Abstract
The competition between Telenomus podisi Ashmead and Trissolcus teretis (Johnson) parasitizing eggs of Diceraeus melacanthus (Dallas) and Euschistus heros (Fabricius) was studied in three different laboratory bioassays to gather knowledge in order to improve stink bug management and to strengthen the preservation of naturally occurring parasitoid species. The impact of parasitoid sequence and time intervals (4 to 192 h) between parasitoid species was evaluated. Competition of Te. podisi and Tr. teretis for the same host favored the parasitoid encountering the egg host first, as it usually outcompetes the second parasitoid. We conclude that it is unwarranted in a short-term goal to release both species together in augmentative biological control programs since the repeated release of Te. podisi led to higher parasitism than any other studied variation of parasitoid sequence. However, simultaneous release of multiple species could be important to help the preservation of the diversity of scelionids in the agroecosystem, a hypothesis that needs to be further investigated in future research.
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References
Agboka K, Schulthess F, Chabi-olaye A, Labo I, Gounou S, Smith H (2002) Self-, intra, and interspecific host discrimination in Telenomus busseolae Gahan and T. isis Polaszek (Hymenoptera: Scelionidae), sympatric egg parasitoids of the African cereal stem borer Sesamiacalamistis Hampson (Lepidoptera: Noctuidae). J Insect Behav 15:1–12
Agrolink. Disponível em: <https://www.agrolink.com.br/agrolinkfito>. Acesso em: 20 out. 2019.
Bueno AF, Corrêa-Ferreira BS, Roggia S, Bianco R (2015a) Silenciosos e daninhos. Rev Cult 196:25–27
Bueno AF, Bortolotto OC, Pomari-Fernandes A, França-Neto JB (2015b) Assessment of a more conservative stink bug economic threshold for managing stink bugs in Brazilian soybean. Crop Prot 71:132–137
Burr IW, Foster LA (1972) A test for equality of variances. University of Purdue, West Lafayette
CABI (2020) Invasive species compendium. Disponível em: <https://www.cabi.org/isc/datasheet/54888#REF-DDB%2D%2D25> Acessoem 30 de Novembro 2020.
Carneiro TR, Fernandes OA, Cruz I (2009) Influence of females intraspecific competition and lack of host on Telenomusremus Nixon (Hymenoptera: Scelionidae) parasitism on Spodopterafrugiperda (JE Smith) (Lepidoptera, Noctuidae) eggs. Rev Bras Entomol 53:482–486
Cingolani MF, Greco NM, Liljesthröm GG (2013) Multiparasitism of Piezodorus guildinii eggs by Telenomus podisi and Trissolcus urichi. BioControl 58:37–44
Collier TR, Hunter MS, Kelly SE (2007) Heterospecific ovicide influences the outcome of competition between two endoparasitoids, Encarsiaformosa and Encarsialuteola. Ecol Entomol 32:70–75
Corrêa-Ferreira BS (1986) Ocorrência natural do complexo de parasitoides de percevejos da soja no Paraná. An Soc Entomol Bras 15:189–199
Corrêa-Ferreira BS (2002) Trissolcus basalis para controle de percevejos na soja. pages 449-476. In: Parra JR, Botelho P S M, Corrêa-Ferreira BS, Bento J M S (Editores) Controle biológico no Brasil: Parasitóides e Predadores. Editora Manole Ltda São Paulo 635p; Utilizacão do parasitoide Trissolcus basalis (Wollaston) no controle de percevejos da soja. Embrapa, Londrina, Brazil.
Corrêa-Ferreira BS, Moscardi F (1994) Temperature effect on the biology and reproductive performance of the egg parasitoid Trissolcus basalis (Woll.). An Soc Entomol Bras 23:399–399
Corrêa-Ferreira BS, Moscardi F (1995) Seasonal occurrence and host spectrum of egg parasitoids associated with soybean stink bugs. Biol Control 5:196–202
Corrêa-Ferreira BS, Sosa-Gómez DR (2017) Percevejos e o sistema de produção soja-milho. Embrapa Soja-Documentos (INFOTECA-E).
Cusumano A, Peri E, Vinson SB, Colazza S (2011) Interspecific extrinsic and intrinsic competitive interactions in egg parasitoids. BioControl 57:719–734
Cusumano A, Peri E, Vinson SB, Colazza S (2012) The ovipositing female of Ooencyrtustelenomicida relies on physiological mechanisms to mediate intrinsic competition with Trissolcus basalis. Entomol Exp Appl 143:155–163
De Moraes CM, Mescher MC (2005) Intrinsic competition between larval parasitoids with different degrees of host specificity. Ecol Entomol 30:564–570
De Moraes CM, Cortesero AM, Stapel JO, Lewis WJ (1999) Intrinsic and extrinsic competitive interactions between two larval parasitoids of Heliothis virescens. Ecol Entomol 24:402–410
Favetti BM, Butnariu AR, Doetzer AK (2014) Storage of Euschistus heros eggs (Fabricius) (Hemiptera: Pentatomidae) in liquid nitrogen for parasitization by Telenomus podisi Ashmead (Hymenoptera: Platygastridae). Neotrop Entomol 1:291–293
Foerster LA, Queiróz JM (1990) Incidência natural de parasitismo de pentatomídeos da soja no Centro-Sul do Paraná. An Soc Entomol Bras 5:221–232
Gerling D (1972) The developmental biology of Telenomus remus Nixon (Hym., Scelionidae). B Entomol Res 61:385–388
Godfray HCJ (1994) Parasitoids: behavioral and evolutionary ecology. Princeton University Press, Princeton, USA
Harvey JA, Poelman EH, Tanaka T (2013) Intrinsic inter- and intraspecific competition in parasitoid wasps. Ann Rev Entomol 58:333–351
Hokyo N, Kiritani K, Nakasuji F, Shiga M (1966) Comparative biology of the two scelionid egg parasites of Nezaraviridula L. (Hemiptera: Pentatomidae). Appl Entomol Zool 1:94–102
Koppel AL, Herbert DA Jr, Kuhar TP, Kamminga K (2009) Survey of stink bug (Hemiptera: Pentatomidae) egg parasitoids in wheat, soybean, and vegetable crops in southeast Virginia. Environ Entomol 38:375–379
Laumann RA, Moraes MCB, Silva JPD, Vieira AMC, Silveira SD, Borges M (2010) Egg parasitoid wasps as natural enemies of the Neotropical stink bug Dichelops melacanthus. Pesq Agropec Bras 45:442–449
Mackauer M (1990) Host discrimination and larval competition in solitary endoparasitoids. In: Mackauer M, Ehler LE, Roland J (eds) Critical issues in biological control. Entercept Ltd., Andover, UK, pp 41–62
Medeiros MA, Loiácono MS, Borges M, Schmidat FVG (1998) Incidência natural de parasitoides em ovos de percevejos (Hemíptera: Pentatomidae) encontrados na soja no distrito Federal. Pesq Agropec Bras 33:1431–1435
Netting JF, Hunter MS (2000) Ovicide in the white fly parasitoid, Encarsia formosa. Anim Behav 60:217–226
Orr DB, Russin JS, Boethel DJ, Jones WA (1986) Stink bug (Hemiptera: Pentatomidae) egg parasitism in Louisiana soybeans. Environ Entomol 15:1250–1254
Osorio D, Vorobyev M (2008) A review of the evolution of animal colour vision and visual communication signals. Vision Res 48:2042–2051
Panizzi AR, Corrêa-Ferreira BS (1997) Dynamics in the insect fauna adaptation to soybean in the tropics. Trends Entomol 1:71–88
Panizzi AR, Slansky JRF (1985) Review of phytophagous pentatomids (Hemiptera: Pentatomidae) associated with soybean in the Americas. Fla Entomol 68:184–214
Panizzi AR, Parra JRP, Santos CH, Carvalho DR (2000) Rearing the southern green stink bug using artificial dry diet and artificial plant. Pesq Agropec Bras 35:1709–1715
Pedersen BS, Mills NJ (2004) Single versus multiple introduction in biological control: the roles of parasitoid efficiency, antagonism and niche overlap. J Appl Ecol 41:973–984
Peitsch D, Fietz A, Hertel H, de Souza J, Ventura DF, Menzel R (1992) The spectral input systems of hymenopteran insects and their receptor-based colour vision. J Comp Physiol 170:23–40
Peres WAA, Corrêa-Ferreira BS (2004) Methodology of mass multiplication of Telenomus podisi Ashmead and Trissolcus basalis (Hymenoptera: Scelionidae) on eggs of Euschistus heros (Hemiptera: Pentatomidae). Neotrop Entomol 33:457–462
Queiroz AP, Taguti EA, Bueno AF, Grande MLM, Costa CO (2018) Host preferences of Telenomus podisi (Hymenoptera: Scelionidae): parasitism on eggs of Dichelops melacanthus, Euschistus heros, and Podisus nigrispinus (Hemiptera: Pentatomidae). Neotrop Entomol 47:543–552
SAS Institute (2009) SAS User’s Guide: Statistics, Version 8e. SAS Institute, Cary, NC
Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52:591–611
Silva CC, Laumann RA, Blassioli MC, Pareja M, Borges M (2008) Euschistus heros mass rearing technique for the multiplication of Telenomus podisi. Pesq Agropec Bras 43:575–580
Silva GV, Bueno AF, Neves PMOJ, Favetti BM (2018) Biological characteristics and parasitism capacity of Telenomus podisi (Hymenoptera: Platygastridae) on eggs of Euschistus heros (Hemiptera: Pentatomidae). J Agric Sci 10:210–220
Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press, Princeton, New Jersey, USA
Sujii ER, Costa MLM, Pires CSS, Colazza S, Borges M (2002) Inter and intra-guild interactions in egg parasitoid species of the soybean stink bug complex. Pesq Agropec Bras 37:1541–1549
Tillman PG (2011) Natural biological control of stink bug (Heteroptera: Pentatomidae) eggs in corn, peanut, and cotton farmscapes in Georgia. Environ Entomol 40:303–314
Tillman PG, Powell JE (1992) Interspecific discrimination and larval competition among Microplitisde molitor, Cotesia kazak (Hym.: Braconidae), and Hyposoter didymator (Hym.: Ichneumonidae), parasitoids of Heliothis virescens (Lep.: Noctuidae). Entomophaga 37:439–451
van Alphen JJM, Visser ME (1990) Superparasitism as an adaptive strategy for insect parasitoids. Ann Rev Entomol 35:59–79
van Lenteren JC, Bolckmans K, Köhl J, Ravensberg WJ, Urbaneja A (2018) Biological control using invertebrates and microorganisms: plenty of new opportunities. BioControl 63:39–59
Volkoff N, Colazza S (1992) Growth patterns of teratocytes in the immature stages of Trissolcusbasalis(Woll.) (Hymenoptera: Scelionidae), an egg parasitoid of Nezaraviridula (L.) (Heteroptera: Pentatomidae). Int J Insect Morphol Embryol 21:323–336
Yeargan KV (1979) Parasitism and predation of stink bug eggs in soybean and alfalfa fields. Environ Entomol 8:715–719
Zerbino MS, Panizzi AR (2019) The underestimated role of pest pentatomid parasitoids in Southern South America. Arthropod-Plant Inte 10:1–16
Acknowledgements
Thanks are extended to Dagmar Frish for English editing the manuscript and to Dr Valmir Antônio Costa (Instituto Biológico de Campinas) for parasitoid identification (voucher specimen from IBCBE 003272 to IBCBE 003425 were deposited at the “Coleção de Insetos Entomófagos Oscar Monte,” Instituto Biológico de Campinas, Campinas, São Paulo, Brazil).
Funding
The authors thank Embrapa Soja, the Coordination for the Improvement of Higher Education Personnel (CAPES), and the National Council for Scientific and Technological Development (CNPq) for their financial support (project number 402797/2016-7) and fellowship (project number 302645/2018-7).
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Ana Paula de Queiroz, Adeney de Freitas Bueno, and Antônio Ricardo Panizzi: contributed to the study design and wrote the paper. Ana Paula de Queiroz: conducted the sampling. Adeney de Freitas Bueno and Antônio Ricardo Panizzi: contributed reagents/material/analysis tools. Ana Paula de Queiroz, Bruna Magda Favetti: conducted the experiments. All authors have read and approved the manuscript.
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de Queiroz, A.P., Bueno, A.d.F., Panizzi, A.R. et al. Intrinsic Interspecific Competition Between Telenomus podisi and Trissolcus teretis (Hymenoptera: Scelionidae). Neotrop Entomol 50, 453–461 (2021). https://doi.org/10.1007/s13744-021-00851-9
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DOI: https://doi.org/10.1007/s13744-021-00851-9