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Experimental test of biotic resistance to an invasive herbivore provided by potential plant mutualists

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Abstract

Understanding the influence of resident species on the success of invaders is a core objective in the study and management of biological invasions. We asked whether facultative food-for-protection mutualism between resident, nectar-feeding ants and extrafloral nectar-bearing plants confers biotic resistance to invasion by a specialist herbivore. Our research focused on the South American cactus-feeding moth Cactoblastis cactorum Berg (Lepidopetra: Pyralidae) in the panhandle region of Florida. This species has been widely and intentionally redistributed as a biological control agent against weedy cacti (Opuntia spp.) but arrived unintentionally in the southeast US, where it attacks native, non-target cacti and is considered a noxious invader. The acquired host-plants of C. cactorum in Florida secrete extrafloral nectar, especially on young, vegetative structures, and this attracts ants. We conducted ant-exclusion experiments over 2 years (2008 and 2009) at two sites using potted plants of two vulnerable host species (O. stricta and O. ficus-indica) to evaluate the influence of cactus-visiting ants (total of eight species) at multiple points in the moth life cycle (oviposition, egg survival, and larval survival). We found that the presence of ants often increased the mortality of lab-reared C. cactorum eggsticks (stacks of cohered eggs) and larvae that we introduced onto plants in the field, although these effects were variable across sites, years, host-plant species, ant species, and/or between old and young plant structures. In contrast to these “staged” encounters, we found that ants had little influence on the survival of cactus moths that occurred naturally at our field sites, or on moth damage and plant growth. In total, our experimental results suggest that the influence of cactus-visiting ants on C. cactorum invasion dynamics is weak and highly variable.

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References

  • Baker AJ, Stiling P (2009) Comparing the effects of the exotic cactus-feeding moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae) and the native cactus-feeding moth, Melitara prodenialis (Walker) (Lepidoptera: Pyralidae) on two species of Florida Opuntia. Biol Invasions 11:619–624

    Article  Google Scholar 

  • Barton AM (1986) Spatial variation in the effects of ants on an extrafloral nectary plant. Ecology 62:495–504

    Article  Google Scholar 

  • Bentley BL (1977) Extrafloral nectaries and protection by pugnacious bodyguards. Annu Rev Ecol Syst 8:407–428

    Article  CAS  Google Scholar 

  • Bronstein JL (1998) The contribution of ant-plant protection studies to our understanding of mutualism. Biotropica 30:150–161

    Article  Google Scholar 

  • Center TD, Frank JH, Dray FA (1995) Biological invasions: stemming the tide in Florida. Fla Entomol 78:45–55

    Article  Google Scholar 

  • Chamberlain SA, Holland JN (2008) Density-mediated context-dependent consumer-resource interactions between ants and extrafloral nectar plants. Ecology 89:1364–1374

    Article  PubMed  Google Scholar 

  • Chamberlain SA, Holland JN (2009) Quantitative synthesis of context dependency in ant-plant mutualisms. Ecology 90:2384–2392

    Article  PubMed  Google Scholar 

  • de la Fuente MA, Marquis RJ (1999) The role of ant-tended extrafloral nectaries in the protection and benefit of a Neotropical rainforest tree. Oecologia 118:192–202

    Article  Google Scholar 

  • Di Giusto B, Anstett M, Dounias E, McKey DB (2001) Variation in the effectiveness of biotic defence: the case of opportunistic ant-plant protection mutualism. Oecologia (Berlin) 129:367–375

    Google Scholar 

  • Elton CS (1958) The ecology of invasions by animals and plants. Methuen, London

    Google Scholar 

  • Frederickson ME (2005) Ant species confer different partner benefits on two neotropical myrmecophytes. Oecologia 143:387–395

    Article  PubMed  Google Scholar 

  • Griffith MP (2004) The origins of an important cactus crop, Opuntia ficus-indica (Cactaceae): new molecular evidence. Am J Bot 91:1915–1921

    Article  Google Scholar 

  • Habeck DH, Bennett FD (1990) Cactoblastis cactorum Berg (Lepidoptera: Pyralidae), a phycitine new to Florida. Florida Department of Agriculture and Consumer Services, Division of Plant Industries, Florida

    Google Scholar 

  • Heil M, Fiala BBM, Linsenmair KE (2000) Temporal, spatial and biotic variations in extrafloral nectar secretion by Macaranga tanarius. Funct Ecol 14:749–757

    Article  Google Scholar 

  • Hight SD, Carpenter JE (2009) Flight phenology of male Cactoblastis cactorum (Lepidoptera: Pyralidae) at different lattitudes in the southeastern United States. Fla Entomol 92:208–216

    Article  Google Scholar 

  • Hight SD, Carpenter JE, Bloem KA, Bloem S, Pemberton RW, Stiling P (2002) Expanding geographic range of Cactoblastis cactorum (Lepidoptera: Pyralidae) in North America. Fla Entomol 85:527–529

    Article  Google Scholar 

  • Holway DA, Lach L, Suarez AV, Tsutsui ND, Case TJ (2002) The causes and consequences of ant invasions. Annu Rev Ecol Syst 33:181–233

    Article  Google Scholar 

  • Inouye DW, Taylor OR Jr (1979) A temperate region ant-plant-seed predator system: consequences of extra floral nectar secretion by Helianthella quiquenervis. Ecology 60:1–7

    Article  Google Scholar 

  • Johnson DM, Stiling P (1996) Host specificity of Cactoblastis cactorum (Lepidoptera: Pyralidae), an exotic Opuntia-feeding moth, in Florida. Environ Entomol 25:743–748

    Google Scholar 

  • Johnson DM, Stiling PD (1998) Distribution and dispersal of Cactoblastis cactorum (Lepidoptera: Pyralidae), an exotic Opuntia-feeding moth, in Florida. Fla Entomol 81:12–22

    Article  Google Scholar 

  • Legaspi JC, Legaspi JBC (2007) Life table analysis for Cactoblastis cactorum immatures and female adults under five constant temperatures: implications for pest management. Ann Entomol Soc Am 100:497–505

    Article  Google Scholar 

  • Legaspi JC, Baez I, Legaspi JBC (2008) Phenology of the blue cactus moth, Melitara prodenialis (Lepidopera: Pyralidae). Subtropical Plant Sci 60:66–68

    Google Scholar 

  • Legaspi JC, Baez I, Legaspi JBC (2009a) Reproduction, longevity, and survival of Cactoblastis cactorum (Lepidoptera: Pyradliae). Ann Entomol Soc Am 102:445–449

    Article  Google Scholar 

  • Legaspi JC, Baez I, Legaspi JBC (2009b) Phenology and egg production of the cactus moth (Lepidoptera: Pyralidae): comparison of field census data and life stage development in the field. J Entomol Sci 44:341–352

    Google Scholar 

  • Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989

    Article  Google Scholar 

  • MacGowan JA, Hill JG, Deyrup MA (2007) Brachymyrmex paragonicus (Hymenoptera: Formicidae), an emerging pest species in the southeastern United States. Fla Entomol 90:457–464

    Article  Google Scholar 

  • Mahr DL (2001) Cactoblastis cactorum (Lepidoptera: Pyralidae) in North America: a workshop of assessment and planning. Fla Entomol 84:465–473

    Article  Google Scholar 

  • Maron JL, Vila M (2001) When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95:361–373

    Article  Google Scholar 

  • Matthews CR, Brown MW, Bottrell DG (2007) Leaf extrafloral nectaries enhance biological control of a key economic pest, Grapholita molesta (Lepidoptera: Tortricidae), in Peach (Rosales: Rosaceae). Environ Entomol 36:383–389

    Article  Google Scholar 

  • McCullough DG, Work TT, Cavey JF, Liebhold AM, Marshall D (2006) Interceptions of nonindigenous plant pests at US ports of entry and border crossing over a 17-year period. Biol Invasions 8:611–630

    Article  Google Scholar 

  • Miller TEX (2007) Does having multiple partners weaken the benefits of facultative mutualism? A test with cacti and cactus-tending ants. Oikos 116:500–512

    Article  Google Scholar 

  • Mody K, Linsenmair KE (2004) Plant-attracted ants affect arthropod community structure but not necessarily herbivory. Ecol Entomol 29:217–225

    Article  Google Scholar 

  • Ness JH, Bronstein JL (2004) The effects of invasive ants on prospective mutualists. Biol Invasions 6:445–461

    Article  Google Scholar 

  • Ness JH, Morris WF, Bronstein JL (2006) Integrating quality and quantity of mutualistic service to contrast ant species protecting Ferocactus wislizeni. Ecology 87:912–921

    Article  CAS  PubMed  Google Scholar 

  • Oliveira PS, Rico-Gray V, Diez-Castelazo C, Castillo-Guevara C (1999) Interactions between ants, extrafloral nectaries, and insect herbivores in Neotropical sand dunes: herbivore deterrence by visiting ants increases fruit set in Opuntia stricta (Cactaceae). Funct Ecol 13:623–631

    Article  Google Scholar 

  • Palmer TM, Brody AK (2007) Mutualism as reciprocal exploitation: African plant-ants defend foliar but not reproductive structures. Ecology 88:3004–3011

    Article  PubMed  Google Scholar 

  • Pettey FW (1948) The biological control of prickly pear in South Africa. Department of Agriculture of the Union of South Africa

  • Pickett CH, Clark WD (1979) The function of extrafloral nectaries in Opuntia acanthocarpa (Cactaceae). Am J Bot 66:618–625

    Article  CAS  Google Scholar 

  • Rashbrook VK, Compton SG, Lawton JH (1992) Anti-herbivore interactions: reasons for the absence of benefits to a fern with foliar nectaries. Ecology 73:2167–2174

    Article  Google Scholar 

  • Rico-Gray V, Oliveira PS (2007) The ecology and evolution of ant-plant interactions. University of Chicago Press, Chicago

    Google Scholar 

  • Robbins M, Miller TEX (2009) Patterns of ant activity on Opuntia stricta (Cactaceae), a native host-plant of the invasive cactus moth, Cactoblastis cactorum (Lepidoptera: Pyralidae). Fla Entomol 92:391–393

    Article  Google Scholar 

  • Robertson HG (1984) Egg predation by ants as a partial explanation of the difference in performance of Cactoblastis cactorum on cactus weeds in South Africa and Australia. In: Delfosse ES (ed) Proc. VI Symp. Biol. Contr. Weeds, Vancouver, pp 83–88

  • Robertson HG (1988) Spatial and temporal patterns of predation by ants on eggs of Cactoblastis cactorum. Ecol Entomol 13:207–214

    Article  Google Scholar 

  • Rosumek FB, Silveira FAO, Neves FdS, Barbosa NPDU, Diniz L, Oki Y, Pezzini F, Fernandes GW, Cornelissen T (2009) Ants on plants: a meta-analysis of the role of ants as plant biotic defenses. Oecologia

  • Rudgers JA, Strauss SY (2004) A selection mosaic in the facultative mutualism between ants and wild cotton. Proc R Soc Lond Ser B 271:2481–2488

    Article  Google Scholar 

  • Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1:21–32

    Article  Google Scholar 

  • Simonson SE, Stohlgren TJ, Tyler L, Gregg WP, Muir R, Garrett LJ (2005) Preliminary assessment of the potential impacts and risks of the invasive cactus moth, Cactoblastis cactorum Berg, in the US and Mexico. International Atomic Energy Agency, Vienna

    Google Scholar 

  • Stiling P, Moon D, Gordon D (2004) Endangered cactus restoration: mitigating the non-target effects of a biological control agent (Cactoblastis cactorum) in Florida. Restor Ecol 12:605–610

    Article  Google Scholar 

  • Zimmerman HG, Moran VC, Hoffmann JH (2001) The renowned cactus moth, Cactoblastis cactorum (Lepidoptera: Pyralidae): its natural history and threat to native Opuntia floras in Mexico and the United States of America. Fla Entomol 84:543–551

    Article  Google Scholar 

  • Zimmerman HG, Bloem S, Klein H (2004) Biology, history, threat, surveillance and control of the cactus moth, Cactoblastis cactorum. Joint FAO/IAEA Programme of Nuclear Techniques in Food and Agriculture, IAEA, Vienna

    Google Scholar 

Download references

Acknowledgments

We acknowledge the valuable field and laboratory assistance provided by Elizabeth Aninakwa, Ignacio Baez, Keith Marshall, Jr., Neil Miller, Meredith Robbins, and Maggie Simon. Jes Hines, Tomomi Suwa, and Amy Savage provided helpful feedback on the manuscript. This research was supported by a grant from the US Department of Agriculture (CSREES-2007-02270) and a Rice University Huxley Fellowship to T.E.X.M.

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Correspondence to Tom E. X. Miller.

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Miller, T.E.X., Legaspi, J.C. & Legaspi, B. Experimental test of biotic resistance to an invasive herbivore provided by potential plant mutualists. Biol Invasions 12, 3563–3577 (2010). https://doi.org/10.1007/s10530-010-9751-6

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