A Review of the Biology of Cerataphidini (Hemiptera, Aphididae, Hormaphidinae), Focusing Mainly on Their Life Cycles, Gall Formation, and Soldiers
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Hindawi Publishing Corporation Psyche Volume 2010, Article ID 380351, 34 pages doi:10.1155/2010/380351 Review Article A Review of the Biology of Cerataphidini (Hemiptera, Aphididae, Hormaphidinae), Focusing Mainly on Their Life Cycles, Gall Formation, and Soldiers Shigeyuki Aoki1 and Utako Kurosu2 1 Faculty of Economics, Rissho University, Osaki 4-2-16, Tokyo 141-8602, Japan 2 Faculty of Economics, Chuo University, 742-1 Higashinakano, Hachioji, Tokyo 192-0393, Japan Correspondence should be addressed to Shigeyuki Aoki, [email protected] Received 22 September 2010; Accepted 8 December 2010 Academic Editor: Ai-Ping Liang Copyright © 2010 S. Aoki and U. Kurosu. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Species of the aphid tribe Cerataphidini (Hormaphidinae) form galls of various shapes on Styrax trees, their primary host, throughout East and Southeast Asia including tropical rainforests. All known species of the tribe produce second-instar sterile soldiers on the primary host and some also produce first-instar sterile soldiers on the secondary host. Here, we review their complicated life cycles with or without host alternation, the formation process of their remarkable galls (flower-like multiple- cavity galls in particular), and all morphs including soldiers. The life cycles of cerataphidines are basically the same as those of the subfamily Eriosomatinae, but in tropical and subtropical regions their life cycles are not very rigidly tuned to seasonal changes in the climate if any. In addition, cerataphidine galls in these regions last at least several months, or at times even for over one year; thus it often takes longer than one year to complete their life cycles. 1. Introduction kinds in temperate, subtropical, and tropical regions. Second, we focus on how their galls, their flower-like multiple-cavity The tribe Cerataphidini is an aphid group of approximately galls in particular, are formed by the aphids and explain the 90 species [1], whose members produce sterile soldiers [2, 3]. hypothesis that the aphids may exploit the mechanism of Sofarasisknown,allspeciesproducesterilesecond-instar flower formation in the host plant for their gall formation. soldiers in their galls on the primary host, and some species Third, we present a review of aphid morphs that appear in also produce sterile first-instar soldiers in their open colonies the life cycles. In this section, behavioral aspects of soldiers on the secondary host [4–7]. They induce remarkable galls are reviewed and discussed. on trees of the genus Styrax (Styracaceae), which become huge (up to 35 cm across) in some species [8–11]. For these reasons, the group has recently attracted much attention 2. General Features of the Tribe Cerataphidini from researchers both inside and outside aphidology [12– 14]. However, although some good reviews of aphid soldiers 2.1. Taxonomic Position. The tribe Cerataphidini belongs to in general have been published [6, 7, 15], no extensive review the gall-forming subfamily Hormaphidinae. The Horma- of the life cycles of Cerataphidini (nor of their gall formation) phidinae is a sister group of another gall-forming subfamily, has been available to date. Because their life cycles and the the Eriosomatinae (formerly called “Pemphiginae”) [50] process of gall formation are complicated, it can be difficult (but see also [51]), whose life cycles have been studied better for non-aphidologists (and even aphidologists, too) to gain [52–54] because many species are distributed in Europe a thorough understanding of their biology. In this review, and North America. The Hormaphidinae consists of three we first focus on the life cycles and illustrate their various tribes, Cerataphidini, Hormaphidini, and Nipponaphidini, 2 Psyche Table 1: Primary hosts of Cerataphidini. Cerataphidine genus Styrax species Styrax series Astegopteryx S.suberifolius [16],S.benzoides[17],S.benzoin[18, 19] Benzoin S. japonicus [20, 21],S.formosanus[22], S. obassia [23, 24],S. Ceratovacuna Cyrta, Benzoin tonkinensis 1,S.serrulatus2, S. paralleloneurus [25] Pseudoregma S. suberifolius [26, 27],S.benzoides[28], S. paralleloneurus [29] Benzoin S. suberifolius [30],S.?benzoin[31],S.fraserensis[32],S. Ceratoglyphina Benzoin paralleloneurus [31] Chaitoregma Unknown Cerataphis (with Buchnera) S. suberifolius [33],S.subpaniculatus[10] Benzoin, Cyrta Cerataphis (without Buchnera) S. benzoides 3,S.benzoin[34],S.suberifolius[35] Benzoin S. japonicus [36],S.formosanus[37, 38], S. obassia [39], S. tonkinensis Tuberaphis Cyrta [11],S.subpaniculatus[40, 41] Glyphinaphis Unknown 1 The junior author found many galls of Ceratovacuna sp. formed on Styrax tonkinensis at Nangoa, northern Vietnam, on 11 May 1997. 2We examined a gall of Ceratovacuna sp. collected from Styrax serrulatus by P. W. Fritsch at Ithum Khola River (5000 ft alt.), eastern Nepal, in September 1994. 3We found some galls of Cerataphis sp. near brasiliensis on Styrax benzoides in Chiang Mai, northern Thailand, on 3 November 2002. Table 2: Secondary hosts of Cerataphidini. Tuberaphis, and Glyphinaphis.ThegenusAleurodaphis was once placed in this tribe [36, 42], but molecular data did Cerataphidine genus Plants not support this placement [6, 56]. In addition, one species Gramineae (Bambusoidea, grass) [42], of Aleurodaphis was found to induce galls on Stewartia Astegopteryx Zingiberaceae [42], Palmae [42], monadelpha (Theaceae) [57], not on Styrax.Themonotypic Pandanaceae [42], Musaceae [43, 44] genus Doraphis has also been placed in the Cerataphidini Ceratovacuna Gramineae (Bambusoidea, grass) [42] [1, 54], perhaps because the second generation on Populus Gramineae (Bambusoidea, grass) [42], Pseudoregma has a pair of frontal horns. However, its life cycle [52]is Zingiberaceae [42] similar to those of Hamamelistes species (Hormaphidini) Ceratoglyphina Gramineae (Bambusoidea) [42] [58, 59] in that coccidiform first-instar nymphs hibernate on Chaitoregma Gramineae (Bambusoidea) [45] twigs of the host tree, and the genus is unlikely to belong to Gramineae (Bambusoidea) [46], Palmae the Cerataphidini. [42], Pandanaceae [42], Orchidaceae Within the Cerataphidini, the first four genera (Aste- Cerataphis [42], Araceae [42], Strelitziaceae [47], gopteryx, Ceratovacuna, Pseudoregma,andCeratoglyphina) Smilacaceae [48], Moraceae [43], are known to induce peculiar, multiple-cavity galls and, 1 Zingiberaceae together with Chaitoregma whose galls are unknown, consti- Tuberaphis Loranthaceae [42], Santalaceae [49] tute a monophyletic clade [20, 60]. This has been confirmed Glyphinaphis Gramineae (Bambusoidea) [42] by molecular phylogenetic analyses [18, 31, 56, 61]. The 1 We examined specimens (apterous adults and nymphs) of Cerataphis sp. genera Cerataphis and Tuberaphis form single-cavity galls collected from a plant of Zingiberaceae by T. Fukatsu at Genting Highland, as many other gall aphids do. Galls of Glyphinaphis are yet West Malaysia, on 17 November 1995. unknown. So far as is known, all species of Tuberaphis and Glyphinaphis and most (but not all) species of Cerataphis harbor extracellular, eukaryotic symbionts instead of the in addition to a few genera (Aleurodaphis, Doraphis, Proto- prokaryote Buchnera [60]. If the acquisition of the extra- hormaphis, and Tsugaphis) whose taxonomic positions are cellular symbionts happened only once in the lineage, the unclear within the subfamily and which have been tentatively species group with the extracellular symbionts (Tuberaphis, assigned to some of the three tribes. The members within Glyphinaphis, and some Cerataphis) constitutes a mono- each tribe are well unified in the sense that the primary hosts phyletic clade, but the genus Cerataphis, which includes of Hormaphidini, Nipponaphidini, and Cerataphidini are species with extracellular symbionts (e.g., C. brasiliensis, C. confined to a single plant genus, Hamamelis (Hamameli- jamuritsu) and those without them (C. vandermeermohri, C. daceae), Distylium (Hamamelidaceae), and Styrax (Styra- bambusifoliae), is not [33]. Molecular phylogenetic analyses caceae), respectively. (Galls of some nipponaphidines have have not yet definitely settled the issue [18, 31, 56, 61, recently been found on trees of the genera Distyliopsis and 62]. Sycopsis (Hamamelidaceae) in Taiwan [55].) 2.2. Genera within the Cerataphidini. The Cerataphidini 2.3. Geographic Distribution. Cerataphidines are mainly dis- consists of the following eight genera, Astegopteryx, Ceratova- tributed in East and Southeast Asia. They induce galls on cuna, Pseudoregma, Ceratoglyphina, Chaitoregma, Cerataphis, trees of the genus Styrax, their primary host. All known Psyche 3 primary-host generations have been found there. The north- Sasa, etc.) as the secondary host. Palmae (palms) and/or ernmost record is of Tuberaphis styraci on Styrax obassia Zingiberaceae (gingers) are also often used by tropical species in Sapporo (43◦N), Hokkaido, northern Japan [63]. The of the genera Pseudoregma, Astegopteryx, and Cerataphis.The southernmost record is in Java [42, 64]. The westernmost genus Tuberaphis is peculiar in that its secondary hosts are record is in eastern India or Nepal (see footnote 2 of Table 1), confined to mistletoes of the families Santalaceae (Viscum) and the eastern border is approximately the line from Japan [49] and Loranthaceae (Loranthus, Scurrula, Dendrophtho¨e, through Sulawesi [65] to Java. Trees of the genus