Skip to main content
Log in

Analysis of biological traits of Anagyrus cachamai and Anagyrus lapachosus to assess their potential as biological control candidate agents against Harrisia cactus mealybug pest in Puerto Rico

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

The Harrisia cactus mealybug (HCM), Hypogeococcus sp. (Hemiptera: Pseudococcidae), is devastating native cacti in Puerto Rico and threatens cacti throughout the Caribbean, Mexico, Central and North America. In South America, its native area, various natural enemies keep HCM under control. Two South American parasitoids, Anagyrus cachamai Triapitsyn, Logarzo & Aguirre and A. lapachosus Triapitsyn, Aguirre & Logarzo (Hymenoptera: Encyrtidae), were selected as potential biological control agents. Rearing protocol to conduct mass production, specificity studies and several aspects of the biology of these species were studied under laboratory conditions in Argentina. Anagyrus cachamai and A. lapachosus successfully attacked early instars of Hypogeococcus sp., have a balanced sex ratio, exhibited a development time synchronized with that of the host, and presented differences in their reproductive biology and development time. All these characteristics make these parasitoids promising candidates for introduction as biological control agents against the HCM pest in Puerto Rico.

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
Fig. 5

Similar content being viewed by others

References

  • Aguirre M, Diaz-Soltero H, Claps L, Saracho Bottero A, Triapitsyn S, Hasson E, Logarzo G (2016) Studies on the biology of Hypogeococcus pungens (sensu stricto) (Hemiptera: Pseudococcidae) in Argentina to aid the identification of the mealybug pest of Cactaceae in Puerto Rico. J Insect Sci 58:1–7

    Google Scholar 

  • Althoff DM (2003) Does parasitoid attack strategy influence host specificity? A test with new world braconids. Ecol Entomol 28:500–502

    Article  Google Scholar 

  • Avidov Z, Rossler Y, Rosen D (1967) Studies on an Israel strain of Anagyrus pseudococci (Girault) (Hymenoptera: Encyrtidae). II. Some biological aspects. Entomophaga 12:111–118

    Article  Google Scholar 

  • Beddington J, Free C, Lawton J (1978) Characteristics of successful natural enemies in models of biological control of insects. Nature 273:513–519

    Article  CAS  PubMed  Google Scholar 

  • Berndt L, Wratten S (2005) Effects of alyssum flowers on the longevity, fecundity, and sex ratio of the leafroller parasitoid Dolichogenidea tasmanica. Biol Control 32:65–69

    Article  Google Scholar 

  • Blumberg D (1997) Parasitoid encapsulation as a defense mechanism in the Coccoidea (Homoptera) and its importance in biological control. Biol Control 8:225–236

    Article  Google Scholar 

  • Blumberg D, van Driesche R (2001) Encapsulation rates of three Encyrtid parasitoids by three mealybug species (Homoptera: Pseudococcidae) found commonly as pests in commercial greenhouses. Biol Control 22:191–199

    Article  Google Scholar 

  • Blumberg D, Klein M, Mendel Z (1995) Response by encapsulation of four mealybug species (Homoptera, Pseudococcidae) to parasitization by Anagyrus pseudococci. Phytoparasitica 23:157–163

    Article  Google Scholar 

  • Carrera-Martínez R, Aponte-Díaz L, Ruiz-Arocho J, Jenkins D (2015) Symptomatology of infestation by Hypogeococcus pungens: contrasts between host species. Haseltonia 21:14–18

    Article  Google Scholar 

  • Charnov E (1979) The genetical evolution of patterns of sexuality: Darwinian fitness. Am Nat 113:465–480

    Article  Google Scholar 

  • Charnov E (1982) The theory of sex allocation. Monographs in population biology. Princeton University Press, Princeton

    Google Scholar 

  • Charnov E, Los-den Hartogh R, Jones W, van den Assem J (1981) Sex ratio evolution in a variable environment. Nature 289:27–33

    Article  CAS  PubMed  Google Scholar 

  • Chow A, Heinz K (2006) Control of Liriomyza langei on chrysanthemum by Diglyphus isaea produced with a standard or modified parasitoid rearing technique. J Appl Entomol 130:113–121

    Article  Google Scholar 

  • Coppel H, Mertins J (1977) Biological insect pest suppression. Springer, New York

    Book  Google Scholar 

  • Cross A, Moore D (1992) Developmental studies on Anagyrus mangicola (Hymenoptera: Encyrtidae), a parasitoid of the mealybug Rastrococcus invadens (Homoptera: Pseudococcidae). Bull Entomol Res 82:307–312

    Article  Google Scholar 

  • Deas J, Hunter M (2014) Egg and time limitation mediate an egg protection strategy. J Evol Biol 27:920–928

    Article  CAS  PubMed  Google Scholar 

  • Doutt R, DeBach P (1964) Some biological control concepts and questions. In: DeBach P (ed) Biological control of insect pests and weeds. Chapman and Hall Ltd, London, pp 118–142

    Google Scholar 

  • Ehler L (1995) Biological control of obscure scale (Homoptera: Diaspididae) in California: an experimental approach. Environ Entomol 24:779–795

    Article  Google Scholar 

  • Gibb H, Hilszczański J, Hjältén J, Danell K, Ball JP, Pettersson RB, Alinvi O (2008) Responses of parasitoids to saproxylic hosts and habitat: a multi-scale study using experimental logs. Oecologia 155:63–74

    Article  CAS  PubMed  Google Scholar 

  • Godfray H (1994) Parasitoids: behavioral and evolutionary ecology. Princeton University Press Books, Princeton

    Google Scholar 

  • Granara de Willink M (1981) Nueva especie de Hypogeococcus Rau de Tucumán, República Argentina (Homoptera: Pseudococcidae). Neotrópica 27:61–65

    Google Scholar 

  • Harvey J, Kadash K, Strand M (2000) Differences in larval feeding behavior correlate with altered developmental strategies in two parasitic wasps: implications for the size-fitness hypothesis. Oikos 88:621–629

    Article  Google Scholar 

  • Harvey J, Harvey I, Thompson D (2001) Lifetime reproductive success in the solitary endoparasitoid, Venturia canescens. J Insect Behav 14:573–593

    Article  Google Scholar 

  • Haye T, Broadbent A, Whistlecraft J, Kuhlmann U (2005) Comparative analysis of the reproductive biology of two Peristenus species (Hymenoptera: Braconidae), biological control agents of Lygus plant bugs (Hemiptera: Miridae). Biol Control 32:442–449

    Article  Google Scholar 

  • Heimpel G, Rosenheim J (1998) Egg limitation in parasitoids: a review of the evidence and a case study. Biol Control 11:160–168

    Article  Google Scholar 

  • Hilszczańsk J, Gibb H, Hjältén J, Atlegrim O, Johansson T, Pettersson R, Ball J, Danell K (2005) Parasitoids (Hymenoptera, Ichneumonoidea) of saproxylic beetles are affected by forest successional stage and dead wood characteristics in boreal spruce forest. Biol Conserv 126:456–464

    Article  Google Scholar 

  • Hoelmer K, Kirk A (2005) Selecting arthropod biological control agents against arthropod pests: can the science be improved to decrease the risk of realizing ineffective agents? Biol Control 34:255–264

    Article  Google Scholar 

  • Huffaker CB, Messenger PS, DeBach P (1971) The natural enemy component in natural control and the theory of biological control. In: Huffaker CB (ed) Biological control. Plenum Press, New York, pp 16–67

    Google Scholar 

  • Huffaker CB, Luck RF, Messenger PS (1977) The ecological basis of biological control. Proceeding of the XV international congress of entomology, Washington DC, pp 560–586

    Google Scholar 

  • Jervis M, Copland M (1996) The life cycle. In: Jervis M, Kidd N (eds) Insect natural enemies: practical approaches to their study and evaluation. Chapman and Hall, London, pp 63–161

    Chapter  Google Scholar 

  • Jervis M, Ferns P (2004) The timing of egg maturation in insects: ovigeny index and initial egg load as measures of fitness and of resource allocation. Oikos 107:449–461

    Article  Google Scholar 

  • Jervis M, Heimpel G, Ferns P, Harvey J, Kidd N (2001) Life-history strategies in parasitoid wasps: a comparative analysis of ‘ovigeny’. J Anim Ecol 70:442–458

    Article  Google Scholar 

  • Kaplan E, Meier P (1958) Nonparametric estimation from incomplete observations. J Am Stat Assoc 53:457–481

    Article  Google Scholar 

  • Kapranas A, Tena A (2015) Encyrtid parasitoids of soft scale insects: biology, behavior, and their use in biological control. Annu Rev Entomol 60:195–211

    Article  CAS  PubMed  Google Scholar 

  • Kidd N, Jervis M (2007) Population dynamics. In: Jervis M (ed) Insects as natural enemies: a practical perspective. Springer, Dordrecht, pp 435–524

    Chapter  Google Scholar 

  • King B (1993) Sex ratio manipulation by parasitoid wasps. In: Wrench D, Ebbert M (eds) Evolution and diversity of sex ratio in insects and mites. Chapman and Hall, New York, pp 418–441

    Chapter  Google Scholar 

  • Lane S, Mills N, Getz W (1999) The effects of parasitoid fecundity and host taxon on the biological control of insect pests: the relationship between theory and data. Ecol Entomol 24:181–190

    Article  Google Scholar 

  • Lebrija-Trejos E, Pérez-García E, Meave J, Poorter L, Bongers F (2011) Environmental changes during secondary succession in a tropical dry forest in Mexico. J Trop Ecol 27:477–489

    Article  Google Scholar 

  • Martínez-Martínez L, Bernal J (2002) Ephestia kuehniella Zeller as a factitious host for Telenomus remus Nixon: host acceptance and suitability. J Entomol Sci 37:10–26

    Article  Google Scholar 

  • Mason P, De Clercq P, Heimpel G, Kenis M (2008) Attributes of biological control agents against arthropods: what are we looking for? In: Mason P, Gillespie D, Vincent C (eds) Proceedings of the III international symposium on biological control of arthropods. Morgantown: USDA Forest Service, pp 385-392

  • Nieves E (2013) Evaluación del parasitoide, Pseudapanteles dignus (Hymenoptera: Braconidae) como agente de control biológico de la “polilla del tomate”, Tuta absoluta (Lepidoptera: Gelechiidae). PhD thesis, Universidad Nacional de La Plata (UNLP), Argentina, 129 pp

  • Ode P, Hardy I (2008) Parasitoid sex ratios and biological control. In: Wajnberg E, Bernstein C, van Alphen J (eds) Behavioral ecology of insect parasitoids: from theoretical approaches to field applications. Blackwell Publishing, Oxford, pp 253–291

    Chapter  Google Scholar 

  • Odebiyi J, Bokonon-Ganta A (1986) Biology of Epidinocarsis (= Apoanagyrus) lopezi (Hymenoptera: Encyrtidae) an exotic parasitoid of cassava mealybug, Phenacoccus manihoti (Homoptera: Pseudococcidae) in Nigeria. Entomophaga 31:251–260

    Article  Google Scholar 

  • Patil N, Baker P, Pollard G (1993) Life histories of Psyllaephagus yaseeni (Hymenoptera: Encyrtidae) and Tamarixia leucaenae (Hymenoptera: Eulophidae), parasitoids of the leucaena psyllid, Heteropsylla cubana. Entomophaga 38:565–577

    Article  Google Scholar 

  • Pennacchio F, Strand M (2006) Evolution of developmental strategies in parasitic Hymenoptera. Annu Rev Entomol 51:233–258

    Article  CAS  PubMed  Google Scholar 

  • Pérez SYCM, Zimmermann H, Golubov J, Arias S (2006) El piojo harinoso otro cactófago invasor amenaza nuestra biodiversidad desde Estados Unidos y las Islas del Caribe. CONABIO. Biodiversitas 66:10–11

    Google Scholar 

  • Pexton J, Mayhew P (2002) Siblicide and life history evolution in parasitoids. Behav Ecol 13:690–695

    Article  Google Scholar 

  • Pitcairn M, Gutierrez A (1992) Influence of adult size and age on the fecundity and longevity of Tetrastichus incertus (Hymenoptera: Eulophidae). Ann Entomol Soc Am 85:53–57

    Article  Google Scholar 

  • Quesada M, Sanchez-Azofeifa G, Álvarez-Añorve M, Stoner K, Avila-Cabadilla L, Calvo-Alvarado J, Castillo A, Espírito-Santo M, Fagundes M, Fernandes G, Gamon J, Lopezaraiza-Mikel M, Lawrence D, Morellato L, Powers J, Neves F, Rosas-Guerrero V, Sáyago R, Sánchez-Montoya G (2009) Succession and management of tropical dry forests in the Americas: review and new perspectives. For Ecol Manage 258:1014–1024

    Article  Google Scholar 

  • R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.r-project.org

  • Rosenheim J, Heimpel G, Mangel M (2000) Egg maturation, egg resorption and the costliness of transient egg limitation in insects. Proc R Soc Lond B Biol Sci 267:1565–1573

    Article  CAS  Google Scholar 

  • Sagarra L, Vincent C, Stewart R (2000) Fecundity and survival of Anagyrus kamali (Hymenoptera: Encyrtidae) under different feeding and storage temperature conditions. Eur J Entomol 97:177–181

    Article  Google Scholar 

  • Sagarra L, Vincent C, Stewart R (2001) Suitability of nine mealybug species (Homoptera: Pseudococcidae) as hosts for the parasitoid Anagrus kamali (Hymenoptera: Encyrtidae). Fla Entomol 84:112–116

    Article  Google Scholar 

  • Sandlan K (1979) Host feeding and its effects on the physiology and behaviour of the ichneumonid parasite Coccygomimus turionellae. Physiol Entomol 4:383–392

    Article  Google Scholar 

  • Segarra-Carmona AE, Ramírez-Lluch A, Cabrera-Asencio I, Jiménez-López AN (2010) First report of a new invasive mealybug, the Harrisia cactus mealybug Hypogeococcus pungens (Hemiptera: Pseudococcidae). J Agr U Puerto Rico 94:183–187

    Google Scholar 

  • Stiling P (1990) Calculating the establishment rates of parasitoids in classical biological control. Am Entomol 36:225–230

    Article  Google Scholar 

  • Stiling P (1993) Why do natural enemies fail in classical biological control programs? Am Entomol 1:31–37

    Article  Google Scholar 

  • Suma P, Mansour R, La Torre I, Ali Bugila A, Mendel Z, Franco J (2012) Developmental time, longevity, reproductive capacity and sex ratio of the mealybug parasitoid Anagyrus sp. nr. pseudococci (Girault) (Hymenoptera: Encyrtidae). Biocontrol Sci Technol 22:737–745

    Article  Google Scholar 

  • Therneau T (2015) survival: A package for survival analysis in S. version 2.38. https://CRAN.R-project.org/package=survival

  • Triapitsyn S, Logarzo G, Aguirre M, Aquino D (2014) Two new species of Anagyrus (Hymenoptera: Encyrtidae) from Argentina, parasitoids of Hypogeococcus spp. (Hemiptera: Pseudococcidae), with taxonomic notes on some congeneric taxa. Zootaxa 3861:201–230

    Article  PubMed  Google Scholar 

  • Triapitsyn S, Aguirre M, Logarzo G (2016) A new Anagyrus (Hymenoptera: Encyrtidae) from Argentina, parasitoid of Hypogeococcus sp. (Hemiptera: Pseudococcidae) on Harrisia pomanensis (Cactaceae). Zootaxa 4114:590–594

    Article  PubMed  Google Scholar 

  • Triapitsyn SV, Aguirre MB, Logarzo GA, Hight SD, Ciomperlik MA, Rugman-Jones PF, Verle Rodrigues JC (2018) Complex of primary and secondary parasitoids (Hymenoptera: Encyrtidae and Signiphoridae) of Hypogeoccoccus spp. mealybugs (Hemiptera: Pseudococcidae) in the New World. Fla Entomol 101:411–434

    Article  Google Scholar 

  • van Baalen M (2002) The evolution of parasitoid egg load. In: Hochberg M, Ives A (eds) Parasitoid population biology. Princeton University Press, Princeton, pp 103–120

    Google Scholar 

  • van Driesche R (2004) Assessing host ranges for parasitoids and predators used for classical biological control: a guide to best practice. Forest Health Technology Enterprise Team, USDA-Forest Service, Morgantown

    Google Scholar 

  • van Driesche R, Bellotti A, Herrera C, Castillo J (1986) Encapsulation rates of two encyrtid parasitoids by two Phenacoccus spp. of cassava mealybugs in Colombia. Entomol Exp App 42:79–82

    Article  Google Scholar 

  • Waage J (1990) Ecological theory and the selection of biological control agents. In: Mackauer M, Ehler L, Roland J (eds) Critical issues in biological control. Intercept, Andover, pp 135–157

    Google Scholar 

  • Waage J, Hassell M (1982) Parasitoids as biological control agents—a fundamental approach. Parasitology 84:241–268

    Article  Google Scholar 

  • Wäckers F, van Rijn P, Heimpel G (2008) Honeydew as a food source for natural enemies: making the best of a bad meal? Biol Control 45:176–184

    Article  Google Scholar 

  • Williams D, Granara de Willink M (1992) Mealybugs of Central and South America. CAB International, London

    Google Scholar 

  • Wogin M, Gillespie D, Haye T, Roitberg B (2012) Female-biased sex ratio shifts in a solitary parasitoid and their effects on virginity, population dynamics, and biological control. Entomol Exp Appl 146:165–176

    Article  Google Scholar 

  • Yano E (2006) Ecological considerations for biological control of aphids in protected culture. Popul Ecol 48:333–339

    Article  Google Scholar 

  • Zimmermann H, Pérez SYCM (2010) La amenaza de los piojos harinosos Hypogeococcus pungens e Hypogeococcus festerianus (Hemiptera: Pseudococcidae) a las cactáceas mexicanas y del Caribe. Cact Succ J 55:4–17

    Google Scholar 

Download references

Acknowledgements

We thank Mariel Guala (FuEDEI) for her excellent technical assistance, Nadia Jiménez (FuEDEI) for her help with statistical analysis, and Arabella Peard Bugliani (FuEDEI) for her thoughtful comments on the manuscript. This study was supported by the USDA-APHIS Invasive Species Coordination Program from 2014 to 2016 (APH-HQ-16-0181), and USDA-APHIS Farm Bill funding for Fiscal Year 2017 (Farm Bill FY 17: 6.0385.01).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to María B. Aguirre.

Ethics declarations

Conflict of interest

All authors declare that there are no conflicts of interests.

Ethical approval

This article does not contain any studies with human participants or animals (vertebrates) performed by any of the authors.

Additional information

Handling Editor: Stefano Colazza

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Aguirre, M.B., Logarzo, G.A., Triapitsyn, S.V. et al. Analysis of biological traits of Anagyrus cachamai and Anagyrus lapachosus to assess their potential as biological control candidate agents against Harrisia cactus mealybug pest in Puerto Rico. BioControl 64, 539–551 (2019). https://doi.org/10.1007/s10526-019-09956-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-019-09956-y

Keywords

Navigation