Intraspecific alkaloid variation in ladybird eggs and its effects on con- and hetero-specific intraguild predators
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Abstract
Egg predation and cannibalism are common phenomena in predatory ladybirds despite the presence of defensive alkaloids. Consumption of heterospecific eggs negatively affects survivorship and development; however, intraspecific variation in quantities of alkaloids and post-ingestion responses to con- and hetero-specific alkaloids, are not well understood. We examined variation in the quantity of alkaloids in eggs of Harmonia axyridis (Pallas), Coccinella septempunctata L., and Hippodamia convergens (Guérin) using gas chromatography-mass spectrometry, and show a link between heterospecific alkaloids and their toxicity and/or costs by feeding high and low alkaloid eggs to first instar H. axyridis and C. septempunctata. The repeatability of alkaloid measurements in eggs in an egg cluster was high; however, the amount of alkaloids varied significantly between egg clutches within and among females. This variation affected egg consumption by C. septempunctata when fed H. axyridis eggs. Harmonia axyridis accumulated their own alkaloid by cannibalism and synthesized it de novo, but C. septempunctata lost some portion of the consumed conspecific alkaloids. Both species lost most of the consumed heterospecific alkaloids, but C. septempunctata died within 3 days. Most H. axyridis survived to the second instar, but C. septempunctata alkaloids led to a significant reduction in weight gain compared to an aphid control. In addition, ingestion of high alkaloid C. septempunctata extended development of H. axyridis compared to the aphid control or conspecific eggs. Harmonia axyridis had greater abilities to process ingested con- and hetero-specific alkaloids compared with C. septempunctata, which may, in part, explain their interspecific interactions in nature.
Keywords
Defensive alkaloids Predatory ladybirds Intraguild predation Harmonia axyridis Coccinella septempunctataNotes
Acknowledgments
We thank S. Moser, S. Stamper, S. Bessin, S. Sams, M. Eskelson, S. Romero, S. Colvin, J. Harwood, C. Fox, B. Wallin, T. Sutton and E. O’Neill for insect collections, laboratory arrangements and experimental help. We also thank two anonymous reviewers and editors for their very helpful comments on the manuscript. This experiment was supported by USDA-NRI (2007-02286). This paper is publication number 09-08-089 of the University of Kentucky Agricultural Experiment Station.
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References
- Agarwala BK, Dixon AFG (1992) Laboratory study of cannibalism and interspecific predation in ladybirds. Ecol Entomol 17:303–309CrossRefGoogle Scholar
- Agarwala BK, Bhattacharya S, Bardhanroy P (1998) Who eats whose eggs? Intra- versus inter-specific interactions in starving ladybird beetles predaceous on aphids. Ethol Ecol Evol 10:361–368Google Scholar
- Alam N, Choi IS, Song KS, Hong J, Lee CO, Jung JH (2002) A new alkaloid from two coccinellid beetles Harmonia axyridis and Aiolocaria hexaspilota. Bull Kor Chem Soc 23:497CrossRefGoogle Scholar
- Aniszewski T (2007) Alkaloids—secrets of life, alkaloid chemistry, biological significance, applications and ecological role. Elsevier, AmsterdamGoogle Scholar
- Braconnier MF, Braekman JC, Daloze D (1985a) Synthesis of the racemic form of (Z)-1, 17-diaminooctadec-9-ene, an aliphatic diamine from Coccinellidae: determination of the absolute configuration of the (+)-naturally-occurring antipode. Bull Soc Chim Belg 94:605–613Google Scholar
- Braconnier MF, Braekman JC, Daloze D, Pasteels JM (1985b) (Z)-1, 17-diaminooctadec-9-ene, a novel aliphatic diamine from Coccinellidae. Cell Mol Life Sci 41:519–520CrossRefGoogle Scholar
- Brown MW (2003) Intraguild responses of aphid predators on apple to the invasion of an exotic species, Harmonia axyridis. Biocontrol 48:141–153CrossRefGoogle Scholar
- Brown MW, Miller SS (1998) Coccinellidae (Coleoptera) in apple orchards of eastern West Virginia and the impact of invasion by Harmonia axyridis. Entomol News 109:143–151Google Scholar
- Camarano S, González A, Rossini C (2009) Biparental endowment of endogenous defensive alkaloids in Epilachna paenulata. J Chem Ecol 35:1–7CrossRefPubMedGoogle Scholar
- Cottrell TE (2004) Suitability of exotic and native lady beetle eggs (Coleoptera: Coccinellidae) for development of lady beetle larvae. Biol Control 31:362–371CrossRefGoogle Scholar
- Cottrell TE (2005) Predation and cannibalism of lady beetle eggs by adult lady beetles. Biol Control 34:159–164CrossRefGoogle Scholar
- Cottrell TE (2007) Predation by adult and larval lady beetles (Coleoptera: Coccinellidae) on initial contact with lady beetle eggs. Environ Entomol 36:390–401CrossRefPubMedGoogle Scholar
- Daloze D, Braekman J-C, Pasteels JM (1995) Ladybird defense alkaloids: structural, chemotaxonomic and biosynthetic aspects (Col.: Coccinellidae). Chemoecology 5(6):173–183Google Scholar
- de Jong PW, Holloway GJ, Brakefield PM, de Vos H (1991) Chemical defense in ladybird beetles (Coccinellidae). II: amount of reflex fluid, the alkaloid adaline and individual variation in defence in 2-spot ladybirds (Adalia bipunctata). Chemoecology 2:15–19CrossRefGoogle Scholar
- Dixon AFG, Guo Y (1993) Egg and cluster size in ladybird beetles (Coleoptera: Coccinellidae): the direct and indirect effects of aphid abundance. Eur J Entomol 90:457–463Google Scholar
- Dussourd DE, Ubik K, Harvis CA, Resch J, Meinwald J (1988) Biparental defensive endowment of eggs with acquired plant alkaloid in the moth Utetheisa ornatrix. Proc Natl Acad Sci USA 85:5992–5996CrossRefPubMedGoogle Scholar
- Eisner T, Eisner M (1991) Unpalatability of the pyrrolizidine alkaloid-containing moth Utetheisa ornatrix, and its larva, to wolf spiders. Psyche 98:111–118CrossRefGoogle Scholar
- Eisner T, Eisner M, Rossini C, Iyengar VK (2000) Chemical defense against predation in an insect egg. Proc Natl Acad Sci USA 97:1634–1639CrossRefPubMedGoogle Scholar
- Fox LR (1975) Cannibalism in natural populations. Annu Rev Ecol Syst 6:87–106CrossRefGoogle Scholar
- González A, Rossini C, Eisner M, Eisner T (1999) Sexually transmitted chemical defense in a moth (Utetheisa ornatrix). Proc Natl Acad Sci USA 96:5570–5574CrossRefPubMedGoogle Scholar
- Hare JF, Eisner T (1993) Pyrrolizidine alkaloid deters ant predators of Utetheisa ornatrix eggs: effects of alkaloid concentration, oxidation state, and prior exposure of ants to alkaloid-laden prey. Oecologia 96:9–18CrossRefGoogle Scholar
- Hodek I (1973) Biology of Coccinellidae. Academia, PragueGoogle Scholar
- Holloway G, de Jong P, Brakefield P, de Vos H (1991) Chemical defence in ladybird beetles (Coccinellidae). I: distribution of coccinelline and individual variation in defence in 7-spot ladybirds (Coccinella septempunctata). Chemoecology 2:7–14CrossRefGoogle Scholar
- Kajita Y, Takano F, Yasuda H, Agarwala BK (2000) Effects of indigenous ladybird species (Coleoptera: Coccinellidae) on the survival of an exotic species in relation to prey abundance. Appl Entomol Zool 4:437–479Google Scholar
- King AG, Meinwald J (1996) Review of the defensive chemistry of coccinellids. Chem Rev 96:1105–1122CrossRefGoogle Scholar
- Koide T (1962) Observations on the feeding habit of the larva of Coccinella septempunctata bruckii Mulsant: the feeding behaviour and number of prey fed under different temperatures. Kontyû 30:236–241Google Scholar
- Laurent P, Braekman JC, Daloze D, Pasteels JM (2002) In vitro production of adaline and coccinelline, two defensive alkaloids from ladybird beetles (Coleoptera: Coccinellidae). Insect Biochem Mol Biol 32:1017–1023CrossRefPubMedGoogle Scholar
- Osawa N (1989) Sibling and non-sibling cannibalism by larvae of a lady beetle Harmonia axyridis Pallas (Coleoptera: Coccinellidae) in the field. Res Popul Ecol 31:153–160CrossRefGoogle Scholar
- Osawa N (1992a) A life table of the ladybird beetle Harmonia axyridis Pallas (Coleoptera: Coccinellidae) in relation to the aphid abundance. Jpn J Entomol 60:575–579Google Scholar
- Osawa N (1992b) Sibling cannibalism in the ladybird beetle Harmonia axyridis: fitness consequences for mother and offspring. Res Popul Ecol 34:45–55CrossRefGoogle Scholar
- Pasteels JM (2007) Chemical defense, offence and alliance in ants-aphids-ladybirds relationships. Popul Ecol 49:5–14CrossRefGoogle Scholar
- Polis GA (1981) The evolution and dynamics of intraspecific predation. Annu Rev Ecol Syst 12:225–251CrossRefGoogle Scholar
- Rieder JP, Newbold TAS, Sato S, Yasuda H, Evans EW (2008) Intra-guild predation and variation in egg defence between sympatric and allopatric populations of two species of ladybird beetles. Ecol Entomol 33:53–58Google Scholar
- Rosenheim JA (1998) Higher-order predators and the regulation of insect herbivore populations. Annu Rev Entomol 43:421–447CrossRefPubMedGoogle Scholar
- Rosenheim JA, Kaya HK, Ehler LE, Marois JJ, Jaffee BA (1995) Intraguild predation among biological-control agents: theory and evidence. Biol Control 5:303–335CrossRefGoogle Scholar
- Rosenthal GA, Berenbaum M (1992) Herbivores: their interactions with secondary plant metabolites. Academic, San DiegoGoogle Scholar
- SAS 9.1 (2002) SAS Institute, CaryGoogle Scholar
- Sato S, Dixon AFG (2004) Effect of intraguild predation on the survival and development of three species of aphidophagous ladybirds. Agric For Entomol 6:21–24CrossRefGoogle Scholar
- Sato S, Dixon AFG, Yasuda H (2003) Effect of emigration on cannibalism and intraguild predation in aphidophagous ladybirds. Ecol Entomol 28:628–633CrossRefGoogle Scholar
- Sato S, Jimbo R, Yasuda H, Dixon AFG (2008) Cost of being an intraguild predator in predatory ladybirds. Appl Entomol Zool 43:143–147CrossRefGoogle Scholar
- Schellhorn NA, Andow DA (1999) Cannibalism and interspecific predation: role of oviposition behavior. Ecol Appl 9:418–428Google Scholar
- Schroeder FC, González A, Meinwald J, Eisner T (2000) Chemical defense: bestowal of a nuptial alkaloidal garment by a male moth on its mate. Proc Natl Acad Sci USA 97:14406–14411CrossRefPubMedGoogle Scholar
- Sloggett JJ, Haynes KF, Obrycki JJ (2009a) Hidden costs to an invasive intraguild predator from chemically defended native prey. Oikos 118:1396–1404CrossRefGoogle Scholar
- Sloggett JJ, Obrycki JJ, Haynes KF (2009b) Identification and quantification of predation: novel use of gas chromatography-mass spectrometric analysis of prey alkaloid markers. Funct Ecol 23:416–426CrossRefGoogle Scholar
- Snyder WE, Hurd LE (1995) Egg-hatch phenology and intraguild predation between two mantid species. Oecologia 104:496–500CrossRefGoogle Scholar
- Stewart LA, Dixon AFG, Ruzicka Z, Iperti G (1991) Clutch and egg size in ladybird beetles. Entomophaga 36:329–333CrossRefGoogle Scholar
- Takahashi K (1989) Intra- and inter-specific predations of lady beetles in spring alfalfa fields. Jpn J Appl Entomol Zool 57:199–203Google Scholar
- Tursch B, Daloze D, Dupont M, Pasteels JM, Tricot M-C (1971a) A defensive alkaloid in a carnivorous beetle. Experientia 27:1380–1381CrossRefGoogle Scholar
- Tursch B, Daloze D, Dupont M, Hootele C, Kaisin M, Pasteels JM, Zimmermann D (1971b) Coccinelline, the defensive alkaloids of the beetle Coccinella septempunctata. Chimia 25:307–308Google Scholar
- Tursch B, Daloze D, Braekman JC, Hootele C, Cravador A, Losman D, Karlsson R (1974) Chemical ecology of arthropods. IX: structure and absolute configuration of hippodamine and convergine, two novel alkaloids from the American ladybug Hippodamia convergens (Coleoptera: Coccinellidae). Tetrahedron Lett 5:409–412CrossRefGoogle Scholar
- Yasuda H, Ohnuma N (1999) Effect of cannibalism and predation on the larval performance of two ladybird beetles. Entomol Exp Appl 93:63–67CrossRefGoogle Scholar
- Yasuda H, Shinya K (1997) Cannibalism and interspecific predation in two predatory ladybirds in relation to prey abundance in the field. Entomophaga 42:153–163CrossRefGoogle Scholar
- Yasuda H, Evans EW, Kajita Y, Urakawa K (2004) Asymmetric larval interactions between introduced and indigenous ladybirds in North America. Oecologia 141:722–731CrossRefPubMedGoogle Scholar