Abstract
Mesophthirus engeli (Mesophthiridae incerti ordinis), described as a feather-feeding parasite of dinosaurs, has recently been reinterpreted as an early instar nymph (crawler) of a primitive scale insect. Mesophthirus has no specific similarities to bird lice, although life on feathers should modify parasites in a similar way. Based on re-examination of photographs of the type specimens of M. engeli, the subfamily Mesophthirinae stat. nov. is assigned to the archaic extant family Xylococcidae s.l. (recorded since the Hauterivian), next to the extant subfamilies Xylococcinae and Stigmacoccinae. Xylococcid honeydew is an important food resource for birds and other arboreal vertebrates. Like their modern relatives, Mesophthirinae lived under the bark of trees and produced copious honeydew. Early birds and their precursors, small feathered dinosaurs, may well have fed on honeydew and the mesophthirines themselves. Scale insect crawlers are adapted to wind transport and phoresy on insects and vertebrates, so finding Mesophthirus on feathers is expected.
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REFERENCES
Beggs, J.R. and Wilson, P.R., The kaka Nestor meridionalis, a New Zealand parrot endangered by introduced wasps and mammals, Biol. Conserv., 1991, vol. 56, pp. 23–38. https://doi.org/10.1016/0006-3207(91)90086-O
Blagoveshtchensky, D.I., Chewing lice (Insecta: Mallophaga), in Fauna SSSR (Fauna of the USSR), 1959, vol. 72.
Borchsenius, N.S., Chervetsy i shchitovki SSSR (Coccoidea) (Mealybugs and Scale Insects of USSR (Coccoidea)), Moscow-Leningrad: Akad. Nauk SSSR, 1950.
Borchsenius, N.S., Mealybugs and Scale insects (Coccoidea): Soft scales (Coccidae), Fauna SSSR, N.S., 1957, no. 66, 1–494.
Clay, T., Piercing mouth-parts in the biting lice (Mallophaga), Nature, 1949, vol. 164, p. 617. https://doi.org/10.1038/164617a0
Cockerell, T.D.A., Tables for the determination of the genera of Coccidae, Can. Entomol., 1899, vol. 31, pp. 273–279, 330–333.
Cockerell, T.D.A. and Bueker, E.D., Some geophilous mealy-bugs from Australia (Homoptera, Coccoidea), Am. Mus. Novit., 1930, no. 441, pp. 1–7.
Cook, L.G., Gullan, P.J., and Stewart, A.C., First-instar morphology and sexual dimorphism in the gall-inducing scale insect Apiomorpha Rubsaamen (Hemiptera: Coccoidea: Eriococcidae), J. Nat. Hist., 2000, vol. 34, pp. 879–894. https://doi.org/10.1080/002229300299291
Dietz, H.F. and Morrison, H., The Coccidae or scale insects of Indiana, Ann. Rep. State Entomol. Indiana, 1916, vol. 8, pp. 195–321.
Foldi, I., Defense strategies in scale insects: phylogenetic inference and evolutionary scenarios (Hemiptera, Coccoidea), Mém. Mus. Nat. Hist. Nat., (N.S.), Ser. A, Zool., 1997a, vol. 173, pp. 203–230.
Foldi, I., Internal anatomy of the adult female, in Soft Scale Insects: Their Biology, Natural Enemies and Control, Ben-Dov, Y. and Hodgson, C.J., Eds., Elsevier, 1997b, pp. 73–90 (World Crop Pests. vol. 7A). https://doi.org/10.1016/S1572-4379(97)80045-0
Gamper, H.A. and Koptur, S., Honeydew foraging by birds in tropical montane forests and pastures of Mexico, J. Trop. Ecol., 2010, vol. 26, pp. 335–341. https://doi.org/10.1017/S0266467409990654
Gao, T.P., Yin, X.C., Shih, C.K., et al., New insects feeding on dinosaur feathers in mid-Cretaceous amber, Nat. Commun., 2019, vol. 10, no. 5424, pp. 1–7. https://doi.org/10.1038/s41467-019-13516-4
Gao, T.P., Yin, X.Ch., Shih, Ch.K., et al., Reply to: “Insects with 100 million-year-old dinosaur feathers are not ectoparasites” and “Crawlers of the scale insect Mesophthirus (Homoptera Xylococcidae) on feathers in Burmese amber—wind transport or phoresy on dinosaurs?” Paleontol. J., 2022, vol. 56, no. 3, pp. 333–337.
García Morales, M., Denno, B.D., Miller, D.R., et al., ScaleNet: A literature-based model of scale insect biology and systematics, Database, 2016. http://scalenet.info. https://doi.org/10.1093/database/bav118
Gardner-Gee, R. and Beggs, J.R., Challenges in food-web restoration: an assessment of the restoration requirements of a honeydew-gecko trophic interaction in the Auckland region, New Zealand, Restor. Ecol., 2010, vol. 18, pp. 295–303. https://doi.org/10.1111/j.1526-100X.2010.00650.x
Gavrilov-Zimin, I.A., Ontogenesis, morphology and higher classification of archaeococcids (Homoptera: Coccinea: Orthezioidea), Zoosyst. Ross., 2018, Suppl. 2, pp. 1–260.
Gaze, P.D. and Clout, M.N., Honeydew and its importance to birds in beech forests of South Island, New Zealand, N. Zeal. J. Ecol., 1983, vol. 6, pp. 33–37.
Gimmel, M.L., Szawaryn, K., Cai, C., and Leschen, R.A., Mesozoic sooty mould beetles as living relicts in New Zealand, Proc. R. Soc. B., 2019, vol. 286, 20192176. https://doi.org/10.1098/rspb.2019.2176
Grandi, G., Introduzione allo Studio dell’Entomologia: Organizzazione, Sviluppo, Vita. Apterigoti ed Esopterigoti, vol. 1, Bologna: Edizioni agricole, 1951.
Greathead, D.J., Crawler behaviour and dispersal, in Soft Scale Insects: Their Biology, Natural Enemies and Control, Ben-Dov, Y. and Hodgson, C.J., Eds., Elsevier, 1997, pp. 339–342 (World Crop Pests. vol. 7A). https://doi.org/10.1016/S1572-4379(97)80063-2
Greenberg, R., Caballero, C.M., and Bichier, P., Defense of homopteran honeydew by birds in the Mexican highlands and other warm temperate forests, Oikos, 1993, vol. 68, pp. 519–524. https://doi.org/10.2307/3544920
Grimaldi, D.A. and Vea, I.M., Insects with 100 million-year-old dinosaur feathers are not ectoparasites, Nat. Commun., 2021, vol. 12, no. 1469, pp. 1–3. https://doi.org/10.1038/s41467-021-21751-x
Gullan, P.J. and Cook, L.G., Phenacoleachia Cockerell (Hemiptera: Coccoidea: Phenacoleachiidae) re-visited, Boll. Zool. Agrar. Bachic., 2001, vol. 33, pp. 163–173.
Hanks, L.M. and Denno, R.F., Dispersal and adaptive deme formation in sedentary coccoid insects, in Genetic Structure and Local Adaptation in Natural Insect Populations, Boston: Springer, 1998, pp. 239–262. https://doi.org/10.1007/978-1-4757-0902-5_11
Heie, O.E., Why are there so few aphid species in the temperate areas of the southern hemisphere? Eur. J. Entomol., 2013, vol. 91, pp. 127–133.
Hubbard, H.G. and Pergande, T., A new coccid on birch, USDA Entomol. Bull., (N.S.), 1898, no. 18, pp. 13–26.
Kilham, L., Feeding behavior of downy woodpeckers. I. Preference for paper birches and sexual differences, Auk, 1970, vol. 87, pp. 544–556. https://doi.org/10.2307/4083797
Köster, F. and Stoewesand, H., Schildläuse als Honigtaulieferanten für kolibris und insekten, Bonn. Zool. Beitr., 1973, vol. 24, pp. 15–23.
Koteja, J., Eriococcid crawlers (Homoptera, Coccinea) from Baltic amber, Pol. Pis. Entomol., 1988a, vol. 58, pp. 503–524.
Koteja, J., Succinikermes kulickae gen. et sp. n. (Homoptera, Coccinea) from Baltic amber, Pol. Pis. Entomol., 1988b, vol. 58, pp. 525–535.
Koteja, J., Essays on coccids (Homoptera): Sudden death in amber? Pol. Pis. Entomol., 1998, vol. 67, pp. 185–218.
Koteja, J., Scale insects (Homoptera, Coccinea) from Upper Cretaceous New Jersey amber, in Studies on Fossils in Amber, with Particular Reference to the Cretaceous of New Jersey, Grimaldi, D., Ed., Leiden: Backhuys, 2000, pp. 147–229.
Koteja, J., Xylococcidae and related groups (Hemiptera: Coccinea) from Baltic amber, Pr. Muz. Ziemi, 2008, vol. 49, pp. 19–56.
Koteja, J. and Azar, D., Scale insects from Lower Cretaceous amber of Lebanon (Hemiptera: Sternorrhyncha: Coccinea), Alavesia, 2008, vol. 2, pp. 133–167.
Koteja, J. and Liniowska, E., The clypeolabral shield in the taxonomy of the Coccinea (Homoptera), Pol. Pis. Entomol., 1976, vol. 46, pp. 653–681.
Kučerová, Z., Stored product psocids (Psocoptera): External morphology of eggs, Eur. J. Entomol., 2002, vol. 99, pp. 491–503. https://doi.org/10.14411/eje.2002.066
Kunkel, H., Scale insect honeydew as forage for honey production, in Soft Scale Insects: Their Biology, Natural Enemies and Control, Ben-Dov Y. and Hodgson C.J., Eds., Elsevier, 1997, pp. 291–302 (World Crop Pests. vol. 7A). https://doi.org/10.1016/S1572-4379(97)80059-0
Lara, C., Martínez-García, V., Ortiz-Pulido, R., et al., Temporal-spatial segregation among hummingbirds foraging on honeydew in a temperate forest in Mexico, Curr. Zool., 2011, vol. 57, pp. 56–62. https://doi.org/10.1093/czoolo/57.1.56
Latta, S.C., Gamper, H.A., and Tietz, J.R., Revising the convergence hypothesis of avian use of honeydew: evidence from Dominican subtropical dry forest, Oikos, 2001, vol. 93, pp. 250–259. https://doi.org/10.1034/j.1600-0706.2001.930208.x
Lefèvre, U., Cau, A., Hu, D., and Godefroit, P., Feather evolution in Pennaraptora, in The Evolution of Feathers: from Their Origin to the Present, Foth, C. and Rauhut, O., Eds., Cham: Springer, 2020, pp. 103–118. https://doi.org/10.1007/978-3-030-27223-4_7
Leonardi, G., Monografia delle Cocciniglie Italiane, Portici: Della Torre, 1920.
Liu, Z.J., Huang, D., Cai, C., and Wang, X., The core eudicot boom registered in Myanmar amber, Sci. Rep., 2018, vol. 8, 16765. https://doi.org/10.1038/s41598-018-35100-4
Lobdell, G.H., Two-segmented tarsi in coccids: other notes (Homoptera), Ann. Entomol. Soc. Am., 1937, vol. 30, pp. 75–80. https://doi.org/10.1093/aesa/30.1.75
Magsig-Castillo, J., Morse, J.G., Walker, G.P., et al., Phoretic dispersal of armored scale crawlers (Hemiptera: Diaspididae), J. Econ. Entomol., 2010, vol. 103, pp. 1172–1179. https://doi.org/10.1603/EC10030
Martins-Mansani, M., Faita, M.R., Orth, A.I., et al., Production of honeydew by scale insects associated with bracatinga (Mimosa scabrella Benth) in Serra Catarinense, Southern Brazil, Rev. Bras. Entomol., 2021, vol. 65, e20200072. https://doi.org/10.1590/1806-9665-RBENT-2020-0072
McClure, M.S., Role of wind, birds, deer, and humans in the dispersal of hemlock woolly adelgid (Homoptera: Adelgidae), Environ. Entomol., 1990, vol. 19, pp. 36–43. https://doi.org/10.1093/ee/19.1.36
Mordvilko, A.A., Steingel, Th.R., and Šulc, K., Instruktsiya dlya sobiraniya i sokhraneniya tlei (Aphidae), chervetsov (Coccidae), listovykh blokh (Psyllidae) i aleirodid (Aleurodidae) (Instruction for Collecting and Preserving Aphids (Aphidae), Scale Insects (Coccidae), Jumping Plant Lice (Psyllidae), and Whiteflies (Aleurodidae)), St-Petersburg: Zool. Mus. Imp. Akad. Nauk, 1910.
Morrison, H., Descriptions of new genera and species belonging to the coccid family Margarodidae, Proc. Biol. Soc. Wash., 1927, vol. 40, pp. 99–109.
Morrison, H., A classification of the higher groups and genera of the coccid family Margarodidae, USDA Tech. Bull., 1928, vol. 52, pp. 1–239.
Morrison, H., Some neotropical scale insects associated with ants (Hemiptera-Coccidae), Ann. Entomol. Soc. Am., 1929, vol. 22, pp. 33–60. https://doi.org/10.1093/aesa/22.1.33
O’Connor, J., The plumage of basal birds, in The Evolution of Feathers: from Their Origin to the Present, Foth, C. and Rauhut, O., Eds., Cham: Springer, 2020, pp. 147–172. https://doi.org/10.1007/978-3-030-27223-4_9
Perkovsky, E. and Wegierek, P., Aphid–Buchnera–Ant symbiosis; or why are aphids rare in the tropics and very rare further south? Earth Environ. Sci. Trans. R. Soc. Edinburgh, 2018, vol. 107, pp. 297–310. https://doi.org/10.1017/S1755691017000147
Poinar, G.O., Jr., Fossil evidence of scale phoresy on spiders, Beitr. Araneol., 2004, vol. 3, pp. 1878–1880.
Poinar, G.O., Jr., Lambert, J.B., and Wu, Y., Araucarian source of fossiliferous Burmese amber: Spectroscopic and anatomical evidence, J. Bot. Res. Inst. Texas, 2007, vol. 1, pp. 449–455.
Poinar, G.O., Jr., Iwaniec, U.T., Chambers, K.L., and Vega, F.E., Valviloculus pleristaminis gen. et sp. nov., a Lauralean fossil flower with valvate anthers from mid-Cretaceous Myanmar amber, J. Bot. Res. Inst. Texas, 2020, vol. 14, pp. 359–366. https://doi.org/10.17348/jbrit.v14.i2.1014
Poinar, G.O., Jr., Chambers, K.L., and Vega, F.E., Tropidogyne euthystyla sp. nov., a new small-flowered addition to the genus from mid-Cretaceous Myanmar amber, J. Bot. Res. Inst. Texas, 2021, vol. 15, pp. 113–119. https://doi.org/10.17348/jbrit.v15.i1.1053
Ponomarenko, A.G., A new insect from Cretaceous of Transbaikalia, a possible parasite of pterosaurians, Paleontol. J., 1976, vol. 10, pp. 339–343.
Reichholf, H. and Reichholf, J., “Honigtau” der Bracaatinga-Schildlaus als Winternahrung von Kolibris (Trochilida) in Süd-Brasilien, Bonn. Zool. Beitr., 1973, vol. 24, pp. 7–14.
Reynolds, D.R., Reynolds, A.M., and Chapman, J.W., Non-volant modes of migration in terrestrial arthropods, Anim. Migr., 2015, vol. 2, pp. 8–28. https://doi.org/10.2478/ami-2014-0002
Roberts, P. and Seabrook, W.A., A relationship between black rats (Rattus rattus), Seychelles fruit bats (Pteropus seychellensis aldabrensis) and the coccoid (Icerya seychellarum) (Insecta, Homoptera) on Aldabra Atoll, Seychelles, J. Zool., 1989, vol. 218, pp. 332–334. https://doi.org/10.1111/j.1469-7998.1989.tb02543.x
Russo, N.J., Cheah, C.A.J., and Tingley, M.W., Experimental evidence for branch-to-bird transfer as a mechanism for avian dispersal of the hemlock woolly adelgid (Hemiptera: Adelgidae), Environ. Entomol., 2016, vol. 45, pp. 1107–1114. https://doi.org/10.1093/ee/nvw083
Shcherbakov, D.E., Cretaceous Saurophthiridae (Aphaniptera) as pupiparous pre-fleas of diving pterosaurs, Paleontol. J., 2017, vol. 51, pp. 183–185. https://doi.org/10.1134/S0031030117020149
Shemesh, A.O., ‘He said that the manna is that called taranjebin’: Ibn Ezra against Hiwi al-Balkhi’s interpretation of the biblical story of the manna, HTS Theol. Stud., 2021, vol. 77, no. 4, pp. 1–8. https://doi.org/10.4102/hts.v77i4.6342
Shi, G., Grimaldi, D.A., Harlow, G.E., et al., Age constraint on Burmese amber based on U–Pb dating of zircons, Cret. Res., 2012, vol. 37, pp. 155–163. https://doi.org/10.1016/j.cretres.2012.03.014
Smith, A.P., Diet and feeding strategies of the marsupial sugar glider in temperate Australia, J. Anim. Ecol., 1982, vol. 51, pp. 149–166. https://doi.org/10.2307/4316
Stephens, G.R. and Aylor, D.E., Aerial dispersal of red pine scale, Matsucoccus resinosae (Homoptera: Margarodidae), Environ. Entomol., 1978, vol. 7, pp. 556–563. https://doi.org/10.1093/ee/7.4.556
Taylor, R.M. and Foster, W.A., Spider nectarivory, Am. Entomol., 1996, vol. 42, pp. 82–86. https://doi.org/10.1093/ae/42.2.82
Teixeira, F.D. and Azevedo, F.C.C. de, Honeydew foraging by birds in an Atlantic Forest fragment of Minas Gerais State, Brazil, Biota Neotrop., 2013, vol. 13, pp. 391–394. https://doi.org/10.1590/S1676-06032013000400035
Towns, D.R., Interactions between geckos, honeydew scale insects and host plants revealed on islands in northern New Zealand, following eradication of introduced rats and rabbits, in Turning the Tide: The Eradication of Invasive Species, Proc. Int. Conf. on Eradication of Island Invasives, Veitch, C.R. and Clout, M.N., Eds., Gland–Cambridge: IUCN, 2002, pp. 329–335.
Vea, I.M. and Grimaldi, D.A., Diverse new scale insects (Hemiptera: Coccoidea) in amber from the Cretaceous and Eocene with a phylogenetic framework for fossil Coccoidea, Am. Mus. Novit., 2015, no. 3823, pp. 1–15. https://doi.org/10.1206/3823.1
Wang, S., Shi, C., Cai, H.H., et al., Cretaceous fire-resistant angiosperms (preprint), Res. Sq., 2021. https://doi.org/10.21203/rs.3.rs-494355/v1
Washburn, J.O. and Frankie, G.W., Dispersal of a scale insect, Pulvinariella mesembryanthemi (Homoptera: Coccoidea) on iceplant in California, Environ. Entomol., 1981, vol. 10, pp. 724–727. https://doi.org/10.1093/ee/10.5.724
Washburn, J.O. and Washburn, L., Active aerial dispersal of minute wingless arthropods: exploitation of boundary-layer velocity gradients, Science, 1984, vol. 223, pp. 1088–1089. https://doi.org/10.1126/science.223.4640.1088
Xing, L., Cockx, P., and McKellar, R.C., Disassociated feathers in Burmese amber shed new light on mid-Cretaceous dinosaurs and avifauna, Gondwana Res., 2020, vol. 82, pp. 241–253. https://doi.org/10.1016/j.gr.2019.12.017
Yu, T., Kelly, R., Mu, L., et al., An ammonite trapped in Burmese amber, PNAS, 2019, vol. 116, pp. 11345–11350. https://doi.org/10.1073/pnas.1821292116
Zahradník, J., Scale insects—Coccinea, Klíč zvířeny ČSR, 1959, vol. 3, pp. 527–552.
ACKNOWLEDGMENTS
The author is very grateful to Tai-ping Gao (Capital Normal University, Beijing) for original photographs of Mesophthirus, San-an Wu (Beijing Forestry University) and R.A. Rakitov (Borissiak Paleontological Institute, Russian Academy of Sciences; PIN) for photographs of modern scale insects and consultations on their morphology, and N.V. Zelenkov (PIN) for consultations on bird and dinosaur feathers.
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Don’t draw a sword against a louse (Chinese proverb)
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Shcherbakov, D.E. Crawlers of the Scale Insect Mesophthirus (Homoptera: Xylococcidae) on Feathers in Burmese Amber—Wind Transport or Phoresy on Dinosaurs?. Paleontol. J. 56, 338–348 (2022). https://doi.org/10.1134/S0031030122030121
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DOI: https://doi.org/10.1134/S0031030122030121