Abstract
Aphids are common herbivores in the strawberry crop that can reduce plant vigor and fruit quality and also transmit viruses. Aphid species prefer diverse plant organs, which represent particular habitats of different quality for aphids and for the development of natural enemies’ populations. Different habitat units (young leaves, mature leaves, buds, flowers) of strawberry were sampled fortnightly during all seasons. We identified seven aphid species, namely Chaetosiphon fragaefolii, Aphis gossypii, and Macrosiphum euphorbiae, the most abundant. During the autumn, C. fragaefolli and M. euphorbiae were scarce and A. gossypii was denser on mature leaves, while during summer M. euphorbiae was absent. During the winter, C. fragaefolii predominated on buds and young leaves, A. gossypii on flowers, and both species on mature leaves. During the spring, C. fragaefolii was even more abundant on buds, A. gossypii predominated on mature leaves, and the three species were equally abundant on flowers and young leaves. Parasitoids emerged from A. gossypii, M. euphorbiae and Myzus persicae, but not from C. fragaefolii. Three Aphidius and two Aphelinus species were recovered. All primary parasitoid species emerged from A. gossypii, and secondary parasitoids emerged only from this aphid. Aphis gossypii parasitism on mature leaves was markedly higher in winter and summer than in autumn and spring. Parasitism of A. gossypii was independent of its density, and the number of parasitized aphids was never higher than six. Our results contribute to define the most appropriate sample unit to estimate aphid density of different species and provide information about seasonal natural parasitism.
Similar content being viewed by others
References
Agresti A (2015) Foundations of linear and generalized linear models. Wiley, New Jersey, p 444
Ammar ED, Hall DG, Shatters RG Jr (2013) Stylet morphometrics and citrus leaf vein structure in relation to feeding behavior of the asian citrus psyllids Diaphorina citri, vector of citrus huanglongbing BACTERIUM. PLoS One 8(3):e59914. https://doi.org/10.1371/journal.pone.0059914
Beddington JR, Free CA, Lawton JH (1978) Characteristics of successful natural enemies in models of biological control of insect pests. Nature 273:513–519
Blackman RL, Eastop VF (2000) Aphids on the world’s crops. Wiley, Chichester, p 466
Bouçek Z, Subba Rao BR, Farooqi SI (1978) A preliminary review of Pteromalidae (Hymenoptera) of India and adjacent countries. Orient Insects 12:433–468
Brodeur J (2000) Host specificity and trophic relationships of hyperparasitoids. In: Hochberg ME, Ives AR (eds) Parasitoid population biology. Princeton University Press, Princeton, pp 139–183
Brodeur J, McNeil JN (1994) Life history of the aphid hyperparasitoid Asaphes vulgaris Walker (Pteromalidae): possible consequences on the efficacy of the primary parasitoid Aphidius nigripes Ashmead (Aphidiidae). Can Entomol 126:1493–1497
Byeon YW, Tuda M, Kim JH, Choi MY (2011) Functional responses of aphid parasitoids, Aphidius colemani (Hymenoptera: Braconidae) and Aphelinus asychis (Hymenoptera: Aphelinidae). Biocontrol Sci Techn 21:57–70
Cédola CV, Greco NM (2010) Presence of the aphid, Chaetosiphon fragaefolii, on strawberry in Argentina. J Insect Sci 10:9
Cédola CV, Gugole Ottaviano MF, Brentassi ME, Cingolani MF, Greco NM (2012) Negative interaction between twospotted spider mites and aphids mediated by feeding damage and honeydew. Bull Entomol Res 103:233–240
Costamagna AC, Landis DA (2006) Predators exert top-down control of soybean aphid across a gradient of agricultural management systems. Ecol Appl 16:1619–1628
De Conti BF, Bueno VHP, Sampaio MV, van Lenteren JC (2011) Development and survival of Aulacorthum solani, Macrosiphum euphorbiae and Uroleucon ambrosiae at six temperatures. Bull Insectol 64:63–68
De Santis L (1967) Catálogo de los Himenópteros Argentinos de la Serie Parasítica, incluyendo Bethyloidea. La Plata, Comisión de Investigación Científica de la provincia de Buenos Aires, p 155
Dixon AFG (1998) Aphid ecology. An optimization approach. Chapman and Hall, London, p 312
Eastop VF (1958) A study of Aphididae (Homoptera) of East Africa. Colonial Research Publication, London, p 126
Frewin AJ, Xue Y, Welsman JA, Broadbent AB, Schaafsma AW, Hallett RH (2010) Development and parasitism by Aphelinus certus (Hymenoptera: Aphelinidae), a parasitoid of Aphis glycines (Hemiptera: Aphididae). Environ Entomol 39:1570–1578
Ganyo KK, Kodjo Tounou A, Agboton C, Dannon EA, Pittendrigh BR, Tamò M (2012) Interaction between the aphid parasitoid Lysiphlebus testaceipes (Hymenoptera: Aphidiidae) and its hyperparasitoid Syrphophagus africanus (Hymenoptera: Encyrtidae). Int J Trop Insect Sci 32:45–55
Gardner SM, Dixon AFG (1985) Plant structure and the foraging success of Aphidius rhopalosiphi (Hymenoptera: Aphidiidae). Ecol Entomol 10:171–179
Gerardo NM, Altincicek B, Anselme C, Atamian H, Barribeau SM, de Vos M, Duncan EJ, Evans JD, Gabaldón T, Ghanim M, Heddi A, Kaloshian I, Latorre A, Moya A, Nakabachi A, Parker BJ, Pérez-Brocal V, Pignatelli M, Rahbe Y, Ramsey JS, Spragg CJ, Tamames J, Tamarit D, Tamborindeguy C, Vincent-Monegat C, Vilcinskas A (2010) Immunity and other defenses in pea aphids, Acyrthosiphon pisum. Genome Biol 11:R21
Gonzáles WL, Gianoli E, Niemeyer HM (2001) Plant quality vs. risk of parasitism: within-plant distribution and performance of the corn leaf aphid Rhopalosiphum maidis. Agr Forest Entomol 3:29–33
Gould GG, Jones CG, Rifleman P, Perez A, Coleman JS (2007) Variation in eastern cottonwood (Populus deltoides Bartr.) phloem sap content caused by leaf development may affect feeding site selection behavior of the aphid, Chaitophorous populicola Thomas (Homoptera: Aphididae). Environ Entomol 36:1212–1225
Greco NM, Liljesthröm GG, Gugole Ottaviano MF, Cluigt N, Cingolani MF, Zembo JC, Sánchez NE (2011) Pest management plan for the two-spotted spider mite, Tetranychus urticae, based on the natural occurrence of the predatory mite Neoseiulus californicus in strawberries. Int J Pest Manage 57:299–308
Grevstad FS, Klepetka BW (1992) The influence of plant architecture on the foraging efficiencies of a suite of ladybird beetles feeding on aphids. Oecologia 92:399–404
He X, Teulon DAJ, Wang Q (2006) Oviposition strategy of Aphidius ervi (Hymenoptera: Aphidiidae) in response to host density. N Z Plant Protect 59:195–201
Hosseini-Tabesh B, Sahragard A, Karimi-Malati A (2015) A laboratory and field condition comparison of life table parameters of Aphis gossypii Glover (Hemiptera: Aphididae). J Plant Protect Res 55:1–7
Iemma LGR, Tavares MT, Sousa-Silva CR (2016) First report of Syrphophagus aphidivorus (Hymenoptera: Encyrtidae) on Aphidius ervi in alfalfa crops in State of São Paulo, Brazil. Brazil J Biol 77:422–423
Isaacs R, Schilder A, Miles T, Longstroth M (2008) Blueberry aphid and blueberry shoestring virus. Extension Bulletin E-3050, East Lansing
Jansson RK, Smilowitz Z (1986) Influence of nitrogen on population parameters of potato insects: abundance, population growth, and within-plant distribution of the green peach aphid, Myzus persicae (Homoptera: Aphididae). Environ Entomol 15:49–55
Kareiva P, Sahakian R (1990) Tritrophic effects of a simple architectural mutation in pea plants. Nature 345:433–434
Killiny N (2017) Metabolite signature of the phloem sap of fourteen citrus varieties with different degrees of tolerance to Candidatus Liberibacter asiaticus. Physiol Mol Plant Pathol 97:20–29
Krczal H (1982) Investigations on the biology of the strawberry aphid (Chaetosiphon fragaefolii), the most important vector of strawberry viruses in West Germany. Acta Hortic 129:63–68
Kutner MH, Nachtsheim CJ, Neter J, Li W (2005) Applied linear statistical models. McGraw-Hill, Boston, p 1396
Lampert EP (1989) Seasonal abundance and within-plant distribution of aphids (Homoptera: Aphididae) on flue-cured tobacco. J Econ Entomol 82:114–118
Lester PJ, Holtzer TO (2002) Patch and prey utilization behaviors by Aphelinus albipodus and Diaeretiella rapae (Hymenoptera: Aphelinidae and Aphidiidae) on Russian wheat aphid (Homoptera: Aphididae). Biol Control 24:183–191
Liu SS (1985) Aspects of the numerical and functional respones of the aphid parasite, Aphidius sonchi, in the laboratory. Entomol Exp Appl 37:247–256
Lyman Ott R, Longnecker M (2010) An introduction to statistical methods and data analysis. Brooks/Cole Cengage Learning, Belmont, p 1273
Mace KC, Mills NJ (2016) Nitrogen-mediated interaction: a walnut-aphid-parasitoid system. Environ Entomol 45:891–896
Mackauer M (1983) Quantitative assessment of Aphidius smithi (Hymenoptera: Aphidiidae): fecundity, intrinsic rate of increase, and functional response. Can Entomol 115:399–415
Martin RR, Tzanetakis IE (2006) Characterization and recent advances in detection of strawberry viruses. Plant Dis 90:384–396
Martin RR, Tzanetakis IE (2015) Control of virus diseases of berry crops. Adv Virus Res 91:271–309
Merritt SZ (1996) Within-plant variation in concentrations of amino acids, sugar, and sinigrin in phloem sap of black mustard, Brassica nigra (L.) Koch (Cruciferae). J Chem Ecol 22:1133–1145
Morris WF (1992) The effects of natural enemies, competition, and host plant water availability on an aphid population. Oecologia 90:359–365
Myers SW, Gratton C (2006) Influence of potassium fertility on soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), population dynamics at a field and regional scale. Environ Entomol 35:219–227
Nieto Nafría JM (1976) Los pulgones (Hom: Aphidinea) de las plantas cultivadas en España, I: rosales, fresales, frambuesos. Boletín de Sanidad Vegetal Plagas 2:97–112
Perrenoud S (1990) Potassium and plant health. Switzerland, International Potash Institute, p 365
Petitt FL, Loader CA, Schon MK (1994) Reduction of nitrogen concentration in the hydroponic solution on population growth rate of the aphids (Homoptera: Aphididae) Aphis gossypii on cucumber and Myzus persicae on pepper. Environ Entomol 23:930–936
Price PW (1988) Inversely density-dependent parasitism: the role of plant refuges for hosts. J Anim Ecol 57:89–96
Price PW, Bouton CE, Gross P, McPherson BA, Thompson JN, Weis AE (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu Rev Ecol Syst 11:41–65
Rabasse JM, Trouvé C, Geria AM, Quignou A (2001) Aphid pests of strawberry crops and their parasitoids in France. Mededelingen (Rijksuniversiteit te Gent. Fakulteit van de Landbouwkundige en Toegepaste Biologische Wetenschappen) 66:293–301
Raupp MJ, Denno RF (1983) Leaf age as a predictor of herbivore distribution and abudance. In: Denno RF, McClure MS (eds) Variable plants and herbivores in natural and managed systems. Academic Press, New York, pp 91–124
Reed DK, Kindler SD, Springer TL (1992) Interactions of Russian wheat aphid, a hymenopterous parasitoid and resistant and susceptible slender wheatgrasses. Entomol Exp Appl 64:239–246
Remaudière G, Remaudière M (1997) Catalogue des aphididae du monde/catalogue of the world’s aphididae (Homoptera Aphidoidea). INRA Editions (Collection Techniques et Pratiques), Paris, p 475
Rondon SI, Cantliffe DJ (2004) Chaetosiphon fragaefolii (Homoptera: Aphididae): A potential new pest in Florida? Fla Entomol 87:612–615
Rondon SI, Cantliffe DJ, Price JF (2005) Population dynamics of the cotton aphid, Aphis gossypii (Homoptera: Aphididae), on strawberries grown under protected structure. Fla Entomol 88:152–158
Rosenthal GA, Berenbaum MR (1992) Herbivores: their interactions with secondary plant metabolites. Academic Press, San Diego, p 452
Servicio Meteorológico Nacional Argentina (2017) Boletín agrometeorológico decádico. http://www.smn.gov.ar/?mod=agroandid=3 Accessed 13 June 2017
Simbaqueda R, Serna F, Posada-Flórez FJ (2014) Curaduría, morfología e identificación de áfidos (Hemiptera: Aphididae) del Museo Entomológico UNAB. Primera aproximación. Boletín Científico Centro de Museos Museo de Historia Natural 18:222–246
Starý P, Gerding M, Norambuena H (1991) Identificación de parasitoides de áfidos de los cereales. Instituto de Investigaciones Agropecuarias, INIA, Quilamapu, Chillán, Chile, p 8
Thompson JR, Wetzel S, Klerks MM, Vašková D, Schoen CD, Špak J, Jelkmann W (2003) Multiplex RT-PCR detection of four aphid-borne strawberry viruses in Fragaria spp. in combination with a plant mRNA specific internal control. J Virol Methods 111:85–93
Trumble JT, Oatman ER (1984) Dispersion analyses and resource utilization of aphid parasitoids in a non-depletable environment. Res Popul Ecol 26:124–133
van Lenteren JC (2012) Internet book of biological control, version 6. The Netherlands, IOBC Global, p 182
Whitham TG (1980) The theory of habitat selection: examined and extended using pemphigus aphids. Am Nat 115:449–466
Xiao H, Huang DW (2000) A taxonomic study on Asaphes (Hymenoptera: Pteromalidae) from China, with descriptions of four new species. Entomologia Sinica 7:193–202
Zamani A, Talebi A, Fathipour Y, Baniameri V (2006) Temperature-dependent functional response of two aphid parasitoids, Aphidius colemani and Aphidius matricariae (Hymenoptera: Aphidiidae), on the cotton aphid. J Pest Sci 79:183–188
Zumoffen L, Rodriguez M, Gerding M, Salto CE, Salvo A (2015) Plantas, áífidos y parasitoides: interacciones tróficas en agroecosistemas de la provincia de Santa Fe, Argentina y clave para la identificación de los Aphidiinae y Aphelinidae (Hymenoptera) conocidos de la región. Revista de la Sociedad Entomológica Argentina 74:133–144
Acknowledgements
This study was supported by the Agencia Nacional de Promoción Científica y Tecnológica de Argentina (the National Agency for Promotion of Science and Technology of Argentina), Grant PICT 2012–1624, Grant PICT 2015-1427 and the Programa de Incentivos a Docentes-Investigadores del Ministerio de Cultura y Educación de la Nación de Argentina (Program of Incentives for Professors-Researchers of the National Ministry of Culture and Education of Argentina) grant 11/N712. We would like to thank Graciela Minardi for the statistical analyses, and Francisco Rubén La Rossa, Albano Giudici and Juan José Martínez for species identity confirmation.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Cingolani, M.F., Greco, N. Spatio-temporal variation of strawberry aphid populations and their parasitoids. Appl Entomol Zool 53, 205–214 (2018). https://doi.org/10.1007/s13355-018-0544-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13355-018-0544-1