi.org/10.1890/1051-0761(2006)016{[}0632:CRWADB]2.0.CO;2
Coux C, Rader R, Bartomeus I, Tylianakis JM (2016) Linking species functional roles to their network roles. Ecol Lett 19:762–770. https://doi.org/10.1111/ele.12612
Cronquist A (1982) Map of the floristic Provinces of North America. Brittonia 34:144–145
Cuartas-Hernández S, Medel R (2015) Topology of plant-flower-visitor networks in a tropical mountain forest: Insights on the role of altitudinal and temporal variation. PLoS ONE. https://doi.org/10.1371/journal.pone.0141804
Danieli-Silva A, de Souza JMT, Donatti AJ, Campos RP, Vicente-Silva J, Freitas L, Varassin IG (2012) Do pollination syndromes cause modularity and predict interactions in a pollination network in tropical high-altitude grasslands? Oikos 121:35–43. https://doi.org/10.1111/j.1600-0706.2011.19089.x
De Frutos Á, Navarro T, Pueyo Y, Alados CL (2015) Inferring resilience to fragmentation-induced changes in plant communities in a semi-arid Mediterranean ecosystem. PLoS ONE 10:1–18. https://doi.org/10.1371/journal.pone.0118837
Dohzono I, Yokoyama J (2010) Impacts of alien bees on native plant–pollinator relationships: a review with special emphasis on plant reproduction. Appl Entomol Zool 45:37–47. https://doi.org/10.1303/aez.2010.37
Dormann CF, Strauss R (2014) A method for detecting modules in quantitative bipartite networks. Methods Ecol Evol 5:90–98. https://doi.org/10.1111/2041-210X.12139
Dormann CF, Fruend J, Gruber B (2017) Package ‘bipartite’, GitHub repository, pp 1–158. https://github.com/biometry/bipartite
Dupont YL, Padrón B, Olesen JM, Petanidou T (2009) Spatio-temporal variation in the structure of pollination networks. Oikos 118:1261–1269. https://doi.org/10.1111/j.1600-0706.2009.17594.x
Elle E, Gielens GA, Elwell SL (2012) The use of pollination networks in conservation. Botany 90:525–534. https://doi.org/10.1139/b2012-061
Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD (2004) Pollination syndromes and floral specialization. Annu Rev Ecol Evol Syst 35:375–403. https://doi.org/10.1146/annurev.ecolsys.34.011802.132347
Ferreira PA, Boscolo D, Viana BF (2013) What do we know about the effects of landscape changes on plant–pollinator interaction networks? Ecol Indic 31:35–40. https://doi.org/10.1016/j.ecolind.2012.07.025
Fontaine C, Dajoz I, Meriguet J, Loreau M (2006) Functional diversity of plant–pollinator interaction webs enhances the persistence of plant communities. PLoS Biol 4:0129–0135. https://doi.org/10.1371/journal.pbio.0040001
Fuchs MA (2001) Towards a recovery strategy for garry oak and associated ecosystems in Canada: ecological assessment and literature review. Technical Report GBEI/EC-00-030. Environment Canada, Canadian Wildlife Service, Pacific and Yukon Region, pp 1–118
Giannini TC, Garibaldi LA, Acosta AL, Silva JS, Maia KP, Saraiva AM, Guimarães PR Jr, Kleinert AMP (2015) Native and non-native supergeneralist bee species have different effects on plant-bee networks. PLoS ONE 10:1–13. https://doi.org/10.1371/journal.pone.0137198
Gibson RH, Knott B, Eberlein T, Memmott J (2011) Sampling method influences the structure of plant–pollinator networks. Oikos 120:822–831. https://doi.org/10.1111/j.1600-0706.2010.18927.x
Gielens G, Gillespie S, Neame L, Elle E (2014) Pollen limitation is uncommon in an endangered oak savannah ecosystem. Botany 92:743–748. https://doi.org/10.1139/cjb-2014-0054
Glenny WR, Runyon JB, Burkle LA (2018) Drought and increased CO2 alter floral visual and olfactory traits with context-dependent effects on pollinator visitation. New Phytol 220:785–798. https://doi.org/10.1111/nph.15081
Goldstein J, Zych M (2016) What if we lose a hub? Experimental testing of pollination network resilience to removal of keystone floral resources. Arthropod Plant Interact 10:263–271. https://doi.org/10.1007/s11829-016-9431-2
Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science. https://doi.org/10.1126/science.1255957
Jha S, Vandermeer JH (2009) Contrasting bee foraging in response to resource scale and local habitat management. Oikos 118:1174–1180. https://doi.org/10.1111/j.1600-0706.2009.17523.x
Junker RR, Blüthgen N, Brehm T, Binkenstein J, Paulus J, Schaefer HM, Stang M (2013) Specialization on traits as basis for the niche-breadth of flower visitors and as structuring mechanism of ecological networks. Funct Ecol 27:329–341. https://doi.org/10.1111/1365-2435.12005
Kaiser-Bunbury CN, Muff S, Memmott J, Müller CB, Caflisch A (2010) The robustness of pollination networks to the loss of species and interactions: a quantitative approach incorporating pollinator behaviour. Ecol Lett 13:442–452. https://doi.org/10.1111/j.1461-0248.2009.01437.x
Kennedy C, Lonsdorf E, Neel MC, Williams NW, Ricketts TH, Winfree R, Bommarco R, Brittain C, Burley AL, Cariveau D, Carvalheiro G, Chacoff NP, Cunningham SA, Danforth BN, Dudenhöffer JH, Elle E, Gaines HR, Garibaldi LA, Gratton C, Holzschuh A, Isaacs R, Javorek SK, Jha S, Klein AM, Krewenka K, Mandelik Y, Mayfield MM, Morandin L, Neame L, Otieno M, Park M, Potts SG, Rundlöf M, Saez A, Steffan-Dewenter I, Taki H, Viana BF, Westphal C, Wilson JK, Greenleaf SS, Kremen C (2013) A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecol Lett 16:584–599. https://doi.org/10.1111/ele.12082
Klinkenberg B (ed) (2018) E-Flora BC: electronic atlas of the Flora of British Columbia [eflora.bc.ca]. Lab for Advanced Spatial Analysis, Department of Geography, University of British Columbia, Vancouver. Accessed Summer 2018
Lance RF, Bailey P, Lindsay DL, Cobb NS (2017) Precipitation and the robustness of a plant and flower-visiting insect network in a xeric ecosystem. J Arid Environ 144:48–59. https://doi.org/10.1016/j.jaridenv.2017.03.015
Lázaro A, Tur C (2018) Los cambios de uso del suelo como responsables del declive de polinizadores. Ecosistemas 27(2):23–33. https://doi.org/10.7818/ECOS.1378
Locky DA, Bayley SE (2010) Plant diversity in wooded moderate-rich fens across boreal western Canada: an ecoregional perspective. Biodivers Conserv 19:3525–3543. https://doi.org/10.1007/s10531-010-9914-x
Lucas A, Bodger O, Brosi BJ, Ford CR, Forman DW, Greig C, Hegarty M, Neyland PJ, de Vere N (2018) Generalization and specialization in hoverfly (Syrphidae) grassland pollen transport networks revealed by DNA metabarcoding. J Anim Ecol 87:1008–1021. https://doi.org/10.1111/1365-2656.12828
Mallinger RE, Gaines-day HR, Gratton C (2017) Do managed bees have negative effects on wild bees? A systematic review of the literature. PLoS ONE 12:1–32
Mayer C, Adler LS, Armbruster WS, Dafni A, Eardley C, Huang SQ, Kevan PG, Ollerton J, Packer L, Ssymank A, Stout JC, Potts SG (2011) Pollination ecology in the 21st century: key questions for future research. J Pollinat Ecol 3:8–23
McDonald R, McKnight M, Weiss D, Selig E, O’Connor M, Violin C, Moody A (2005) Species compositional similarity and ecoregions: do ecoregion boundaries represent zones of high species turnover? Biol Conserv 126:24–40. https://doi.org/10.1016/j.biocon.2005.05.008
Mello MAR, de Santos GM, Mechi MR, Hermes MG (2011) High generalization in flower-visiting networks of social wasps. Acta Oecol 37:37–42. https://doi.org/10.1016/j.actao.2010.11.004
Menz MHM, Phillips RD, Winfree R, Kremen C, Aizen MA, Johnson SD, Dixon KW (2011) Reconnecting plants and pollinators: challenges in the restoration of pollination mutualisms. Trends Plant Sci 16:4–12. https://doi.org/10.1016/j.tplants.2010.09.006
Michener CD (2007) The bees of the world, 2nd edn. Johns Hopkins University Press, Baltimore
Minckley RL, Cane JH, Kervin L (2000) Origins and ecological consequences of pollen specialization among desert bees. Proc R Soc B Biol Sci 267:265–271
Montero-Castaño A, Vilà M (2017) Influence of the honeybee and trait similarity on the effect of a non-native plant on pollination and network rewiring. Funct Ecol 31:142–152. https://doi.org/10.1111/1365-2435.12712
Morales JM, Vázquez DP (2008) The effect of space in plant–animal mutualistic networks: insights from a simulation. Oikos 117:1362–1370
Neame LA, Griswold T, Elle E (2013) Pollinator nesting guilds respond differently to urban habitat fragmentation in an oak-savannah ecosystem. Insect Conserv Divers 6:57–66. https://doi.org/10.1111/j.1752-4598.2012.00187.x
Ogilvie JE, Forrest JR (2017) Interactions between bee foraging and floral resource phenology shape bee populations and communities. Curr Opin Insect Sci 21:75–82. https://doi.org/10.1016/j.cois.2017.05.015
Oksanen J (2015) Multivariate analysis of ecological communities in R: vegan tutorial, pp 1-43. https://www.mooreecology.com/uploads/2/4/2/1/24213970/vegantutor.pdf
Oksanen, J, Blanchet F, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin P, O'Hara RB, Simpson G, Solymos P, Henry M, Stevens H, Szoecs E, Wagner H (2019) Package ‘vegan’, GitHub repository, pp 1–296. https://cran.r-project.org, https://github.com/vegandevs/vegan
Olesen JM, Bascompte J, Elberling H, Jordano P (2008) Temporal dynamics in a pollination networks. Ecology 89:1573–1582. https://doi.org/10.1890/07-0451.1
Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326. https://doi.org/10.1111/j.1600-0706.2010.18644.x
Olsson O, Bolin A, Smith HG, Lonsdorf EV (2015) Modeling pollinating bee visitation rates in heterogeneous landscapes from foraging theory. Ecol Modell 316:133–143. https://doi.org/10.1016/j.ecolmodel.2015.08.009
Ozinga WA, Schaminée JHJ, Bekker RM, Bonn S, Poschlod P, Tackenerg O, Bakker J, van Groenendael JM (2005) Predictability of plant species composition from environmental conditions is constrained by dispersal limitation. Oikos 108:555–561. https://doi.org/10.1111/j.0030-1299.2005.13632.x
Pauw A, Stanway R (2015) Unrivalled specialization in a pollination network from South Africa reveals that specialization increases with latitude only in the Southern Hemisphere. J Biogeogr 42:652–661. https://doi.org/10.1111/jbi.12453
Pellissier L, Albouy C, Bascompte J, Farwig N, Graham C, Loreau M, Maglianesi MA, Melian CJ, Pitteloud C, Roslin T, Rohr R, Saavedra S, Thuiller W, Woodward G, Zimmermann NE, Gravel D (2018) Comparing species interaction networks along environmental gradients. Biol Rev 93:785–800. https://doi.org/10.1111/brv.12366
Pisanty G, Mandelik Y (2015) Profiling crop pollinators: life history traits predict habitat use and crop visitation by Mediterranean wild bees. Ecol Appl 25:742–752. https://doi.org/10.1890/14-0910.1.sm
Poisot T, Kéfi S, Morand S, Stanko M, Marquet PA, Hochberg ME (2015) A continuum of specialists and generalists in empirical communities. PLoS ONE 10:1–12. https://doi.org/10.1371/journal.pone.0114674
Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353. https://doi.org/10.1016/j.tree.2010.01.007
Santamaría S, Galeano J, Pastor JM, Méndez M (2014) Robustness of alpine pollination networks: effects of network structure and consequences for endemic plants. Arctic Antarct Alp Res 46:568–580. https://doi.org/10.1657/1938-4246-46.3.568
Santamaría S, Galeano J, Pastor JM, Méndez M (2016) Removing interactions, rather than species, casts doubt on the high robustness of pollination networks. Oikos 125:526–534. https://doi.org/10.1111/oik.02921
Schiestl FP, Johnson SD (2013) Pollinator-mediated evolution of floral signals. Trends Ecol Evol 28:307–315. https://doi.org/10.1016/j.tree.2013.01.019
Schultz CB, Henry E, Carleton A, Hicks T, Thomas R, Potter A, Collins M, Linders M, Fimbel C, Black S, Anderson HE, Diehl G, Hamman S, Gilbert R, Foster J, Hays D, Wilderman D, Davenport R, Steel E, Page N, Lilley PL, Heron J, Kroeker N, Webb C, Reader B (2011) Conservation of Prairie-Oak Butterflies in Oregon, Washington, and British Columbia. Northwest Sci 85:361–388. https://doi.org/10.3955/046.085.0221
Shackelford G, Steward PR, Benton TG, Kunin WE, Potts SG, Biesmeijer JC, Sait M (2013) Comparison of pollinators and natural enemies: a meta-analysis of landscape and local effects on abundance and richness in crops. Biol Rev 88:1002–1021. https://doi.org/10.1111/brv.12040/abstract
Smith HA, Chaney WE (2007) A survey of syrphid predators of Nasonovia ribisnigri in organic lettuce on the central coast of Californ. Biol Microb Control 100:39–48. https://doi.org/10.1603/0022-0493(2007)100[39:ASOSPO]2.0.CO;2
Soares RGS, Ferreira PA, Lopes LE (2017) Can plant–pollinator network metrics indicate environmental quality? Ecol Indic 78:361–370. https://doi.org/10.1016/j.ecolind.2017.03.037
Spiesman BJ, Inouye BD (2013) Habitat loss alters the architecture of plant–pollinator interaction networks. Ecology 94:2688–2696. https://doi.org/10.1890/13-0977.1
Steffan-Dewenter I, Munzenberg U, Bürger C, Thies C, Tscharntke T (2002) Scale-dependent effects of landscape context on three pollinator guilds. Ecology 83:1421–1432. https://doi.org/10.1890/0012-9658(2002)083[1421:SDEOLC]2.0.CO;2
Trøjelsgaard K, Olesen JM (2013) Macroecology of pollination networks. Glob Ecol Biogeogr 22:149–162. https://doi.org/10.1111/j.1466-8238.2012.00777.x
Vanbergen AJ (2013) Threats to an ecosystem service: pressures on pollinators. Front Ecol Environ 11:251–259. https://doi.org/10.1890/120126
Vázquez DP, Lomascolo SB, Maldonado MB, Chacoff NP, Dorado J, Stevani EL, Vitale NL (2012) The strength of plant–pollinator interactions. Ecology 93:719–725
Vázquez DP, Ramos-Jiliberto R, Urbani P, Valdovinos FS (2015) A conceptual framework for studying the strength of plant–animal mutualistic interactions. Ecol Lett 18:385–400. https://doi.org/10.1111/ele.12411
Vanbergen AJ, Woodcock BA, Heard MS, Chapman DS (2017) Network size, structure and mutualism dependence affect the propensity for plant-pollinator extinction cascades. Funct Ecol 31(6):1285–1293
Vesely DG, Rosenberg DK (2010) Wildlife conservation in the willamette valley’s remnant prairies and oak habitats: a research synthesis. Interagency Special Status Sensitive Species Program, pp 1–132
Vieira MC, Almeida-Neto M (2015) A simple stochastic model for complex coextinctions in mutualistic networks: robustness decreases with connectance. Ecol Lett 18:144–152. https://doi.org/10.1111/ele.12394
Wagenmakers E-J, Farrell S (2004) AIC model selection using Akaike weights AIC model selection using Akaike weights. Psychon Bull Rev 11:192–196. https://doi.org/10.3758/BF03206482
Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043–1060
Watts S, Dormann CF, González AMM, Ollerton J (2016) The influence of floral traits on specialization and modularity of plant–pollinator networks in a biodiversity hotspot in the Peruvian Andes. Ann Bot. https://doi.org/10.1093/AOB/MCW114
Wiken E, Nava FJ, Griffith G (2011) North American terrestrial ecoregions—level III. Commission for Environmental Cooperation, Montreal
Williams NM, Crone EE, Roulston TH, Minckley RL, Packer L, Potts SG (2010) Ecological and life-history traits predict bee species responses to environmental disturbances. Biol Conserv 143:2280–2291. https://doi.org/10.1016/j.biocon.2010.03.024
Winfree R, Bartomeus I, Cariveau DP (2011) Native pollinators in anthropogenic habitats. Annu Rev Ecol Evol Syst 42:1–22. https://doi.org/10.1146/annurev-ecolsys-102710-145042
Winfree R, Williams NM, Dushoff J, Kremen C (2014) Species abundance, not diet breadth, drives the persistence of the most linked pollinators as plant-pollinator networks disassemble. Am Nat 183:600–611
Wray JC, Elle E (2014) Flowering phenology and nesting resources influence pollinator community composition in a fragmented ecosystem. Landsc Ecol 30:261–272. https://doi.org/10.1007/s10980-014-0121-0
Wu P, Axmacher JC, Song X, Zhang X, Xu H, Chen C, Yu Z, Liu Y (2018) Effects of plant diversity, vegetation composition, and habitat type on different functional trait groups of wild bees in Rural Beijing. J Insect Sci. https://doi.org/10.1093/jisesa/iey065
Zurbuchen A, Cheesman S, Klaiber J, Müller A, Hein S, Dorn S (2010) Long foraging distances impose high costs on offspring production in solitary bees. J Anim Ecol 79:674–681. https://doi.org/10.1111/j.1365-2656.2010.01675.x
Acknowledgements
We thank Sandra Gillespie, Melissa Guzman, and Allison Dennert for commenting on the manuscript, and Emily Merlo for assistance with field work. Additionally, we thank Daniel Greenburg, Collin Bailey, and Philina English for statistical advice. We are grateful to all the land managers for giving us permission to conduct our study in their sites and Terry Griswold and Jason Gibbs for assistance with some insect identification. This project was funded by the Natural Sciences and Engineering Research Council (NSERC; R311 614; Discovery Grant to EE) with partial funding from the Graduate and Postdoctoral Studies program at Simon Fraser University (to TK).
Author information
Authors and Affiliations
Contributions
TK and EE conceived, designed, and executed this study and wrote the manuscript. TK analyzed the data and created the figures and tables.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Anne Worley.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kelly, T., Elle, E. Effects of community composition on plant–pollinator interaction networks across a spatial gradient of oak-savanna habitats. Oecologia 193, 211–223 (2020). https://doi.org/10.1007/s00442-020-04661-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-020-04661-5