Molecular phylogeny of Pemphiginae (Hemiptera: Aphididae) inferred from nuclear gene EF-1alpha sequences

Three traditional tribes of Fordini, Pemphigini and Eriosomatini comprise Pemphiginae, and there are two subtribes in Fordini and Pemphigini, respectively. Most of the species in this subfamily live heteroecious holocyclic lives with distinct primary host specificity. The three tribes of Pemphigini (except Prociphilina), Eriosomatini and Fordini use three families of plants, Salicaceae (Populus), Ulmaceae (Ulums) and Anacardiaceae (Pistacia and Rhus), as primary hosts, respectively, and form galls on them. Therefore, the Pemphigids are well known as gall makers, and their galls can be divided into true galls and pseudo-galls in type. We performed the first molecular phylogenetic study of Pemphiginae based on molecular data (EF-1alpha sequences). Results show that Pemphiginae is probably not a monophylum, but the monophyly of Fordini is supported robustly. The monophyly of Pemphigini is not supported, and two subtribes in it, Pemphigina and Prociphilina, are suggested to be raised to tribal level, equal with Fordini and Eriosomatini. The molecular phylogenetic analysis does not show definite relationships among the four tribes of Pemphiginae, as in the previous phylogenetic study based on morphology. It seems that the four tribes radiated at nearly the same time and then evolved independently. Based on this, we can speculate that galls originated independently four times in the four tribes, and there is no evidence to support that true galls are preceded by pseudo-galls, as in the case of thrips and willow sawflies.     

Systematic status of the genus Formosaphis Takahashi and the evolution of galls based on the molecular phylogeny of Pemphigini (Hemiptera: Aphididae: Eriosomatinae)

Abstract.  Aphids of the tribe Pemphigini (Hemiptera: Aphididae: Eriosomatinae) can induce pseudo-galls or galls on their primary host plants. Those belonging to subtribe Prociphilina often produce pseudo-galls, and those of the other subtribe, Pemphigina, can form not only pseudo-galls but also true galls. Pseudo-galls are all formed on the leaves, whereas true galls, although all similar in shape, can be located on the joint of the leaf blade and the petiole, the middle of the petiole and the branches of the host plant. From a first phylogenetic analysis of Pemphigini based on nuclear elongation factor-1α (EF-1α) sequences, no support was found for the monophyly of Pemphigini, but subtribe Pemphigina was monophyletic with robust support. Formosaphis obviously clusters with Pemphigina which has Populus as a primary host. Formosaphis belongs to Pemphigini and its unknown primary host is probably Populus. The evolution of galls in Pemphigina is discussed based on the phylogenetic tree drawn from EF-1α sequences and mitochondrial cytochrome oxidase subunit I (COI) sequences. The results suggest that, in this subtribe, the closed gall is preceded by an open pseudo-gall, and the galls move their locations from the joint of the leaf blade and the petiole to the middle of the petiole and, eventually, to the branch of the host plant. Such an evolutionary tendency may provide aphids with more protection and nutrition.     

The evolution of host plant manipulation by insects: molecular and ecological evidence from gall-forming aphids on Pistacia

One of the most striking characteristics of gall-forming insects is the variability in gall position, morphology, and complexity. Our knowledge of the driving forces behind the evolutionary divergence of gall types is limited. Natural enemies, competition, and behavioral constraints might be involved. We present a cladogram, based on sequences of COI and COII (1952bp), of mitochondrial DNA for the evolution of 14 species of gall-forming aphids (Fordinae). These insects induce five gall types with remarkable morphological variation on Pistacia spp. hosts. The parsimony cladogram divides the Fordinae into three lineages, Fordini and Baizongiini, and a third (new) sister group including the previously Fordini member, Smynthurodes betae (West). We then use ecological data to trace and explain the evolution of gall morphology. The aphids seem to have evolved gradually towards better ability to manipulate their host plant, induce stronger sinks, and gain higher reproductive success. We suggest that the ancestral gall type was a simple, open, "pea"-sized gall located on the leaflet midvein. Some Fordini and S. betae evolved a two-gall life cycle, inducing a new gall type on the leaflet margin. The Baizongiini improved the manipulation of their host by inducing larger galls near the midvein, with stronger sinks supporting thousands of aphids. Similar gall types are induced at similar sites on different Pistacia hosts suggesting control of the aphids on gall morphology and frequent host shifts. Thus, even extreme specialization (specific gall and host) is flexible.     

瘿绵蚜科虫瘿的多样性研究

是否形成虫瘿及虫瘿的位置、形态等是蚜虫生物学的重要特征.本文在已有标本采集记录和资料的基础上,从形成虫瘿的寄主植物、虫瘿的类型、虫瘿着生的部位和虫瘿的形态结构4方面对瘿绵蚜的虫瘿多样性进行了系统研究.结果表明该科蚜虫的虫瘿在类型上有虫瘿和伪虫瘿之别;在着生部位上,有叶片、侧脉、主脉、叶柄、复叶总轴、嫩枝等不同部位;就虫瘿而言,在形状上有尖椒状、鸡冠状、袋状、球状、黄瓜状、枫叶状和倍花状之分,在结构上有单室和多室两类.同时,基于系统分类及虫瘿多样性研究的结果,初步探讨了瘿绵蚜科虫瘿的演化,为进一步从分子水平深入研究虫瘿演化奠定基础.     

Phylogeny of Rhus gall aphids (Hemiptera : Pemphigidae) based on combined molecular analysis of nuclear EF1α and mitochondrial COII genes

Rhus gall aphids (Fordinae : Melaphidini) have a disjunct distribution in East Asia and North America and have specific host plant relationships. Some of them are of economic importance and all species form sealed galls which show great variation in shape, size, structure, and galling‐site. We present a phylogeny incorporating ten species and four subspecies of Rhus gall aphids based on 1694 base pairs of nuclear elongation factor‐1α (EF1α) and mitochondrial cytochrome oxidase subunit II (COII) DNA sequence data. The results suggest that Melaphidini is monophyletic and at the genus level, Schlechtendalia, Nurudea, and Floraphis were each monophyletic. Kaburagia and Meitanaphis were not monophyletic and therefore inconsistent with the current classification. The North American sumac gall aphid, Melaphis rhois, was most closely related to the East Asian Floraphis species, although this was poorly supported. The conservation of gall morphology with respect to aphid phylogeny rather than their host plants suggests that gall morphology is largely determined by the aphids. While there is no evidence of strict co‐speciation between the aphids and their primary host plants, switching between recently diverged host plants may be involved in the speciation process in Melaphidini.     

Evolutionary relationships of Pemphigus and allied genera (Hemiptera: Aphididae: Eriosomatinae) and their primary endosymbiont,Buchnera aphidicola

Aphids harbor primary endosymbionts, Buchnera aphidicola, in specialized cells within their body cavities. Aphids and Buchnera have strict mutualistic relationships in nutrition exchange. This ancient association has received much attention from researchers who are interested in endosymbiotic evolution. Previous studies have found parallel phylogenetic relationships between non‐galling aphids and Buchnera at lower taxonomic levels (genus, species). To understand whether relatively isolated habitats such as galls have effect on the parallel relationships between aphids and Buchnera, the present paper investigated the phylogenetic relationships of gall aphids from Pemphigus and allied genera, which induce pseudo‐galls or galls on Populus spp. (poplar) and Buchnera. The molecular phylogenies inferred from three aphid genes (COI, COII and EF‐1α) and two Buchnera genes (gnd, 16S rRNA gene) indicated significant congruence between aphids and Buchnera at generic as well as interspecific levels. Interestingly, both aphid and Buchnera phylogenies supported three main clades corresponding to the galling locations of aphids, namely leaf, the joint of leaf blade and petiole, and branch of the host plant. The results suggest phylogenetic conservatism of gall characters, which indicates gall characters are more strongly affected by aphid phylogeny, rather than host plants.     

Molecular phylogeny of Iberian Fordini (Aphididae: Eriosomatinae): implications for the taxonomy of genera Forda and Paracletus

Abstract Mediterranean representatives of the galling aphid tribe Fordini (Hemiptera: Aphididae: Eriosomatinae) are usually grouped under the subtribe term Fordina. Aphids within Fordina display two‐year life cycles, alternating between Pistacia shrubs, where they induce conspicuous galls, and roots of Poaceae species. The high number of morphs present in a given species, the lack of knowledge of the complete cycle in some species, and the similarity between homologous morphs observed in different species pose many taxonomic problems in this group. We present results of a survey to elucidate the phylogenetic relationships among Fordini species present in the Iberian Peninsula and the Canary Islands. Sequences from the nuclear long‐wavelength opsin (LWO) and translation elongation factor 1α (EF‐1α) genes and from a region of the mitochondrial DNA containing the genes encoding the subunits six and eight of the F‐ATPase were used to infer relationships among 10 Fordina species, namely Smynthurodes betae, Aploneura lentisci, Baizongia pistaciae, two Geoica species (G. utricularia and G. setulosa), three species of Forda and two of Paracletus. Relationships between and within representatives of the genera Forda and Paracletus, both exemplifying taxonomic and ecological problems, were investigated in greater depth through extensive sampling and morphometric analysis. A total of eight, six and six samples from F. formicaria, F. marginata and F. riccobonii, respectively, were included in the survey, along with 40 and 4 samples classified initially as P. cimiciformis and P. donisthorpei, respectively. Our results are relevant to current studies on the evolution of host selection by aphids and on the evolution of gall morphology. Our phylogeny suggests that the group can be divided into two main clades. One clade is composed of aphids inducing small, low‐capacity galls on either P. atlantica or P. terebinthus (Smynthurodes betae and genera Forda and Paracletus). The second clade is composed of species inducing larger galls on P. lentiscus and P. terebinthus (Aploneura lentisci, Baizongia pistaciae and Geoica species). Our results suggest that revision of diagnostic characters used in the taxonomy of Paracletus is needed, and suggest Forda rotunda as a new synonym of Paracletus cimiciformis syn.n.     

The evolution of inquilinism, host-plant use and mitochondrial substitution rates in Tamalia gall aphids

We used mitochondrial DNA data to infer phylogenies for 28 samples of gall-inducing Tamalia aphids from 12 host-plant species, and for 17 samples of Tamalia inquilinus, aphid 'inquilines' that obligately inhabit galls of the gall inducers and do not form their own galls. Our phylogenetic analyses indicate that the inquilines are monophyletic and closely related to their host aphids. Tamalia coweni aphids from different host plants were, with one exception, very closely related to one another. By contrast, the T. inquilinus aphids were strongly genetically differentiated among most of their host plants. Comparison of branch lengths between the T. coweni clade and the T. inquilinus clade indicates that the T. inquilinus lineage evolves 2.5-3 times faster for the cytochrome oxidase I gene. These results demonstrate that: (1) Tamalia inquilines originated from their gall-inducing hosts, (2) communal (multi-female) gall induction apparently facilitated the origin of inquilinism, (3) diversification of the inquilines has involved rapid speciation along host-plant lines, or the rapid evolution of host-plant races, and (4) the inquilines have undergone accelerated molecular evolution relative to their hosts, probably due to reduced effective population sizes. Our findings provide insight into the behavioural causes and evolutionary consequences of transitions from resource generation to resource exploitation.     

A galling aphid with extra life-cycle complexity: Population ecology and evolutionary considerations

In most gall-forming aphids, only the fundatrix is able to induce a gall on the host plant. In Smynthurodes betae Westw. (and a few other species), F₂ descendants emerge from the mother gall and induce their own, morphologically different galls. This constitutes an added complexity to the already very complex life cycle of gall-forming aphids. We investigated the ecology of S. betae on marked trees and shoots at four sites in Israel. Gall initiation, gall distribution and density, and temporal changes in clone size within the galls were investigated during two consecutive years. We discuss the possibility that the two-gall life cycle evolved from the typical one-gall system of most gall aphids, and the possible selective advantage of this added complexity in the life-history strategy of gall aphids. Although the total reproductive output of S. betae is not higher than in related species with a single gall per life cycle, there seems to be an advantage in the subdivision of each aphid clone into several galls, thus reducing the risk of the accidental extinction of the clone (genotype) by environmental factors, including parasites and predators.     

Biology of Asphondyliini (Diptera: Cecidomyiidae)

The family Cecidomyiidae (Diptera) including about 6100 described species displays diverse feeding habits. The tribe Asphondyliini is a well‐circumscribed monophyletic group of Cecidomyiidae and all species are known as gall inducers. Species belonging to this tribe exhibit fascinating ecological traits such as host alternation, polyphagy, extended diapause, induction of dimorphic galls and association with fungal symbionts. For these reasons, biogeographical and phylogenetic studies of Asphondyliini are of interest in elucidating the evolution of these traits, and particularly the processes of host‐range expansion, host‐plant shift and shifts in gall‐bearing organs. In order to facilitate further evolutionary studies of Asphondyliini, I review studies of systematics, biogeography, phylogeny, speciation, cytology, behavior, ecology, physiology, biological interaction and economic importance in this tribe.     

The evolution of gall parasitism accompanied by a host shift in the gall aphid, Eriosoma yangi (Homoptera: Aphidoidea)

Eriosoma aphids form leaf-roll galls on various elm species. Eriosoma yangi occurring on the Japanese elm is an obligatory "cuckoo" parasite, invading and usurping galls of other Eriosoma species. But another host race of E. yangi induces its own galls on the Chinese elm. Multivariate morphometries show that the two host races differ significantly in quantitative characters. Overwintering eggs of the parasitic form were experimentally transferred to the Chinese elm. The resultant larvae still exhibited a parasitic habit and developed into adults, which multivariate morphometries classified as the parasitic form. This form is considered different enough from the gall maker to be given a species rank. Eriosoma aphids facultatively invade other Eriosoma galls, where they sometimes deposit offspring. It is hypothesized that the parasitic form on the Japanese elm originated from a founder population which had migrated from the Chinese elm. On this new host, only those fundatrices that invade other species' galls will be able to leave offspring, because aphid fundatrices cannot gall plants other than their primary hosts. It is assumed that the parasitic form was established under intense selective pressure following a population bottleneck. This hypothesis was corroborated by field investigations at sites where the two forms occur sympatrically.     

Morphological phylogeny of gall‐forming aphids of the tribe Eriosomatini (Aphididae: Eriosomatinae)

Aphids of the tribe Eriosomatini are typically associated with the tree genera Ulmus and Zelkova as the primary host, on which they induce several types of leaf gall. To elucidate evolutionary changes in the aphid–host associations and gall morphology, phylogenetic relationships were inferred using 36 species (28 in the ingroup) and based on 52 morphological characters. Phylogenetic analysis with equal character weighting led to hundreds of most‐parsimonious trees, and the strict consensus of these was poorly resolved. However, the successive weighting of characters yielded three most‐parsimonious trees. The strict consensus of these supported the monophyly of the Eriosomatini and the monophyly of most genera. Reconstruction of the aphid–host associations on the consensus tree indicated that the ancestral Eriosomatini were associated with Zelkova and that the association with Ulmus evolved twice independently. Ancestral reconstruction suggests that galls of the leaf‐roll type are ancestral to those of the completely and incompletely closed pouch type, and that each type of pouch galls evolved independently. It is suggested that despite early diversification of the Eriosomatini on Zelkova species, Zelkova‐associated eriosomatines had become extinct or survived as relict parthenogens on the secondary host due to the elimination of Zelkova in most regions since the late Tertiary. In contrast, two large genera in the Eriosomatini, Eriosoma and Tetraneura, are associated with the largest elm section Ulmus whose elements are distributed widely in Eurasia, including boreal regions. Therefore, the available evidence suggests that the present species diversity and distribution patterns of the eriosomatines have been largely affected by the diversification and extinction of their host plants during the late Tertiary and Quaternary.     

Abundance of Gall Midges on Poulsenia armata (Moraceae): Importance of Host Plant Size and Light Environment in Tropical Rain Forests1

We studied the effects of contrasting light environments on the relationship between the host plant size of Poulsenia armata and the abundance of two gall midges in a tropical rain forest in Veracruz, Mexico. The number and density of two gall morphs (i.e., laminar and vein‐petiole galls) were positively correlated with plant size only in trees found in the forest but not in gaps. The availability of foliar area of P. armata trees was greater in forest gaps than in the forest. The foliar area was positively correlated with the abundance of laminar galls in trees in forest sites, but not with vein‐petiole galls. We concluded that the abundance of two morphs of gall midges on P. armata was associated with host plant size only in the forest trees. Larger plants had more galls than small plants, although this relationship was affected by local light environments.     

Insect herbivores as potential causes of mortality and adaptation in gallforming insects

Summary Recent studies have suggested that plant galls benefit only the insects living in them and not the host plants, and that galls are induced by insects primarily to improve the plant as a microenvironment or a food source. The potential advantage to insects of protection from their predators and parasitoids has been considered unclear and perhaps minor in importance. However, the potential threat to gallforming insects from other insect herbivores has usually been relatively neglected. This paper notes literature and observations which suggest that herbivores may either consume or be deterred by galls. Even soft leaf galls produced by Hormaphis and Phylloxera aphids appeared to deter some herbivores in the field. The threat of herbivory to galls might help explain general patterns of gall ecology and morphology, and deserves closer attention.     

Evolution of the gall wasp-host plant association

Gall wasps, or cynipids, form the second largest radiation of galling insects with more than 1300 described species. According to current views, the first cynipids were phytophagous and developed in herb stems of the Asteraceae without modifying plant growth or development. The first galls were supposedly multichambered stem swellings, and subsequent trends involved increase in gall complexity and reduction in the number of larval chambers. Gall wasps also have many of the features believed to be characteristic for phytophagous insects radiating in parallel with their host plants. We tested these hypotheses by mapping characters onto a recent estimate of higher cynipid relationships from a morphology-based analysis of exemplar taxa, controlling for phylogenetic uncertainty using bootstrapping. Characters were also mapped onto a metatree including all gall wasps, assembled from phylogenetic analyses as well as recent classifications. The results contradict many of the current hypotheses. The first cynipids with extant descendants were not Asteraceae stem feeders but induced distinct single-chambered galls in reproductive organs of herbaceous Papaveraceae, or possibly Lamiaceae. There has been a general trend toward more complex galls but the herb-stem feeders evolved from ancestors inducing distinct galls and their larval chambers are best understood as cryptic galls. Woody hosts have been colonized only three times, making the apparently irreversible transition from herbs to woody hosts one of the most conservative features of the gall wasp-host plant association. The evolution of host plant preferences is characterized by colonization of preexisting host-plant lineages rather than by parallel cladogenesis. Cynipids are mono- or oligophagous and host-plant choice is strongly phylogenetically conserved. Yet, the few major host shifts have involved remarkably distantly related plants. Many shifts have been onto plant species already exploited by other gall wasps, suggesting that interspecific parasitism among cynipids facilitates colonization of novel host plants.     

The origin and genetic differentiation of the socially parasitic aphid Tamalia inquilinus

Social and brood parasitisms are nonconsumptive forms of parasitism involving the exploitation of the colonies or nests of a host. Such parasites are often related to their hosts and may evolve in various ecological contexts, causing evolutionary constraints and opportunities for both parasites and their hosts. In extreme cases, patterns of diversification between social parasites and their hosts can be coupled, such that diversity of one is correlated with or even shapes the diversity of the other. Aphids in the genus Tamalia induce galls on North American manzanita (Arctostaphylos) and related shrubs (Arbutoideae) and are parasitized by nongalling social parasites or inquilines in the same genus. We used RNA sequencing to identify and generate new gene sequences for Tamalia and performed maximum‐likelihood, Bayesian and phylogeographic analyses to reconstruct the origins and patterns of diversity and host‐associated differentiation in the genus. Our results indicate that the Tamalia inquilines are monophyletic and closely related to their gall‐forming hosts on Arctostaphylos, supporting a previously proposed scenario for origins of these parasitic aphids. Unexpectedly, population structure and host‐plant‐associated differentiation were greater in the non‐gall‐inducing parasites than in their gall‐inducing hosts. RNA‐seq indicated contrasting patterns of gene expression between host aphids and parasites, and perhaps functional differences in host‐plant relationships. Our results suggest a mode of speciation in which host plants drive within‐guild diversification in insect hosts and their parasites. Shared host plants may be sufficient to promote the ecological diversification of a network of phytophagous insects and their parasites, as exemplified by Tamalia aphids.     

Soldier caste with morphological and reproductive division in the aphid tribe Nipponaphidini

Summary. We investigated demographic, morphological and histological aspects of Distylaphis foliorum, a gall-forming nipponaphidine aphid from Java, Indonesia, whose first instar nymphs had been reported to have enlarged forelegs and attack other insects. The gall inhabitants of D. foliorum consisted of two discrete populations; one developing normally and the other remaining at the first instar. Morphometric analysis identified two types of first instar nymphs; nymphs with relatively long forelegs and slender abdomen, and nymphs with relatively short forelegs and fat abdomen. The former nymphs were found from both young galls and mature galls, while the latter nymphs were from young galls only. Histological analysis strongly suggested a reproductive division in the first instar. In the former nymphs from mature galls, ovaries and mycetomes were degenerate and replaced by well-developed fat body cells. These results indicated that D. foliorum has a morphologically differentiated sterile soldier caste in the first instar. This study is the first report of a soldier caste with morphological and reproductive division in the aphid tribe Nipponaphidini, and suggests that highly specialized soldier castes have evolved at least four times in aphids.Received 25 June 2004; revised 24 September 2004; accepted 11 October 2004.     

EVOLUTION OF PARASITISM AMONG CLOSELY RELATED SPECIES: PHYLOGENETIC RELATIONSHIPS AND THE ORIGIN OF INQUILINISM IN GALL WASPS (HYMENOPTERA,CYNIPIDAE)

A new term, agastoparasitism, is proposed for parasitism among closely related species. Cynipid inquilines are typical agastoparasites. They cannot induce galls; instead their larvae live inside the galls formed by other cynipids. As in many other groups of agastoparasites, there are two competing hypotheses for the evolutionary origin of cynipid inquilines: either they arose from one of their cynipid hosts, and later radiated to exploit other gall-inducing cynipids (monophyletic origin), or they arose repeatedly, each inquiline from its host (polyphyletic origin). These hypotheses for the origin of cynipid inquilines were tested by a phylogenetic analysis of representative species of cynipid gall inducers and inquilines based on adult morphological characters. The analysis supported the monophyly of the inquilines and indicated an origin from gall inducers related to the genus Diastrophus, one of the current host groups. To examine whether the result of the analysis was influenced by convergent similarities among inquilines because of their similar mode of life, all putative apomorphies shared by some or all of the inquilines but not occurring in any of the gall inducers were removed. Despite this, the phylogenetic conclusions essentially remained the same, that is, the support for inquiline monophyly was not caused by convergent evolution. Based on these results, adaptive aspects of the evolutionary origin and maintenance of cynipid inquilinism are discussed, as well as general patterns in the evolution of agastoparasitism.     

Phylogeny,Evolution and Classification of Gall Wasps: The Plot Thickens

Gall wasps (Cynipidae) represent the most spectacular radiation of gall-inducing insects. In addition to true gall formers, gall wasps also include phytophagous inquilines, which live inside the galls induced by gall wasps or other insects. Here we present the first comprehensive molecular and total-evidence analyses of higher-level gall wasp relationships. We studied more than 100 taxa representing a rich selection of outgroups and the majority of described cynipid genera outside the diverse oak gall wasps (Cynipini), which were more sparsely sampled. About 5 kb of nucleotide data from one mitochondrial (COI) and four nuclear (28S, LWRh, EF1alpha F1, and EF1alpha F2) markers were analyzed separately and in combination with morphological and life-history data. According to previous morphology-based studies, gall wasps evolved in the Northern Hemisphere and were initially herb gallers. Inquilines originated once from gall inducers that lost the ability to initiate galls. Our results, albeit not conclusive, suggest a different scenario. The first gall wasps were more likely associated with woody host plants, and there must have been multiple origins of gall inducers, inquilines or both. One possibility is that gall inducers arose independently from inquilines in several lineages. Except for these surprising results, our analyses are largely consistent with previous studies. They confirm that gall wasps are conservative in their host-plant preferences, and that herb-galling lineages have radiated repeatedly onto the same set of unrelated host plants. We propose a revised classification of the family into twelve tribes, which are strongly supported as monophyletic across independent datasets. Four are new: Aulacideini, Phanacidini, Diastrophini and Ceroptresini. We present a key to the tribes and discuss their morphological and biological diversity. Until the relationships among the tribes are resolved, the origin and early evolution of gall wasps will remain elusive.     

Direct and indirect interactions involving ants, insect herbivores, parasitoids, and the host plant Baccharis dracunculifolia (Asteraceae)

Abstract.  1. The relative importance of direct and indirect interactions in controlling organism abundance is still an unresolved question. This study investigated the role of the direct and indirect interactions involving ants, aphids, parasitoids, and the host plant Baccharis dracunculifolia (Asteraceae) on a galling herbivore Baccharopelma dracunculifoliae (Homoptera: Psyllidae).
2. The effects of these interactions on the galling herbivore's performance were evaluated by an exclusion experiment during two consecutive generations of the galling insect.
3. Ants had a direct negative effect on the performance of the galling herbivore by reducing the number of nymphs per gall. In contrast, ants had no indirect effects on gall mortality through the associated parasitoids.
4. Aphids negatively affected gall development, suggesting that galls and aphids might be partitioning photoassimilates and nutrients moving throughout host-plant tissues.
5. In addition, galls that developed during the rainy season were heavier, indicating that variation in the host plant, due to weather changes, can affect the development of B. dracunculifoliae galls. However, variation in the development of B. dracunculifoliae galls due to presence of aphids or the weather changes did not affect parasitoid attack.
6. These results suggest that direct interactions between ants and galls influenced galling insect abundance, whereas numerical indirect effects involving galling insects, ants, aphids, and host plants were less conspicuous.