Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-10T09:49:39.309Z Has data issue: false hasContentIssue false
  • English
  • Français

Potential displacement of the native Tenuisvalvae notata by the invasive Cryptolaemus montrouzieri in South America suggested by differences in climate suitability

Published online by Cambridge University Press:  11 June 2021

Larissa F. Ferreira Open the ORCID record for Larissa F. Ferreira [Opens in a new window] ,
Christian S. A. Silva-Torres Open the ORCID record for Christian S. A. Silva-Torres [Opens in a new window] ,
Jorge B. Torres Open the ORCID record for Jorge B. Torres [Opens in a new window]  and
Robert C. Venette Open the ORCID record for Robert C. Venette [Opens in a new window]
Larissa F. Ferreira
Affiliation:
Universidade Federal Rural de Pernambuco (UFRPE), Departamento de Agronomia – Entomologia, Rua Dom Manoel de Medeiros, s/n, Dois Irmãos, 52171-900, Recife, PE, Brazil
Christian S. A. Silva-Torres*
Affiliation:
Universidade Federal Rural de Pernambuco (UFRPE), Departamento de Agronomia – Entomologia, Rua Dom Manoel de Medeiros, s/n, Dois Irmãos, 52171-900, Recife, PE, Brazil
Jorge B. Torres
Affiliation:
Universidade Federal Rural de Pernambuco (UFRPE), Departamento de Agronomia – Entomologia, Rua Dom Manoel de Medeiros, s/n, Dois Irmãos, 52171-900, Recife, PE, Brazil
Robert C. Venette
Affiliation:
Northern Research Station, USDA Forest Service, 1561 Lindig Street, St. Paul, MN55108-6125, USA
*
Author for correspondence: Christian S. A. Silva-Torres, Email: sherleyjbt@yahoo.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Tenuisvalvae notata (Mulsant) (Coccinellidae) is a predatory ladybird beetle native to South America. It specializes in mealybugs prey (Pseudococcidae), but relatively little is known about its ecology. In contrast, the ladybird beetle Cryptolaemus montrouzieri Mulsant (Coccinellidae) is indigenous to Australia and has been introduced to many countries worldwide including Brazil for biological control of mealybugs. The potential impacts of these introductions to native coccinellids have rarely been considered. The software CLIMEX estimated the climate suitability for both species as reflected in the Ecoclimatic Index (EI). Much of South America, Africa, and Australia can be considered climatically suitable for both species, but in most cases, the climate is considerably more favorable for C. montrouzieri than T. notata, especially in South America. The CLIMEX model also suggests seasonal differences in growth conditions (e.g. rainfall and temperature) that could affect the phenology of both species. These models suggest that few locations in South America would be expected to provide T. notata climatic refugia from C. montrouzieri. Although other ecological factors will also be important, such as prey availability, this analysis suggests a strong potential for displacement of a native coccinellid throughout most of its range as a consequence of the invasion by an alien competitor.

Keywords

Biological controlexotic speciesinterspecific interactionpredatorssoftware CLIMEX
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 111 , Issue 5 , October 2021 , pp. 605 - 615
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Allen, JC, Foltz, JL, Dixon, WN, Liebhold, AM, Colbert, JJ, Régnière, J, Gray, DR, Wilder, JW and Christie, I (1993) Will the gypsy moth become a pest in Florida? Florida Entomologist 76, 102–113.CrossRefGoogle Scholar
Babu, TR and Azam, KM (1987) Biology of Cryptolaemus montrouzieri Mulsant, (Coccinellidae: Coleoptera) in relation with temperature. Entomophaga 32, 381–386.CrossRefGoogle Scholar
Bahlai, CA, Colunga-Garcia, M, Gage, SH and Landis, DA (2015) The role of exotic lady beetles in the decline of native lady beetle populations: evidence from long-term monitoring. Biological Invasions 17, 1005–1024.CrossRefGoogle Scholar
Barahona-Segovia, RM, Grez, AA and Bozinovic, F (2016) Testing the hypothesis of greater eurythermality in invasive than in native ladybird species: from physiological performance to life-history strategies. Ecological Entomology 41, 182–191.CrossRefGoogle Scholar
Barbosa, PRR, Oliveira, MD, Giorgi, JA, Silva-Torres, CSA and Torres, JB (2014 a) Predatory behavior and life history of Tenuisvalvae notata (Coleoptera: Coccinellidae) under variable prey availability conditions. Florida Entomologist 97, 1026–1034.CrossRefGoogle Scholar
Barbosa, PRR, Oliveira, MD, Giorgi, JA, Oliveira, JEM and Torres, JB (2014 b) Suitability of two prey species for development, reproduction, and survival of Tenuisvalvae notata (Coleoptera: Coccinellidae). Annals of the Entomological Society of America 107, 1102–1109.CrossRefGoogle Scholar
Beaumont, LJ, Hughes, L and Poulsen, M (2005) Predicting species distributions: use of climatic parameters in BIOCLIM and its impact on predictions of species current and future distributions. Ecological Modelling 186, 250–269.CrossRefGoogle Scholar
Briere, JF and Pracros, P (1998) Comparison of temperature dependent growth models with the development of Lobesia botrana (Lepidoptera: Tortricidae). Environmental Entomology 27, 94–101.CrossRefGoogle Scholar
Caltagirone, LE and Doutt, RL (1989) The history of the Vedalia beetle importation into California and its impact on the development of biological control. Annual Review of Entomology 34, 1–16.CrossRefGoogle Scholar
Ceballo, FA, Walter, GH and Rochester, W (2010) The impact of climate on the biological control of citrus mealybug Planococcus citri (Risso) by the parasitoid Coccidoxenoides perminutus Girault as predicted by the climate-matching program CLIMEX. Philippine Agricultural Scientist 93, 317–328.Google Scholar
Chakupurakal, J, Markham, RH, Neuenschwander, P, Sakala, M, Malambo, C, Mulwanda, D, Banda, E, Chalabesa, A, Bird, T and Haug, T (1994) Biological control of the cassava mealybug, Phenacoccus manihoti (Homoptera: Pseudococcidae), in Zambia. Biological Control 4, 254–262.CrossRefGoogle Scholar
da Silva VC, P, Kaydan, MB, Silva-Torres, CSA and Torres, JB (2019) Mealybug species (Hemiptera: Coccomorpha: Pseudococcidae) on soursop and sugar apple (Annonaceae) in North-East Brazil, with description of a new species of Pseudococcus Westwood. Zootaxa 4604, 525–538.CrossRefGoogle ScholarPubMed
De Bach, P (1968) Control biológico de las plagas de insectos y malas hierbas. México: Compañía Editorial Continental, p. 927.Google Scholar
De Bach, P and Schlinger, EI (1964) Biological Control of Insect Pests and Weeds. New York: Reinhold, p. 844.Google Scholar
De Bortoli, SA, De Laurentis, VL, Gravena, AR, Vacari, AM and De Bortoli, CP (2014) Resposta funcional da joaninha Cryptolaemus predando cochonilha branca em diferentes temperaturas e substratos vegetais. Revista Caatinga 27, 63–71.Google Scholar
Diepenbrock, LM, Fothergill, K, Tindall, KV, Losey, JE, Smyth, RR and Finke, DL (2016) The influence of exotic lady beetle (Coleoptera: Coccinellidae) establishment on the species composition of the native lady beetle community in Missouri. Environmental Entomology 45, 855–864.CrossRefGoogle ScholarPubMed
Dixon, AFG (2000) Insect Predator-Prey Dynamics: Ladybird Beetles and Biological Control. Cambridge, UK: Cambridge University Press, p. 257.Google Scholar
Dreyer, BS, Neuenschwander, P, Baumgärtner, J and Dorn, S (1997 a) Trophic influences on survival, development and reproduction of Hyperaspis notata (Col., Coccinellidae). Journal of Applied Entomology 121, 249–256.CrossRefGoogle Scholar
Dreyer, BS, Neuenschwander, P, Bouyjou, B, Baumgärtner, J and Dorn, S (1997 b) The influence of temperature on the life table of Hyperaspis notata. Entomologia Experimentalis et Applicata 84, 85–92.CrossRefGoogle Scholar
Elliott, N, Kieckhefer, R and Kauffman, W (1996) Effects of an invading coccinellid on native coccinellids in an agricultural landscape. Oecologia 105, 537–544.CrossRefGoogle Scholar
Evans, EW and Toler, TR (2007) Aggregation of polyphagous predators in response to multiple prey species: ladybirds (Coleoptera: Coccinellidae) foraging in alfalfa. Population Ecology 49, 29–36.CrossRefGoogle Scholar
Evans, EW, Soares, AO and Yasuda, H (2011) Invasions by ladybugs, ladybirds, and other predatory beetles. BioControl 56, 597–611.CrossRefGoogle Scholar
Fan, Y, Groden, E and Drummond, FA (1992) Temperature-dependent development of Mexican bean beetle (Coleoptera: Coccinellidae) under constant and variable temperatures. Journal of Economic Entomology 85, 1762–1770.CrossRefGoogle Scholar
Fand, BB, Gautam, RD and Suroshe, SS (2010) Effect of developmental stage and density of Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae) on the predatory performance of four coccinellid predators. Journal of Biological Control 24, 110–115.Google Scholar
Ferreira, LF (2019) Resposta biológica e de predação de Tenuisvalvae notata (Mulsant) (Coleoptera: Coccinellidae) sob diferentes temperaturas e presas e uso do CLIMEX para prever sua distribuição geográfica (dissertation). Universidade Federal Rural de Pernambuco, Recife.Google Scholar
Ferreira, LF, Silva-Torres, CSA, Venette, RC and Torres, JB (2020) Temperature and prey assessment on the performance of the mealybug predator Tenuisvalvae notata (Coleoptera: Coccinellidae). Austral Entomology 59, 178–188.CrossRefGoogle Scholar
Follet, PA and Duan, JJ (2000) Nontarget Effects of Biological Control. New York: Springer Science Business Media, p. 315.CrossRefGoogle Scholar
Giorgi, JA, Barbosa, PRR, Oliveira, JEM and Torres, JB (2018) Prodilis hattie Gordon and Hanley (Coleoptera: Coccinellidae: Cephaloscymnini): new research on native natural predators of the false carmine cochineal, Dactylopius opuntiae (Cockerell) (Hemiptera: Dactylopiidae), in the Brazilian semiarid region. Coleopterists Bulletin 72, 562–565.CrossRefGoogle Scholar
Gutierrez, AP, Daane, KM, Ponti, L, Walton, VM and Ellis, CK (2008) Prospective evaluation of the biological control of vine mealybug: refuge effects and climate. Journal of Applied Biology 45, 524–536.Google Scholar
Harmon, JP, Stephens, E and Losey, J (2007) The decline of native coccinellids (Coleoptera: Coccinellidae) in the United States and Canada. Journal of Insect Conservation 11, 85–94.CrossRefGoogle Scholar
Herren, HR and Neuenschawander, P (1991) Biological control of cassava pests in Africa. Annual Review of Entomology 36, 257–283.CrossRefGoogle Scholar
Hodek, I and Michaud, JP (2008) Why is Coccinella septempunctata so successful? (A point-of-view). European Journal of Entomology 105, 1–12.CrossRefGoogle Scholar
Jalali, SK, Singh, SP and Biswas, SR (1999) Effect of temperature and female age on the development and progeny production of Cryptolaemus montrouzieri Mulsant (Coleoptera: Coccinellidae). Entomon 24, 293–296.Google Scholar
Jalali, MA, Mehrnejad, MR and Kontodimas, DC (2014) Temperature-dependent development of the five psyllophagous ladybird predators of Agonoscena pistaciae (Hemiptera: Psyllidae). Annals of the Entomological Society of America 107, 445–452.CrossRefGoogle Scholar
Kairo, MTK, Paraiso, O, Gautam, RD and Peterkin, DD (2013) Cryptolaemus montrouzieri (Mulsant) (Coccinellidae: Scymninae): a review of biology, ecology, and use in biological control with particular reference to potential impact on non-target organisms. CAB Reviews 8, 1–20.CrossRefGoogle Scholar
Kajita, Y and Evans, EW (2010) Relationships of body size, fecundity, and invasion success among predatory lady beetles (Coleoptera: Coccinellidae) inhabiting alfalfa fields. Annals of the Entomological Society of America 103, 750–756.CrossRefGoogle Scholar
Kim, H and Lee, JH (2008) Phenology simulation model of Scotinophara lurida (Hemiptera: Pentatomidae). Environmental Entomology 37, 660–669.CrossRefGoogle Scholar
Koch, RL, Venette, RC and Hutchison, WD (2006) Invasions by Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in the western hemisphere: implications for South America. Neotropical Entomology 35, 421–434.CrossRefGoogle ScholarPubMed
Löhr, B, Varela, AM and Santos, B (1990) Exploration for natural enemies of the cassava mealybug Phenacoccus manihoti (Homoptera: Pseudococcidae), in South America for the biological control of this pest introduced in Africa. Bulletin of Entomological Research 80, 417–425.CrossRefGoogle Scholar
Lopes, FSC (2016) Bioprospecção, identificação e manejo de cochonilhas-farinhentas (Hemiptera: Pseudococcidae) e insetos associados em agroecossistemas de videira no Submédio do vale do São Francisco (thesis). Universidade Federal Rural de Pernambuco, Recife.Google Scholar
MacLeod, A, Evans, HF and Baker, RHA (2002) An analysis of pest risk from an Asian longhorn beetle (Anoplophora glabripennis) to hardwood trees in the European community. Crop Protection 21, 635–645.CrossRefGoogle Scholar
Maes, S, Grégoire, JC and De Clercq, P (2015) Cold tolerance of the predatory ladybird Cryptolaemus montrouzieri. BioControl 60, 199–207.CrossRefGoogle Scholar
Mani, M and Krishnamoorthy, A (2008) Biological suppression of the mealybugs Planococcus citri (Risso), Ferrisia virgata (Cockerell) and Nipaecoccus viridis (Newstead) on pummel with Cryptolaemus montrouzieri Mulsant in India. Journal of Biological Control 22, 169–172.Google Scholar
Marques, CEM, Lima, MS, Melo, JWS, Barros, R and Paranhos, BAJ (2015) Evaluation of Ferrisia dasylirii (Cockerell) (Hemiptera: Pseudococcidae) and non-prey foods on the development, reproduction, and survival of Cryptolaemus montrouzieri Mulsant (Coleoptera: Coccinellidae). The Coleopterists Bulletin 69, 343–348.CrossRefGoogle Scholar
Moerkens, R, Gobin, B, Peusens, G, Helsen, H, Hilton, R, Dib, H, Suckling, DM and Leirs, H (2011) Optimizing biocontrol using phenological day degree models: the European earwig in pipfruit orchards. Agricultural and Forest Entomology 13, 301–312.CrossRefGoogle Scholar
Nietschke, BS, Magarey, RD, Borchert, DM, Calvin, DD and Jones, E (2007) A developmental database to support insect phenology models. Crop Protection 26, 1444–1448.CrossRefGoogle Scholar
Oliveira, CM (2020) Interações intra- e interespecíficas e tabela de fertilidade de Cryptolaemus montrouzieri Mulsant e Tenuisvalvae notata (Mulsant) (Coleoptera: Coccinellidae) (thesis). Universidade Federal Rural de Pernambuco, Recife.Google Scholar
Peronti, ALBG, Martinelli, NM, Alexandrino, JG, Marsaro-Júnior, AL, Penteado-Dias, AM and Almeida, LM (2016) Natural enemies associated with Maconellicoccus hirsutus (Hemiptera: Pseudococcidae) in the state of São Paulo, Brazil. Florida Entomologist 99, 21–25.CrossRefGoogle Scholar
Peterson, AT (2003) Predicting the geography of species’ invasions via ecological niche modelling. Quarterly Review of Biology 78, 419–433.CrossRefGoogle Scholar
Pluke, RWH, Escribano, A, Michaud, JP and Stansly, PA (2005) Potential impact of lady beetles on Diaphorina citri (Homoptera: Psyllidae) in Puerto Rico. Florida Entomologist 88, 123–128.CrossRefGoogle Scholar
Poutsma, J, Loomans, AJM, Aukema, B and Heijerman, T (2008) Predicting the potential geographical distribution of the harlequin ladybird, Harmonia axyridis, using the CLIMEX model. BioControl 53, 103–125.Google Scholar
Rehman, SA and Kumar, R (2018) Scenario of insect pests under changing climatic situations. International Journal of Chemical Studies 6, 77–81.Google Scholar
Roy, K, Jablonski, D and Valentine, JW (2002) Body size and invasion success in marine bivalves. Ecology Letters 5, 163–167.CrossRefGoogle Scholar
Sá, MGR, Oliveira, JEM, Costa, VA and Lopes, PRC (2020) Biodiversity of natural enemies of Pseudococcidae in the semiarid region of Brazil. Journal of Agricultural Science 12, 24.CrossRefGoogle Scholar
Saljoqi, AUR, Nasir, M, Khan, J, Ehsan-ul-Haq Asad, N and Raza, I (2014) The impact of temperature on biological and life table parameters of Cryptolaemus montrouzieri Mulsant (Coleoptera: Coccinellidae) fed on cotton mealy bug, Phenacoccus solenopsis Tinsley. Pakistan Journal of Zoology 46, 1591–1597.Google Scholar
Sanches, FN and Carvalho, RS (2010) Procedimentos para manejo da criação e multiplicação do predador exótico Cryptolaemus montrouzieri. Circular técnica 99, EMBRAPA Mandioca e Fruticultura, Cruz das Almas, BA, 5p.Google Scholar
Sconiers, WB and Eubanks, MD (2017) Not all droughts are created equal? The effects of stress severity on insect herbivore abundance. Arthropod-Plant Interact 11, 45–60.CrossRefGoogle Scholar
Sloggett, JJ (2017) Harmonia Axyridis (Coleoptera: Coccinellidae): Smelling the rat in Native Ladybird Declines. European Journal of Entomology 114: 455–461.CrossRefGoogle Scholar
Solangi, GS, Karamaouna, F, Kontodimas, D, Milonas, P, Lohar, MK, Abro, GH and Mahmood, R (2013) Effect of high temperatures on survival and longevity of the predator Cryptolaemus montrouzieri Mulsant. Phytoparasitica 41, 213–219.CrossRefGoogle Scholar
Sullivan, DJ, Castillo, JA and Bellotti, AC (1991) Comparative biology of six species of coccinellid beetles (Coleoptera: Coccinellidae) predaceous on the mealybug, Phenacoccus herreni (Homoptera: Pseudococcidae), a pest on cassava in Colombia, South America. Environmental Entomology 20, 685–689.CrossRefGoogle Scholar
Sutherst, RW and Maywald, G (2005) A climate model of the red imported fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae): implications for invasion of new regions, particularly Oceania. Environmental Entomology 34, 317–335.CrossRefGoogle Scholar
Sutherst, RW, Maywald, GF and Kriticos, DJ (2007) CLIMEX version 3: User's Guide. South Yarra: Hearne Scientific Software.Google Scholar
Torres, JB and Giorgi, JA (2018) Management of the false carmine cochineal Dactylopius opuntiae (Cockerell): Perspective from state of Pernambuco, Brazil. Phytoparasitica 46, 331–340.CrossRefGoogle Scholar
Turnipseed, RK, Ugine, TA and Losey, JE (2014) Effect of prey limitation on competitive interactions between a native lady beetle, Coccinella novemnotata, and an invasive lady beetle, Coccinella septempunctata (Coleoptera: Coccinellidae). Environmental Entomology 43, 969–976.CrossRefGoogle Scholar
Venette, RC (2017) Climate analyses to assess risks from invasive forest insects: simple matching to advanced models. Current Forestry Reports 3, 255–268.CrossRefGoogle Scholar
Wu, H, Zhang, Y, Liu, P, Xie, J, He, Y, Deng, C, De Clercq, P and Pang, H (2014) Cryptolaemus montrouzieri as a predator of the striped mealybug, Ferrisia virgata, reared on two hosts. Journal of Applied Entomology 138, 662–669.CrossRefGoogle Scholar
Wyckhuys, KAG, Koch, RL, Kula, RR and Heimpel, GE (2009) Potential exposure of a classical biological control agent of the soybean aphid, Aphis glycines, on non-target aphids in North America. Biological Invasions 11, 857–871.CrossRefGoogle Scholar