Species identity of Macrolophus melanotoma (Costa 1853) and Macrolophus pygmaeus (Rambur 1839) (Insecta: Heteroptera: Miridae) based on morphological and molecular data and bionomic implications

Insect Systematics and Evolution

Volumn 37, Issue 4, 2006, Pages 385-404

  Martinez Cascales, Jose Isidro ^a   Cenis, Jose Luis ^a   Cassis, Gerasimos ^b   Sanchez, Juan Antonio ^a  

^a INSTITUTO MURCIANO DE INVESTIGACIÓN Y DESARROLLO AGRARIO Y ALIMENTARIO IMIDA   (Spain)

^b AUSTRALIAN MUSEUM   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CYRTOPELTIS; DICYPHUS; DICYPHUS TAMANINII; HETEROPTERA; INSECTA; MACROLOPHUS; MACROLOPHUS MELANOTOMA; MACROLOPHUS PYGMAEUS; MIRIDAE;

EID: 33846698879     PISSN: 1399560X     EISSN: None     Source Type: Journal    
DOI: 10.1163/187631206788831470     Document Type: Review

References (89)

1. Abdullahi, I., Atiri, G. I., Thottappilly, G. & Winter, S. (2004) Discrimination of cassava-associated Bemisia tabaci in Africa from polyphagous populations, by PCR-RFLP of the internal transcribed spacer regions of ribosomal DNA. Journal of Applied Entomology 128: 81-87.
2. Alomar, O., Goula, M. & Albajes, R. (1994) Mirid bugs for biological control: identification, survey in non-cultivated winter plants, and colonization of tomato fields. IOBC Western Palaearctic Region Section Bulletin 17: 217-223.
3. Alomar, O., Goula, M. & Albajes, R. (2002) Colonisation of tomato fields by predatory mirid bugs (Hemiptera: Heteroptera) in northern Spain. Agriculture, Ecosystems & Environment 89: 105-115.
4. Alomar, O., Riudavets, J. & Castañé, C. (2003) Macrolophus caliginosus in the biological control of Bemisia tabaci in greenhouse melons. IOBC Western Palaearctic Region Section Bulletin 26: 125-129.
5. Alomar, O. & Albajes, R. (1996) Greenhouse whitefly (Homoptera: Aleyrodidae) predation and tomato fruit injury by the zoophytophagous predator Dicyphus tamaninii (Heteroptera: Miridae). Pp. 155-177
6. in Alomar, O. & Wiedenmann, R.N.: Zoophytophagous Heteroptera: Implications for Life History and Integrated Pest Management. Entomological Society of America, Lanham, MD.
7. Alomar, O. & Albajes, R. (2003) Habitat management for conservation of the native predator Macrolophus caliginosus. IOBC Western Palaearctic Region Section Bulletin 26: 7-11.
8. Alvarado P., Baltá, O. & Alomar, O. (1997) Efficiency of four Heteroptera as predators of Aphis gossypii and Macrosiphum euphorbiae (Hom.: Aphididae). Entomophaga 42: 215-226.
9. Arnó J., Alonso, E. & Gabarra, R. (2003) Role of the parasitoid Diglyphus isaea Walker and the predator Macrolophus caliginosus Wagner in the control of leafminers. IOBC Western Palaearctic Region Section Bulletin 26: 79-84.
10. Arnó J., Gabarra, R. & Albajes, R. (2005) Conservación de míridos depredadores para el control biológico en cultivos de tomate bajo invernadero: historia, éxitos y limitaciones. Phytoma España 165: 40-43.
11. Athanassiou C. G., Kavallieratos, N. G., Ragkou, V. S. & Buchelos C. T. (2003) Seasonal abundance and spatial distribution of the predator Macrolophus costalis and its prey Myzus persicae on tobacco. Phytoparasitica 31: 8-18.
12. Barnadas, I., Gabarra, R. & Albajes, R. (1998) Predatory capacity of two mirid bugs preying on Bemisia tabaci. Entomologia Experimentalis et Applicata 86: 215-219.
13. Berlocher, S. H. (1984) Insect molecular systematics. Annual Review of Entomology 29: 403-433.
14. Bolte, K. B. (1996) Techniques for obtaining scanning electron micrographs of minute arthropods. Proceedings of the Entomological Society of Ontario 127: 67-87.
15. Boyarin, V. V. (2000) Application of Macrolophus in protected soil. Zashchita i Karantin Rastenii 11: 20
16. Brower, A. V. Z. & Desalle, R. (1994) Practical and theoretical considerations for choice of a DNA sequence region in insects molecular systematics, with a short review of published studies using nuclear gene regions. Annals of the Entomological Society of America 87: 702-716.
17. Carapezza, A. (1995) The specific identities of Macrolophus melanotoma (A. Costa, 1853) and Stenodema curticolle (A. Costa, 1853) (Insecta Heteroptera, Miridae). Naturalista Siciliano 19: 295-298.
18. Carapezza, A., Faraci, F. & Péricart, J. (1995) Designation of lectotypes and paralectotypes of Palaearctic Heteroptera in the collection of Achille Costa (Museo di Zoologia dell'Università di Napoli). Naturalista Siciliano 19: 279-294.
19. Carvalho, J. C. M. (1958) A catalogue of the Miridae of the world. Part II. Arquivos do Museu National, Rio de Janeiro 45: 1-216.
20. Cassis, G. (1986) A systematic study of the subfamily Dicyphinae (Heteroptera, Miridae). Ph.D. Thesis, Oregon State University. University Microfilms International, Ann Arbor.
21. Castañé, C., Alomar, O., Goula, M. & Gabarra, R. (2000) Natural populations of Macrolophus caliginosus and Dicyphus tamaninii in the control of the greenhouse whitefly in tomato crops. IOBC Western Palaearctic Region Section Bulletin 23:221-224.
22. Castañé, C., Alomar, O. & Riudavets, J. (2003) Potential risk of damage to zucchinis caused by mirid bugs. IOBC Western Palaearctic Region Section Bulletin 26: 135-138.
23. Castañé, C., Alomar, O., Goula, M. & Gabarra, R. (2004) Colonization of tomato greenhouses by the predatory mirid bugs Macrolophus caliginosus and Dicyphus tamaninii. Biological Control 30: 591-597.
24. Caterino, M. S., Cho, S. & Sperling, F. A. H. (2000) The current state of insect molecular systematics: a thriving tower of babel. Annual Review of Entomology 45: 1-54.
25. Cenis, J. L., Perez, P. & Fereres, A. (1993) Identification of aphid (Homoptera: Aphididae) species and clones by Random Amplified Polymorphic DNA. Annals of the Entomological Society of America 86: 545-550.
26. Constant, B., Grenier, S., Febvay, G. & Bonnot, G. (1996). Host plant hardness in oviposition of Macrolophus caliginosus (Hemiptera: Miridae). Journal of Economic Entomology 89: 1446-1452.
27. Costa, A. (1853) Cimicum Regni Neapolitani Centuria tertia et quartae fragmentum. Napoli. 77 ("73") (Preprint from 1855, Atti del Reale Istituto d'Incoraggiamento alle Scienze Naturali Napoli 8: 225-299).
28. Crozier, Y. C., Koulianos, S. & Crozier, R. H. (1991) An improved test for africanized honeybee mitochondrial DNA. Experientia 47: 968-969.
29. DeBach, P. (1964) Biological control of insect pests and weeds. Chapman and Hall Ltd. London.
30. Enkegaard, A., Brödsgaard, H. F. & Hansen, D. L. (2001) Macrolophus caliginosus: functional response to whiteflies and preference and switching capacity between whiteflies and spider mites. Entomologia Experimentalis et Applicata 101: 81-88.
31. Favyas, C., Perdikis, D. & Lykouressis D. (2003) Biological characteristics of Macrolophus caliginosus (Hemiptera: Miridae) when feeding on the non-cultivated plant Dittrichia viscosa (Asteraceae). IOBC Western Palaearctic Region Section Bulletin 26:139.
32. Fieber, F. X. (1858) Criterion zur genetischen Theilung der Phytocoriden (Capsini aut.). Wiener Entomologische Monatschrift 2: 289-327, 329-347, 388.
33. Fieber, F. X. (1861) Die europäischen Hemiptera. Halbflügler (Rhynchota Heteroptera). Pp. 113-444. Gerold's Sohn, Wien.
34. Figuls, M., Castañé, C. & Gabarra, R. (1999). Residual toxicity of some insecticides on the predatory bugs Dicyphus tamaninii and Macrolophus caliginosus, BioControl. 44: 89-98.
35. Gabarra, R., Alomar, O., Castañé, C., Bordas, E., Albajes, R. & Malausa, J. C. (1990) Mirid bugs. Polyphagous predators in glasshouse crops: perspectives and problems. Sting 10: 3.
36. Gillespie, D. R., McGregor, R. R, Sanchez, J. A, Vanlaerhoven, S. L., Quiring, D. M. J., Roitberg, B. D., Foottit, R. G., Schwartz, M. D. & Shipp, J. L. 2006. Dicyphus hesperus (Hemiptera: Miridae) as a success story in development of endemic natural enemies as biological control agents. In Vincent, C., Goettel, M. & Lazarovits, G.: Case Studies in Biological Control: A Global Perspective. CABI Publishing, UK. in press.
37. Goula, M. & Alomar, O. (1994) Miridos (Heteroptera Miridae) de interés en el control integrado de plagas en tomate. Guía para su identificatión. Boletín de Sanidad Vegetal-Plagas 20: 131-143.
38. Hansen, D. L., Brödsgaard, H. F. & Enkegaard, A. (1999). Life table characteristics of Macrolophus caliginosus preying upon Tetranychus urticae. Entomologia Experimentalis et Applicata 93: 269-275.
39. Henry, T. J. & Wheeler, A. G. Jr. (1988) Family Miridae Hahn, 1833 (=Capsidae Burmeister, 1835). The plant bugs. Pp. 251-507 in Henry, T. J. & Froeschner, R. C.: Catalog of the Heteroptera, or True Bugs of Canada and the Continental United States. E. J. Brill, Lleiden, New York.
40. Herrich-Schaeffer, G. A. W. (1835) Fauna insectorum Germaniae initia oder Deutschlands Insecten. Vol. 135. Flessecker, Nürnberg.
41. Huelsenbeck, J. P. (1995) Performance of phylogenetic methods in simulation. Systematic Biology 44: 17-48.
42. Josifov, M. (1961) Macrolophus nubilis geranii n. subsp. (Hem. Het. Miridae). Comptes Rendus de l'Académie Bulgare des Sciences 14: 87-89.
43. Josifov, M. (1968) Eine Heteropterenausbeute von der Insel Kreta. Annales Zoologici, Warszawa 25: 453-457.
44. Josifov, M. (1992) Zur Taxonomie der paläarktischen Macrolophus-Arten (Insecta, Heteroptera: Miridae). Reichenbachia 29: 1-4.
45. Kaspar, B. (1982) Étude de la biologie et du comportement d'un Héteroptère Miride, Macrolophus caliginosus (Wagner) en vue de son utilisation pour la lutte biologique. Thesis, Université des Sciences et Techniques du Languedoc, Montpellier.
46. Kerzhner, I. M. & Josifov, M. (1999) Cimicomorpha II: Miridae. Vol 3, 577 pp. in Aukema, B. & Rieger, C.: Catalogue of the Heteroptera of the Palaearctic Region. Wageningen, The Netherlands.
47. Kumar, S., Tamura, K. & Nei, M. (2004) MEGA 3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics 5: 150-163.
48. Lalonde, R. G., McGregor, R. R., Gillespie, D. R. & Roitberg, B. D. (1999) Plant-feeding by arthropod predators contributes to the stability of predator-prey population dynamics. Oikos 87: 603-609.
49. Lu, Y. J., Adang, M. J., Isenhour, D. J. & Kochert, G. D. (1992) RFLP analysis of genetic variation in North American populations of the fall armyworm moth Spodoptera frugiperda (Lepidoptera: Noctuidae). Molecular Ecology 1: 199-208.
50. Lucas, E. & Alomar, O. (2001) Macrolophus caliginosus Wagner as an intraguild prey for the zoophytophagous Dicyphus tamaninii Wagner (Heteroptera: Miridae). Biological Control 20: 147-152.
51. Lucas, E. & Alomar, O. (2002) Impact of the presence of Dicyphus tamaninii (Wagner) (Heteroptera: Miridae) on whitefly (Hompptera: Aleyrodidae) predation by Macrolophus caliginosus (Wagner) (Heteroptera: Miridae). Biological Control 25: 123-128.
52. Lykouressis, D., Perdikis, D. & Tsagarakis, A. (1999-2000) The effects of natural enemies on aphid populations on processing tomato. Entomologia Helenica 13: 35-42.
53. Lykouressis, D., Perdikis, D. & Michalaki, M. (2001a) Nymphal development and survival of Macrolophus pygmaeus Rambur (Hemiptera: Miridae) on two eggplant varieties as affected by temperature and presence/absence of prey. Biological Control 20: 222-227.
54. Lykouressis, D., Perdikis, D. & Tsagarakis, A. (2001b) Polyphagous mirids in Greece: host plants and abundance in traps placed in some crops. Bollettino del Laboratorio di Entomologia Agraria "Filippo Silvestri" 56: 57-68.
55. Malausa, J. C., Drescher, J. & Franco, E. (1987) Perspectives for the use of a predaceous bug Macrolophus caliginosus Wagner (Heteroptera, Miridae) on glasshouse crops. IOBC Western Palaearctic Region Section Bulletin 10: 106-107.
56. Malausa, J. C. (1989) Lutte integree sous serre: les punaises predatrices Mirides dans les cultures de Solanacees du sud-est de la France. Revue Horticole 298: 39-43.
57. Malausa, J. C. & Trottin-Caudal, Y. (1996) Advances in the strategy of use of the predaceous bug Macrolophus caliginosus (Heteroptera: Miridae) in glasshouse crops. Pp. 178-189 in Alomar, O. & Wiedenmann, R.N.: Zoophytophagous Heteroptera: Implications for Life History and Integrated Pest Management. Entomological Society of America, Lanham, MD.
58. Margaritopoulos, J. T., Tsitsipis, J. A. & Perdikis, D. C. (2003) Biological characteristics of the mirids Macrolophus costalis and Macrolophus pygmaeus preying on the tobacco form of Myzus persicae (Hemiptera: Aphididade). Bulletin of Entomological Research 93: 39-45.
59. Martinez-Cascales, J. I., Cenis, J. L., Sanchez, J. A. (2006) Differentiation of Macrolophus pygmaeus (Rambur 1839) and Macrolophus melanotoma (Costa 1853) (Heteroptera: Miridae) based on molecular data. IOBC Western Palaearctic Region Section Bulletin 29: 223-234.
60. Perdikis, D. & Lykouressis, D. (2000) Effects of various items, host plants, and temperatures on the development and survival of Macrolophus pygmaeus Rambur (Hemiptera: Miridae). Biological Control 17: 55-60.
61. Perdikis, D. C. & Lykouressis, D. P. (2002) Thermal requirements for development of the polyphagous predator Macrolophus pygmaeus (Hemiptera: Miridae). Environmental Entomology 31: 661-667.
62. Perdikis, D. C. & Lykouressis, D. P. (2003) Aphis gossypii (Hemiptera: Aphididae) as a factor inhibiting the survival and population increase of the predator Macrolophus pygmaeus (Hemiptera: Miridae) on cucumber. European Journal of Entomology 100: 501-508.
63. Perdikis, D. C. & Lykouressis, D. P. (2004) Myzus persicae (Homoptera: Aphididae) as suitable prey for Macrolophus pygmaeus (Hemiptera: Miridae) popula
64. tion increase on pepper plants. Environmental Entomology 33: 499-505.
65. Perdikis, D. C., Margaritopoulos, J. T., Stamatis, C., Mamuris, Z., Lykouressis, D. P. Tsitsipis, J. A., & Pekas, A. (2003) Discrimination of the closely related biocontrol agents Macrolophus melanotoma (Hemiptera: Miridae) and M. pygmaeus using mitochondrial DNA analysis. Bulletin of Entomological Research 93: 507-514.
66. Posada, D. (2003) Selecting models of evolution. Pp. 256-279 in Salemi, M. & Vandamme A.M.: The Phylogenetic Handbook. A Practical Approach to DNA and Protein Phylogeny. Cambridge University Press.
67. Posada, D. & Crandall, K. A. (1998) Modeltest: Testing the model of DNA substitution. Bioinformatics 14: 817-818.
68. Rambur, P. (1839) Faune entomologique de l'Andalousie. Pp. 97-176. Arthur Bertrand, Paris.
69. Reuter, O. M. (1883). Hemiptera Gymnocerata Europae. Hé miptères Gymnocérates d'Europe, du bassin de la Mediterranée et de l'Assie Russe. III. Acta Societas Scientiarum Fennicae 13: 438.
70. Reuter, O. M. (1895) Ad cognitionem Capsidarum. III. Capsidae ex Africa boreali. Revue d'Entomologie 14: 131-142.
71. Sampson, C. R. & Jacobson, J. (1999) Macrolophus caliginosus Wagner (Heteroptera: Miridae): a predator causing damage to UK pomatoes. IOBC Western Palaearctic Region Section Bulletin 22: 213-216.
72. Sanchez, J. A., Martinez-Cascales, J. I. & Lacasa, A. (2003) Abundance and wild host plants of predator mirids (Heteroptera: Miridae) in horticultural crops in the Southeast of Spain. IOBC Western Palaearctic Region Section Bulletin 26 (10): 147-152.
73. Sanchez, J. A., Gillespie, D. R. & McGregor, R. R. (2004) Plant preference in relation to life history traits in the zoophytophagous predator Dicyphus hesperus. Entomologia Experimental et Applicata 112: 7-19.
74. Sanchez, J. A., Cassis, G. & Martinez-Cascales J. I. (2006) Description of a new species of Dicyphus Fieber (Insecta: Heteroptera: Miridae) from Portugal based on morphological and molecular data, Insect Systematics and Evolution 37: 281-300.
75. Say, T. (1832) Descriptions of new species of Heteropterous Hemiptera of North America. New Harmony, Indiana.
76. Schuh, R. T. (1995). Plant Bugs of the World (Insecta: Heteroptera; Miridae): systematic catalog, distributions, host list and bibliography. The New York Entomological Society I-xii. New York.
77. Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H. & Flook, P. (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of Ame rica 87: 651-701.
78. Sullivan, J., Markert, J. A. & Kilpatrick, W. (1997) Phylogeography and molecular systematics of the Peromycus aztecus species group (Rodentia: Muridae) inferred using parsimony and likelihood. Systematic Biology 46: 426-440.
79. Sullivan, J. & Swofford, D. L. (1997) Are Guinea pigs rodents? The importance of adequate models in molecular phylogenetics. Journal of Mammalian Evolution 4: 77-86.
80. Swearingen, M., Headrick, D. & Bellow, T. (1997) Comparison of fixation and drying procedure for scanning electron microscopy among insect body types. Proceedings of the Entomological Society of Washington 99: 513-522.
81. Swofford, D. L. (2002) PAUP*. Phylogenetic Analysis Using Parsimony (* and other methods). Version 4.0b10. Sunderland, Massachusetts (USA): Sinauer Associates; Inc.
82. Swofford, D. L. & Sullivan, J. (2003) Phylogenetic inference based on parsimony and other methods: Practice. Pp. 160-206 in Salemi, M. & Vandamme A. M.: The Phylogenetic Handbook. A Practical Approach to DNA and Protein Phylogeny. Cambridge University Press.
83. Tavella, L., Alma, A. & Sargiotto, C. (1997) Samplings of Miridae Dicyphinae in tomato crops of north western Italy. IOBC Western Palaearctic Region Section Bulletin 20: 249-256.
84. Tavella, L. & Goula, M. (2001) Dicyphini collected in horticultural areas of north-western Italy (Heteroptera Miridae). Bollettino di Zoologia Agraria e di Bachicoltura 33: 93-102.
85. Wagner, E. (1951a) Contributo alla conoscenza della fauna emitterologica italiana, II. Zwei neue Minden-Arten und eine bisher übersehene Art aus Italien (Hem. Het.). B. Macrolophus caliginosus n. sp., eine neue Miridenart aus Italien (Hem. Het.). Bollettino dell'Associazione Romana di Entomologia 5 (1950): 29-31.
86. Wagner, E. (1951b) Zur Systematik der Gattung Dicyphus (Hem. Het., Miridae). Commentationes Biologicae 12: 1-36.
87. Wagner, E. (1957) Macrolophus brevicornis nov. spec. (Hem. Het. Miridae). Entomologisches Nachrichtenblatt Österreichischer und Schweizer Entomologen 9: 14-15.
88. Wagner, E. (1959) Über einige mediterrane Miridae (Hem. Het.). Acta Entomologica Musei Nationalis Pragae 33: 339-358.
89. Wagner, E. & Weber, H. (1964). Héteroptères Miridae. Faune de la France. Fédération Française des Sociétés de Sciences Naturelles. Office Centrale de Faunistique. Paris.