Abstract
Ecological immunology assumes that the host immune efficiency is correlated with its survival after pathogen challenge. To test this hypothesis, we challenged Phyllophaga polyphylla (Bates) larvae with the naturally occurring fungus Metarhizium pingshaense on two consecutive years (2011 and 2012). In each year, we injected the blastospores of M. pingshaense and then used levels of prophenoloxidase (proPO), phenoloxidase (PO) and total haemolymph serum protein as indicators of immune efficiency. Larvae were injected with (1) phosphate buffered saline (PBS) + Tween and viable blastospores of M. pingshaense, (2) PBS + Tween and non-viable blastospores of M. pingshaense, (3) PBS + Tween, or (4) non-manipulated. Overall, levels of PO, proPO and total haemolymph serum protein in larvae after 12 h were similar amongst treatments within each year of collection. However, larvae collected in 2011 showed higher PO and proPO activity but lower total haemolymph serum protein compared with larvae collected in 2012. A survival study injecting viable blastospores showed that larvae collected in both years died within 48 h; however, when non-viable blastospores were injected, which were still toxic to larvae, mortality was greater in larvae collected in 2011 compared with larvae collected in 2012. Altogether, these results indicate that PO, proPO and total haemolymph serum protein do not predict immune strength of P. polyphylla against blastospores of M. pingshaense, but higher values of PO and proPO were correlated with higher survival rates against non-infective but toxic agents. The possible role of some abiotic factors over the differences observed for immune components of P. polyphylla in different years of collection is discussed.
Similar content being viewed by others
References
Adamo SA (2004) Estimating disease resistance in insects: phenoloxidase and lysozyme-like activity and disease resistance in the cricket Gryllus texensis. J Insect Physiol 50:209–216
Adamo SA, Jensen M, Younger M (2001) Changes in lifetime immunocompetence in male and female Gryllus texensis: trade-offs between immunity and reproduction. Anim Behav 62:417–425
Ardia DR, Gantz JE, Schneider BC, Strebel S (2012) Costs of immunity in insects: an induced immune response increases metabolic rate and decreases antimicrobial activity. Funct Ecol 26:732–739
Binggeli O, Neyen C, Poidevin M, Lemaitre B (2014) Prophenoloxidase activation is requeried for survival to microbial infections in Drosophila. PLoS Pathog 10(5):e1004067. doi:10.1371/journal.ppat.1004067
Boguś MI, Kędra E, Bania J, Szczepanik M, Czygier M, Jabłoński P, Pasztaleniec A, Samborski J, Mazgajskaa J, Polanowski A (2007) Different defense strategies of Dendrolimus pini, Galleria mellonella, and Calliphora vicina against fungal infection. J Insect Physiol 53:909–922
Brown VK, Gange AC (1990) Insect herbivory below ground. Adv Ecol Res 20:1–58
Bulet P, Hetru C, Dimarcq JL, Hoffmann D (1999) Antimicrobial peptides in insects: structure and function. Dev Comp Immunol 23:329–344
Carrillo-Benítez MG, Guzmán-Franco AW, Alatorre-Rosas R, Enríquez-Vara JN (2013) Diversity and genetic population structure of fungal pathogens infecting white grub larvae in agricultural soils. Microb Ecol 65:437–449
Cornet S, Biard C, Moret Y (2009) Variation in immune defense among populations of Gammarus pulex (Crustacea: Amphipoda). Oecologia 159:257–269
De Block M, Stoks R (2008) Short-term larval food stress and associated compensatory growth reduce adult immune function in a damselfly. Ecol Entomol 33:796–801
Després L, David JP, Gallet C (2007) The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol Evol 22:298–307
R Development Core Team (2011) R: a language and environment for statistical computing. Vienna, Austria: the R Foundation for Statistical Computing. ISBN: 3-900051-07-0. Available online at http://www.R-project.org/.
Enríquez-Vara JN, Córdoba-Aguilar A, Guzmán-Franco AW, Alatorre-Rosas R, Contreras-Garduño J (2012) Is survival after pathogen exposure explained by host’s immune strength? A test with two species of white grubs (Coleoptera: Scarabeidae) exposed to fungal infection. Environ Entomol 4:959–965
Enríquez-Vara JN, Guzmán-Franco AW, Alatorre-Rosas R, González-Hernández H, Córdoba-Aguilar A, Contreras-Garduño J (2014) Immune response of Phyllophaga polyphylla larvae is not an effective barrier against Metarhizium pingshaense. Invertebr Surviv J 11:240–246
Erb M, Lu J (2013) Soil abiotic factors influence interactions between belowground herbivores and plant roots. J Exp Bot 64:1295–1303
Franssens V, Simonet G, Breugelmans B, Van SS, Hoef VV, Broeck JV (2008) The role of hemocytes, serine protease inhibitors and pathogen-associated patterns in prophenoloxidase activation in the desert locust, Schistocerca gregaria. Peptides 29:235–241
Gillespie JP, Bailey AM, Cobb B, Vilcinskas A (2000) Fungi as elicitors of insect immune responses. Arch Insect Biochem 44:49–68
Goettel MR, Inglis GD (1997) Fungi: hyphomycetes. In: Lacey LA (ed) Manual of techniques in insect pathology. Academic, London, pp 213–249
González-Santoyo I, Córdoba-Aguilar A (2012) Phenoloxidase: a key component of the insect immune system. Entomol Exp Appl 142:1–16
Gottar M, Gobert V, Matskevich AA, Reichhart JM, Wang C, Butt TM, Belvin M, Hoffmann JA, Ferrandon D (2006) Dual detection of fungal infections in Drosophila via recognition of glucans and sensing of virulence factors. Cell 127:1425–1437
Gruber C, Kortet R, Vainikka P, Rantala MJ, Pikkarainen A, Jussila J, Makkonen J, Kokko H, Hirvonen H (2014) Variation in resistance to the invasive crayfish plague and immune defence in the native noble crayfish. Ann Zool Fenn 51:371–389
Guzmán-Franco AW, Hernández-Lopez J, Enríquez-Vara JN, Alatorre-Rosas R, Tamayo-Mejía F, Ortega-Arenas LD (2012) Susceptibility of Phyllophaga polyphylla and Anomala cincta larvae to Beauveria bassiana and Metarhizium anisopliae isolates, and the interaction with soil properties. BioControl 57:553–563
INIFAP (2013) Red de estaciones del INIFAP: Estaciones del estado de Guanajuato. http://clima.inifap.gob.mx/redinifap/. Accessed in August 2013
Jackson TA, Klein MG (2006) Scarabs as pests: a continuing problem. Coleopts Bull 60:102–119
Moreno-García M, Lanz-Mendoza H, Córdoba-Aguilar A (2010) Genetic variance and genotype-by-environment interaction of immune response in Aedes aegypti (Diptera: Culicidae). J Med Entomol 47:111–120
Moreno-García M, Córdoba-Aguilar A, Condé R, Lanz-Mendoza H (2013) Current immunity markers in insect ecological immunology: assumed trade-offs and methodological issues. Bull Entomol Res 103:127–139
Nappi A, Vass E, Frey F, Carton Y (2000) Nitric oxide involvement in Drosophila immunity. Nitric Oxide 4:423–430
Ribaut JM, Pilet PE (1991) Effect of water stress on growth osmotic potential and abscisic acid content of maize roots. Physiology Plantarum 81:156–162
Rivero A (2006) Nitric oxide: an antiparasitic molecule of invertebrates. Trends Parasitol 22:219–225
Roberts KE, Hughes WOH (2014) Immunosenescence and resistance to parasite infection in the honey bee, Apis mellifera. J Invertebr Pathol 121:1–6
Schmid-Hempel P (2003) Variation in immune defense as a question of evolutionary ecology. Proc R Soc London, Ser B 270:357–366
Schmid-Hempel P (2005) Evolutionary ecology of insect immune defenses. Ann Rev Entomol 50:529–551
Schmid-Hempel P (2011) Evolutionary parasitology: the integrated study of infections, immunology, ecology, and genetics. Oxford University Press, Inc., New York, 496p
Schulenburg H, Kurtz J, Moret Y, Siva-Jothy MT (2009) Introduction. Ecological immunology. Philos T Roy Soc B 364:3–14
Siva-Jothy MT, Thompson JJW (2002) Short-term nutrient deprivation affects immune function. Physiol Entomol 27:206–212
Smilanich AM, Dyer LA, Chambers JQ, Bowers MD (2009) Immunological cost of chemical defence and the evolution of herbivore diet breadth. Ecol Lett 12:612–621
Söderhäll K, Cerenius L (1998) Role of the prophenoloxidase-activating system in invertebrate immunity. Curr Opin Immunol 10:23–28
Southwood TRE, Henderson PA (2000) Ecological methods. Blackwell Science Ltd, Oxford, 592p
Zhao P, Lu Z, Strand MR, Jiang H (2011) Antiviral, anti-parasitic, and cytotoxic effects of 5,6-dihydroxyindole (DHI), a reactive compound generated by phenoloxidase during insect immune response. Insect Bioch Mol Biol 41:645–652
Acknowledgments
This research is part of JNEV’s PhD studies and he received a scholarship from CONACYT Mexico. This study was financed by Fundación Guanajuato Produce, A.C., project number FGP521/09-SIFP-11-2007-0271. JCG was financed by CONACyT (grant no. 152666) and the Apoyo Institucional para la Investigación (Universidad de Guanajuato 2014, 2015). ACA was supported by both UNAM-PAPIIT and grant number IN222312.
Author information
Authors and Affiliations
Corresponding author
Additional information
Edited by Guilherme D Rossi – UNESP
Rights and permissions
About this article
Cite this article
Enríquez-Vara, J.N., Contreras-Garduño, J., Guzmán-Franco, A.W. et al. Temporal Variation in Immune Components of the White Grub Phyllophaga polyphylla (Bates) (Coleoptera: Melolonthidae). Neotrop Entomol 44, 466–473 (2015). https://doi.org/10.1007/s13744-015-0308-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13744-015-0308-3