Abstract
Herbivores are attracted to young shoots and leaves because of their tender tissues. However, in extrafloral nectaried plants, young leaves also attract patrolling ants, which may chase or prey on herbivores. We examined this scenario in extrafloral nectaried shrubs of Banisteriopsis malifolia resprouting after fire, which promoted both the aseasonal production of leaves and the activity of extrafloral nectaries (EFNs). Results were compared between resprouting (burned) and unburned control plants. The aggressive ant species Camponotus crassus and the herbivorous thrips Pseudophilothrips obscuricornis were respectively rapidly attracted to resprouting plants because of the active EFNs and their less sclerophyllous leaves. The abundance of these insects was almost negligible in the control (unburned) shrubs. Ants failed to protect B. malifolia, as no thrips were preyed upon or injured by ants in resprouting plants. Consequently, on average, 37 % of leaves from resprouting shrubs had necrosis marks. Upon contact with ants, thrips released small liquid droplets from their abdomen, which rapidly displaced ants from the surroundings. This study shows that P. obscuricornis disrupted the facultative mutualism between C. crassus and B. malifolia, since ants received extrafloral nectar from plants, but were unable to deter herbivore thrips.
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References
Altmann J (1974) Observational study of behaviour: sampling methods. Behavior 49:221–267
Alves-Silva E (2011) Post fire resprouting of Banisteriopsis malifolia (Malpighiaceae) and the role of extrafloral nectaries on the associated ant fauna in a Brazilian savanna. Sociobioloy 58:327–339
Alves-Silva E, Del-Claro K (2010) Thrips in neotropics: what do we know so far? Trends Entomol 6:77–88
Alves-Silva E, Del-Claro K (2011) Ectoparasitism and phoresy in Thysanoptera: the case of Aulacothrips dictyotus (Heterothripidae) in the Neotropical savanna. J Nat Hist 45:393–405. doi:10.1080/00222933.2010.534189
Alves-Silva E, Del-Claro K (2013) Effect of post-fire resprouting on leaf fluctuating asymmetry, extrafloral nectar quality, and ant-plant-herbivore interactions. Naturwissenschaften 100:525–532. doi:10.1007/s00114-013-1048-z
Alves-Silva E, Barônio GJ, Torezan-Silingardi HM, Del-Claro K (2013) Foraging behavior of Brachygastra lecheguana (Hymenoptera: Vespidae) on Banisteriopsis malifolia (Malpighiaceae): extrafloral nectar consumption and herbivore predation in a tending ant system. Entomol Sci 16:162–169. doi:10.1111/ens.12004
Araújo APA, De Paula JDA, Carneiro MAA, Schoereder JH (2006) Effects of host plant architecture on colonization by galling insects. Austral Ecol 31:343–348. doi:10.1111/j.1442-9993.2006.01563.x
Bacelar EA, Correia CM, Moutinho-Pereira JM, Gonçalves BC, Lopes JI, Torres-Pereira JM (2004) Sclerophylly and leaf anatomical traits of five field-grown olive cultivars growing under drought conditions. Tree Physiol 24:233–239. doi:10.1093/treephys/24.2.233
Bakker FM, Sabelis MW (1989) How larvae of thrips-tabaci reduce the attack success of phytoseiid predators. Entomol Exp Appl 50:47–51. doi:10.1111/j.1570-7458.1989.tb02313.x
Basset Y (1991) Influence of leaf traits on the spatial distribution of insect herbivores associated with an overstorey rainforest tree. Oecologia 87:388–393. doi:10.1007/BF00634596
Blum MS, Footit R, Fales HM (1992) Defensive chemistry and function of the anal exudate of the thrips Haplothrips leucanthemi. Comp Biochem Phys C 102:209–211. doi:10.1016/0742-8413(92)90066-G
Carter PE, Rypstra AL (1995) Top–down effects in soybean agroecosystems: spider density affects herbivore damage. Oikos 72:433–439
Cavalleri A, Kaminski LA, Mendonça MS Jr (2010) Ectoparasitism in Aulacothrips (Thysanoptera: Heterothripidae) revisited: host diversity on honeydew-producing hemiptera and description of a new species. Zool Anz 249:209–221. doi:10.1016/j.jcz.2010.09.002
Chen Y, Williams KA (2006) Quantifying western flower thrips (Frankliniella occidentalis Pergande) Thysanoptera:Thripidae) damage on Ivy Geranium (Pelargonium peltatum (L.) L’Her ex Ait.) (Geraniaceae Juss.) with Adobe® Photoshop™ and Scion® Image Software. J Kans. Entomol Soc 79:83–87. doi:10.1111/j.1439-0418.1993.tb00422.x
Cornelissen T, Fernandes GW, Vasconcelos-Neto J (2008) Size does matter: variation in herbivory between and within plants and the plant vigor hypothesis. Oikos 117:1121–1130. doi:10.1111/j.0030-1299.2008.16588.x
Costa FV, Fagundes M, Neves FS (2010) Arquitetura da planta e diversidade de galhas associadas à Copaifera langsdorffii (Fabaceae). Ecol Austral 20:9–17
Cuda JP, Gillmore JL, Medal JC, Pedrosa-Macedo JH (2008) Mass rearing of Pseudophilothrips ichini (Thysanoptera: Phlaeothripidae), an approved biological control agent for Brazilian peppertree, Schinus terebinthifolius (Sapindales: Anacardiaceae). Fla Entomol 91:338–340. doi:10.1653/0015-4040(2008)91[338:MROPIT]2.0.CO;2
Del-Claro K, Berto V, Réu W (1996) Effect of herbivore deterrence by ants on the fruit set of an extrafloral nectary plant, Qualea multiflora (Vochysiaceae). J Trop Ecol 12:887–892. doi:10.1017/S0266467400010142
Del-Claro K, Marullo R, Mound LA (1997) A new Brazilian species of Heterothrips (Insecta: Thysanoptera) interacting with ants in Peixotoa tomentosa flowers (Malpighiaceae). J Nat Hist 31:1307–1312. doi:10.1080/00222939700770731
Freitas AVL, Oliveira PS (1996) Ants as selective agents on herbivore biology: effects on the behaviour of a non-myrmecophilous butterfly. J Anim Ecol 65:205–210
Gaume L, Shenoy M, Zacharias M, Borges RM (2006) Co-existence of ants and an arboreal earthworm in a myrmecophyte of the Indian Western Ghats: anti-predation effect of the earthworm mucus. J Trop Ecol 22:341–344. doi:10.1017/s0266467405003111
Howard DF, Blum MS, Fales HM (1983) Defense in thrips: forbidding fruitiness of a lactone. Science 220:335–336. doi:10.1126/science.220.4594.335
Hunter MD, Price PW (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top–down forces in natural communities. Ecology 73:724–732
Jolliffe IT (2002) Principal component analysis, 2nd edn. Springer, New York
Jones ME, Paine TD, Fenn ME (2008) The effect of nitrogen additions on oak foliage and herbivore communities at sites with high and low atmospheric pollution. Environ Pollut 151:434–442. doi:10.1016/j.envpol.2007.04.020
Kawai A (1990) Life cycle and population dynamics of Thrips palmi Karny. Jarq-Jpn Agr Res 23:282–288
Kersch MF, Fonseca CR (2005) Abiotic factors and the conditional outcome of an ant-plant mutualism. Ecology 86:2117–2126. doi:10.1890/04-1916
Lawton JH (1983) Plant architecture and the diversity of phytophagous insects. Annu Rev Entomol 28:23–29. doi:10.1146/annurev.en.28.010183.000323
Leather SR (1986) Insect species richness of the British Rosaceae: the importance of host range, plant architecture, age of establishment, taxonomic isolation and species-area relationships. J Anim Ecol 55:841–860
Lill JT, Marquis RJ (2003) Ecosystem engineering by caterpillars increases insect herbivore diversity on white oak. Ecology 84:682–690. doi:10.1890/0012-9658(2003)084[0682:EEBCII]2.0.CO;2
Macel M, Bruinsma M, Dijkstra SM, Ooijendijk T, Niemeyer HM, Klinkhamer PGL (2005) Differences in effects of pyrrolizidine alkaloids on five generalist insect herbivore species. J Chem Ecol 31:1493–1508. doi:10.1007/s10886-005-5793-0
Magalhães S, van Rijn P, Montserrat M, Pallini A, Sabelis M (2007) Population dynamics of thrips prey and their mite predators in a refuge. Oecologia 150:557–568. doi:10.1007/s00442-006-0548-3
Manrique V, Cuda JP, Overholt WA, Williams DA, Wheeler GS (2008) Effect of host-plant genotypes on the performance of three candidate biological control agents of Schinus terebinthifolius in Florida. Biol Control 47:167–171. doi:10.1016/j.biocontrol.2008.07.005
Marquis RJ, Diniz IR, Morais HC (2001) Patterns and correlates of interspecific variation in foliar insect herbivory and pathogen attack in Brazilian cerrado. J Trop Ecol 17:127–148. doi:10.1017/S0266467401001080
Medeiros MB, Miranda HS (2008) Post-fire resprouting and mortality in cerrado woody plant species over a three-year period. Edinb J Bot 65:53–68. doi:10.1017/S0960428608004708
Milne M, Walter GH (2000) Feeding and breeding across host plants within a locality by the widespread thrips Frankliniella schultzei, and the invasive potential of polyphagous herbivores. Divers Distrib 6:243–257. doi:10.1046/j.1472-4642.2000.00089.x
Mody K, Linsenmair KE (2004) Plant-attracted ants affect arthropod community structure but not necessarily herbivory. Ecol Entomol 29:217–225. doi:10.1111/j.1365-2311.2004.0588.x
Moog U, Fiala B, Federle W, Maschwitz U (2002) Thrips pollination of the dioecious ant plant Macaranga hullettii (Euphorbiaceae) in Southeast Asia. Am J Bot 89:50–59. doi:10.3732/ajb.89.1.50
Moreno JM, Oechel WC (1991) Fire intensity and herbivory effects on postfire resprouting of Adenostoma fasciculatum in southern California chaparral. Oecologia 85:429–433. doi:10.1007/BF00320621
Morse JG, Hoddle MS (2006) Invasion biology of thrips. Annu Rev Entomol 51:67–89. doi:10.1146/annurev.ento.51.110104.151044
Mound LA, Terry I (2001) Thrips pollination of the central Australian cycad, Macrozamia macdonnellii (Cycadales). Int J Plant Sci 162:147–154. doi:10.1086/317899
Nascimento EA, Del-Claro K (2010) Ant visitation to extrafloral nectaries decreases herbivory and increases fruit set in Chamaecrista debilis (Fabaceae) in a Neotropical savanna Flora. Flora Morphol Distrib Funct Ecol Plants 205:754–756. doi:10.1016/j.flora.2009.12.040
Oliveira PS, Freitas AVL (2004) Ant-plant-herbivore interactions in the neotropical cerrado savanna. Naturwissenschaften 91:557–570. doi:10.1007/s00114-004-0585-x
Paine TD (1992) Cuban laurel thrips (Thysanoptera: Phlaeothripidae) biology in Southern California: Seasonal abundance, temperature dependent development, leaf suitability, and predation. Ann Entomol Soc Am 85:164–172
Peng RK, Christian K (2004) The weaver ant, Oecophylla smaragdina (Hymenoptera: Formicidae), an effective biological control agent of the red-banded thrips, Selenothrips rubrocinctus (Thysanoptera: Thripidae) in mango crops in the Northern Territory of Australia. Int J Pest Manag 50:107–114. doi:10.1080/09670870410001658125
Power ME (1992) Top–down and bottom-up forces in food webs: do plants have primacy. Ecology 73:733–746. doi:10.2307/1940153
Read J, Sanson GD, Garine-Wichatitsky M, Jaffré T (2006) Sclerophylly in two contrasting tropical environments: low nutrients vs. low rainfall. Am J Bot 93:1601–1614. doi:10.3732/ajb.93.11.1601
Reich PB, Abrams MD, Ellsworth DS, Kruger EL, Tabone TJ (1990) Fire affects ecophysiology and community dynamics of central Wisconsin oak forest regeneration. Ecology 71:2179–2190. doi:10.2307/1938631
Rieske LK, Housman HH, Arthur MA (2002) Effects of prescribed fire on canopy foliar chemistry and suitability for an insect herbivore. Forest Ecol Manag 160:177–187. doi:10.1016/S0378-1127(01)00444-3
Santos J, Silveira F, Fernandes G (2008) Long term oviposition preference and larval performance of Schizomyia macrocapillata (Diptera: Cecidomyiidae) on larger shoots of its host plant Bauhinia brevipes (Fabaceae). Evol Ecol 22:123–137. doi:10.1007/s10682-007-9162-z
Schmidt IB, Sampaio AB, Borghetti F (2005) Efeitos da época de queima sobre a reprodução sexuada e estrutura populacional de Heteropterys pteropetala (Adr. Juss.), Malpighiaceae, em áreas de Cerrado sensu stricto submetidas a queimas bienais. Acta Bot Bras 19:927–934
Seyffarth JAS, Calouro AM, Price PW (1996) Leaf rollers in Ouratea hexasperma (Ochnaceae): fire effect and the plant vigor hypothesis. Rev Bras Biol 56:135–137
Silva IA, Valenti MW, Silva-Matos DM (2009) Fire effects on the population structure of Zanthoxylum rhoifolium Lam (Rutaceae) in a Brazilian savanna. Braz J Biol 69:813–818. doi:10.1590/S1519-69842009000400008
Van Mele P (2008) A historical review of research on the weaver ant Oecophylla in biological control. Agric For Entomol 10:13–22. doi:10.1111/j.1461-9563.2007.00350.x
Varanda EM, Pais MP (2006) Insect folivory in Didymopanax vinosum (Apiaceae) in a vegetation mosaic of Brazilian Cerrado. Braz J Biol 66:671–680. doi:10.1590/S1519-69842006000400011
Vieira EM, Andrade I, Price PW (1996) Fire effects on a Palicourea rigida (Rubiaceae) gall midge: a test of the plant vigor hypothesis. Biotropica 28:210–217
Wcislo WT, Schatz B (2003) Predator recognition and evasive behavior by sweat bees, Lasioglossum umbripenne (Hymenoptera: Halictidae), in response to predation by ants, Ectatomma ruidum (Hymenoptera: Formicidae). Behav Ecol Sociobiol 53:182–189. doi:10.1007/s00265-002-0564-1
Acknowledgments
The authors would like to thank A. Bächtold, P.K.M. Mendonça, L. A. Kaminski and D. Lange for suggestions on early versions of the manuscript and the staff of the Clube de Caça e Pesca Itororó de Uberlândia, where the fieldwork was carried out. We are also grateful to CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior), CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) and Fapemig (Fundação de Amparo à Pesquisa do Estado de Minas Gerais) for financial support.
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Alves-Silva, E., Del-Claro, K. Fire triggers the activity of extrafloral nectaries, but ants fail to protect the plant against herbivores in a neotropical savanna. Arthropod-Plant Interactions 8, 233–240 (2014). https://doi.org/10.1007/s11829-014-9301-8
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DOI: https://doi.org/10.1007/s11829-014-9301-8