Comparing galling insect richness among Neotropical savannas: effects of plant richness, vegetation structure and super-host presence

Plant species diversity maintains the stability of ecosystems and the diversity of consumer species such as insect herbivores. Considering that gall-inducing insects are highly specialized on their host plants and dependent on the occurrence, abundance and distribution of plants, we evaluated the diversity patterns of gall-inducing insect along Brazilian Neotropical savannas and the potential role of plant species richness, vegetation structure and super-host presence on determining these patterns. We found 1,882 individual plants that belonged to 64 different host plant species grouped in 31 families, associated to 112 galling insect species. The galling richness was positively influenced by plant species richness and the presence of the super-host genus Qualea (Vochysiaceae). Plant species richness explained 48 % of the galling richness and areas with presence of super-hosts had more than twice of galling species than areas where they were absent. On the other hand, we found no evidence that larger plants hosted more species of galling insects. We observed that for the diversity of galling insects in the Brazilian Cerrado, vegetation structure explained almost the same portion as plant richness, because structural variables did not have an effect on residuals of galling richness and plant richness regression. Our findings suggests that plant richness has a more important role on the mitigation of natural enemies and adaptive radiation of galling species, while structural aspects of the vegetation does not seem to have that effect. Furthermore, we show that the super-host taxa provide an increment in local galling richness because they present a great diversity of local number of gall morphospecies (i.e. alpha diversity) and the high turnover of morphospecies among different localities (i.e. beta diversity). Therefore we argue that the quality of resources (richness and super host presence) appears to be a most important factor for the diversity of galling insects in Neotropical systems, than the amount of resources.     

Cytological and histochemical gradients on two <Emphasis Type="BoldItalic">Copaifera langsdorffii</Emphasis> Desf. (Fabaceae)—Cecidomyiidae gall systems

Previous ultrastructural and histochemical analysis proposed patterns in the accumulation of substances in galls of Diptera: Cecidomyiidae in some plant species of the temperate region. Similar analyses were done to verify the conservativeness of these patterns in the Neotropical region, where a great number of species of Cecidomyiidae is responsible for a wide diversity of morphotypes. Two gall morphotypes induced by Cecidomyiidae in a unique host plant, Copaifera langsdorffii, were studied. The gradients of carbohydrates and the activity of invertases and acid phosphatases were similar, but the cytological gradients and distribution of proteins evidenced that the sites of the induction as well as the amount of neoformed tissues may be peculiar to each gall system. The production of lipids just in the secretory cavities either in the non-galled or galled tissues indicated a potentiality of the host plant which could not be manipulated by the galling insects. Further, the absence of nucleus in the nutritive tissue, an exclusive feature of the horn-shaped galls, indicates cell death attributed to the feeding habit of the galling herbivore.     

Edge effect benefits galling insects in the Brazilian Amazon

We investigated the influence of edge effects on communities of galling insects in the Brazilian Amazon. For this, were performed data analyses comparing the galling richness between disturbed and undisturbed areas, and subsequently evaluated the richness of galling at different distances from the forest edge. We registered 194 galling insect morphotypes in 116 host plant species. Galling insect richness was more pronounced in disturbed areas and closer to the forest edge, both to community in general as to specific host plant taxa. These results indicate positive responses of galling insect richness to edge effects in forest environments. Edge effect could influence the galling distribution in modified habitats because increases the stress conditions of the plants and decreases the attack pressure of natural enemies.     

Diversity of galling arthropods and host plants in a subtropical forest of Porto Alegre, southern Brazil

Many hypotheses have been proposed to explain diversity patterns of galling insects. However, there are contradictory evidences on the evolutionary and ecological factors responsible for the trends. Furthermore, questions such as arthropod seasonality, sampling sufficiency and sampling team experience have been almost ignored. This study records galling arthropod diversity while paying attention to these questions. Seasonal sampling of galling arthropods and host plants were conducted in a humid subtropical forest of southern Brazil. Four transects were sampled twice per season, with two persons searching the vegetation for galls during 1h30min. After 96h.persons of sampling, 130 gall morphotypes on 84 species of host plants were recorded. An analysis of the numbers of galls and gall morphotypes found per transect along time showed that sampling team experience influences galler richness results and the interpretation of galler seasonality patterns. Different species had distinct seasonal patterns. Galling arthropod richness was bound to plant richness. Our results suggest that sampling team experience is an important factor that must be explicitly considered, as well as seasonality patterns of different galling species, at least for tropical/subtropical areas. Although sampling sufficiency was not reached, fauna heterogeneity at small spatial scales seems substantial: despite the proximity of the sampled transects (500 m), they harboured significantly specific faunas. This work adds to the literature records suggesting that both plant richness and specific composition of the vegetation have a strong influence on galler richness at least for local scales.     

Gall‐forming insect species richness along a non‐scleromorphic vegetation rainfall gradient in South Africa: The importance of plant community composition

Abstract Currently there is no single accepted hypothesis to explain gall‐forming insect species richness at a particular locality. Hygrothermal stress, soil nutrient availability, plant species richness, plant structural complexity, plant family or genus size, and host plant geographical range size have all been implicated in the determination of gall‐forming insect species richness. Previous studies of such richness at xeric sites have included predominantly scleromorphic vegetation, usually on nutrient‐poor soils. This study is the first to investigate gall‐forming insect species richness of xeric, non‐scleromorphic vegetation. Two habitat types were sampled at each of five localities across a rainfall gradient in the savanna biome of South Africa. The habitat types differed with respect to plant species composition and topography. Gall‐forming insect species richness did not increase with increasing hygrothermal stress or decreasing soil fertility. Rather, gall‐forming insect species richness was largely dependent on the presence of Terminalia sericea as well as other members of the Combretaceae and Mimosaceae. Plots where all these taxa were present had the highest gall‐forming insect species richness, up to 15 species, whereas plots with none of these taxa had a maximum of four galling‐insect species. Despite herb, shrub and tree strata not differing in gall‐forming insect species richness, insect galls were more common on woody than non‐woody plants. Also, stem galls were more frequent than apical or leaf galls. An alternative hypothesis to explain local gall‐forming insect species richness is suggested: galling insects may preferentially select those plant species with characteristics such as chemical toxicity, mechanical strength, degree of lignification or longevity that can be manipulated to benefit the galler. Thus plant community composition should be considered when attempting to explain gall‐forming insect species richness patterns.     

Interactions among three trophic levels and diversity of parasitoids: a case of top-down processes in Mexican tropical dry forest

The objective of this study was to analyze the relationship between plant hosts, galling insects, and their parasitoids in a tropical dry forest at Chamela-Cuixmala Biosphere Reserve in western Mexico. In 120 transects of 30 by 5 m (60 in deciduous forest and 60 in riparian habitats), 29 galling insects species were found and represented in the following order: Diptera (Cecidomyiidae, which induced the greatest abundance of galls with 22 species; 76%), Homoptera (Psylloidea, 6.9%; Psyllidae, 6.9%; Triozidae, 3.4%), Hymenoptera (Tanaostigmatidae, 3.4%; which were rare), and one unidentified morphospecies (3.4%). In all cases, there was a great specificity between galling insect species and their host plant species; one galling insect species was associated with one specific plant species. In contrast, there was no specificity between parasitoid species and their host galling insect species. Only 11 species of parasitoids were associated with 29 galling insect species represented in the following families: Torymidae (18.2%), Eurytomidae (18.2%), Eulophidae (18.2%), Eupelmidae (9.1%), Pteromalidae (9.1%), family Braconidae (9.1%), Platygastridae (9.1%), and one unidentified (9.1%). Most parasitoid species parasitized several gall species (Torymus sp.: 51.1%, Eurytoma sp.: 49.7%, Torymoides sp.: 46.9%). Therefore, the effects of variation in plant defenses do not extend to the third trophic level, because a few species of parasitoids can determine the community structure and composition of galling insect species in tropical plants, and instead, top-down processes seem to be regulating trophic interactions of galling insect species in tropical gall communities.     

Does host‐plant diversity explain species richness in insects? A test using Coccidae (Hemiptera)

1. The megadiverse herbivores and their host plants are a major component of biodiversity, and their interactions have been hypothesised to drive the diversification of both. 2. If plant diversity influences the diversity of insects, there is an expectation that insect species richness will be strongly correlated with host‐plant species richness. This should be observable at two levels (i) more diverse host‐plant groups should harbour more species of insects, and (ii) the species richness of a group of insects should correlate with the richness of the host groups it uses. However, such a correlation is also consistent with a hypothesis of random host use, in which insects encounter and use hosts in proportion to the diversity of host plants. Neither of these expectations has been widely tested. 3. These expectations were tested using data from a species‐rich group of insects – the Coccidae (Hemiptera). 4. Significant positive correlations were found between the species richness of coccid clades (genera) and the species richness of the host‐plant family or families upon which the clades occur. On a global scale, more closely related plant families have more similar communities of coccid genera but the correlation is weak. 5. Random host use could not be rejected for many coccids but randomisation tests and similarity of coccid communities on closely related plant families show that there is non‐random host use in some taxa. Overall, our results support the idea that plant diversity is a driver of species richness of herbivorous insects, probably via escape‐and‐radiate or oscillation‐type processes.     

Gall-inducing insect species richness as indicators of forest age and health

The changes in the plant community that occur during the process of succession affect the availability of resources for the community of herbivores. In this study, the richness of galling insects was evaluated in restored stands of Amazonian tropical rain forest of several ages (0-21 yr), as well as in areas of primary forest in Brazil. The richness of gallers increased with the age of the restored stands. Fifty-eight percent of the variation in the richness of galling insects was explained by forest stand age, but an increase in richness was observed at intermediate stages of succession. The greatest similarity among groups was found between the initial successional stages and intermediate ones. The results indicate a recovery of both host plants and insect community and that succession directly affects the richness and composition of these herbivores.     

Biodiversity of galling insects: historical, community and habitat effects in four neotropical savannas

Five hypotheses were tested to explain the pattern of galling insect species richness in four neotropical savanna physiognomies, 'canga ', 'campo sujo', 'cerrado' s. st., and 'cerradão', that occur in Minas Gerais, southeastern Brazil. We found 125 species of galling insects on 80 host plant species. The increase of plant species richness explained 35% of the variation in galling insect richness, corroborating the plant species richness hypothesis. Most of the galling species occurred on trees, followed by shrubs, and herbs. However, the difference in mean number of galls was only statistically significant between herbs and trees, corroborating partially the plant structural complexity hypothesis. A significant relationship was observed between galling species richness and density of herbs, and shrubs, corroborating partially the resource concentration hypothesis. Galling insect richness showed a negative correlation with magnesium, potassium, and zinc on soil, corroborating the soil fertility hypothesis. The content of magnesium, potassium, iron and CTC (T) explained 72% of the variation in galling insect richness. Plant family size positively influenced galling insect richness, corroborating the plant family size hypothesis. Overall, the results corroborate the hypothesis that predicts that habitat stress is the main factor generating the patterns of galling insect richness in Brazilian savannas.     

Diversity of galling insects in Styrax pohlii (Styracaceae): edge effect and use as bioindicators

Impacts of forest fragmentation and edge effect on plant-herbivores interactions are relatively unknown, and the relationships between galling insects and their host plants are very susceptible to environmental variations. The goal of our study was to test the edge effect hypothesis for galling insects associated with Styrax pohlii (Styracaceae) host plant. Samplings were conducted at a fragment of semi-deciduous forest in Goiania, Goiás, Brazil. Thirty host plant individuals (15 at fragment edge and 15 in its interior) were sampled in July of 2007; in each plant, 10 apical branches were collected at the top, middle and bottom crown levels. Our results supported the prediction of greater richness of gall morphotypes in the edge habitat compared with remnant interior. In a similar way, gall abundance and frequency of attacked leaves were also greater in the fragment edge. These findings consequently suggest a positive response of galling insect diversity to edge effect; in the Saint-Hilaire forest, this effect probably operates through the changes in microclimatic conditions of edge habitats, which results in an increased hygrothermal stress, a determinant factor to distribution patterns of galling insects. We also concluded that these organisms could be employed as biological indicators (i) because of their host-specificity, (ii) they are sensitive to changes in plant quality, and (iii) present dissimilar and specific responses to local variation in habitat conditions.     

Relationship between plant development, tannin concentration and insects associated with Copaifera langsdorffii (Fabaceae)

Plant development is the main factor that determines the insect-ontogeny interaction, since it leads to variations in resource quality and availability. The aim of this study was to test the hypothesis that plant development and varying tannin concentration leads to changes in species richness, abundance and composition of ants, free-feeding herbivores and galling insects associated with Copaifera langsdorffii (Fabaceae). The plant ontogeny and tannin concentration effects on insects were tested on 60 individuals with height varying from 0.9 to 11.0 m. A positive correlation was observed for tree height and species richness and abundance of ants, free-feeding and galling insects. In contrast, we did not find a significant relation between leaf tannin concentration and plant height, or richness and abundance of the different insect guilds. The assemblage of ants (composition of species) did not change between saplings and adults of C. langsdorffii. However, the assemblage of free-feeding herbivores and galling insects varied between the two development stages studied. The present study reveals an ontogenetic succession pattern for herbivore insects along the C. langsdorffii growth, probably due to both indirect and direct benefits from the host plant architecture and quality. Those plants with more complex architectures should support a wider diversity of insects, since they present higher number of sites for egg laying, housing, feeding and better environmental conditions. This is the first work to investigate the host plant ontogeny effect on insects in Cerrado “Savanna” vegetation. The pattern described, along with other previous studies, suggests a vast occurrence of ontogenetic succession in tropical areas.     

Subtropical Interactions: Comparing Galling Insect and Host Plant Diversity in Southern Brazil and Florida

Gall-inducing insects seem to have a diversity pattern distinct from the usual latitudinal decrease in species, with more species occurring in xeric environments instead. Many questions regarding galler diversity over geographical scales remain unanswered: for example, little is known about beta diversity, and the role super host plants play in local/regional richness. Our aim was to compare galling insect and host plant diversity in different biogeographical regions, but under similar environmental conditions. We sampled short stature coastal woodlands on sandy soils of the Atlantic coast in both USA (Florida) and Brazil (Rio Grande do Sul, RS), between 25° and 30° latitude. Little-used 200-m long trails were searched during 90 min for galls; there were four trails in USA and five in Brazil. Gall functional traits (galled plant organ, gall shape and colour) proportions were not different between Florida and RS. Local galling and host plant species richness also did not differ, and neither did regional galling diversity. The beta diversity pattern, however, was distinct: sites in Florida have more similar galling faunas than sites in RS. Common diversity patterns indicate common environmental biotic (plant diversity, vegetation structure) and abiotic (climate, soil) factors might be contributing to these similar responses. As Brazilian sites are in the Atlantic forest hotspot, a high galling insect beta diversity might be caused by a higher heterogeneity at larger scales—sample-based rarefaction curves were ascending for Brazil, but not for USA. Myrtaceans were super hosts in Brazil, but not in Florida, where oaks take up this role.     

Different relationships between galling and non-galling herbivore richness and plant species richness: a meta-analysis

The plant richness hypothesis (PRH) is used to explain herbivorous insect richness based on the number of plant species, predicting a positive relationship. However, the influence of plant richness on insect distribution can become stronger with greater levels of specialization of herbivores. In this meta-analysis, I tested whether there is any difference in the correlation force recorded between studies that investigated endophagous versus exophagous herbivores, and galling versus non-galling guilds, in order to determine whether more specialized groups have a stronger relationship. Furthermore, I calculated whether effect sizes were homogeneous between galling studies carried out at local and regional scales, and between tropical and temperate regions. A total of 52 correlations were analyzed between plant species richness and herbivore species richness, with 18 correlations derived from galling herbivores and 34 from non-galling herbivores. The effect sizes were significant and positive in all studies, being higher for endophages than for exophages, and for galling than for non-galling studies. These results provide evidence that groups of insects with a higher level of host specialization and specificity (e.g., endophagous and galling) exhibit a greater dependence on plant richness. There was no difference in effect sizes for galling studies between the local and regional level or between tropical and temperate groups. Despite the large variability found for galling studies, effect sizes were consistent independently of climatic region and latitudinal variation. These results suggest that the PRH for galling insects can be generalized to most ecosystem and vegetation types.     

Determinants of assemblage size for the parasitoids of Cecidomyiidae (Diptera)

Summary The parasitoids known to attack 191 phytophagous species of gall midges (Cecidomyiidae) were used to examine factors influencing parasitoid assemblage size. The number of parasitoid species a midge species supports was tested against nine variables describing geographical, biological and ecological attributes of hosts. The apparency of midge larvae was found to have the greatest influence on parasitoid assemblage size; highly visible species support more parasitoids than less visible ones. Pupation site and midge voltinism also significantly affect associated parasitoids, at least for highly apparent hosts. Biogeographic region, host-plant architecture and the plant parts infested were found to be of secondary importance. The surface texture of infested plant parts, the number of midge larvae occupying galls and the diversity of plant tissues infested have minimal apparent effects on parasitoid richness. Parasitoid assemblage size and total parasitism rates were also found to be positively correlated for 73 galling and nongalling midge species, and gallers typically suffer higher levels of parasitism than non-gallers. Using these data to test the enemy hypothesis, which proposes that the galling habit has evolved to escape attack from parasitoids, we conclude that parasitoid pressure cannot account for the presence of galls in the Cecidomyiidae.     

A meta-analysis of the effects of galling insects on host plant secondary metabolites

The idea that galling insects actively manipulate host plant chemistry has been previously documented but has not been quantified across a range of galler and host plant taxa. We present the first quantitative review of the relationship between insect galling and levels of secondary metabolites in host plants. Using meta-analytic techniques, we examined this relationship across 40 galler and host plant species combinations. We found that galling insects are associated with significantly higher levels of tannins and phenolics; however, no difference was found for volatiles. Hymenoptera, Diptera and Hemiptera were associated with higher levels of secondary metabolites; however, only Hymenoptera was significant. The climatic zone of the study area did not explain significant differences in gall-induced secondary metabolites. Overall the results show that the ability of galling insects to manipulate host plant secondary chemistry is widespread across insect and plant taxa. The evolutionary success of galling insects may be in part due to this unique ability.     

Phytophagous insect assemblages and the regional species pool: patterns and asymmetries

We describe three models predicting relationships between: (a) the taxonomic composition of the regional species pool of phytophagous insects and the composition of the phytophagous insect fauna on a host taxon; and (b) the faunal composition of two host taxa. The predictions of these models were compared with empirical data representing the regional pool of phytophages in Central Europe and the faunas of two plant taxa: the cabbage plants (Brassicaceae) and the thistles (Asteraceae: Cardueae). Three important findings emerge at a general level. (1) Different taxonomic levels of insects (orders, families, genera) of the regional pool and on the investigated host taxa are well correlated in terms of species richness, but there is no consistent trend in the variance explained by this correlation across taxonomic levels. (2) The model considering evolutionary interactions and speciation processes is consistent with patterns found in the empirical data. (3) Asymmetries in sampled species numbers of insect families on both host taxa may be accounted for by reference to the biology of these insects. We conclude that the faunas of single host taxa can provide the basis for extrapolating to the regional pool, at least at high taxonomic levels.     

Host Plant Specialization and Species Turnover of Caterpillars Among Hosts in the Brazilian Cerrado

Decrease in the species composition similarity of herbivore assemblages with increasing phylogenetic distance between host plants is a widespread pattern. Here we used data for caterpillars in the Brazilian Cerrado to investigate how the similarity in caterpillar species composition decreases as the taxonomic level and genetic distance (GD) of their host plants increases. In addition, we elucidate the plant taxonomic level that provides the greatest contribution to turnover in the caterpillar species composition among host taxa. Adult Lepidoptera were reared from caterpillars collected from 52 plants over 13 yr in the same area, with each host plant sampled for 1 yr. Most species were specialists, with 66 percent of genus specialists among the nonsingleton species. The similarity in caterpillar species composition across plant taxa decreased from host species to genera, and from host genera to orders. Above this level, the similarity was consistently low. The GD between plants explained 82 percent of the variation in the similarity of caterpillar species composition. The contribution of caterpillar species turnover among host orders from the same superorder and among host superorders from the same subclass explained 70 percent of the caterpillar species richness as a whole. Our results lend support to the view that most tropical caterpillars are host specialists. Our findings further indicate that the number of orders and superorders of plants provide the greatest contribution to the total caterpillar richness compared with all of the other host taxonomic levels combined. Abstract in Portuguese is available at http://www.blackwell‐synergy.com/loi/btp .     

The adaptive significance of insect gall distribution: survivorship of species in xeric and mesic habitats

Summary We studied the relationship between habitat moisture and gall-forming insect populations. Population sizes for most galling taxa were significantly larger in xeric habitats compared with mesic habitats. Our results indicate that the differential abundance of galling insects in these habitats is due primarily to differential mortality and survivorship. Mortality factors acting upon eight insect galling species (belonging to eight genera and four families) were measured on six species (five genera and five families) of host plants. Survival was significantly higher for galling populations inhabiting xeric habitats compared with mesic habitats. Parasitism was higher in mesic habitats in seven of eight habitats and fungus-induced diseases were higher in five of seven habitats. Mortality due to predation and other (unknown) factors showed no clear trends. Overall, there was a tendency towards lower mortality and consequently higher survival for populations inhabiting xeric habitats. We hypothesize that reduced mortality caused by natural enemies and endophytic fungi has contributed to the speciation and radiation of galling insects in apparently harsh environments.     

Insect herbivores associated with Baccharis dracunculifolia (Asteraceae): responses of gall-forming and free-feeding insects to latitudinal variation

The spatial heterogeneity hypothesis has been invoked to explain the increase in species diversity from the poles to the tropics: the tropics may be more diverse because they contain more habitats and micro-habitats. In this paper, the spatial heterogeneity hypothesis prediction was tested by evaluating the variation in richness of two guilds of insect herbivores (gall-formers and free-feeders) associated with Baccharis dracunculifolia (Asteraceae) along a latitudinal variation in Brazil. The seventeen populations of B. dracunculifolia selected for insect herbivores sampling were within structurally similar habitats, along the N-S distributional limit of the host plant, near the Brazilian sea coast. Thirty shrubs were surveyed in each host plant population. A total of 8 201 galls and 864 free-feeding insect herbivores belonging to 28 families and 88 species were sampled. The majority of the insects found on B. dracunculifolia were restricted to a specific site rather than having a geographic distribution mirroring that of the host plant. Species richness of free-feeding insects was not affected by latitudinal variation corroborating the spatial heterogeneity hypothesis. Species richness of gall-forming insects was positively correlated with latitude, probably because galling insect associated with Baccharris genus radiated in Southern Brazil. Other diversity indices and evenness estimated for both gall-forming and free feeding insect herbivores, did not change with latitude, suggesting a general structure for different assemblages of herbivores associated with the host plant B. dracunculifolia. Thus it is probable that, insect fauna sample in each site resulted of large scale events, as speciation, migration and coevolution, while at local level, the population of these insects is regulated by ecological forces which operate in the system.     

Edge effect and species–area relationships in the gall-forming insect fauna of natural forest patches in the Brazilian Pantanal

The aim of this study was to (i) measure differences in species richness between edge habitats versus interior habitats, or more precisely the edge effect, and (ii) test the species–area relationship for gall-forming insects in natural forest patches in a Brazilian floodplain (Pantanal of Mato Grosso do Sul). These patches are regionally known as capões, basically composed of woody vegetation. Twenty-seven patches were surveyed. In each patch two transects were conducted for gall sampling. One transect encircled the patches while the other was conducted in the interior of the patch, totaling 54h of sampling. Host plant and galling insect species composition differed quite characteristically between the edge and the interior of patches, but galling insect richness did not. When insect gall richness was expressed as the ratio between insect gall and host plant richness (gall per plant ratio), a weak species–area relationship was found. Our results suggest that the number of galling insects per individual plant is not affected by the size of the patch. Despite these results, the natural forest patches found in this region seem well suited for long-term studies addressing species–area relationships. With regard to herbivorous insects, these studies should be combined with research on host plant dynamics during flooding and dry seasons.