Biology and Management of Pest Diabrotica Species in South America
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insects Review Biology and Management of Pest Diabrotica Species in South America Guillermo Cabrera Walsh 1,* , Crébio J. Ávila 2, Nora Cabrera 3, Dori E. Nava 4, Alexandre de Sene Pinto 5 and Donald C. Weber 6 1 ARS-SABCL/FuEDEI (Foundation for the Study of Invasive Species), Hurlingham B1686EFA, Argentina 2 EMBRAPA Agropecuaria Oeste, Dourados, Mato Grosso de Sul Caixa-postal 449, Brazil; [email protected] 3 Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, La Plata B1900FWA, Argentina; [email protected] 4 EMBRAPA Clima Temperado, Pelotas, Rio Grande do Sul Caixa-Postal 403, Brazil; [email protected] 5 Centro Universitario Moura Lacerda, Ribeirão Preto, São Paulo 14076-510, Brazil; [email protected] 6 USDA-ARS Invasive Insect Biocontrol & Behavior Laboratory, Baltimore Avenue, Beltsville, MD 10300, USA; [email protected] * Correspondence: [email protected]; Tel.: +54-11-4452-4838 Received: 27 May 2020; Accepted: 4 July 2020; Published: 8 July 2020 Abstract: The genus Diabrotica has over 400 described species, the majority of them neotropical. However, only three species of neotropical Diabrotica are considered agricultural pests: D. speciosa, D. balteata, and D. viridula. D. speciosa and D. balteata are polyphagous both as adults and during the larval stage. D. viridula are stenophagous during the larval stage, feeding essentially on maize roots, and polyphagous as adults. The larvae of the three species are pests on maize, but D. speciosa larvae also feed on potatoes and peanuts, while D. balteata larvae feed on beans and peanuts. None of these species express a winter/dry season egg diapause, displaying instead several continuous, latitude-mediated generations per year. This hinders the use of crop rotation as a management tool, although early planting can help in the temperate regions of the distribution of D. speciosa. The parasitoids of adults, Celatoria bosqi and Centistes gasseni, do not exert much control on Diabrotica populations, or show potential for inundative biocontrol plans. Management options are limited to insecticide applications and Bt genetically modified (GM) maize. Other techniques that show promise are products using Beauveria bassiana and Heterorhabditis bacteriophora, semiochemical attractants for monitoring purposes or as toxic baits, and plant resistance. Keywords: Diabrotica speciosa; Diabrotica balteata; Diabrotica viridula; rootworm management; maize pests; cucurbitacins; semiochemicals 1. General Biology of South American Pest Diabrotica The genus Diabrotica has over 400 described species [1], the majority of them neotropical, but only 7 species, plus six subspecies, are considered agricultural pests in the Americas [2]. Of these, only three species are considered agricultural pests in South America: D. speciosa (Germar) with subspecies speciosa and vigens, D. balteata (LeConte), and D. viridula (F.) (Figure1). The genus Diabrotica is divided into three species groups: virgifera, fucata, and signifera [3,4]. However, studies on South American virgifera group species suggest that these groups are not as well defined as previously thought [5,6]. D. speciosa and D. balteata are in the fucata group, which is the group with the largest number of species. The species in this group that have been studied are polyphagous both as adults and during the larval stage. Another characteristic of the North American pest Diabrotica of the fucata species group is that Insects 2020, 11, 421; doi:10.3390/insects11070421 www.mdpi.com/journal/insects InsectsInsects2020 2020, ,11 11,, 421 x FOR PEER REVIEW 2 2of of 19 18 as adults and during the larval stage. Another characteristic of the North American pest Diabrotica of theythe fucata overwinter species as group adults is and that lack they resistant overwinter stages as to adults deal withand lack harsh resistant climatic stages conditions to deal [2 ].withD. viridulaharsh isclimatic in the conditionsvirgifera group, [2]. D. the viridula same is clade in the of virgifera the Northern, group, the Western, same clade and of Mexican the Northern, corn rootworms Western, (Diabroticaand Mexican barberi corn, Diabrotica rootworms virgifera (Diabrotica virgifera barberi,, and DiabroticaDiabrotica virgifera virgifera virgifera zeae, respectively)., and Diabrotica The virgifera larvae ofzeae the, respectively). North American The larvae species of in the the Northvirgifera Americangroup feedspecies exclusively in the virgifera on Poaceae group feed [7], although exclusively the hoston Poaceae range has [7], beenalthough observed the host or range tested has for been only ob a fewserved of theor tested species for in only the a group few of [ 8the]. Thespecies North in Americanthe group pest [8]. speciesThe North in the Americanvirgifera pestspecies species group in arethe univoltine,virgifera species or sometimes group are semivoltine, univoltine, andor possesssometimes diapausing semivoltine, eggs thatand allowpossess them diapausing to overwinter eggs inthat temperate allow them climates to overwinter or survive dryin temperate seasons in theclimates subtropics or survive [9,10], dry both seasons situations in the during subtropics which the[9,10], adult both cannot situations find sustenanceduring which or survivethe adult the extremecannot find conditions. sustenance or survive the extreme conditions. Diabrotica balteata (photo Stephen Diabrotica speciosa adult feeding on Diabrotica viridula Cresswell) a bean leaf (photo Dirceu N. Gassen) FigureFigure 1.1. PhotographsPhotographs of the adult of the three species species of of pest pest DiabroticaDiabrotica fromfrom South South America. America. D.D. speciosaspeciosa isis distributeddistributed throughoutthroughout South America, from from agricultural agricultural patches patches in in the the temperate temperate PatagonianPatagonian steppessteppes toto thethe tropics,tropics, with the exception of of Chile, Chile, and and up up to to altitudes altitudes of of over over 2500 2500 m m aboveabove seasea level [2,11] [2,11] (Figure (Figure 2).2). It Itis isthe the best best studied studied DiabroticaDiabrotica speciesspecies in South in South America America due to dueits toimpact its impact on many on manycrops. crops.The adult The has adult over has 132 over reco 132rded recorded host species, host in species, 24 different in 24 diplantfferent families plant families[11, and[11, literature and literature therein]. therein] Larval. Larvalhosts hostsare not are as not well as wellknown, known, but butD. D.speciosa speciosa hashas at atleast least five five confirmedconfirmed larvallarval hosts:hosts: maizemaize ((ZeaZea maysmays L.), wheat (Triticum spp.), Johnsongrass ( (SorghumSorghum halepense halepense Persoon),Persoon), peanutpeanut ((ArachisArachis hypogaeahypogaea L.),L.), and potato ( Solanum tuberosum tuberosum L.).L.). Another Another four four plant plant species species hostedhosted full full development development in in the the laboratory laboratory [11 [11–15].–15]. However, However, the the fact fact that that larvae larvae can developcan develop on plant on speciesplant species in four in families four families of three of dithreefferent different orders orde suggestsrs suggests that there that there could could be many be many more more larval larval hosts thathosts simply that simply have not have been not discovered been discovered because because of the of hypogeous the hypogeou habits habit of the of larva. the larva. D. speciosa is documented in most crops in South America, but is considered mainly a horticultural pest as an adult, and a pest of potato, maize, and peanuts as larva [11,13,16]. Yet these generalizations are not without exceptions. In Brazil, this species is considered a pest of maize as a larva, and a minor pest as an adult as well [17,18]. It is also regarded as an important pest of potato during both the adult and larval stages, although this depends heavily on the cultivar [19]. In addition, the adult is also regarded as an important pest of seedlings and young plants of some extensive crops, such as soybeans, beans (Phaseolus vulgaris), cotton, sunflower, maize, tobacco, wheat, and canola [20–22], and, curiously, of table grapes [23] (Table1). Insects 2020, 11, 421 3 of 18 Insects 2020, 11, x FOR PEER REVIEW 3 of 19 Figure 2. Distribution of Diabrotica speciosa inin SouthSouth AmericaAmerica (crosshatched(crosshatched area).area). TableD. speciosa 1. Main is crops documented attacked by thein Southmost Americancrops inpest SoutDiabroticah America,species, but and is current considered and potential mainly a horticulturalcontrol methods. pest as an adult, and a pest of potato, maize, and peanuts as larva [11,13,16]. Yet these generalizations D.are balteata not without D. speciosa exceptions. D. viridulaIn Brazil, thisControl species Methods is considered Promising a Controlpest of Methods maize as a larva,Host and Crop a minor Adults pest Larvae as an Adults adult Larvae as well Adults [17,18]. Larvae It Adultsis also regarded Larvae as an Adultsimportant pest Larvae of potato intercropping duringbeans both the x adult x and larval x stages, x although thisCb, depends Op, Nn, Py 1 heavily on the cultivar [19]. In plant resistance addition,cucurbits the adult x is also regarded x as an important pest Cb, Op,of Nn,seedlings Py cucurbitacin and young baits plants of some IGR 1 extensive crops, such as soybeans, beans (Phaseolus vulgaris), cotton, sunflower, maize,seed treatment tobacco, Cb, Bt maize silicon with fungi, wheat,maize