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

Authors: Jing Chen; Ge-Xia Qiao
Journal: Psyche
 (2012)

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## 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.


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## Body

## 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 Table1.Table 1
Taxonomy of galling aphids and host plants bearing galls in China.
FamilySubfamily/tribeGeneraHost plantsAdelgidaeAdelges, PineusPiceaPhylloxeridaeAcanthochermesQuercusViteusVitisAphididaeEriosomatinaeEriosomatiniAphidounguis, Colopha, Eriosoma, Kaltenbachiella, TetraneuraUlmusFordiniAploneura, Baizongia, Chaetogeoica, Forda, Namaforda, SmynthurodesPistaciaFloraphis,Kaburagia,Meitanaphis, Nurudea, SchlechtendaliaRhusPemphiginiEpipemphigus, Pachypappa, Pachypappella, Pemphigus, ThecabiusPopulusProciphilusCaprifoliaceae, Oleaceae, RosaceaeHormaphidinaeCerataphidiniAleurodaphisSinojackiaAstegopteryx, Cerataphis, Ceratoglyphina, Ceratovacuna, Ktenopteryx,PseudoregmaStyraxTuberaphisStyrax,ViscumHormaphidiniHamamelistesBetulaNipponaphidiniAsiphonipponaphis, Metanipponaphis, Neothoracaphis, NipponaphisDistyliumAphidinaeAphidiniAphisMalvaceae,PrunusCryptosiphumArtemisiaHyalopterusRosaceaeMacrosiphiniCryptaphisGeraniumCryptomyzus, HyperomyzusRibesDiuraphisPooideaeDysaphis,Myzus,Ovatus, Sappaphis, Sorbaphis, TuberocephalusRosaceaeHayhurstiaChenopodiumLipaphisCruciferaeNeorhopalomyzusLoniceraRhopalosiphoninusDeutzia, SyringaSemiaphisLonicera, UmbelliferaeChaitophorinaeChaitophorusPopulusPeriphyllusAcer, Aesculus, KoelreuteriaMindarinaeMindarusAbiesMyzocallidinaeTinocallisSapindus, LagerstroemiaPhyllaphidinaePhyllaphisFagusThelaxinaeKurisakiaQuercusOut 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 Table2.Table 2
Endemic galling aphid species in China.
SpeciesDistributionHost plants bearing gallsGall morphologyAdelgidaeAdelges (Gilletteella) glandulae (Zhang)Sichuan, YunnanPicea brachytyla, P. likiangensis, P. likiangensis var. balfouriana, P. purpureaLeaf gall, cone-like, multiple-cavity, without associated needles [33].Adelges (Sacchiphantes) roseigallis (Li & Tsai)GansuPicea asperata, P. crassifoliaLeaf gall, cone-like [34].Pineus (Pineus) armandicola Zhang, Zhong & ZhangYunnanPicea likiangensisLeaf gall, cone-like or torch-like, multiple-cavity [35].Pineus (Pineus) sichunanus ZhangSichuan, YunnanPicea brachytyla, P. likiangensis, P. likiangensisvar.balfouriana, P. purpureaLeaf gall, broom-like or torch-like, multiple-cavity [33].PhylloxeridaeAcanthochermes similiquercus Jiang, Huang & QiaoSichuanQuercus sp.Small spherical gall on the leaf with an opening on the lower surface [36].Eriosomatinae EriosomatiniEriosoma cerum ZhangBeijing, Hebei, Inner MongoliaUlmus pumilaLeaf edge curls downward [37].Eriosoma fukangense ZhangXinjiangUlmus pumilaLeaf rolls, screw-like [37].Eriosoma multilocularis Zhang & ZhangBeijing, HebeiUlmus pumilaMultiple-cavity gall on the underside of leaves, with longitudinal ridges on lateral sides [38].Eriosoma spirifolium ZhangXinjiangUlmus pumilaLeaf curls, spiral-shaped [37].Eriosoma togrogum ZhangInner Mongolia, ShaanxiUlmus pumilaLeaf pseudogall [39].Eriosoma ulmipumilicola Zhang & ZhangHebeiUlmus pumilaLeaf rolls and swellings [37].Eriosoma usuenseZhang & QiaoXinjiangUlmus pumilaLeaf spirally twisted [37].Kaltenbachiella glabra AkimotoTaiwanUlmus uyematsuiAlmost globular gall, without hairs, arising upward from the midrib of leaves [40].Tetraneura (Indotetraneura) asymmachia Zhang & ZhangLiaoningUlmus parvifolia, U. pumilaLeaf gall, irregular pouch-like, stalked, smooth, with secondary exit laterally [37].Tetraneura (Tetraneura) aequiunguis Zhang & ZhangInner Mongolia, ShandongUlmus sp.Leaf gall [41].Tetraneura (Tetraneura) persicina Zhang & ZhangLiaoning, ShandongUlmus pumilaLeaf gall, peach-shaped, stalked [37].Tetraneura (Tetraneura) triangula Zhang & ZhangHebei, Shandong, TianjinUlmus pumilaIrregular-shaped gall on the upper side of leaves [37].Tetraneura (Tetraneura) ulmicema ZhangNingxiaUlmus glabraLeaf gall, smooth, without hairs [37].Eriosomatinae FordiniChaetogeoica foliodentata (Tao)Jiangsu, Shaanxi, Shandong, Sichuan, Yunnan, ZhejiangPistacia chinensis, P. weinmannifoliaCockscomb-like gall, arising from the midrib on the upper surface of leaves [37].Chaetogeoica ovagalla (Zhang)ShandongPistacia chinensisElongate oval gall, arising from the midrib of leaves [42].Chaetogeoica sensucopia (Zhang)ShandongPistacia chinensisSmall elongate oval gall, arising from the midrib of leaves [42].Chaetogeoica ulmidrupa ZhangShandongPistacia aculeataDimidiate gall, with a longitudinal ridge [43].Chaetogeoica yunlongensis (Zhang & Zhong)Shaanxi, YunnanPistacia chinensisCucumber-shaped gall, arising from the midrib of leaves [42].Floraphis chouiXiangShaanxiRhus potaniniiGall produced on leaflets, branched with every branch obconical [44].Floraphis meitanensis Tsai & TangGuizhou, Hunan, SichuanRhus punjabensis var. sinicaGall produced on the main axis of a compound leaf, flattened, branched from base [37, 45].Kaburagia rhusicola ensigallis (Tsai & Tang)Guizhou, Hubei, Hunan, SichuanRhus punjabensis var. sinicaElongate jujube-like gall, with a pointed tip, arising from the main vein or secondary vein on the base of leaves [37].Kaburagia rhusicola ovatirhusicola XiangHubei, Shaanxi, YunnanRhus potaniniiGall obovate, outer surface with prominent net-like veins, produced on leaflet [44].Kaburagia rhusicola ovogallis (Tsai & Tang)Guizhou, Hubei, Hunan, SichuanRhus chinensis, R. punjabensis var. sinicaGall ovate, tip rounded, with short hairs, arising from the secondary vein on the base of leaves [37].Meitanaphis elongallis Tsai & TangGuizhou, Hubei, HunanRhus punjabensis var. sinicaGall 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, SichuanRhus chinensis, R. chinensis var. roxburghii, R. punjabensis var. sinicaGall ovate, somewhat flattened, with short soft hairs, arising from the secondary vein on the base of leaves [37].Eriosomatinae PemphiginiEpipemphigus chomoensis (Zhang)TibetPopulus 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, YunnanPopulus bonatii, P. cathayana, P. yunnanensisGall 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 ZhangHebeiPopulus sp.Leaf folds [37].Pemphigus circellatus Zhang & ZhongYunnanPopulus tremula var. davidiana, P. yunnanensisBig opened gall on the branch [47].Pemphigus cylindricus ZhangTibetPopulus sp.Cylinder-shaped leaf gall [48].Pemphigus mangkamensis ZhangTibetPopulus sp.Cockscomb-like gall on the upper side of leaves [48].Pemphigus sinobursarius ZhangHeilongjiang, Inner Mongolia, Liaoning, Ningxia, YunnanPopulus cathayana, P. euphratica, P. simoniiRound pouch-like gall, arising from the base of midrib on the under surface of leaves [46].Pemphigus tibetensis ZhangBeijing, Gansu, Hebei, Tibet, XinjiangPopulus cathayanaPomegranate-like gall, with thick wall and a primary exit, produced on the twig [46].Pemphigus turritus ZhangGansuPopulus purdomiiSharp 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 ZhangGansuPopulus purdomiiFlattened globular gall, arising from the base of midrib on the upper surface of leaves, with a secondary exit [37, 49].Pemphigus yangcola ZhangYunnanPopulus yunnanensisSemispherical gall on the twig, smooth, with primary exit [46].Prociphilus (Prociphilus) gambosae Zhang & ZhangHebeiSyringa oblataLeaf curls [50].Prociphilus (Prociphilus) ligustrifoliae (Tseng & Tao)Guizhou, Shaanxi, Sichuan, YunnanLigustrum japonicum, L. lucidumLeaf curls [51].Thecabius (Oothecabius) sequelus ZhangHebei, XinjiangPopulus simoniiLeaf folds and swellings along the midrib, dumpling-shaped [52].Thecabius (Parathecabius) zhongi ZhangGansuPopulus cathayanaDumpling-shaped pseudogall, formed by folding of the two halves of a leaf together [52].Thecabius (Thecabius) beijingensis ZhangBeijing, Hebei, Heilongjiang, Liaoning, ShanxiPopulus beijingensis, P. cathayana, P. koreanaLeaf folds and rolls up along the midrib, forming a swollen sausage-shaped pseudogall [52].HormaphidinaeAleurodaphis sinojackiae Qiao & JiangJiangsu, ZhejiangSinojackia xylocarpaLeaf curls, boat-shaped [53].Asiphonipponaphis vasigalla Chen, Sorin & QiaoHunanDistylium chinenseVase-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, TaiwanStyrax suberifoliaLarge bell-shaped gall on the branch, covered with much white wax [55].Hamamelistes similibetulae (Qiao & Zhang)TibetBetula albosinensisSmall conical gall on the upper side of leaves [56].Ktenopteryx eosocallis Qiao & ZhangFujian, GuangxiStyrax odoratissimaLeaf deformation [57].Tuberaphis cymigalla (Qiao & Zhang)FujianDistylium racemosum (unlikely, requiring further confirmation)Branched gall on the twig [58].Tuberaphis viscisucta(Zhang)YunnanViscum albumLeaf curls [59].AphidinaeCryptosiphum artemisiae linanenseZhangGansu, Hebei, Heilongjiang, Jilin, Liaoning, ZhejiangArtemisia argyi, A. atrovirens, A. mongolica, A. selengensisLeaf rolls, fist-like [60].Cryptosiphum atriplicivorum ZhangGansuArtemisia sp.Leaf rolls and swellings [39].Neorhopalomyzus lonicerisuctus Zhang, Zhong & ZhangSichuan, YunnanLonicerasp.Leaf curls [61].Sappaphis dipirivora ZhangBeijingPyrus sp.Leaf rolls and swellings [62].Sappaphis sinipiricola ZhangHebei, HenanPyrus betulaefoliaLeaf rolls [62].Tuberocephalus (Trichosiphoniella) tianmushanensis ZhangBeijing, ZhejiangPrunus paucifloraLeaf curls, cylinder-shaped [60].Tuberocephalus (Trichosiphoniella) tuberculus Su, Jiang & QiaoSichuanAn unidentified species of RosaceaePseudogall along the lateral vein of young leaves [63].ChaitophorinaePeriphyllus acerihabitans ZhangJiangsu, ZhejiangAcer buergerianumLeaf 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) A gall ofAdelges 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 vasigallaChen, 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 ofMetanipponaphis 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 Artemisiasp. (Miyun, Beijing, China; 25 July 2009).
(a)(b)(c)(d)(e)(f)(g)(h)(i)(j)(k)(l)(m)(n)(o)


### 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 punjabensisvar. 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 chinenseharbors at least four species of Hormaphidinae, that is, Asiphonipponaphis vasigallaChen, 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 ofAcanthochermes 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 chinenseserve 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 vasigallaforms 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].


## 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) A gall ofAdelges 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 vasigallaChen, 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 ofMetanipponaphis 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 Artemisiasp. (Miyun, Beijing, China; 25 July 2009).
(a)(b)(c)(d)(e)(f)(g)(h)(i)(j)(k)(l)(m)(n)(o)


## 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 punjabensisvar. 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 chinenseharbors at least four species of Hormaphidinae, that is, Asiphonipponaphis vasigallaChen, 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 ofAcanthochermes 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 chinenseserve 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 vasigallaforms 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 includePicea, 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  artemisiaeon 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 (Table1). 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 Pistaciaand 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.



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*Source: 621934-2012-02-29.xml*