Abstract
Urbanization decreases the abundance of native species, which may enable exotics to experience enemy release in urban areas, enhancing their invasive capacity. The invasive autogamous orchid, Spathoglottis plicata, acquires some biotic resistance in Puerto Rico from a native orchid weevil specialist, Stethobaris polita. The distribution of S. polita along an urbanization gradient may affect the distribution of S. plicata and its future spread. To determine the effect of land cover on both species and the impact of S. polita on the spread of S. plicata, we modeled the distribution of the interaction between the two species and additionally assessed weevil abundance and the damage they do in different land cover types and localities. Land cover was the most important predictor of distribution for both species. S. plicata occurs in forests, pastures, and urban areas; however, S. polita is largely absent from urban areas, including urban forests, and along rivers within wet forests. This distribution likely reflects the dispersal ability of S. plicata, in addition to potential human intervention, and the inability of S. polita to penetrate or become established within the urban matrix. Thus, within the invasive range of S. plicata in Puerto Rico, geographical heterogeneity in acquired interactions is expected to result in higher seed production within areas of enemy release. The orchid is likely to spread more rapidly in urban forests, as well as along forest rivers, where S. polita is sparse.
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References
Abelleira Martínez OJ, Rodríguez MA, Rosario I, Soto N, López A, Lugo AE (2010) Structure and species composition of novel forests dominated by an introduced species in northcentral Puerto Rico. New For 39:1–18
Ackerman JD (2007) Invasive orchids: weeds we hate to love? Lankesteriana 7:19–21
Ackerman JD (2012) Orchidaceae. In: Acevedo P, Strong M (eds) Catalogue of seed plants of the West Indies. Smithsonian contributions to botany, vol 98. pp 622–667
Ackerman JD, Collaborators (2014) Orchid flora of the Greater Antilles. NY Bot Garden 109:1–625
Ackerman JD, Falcón W, Molinari J, Vega C, Espino I, Cuevas AA (2014) Biotic resistance and invasional meltdown: consequences of acquired interspecific interactions for an invasive orchid, Spathoglottis plicata in Puerto Rico. Biol Invasions 16:2435–2447. https://doi.org/10.1007/s10530-014-0676-3
Ackerman JD, Tremblay RL, Rojas Sandoval J, Hernández Figueroa E (2017) Biotic resistance in the tropics: patterns of plant invasions within an island. Biol Invasions 19:315–328. https://doi.org/10.1007/s10530-016-1281-4
Allendorf FW, Lundquist LL (2003) Introduction: population biology, evolution, and control of invasive species. Conserv Biol 17:24–30. https://doi.org/10.1046/j.1523-1739.2003.02365.x
Allison PD, SAS Institute (2012) Logistic regression using SAS: theory and application, 2nd edn. SAS Institute, Cary, North Carolina
Arnold TW (2010) Uninformative parameters and model selection using Akaike’s Information Criterion. J Wildl Manag 74:1175–1178. https://doi.org/10.2193/2009-367
Bayman P, Mosquera-Espinosa AT, Saladini-Aponte CM, Hurtado-Guevara NC, Viera-Ruiz NL (2016) Age-dependent mycorrhizal specificity in an invasive orchid, Oeceoclades maculata. Am J Bot 103:1880–1889
Bergman E, Ackerman JD, Thompson J, Zimmerman JK (2006) Land-use history affects the distribution of the saprophytic orchid Wullschlaegelia calcarata in Puerto Rico’s tabonuco forest. Biotropica 38:492–499. https://doi.org/10.1111/j.1744-7429.2006.00167.x
Blackburn TM, Pyšek P, Bacher S, Carlton JT, Duncan RP, Jarošik V, Wilson JRU, Richardson DM (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339. https://doi.org/10.1016/j.tree.2011.03.023
Burton ML, Samuelson LJ, Pan S (2005) Riparian woody plant diversity and forest structure along an urban-rural gradient. Urban Ecosyst 8:93–106. https://doi.org/10.1007/s11252-005-1421-6
Byers JE (2002) Impact of non-indigenous species on natives enhanced by anthropogenic alteration of selection regimes. Oikos 97:449–458. https://doi.org/10.1034/j.1600-0706.2002.970316.x
Crustinger GM, Collins MD, Fordyce JA, Gompert Z, Nice CC, Sanders NJ (2006) Plant genotypic diversity predicts community structure and governs an ecosystem process. Science 313:966–968. https://doi.org/10.1126/science.1128326
Daehler CC (1998) The taxonomic distribution of invasive angiosperm plants: ecological insights and comparison to agricultural weeds. Biol Conserv 84:167–180
Daehler CC (2003) Performance comparisons of co-occurring native and alien invasive plants: implications for conservation and restoration. Annu Rev Ecol Evol Syst 34:183–211. https://doi.org/10.1146/annurev.ecolsys.34.011802.132403
Damon A, Valle-More J (2008) Retrospective spatial analysis of the pollination of two miniature epiphytic orchids with different pollination strategies in a coffee plantation in Soconusco, Chiapas, Mexico. Bot J Linn Soc 158:448–459
Denslow JS, Space JC, Thomas PA (2009) Invasive exotic plants in the tropical Pacific islands: patterns of diversity. Biotropica 41:162–170
Denys C, Schmidt H (1998) Insect communities on experimental mugwort (Artemisia vulgaris L.) plots along an urban gradient. Oecologia 113:269–277. https://doi.org/10.1007/s004420050378
Dinno A (2015) Nonparametric pairwise comparisons in independent groups using Dunn’s test. Stata J 15:292–300
Ewel JJ, Whitmore TN (1973) The ecological life zones of Puerto Rico and the U.S. Virgin Islands. Forest service research paper ITF-18. Institute of Tropical Forestry, Forest Service, U.S. Department of Agriculture
Fagan WF, Lewis M, Neubert MG, Aumann C, Apple JL, Bishop JG (2005) When can herbivores slow or reverse the spread of an invading plant? A test case from Mount St. Helens. Am Nat 166:669–685. https://doi.org/10.2307/3491230
Falcón W, Ackerman JD, Tremblay RL (2017) Quantifying how acquired interactions with native and invasive insects influence population growth rates of a non-indigenous plant. Biol Invas 19:895–911. https://doi.org/10.1007/s10530-016-1318-8
Fekete R, Nagy T, Bódis J, Biró E, Löki V, Süveges K, Takács A, Tökölyi J, Molnár A (2017) Roadside verges as habitats for endangered lizard-orchids (Himantoglossum spp.): ecological traps or refuges? Sci Total Environ 607:1001–1008
Fick SE, Hijmans RJ (2017) Worldclim 2: new 1-km spatial resolution climate surfaces for global land areas. Int J Climatol 37:4302–4315. https://doi.org/10.1002/joc.5086
Fine PVA, Mesones I, Coley PD (2004) Herbivores promote habitat specialization by trees in Amazonian forests. Science 305:663–665. https://doi.org/10.1126/science.1098982
Global Compendium of Weeds (2011) Hawaii ecosystem risk project. http://www.hear.org/gcw/. Accessed 2018 June 3
Gomez-Gomez F, Rodriguez-Martinez J, Santiago M (2014) Hydrology of Puerto Rico and the outlying islands of Vieques, Culebra, and Mona. U.S. Department of the Interior & U.S. Geological Survey, Reston
Goosem S (2009) Invasive weeds in the wet tropics. In: Stork NE, Turton SM (eds) Living in a dynamic tropical forest landscape. Blackwell, Oxford, pp 307–321
Gould WA, Alarcon C, Fevold B, Jimenez ME, Martinuzzi S, Potts G, Quinones M, Mariano S, Ventosa E (2008) The Puerto Rico gap analysis project volume 1: land cover, vertebrate species, distributions, and land stewardship, vol 1. USDA Forest Service International Institute of Tropical Forestry, Río Piedras
Horvitz CC, Pascarella JB, McMann S, Freedman A, Hofstetter RH (1998) Functional roles of invasive non-indigenous plants in hurricane-affected subtropical hardwood forests. Ecol Appl 8:947–974. https://doi.org/10.2307/2640954
Huang D, Su Z, Zhang R, Koh LP (2010) Degree of urbanization influences the persistence of Dorytomus weevils (Coleoptera: Curculionoidae) in Beijing, China. Landsc Urban Plan 96(3):163–171. https://doi.org/10.1016/j.landurbplan.2010.03.004
Jersáková J, Kindlmann P, Střítieský M (2002) Population dynamics of Orchis morio in the Czedh Republic under human influence. In: Kindlmann P, Willems JH, Whigham DF (eds) Trends and fluctuations and underlying mechanisms in terrestrial orchid popoulations. Backhuys Publishers, Leiden, pp 209–224
Jolliffe K (2010) Epiphytic orchids of the Seychelles. Kapisen 10(10):6–8
Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170. https://doi.org/10.1016/s0169-5347(02)02499-0
Kennaway T, Helmer EJ (2007) The forest types and ages cleared for land development in Puerto Rico. GISci Remote Sens 44:356–382
Leong TM, Wee YC (2013) Observations of pollination in the pigeon orchid, Dendrobium crumenatum Swartz (Orchidaceae) in Singapore. Nat Singap 6:91–96
Lieurance D, Cipollini D (2012) Damage levels from arthropod herbivores on Lonicera maackii suggest enemy release in its introduced range. Biol Invas 14:863–873. https://doi.org/10.1007/s10530-011-0123-7
Light MHS, MacConaill M (2011) Potential impact of insect herbivores on orchid conservation. Eur J Environ Sci 1:115–124. https://doi.org/10.14712/23361964.2015.54
Liu C, Berry PM, Dawson TP, Pearson RG (2005) Selecting thresholds of occurrence in the prediction of species distributions. Ecography 28:385–393. https://doi.org/10.1111/j.0906-7590.2005.03957
Löki V, Tökölyi J, Süveges K, Lovas-Kiss Á, Hürkan K, Sramkó G, Molnár A (2015) The orchid flora of Turkish graveyards: a comprehensive field survey. Willdenowia 45:231–243
Louda SM (1982) Distribution ecology: variation in plant recruitment over a gradient in relation to insect seed predation. Ecol Monogr 52:25–41. https://doi.org/10.2307/2937343
Luer CA (1972) The native orchids of Florida. New York Botanical Garden, New York
McCormick M, Jacquemyn H (2013) What constrains the distribution of orchid populations? New Phytol 202:392–400. https://doi.org/10.1111/nph.12639
McIntyre NE (2000) Ecology of urban arthropods: a review and a call to action. Ann Entomol Soc Am 93:825–835. https://doi.org/10.1603/0013-8746(2000)093%5b0825:eouaar%5d2.0.co;2
McKinney ML (2002) Urbanization, biodiversity, and conservation. Bioscience 52:883–890. https://doi.org/10.1641/0006-3568(2002)052%5b0883:ubac%5d2.0.co;2
McKinney ML (2006) Urbanization as a major cause of biotic homogenization. Biol Conserv 127:247–260. https://doi.org/10.1016/j.biocon.2005.09.005
Murren CJ, Ellison AM (1998) Seed dispersal characteristics of Brassavola nodosa (Orchidaceae). Am J Bot 85:675–680
Niinemets Ü, Peñuelas J (2008) Gardening and urban landscaping: significant players in global change. Trends Plant Sci 13:60–65
O’Brien CW, Turnbow RH Jr. (2011) An annotated list of Curculionidae (Coleoptera) of Dominica (excluding Scolytinae and Platypodidae). Insecta Mundi 0179:1–31
Pemberton RW, Collins TM, Koptur S (2008) An Asian orchid, Eulophia graminea (Orchidaceae: Cymbidieae), naturalizes in Florida. Lankesteriana 8:5–14
Phillips RD, Peakall R, Hutchinson MF, Linde CC, Xu T, Dixon KW, Hopper SD (2014) Specialized ecological interactions and plant species rarity: the role of pollinators and mycorrhizal fungi across multiple spatial scales. Biol Conserv 169:285–295. https://doi.org/10.1016/j.biocon/2013.11.027
Phillips SJ, Dudik M, Schapire RE (2018) Maxent software for modeling species niches and distributions (Version 3.4.1). http://biodiversityinformatics.amnh.org/open_source/maxent/. Accessed 30 July 2018
Prakash N, Lee-Lee A (1973) Life history of a common Malaysian orchid Spathoglottis plicata. Phytomorphology 23:9–17
Puerto Rico GAP Analysis Project (2006) PRGAP landcover. USDA Forest Service, International Institute of Tropical Forestry, Río Piedras
Pyšek P, Richardson DM (2008) Traits associated with invasiveness in alien plants: where do we stand? In: Nentwig W (ed) Biological invasions, ecological studies, vol 193. Springer, Berlin, pp 97–125
Pyšek P, Varošik V, Hulme PE, Kühn I, Wild J, Arianoutsou M, Bacher S, Chiron F, Didžiulis Essl F, Genovesi P, Gherardi F, Hejda M, Kark S, Lambdon PW, Desprez-Loustau M-L, Nentwig W, Pergl J, Poboljšaj K, Rabitsch W, Roques A, Roy DB, Shirley S, Solarz W, Vilà Winter M (2010) Disentangling the role of environmental and human pressures on biological invasions across Europe. Proc Nat Acad Sci USA 107:12157–12162. https://doi.org/10.1073/pnas.1002314107
Recart W, Ackerman JD, Cuevas AA (2013) There goes the neighborhood: apparent competition between invasive and native orchids mediated by a specialist florivorous weevil. Biol Invasions 15:283–293. https://doi.org/10.1007/s10530-012-0283-0
Reichard SH, White P (2001) Horticulture as a pathway of invasive plant introductions in the United States. Bioscience 51:103–113
Rejmánek M, Pitcairn MJ (2002) When is eradication of exotic pest plants a realistic goal? In: Veitch CR, Clut MN (eds) Turning the tide: the eradication of invasive species. IUCN, Gland, pp 249–253
Richardson DM (2011) Invasion science. The roads travelled and the roads ahead. In: Richardson DM (ed) Fifty years of invasion ecology: the legacy of Charles Elton. Wiley-Blackwell, Oxford, pp 397–407
Rojas-Sandoval J, Acevedo-Rodríguez P (2015) Naturalization and invasion of alien plants in Puerto Rico and the Virgin Islands. Biol Invasions 17:149–163. https://doi.org/10.1007/s10530-014-0712-3
Rojas-Sandoval J, Tremblay RL, Acevedo-Rodríguez P, Díaz-Soltero H (2017) Invasive plant species of the West Indies: geographical, ecological, and floristic insights. Ecol Evol 7:4522–4533. https://doi.org/10.1002/ece3.2984
Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:170–176. https://doi.org/10.1016/s0169-5347(02)02495-3
Shefferson RP, Kull T, Kadri T (2008) Mycorrhizal interactions of orchids colonizing Estonian mine tailings hills. Am J Bot 95:156–164
Simberloff D, Martin J-L, Genovesi P, Maris V, Wardle DA, Aronson J, Courchamp F, Galil B, García-Berthou E, PascalM PP, Sousa R, Rabacchi E, Vilá M (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66
Su Z, Zhang R, Qiu J (2011) Decline in the diversity of willow trunk-dwelling weevils (Coleoptera: Curculionoidea) as a result of urban expansion in Beijing, China. J Insect Conserv 15:367–377. https://doi.org/10.1007/s10841-010-9310-6
Suarez AV, Holway DA, Case TJ (2001) Patterns of spread in biological invasions dominated by long-distance jump dispersal: insights from Argentine ants. Proc Natl Acad Sci 98:1095–1100. https://doi.org/10.1073/pnas.98.3.1095
Suárez JP, Eguigueren JS, Herrera P, Jost L (2016) Do mycorhizal fungi drive speciation in Teagueia (Orchidaceae) in the upper Pastaza watershed of Ecuador? Symbiosis 69:161–168. https://doi.org/10.1007/s13199-016-0399-6
Thompson S, Wright F (1995) Spathoglottis plicata (Orchidacceae): new to Dominica, another record from the Lesser Antilles. Caribb J Sci 31:148–149
Turner K, Lefler L, Freedman B (2005) Plant communities of selected urbanized areas of Halifax, Nova Scotia, Canada. Landsc Urban Plan 71(2–4):191–206. https://doi.org/10.1016/j.landurbplan.2004.03.003
Václavíik T, Meetemeyer RK (2012) Equilibrium or not? Modelling potential distribution of invasive species in different stages of invasion. Divers Distrib 18:73–83
Acknowledgements
We thank Wilfredo Falcón for assistance with Maxent and data collection; Raymond Tremblay for assistance with the GLM; Kai Griebenow for localities of urban populations; and Christine Folks for assistance in the field. Funding was provided by a grant from the National Science Foundation-Research Experience for Undergraduates program (DBI-1559679, A. Ramírez, PI).
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Soifer, L.G., Ackerman, J.D. Extremes of forest–urban gradient offer some refuge for alien orchid invasion. Biol Invasions 21, 2143–2157 (2019). https://doi.org/10.1007/s10530-019-01963-5
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DOI: https://doi.org/10.1007/s10530-019-01963-5