Abstract
The recent decline in pollinator biodiversity, notably in the case of wild bee populations, puts both wild and agricultural ecosystems at risk of ecological community collapse. This has triggered calls for further study of these mutualistic communities in order to more effectively inform restoration of disturbed plant–pollinator communities. Here, we use a dynamic network model to test a variety of translocation strategies for restoring a community after it experiences the loss of some of its species. We consider the reintroduction of extirpated species, both immediately after the original loss and after the community has reequilibrated, as well as the introduction of other native species that were originally absent from the community. We find that reintroducing multiple highly interacting generalist species best restores species richness for lightly disturbed communities. However, for communities that experience significant losses in biodiversity, introducing generalist species that are not originally present in the community may most effectively restore species richness, although in these cases the resultant community often shares few species with the original community. We also demonstrate that the translocation of a single species has a minimal impact on both species richness and the frequency of community collapse. These results have important implications for restoration practices in the face of varying degrees of community perturbations, the refinement of which is crucial for community management.
Similar content being viewed by others
References
Aizen MA, Garibaldi LA, Cunningham SA, Klein AM (2009) How much does agriculture depend on pollinators? Lessons from long-term trends in crop production. Ann Bot 103:1579–1588. doi:10.1093/aob/mcp076
Akçakaya HR (2000) Conservation and management for multiple species: integrating field research and modeling into management decisions. Environ Manage 26:S75–S83. doi:10.1007/s002670010063
Albert R, Barabási A-L (2002) Statistical mechanics of complex networks. Rev Mod Phys 74:47–97. doi:10.1103/RevModPhys.74.47
Allen-Wardell G, Bernhardt P, Bitner R et al (1998) The potential consequences of pollinator declines on the conservation of biodiversity and stability of food crop yields. Conserv Biol 12:8–17. doi:10.2307/2387457
Almeida-Neto M, Guimarães P, Guimarães PR et al (2008) A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117:1227–1239. doi:10.1111/j.0030-1299.2008.16644.x
Barrows CW, Swartz MB, Hodges WL et al (2005) A framework for monitoring multiple-species conservation plans. J Wildl Manag 69:1333–1345. doi:10.2193/0022-541X(2005)69[1333:AFFMMC]2.0.CO;2
Bascompte J (2008) Mutualistic networks. Front Ecol Environ 7:429–436. doi:10.1890/080026
Bascompte J, Jordano P (2007) Plant-animal mutualistic networks: the architecture of biodiversity. Annu Rev Ecol Evol Syst 38:567–593. doi: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 100:9383–9387. doi:10.1073/pnas.1633576100
Benayas JMR, Newton AC, Diaz A, Bullock JM (2009) Enhancement of biodiversity and ecosystem services by ecological restoration: a meta-analysis. Science 325:1121–1124. doi:10.1126/science.1172460
Biesmeijer JC, Roberts SPM, Reemer M et al (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313:351–354. doi:10.1126/science.1127863
Bjerknes A-L, Totland Ø, Hegland SJ, Nielsen A (2007) Do alien plant invasions really affect pollination success in native plant species? Biol Conserv 138:1–12. doi:10.1016/j.biocon.2007.04.015
Bond WJ (1994) Do mutualisms matter? Assessing the impact of pollinator and disperser disruption on plant extinction. Philos Trans Biol Sci 344:83–90. doi:10.2307/56158
Bullock JM, Aronson J, Newton AC et al (2011) Restoration of ecosystem services and biodiversity: conflicts and opportunities. Trends Ecol Evol 26:541–549. doi:10.1016/j.tree.2011.06.011
Burkle LA, Marlin JC, Knight TM (2013) Plant-pollinator interactions over 120 years: loss of species, co-occurrence, and function. Science 339:1611–1615. doi:10.1126/science.1232728
Cadotte MW, Carscadden K, Mirotchnick N (2011) Beyond species: functional diversity and the maintenance of ecological processes and services. J Appl Ecol 48:1079–1087. doi:10.1111/j.1365-2664.2011.02048.x
Campbell C, Yang S, Albert R, Shea K (2011) A network model for plant–pollinator community assembly. Proc Natl Acad Sci 108:197–202. doi:10.1073/pnas.1008204108
Campbell C, Yang S, Shea K, Albert R (2012) Topology of plant-pollinator networks that are vulnerable to collapse from species extinction. Phys Rev E 86:021924. doi:10.1103/PhysRevE.86.021924
Cara AD, Garg A, Micheli GD et al (2007) Dynamic simulation of regulatory networks using SQUAD. BMC Bioinforma 8:462. doi:10.1186/1471-2105-8-462
Colwell RK, Dunn RR, Harris NC (2012) Coextinction and persistence of dependent species in a changing world. Annu Rev Ecol Evol Syst 43:183–203. doi:10.1146/annurev-ecolsys-110411-160304
Devoto M, Bailey S, Craze P, Memmott J (2012) Understanding and planning ecological restoration of plant–pollinator networks. Ecol Lett 15:319–328. doi:10.1111/j.1461-0248.2012.01740.x
Dixon KW (2009) Pollination and restoration. Science 325:571–573. doi:10.1126/science.1176295
Dobson A, Allesina S, Lafferty K, Pascual M (2009) The assembly, collapse and restoration of food webs. Philos Trans R Soc B Biol Sci 364:1803–1806. doi:10.1098/rstb.2009.0002
Dunn RR, Harris NC, Colwell RK et al (2009) The sixth mass coextinction: are most endangered species parasites and mutualists? Proc R Soc B Biol Sci 276:3037–3045. doi:10.1098/rspb.2009.0413
Espinosa-Soto C, Padilla-Longoria P, Alvarez-Buylla ER (2004) A gene regulatory network model for cell-fate determination during Arabidopsis thaliana flower development that is robust and recovers experimental gene expression profiles. Plant Cell 16:2923–2939. doi:10.1105/tpc.104.021725
Fitzpatrick Ú, Murray TE, Paxton RJ et al (2007) Rarity and decline in bumblebees—a test of causes and correlates in the Irish fauna. Biol Conserv 136:185–194. doi:10.1016/j.biocon.2006.11.012
Forup ML, Memmott J (2005) The restoration of plant–pollinator interactions in hay meadows. Restor Ecol 13:265–274. doi:10.1111/j.1526-100X.2005.00034.x
Forup ML, Henson KSE, Craze PG, Memmott J (2008) The restoration of ecological interactions: plant–pollinator networks on ancient and restored heathlands. J Appl Ecol 45:742–752. doi:10.1111/j.1365-2664.2007.01390.x
Garibaldi LA, Steffan-Dewenter I, Winfree R et al (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339:1608–1611. doi:10.1126/science.1230200
Glass L (1975) Classification of biological networks by their qualitative dynamics. J Theor Biol 54:85–107. doi:10.1016/S0022-5193(75)80056-7
Hanski I (1994) A practical model of metapopulation dynamics. J Anim Ecol 63:151–162. doi:10.2307/5591
Herrera CM (1988) Variation in mutualisms: the spatiotemporal mosaic of a pollinator assemblage. Biol J Linn Soc 35:95–125. doi:10.1111/j.1095-8312.1988.tb00461.x
IUCN/SSC Re-introduction Specialist Group (1998) IUCN guidelines for re-introductions. IUCN, Gland, Cambridge
Jordano P, Bascompte J, Olesen JM (2003) Invariant properties in coevolutionary networks of plant–animal interactions. Ecol Lett 6:69–81. doi:10.1046/j.1461-0248.2003.00403.x
Kaiser-Bunbury CN, Memmott J, Müller CB (2009) Community structure of pollination webs of Mauritian heathland habitats. Perspect Plant Ecol Evol Syst 11:241–254. doi:10.1016/j.ppees.2009.04.001
Kaiser-Bunbury CN, Traveset A, Hansen DM (2010) Conservation and restoration of plant–animal mutualisms on oceanic islands. Perspect Plant Ecol Evol Syst 12:131–143. doi:10.1016/j.ppees.2009.10.002
Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Annu Rev Ecol Syst 29:83–112. doi:10.1146/annurev.ecolsys.29.1.83
Klein A-M, Steffan–Dewenter I, Tscharntke T (2003) Fruit set of highland coffee increases with the diversity of pollinating bees. Proc R Soc Lond B Biol Sci 270:955–961. doi:10.1098/rspb.2002.2306
Klein A-M, Vaissière BE, Cane JH et al (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc B Biol Sci 274:303–313. doi:10.1098/rspb.2006.3721
Kremen C (2005) Managing ecosystem services: what do we need to know about their ecology? Ecol Lett 8:468–479. doi:10.1111/j.1461-0248.2005.00751.x
Kremen C, Williams NM, Aizen MA et al (2007) Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land-use change. Ecol Lett 10:299–314. doi:10.1111/j.1461-0248.2007.01018.x
Krumsiek J, Pölsterl S, Wittmann DM, Theis FJ (2010) Odefy—from discrete to continuous models. BMC Bioinforma 11:233. doi:10.1186/1471-2105-11-233
LaBar T, Campbell C, Yang S et al (2013) Global versus local extinction in a network model of plant–pollinator communities. Theor Ecol 6:495–503. doi:10.1007/s12080-013-0182-8
Li S, Assmann SM, Albert R (2006) Predicting essential components of signal transduction networks: a dynamic model of guard cell abscisic acid signaling. PLoS Biol 4:e312. doi:10.1371/journal.pbio.0040312
Lipsey MK, Child MF, Seddon PJ et al (2007) Combining the fields of reintroduction biology and restoration ecology. Conserv Biol. doi:10.1111/j.1523-1739.2007.00806.x
Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228. doi:10.1016/j.tree.2005.02.004
MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton
Mason O, Verwoerd M (2007) Graph theory and networks in biology. IET Syst Biol 1:89–119. doi:10.1049/iet-syb:20060038
Maunder M (1992) Plant reintroduction: an overview. Biodivers Conserv 1:51–61. doi:10.1007/BF00700250
Memmott J, Waser NM, Price MV (2004) Tolerance of pollination networks to species extinctions. Proc R Soc Lond B Biol Sci 271:2605–2611. doi:10.1098/rspb.2004.2909
Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant-pollinator interactions. Ecol Lett 10:710–717. doi:10.1111/j.1461-0248.2007.01061.x
Menz MHM, Phillips RD, Winfree R et al (2011) Reconnecting plants and pollinators: challenges in the restoration of pollination mutualisms. Trends Plant Sci 16:4–12. doi:10.1016/j.tplants.2010.09.006
Montoya D, Rogers L, Memmott J (2012) Emerging perspectives in the restoration of biodiversity-based ecosystem services. Trends Ecol Evol 27:666–672. doi:10.1016/j.tree.2012.07.004
Neal PR (1998) Pollinator restoration. Trends Ecol Evol 13:132–133. doi:10.1016/S0169-5347(97)01322-0
Newman MEJ (2003) The structure and function of complex networks. SIAM Rev 45:167–256. doi:10.1137/S003614450342480
Olesen JM, Jordano P (2002) Geographic patterns in plant–pollinator mutualistic networks. Ecology 83:2416–2424. doi:10.1890/0012-9658(2002)083[2416:GPIPPM]2.0.CO;2
Olesen JM, Bascompte J, Dupont YL, Jordano P (2007) The modularity of pollination networks. Proc Natl Acad Sci 104:19891–19896. doi:10.1073/pnas.0706375104
Olesen JM, Bascompte J, Elberling H, Jordano P (2008) Temporal dynamics in a pollination network. Ecology 89:1573–1582. doi:10.1890/07-0451.1
Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326. doi:10.1111/j.1600-0706.2010.18644.x
Palmer MA, Ambrose RF, Poff NL (1997) Ecological theory and community restoration ecology. Restor Ecol 5:291–300. doi:10.1046/j.1526-100X.1997.00543.x
Pocock MJO, Evans DM, Memmott J (2012) The robustness and restoration of a network of ecological networks. Science 335:973–977. doi:10.1126/science.1214915
Potts SG, Biesmeijer JC, Kremen C et al (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353. doi:10.1016/j.tree.2010.01.007
Ricciardi A, Simberloff D (2009) Assisted colonization is not a viable conservation strategy. Trends Ecol Evol 24:248–253. doi:10.1016/j.tree.2008.12.006
Rodriguez LF (2006) Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biol Invasions 8:927–939. doi:10.1007/s10530-005-5103-3
Rodríguez-Gironés MA, Gonzálvez FG, Llandres AL et al (2013) Possible role of weaver ants, Oecophylla smaragdina, in shaping plant–pollinator interactions in South-East Asia. J Ecol 101:1000–1006. doi:10.1111/1365-2745.12100
Russo L, DeBarros N, Yang S et al (2013) Supporting crop pollinators with floral resources: network-based phenological matching. Ecol Evol 3:3125–3140. doi:10.1002/ece3.703
Sachs JL, Simms EL (2006) Pathways to mutualism breakdown. Trends Ecol Evol 21:585–592. doi:10.1016/j.tree.2006.06.018
Sargent RD, Otto SP (2006) The role of local species abundance in the evolution of pollinator attraction in flowering plants. Am Nat 167:67–80. doi:10.1086/an.2006.167.issue-1
Schlaepfer MA, Sax DF, Olden JD (2011) The potential conservation value of non-native species. Conserv Biol 25:428–437. doi:10.1111/j.1523-1739.2010.01646.x
Shackelford N, Hobbs RJ, Burgar JM et al (2013) Primed for change: developing ecological restoration for the 21st century. Restor Ecol 21:297–304. doi:10.1111/rec.12012
Shea K, Possingham HP (2000) Optimal release strategies for biological control agents: an application of stochastic dynamic programming to population management. J Appl Ecol 37:77–86. doi:10.1046/j.1365-2664.2000.00467.x
Stang M, Klinkhamer PGL, Waser NM et al (2009) Size-specific interaction patterns and size matching in a plant–pollinator interaction web. Ann Bot 103:1459–1469. doi:10.1093/aob/mcp027
Strogatz SH (2001) Exploring complex networks. Nature 410:268–276. doi:10.1038/35065725
Suding KN, Hobbs RJ (2009) Threshold models in restoration and conservation: a developing framework. Trends Ecol Evol 24:271–279. doi:10.1016/j.tree.2008.11.012
Suding KN, Gross KL, Houseman GR (2004) Alternative states and positive feedbacks in restoration ecology. Trends Ecol Evol 19:46–53. doi:10.1016/j.tree.2003.10.005
Tenhumberg B, Tyre AJ, Shea K, Possingham HP (2004) Combinación de Poblaciones Silvestres y Cautivas para Maximizar la Persistencia de Especies: Estrategias de Translocación Óptima. Conserv Biol 18:1304–1314. doi:10.1111/j.1523-1739.2004.00246.x
Thakar J, Saadatpour-Moghaddam A, Harvill ET, Albert R (2009) Constraint-based network model of pathogen–immune system interactions. J R Soc Interface 6:599–612. doi:10.1098/rsif.2008.0363
Thébault E, Fontaine C (2010) Stability of ecological communities and the architecture of mutualistic and trophic networks. Science 329:853–856. doi:10.1126/science.1188321
Tylianakis JM, Laliberté E, Nielsen A, Bascompte J (2010) Conservation of species interaction networks. Biol Conserv 143:2270–2279. doi:10.1016/j.biocon.2009.12.004
Verberk WCEP, van der Velde G, Esselink H (2010) Explaining abundance-occupancy relationships in specialists and generalists: a case study on aquatic macroinvertebrates in standing waters. J Anim Ecol 79:589–601. doi:10.1111/j.1365-2656.2010.01660.x
Wang R-S, Saadatpour A, Albert R (2012) Boolean modeling in systems biology: an overview of methodology and applications. Phys Biol 9:055001. doi:10.1088/1478-3975/9/5/055001
Williams NM (2011) Restoration of nontarget species: bee communities and pollination function in riparian forests. Restor Ecol 19:450–459. doi:10.1111/j.1526-100X.2010.00707.x
Winfree R (2010) The conservation and restoration of wild bees. Ann N Y Acad Sci 1195:169–197. doi:10.1111/j.1749-6632.2010.05449.x
Winfree R, Williams NM, Dushoff J, Kremen C (2007) Native bees provide insurance against ongoing honey bee losses. Ecol Lett 10:1105–1113. doi:10.1111/j.1461-0248.2007.01110.x
Yoshikawa T, Isagi Y (2013) Determination of temperate bird–flower interactions as entangled mutualistic and antagonistic sub-networks: characterisation at the network and species levels. J Anim Ecol. doi:10.1111/1365-2656.12161
Acknowledgments
We are grateful to two referees for their insightful comments on this work. We acknowledge members of the Shea research lab for helpful discussions during the preparation of this research. This work was supported by NSF grant DEB-0815373 and an NSF REU to K.S., NSF grant PHY 1205840 to R.A., NSF grant DMS-1313115 to K.S. and R.A., and the Biology Department (Presbyterian College) to SY.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(PDF 253 kb)
Rights and permissions
About this article
Cite this article
LaBar, T., Campbell, C., Yang, S. et al. Restoration of plant–pollinator interaction networks via species translocation. Theor Ecol 7, 209–220 (2014). https://doi.org/10.1007/s12080-013-0211-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12080-013-0211-7