Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-18T20:22:02.004Z Has data issue: false hasContentIssue false
  • English
  • Français

Field distribution patterns of pests are asymmetrically affected by the presence of other herbivores

Published online by Cambridge University Press:  07 April 2020

A. A. Paz Neto Open the ORCID record for A. A. Paz Neto [Opens in a new window] ,
J. W. S. Melo ,
D. B. Lima ,
M. G. C. Gondim Junior  and
A. Janssen
A. A. Paz Neto*
Affiliation:
Departamento de Agronomia – Entomologia, Universidade Federal Rural de Pernambuco, Av. Dom Manoel de Medeiros s/n, Dois Irmãos, 52171-900 Recife, PE, Brazil
J. W. S. Melo
Affiliation:
Departamento de Fitotecnia, Universidade Federal do Ceará, Fortaleza, CE, Brazil
D. B. Lima
Affiliation:
Departamento de Zoologia, Universidade Federal de Pernambuco, Recife, Pernambuco, Brazil
M. G. C. Gondim Junior
Affiliation:
Departamento de Agronomia – Entomologia, Universidade Federal Rural de Pernambuco, Av. Dom Manoel de Medeiros s/n, Dois Irmãos, 52171-900 Recife, PE, Brazil
A. Janssen
Affiliation:
Evolutionary and Population Biology, IBED, University of Amsterdam, Science Park 904, 1098 XH Amsterdam, The Netherlands
*
Author for correspondence: A. A. Paz Neto, Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Because plant phenotypes can change in response to attacks by herbivores in highly variable ways, the distribution of herbivores depends on the occurrence of other herbivore species on the same plant. We carried out a field study to evaluate the co-occurrence of three coconut pests, the mites Aceria guerreronis (Acari: Eriophyidae), Steneotarsonemus concavuscutum (Acari: Tarsonemidae) and the moth Atheloca bondari (Lepidoptera: Pyralidae). The eriophyid mite Ac. guerreronis is the most important coconut pest around the world, whereas S. concavuscutum and At. bondari are economically important only in some areas along the Brazilian coast. A previous study suggested that the necrosis caused by Ac. guerreronis facilitates the infestation of At. bondari larvae. Because all three species infest the area under the perianths on coconuts and S. concavuscutum also causes necrosis that could facilitate At. bondari, we evaluated the co-occurrence of all three species. We found that the occurrence of At. bondari was positively associated with Ac. guerreronis, but negatively associated with S. concavuscutum. In addition, the two mite species showed negative co-occurrence. Atheloca bondari was found on nuts of all ages, but more on nuts that had fallen than on those on the trees, suggesting that nuts infested by At. bondari tend to fall more frequently. We discuss the status of At. bondari as a pest and discuss experiments to test the causes of these co-occurrence patterns.

Keywords

Cocos nuciferafacilitative occurrenceindirect interactionmite–insect–plant associationplant-trait induced by herbivory
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 110 , Issue 5 , October 2020 , pp. 611 - 619
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahuja, SC, Ahuja, S and Ahuja, U (2014) Coconut-history, uses, and folklore. Asian Agri-History 18, 221–248.Google Scholar
Ali, JG and Agrawal, AA (2014) Asymmetry of plant-mediated interactions between specialist aphids and caterpillars on two milkweeds. Functional Ecology 28, 1404–1412.CrossRefGoogle Scholar
Allesina, S, Grilli, J, Barabás, G, Tang, S, Aljadeff, J and Maritan, A (2015) Predicting the stability of large structured food webs. Nature Communications 6, 1–6.CrossRefGoogle ScholarPubMed
Anderson, KE, Inouye, BD and Underwood, N (2009) Modeling herbivore competition mediated by inducible changes in plant quality. Oikos 118, 1633–1646.CrossRefGoogle Scholar
Beevi, SN, Mohan, P, Paul, A and Mathew, B (2006) Germination and seedling characters in coconut (Cocos nucifera L.) as affected by eriophyid mite (Aceria guerreronis Keifer) infestation. Journal of Tropical Agriculture 44, 76–78.Google Scholar
Benkman, CW (2013) Biotic interaction strength and the intensity of selection. Ecology Letters 16, 1054–1060.CrossRefGoogle ScholarPubMed
Bento, JMS, Nava, DE, Chagas, MCM and Costa, AH (2006) Biology and mating behavior of the coconut moth Atheloca subrufella (Lep.: Phycitidae). Florida Entomologist 89, 199–203.CrossRefGoogle Scholar
Bertness, MD and Callaway, R (1994) Positive interactions in communities. Trends in Ecology & Evolution 5347, 90087–6.Google Scholar
Bondar, G (1940) Insetos nocivos e moléstias do coqueiro (Cocos nucifera) no Brasil. Bahia, Tipographía Naval, 160p.Google Scholar
Bukovinszky, T, van Veen, FJF, Jongema, Y and Dicke, M (2008) Supporting online material for: direct and indirect effects of resource quality on food web structure. Science (New York, N.Y.) 319, 804.CrossRefGoogle Scholar
Capitán, JA, Cuenda, S and Alonso, D (2015) How similar can co-occurring species be in the presence of competition and ecological drift? Journal of the Royal Society Interface 12, 20150604.CrossRefGoogle ScholarPubMed
Chan, E and Elevitch, CR (2006) Cocos nucifera (coconut): species profiles for pacific island agroforestry. In Elevitch, CR (ed.), Hōlualoa: Permanent Agriculture Resources, pp. 277–302.Google Scholar
Cock, MJW and Burris, DH (2013) Neotropical palm-inflorescence feeding moths (Lepidoptera: Batrachedridae, Blastobasidae, Cosmopterigidae, Gelechiidae, Pyralidae, Tineidae): a review of the literature and new records from Trinidad, West Indies. Journal of Research on the Lepidoptera 46, 1–21.Google Scholar
Cock, MJW, Gallego, CN and Godfray, HCJ (1985) Biological control of Tirathaba rufivena in the Philippines. In Ferrar, P and Stechmann, DH (eds), Biological Control in the South Pacific. Kingdom of Tonga, Report on an International Workshop held at Government Experimental Farm, Vaini, pp. 17–25.Google Scholar
Cornelissen, T, Cintra, F and Santos, JC (2016) Shelter-building insects and their role as ecosystem engineers. Neotropical Entomology 45, 1–12.CrossRefGoogle ScholarPubMed
Crawley, MJ (2013) The R Book. Chichester, UK: John Wiley & Sons.Google Scholar
Dicke, M, van Loon, JJA and Soler, R (2009) Chemical complexity of volatiles from plants induced by multiple attack. Nature Chemical Biology 5, 317–324.CrossRefGoogle ScholarPubMed
Eubanks, MD and Finke, DL (2014) Interaction webs in agroecosystems: beyond who eats whom. Current Opinion in Insect Science 2, 1–6.CrossRefGoogle ScholarPubMed
Fernando, LCP and Aratchige, NS (2010) Status of coconut mite Aceria guerreronis and biological control research in Sri Lanka. In Sabelis, M and Bruin, J (eds), Trends in Acarology. Dordrecht: Springer, pp. 419–423.CrossRefGoogle Scholar
Ferreira, JMS, Araújo, RPC and Sarro, FB (2002) Insetos e ácaros. In Ferreira, JMS (ed.), Coco: Fitossanidade. Aracaju: Embrapa Tabuleiros Costeiros, pp. 10–40.Google Scholar
Giron, D, Dubreuil, G, Bennett, A, Dedeine, F, Dicke, M, Dyer, LA, Erb, M, Harris, MO, Huguet, E, Kaloshian, I, Kawakita, A, Lopez-Vaamonde, C, Palmer, TM, Petanidou, T, Poulsen, M, Sallé, A, Simon, JC, Terblanche, JS, Thiéry, D, Whiteman, NK, Woods, HA and Pincebourde, S (2018) Promises and challenges in insect–plant interactions. Entomologia Experimentalis et Applicata 166, 319–343.CrossRefGoogle Scholar
Glas, JJ, Alba, JM, Simoni, S, Villarroel, CA, Stoops, M, Schimmel, B, Schuurink, RC, Sabelis, MW and Kant, MR (2014) Defense suppression benefits herbivores that have a monopoly on their feeding site but can backfire within natural communities. BMC Biology 12, 98.Google ScholarPubMed
Gouinguené, SP and Turlings, TCJ (2002) The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiology 129, 1296–307.CrossRefGoogle ScholarPubMed
Griffith, DM, Veech, JA and Marsh, CJ (2016) COOCCUR: probabilistic species co-occurrence analysis in R. Journal of Statistical Software 69, 1–17.CrossRefGoogle Scholar
Grinberg-Yaari, M, Alagarmalai, J, Lewinsohn, E, Perl-Treves, R and Soroker, V (2015) Role of jasmonic acid signaling in tomato defense against broad mite, Polyphagotarsonemus latus (Acari: Tarsonemidae). Arthropod-Plant Interactions 9, 361–372.CrossRefGoogle Scholar
Gunn, BF, Baudouin, L and Olsen, KM (2011) Independent origins of cultivated coconut (Cocos nucifera L.) in the old world tropics. PLoS ONE 6, e21143.CrossRefGoogle ScholarPubMed
Haq, MA and Sumangala, KN (2002) Coconut mite invasion, injury and distribution. In Fernando, LCP, Moraes, GJ and Wickramananda, IR (eds), Proceedings of the International Workshop on Coconut Mite (Aceria guerreronis). Sri Lanka: Lunuwila, Coconut Research Institute, pp. 41–49.Google Scholar
Harvey, JA, Ode, PJ, Malcicka, M and Gols, R (2015) Short-term seasonal habitat facilitation mediated by an insect herbivore. Basic and Applied Ecology 17, 447–454.CrossRefGoogle Scholar
Heil, M (2008) Indirect defence via tritrophic interactions. New Phytologist 178, 41–61.CrossRefGoogle ScholarPubMed
Hoe, TK (2018) The current scenario and development of the coconut industry. Planter 94, 413–426.Google Scholar
Howard, FW and Rodriguez, EA (1991) Tightness of the perianth of coconuts in relation to infestation by coconut mites. Florida Entomologist 74, 358–361.CrossRefGoogle Scholar
Howard, MM, Kalske, A and Kessler, A (2018) Eco-evolutionary processes affecting plant-herbivore interactions during early community succession. Oecologia 187, 547–559.CrossRefGoogle ScholarPubMed
Ings, TC, Montoya, JM, Bascompte, J, Blüthgen, N, Brown, L, Dormann, CF, Edwards, F, Figueroa, D, Jacob, U, Jones, JI, Lauridsen, RB, Ledger, ME, Lewis, HM, Olesen, JM, van Veen, FJF, Warren, PH and Woodward, G (2009) Ecological networks – beyond food webs. Journal of Animal Ecology 78, 253–269.Google ScholarPubMed
Ives, AR and Carpenter, SR (2007) Stability and diversity of ecosystems. Science (New York, N.Y.) 317, 58–62.CrossRefGoogle ScholarPubMed
Kant, MR, Jonckheere, W, Knegt, B, Lemos, F, Liu, J, Schimmel, BCJ, Villarroel, CA, Ataide, LMS, Dermauw, W, Glas, JJ, Egas, M, Janssen, A, van Leeuwen, T, Schuurink, RC, Sabelis, MW and Alba, JM (2015) Mechanisms and ecological consequences of plant defence induction and suppression in herbivore communities. Annals of Botany 115, 1015–1051.CrossRefGoogle ScholarPubMed
Karban, R (2011) The ecology and evolution of induced resistance against herbivores. Functional Ecology 25, 339–347.CrossRefGoogle Scholar
Karban, R and Baldwin, IT (1997) Induced Responses to Herbivory. Chicago and London: University of Chicago Press.CrossRefGoogle Scholar
Keifer, HH (1965) Eriophyid studies B-14, Sacramento: California, Departament of Agriculture, pp. 1–20.Google Scholar
Kessler, A and Baldwin, IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annual Review Plant Biology 53, 299–328.CrossRefGoogle ScholarPubMed
Kessler, A and Halitshke, R (2007) Specificity and complexity: the impact of herbivore-induced plant responses on arthropod community structure. Current Opinion Plant Biology 10, 409–414.CrossRefGoogle ScholarPubMed
Kroes, A, Stam, JM, David, A, Boland, W, van Loon, JJA, Dicke, M and Poelman, EH (2016) Plant-mediated interactions between two herbivores differentially affect a subsequently arriving third herbivore in populations of wild cabbage. Plant Biology 18, 981–991.CrossRefGoogle ScholarPubMed
Lawson-Balagbo, LM, Gondim, MGC, Moraes, GJ, Hanna, R and Schausberger, P (2007) Refuge use by the coconut mite Aceria guerreronis: fine scale distribution and association with other mites under the perianth. Biology Control 43, 102–110.CrossRefGoogle Scholar
Lawson-Balagbo, LM, Gondim, MGC, Moraes, GJ, Hanna, R and Schausberger, P (2008) Exploration of the acarine fauna on coconut palm in Brazil with emphasis on Aceria guerreronis (Acari: Eriophyidae) and its natural enemies. Bulletin of Entomological Research 98, 83–96.Google ScholarPubMed
Lee, G, Joo, Y, Kim, SG and Baldwin, IT (2017) What happens in the pith stays in the pith: tissue-localized defense responses facilitate chemical niche differentiation between two spatially separated herbivores. The Plant Journal 92, 414–425.CrossRefGoogle ScholarPubMed
Lever, RJ (1969) Pests of the Coconut Palm. Rome: Food & Agriculture Org.Google Scholar
Li, X, Zhong, Z, Sanders, D, Smit, C, Wang, D, Nummi, P, Zhu, Y, Wang, L, Zhu, H and Hassan, N (2018) Reciprocal facilitation between large herbivores and ants in a semi-arid grassland. Proceedings of the Royal Society B: Biological Sciences 285, 1–9.Google Scholar
Lill, JT and Marquis, RJ (2004) Leaf ties as colonization sites for forest arthropods: an experimental study. Ecological Entomology 29, 300–308.CrossRefGoogle Scholar
Lima, DB, Melo, JWS, Gondim, MGC and Moraes, GJ (2012) Limitations of Neoseiulus baraki and Proctolaelaps bickleyi as control agents of Aceria guerreronis. Experimental and Applied Acarology 56, 233–246.CrossRefGoogle ScholarPubMed
Lima, DB, Oliveira, HKV, Melo, JWS, Gondim, MGC, Sabelis, M, Pallini, A and Janssen, A (2017) Predator performance is impaired by the presence of a second prey species. Bulletin of Entomological Research 107, 313–321.CrossRefGoogle ScholarPubMed
Lofego, AC and Gondim, MGC (2006) A new species of Steneotarsonemus (Acari: Tarsonemidae) from Brazil. Systematic & Applied Acarology 11, 195–203.CrossRefGoogle Scholar
Mathew, MT, Anand, BL and Nair, MKS (2004) The mite and coconut economy of India. Indian Coconut Journal 34, 6–14.Google Scholar
Mathur, V, Tytgat, TOG, Graaf, RM, Kalia, V, Reddy, A, Vet, LEM and van Dam, NM (2013) Dealing with double trouble: consequences of single and double herbivory in Brassica juncea. Chemoecology 23, 71–82.CrossRefGoogle Scholar
McKinlay, KS (1965) Insect damage, crop formation and the yield of coconuts. Bulletin of Entomological Research 56, 67–78.CrossRefGoogle Scholar
Moore, D (2001) Insects of palm flowers and fruits. In Howard, FW, Moore, D, Giblin-Davis, RM and Abad, RG (eds), Insects on Palms. Wallingford: CAB International, pp. 233–266.CrossRefGoogle Scholar
Mougi, A and Kondoh, M (2012) Diversity of interaction types and ecological community stability. Science (New York, N.Y.) 337, 349–51.CrossRefGoogle ScholarPubMed
Nair, CPR (2002) Status of eriophyid mite Aceria guerreronis Keifer in India. In Fernando, LCP, Moraes, GJ and Wickramananda, IR (eds), Proceedings of the International Workshop on Coconut Mite (Aceria guerreronis). Sri Lanka: Lunuwila, Coconut Research Institute, pp. 9–12.Google Scholar
Navia, D, Moraes, GJ, Lofego, AC and Flechtmann, CHW (2005) Acarofauna associada a frutos de coqueiro (Cocos nucifera L.) de algumas localidades das Américas. Neotropical Entomology 34, 349–354.Google Scholar
Navia, D, Gondim, MGC, Aratchige, NS and Moraes, GJ (2013) A review of the status of the coconut mite, Aceria guerreronis (Acari: Eriophyidae), a major tropical mite pest. Experimental and Applied Acarology 59, 67–94.CrossRefGoogle Scholar
Ohgushi, T (2008) Herbivore-induced indirect interaction webs on terrestrial plants: the importance of non-trophic, indirect, and facilitative interactions. Entomologia Experimentalis et Applicata 128, 217–229.CrossRefGoogle Scholar
Ohgushi, T and Hambäck, PA (2015) Toward a spatial perspective of plant-based indirect interaction webs: scaling up trait-mediated indirect interactions. Perspectives in Plant Ecology, Evolution and Systematics 17, 500–509.CrossRefGoogle Scholar
Ohgushi, T, Craig, TP and Price, PW (2007) Ecological Communities: Plant Mediation in Indirect Interaction Webs. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Pieterse, CMJ, van der Does, D, Zamioudis, C, Leon-Reyes, A and van Wees &, CM (2012) Hormonal modulation on plant immunity. Annual Review of Cell and Developmental Biology 28, 489–521.CrossRefGoogle ScholarPubMed
Poelman, EH and Kessler, A (2016) Keystone herbivores and the evolution of plant defenses. Trends in Plant Science 21, 477–485.CrossRefGoogle ScholarPubMed
Poelman, EH, Broekgaarden, C, van Loon, JJA and Dicke, M (2008) Early season herbivore differentially affects plant defence responses to subsequently colonizing herbivores and their abundance in the field. Molecular Ecology 17, 3352–3365.CrossRefGoogle ScholarPubMed
R Development Core Team (2014) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Regi, T and Mathews, C (2004) Growth and vigour of coconuts seedlings raised from eriophyid mite (Aceria guerreronis) infested seed nuts. Journal of Plant Breeding and Crop Science 32, 25–29.Google Scholar
Rezende, D, Melo, JWS, Oliveira, JEM and Gondim, MGC (2016) Estimated drop loss due to coconut mite and financial analysis of controlling the pest using the acaricide abamectin. Experimental and Applied Acarology 69, 297–310.CrossRefGoogle Scholar
Rodriguez-Saona, CR, Musser, RO, Vogel, H, Hum-Musser, SM and Thaler, JS (2010) Molecular, biochemical, and organismal analyses of tomato plants simultaneously attacked by herbivores from two feeding guilds. Journal of Chemical Ecology 36, 1043–1057.Google ScholarPubMed
Rusman, Q, Lucas-Barbosa, D and Poelman, EH (2018) Dealing with mutualists and antagonists: specificity of plant-mediated interactions between herbivores and flower visitors, and consequences for plant fitness. Functional Ecology 32, 1022–1035.CrossRefGoogle Scholar
Sanders, D, Jones, CG, Thébault, E, Bouma, TJ, van der Heide, T, van Belzen, J and Barot, S (2014) Integrating ecosystem engineering and food webs. Oikos 123, 513–524.CrossRefGoogle Scholar
Santana, SWJ, Torres, JB, Gondim, MGC and Barros, R (2009) Infestation of coconut fruits by Aceria guerreronis enhances the pest status of the coconut moth Atheloca subrufella. Annual Applied Biology 155, 277–284.CrossRefGoogle Scholar
Santana, SW, Barros, R, Torres, JB and Gondim, MGC (2010) Técnica de Criação e Aspectos Biológicos de Atheloca Subrufella (Hulst) (Lepidoptera: Phycitidae) em Frutos de Coqueiro. Neotropical Entomology 40, 14–19.CrossRefGoogle Scholar
Schmitz, OJ (1998) Direct and indirect effects of predation and predation risk in old-field interaction webs. The America Naturalist 151, 327–342.CrossRefGoogle ScholarPubMed
Segre, H, Malach, N, Henkin, Z and Kadmon, R (2016) Quantifying competitive exclusion and competitive release in ecological communities: a conceptual framework and a case study. PLoS ONE 11, e0160798.CrossRefGoogle ScholarPubMed
Smit, EHD (1970) Morphological and Anatomical Studies of the Coconut. University of Michigan, Veenman.Google Scholar
Sobral, LF (1994) Nutrição e adubação do coqueiro. In Ferreira, JMS, Warwick, DRN and Siqueira, LA (eds) A cultura do coqueiro no Brasil. Aracaju: EMBRAPA-CPATC, pp. 129–157.Google Scholar
Soler, R, van der Putten, WH, Harvey, JA, Vet, LEM, Dicke, M and Bezemer, TM (2012) Root herbivore effects on aboveground multitrophic interactions: patterns, processes and mechanisms. Journal of Chemical Ecology 38, 755–767.CrossRefGoogle ScholarPubMed
Stam, JM, Kroes, A, Li, Y, Gols, R, van Loon, JJA, Poelman, EH and Dicke, M (2014) Plant interactions with multiple insect herbivores: from community to genes. Annual Review Plant Biology 65, 689–713.CrossRefGoogle Scholar
Stam, JM, Dicke, M and Poelman, EH (2018) Order of herbivore arrival on wild cabbage populations influences subsequent arthropod community development. Oikos 125, 336–342.Google Scholar
Tang, S, Pawar, S and Allesina, S (2014) Correlation between interaction strengths drives stability in large ecological networks. Ecology Letters 17, 1094–1100.CrossRefGoogle ScholarPubMed
Thaler, JS, Karban, R, Ullman, DE, Boege, K and Bostock, RM (2002) Croos-talk between jasmonate and salicylate plant defense pathways: effects on several plant parasites. Oecologia 131, 227–235.CrossRefGoogle ScholarPubMed
Thébault, E and Fontaine, C (2010) Stability of ecological communities and the architecture of mutualistic and trophic networks. Science (New York, N.Y.) 329, 853–856.CrossRefGoogle ScholarPubMed
Uesugi, A, Morrell, K, Poelman, EH, Raaijmakers, CE, Kessler, A and Heil, M (2016) Modification of plant-induced responses by an insect ecosystem engineer influences the colonization behaviour of subsequent shelter-users. Journal of Ecology 104, 1096–1105.Google Scholar
Utsumi, S (2011) Eco-evolutionary dynamics in herbivorous insect communities mediated by induced plant responses. Population Ecology 53, 23–34.CrossRefGoogle Scholar
Vaello, T, Sarde, SJ, Marcos-García, MÁ, Boer, JG and Pineda, A (2018) Modulation of plant-mediated interactions between herbivores of different feeding guilds: effects of parasitism and belowground interactions. Scientific Reports 8, 1–8.CrossRefGoogle ScholarPubMed
Vanderplank, FL (1959) Studies on the coconut pest, Pseudotheraptus wayi brown (Coreidae), in Zanzibar.: II. Some data on the yields of coconuts in relation to damage caused by the insect. Bulletin of Entomological Research 50, 135–149.CrossRefGoogle Scholar
Vries, V, Poelman, EH, Anten, N and Evers, J (2018) Elucidating the interaction between light competition and herbivore feeding patterns using functional-structural plant modelling. Annals of Botany 00, 1–13.Google Scholar
Williams, JM (1974) The effect of artificial rat damage on coconut yields in Fiji. Proceedings of the National Academy of Sciences 20, 275–282.Google Scholar
Williams, RJ and Martinez, ND (2000) Simple rules yield complex food webs. Nature 404, 180–183.CrossRefGoogle ScholarPubMed
Wootton, JT (1994) The nature and consequences of indirect effects in ecological communities. Annual Review of Ecology, Evolution, and Systematics 25, 443–466.CrossRefGoogle Scholar