PsycheVolume 2012 (2012), Article ID 621934, 11 pagesdoi:10.1155/2012/621934

Review Article

Galling Aphids (Hemiptera: Aphidoidea) in China: Diversity and Host Specificity

Jing Chen1,2 and Ge-Xia Qiao¹

¹Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, No. 1 Beichen West Road, Chaoyang District, Beijing 100101, China²College of Life Sciences, Graduate University of Chinese Academy of Sciences, No. 19 Yuquan Road, Shijingshan District, Beijing 100049, China

Received 29 August 2011; Revised 2 November 2011; Accepted 10 November 2011

Academic Editor: Moshe Inbar

Copyright © 2012 Jing Chen and Ge-Xia Qiao. 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.

Abstract.

Gall formation is an interesting plant response to aphid feeding. This paper presents a review of galling aphids in China. Altogether, 157 species and subspecies in ten families and subfamilies are found to induce galls on their host plants. As many as 39% species are endemic to China. The Eriosomatinae include the highest percentage of gall-inducing species. The great diversity of gall morphology may be described in terms of five characteristics: type, site, size, shape, and structure. The host association and host specificity of galling aphids are also discussed.

1. Introduction

Aphids (Hemiptera: Aphidoidea) are an important group of phloem-feeding insects that may limit plant productivity [1] and transmit plant viruses [2]. They feed from the phloem sieve elements by penetrating their slender stylets intercellularly during which specific plant responses are triggered [3, 4]. A remarkable and interesting plant response is the formation of galls. These atypical plant tissue growths, the result of interactions between the inducer and the plant [5], reflect the complex and intimate relationship between plants and insects. Galls provide abundant nutrition [6–11], a favorable microenvironment [6, 7, 12, 13], and protection against natural enemies [6, 7, 14] to the inducer and its offspring. They also mitigate clonal mixing and maintain the genetic integrity [15, 16]. Therefore, galling aphids have been viewed as a useful model system for studying herbivore-plant interactions. Approximately 10–20% of the 4,700 aphid species known worldwide can induce galls on their host plants [17]. Gall traits are important biological characteristics of galling aphids. The shape, structure, and site of galls are highly species specific [18]. Thus, galls are commonly regarded as the extended phenotype of aphids [19–21] and hence helpful for aphid identification and phylogenetic study.

A total of approximately 1,100 aphid species are now known from China, constituting at least 23% of the world’s aphid fauna [22]. Studies of galling aphids in China focus primarily on the subfamilies Eriosomatinae and Hormaphidinae. Zhang et al. [23] and Chen and Qiao [24] systematically studied the diversity of the galls of these two subfamilies, respectively. The evolution of galls in the tribes Fordini and Pemphigini of Eriosomatinae was also discussed [10, 11]. In this paper, galling aphids in China are reviewed with special emphasis on the diversity of gall-inducing species and gall morphology. Host association and host specificity are also considered.

The aphid species information in this paper was obtained from the species records of specimens deposited in the National Zoological Museum of China, Institute of Zoology, Chinese Academy of Sciences, Beijing, China (NZMCAS) and identified by aphid taxonomists of our research group. The information about galls and host plants was taken from field collection records. The host plant species were identified by plant taxonomists of the Institute of Botany, Chinese Academy of Sciences and Beijing Forestry University. The aphid classification system used in this paper follows G. Remaudière and M. Remaudière [25].

2. Galling Aphid Diversity

At present, approximately 157 species and subspecies (14% of the total number of Chinese aphid species) are known to induce galls on their specific host plants in China. They are restricted to ten families and subfamilies, that is, Adelgidae, Phylloxeridae, Eriosomatinae, Hormaphidinae, Aphidinae, Chaitophorinae, Mindarinae, Myzocallidinae, Phyllaphidinae, and Thelaxinae. Of these gall-inducing aphid species, 83 species belong to the subfamily Eriosomatinae, 37 to Aphidinae, and 19 to Hormaphidinae. The principal groups of galling aphids and the host plants bearing galls in China are listed in Table 1.

Table 1: Taxonomy of galling aphids and host plants bearing galls in China.

Family
Subfamily/tribe
Genera
Host plants

Adelgidae

Adelges, Pineus
Picea

Phylloxeridae

Acanthochermes
Quercus

Viteus
Vitis

Aphididae
Eriosomatinae

    Eriosomatini
Aphidounguis, Colopha, Eriosoma, Kaltenbachiella, Tetraneura
Ulmus

    Fordini
Aploneura, Baizongia, Chaetogeoica, Forda, Namaforda, Smynthurodes
Pistacia

Floraphis, Kaburagia, Meitanaphis, Nurudea, Schlechtendalia
Rhus

    Pemphigini
Epipemphigus, Pachypappa, Pachypappella, Pemphigus, Thecabius
Populus

Prociphilus
Caprifoliaceae, Oleaceae, Rosaceae

Hormaphidinae

    Cerataphidini
Aleurodaphis
Sinojackia

Astegopteryx, Cerataphis, Ceratoglyphina, Ceratovacuna, Ktenopteryx, Pseudoregma
Styrax

Tuberaphis
Styrax, Viscum

    Hormaphidini
Hamamelistes
Betula

    Nipponaphidini
Asiphonipponaphis, Metanipponaphis, Neothoracaphis, Nipponaphis
Distylium

Aphidinae

    Aphidini
Aphis
Malvaceae, Prunus

Cryptosiphum
Artemisia

Hyalopterus
Rosaceae

    Macrosiphini
Cryptaphis
Geranium

Cryptomyzus, Hyperomyzus
Ribes

Diuraphis
Pooideae

Dysaphis, Myzus, Ovatus, Sappaphis, Sorbaphis, Tuberocephalus
Rosaceae

Hayhurstia
Chenopodium

Lipaphis
Cruciferae

Neorhopalomyzus
Lonicera

Rhopalosiphoninus
Deutzia, Syringa

Semiaphis
Lonicera, Umbelliferae

Chaitophorinae
Chaitophorus
Populus

Periphyllus
Acer, Aesculus, Koelreuteria

Mindarinae
Mindarus
Abies

Myzocallidinae
Tinocallis
Sapindus, Lagerstroemia

Phyllaphidinae
Phyllaphis
Fagus

Thelaxinae
Kurisakia
Quercus

Out of these galling aphids, 61 species and subspecies are endemic to China, accounting for 39% of the total galling species. Endemic species, localities (province) where galls were collected, host plants bearing galls, and gall morphology are listed in Table 2.

Table 2: Endemic galling aphid species in China.

Species
Distribution
Host plants bearing galls
Gall morphology

Adelgidae

Adelges (Gilletteella) glandulae (Zhang)
Sichuan, Yunnan
Picea brachytyla, P. likiangensis, P. likiangensis var. balfouriana, P. purpurea
Leaf gall, cone-like, multiple-cavity, without associated needles [33].

Adelges (Sacchiphantes) roseigallis (Li & Tsai)
Gansu
Picea asperata, P. crassifolia
Leaf gall, cone-like [34].

Pineus (Pineus) armandicola Zhang, Zhong & Zhang
Yunnan
Picea likiangensis
Leaf gall, cone-like or torch-like, multiple-cavity [35].

Pineus (Pineus) sichunanus Zhang
Sichuan, Yunnan
Picea brachytyla, P. likiangensis, P. likiangensis var. balfouriana, P. purpurea
Leaf gall, broom-like or torch-like, multiple-cavity [33].

Phylloxeridae

Acanthochermes similiquercus Jiang, Huang & Qiao
Sichuan
Quercus sp.
Small spherical gall on the leaf with an opening on the lower surface [36].

Eriosomatinae Eriosomatini

Eriosoma cerum Zhang
Beijing, Hebei, Inner Mongolia
Ulmus pumila
Leaf edge curls downward [37].

Eriosoma fukangense Zhang
Xinjiang
Ulmus pumila
Leaf rolls, screw-like [37].

Eriosoma multilocularis Zhang & Zhang
Beijing, Hebei
Ulmus pumila
Multiple-cavity gall on the underside of leaves, with longitudinal ridges on lateral sides [38].

Eriosoma spirifolium Zhang
Xinjiang
Ulmus pumila
Leaf curls, spiral-shaped [37].

Eriosoma togrogum Zhang
Inner Mongolia, Shaanxi
Ulmus pumila
Leaf pseudogall [39].

Eriosoma ulmipumilicola Zhang & Zhang
Hebei
Ulmus pumila
Leaf rolls and swellings [37].

Eriosoma usuense Zhang & Qiao
Xinjiang
Ulmus pumila
Leaf spirally twisted [37].

Kaltenbachiella glabra Akimoto
Taiwan
Ulmus uyematsui
Almost globular gall, without hairs, arising upward from the midrib of leaves [40].

Tetraneura (Indotetraneura) asymmachia Zhang & Zhang
Liaoning
Ulmus parvifolia, U. pumila
Leaf gall, irregular pouch-like, stalked, smooth, with secondary exit laterally [37].

Tetraneura (Tetraneura) aequiunguis Zhang & Zhang
Inner Mongolia, Shandong
Ulmus sp.
Leaf gall [41].

Tetraneura (Tetraneura) persicina Zhang & Zhang
Liaoning, Shandong
Ulmus pumila
Leaf gall, peach-shaped, stalked [37].

Tetraneura (Tetraneura) triangula Zhang & Zhang
Hebei, Shandong, Tianjin
Ulmus pumila
Irregular-shaped gall on the upper side of leaves [37].

Tetraneura (Tetraneura) ulmicema Zhang
Ningxia
Ulmus glabra
Leaf gall, smooth, without hairs [37].

Eriosomatinae Fordini

Chaetogeoica foliodentata (Tao)
Jiangsu, Shaanxi, Shandong, Sichuan, Yunnan, Zhejiang
Pistacia chinensis, P. weinmannifolia
Cockscomb-like gall, arising from the midrib on the upper surface of leaves [37].

Chaetogeoica ovagalla (Zhang)
Shandong
Pistacia chinensis
Elongate oval gall, arising from the midrib of leaves [42].

Chaetogeoica sensucopia (Zhang)
Shandong
Pistacia chinensis
Small elongate oval gall, arising from the midrib of leaves [42].

Chaetogeoica ulmidrupa Zhang
Shandong
Pistacia aculeata
Dimidiate gall, with a longitudinal ridge [43].

Chaetogeoica yunlongensis (Zhang & Zhong)
Shaanxi, Yunnan
Pistacia chinensis
Cucumber-shaped gall, arising from the midrib of leaves [42].

Floraphis choui Xiang
Shaanxi
Rhus potaninii
Gall produced on leaflets, branched with every branch obconical [44].

Floraphis meitanensis Tsai & Tang
Guizhou, Hunan, Sichuan
Rhus punjabensis var. sinica
Gall produced on the main axis of a compound leaf, flattened, branched from base [37, 45].

Kaburagia rhusicola ensigallis (Tsai & Tang)
Guizhou, Hubei, Hunan, Sichuan
Rhus punjabensis var. sinica
Elongate jujube-like gall, with a pointed tip, arising from the main vein or secondary vein on the base of leaves [37].

Kaburagia rhusicola ovatirhusicola Xiang
Hubei, Shaanxi, Yunnan
Rhus potaninii
Gall obovate, outer surface with prominent net-like veins, produced on leaflet [44].

Kaburagia rhusicola ovogallis (Tsai & Tang)
Guizhou, Hubei, Hunan, Sichuan
Rhus chinensis, R. punjabensis var. sinica
Gall ovate, tip rounded, with short hairs, arising from the secondary vein on the base of leaves [37].

Meitanaphis elongallis Tsai & Tang
Guizhou, Hubei, Hunan
Rhus punjabensis var. sinica
Gall jujube-like, outer surface with many fine longitudinal ridges, arising from the midrib on the lower surface of leaves [37, 45].

Schlechtendalia peitan (Tsai & Tang)
Guizhou, Hunan, Sichuan
Rhus chinensis, R. chinensis var. roxburghii, R. punjabensis var. sinica
Gall ovate, somewhat flattened, with short soft hairs, arising from the secondary vein on the base of leaves [37].

Eriosomatinae Pemphigini

Epipemphigus chomoensis (Zhang)
Tibet
Populus sp.
Gall cockscomb-like, outer surface uneven with 3 small protuberances, situated along the midrib on the upper surface of leaves, with a primary exit on the lower surface [46].

Epipemphigus yunnanensis (Zhang)
Guizhou, Yunnan
Populus bonatii, P. cathayana, P. yunnanensis
Gall cockscomb-like, outer surface uneven with 3–5 acute angled protuberances, situated along the midrib on the upper surface of leaves, with a primary exit on the lower surface [46].

Pachypappella aliquipila Zhang
Hebei
Populus sp.
Leaf folds [37].

Pemphigus circellatus Zhang & Zhong
Yunnan
Populus tremula var. davidiana, P. yunnanensis
Big opened gall on the branch [47].

Pemphigus cylindricus Zhang
Tibet
Populus sp.
Cylinder-shaped leaf gall [48].

Pemphigus mangkamensis Zhang
Tibet
Populus sp.
Cockscomb-like gall on the upper side of leaves [48].

Pemphigus sinobursarius Zhang
Heilongjiang, Inner Mongolia, Liaoning, Ningxia, Yunnan
Populus cathayana, P. euphratica, P. simonii
Round pouch-like gall, arising from the base of midrib on the under surface of leaves [46].

Pemphigus tibetensis Zhang
Beijing, Gansu, Hebei, Tibet, Xinjiang
Populus cathayana
Pomegranate-like gall, with thick wall and a primary exit, produced on the twig [46].

Pemphigus turritus Zhang
Gansu
Populus purdomii
Sharp chilli-like or sharp horn-like gall, arising from the midrib on the upper surface of leaves, with a primary exit on the lower surface [37, 49].

Pemphigus wuduensis Zhang
Gansu
Populus purdomii
Flattened globular gall, arising from the base of midrib on the upper surface of leaves, with a secondary exit [37, 49].

Pemphigus yangcola Zhang
Yunnan
Populus yunnanensis
Semispherical gall on the twig, smooth, with primary exit [46].

Prociphilus (Prociphilus) gambosae Zhang & Zhang
Hebei
Syringa oblata
Leaf curls [50].

Prociphilus (Prociphilus) ligustrifoliae (Tseng & Tao)
Guizhou, Shaanxi, Sichuan, Yunnan
Ligustrum japonicum, L. lucidum
Leaf curls [51].

Thecabius (Oothecabius) sequelus Zhang
Hebei, Xinjiang
Populus simonii
Leaf folds and swellings along the midrib, dumpling-shaped [52].

Thecabius (Parathecabius) zhongi Zhang
Gansu
Populus cathayana
Dumpling-shaped pseudogall, formed by folding of the two halves of a leaf together [52].

Thecabius (Thecabius) beijingensis Zhang
Beijing, Hebei, Heilongjiang, Liaoning, Shanxi
Populus beijingensis, P. cathayana, P. koreana
Leaf folds and rolls up along the midrib, forming a swollen sausage-shaped pseudogall [52].

Hormaphidinae

Aleurodaphis sinojackiae Qiao & Jiang
Jiangsu, Zhejiang
Sinojackia xylocarpa
Leaf curls, boat-shaped [53].

Asiphonipponaphis vasigalla Chen, Sorin & Qiao
Hunan
Distylium chinense
Vase-shaped gall, arising from or near the midrib on the upper surface of leaves, with a flower-shaped opening at the tip when mature [54].

Cerataphis jamuritsu (Takahashi)
Hong Kong, Taiwan
Styrax suberifolia
Large bell-shaped gall on the branch, covered with much white wax [55].

Hamamelistes similibetulae (Qiao & Zhang)
Tibet
Betula albosinensis
Small conical gall on the upper side of leaves [56].

Ktenopteryx eosocallis Qiao & Zhang
Fujian, Guangxi
Styrax odoratissima
Leaf deformation [57].

Tuberaphis cymigalla (Qiao & Zhang)
Fujian
Distylium racemosum (unlikely, requiring further confirmation)
Branched gall on the twig [58].

Tuberaphis viscisucta (Zhang)
Yunnan
Viscum album
Leaf curls [59].

Aphidinae

Cryptosiphum artemisiae linanense Zhang
Gansu, Hebei, Heilongjiang, Jilin, Liaoning, Zhejiang
Artemisia argyi, A. atrovirens, A. mongolica, A. selengensis
Leaf rolls, fist-like [60].

Cryptosiphum atriplicivorum Zhang
Gansu
Artemisia sp.
Leaf rolls and swellings [39].

Neorhopalomyzus lonicerisuctus Zhang, Zhong & Zhang
Sichuan, Yunnan
Lonicera sp.
Leaf curls [61].

Sappaphis dipirivora Zhang
Beijing
Pyrus sp.
Leaf rolls and swellings [62].

Sappaphis sinipiricola Zhang
Hebei, Henan
Pyrus betulaefolia
Leaf rolls [62].

Tuberocephalus (Trichosiphoniella) tianmushanensis Zhang
Beijing, Zhejiang
Prunus pauciflora
Leaf curls, cylinder-shaped [60].

Tuberocephalus (Trichosiphoniella) tuberculus Su, Jiang & Qiao
Sichuan
An unidentified species of Rosaceae
Pseudogall along the lateral vein of young leaves [63].

Chaitophorinae

Periphyllus acerihabitans Zhang
Jiangsu, Zhejiang
Acer buergerianum
Leaf curls [64].

3. Gall Morphological Diversity

3.1. Type

Aphids can induce both pseudogalls and true galls on their host plants. Pseudogalls are commonly found on leaves and appear as leaf folds, leaf rolls, leaf curls, or leaf blisters. In the subfamilies Aphidinae, Chaitophorinae, Mindarinae, Myzocallidinae, Phyllaphidinae, and Thelaxinae, only pseudogalls are produced. Hyalopterus pruni (Geoffroy) produces noticeable leaf-roll pseudogalls on Prunus armeniaca in the spring (Figure 1(n)). Cryptosiphum artemisiae Buckton causes leaves to swell and roll on Artemisia (Figure 1(o)). Different from pseudogalls, true galls are more diverse in shape, complex in structure, and not only located on the leaves. The Adelgidae and Phylloxeridae induce true galls on their host plants. In the Eriosomatinae and Hormaphidinae, both pseudogalls and true galls are formed. A species of Hormaphidinae, Tuberaphis takenouchii (Takahashi), forms broccoli-head-like galls on the twigs of Styrax formosana, found in Taiwan. However, its congeneric species T. viscisucta (Zhang), which occurs in Yunnan, feeds on the leaves of Viscum album and causes the leaf edges to curl downward.

(a)

(b)

(c)

(d)

(e)

(f)

(g)

(h)

(i)

(j)

(k)

(l)

(m)

(n)

(o)

Figure 1: (a) A gall of Adelges sp. on Picea crassifolia (Huangzhong, Xining, Qinghai, China; 8 July 2009): pineapple-like, multiple-cavity, closed. (b) Galls of Acanthochermes similiquercus Jiang, Huang & Qiao on a leaf of Quercus sp. (Baoding, Panzhihua, Sichuan, China; 15 April 2005): spherical, single-cavity, some matured ones are open. (c) Galls of Tetraneura (Tetraneurella) nigriabdominalis (Sasaki) on a leaf of Ulmus sp. (Hulun Buir, Inner Mongolia, China; 1 August 2004): spindle-shaped, single-cavity, closed. (d) A pseudogall of Epipemphigus imaicus (Cholodkovsky) on Populus cathayana (Shangri-La, Yunnan, China; 27 July 2010): silkworm-like, single-cavity, open on the undersurface of the leaf. (e) A gall of Pemphigus bursarius (Linnaeus) on a petiole of Populus simonii (Miyun, Beijing, China; 25 July 2009): bag-like, single-cavity, with a natural lateral opening. (f) A gall of Pemphigus immunis Buckton on a twig of Populus sp. (Miyun, Beijing, China; 25 July 2009): long saccate, single-cavity, closed. (g) A dumpling-shaped leaf-fold pseudogall of Thecabius (Oothecabius) populi (Tao) on Populus ussuriensis (Miyun, Beijing, China; 25 July 2009). (h) A gall of Chaetogeoica foliodentata (Tao) on the leaf midrib of Pistacia weinmannifolia (Qishan, Baoji, Shaanxi, China; 12 July 2004): cockscomb-like, single-cavity, closed. (i) A gall of Tuberaphis owadai Kurosu & Aoki on a twig of Styrax japonica (Yuanyang, Kunming, Yunnan, China; 10 June 2009): coral-like, single-cavity, with many small openings on the projections. (j) Galls of Asiphonipponaphis vasigalla Chen, Sorin & Qiao on the leaf midribs of Distylium chinense (Jishou, Hunan, China; 15 April 2010): vase-shaped, single-cavity, open on the bottom. (k) A gall of Metanipponaphis sp. on a petiole of Distylium chinense (Jishou, Hunan, China; 6 September 2009): global, single-cavity, closed. (l) Galls of Neothoracaphis yanonis (Matsumura) on the leaves of Distylium chinense (Jishou, Hunan, China; 21 May 2009): spherical with a pointed bottom, protruding from both sides of the leaves, single-cavity, closed. (m) A gall of Nipponaphis sp. on a twig of Distylium chinense (Jishou, Hunan, China; 5 September 2009): bottle-shaped, single-cavity, closed. (n) Leaf rolls caused by Hyalopterus pruni (Geoffroy) on Prunus armeniaca (Huangzhong, Xining, Qinghai, China; 8 July 2009). (o) Leaf rolls and swellings caused by Cryptosiphum artemisiae Buckton on Artemisia sp. (Miyun, Beijing, China; 25 July 2009).

3.2. Site

The fundatrix (the first spring generation that hatches from overwintering eggs) of each galling aphid species induces its gall at a specific site on a specific host [26]. Galls may occur on the leaf blade, the leaf vein, the petiole, the main axis of a compound leaf, twigs, branches, and roots. Viteus vitifoliae (Fitch) causes galls on grape leaves and gall-like swellings on grape roots. Pemphigus bursarius (Linnaeus) produces galls on the petioles of Populus simonii (Figure 1(e)). The galls of Floraphis meitanensis Tsai & Tang are located on the main axis of the compound leaf of Rhus punjabensis var. sinica. Among these galls, the leaf gall is the most common type.

The galling site is closely related to the sink strength of galls and therefore has important effects on the reproductive success of the fundatrix [18, 27–29]. Fundatrices compete for galling sites. Intraspecific fights have been reported in different aphid species [28, 30, 31]. Furthermore, one plant species can host several galling aphid species. These species coexist by attacking different organs of a single host plant. In China, Distylium chinense harbors at least four species of Hormaphidinae, that is, Asiphonipponaphis vasigalla Chen, Sorin & Qiao, Neothoracaphis yanonis (Matsumura), Metanipponaphis sp., and Nipponaphis sp.. They form specific galls on the leaf midrib (Figure 1(j)), the leaf blade (Figure 1(l)), the petiole (Figure 1(k)), and the twig (Figure 1(m)), respectively. This observation indicates an adaptive radiation of galling aphids that exploit different ecological niches within a host plant.

3.3. Size

Gall size is also highly variable. Some aphids make very small galls. For example, the galls of Acanthochermes similiquercus Jiang, Huang & Qiao (Figure 1(b)) are small bean sized. Each gall contains only one aphid. In contrast, some galls are extremely large. The galls of Ceratoglyphina styracicola (Takahashi) in Taiwan can reach a diameter of 9 cm and contain 100,000 aphids [32]. It is obvious that gall size is directly linked to aphid colony size. Like the galling site, size is also an important factor influencing the gall sink strength [18, 29]. The species of Hormaphidinae on Distylium chinense serve to illustrate this principle. Large galls of Nipponaphis sp. (Figure 1(m)) divert nutrients from neighboring shoots. The smaller galls of Metanipponaphis sp. (Figure 1(k)) divert nutrients only from neighboring leaves on the same shoot. The smallest galls of Neothoracaphis yanonis (Figure 1(l)) use only the leaf on which they are located.

3.4. Shape

The shapes of aphid galls vary and have been described as chilli-like, cockscomb-like, bag-like, spherical, cucumber-like, flower-like, boat-like, broccoli-head-like, banana-bundle-shaped, and so on. Gall shape is highly species specific. Galls produced by individuals of the same species are distinctively similar in shape [18]. Chaetogeoica foliodentata (Tao) produces cockscomb-like galls on Pistacia weinmannifolia (Figure 1(h)). Epipemphigus imaicus (Cholodkovsky) forms silkworm-like galls on Populus cathayana (Figure 1(d)). Different species induces different shaped galls even on the same organ of the same host plant. On the leaves of Distylium chinense, for example, Asiphonipponaphis vasigalla forms vase-shaped galls (Figure 1(j)), whereas the galls of Neothoracaphis yanonis are spherical with a pointed bottom and protrude from both sides of the leaves (Figure 1(l)). This observation suggests that gall shape is determined by the aphids rather than by the plants and gall is an extended phenotype of the aphids [20]. Fundatrix behavior during gall initiation is assumed to play a decisive role in regulating gall shape, especially complex and peculiar shapes [18, 29].

3.5. Structure

Based on the number of cavities, galls can be divided into single-cavity and multiple-cavity types. The single-cavity gall is the simplest and most common type of aphid gall. The multiple-cavity gall is composed of several subgalls with more complex ontogeny and structure [24, 65]. The Adelgidae and many galling species in the tribe Cerataphidini of Hormaphidinae produce multiple-cavity galls (see [65]). The pineapple-like galls of Adelges sp. (Figure 1(a)) are formed from spruce buds in which the developing leaves enlarge laterally and the margins merge into each other, forming multiple chambers within which the aphids feed [66]. Galls can also be categorized into two types of structure: closed and open. Some galls are initially closed and do not open until maturity. However, other galls remain open during their entire period of development. True galls include both closed and open types. In Shandong, the galls of Tetraneura (Tetraneurella) nigriabdominalis (Sasaki) (Figure 1(c)) are closed from early May through early June and then split laterally. From these slits, the alatae leave the gall to found colonies on the roots of Gramineae. However, the galls of Pemphigus bursarius have a natural lateral opening over an extended period from late May through September (Figure 1(e)). In contrast, pseudogalls are generally open and relatively simple in structure. On Populus ussuriensis, Thecabius (Oothecabius) populi (Tao) causes the leaves to fold downward, forming open dumpling-shaped pseudogalls (Figure 1(g)).

Gall shape and structure are closely related to gall fitness, the number of offspring produced within a gall. Together with gall size, gall shape and structure determine the inner surface area of the gall, the most accurate and practical measure of gall fitness [67]. The inner surface area determines the feeding area available to the nymphs within the gall and is thus correlated with the aphid colony size. It would be interesting to investigate the possibility that aphid galls tend to be more complex in shape and structure (e.g., multiple-cavity galls) to support larger colonies.

Aphid galls show great diversity of type, site, size, shape, and structure. However, these gall traits are also highly species specific. Therefore, they help to identify species, especially species that are difficult to distinguish morphologically [68]. Knowledge of the evolutionary driving forces behind the divergence of gall morphology is limited. Natural enemies [6, 7, 14, 21], competition for galling sites [26], and increasing sink strength [8, 10, 11] might have influenced the divergence of gall traits. The great variety of galls is hypothesized to be related to aphid adaptive radiation [5, 69]. Several case studies of selected aphid groups have been conducted to investigate how gall diversification has influenced aphid speciation. The gall-inducing aphid group Fordini is supposed to have radiated primarily by using different sites on the same plant organ and by enlarging the gall size [8, 10]. Its sister group, the gall-inducing Pemphigini, is assumed to have diversified by attacking different plant organs [11].

4. Host Association and Host Specificity

Gall-bearing host plants are richly abundant in China. These gall-bearing plants belong to at least 64 genera and 27 families. The common gall-bearing plants include Picea, Ulmus, Populus, Styrax, and Distylium (Table 1). Gall-inducing aphids are generally heteroecious, alternate between primary host plants (woody), where galls are produced and the sexual phase of life cycle is completed, and secondary host plants (herbaceous) where only parthenogenetic generations occur. Some aphids, however, are capable of inducing galls on secondary host plants, for example, Hamamelistes similibetulae on Betula albosinensis and Cryptosiphum artemisiae on Artemisia.

Galling aphids are strictly associated with their primary hosts. The host specificity is well defined and represented particularly in the Adelgidae, Eriosomatinae, and Hormaphidinae (Table 1). The pattern of host association differs among aphid lineages. The Adelgidae are restricted to Picea (Pinaceae). The subfamily Eriosomatinae includes three host-specific tribes: Eriosomatini on Ulmus (Ulmaceae), Fordini on Pistacia and Rhus (Anacardiaceae) (Fordina on Pistacia, Melaphidina on Rhus, resp.), and Pemphigini on Populus (Salicaceae). The Hormaphidinae include three tribes: Cerataphidini on Styrax (Styracaceae), Hormaphidini on Hamamelis (Hamamelidaceae), and Nipponaphidini on Distylium (Hamamelidaceae). But the galling species of Hormaphidini in China are restricted to their secondary host Betula (Betulaceae) owing to the absence of primary host in their distribution areas. In Aphidinae, the association is not so rigid. Most gall-inducing species are primarily associated with Rosaceae. Some other remotely related plant species, such as Lonicera (Caprifoliaceae) and Ribes (Saxifragaceae), are also occupied.

The association of galling aphids with their specific host plants is supposed to be ancient [70]. One hypothesis about what plays an important role in shaping aphid-host plant association is “fundatrix specialization” [71–74]. This hypothesis suggests that the fundatrix is highly specialized to the ancestral host and is less able to acquire new hosts than are other morphs over long evolutionary periods. It should be noted that, with few exceptions, the fundatrix, the morph that hatches from the overwintering egg on the primary host in the spring, is the only morph that can induce a gall [18, 29]. Thus, the phylogenetic constraints on the fundatrix would in some degree explain the high host specificity of galling aphids to their primary hosts.

Aphids have very intimate associations with their host plants. The aphids obtain food resources and habitat from their hosts. It is commonly assumed that host plants have a great influence on aphid diversification [75]. Two of the major hypothesized pathways of diversification in phytophagous insects are cospeciation with host plants [76, 77] and speciation through host shift [78]. Both hypotheses rely on some degree of host specialization and suggest that host plant diversity plays a major role in insect diversification [75, 79]. In particular, galling aphids are closely linked with their host plants and, as a whole, occupy a wide range of plant species. Primary host specificity is strong. Different aphid families, subfamilies, or tribes are strictly associated with different plant families or genera. We think that the high host plant diversity should have considerable influence on the diversification of galling aphids and the adaptation to different host plants in different galling lineages might have driven the divergence of galling aphids at higher taxonomic levels.

5. Conclusion

This paper has presented a preliminary review of gall-inducing aphids in China. The major groups of galling aphids were surveyed. The great diversity of gall morphology was analyzed systematically according to type, site, size, shape, and structure. These traits are highly species specific, and most are closely related to gall fitness. The host plants bearing galls are rich in species, and strong primary host specificity was found. We suggest that host association and varied gall morphology might jointly have driven the diversification and adaptive radiation of galling aphids.

Acknowledgments

The work was supported by the National Natural Sciences Foundation of China (Grant no. 30830017), National Science Funds for Distinguished Young Scientists (no. 31025024), National Science Fund for Fostering Talents in Basic Research (no. J0930004), and a grant (no. O529YX5105) from the Key Laboratory of the Zoological Systematics and Evolution of the Chinese Academy of Sciences.

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