Skip to main content

Advertisement

Log in

Can climate change jeopardize predator control of invasive herbivore species? A case study in avocado agro-ecosystems in Spain

  • Published:
Experimental and Applied Acarology Aims and scope Submit manuscript

Abstract

Climate change is one of the most important factors affecting the phenology, distribution, composition and diversity of organisms. In agricultural systems many pests and natural enemies are arthropods. As poikilotherm organisms, their body temperature is highly dependent on environmental conditions. Because higher trophic levels typically have lower tolerance to high temperatures than lower trophic levels, trends towards increasing local or regional temperatures may affect the strength of predator/prey interactions and disrupt pest control. Furthermore, increasing temperatures may create climate corridors that could facilitate the invasion and establishment of invasive species originating from warmer areas. In this study we examined the effect of environmental conditions on the dynamics of an agro-ecosystem community located in southern Spain, using field data on predator/prey dynamics and climate gathered during four consecutive years. The study system was composed of an ever-green tree species (avocado), an exotic tetranychid mite, and two native species of phytoseiid mites found in association with this new pest. We also present a climatological analysis of the temperature trend in the area of study during the last 28 years, as evidence of temperature warming occurring in the area. We found that the range of temperatures with positive per capita growth rates was much wider in prey than in predators, and that relative humidity contributed to explain the growth rate variation in predators, but not in prey. Predator and prey differences in thermal performance curves could explain why natural enemies did not respond numerically to the pest when environmental conditions were harsh.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aponte O, McMurtry JR (1997) Damage on ‘Hass’ avocado leaves, webbing and nesting behaviour of Oligonychus perseae (Acari: Tetranichidae). Exp Appl Acarol 21:265–272

    Article  Google Scholar 

  • Araújo MB, Luoto M (2007) The importance of biotic interactions for modelling species distributions under climate change. Glob Ecol Biogeogr 16:743–753

    Article  Google Scholar 

  • Armstrong WW (1964) Distribution of oil cells in Persea. Master Thesis, University of California, Riverside, p 40

  • Attrill MJ (2009) Changes in coral reef ecosystems as an indicator of climate and global change. In: Letcher T (ed) Climate change: observed impacts on planet Earth. Elsevier B.V, Amsterdam

    Google Scholar 

  • Bakker FM, Klein ME, Mesa NC, Braun AR (1993) Saturation deficit tolerance spectra of phytophagous mites and their phytoseiid predators on cassava. Exp Appl Acarol 17:97–113

    Google Scholar 

  • Beaumont LJ, Hughes L, Pitman AJ (2008) Why is the choice of future climate scenarios for species distribution modelling important? Ecol Lett 11:1135–1146

    PubMed  Google Scholar 

  • Beaumont LJ, Gallagher RV, Thuiller W, Downey PO, Leishman MR, Hughes L (2009) Different climatic envelopes among invasive populations may lead to underestimations of current and future biological invasions. Divers Distrib 15:409–420

    Article  Google Scholar 

  • Benito-Garzon M, Sanchez de Dios R, Sainz-Ollero H (2008) Effects of climate change on the distribution of Iberian tree species. Appl Veg Sci 11:169–178

    Article  Google Scholar 

  • Beveridge OS, Humphries S, Petchey OL (2010) The interacting effects of temperature and food chain length on trophic abundance and ecosystem function. J Anim Ecol 79:693–700

    Article  PubMed  Google Scholar 

  • Bouras SL, Papadoulis GT (2005) Influence of selected fruit tree pollen on life history of Euseius stipulatus (Acari: Phytoseiidae). Exp Appl Acarol 36:1–14

    Article  PubMed  Google Scholar 

  • Broufas GD, Koveos DS (2001) Development, survival and reproduction of Euseius finlandicus (Acari, Phytoseiidae) at different constant temperatures. Exp Appl Acarol 26:441–460

    Article  Google Scholar 

  • Cagnolo L, Molina SI, Valladares GR (2002) Diversity and guild structure of insect assemblages under grazing and exclusion regimes in a montane grassland from Central Argentina. Biodivers Conserv 11:407–420

    Article  Google Scholar 

  • Castagnoli M, Simoni S (1994) The effect of different constant humidities on eggs and larvae of Amblyseius californicus (McGregor) (Acarina: Phytoseiidae). Redia 77:349–359

    Google Scholar 

  • Croft BA, Messing RH, Dunley JE, Strong WB (1993) Effects of humidity on eggs and immatures of Neoseiulus fallacis, Amblyseius andersoni, Metaseiulus occidentalis and Typhlodromus pyri (Phytoseiidae): implications for biological control on apple, caneberry, strawberry and hop. Exp Appl Acarol 17:451–459

    Article  Google Scholar 

  • DeCourcy-Williams ME, Kravar-Garde L, Fenlon JS, Sunderland KD (2004) Phytoseiid mites in protected crops: the effect of humidity and food availability on egg hatch and adult life span of Iphiseius degenerans, Neoseiulus cucumeris, N. californicus and Phytoseiulus persimilis (Acari: Phytoseiidae). Exp Appl Acarol 32:1–13

    Article  Google Scholar 

  • Edwards M (2009) Sea life (pelagic and planktonic ecosystems) as an indicator of climate and global change. In: Letcher T (ed) Climate change: observed impacts on planet Earth. Elsevier B.V, Amsterdam

    Google Scholar 

  • Ferragut F, García-Mari F, Costa-Comelles J, Laborda R (1987) Influence of food and temperature on development and oviposition of Euseius stipulatus and Typhlodromus phialatus (Acari : Phytoseiidae). Exp Appl Acarol 3:317–329

    Article  Google Scholar 

  • Ferrero M, de Moraes GJ, Kreiter S, Tixier M-S, Knapp M (2007) Life tables of Phytoseiulus longipes feeding on Tetranychus evansi at four temperatures (Acari: Phytoseiidae, Tetranychidae). Exp Appl Acarol 41:45–53

    Article  PubMed  Google Scholar 

  • Ferrero M, Gigot C, Tixier MS, Van Houten YM, Kreiter S (2010) Egg hatching response to a range of air humidities for six species of predatory mites. Entomol Exp Appl 135:237–244

    Article  Google Scholar 

  • Fiedler W (2009) Bird ecology as an indicator of climate and global change. In: Letcher T (ed) Climate change: observed impacts on planet Earth. Elsevier B.V, Amsterdam

    Google Scholar 

  • Gilman SE, Urban MC, Tewksbury J, Gilchrist GW, Holt RD (2010) A framework for community interactions under climate change. Trends Ecol Evol 25:325–331

    Article  PubMed  Google Scholar 

  • González-Fernández JJ, de la Peña F, Hormaza JI, Boyero JR, Vela JM, Wong E, Trigo MM, Montserrat M (2009) Alternative food improves the combined effect of an omnivore and a predator on biological pest control. A case study in avocado orchards. Bull Entomol Res 99(5):433–444

    Article  PubMed  Google Scholar 

  • Hance T, van Baaren J, Vernon P, Boivin G (2007) Impact of extreme temperatures on parasitoids in a climate change perspective. Annu Rev Entomol 52:107–126

    Article  PubMed  CAS  Google Scholar 

  • Hegland SJ, Nielsen A, Lázaro A, Bjerknes AL, Totland O (2009) How does climate warming affect plant-pollinator interactions? Ecol Lett 12:189–195

    Article  Google Scholar 

  • Hole DG, Willis SG, Pain DJ, Fishpool LD, Butchart SHM, Collingham YC, Rahbek C, Huntley B (2009) Projected impacts of climate change on a continent-wide protected area network. Ecol Lett 12(5):420–431

    Article  PubMed  Google Scholar 

  • Humphries MM (2009) Mammal ecology as an indicator of climate change. In: Letcher T (ed) Climate change: observed impacts on planet Earth. Elsevier B.V, Amsterdam

    Google Scholar 

  • IPCC (2007) Climate change 2007: impacts, adaptation and vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. In: Parry KL, Canziani OF, Palutikif JP, vann der Linden PJ, Hanson CE (eds) Cambridge University Press, Cambridge

  • Krebs RA, Loeschke L (1994) Effects of exposure to short-term heat stress on fitness components in Drosophila melanogaster. J Evol Biol 7:39–49

    Article  Google Scholar 

  • Lavalle C, Micale F, Houston TD, Camia A, Hiederer R, Lazar C, Conte C, Amatulli G, Genovese G (2009) Climate change in Europe. 3. Impact on agriculture and forestry. A review. Agron Sustain Dev 29:433–446

    Article  Google Scholar 

  • MARM (2011) Anuario de Estadística del Ministerio de de Medio Ambiente y Medio Rural y Marino. Available via dialog http://www.mapa.es/es/estadistica/pags/anuario/2009/indice.asp

  • McMurtry JA, Scriven GT (1965) Studies on predator-prey interactions between Amblyseius hibisci and Oligonychus punicae (Acarina: Phytoseiidae, Tetranichidae) under greenhouse conditions. Ann Entomol Soc Am 59:793–800

    Google Scholar 

  • Mieszkowska N (2009) Intertidal indicators of climate and global change. In: Letcher T (ed) Climate change: observed impacts on planet Earth. Elsevier B.V, Amsterdam

    Google Scholar 

  • Momen FM, Abdel-Khalek A (2008) Effect of the tomato rust mite Aculops lycopersici (Acari: Eriophyidae) on the development and reproduction of three predatory phytoseiid mites. Int J Trop Inst Sci 28:53–57

    Article  Google Scholar 

  • Montserrat M, de la Peña F, Hormaza JI, González-Fernández JJ (2008) How do Neoseiulus californicus (Acari: Phytoseiidae) females penetrate densely webbed spider mite nests? Exp Appl Acarol 44:101–106

    Article  PubMed  CAS  Google Scholar 

  • Morecroft MD, Keith SA (2009) Plant ecology as an indicator of climate and global change. In: Letcher T (ed) Climate change: observed impacts on planet Earth. Elsevier B.V, Amsterdam

    Google Scholar 

  • Mori K, Saito Y, Sakagami T (1999) Efects of the nest web and female attendance on survival of young in a subsocial spider mite, Schizotetranychus longus (Acari: Tetranychidae). Exp Appl Acarol 23:411–418

    Article  Google Scholar 

  • Nguyen TPT, Amano H (2009) Mating duration and egg production of the predaceous mite Neoseiulus californicus (Acari: Phytoseiidae) vary with temperature. J Asia Pac Entomol 12:297–299

    Article  Google Scholar 

  • Nguyen TPT, Amano H (2010) Temperature at immature and adult stages differentially affects mating duration and egg production of Neoseiulus californicus females mated once (Acari: Phytoseiidae). J Asia-Pac Entomol 13(2010):65–68

    Article  Google Scholar 

  • Pelini SL, Prior KM, Parker DJ, Dzurisin JDK, Lindroth RL, Hellmann JJ (2009) Climate change and temporal and spatial mismatches in insect communities. In: Letcher T (ed) Climate change: observed impacts on planet Earth. Elsevier B.V, Amsterdam

    Google Scholar 

  • Platt KA, Thompson WW (1992) Idioblast oil cells of avocado: distribution, isolation, ultraestructure, histiochemistry, and biochemistry. Int J Plant Sci 153:301–310

    Article  CAS  Google Scholar 

  • Platt-Aloia KA, Oross JW, Thompson WW (1983) Ultraestructure and development of oil cells in mesocarp of avocado fruit. Bot Gaz 144:49–55

    Article  Google Scholar 

  • Preisser EL, Strong DR (2004) Climate affects predator control of an herbivore outbreak. Am Nat 163(5):754–762

    Article  PubMed  Google Scholar 

  • Rodriguez-Soana C, Trumble JT (2000) Secretory avocado idioblast oil cells: evidence of their defensive role against non-adapted insect herbivore. Entomologia Experimentalis et Applicatta 94:183–194

    Article  Google Scholar 

  • Rodriguez-Soana C, Millar JG, Trumble JT (1997) Growth inhibitory, insecticidal, and feeding deterrent effects of (12Z,15Z)-1-acetoxy-2-hydroxy-4-oxo-heneicosa-12,15,-dienne, a compound from avocado fruit, to Spodoptera exigua. J Chem Ecol 23:1819–1831

    Article  Google Scholar 

  • Rodriguez-Soana C, Millar JG, Maynard DF, Trumble JT (1998) Novel antifeedant and insecticidal compounds from avocado idioblast cell oil. J Chem Ecol 24:867–889

    Article  Google Scholar 

  • Roy M, Brodeur J, Cloutier C (2003) Effect of temperature on intrinsic rates of natural increase (rm) of a coccinellid and its spider mite prey. Biocontrol 48:57–72

    Article  Google Scholar 

  • Scott M, Berrigan D, Hoffmann AA (1997) Costs and benefits of acclimation to elevated temperature in Trichogramma carverae. Entomol Exp Appl 85:211–219

    Article  Google Scholar 

  • Skirvin DJ, Fenlon JS (2003a) Of mites and movement: the effects of plant connectedness and temperature on movement of Phytoseiulus persimilis. Biol Control 27:242–250

    Article  Google Scholar 

  • Skirvin DJ, Fenlon JS (2003b) The effect of temperature on the functional response of Phytoseiulus persimilis (Acari: Phytoseiidae). Exp Appl Acarol 31:37–49

    Article  PubMed  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research. 3rd edn. WH Freeman and Co., New York, p 887, ISBN: 0-7167-2411-1

  • Stavrinides MC, Lara JR, Mills NJ (2010a) Comparative influence of temperature on development and biological control of two common vineyard pests (Acari: Tetranychidae). Biol Contr 55:126–131

    Article  Google Scholar 

  • Stavrinides MC, Daane KM, Lampinen BD, Mills NJ (2010b) Plant water stress, leaf temperature, and spider mite (Acari: Tetranychidae) outbreaks in California Vineyards. Environ Entomol 39(4):1232–1241

    Article  PubMed  Google Scholar 

  • Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11(12):1351–1363

    Article  PubMed  Google Scholar 

  • Vasconcelos GJN, de Moraes GJ, Júnior ID, Knapp M (2008) Life history of the predatory mite Phytoseiulus fragariae on Tetranychus evansi and Tetranychus urticae (Acari: Phytoseiidae, Tetranychidae) at five temperatures. Exp Appl Acarol 44:27–36

    Article  PubMed  Google Scholar 

  • Vela JM, González-Fernández J, Wong E, Montserrat M, Farré JM, Boyero JR (2007) El ácaro del aguacate (Oligonychus perseae): Estado actual del problema e investigación en Andalucía. Agrícola Vergel 306:301–308

    Google Scholar 

  • Voigt W, Perner J, Davis AJ, Eggers T, Schumacher J, Bahrmann R, Fabian B, Heinrich W, Kohler G, Lichter D, Marstaller R, Sander FW (2003) Trophic levels are differentially sensitive to climate. Ecology 84(9):2444–2453

    Article  Google Scholar 

  • Walzer A, Castagnoli M, Simoni S, Liguori M, Palevsky E, Schausberger P (2007) Intraspecific variation in humidity susceptibility of the predatory mite Neoseiulus californicus: survival, development and reproduction. Biol Control 41:42–52

    Article  Google Scholar 

  • Wang XG, Johnson MW, Daane KM, Opp S (2009a) Combined effects of heat stress and food supply on flight performance of olive fruit fly (Diptera: Tephritidae). Ann Entomol Soc Am 102:727–734

    Article  Google Scholar 

  • Wang XG, Johnson MW, Daane KM, Nadel H (2009b) High summer temperatures affect the survival and reproduction of olive fruit fly (Diptera: Tephritidae). Environ Entomol 38(5):1496–1504

    Article  PubMed  CAS  Google Scholar 

  • Welbourn WC (2007) Triology 46(4): 6. Available via dialog, http://www.freshfromflorida.com/pi/enpp/triology/archive/4604.pdf

  • Wilmers CC, Post E, Hastings A (2007) The anatomy of predator-prey dynamics in a changing climate. J Anim Ecol 76:1037–1044

    Article  PubMed  Google Scholar 

  • Zhang N, Kong J (1985) Responses of Amblyseius fallacies Garman to various relative humidity regimes. Chin J Biol Control 1:6–9

    Google Scholar 

  • Zhang Y, Jewett TJ, Shipp JL (2002) A dynamic model to estimate in-canopy and leaf-surface microclimate of greenhouse cucumber crops. Trans ASAE 45:179–192

    Google Scholar 

  • Zhang Y, Wang L, Wu K, Wyckhuys KAG, Heimpel GE (2008) Flight performance of the soybean aphid, Aphis glycines (Homoptera: Aphididae) under different temperature and humidity regimens. Environ Entomol 37:301–306

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The authors are indebted to Prof. Dr. Gøsta Nachman for his statistical advice and comments on an early version which significantly improved the manuscript. J.A. Jacas and J.I. Hormaza are thanked for their valuable comments on the manuscript. This work was financed by la Junta de Andalucía (Proyecto de Excelencia P08-AGR-3694), the Spanish Ministry of Science and Innovation (AGL2011-30538-C03-03), and the Spanish National Research Council (CSIC, project PIE200940I121). Field surveys would not have been possible without logistic help from J. González Fernández, J.M. Hermoso and E. Guirado. J.M. Sanchez Pulido is thanked for providing data on temperature records in the area of study. M. M. Trigo is thanked for providing data of pollen in the atmosphere. The animals used for the research of this publication are no test animals in the legal sense.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marta Montserrat.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Montserrat, M., Sahún, R.M. & Guzmán, C. Can climate change jeopardize predator control of invasive herbivore species? A case study in avocado agro-ecosystems in Spain. Exp Appl Acarol 59, 27–42 (2013). https://doi.org/10.1007/s10493-012-9560-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10493-012-9560-y

Keywords

Navigation