Abstract
Introduced herbivores often alter predator–prey dynamics between native organisms. We investigated whether the exotic mite Raoiella indica can interfere in the predation relationships between the predator Amblyseius largoensis and the native herbivorous mite Oligonychus pratensis and be favored as a result. Populations of A. largoensis were established in laboratory, one reared with exotic prey and another with native prey. For each population, of A. largoensis were evaluated for: egg-to-adult developmental time, oviposition rate, and feed conversion efficiency (FCE) of females. Also, to observe the interaction with prey, behavioral tests were conducted, evaluating the time to the first attack, oviposition site preference, and prey preference consumption. Regardless of prey offered, there was no prey effect on immature developmental time or female oviposition rate. However, A. largoensis showed superior FCE feed on exotic (11.4%) over native prey (3.9%). Both A. largoensis populations preferred to prey on eggs of native species and also tended to choose oviposition sites containing native prey eggs. Those reared on exotic prey attacked their first prey in less time than those reared on native prey. Therefore, the presence of R. indica affects both predator population growth and the feeding preference for native prey, which causes a risk of displacement of O. pratensis.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
(Data transparency) I allow availability of data and material, available in: https://github.com/Natalydlp/Predator_raoiella_pratensis.git.
Code availability
(Software application or custom code) Not applicable.
References
Asner GP, Vitousek PM (2005) Remote analysis of biological invasion and biogeochemical change. Proc Natl Acad Sci USA 102:4383–4386. https://doi.org/10.1073/pnas.0500823102
Baltz DM, Moyle PB (1993) Invasion resistance to introduced species by a native assemblage of California stream fishes. Ecol Appl 3:246–255. https://doi.org/10.2307/1941827
Barros ME, Lima DB, Mendes JA et al (2020) The establishment of an invasive pest mite, Raoiella indica, affects mite abundance and diversity on coconut plants. Syst Appl Acarol 25:881–894. https://doi.org/10.11158/saa.25.5.9
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Soft. https://doi.org/10.18637/jss.v067.i01
Blum MS, Hilker M (2003) Chemical protection of insect eggs. In: Hilker M, Meiners T (eds) Chemoecology of insect eggs and egg deposition. Blackwell Publishing Ltd, Oxford, pp 61–90
Byers JE (2002) Physical habitat attribute mediates biotic resistance to non-indigenous species invasion. Oecologia 130:146–156. https://doi.org/10.1007/s004420100777
Calvet ÉC, Lima DB, Melo JWS, Gondim MGC (2022) The expansion of invasive mite Raoiella indica can be improved by coexistence with Oligonychus pratensis. Ann Appl Biol 181:288–297. https://doi.org/10.1111/aab.12773
Carrillo D, Peña JE, Hoy MA, Frank JH (2010) Development and reproduction of Amblyseius largoensis (Acari: Phytoseiidae) feeding on pollen, Raoiella indica (Acari: Tenuipalpidae), and other microarthropods inhabiting coconuts in Florida, USA. Exp Appl Acarol 52:119–129. https://doi.org/10.1007/s10493-010-9360-1
Carrillo D, Howard Frank J, Rodrigues JCV, Peña JE (2012) A review of the natural enemies of the red palm mite, Raoiella indica (Acari: Tenuipalpidae). Exp Appl Acarol 57:347–360. https://doi.org/10.1007/s10493-011-9499-4
Choh Y, Sabelis MW, Janssen A (2015) Distribution and oviposition site selection by predatory mites in the presence of intraguild predators. Exp Appl Acarol 67:477–491. https://doi.org/10.1007/s10493-015-9970-8
Congdon BD, Logan JA (1983) Temperature effects on development and fecundity of Oligonychus pratensis (Acari: Tetranychidae). Environ Entomol 12:359–362. https://doi.org/10.1093/ee/12.2.359
Crystal-Ornelas R, Lockwood JL (2020) Cumulative meta-analysis identifies declining but negative impacts of invasive species on richness after 20 yr. Ecology 101:e03082. https://doi.org/10.1002/ecy.3082
da Cruz WP, Krug C, Vasconcelos GJN, de Moraes GJ (2015) Diversity of mites associated with Raoiella indica (Acari: Prostigmata) on coconut palms in the central region of the Brazilian Amazonia, with emphasis on the predaceous Phytoseiidae (Acari: Mesostigmata). Syst Appl Acarol 20:875. https://doi.org/10.11158/saa.20.8.4
David P, Thebault E, Anneville O, Duyck PF, Chapuis E, Loeuille N (2017) Impacts of invasive species on food webs: a review of empirical data. In: Bohan DA, Dumbrell AJ, Massol F (eds) Networks of invasion: a synthesis of concepts. Advances in ecological research. Elsevier, Amsterdam, pp 1–60. https://doi.org/10.1016/bs.aecr.2016.10.001
De Rivera CE, Ruiz GM, Hines AH, Jivoff P (2005) Biotic resistance to invasion: native predator limits or limits abundance and distribution of an introduced crab. Ecology 86:3364–3376. https://doi.org/10.1890/05-0479
Desneux N, Wajnberg E, Wyckhuys KAG et al (2010) Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. J Pest Sci 83:197–215. https://doi.org/10.1007/s10340-010-0321-6
Di Palma A, Beard JJ, Bauchan GR et al (2021) Dorsal setae in Raoiella (Acari: Tenuipalpidae): their functional morphology and implication in fluid secretion. Arthropod Struct Dev 60:101023. https://doi.org/10.1016/j.asd.2020.101023
Domingos CA, Oliveira LO, de Morais EGF et al (2013) Comparison of two populations of the pantropical predator Amblyseius largoensis (Acari: Phytoseiidae) for biological control of Raoiella indica (Acari: Tenuipalpidae). Exp Appl Acarol 60:83–93. https://doi.org/10.1007/s10493-012-9625-y
Dowling APG, Ochoa R, Beard JJ et al (2012) Phylogenetic investigation of the genus Raoiella (Prostigmata: Tenuipalpidae): diversity, distribution, and world invasions. Exp Appl Acarol 57:257–269. https://doi.org/10.1007/s10493-011-9483-z
Ehrenfeld JG (2010) Ecosystem consequences of biological invasions. Annu Rev Ecol Evol Syst 41:59–80. https://doi.org/10.1146/annurev-ecolsys-102209-144650
Eisner T, Attygalle AB, Conner WE et al (1996) Chemical egg defense in a green lacewing (Ceraeochrysa smithi). Proc Natl Acad Sci USA 93:3
Eisner T, Eisner M, Rossini C et al (2000) Chemical defense against predation in an insect egg. Proc Natl Acad Sci USA 97:1634–1639. https://doi.org/10.1073/pnas.030532797
Eisner T, Eisner M, Siegler M (2005) Secret weapons: defenses of insects, spiders, scorpions, and other many-legged creatures. Belknap Press of Harvard Univ. Press, Cambridge
Elton CS (1958) The balance between populations. In: Simberloff D, Ricciardi A (eds) The ecology of invasions by animals and plants. Springer, Boston. https://doi.org/10.1007/978-1-4899-7214-9_6
Evans EW (2004) Habitat displacement of North American ladybirds by an introduced species. Ecology 85:637–647. https://doi.org/10.1890/03-0230
Ferreira J, Melo E, Oliveira A et al (2019) Ocorrência e sintomas de ataque dos ácaros Oligonychus pratensis (Banks) e Tetranychus neocaledonicus André (Acari: Tetranychidae) em coqueiro-anão-verde no Brasil. 228:22
Fidelis EG, Farias ES, Joaquim Da Silva Junior R (2022) Contribution of natural enemies and weather to the population buildup of Raoiella indica on coconut. Syst Appl Acarol. https://doi.org/10.11158/saa.27.8.6
Galvão AS, Gondim MG Jr, Moraes GJD, Oliveira JVD (2007) Biologia de Amblyseius largoensis (Muma) (Acari: Phytoseiidae), um potencial predador de Aceria guerreronis Keifer (Acari: Eriophyidae) em coqueiro. Neotrop Entomol 36:465–470
Gnanvossou D, Hanna R, Yaninek JS, Toko M (2005) Comparative life history traits of three neotropical phytoseiid mites maintained on plant-based diets. Biol Control 35:32–39. https://doi.org/10.1016/j.biocontrol.2005.05.013
Godinho DP, Janssen A, Dias T et al (2016) Down-regulation of plant defence in a resident spider mite species and its effect upon con- and heterospecifics. Oecologia 180:161–167. https://doi.org/10.1007/s00442-015-3434-z
Gondim MGC, Castro TMMG, Marsaro AL et al (2012) Can the red palm mite threaten the Amazon vegetation? Syst Biodivers 10:527–535. https://doi.org/10.1080/14772000.2012.752415
Helle W, Sabelis MW (eds) (1985) Spider mites: their biology, natural enemies, and control. Elsevier, New York
Herbold B, Moyle PB (1986) Introduced species and vacant niches. Am Nat 128:751–760. https://doi.org/10.1086/284600
Holt RD (1977) Predation, apparent competition, and the structure of prey communities. Theor Popul Biol 12:197–229. https://doi.org/10.1016/0040-5809(77)90042-9
Holt RD, Lawton JH (1994) The ecological consequences of shared natural enemies. Annu Rev Ecol Syst 25:495–520. https://doi.org/10.1146/annurev.es.25.110194.002431
Jeppson LR, Keifer HH, Baker EW (1975) Mites injurious to economic plants. University of California Press, Berkeley
Kamburov SS (1971) Feeding, development, and reproduction of Amblyseius largoensis on various food substances. J Econ Entomol 64(3):643–648
Lemos F, Sarmento RA, Pallini A et al (2010) Spider mite web mediates anti-predator behaviour. Exp Appl Acarol 52:1–10. https://doi.org/10.1007/s10493-010-9344-1
Lira VA, Jumbo LOV, de Freitas GS et al (2021) Efficacy of Amblyseius largoensis (Muma) as a biocontrol agent of the red palm mite Raoiella indica (Acari: Tenuipalpidae). Phytoparasitica 49:103–111. https://doi.org/10.1007/s12600-020-00875-8
Lonsdale WM (1999) Global patterns of plant invasions and the concept of invasibility. Ecology 80:1522–1536. https://doi.org/10.1890/0012-9658(1999)080[1522:GPOPIA]2.0.CO;2
Mack RN, Simberloff D, Mark Lonsdale W et al (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710. https://doi.org/10.1890/1051-0761(2000)010[0689:BICEGC]2.0.CO;2
McMurtry JA, Moraes GJD, Sourassou NF (2013) Revision of the lifestyles of phytoseiid mites (Acari: Phytoseiidae) and implications for biological control strategies. Syst Appl Acarol 18:297. https://doi.org/10.11158/saa.18.4.1
Melo JW, Lima DB, Staudacher H, Silva FR, Gondim MGC Jr., Sabelis MW (2015) Evidence of Amblyseius largoensis and Euseius alatus as biological control agent of Aceria guerreronis. Exp Appl Acarol 67:411–421. https://doi.org/10.1007/s10493-015-9963-7
Melo JWS, Navia D, Mendes JA et al (2018) The invasive red palm mite, Raoiella indica Hirst (Acari: Tenuipalpidae), in Brazil: range extension and arrival into the most threatened area, the Northeast Region. Int J Acarol 44:146–149. https://doi.org/10.1080/01647954.2018.1474945
Mendes JA, Lima DB, Sousa Neto EP et al (2018) Functional response of Amblyseius largoensis to Raoiella indica eggs is mediated by previous feeding experience. Syst Appl Acarol 23:1907. https://doi.org/10.11158/saa.23.10.3
Montpellier https://www.montpellier.inra.fr/CBGP/spmweb/notespecies.php?id=613#hosts
Moraes GJ, Castro TMMG, Kreiter S et al (2012) Search for natural enemies of Raoiella indica Hirst in La Réunion Island (Indian Ocean). Acarologia 52:129–134. https://doi.org/10.1051/acarologia/20122043
Mushtaq HMS, Kamran M, Alatawi FJ (2021) Two new life types and assessment of web-associated behavioral characteristics of some Oligonychus species on various host plants. Exp Appl Acarol 83:211–227. https://doi.org/10.1007/s10493-020-00579-y
Navia D, Moraes DF, de Mendonça RS (2015) Acaro-vermelho-das-palmeiras, Raoiella indica Hirst (Prostigmata: Tenuipalpidae). In: Pragas introduzidas: insetos e ácaros. Fealq, p 908
Noonburg EG, Byers JE (2005) More harm than good: when invader vulnerability to predators enhances impact on native species. Ecology 86:2555–2560. https://doi.org/10.1890/05-0143
Nusantara A, Trisyono YA, Suputa S, Martono E (2017) Biology of red palm mite, Raoiella indica, on different coconut varieties. JPTI 21:23
Okada S, Yano S (2021) Oviposition-site shift in phytophagous mites reflects a trade-off between predator avoidance and rainstorm resistance. Biol Lett. https://doi.org/10.1098/rsbl.2020.0669
Peña JE, Rodrigues JCV, Roda A, Carrillo D, Osborne LS (2009) Predator-prey dynamics and strategies for control of the red palm mite (Raoiella indica) (Acari: Tenuipalpidae) in areas of invasion in the Neotropics. Iobc/wprs Bull 50:69–79
Peña JE, Bruin J, Sabelis MW (2012) Biology and control of the red palm mite, Raoiella indica: an introduction. Exp Appl Acarol 57:211–213. https://doi.org/10.1007/s10493-012-9569-2
Pimm S (1989) Theories predicting success and impact of introduced species. In: Biological invasions: a global perspective. Published on behalf of the Scientific Committee on Problems of the Environment (SCOPE) of the International Council of Scientific Unions (ICSU) by Wiley, Chichester, p 525
Pintor LM, Byers JE (2015) Do native predators benefit from non-native prey? Ecol Lett 18:1174–1180. https://doi.org/10.1111/ele.12496
R Development Core Team (2022) RStudio: integrated development environment for R. RStudio, PBC, Boston
Ragsdale DW, Landis DA, Brodeur J et al (2011) Ecology and management of the Soybean aphid in North America. Annu Rev Entomol 56:375–399. https://doi.org/10.1146/annurev-ento-120709-144755
Reusch T (1998) Native predators contribute to invasion resistance to the non-indigenous bivalve Musculista senhousia in southern California, USA. Mar Ecol Prog Ser 170:159–168. https://doi.org/10.3354/meps170159
Robinson JV, Wellborn GA (1988) Ecological resistance to the invasion of a freshwater clam, Corbicula fluminea: fish predation effects. Oecologia 77:445–452. https://doi.org/10.1007/BF00377258
Sarmento RA, Lemos F, Dias CR et al (2011) A herbivorous mite down-regulates plant defence and produces web to exclude competitors. PLoS ONE 6:e23757. https://doi.org/10.1371/journal.pone.0023757
Schausberger P (2003) Cannibalism among phytoseiid mites: a review. Exp Appl Acarol 29:173–191. https://doi.org/10.1023/A:1025839206394
Simberloff D (1981) Community effects of introduced species. In: Nitecki M (ed) Biotic crises in ecological and evolutionary time. Matthew Nitecki, Chicago, p 301
Simberloff D (2011) How common are invasion-induced ecosystem impacts? Biol Invasions 13:1255–1268. https://doi.org/10.1007/s10530-011-9956-3
Strauss SY, Lau JA, Carroll SP (2006) Evolutionary responses of natives to introduced species: What do introductions tell us about natural communities?: Evolutionary responses of natives to introduced species. Ecol Lett 9:357–374. https://doi.org/10.1111/j.1461-0248.2005.00874.x
Taylor B (2022) Raoiella indica (red palm mite). CABI Compendium CABI Compendium: 46792. https://doi.org/10.1079/cabicompendium.46792
Waldbauer GP (1968) The consumption and utilization of food by insects. In: Advances in insect physiology. Elsevier, pp 229–288
Wong JWY, Meunier J, Kölliker M (2013) The evolution of parental care in insects: the roles of ecology, life history and the social environment: the evolution of parental care in insects. Ecol Entomol 38:123–137. https://doi.org/10.1111/een.12000
Zuur AF, Ieno EN, Meesters EHWG (2009) A beginner’s guide to R. Use R. Springer, Dordrecht
Acknowledgements
I’m thankful to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—PROEX (Academic Excellence Program) 88882.183155/2018-01 for financed in part this study.
Author information
Authors and Affiliations
Contributions
Material preparation, data collection and analysis and were performed by Érica Costa Calvet and Nataly De La Pava. The first draft of the manuscript was written by Érica Costa Calvet, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
I consent publication.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Calvet, É.C., Lima, D.B., De La Pava, N. et al. The association between the exotic species Raoiella indica Hirst and the predator Amblyseius largoensis (Muma) may cause displacement of the native species Oligonychus pratensis (Banks). Biol Invasions 26, 757–767 (2024). https://doi.org/10.1007/s10530-023-03205-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-023-03205-1