Abstract
Invasive plant species can have strong direct negative effects on native plants. Depending on the nature of interactions among competitors and consumers within a community, strong indirect interactions may either augment or offset direct effects. We used path analysis to estimate the relative importance of direct and indirect effects of Euphorbia esula, an unpalatable invasive plant, on Balsamorhiza sagittata, a native forb, through “shared defense” and by suppression of native competitors. Our results indicate that E. esula had strong direct negative effects on B. sagittata, but also that its net effect was reduced by 75% because of indirect positive effects. This reduction was because in equal parts of lessened competition from other native plants eliminated from E. esula stands and to lower levels of herbivory inside E. esula stands, apparently caused by indirect defense of B. sagittata by E. esula. To our knowledge, this is the first evidence that invaders may indirectly reduce herbivory on native plants, a phenomenon that may commonly occur with unpalatable invaders. Furthermore, our results highlight the potential complexity of interactions between native and invasive plants.
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Amsberry LK, Maron JL (2006) Effects of herbivore identity on plant fecundity. Plant Ecol 187:39–48
Atsatt PR, O’Dowd DJ (1976) Plant defense guilds. Science 193:24–29
Belcher JW, Wilson SD (1989) Leafy spurge and the species composition of a mixed-grass prairie. J Range Manag 42:172–175
Braithwaite RW, Lonsdale WM, Estbergs JA (1989) Alien vegetation and native biota in tropical Australia: the spread and impact of Mimosa pigra. Biol Conserv 48:189–201
Branson DH, Sword GA (2008) Grasshopper herbivory affects native plant diversity and abundance in a grassland dominated by the exotic grass Agropyron cristatum. Rest Ecol 17:89–96
Burell GC (1982) Winter diets of mule deer in relation to bitterbrush abundance. J Range Manag 35:505–510
Callaway RM (2007) Positive interactions and interdependence in plant communities. Springer, New York
Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Env 2:436–443
Callaway RM, Mahall BE, Wicks C, Pankey J, Zabinski C (2003) Soil fungi and the effects of an invasive forb on grasses: neighbor identity matters. Ecology 84:129–135
Cappuccino N, Arnason JT (2006) Novel chemistry of invasive exotic plants. Biol Lett 2:189–193
Cappuccino N, Carpenter D (2005) Invasive exotic plants suffer less herbivory than non-invasive exotic plants. Biol Lett 1:435–438
Cyr DR, Bewley JD (1989) Carbon and nitrogen reserves of leafy spurge (Euphorbia esula) roots as related to overwintering strategy. Physiol Plant 77:67–72
Dittberner PL, Olson MR (1983) The plant information network (PIN) data base: Colorado, Montana, North Dakota, Utah, and Wyoming. FWS/OBS-83/86. Washington, DC: US Department of the Interior, Fish and Wildlife Service
Feeny P (1976) Plant apparency and chemical defense. Recent Adv Phytochem 10:1–40
Grigulis KA, Sheppard W, Ash JE, Groves RH (2001) The comparative demography of the pasture weed Echium plantagineum between its native and invaded ranges. J App Ecol 38:281–290
Hambäck PA, Beckerman AP (2003) Herbivory and plant resource competition: a review of two interacting interactions. Oikos 101:26–37
Hambäck PA, Pettersson J, Ericson L (2003) Are associational refuges species-specific? Funct Ecol 17:87–93
Hierro JL, Callaway RM (2003) Allelopathy and exotic plant invasion. Plant Soil 256:29–39
Inderjit, Callaway RM, Vivanco JM (2007) Can plant biochemistry contribute to understanding of invasion ecology? Trends in Plant Sci 11:574–580
Jogesh T, Carpenter D, Cappuccino N (2008) Herbivory on invasive exotic plants and their non-invasive relatives. Biol Invasions 10:797–804
Joshi J, Vrieling K (2005) The enemy release and EICA hypothesis revisited: incorporating the fundamental difference between specialist and generalist herbivores. Ecol Lett 8:704–714
Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 410:651–652
Levine JM (1999) Indirect facilitation: evidence and predictions from a riparian community. Ecology 80:1762–1769
Levine JM, Vilà M, D’Antionio CM, Dukes JS, Grigulis K, Lavorel S (2002) Mechanisms underlying the impacts of exotic plant invasions. Proc Royal Soc Biol Sci 270:775–881
Lind EM, Parker JD (2010) Novel weapons testing: are invasive plants more chemically defended than native plants? PLoSONE. doi:10.1371/journal.pone.0010429
Maron JL, Marler M (2008) Field-based competitive impacts between invaders and natives at varying resource supply. J Ecol 96:1187–1197
Meiners SJ (2007) Apparent competition: an impact of exotic shrub invasion on tree regeneration. Biol Invasions 9:849–855
Memmott J, Simon SV, Paynter Q, Sheppard AW, Syrett P (2000) The invertebrate fauna on broom, Cystus scoparius, in two native and two exotic habitats. Acta Oecol 21:213–222
Miller TE (1987) Effects of emergence time on survival and growth in an early old-field community. Oecologia 72:272–278
Müller-Schärer H, Schaffner U, Steinger T (2004) Evolution in invasive plants: implications for biological control. TREE 19:418–422
Munoz AA, Cavieres LA (2008) The presence of a showy invasive plant disrupts pollinator service and reproductive output in native alpine species only at high densities. J Ecol 96:459–467
Orrock JL, Witter MS, Reichman OJ (2008) Apparent competition with an exotic plant reduces native plant establishment. Ecology 89:1168–1174
Parker JD, Burkepile DE, Hay ME (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311:1459–1461
Pearson DE, Callaway RM (2008) Herbicide reveals weed biocontrol insects reduce native plant recruitment through second-order apparent competition. Ecol App 18:1489–1500
Rees M, Brown VK (1992) Interactions between invertebrate herbivores and plant competition. J Ecol 80:353–360
Ridenour WM, Vivanco JM, Feng Y, Horiuchi J, Callaway RM (2008) No evidence for tradeoffs: Centaurea plants from America are better competitors and defenders than plants from the native range. Ecol Monogr 78:369–386
Saccone P, Pagés J, Girel J, Brun J, Michalet R (2010) Acer negundo invasion along a successional gradient: early direct facilitation by native pioneers and late indirect facilitation by conspecifics. New Phytol 187:831–842
Siemann E, Rogers WE (2003) Reduced resistance of invasive varieties of the alien tree Sapium sebiferum to a generalist herbivore. Oecologia 135:451–457
Tahvanainen JO, Root RB (1972) The influence of vegetational diversity of the population ecology of a specialized herbivore, Phyllotreta cruciferaea (Coleoptra: Chrysomelidae). Oecologia 10:321–346
Tallamy DW, Ballard M, D’Amico VD (2010) Can alien plants support generalist insect herbivores? Biol Invasions 12:2285–2292
Trammell MA, Butler JL (1995) Effects of exotic plants on native ungulate use of habitat. J Wildlife Manag 59:808–816
US Department of Agriculture, Forest Service (1988) Range plant handbook, 2nd edn. Dover, Mineola, NY
White EM, Wilson JC, Clarke AR (2006) Biotic indirect effects: a neglected concept in invasion biology. Divers Distrib 12:443–455
Wikeem BM, Pitt MD (1979) Interpreting diet preference of California bighorn sheep on native rangeland in south-central BC. Rangelands 1:200–202
Wikeem BM, Pitt MD (1991) Grazing effects and range trend assessment on California bighorn sheep range. J Range Manag 44:466–470
Acknowledgments
This work was partially funded by the Howard Hughes Medical Institute and the NSF Graduate Research Fellowship Program. The authors would also like to thank Bert Lindler and the Rocky Mountain Elk Foundation, Morgan Valliant and the City of Missoula Parks and Recreation Department, and Joy Sherry for use of their lands for our research. Ragan M. Callaway thanks the NSF for funding.
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Atwater, D.Z., Bauer, C.M. & Callaway, R.M. Indirect positive effects ameliorate strong negative effects of Euphorbia esula on a native plant. Plant Ecol 212, 1655–1662 (2011). https://doi.org/10.1007/s11258-011-9938-7
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DOI: https://doi.org/10.1007/s11258-011-9938-7