Leaf miners: The hidden herbivores

Leaf mining is a form of endophagous herbivory in which insect larvae live and feed within leaf tissue. In this review we discuss aspects of leaf miner ecology, and the current evidence for three hypotheses relating to the evolution of this feeding guild. We also present a summary of the literature coverage relating to these herbivores, which have been relatively poorly studied compared with insects that feed externally such as sap suckers and leaf chewers. The majority of published studies concern leaf miners from the northern hemisphere, with a general focus on those species considered to be agricultural, forestry or horticultural pests. In a more detailed case study, we examine aspects of leaf miner ecology of Australian species. At least 114 species have been recorded as leaf miners in Australia in four orders: Coleoptera, Lepidoptera, Diptera and Hymenoptera. Lepidoptera and Diptera are the most speciose orders of Australian leaf miners; Hymenoptera are represented by a single endemic genus and half of all coleopteran miners are species introduced for biological control. Both the known number of leaf‐mining species in Australia and the known number of hosts have increased in recent years following new targeted surveys. Leaf miners in Australia occur in many habitats and feed on a wide variety of host plants in at least 60 families although most individual species are monophagous. Although much of the research on leaf miners in Australia has focused on species that are commercially important pests or biological control agents, studies on fundamental aspects of leaf miner ecology are increasing. We identify a number of research questions aimed at better understanding the ecology of leaf miners in Australia and elsewhere.     

Community structure of insect herbivores on introduced and native Solidago plants in Japan

We compared community composition, density, and species richness of herbivorous insects on the introduced plant Solidago altissima L. (Asteraceae) and the related native species Solidago virgaurea L. in Japan. We found large differences in community composition on the two Solidago species. Five hemipteran sap feeders were found only on S. altissima. Two of them, the aphid Uroleucon nigrotuberculatum Olive (Hemiptera: Aphididae) and the scale insect Parasaissetia nigra Nietner (Hemiptera: Coccidae), were exotic species, accounting for 62% of the total individuals on S. altissima. These exotic sap feeders mostly determined the difference of community composition on the two plant species. In contrast, the herbivore community on S. virgaurea consisted predominately of five native insects: two lepidopteran leaf chewers and three dipteran leaf miners. Overall species richness did not differ between the plants because the increased species richness of sap feeders was offset by the decreased richness of leaf chewers and leaf miners on S. altissima. The overall density of herbivorous insects was higher on S. altissima than on S. virgaurea, because of the high density of the two exotic sap feeding species on S. altissima. We discuss the importance of analyzing community composition in terms of feeding guilds of insect herbivores for understanding how communities of insect herbivores are organized on introduced plants in novel habitats.     

Incidence of leaf mining in different vegetation types across rainfall,canopy cover and latitudinal gradients

Abstract Leaf miners are insects whose larval stages live between layers of leaf epidermis, feeding on mesophyll and lower epidermis to create mine‐like cavities. Little is known about the ecology or distribution of leaf miners in Australia. We investigated the incidence of leaf miners in relation to aridity, vegetation types, host plant taxonomy, leaf traits, canopy cover and latitude. We surveyed leaf miners at 15 sites in NSW, eastern Australia, situated along a rainfall gradient from 300 to 1700 mm per annum and a latitudinal gradient of 28°S to 33°S, within four vegetation types (mallee, heath, woodland and rainforest). Leaf mining was recorded from 36 plant species, 89% of which had no previous record of mining. The proportion of mined plant species at each site varied, but there was no significant difference between vegetation types. Leaf mining presence was positively correlated with both total leaf length and leaf thickness. No significant correlations were found between the proportion of mined species at a site and rainfall, latitude or foliar projected cover. We conclude that leaf mining is a widespread type of insect herbivory whose distribution patterns are more likely to be influenced by biotic than abiotic factors.     

EVOLUTION OF DIFFERENT GALL TYPES IN WILLOW-FEEDING SAWFLIES (HYMENOPTERA: TENTHREDINIDAE)

The sawflies that feed on the plant family Salicaceae can be divided into eight informal groups based on larval feeding habit or gall type: (1) species with free-living larvae; (2) leaf folders; (3) leaf blade gallers; (4) apical leaf gallers; (5) basal leaf gallers; (6) midrib and petiole gallers; (7) stem gallers; and (8) bud gallers. It has been proposed that the galling habit evolved from free-living larvae via leaf folders, and that the different gall types evolved gradually in the sequence mentioned above. Thus, the galling site would have “wandered” from the leaf margin toward the stem as a result of gradual changes in oviposition site preference. Allozyme data from eight informative loci were used to reconstruct the phylogeny of 18 representative sawfly species. The results suggest that indeed leaf folders seem to be a basal group; leaf blade gallers evolved independently of the other true gallers; apical and basal leaf gallers are not the ancestors of petiole and bud gallers, but they may share a common galling ancestor; bud gallers evolved from midrib/petiole gallers; and stem gallers are polyphyletic. The cause for the observed wandering of the galling site could be intraspecific competition due to a possible “nutrient shading effect” of galls situated closer to the host plant's main vascular system.     

Leaf miner and plant galler species richness on Acacia: relative importance of plant traits and climate

Diversity patterns of herbivores have been related to climate, host plant traits, host plant distribution and evolutionary relationships individually. However, few studies have assessed the relative contributions of a range of variables to explain these diversity patterns across large geographical and host plant species gradients. Here we assess the relative influence that climate and host plant traits have on endophagous species (leaf miners and plant gallers) diversity across a suite of host species from a genus that is widely distributed and morphologically variable. Forty-six species of Acacia were sampled to encapsulate the diversity of species across four taxonomic sections and a range of habitats along a 950 km climatic gradient: from subtropical forest habitats to semi-arid habitats. Plant traits, climatic variables, leaf miner and plant galler diversity were all quantified on each plant species. In total, 97 leaf mining species and 84 plant galling species were recorded from all host plants. Factors that best explained leaf miner richness across the climatic gradient (using AIC model selection) included specific leaf area (SLA), foliage thickness and mean annual rainfall. The factor that best explained plant galler richness across the climatic gradient was C:N ratio. In terms of the influence of plant and climatic traits on species composition, leaf miner assemblages were best explained by SLA, foliage thickness, mean minimum temperature and mean annual rainfall, whilst plant gall assemblages were explained by C:N ratio, %P, foliage thickness, mean minimum temperature and mean annual rainfall. This work is the first to assess diversity and structure across a broad environmental gradient and a wide range of potential key climatic and plant trait determinants simultaneously. Such methods provide key insights into endophage diversity and provide a solid basis for assessing their responses to a changing climate.     

Relationships among Key deer, insect herbivores, and plant quality

Deer can have severe effects on plant communities, which in turn can affect insect communities. We studied the effects of Key deer herbivory on the incidence of insect herbivores that occur within deer habitats in the lower Florida Keys, within the National Key Deer Refuge (NKDR). We analyzed plant chemistry (tannins, nitrogen) and surveyed for the occurrence of insects (above the browse tier) among plant species that were either deer-preferred or less-preferred. Results indicated higher levels of foliar tannins on islands with fewer Key deer and larger amounts of foliar nitrogen on islands with a high density of Key deer. Consequently, leaf miners were significantly more abundant on islands with high deer density, irrespective of deer-preference of plant species. On islands with a high deer density, incidence of leaves damaged by chewing insects was lower on preferred plant species but greater on less-preferred species than on islands with fewer deer. No apparent patterns were evident in the distribution of leaf gallers among plant species or islands with different deer density. Our results imply that plant nutrition levels—either preexisting or indirectly affected by deer deposition—are more important than plant defenses in determining the distribution of insect herbivores in the NKDR. Although high densities of the endangered Key deer have negative effects on some plant species in the NKDR, it seems Key deer might have an indirect positive influence on insect incidence primarily above the browse tier. Further research is warranted to enable fuller understanding of the interactions between Key deer and the insect community.     

Are galling insects better protected against parasitoids than exposed feeders?: a test using tenthredinid sawflies

ABSTRACT.

• 1 Data mostly from the published literature were used to assess the effect of galling on the number of parasitoid species per host species in the phylogeny of nematine sawflies from free external feeders (colonial and solitary) to leaf gallers and shoot gallers.
• 2 The strongest effects of galling were the total elimination of the species-rich cocoon-attacking guild of parasitoids, and eonymphal parasitoids, from the parasitoid community on shoot gallers, all of which are in the genus Euura.
• 3 All tachinid larval parasitoids were also eliminated by the galling habit.
• 4 The cumulative effects of these exclusions resulted in a decline in mean number of parasitoid species per host species from almost sixteen species on external colonial feeders to 4.0 species on shoot gallers.
• 5 General patterns in per cent parasitism by non-tachinid and tachinid larval parasitoids, eonymphal and cocoon parasitoids, on exposed feeders to shoot gallers, showed declines in non-tachinid attack and elimination of tachinid, eonymphal and cocoon parasitoids. But leaf gallers tended to be attacked more than exposed feeders by non-tachinid larval parasitoids.
• 6 The galling habit had a long-term impact by reducing the number of parasitoid species attacking nematine sawfly gallers and per cent mortality inflicted, so that natural enemies may have been important as a selective factor in the evolution of galling nematine sawflies.

     

Evolution of gall morphology and host-plant relationships in willow-feeding sawflies (Hymenoptera: Tenthredinidae)

Abstract.— There are over 200 species of nematine sawflies that induce galls on willows (Salix spp.). Most of the species are monoor oligophagous, and they can be separated into seven or eight different groups based on the type of gall that they induce. We studied the evolution of different gall types and host plant associations by reconstructing the phylogeny of five outgroup and 31 ingroup species using DNA sequence data from the mitochondrial cytochrome b gene. Maximum-parsimony and maximum-likelihood analyses resulted in essentially the same phylogeny with high support for important branches. The results show that: (1) the galling species probably form a monophyletic group; (2) true closed galls evolved only once, via leaf folders; (3) with the possible exception of leaf rollers, all gall type groups are mono- or paraphyletic; (4) similar gall types are closer on the phylogeny than would be expected by a random process; (5) there is an apparent evolutionary trend in galling site from the leaf edge towards the more central parts of the host plant; and (6) many willow species have been colonized several times, which excludes the possiblity of parallel cladogenesis between willows and the gallers; however, there are signs of restrictions in the evolution of host use. Many of the patterns in the evolutionary history of nematine gallers have also been observed in earlier studies on other insect gallers, indicating convergent evolution between the independent radiations.     

Similar responses of insect herbivores to leaf fluctuating asymmetry

Fluctuating asymmetry (FA) represents small, random variation from symmetry and it has been used as an indicator of plant quality and susceptibility to herbivory. In this study, the effects of FA on the responses of distinct herbivore species belonging to several guilds were examined along an environmental gradient in south Florida. This approach was chosen because it relies on a multi-species approach to the study of fluctuating asymmetry and patterns of herbivory between and within plants along an environmental gradient of salinity and plant stress. To examine differences in FA between and within plant communities, seven plant species were investigated. Four of these plants were coastal species and three species occurred in upland communities. Levels of FA were assessed before herbivory and plants were followed for the whole herbivory season in 2006. Coastal plants exhibited significantly higher salt concentration, higher percentage of asymmetric leaves and higher asymmetry levels than upland plants. Herbivore abundance varied widely amongst the seven species studied, but quantitative syntheses of our results indicated significant and positive responses of insect herbivores to leaf asymmetry: insects were 25.11% more abundant on more asymmetric plants and stronger effects of asymmetry were observed for leaf miners compared to gall-formers. As demonstrated by other recent studies, FA might be used as a reliable stress indicator, leading to similar responses of insect herbivores to variation in leaf symmetry.     

Phytochemical correlates of herbivory in a community of native and naturalized cruciferae

Oviposition and larval feeding behaviors of the crucifer specialist Pieris napi macdunnoughii correlate with leaf glucosinolate profils of plant species in a natural community. Profiles are species-specific in this group of eight Cruciferae, but particular glucosinolates are shared by subsets of the community. Pieris accepts two lethal naturalized weeds whose glucosinolate profiles resemble that of an indigenous foodplant. The results suggest that specific glucosinolates constitute insect behavioral cues which are only loosely linked evolutionarily to foodplant suitability, and further suggest that allelochemically similar community associates influence the coevolution of individual plant species with insect herbivores.     

Predicting novel trophic interactions in a non‐native world

Humans are altering the global distributional ranges of plants, while their co‐evolved herbivores are frequently left behind. Native herbivores often colonise non‐native plants, potentially reducing invasion success or causing economic loss to introduced agricultural crops. We developed a predictive model to forecast novel interactions and verified it with a data set containing hundreds of observed novel plant–insect interactions. Using a food network of 900 native European butterfly and moth species and 1944 native plants, we built an herbivore host‐use model. By extrapolating host use from the native herbivore–plant food network, we accurately forecasted the observed novel use of 459 non‐native plant species by native herbivores. Patterns that governed herbivore host breadth on co‐evolved native plants were equally important in determining non‐native hosts. Our results make the forecasting of novel herbivore communities feasible in order to better understand the fate and impact of introduced plants.     

Negative impact of leaf gallers on arctic-alpine dwarf willow, Salix herbacea

According to available evidence, leaf gallers have only minor impacts on their plant hosts. We hypothesised that the relatively large leaf gallers formed by Eupontania sawflies on small, creeping arctic-alpine willows have a strong influence on their host plants. In this study, we specifically tested the effects of leaf galler (Eupontania aquilonis) on the survival and growth of dwarf willow (Salix herbacea) in a mountain snow-bed in northern Finland. We marked galled, leaves-removed and untreated ramets in experimental blocks. In the following year, we measured the growth and survival of the ramets. The mortality of galled shoots was approx. 40% higher, and the mortality of galled ramets approx. 25% higher than in the control ramets and in the leaf-removal treatment. The leaf biomass of galled ramets and the number of leaves were significantly less in galled ramets than in untreated or leaves-removed ramets. It is possible that galling causes fatal resource depletion of shoots in its host plant. The results show that leaf gallers are ecologically more influential than previously thought.     

Clumped distribution of oak leaf miners between and within plants

Leaf miners typically show non-random distributions both between and within plants. We tested the hypothesis that leaf miners on two oak species were clumped on individual host trees and individual branches and addressed whether clumping was influenced by aspects of plant quality and how clumping and/or interactions with other oak herbivores affected leaf-miner survivorship. Null models were used to test whether oak herbivores and different herbivore guilds co-occur at the plant scale. Twenty individual Quercus geminata plants and 20 Quercus laevis plants were followed over the season for the appearance of leaf miners and other herbivores, and foliar nitrogen, tannin concentration, leaf toughness and leaf water content were evaluated monthly for each individual tree. The survivorship of the most common leaf miners was evaluated by following the fate of marked mines in several combinations that involved intra- and inter-specific associations. We observed that all leaf miners studied were clumped at the plant and branch scale, and the abundance of most leaf-miner species was influenced by plant quality traits. Mines that occurred singly on leaves exhibited significantly higher survivorship than double and triple mines and leaves that contained a mine or a leaf gall and a mine and damage by chewers exhibited lowest survivorship. Although leaf miners were clumped at individual host trees, null model analyses indicated that oak herbivores do not co-occur significantly less than expected by chance and there was no evidence for biological mechanisms such as inter-specific competition determining community structure at the plant scale. Thus, despite co-occurrence resulting in reduced survivorship at the leaf scale, such competition was not strong enough to structure separation of these oak herbivore communities.     

Perfect is best: low leaf fluctuating asymmetry reduces herbivory by leaf miners

Fluctuating asymmetry (FA) represents small, random variation from symmetry and can be used as an indicator of plant susceptibility to herbivory. We investigated the effects of FA of two oak species, Quercus laevis and Q. geminata, and the responses of three herbivore guilds: leaf miners, gallers, and chewers. To examine differences in FA and herbivory between individuals, 40 leaves from each tree were collected, and FA indices were calculated. To examine differences in FA and herbivory within-individuals, we sampled pairs of mined and unmined leaves for asymmetry measurements. Differences in growth of leaf miners between leaf types were determined by tracing 50 mines of each species on symmetric leaves and asymmetric leaves. Asymmetric leaves contained significantly lower concentrations of tannins and higher concentrations of nitrogen than symmetric leaves for both plant species. Both frequency of asymmetric leaves on plants and levels of asymmetry positively influenced the abundance of Brachys, Stilbosis and other leaf miners, but no significant relationship between asymmetry and herbivory was observed for Acrocercops. Brachys and Stilbosis mines were smaller on asymmetric leaves, but differences in mine survivorship between symmetric and asymmetric leaves were observed only for Stilbosis mines. This study indicated that leaf miners might use leaf FA as a cue to plant quality, although differential survivorship among leaf types was not observed for all species studied. Reasons for the different results between guilds are discussed.     

Taxonomic homogenization and differentiation across Southern Ocean Islands differ among insects and vascular plants

Aim To investigate taxonomic homogenization and/or differentiation of insect and vascular plant assemblages across the Southern Ocean Islands (SOI), and how they differ with changing spatial extent and taxonomic resolution. Location Twenty‐two islands located across the Southern Ocean, further subdivided into five island biogeographical provinces. These islands are used because comprehensive data on both indigenous and non‐indigenous insect and plant species are available. Methods An existing database was updated, using newly published species records, identifying the indigenous and non‐indigenous insect and vascular plant species recorded for each island. Homogenization and differentiation were measured using Jaccard’s index (JI) of similarity for assemblages across all islands on a pairwise basis, and for island pairs within each of the biogeographical provinces. The effects of taxonomic resolution (species, genus, family) and distance on levels of homogenization or differentiation were examined. To explore further the patterns of similarity among islands for each of the taxa and groupings (indigenous and non‐indigenous), islands were clustered based on JI similarity matrices and using group averaging. Results Across the SOI, insect assemblages have become homogenized (0.7% increase in similarity at species level) while plant assemblages have become differentiated at genus and species levels. Homogenization was recorded only when pairwise distances among islands exceeded 3000 km for insect assemblages, but distances had to exceed 10,000 km for plant assemblages. Widely distributed non‐indigenous plant species tend to have wider distributions across the SOI than do their insect counterparts, and this is also true of the indigenous species. Main conclusions Insect assemblages across the SOI have become homogenized as a consequence of the establishment of non‐indigenous species, while plant assemblages have become more differentiated. The likely reason is that indigenous plant assemblages are more similar across the SOI than are insect assemblages, which show greater regionalization. Thus, although a suite of widespread, typically European, weedy, non‐indigenous plant species has established on many islands, the outcome has largely been differentiation. Because further introductions of insects and vascular plants are probable as climates warm across the region, the patterns documented here are likely to change through time.     

Species richness of herbivores on exotic host plants increases with time since introduction of the host

Aim Species richness of insect herbivores feeding on exotic plants increases with abundance as well as range size of the host in the area of introduction. The formation of these herbivore assemblages requires a certain amount of time, and the richness of insect faunas should also increase with the length of time an exotic plant has been present in the introduced range. Location Central Europe. Methods We analysed the variation in species richness of leaf‐chewing Lepidoptera larvae and sap‐sucking Auchenorrhyncha (Hemiptera) associated with 103 exotic woody plant species in Germany in relation to time since introduction, range size, growth form (trees versus shrubs), biogeographical origin (distance from Central Europe) and taxonomic isolation of the host plant (presence or absence of a native congener in the introduced area). Results Using simple correlation analyses we found for Lepidoptera and Auchenorrhyncha that species richness increased with time since introduction of the host plant. For the Lepidoptera the increase of species richness with time since introduction remained significant even after removing the effects of all other independent variables. Main conclusions Our results provide some evidence that assemblages of insects on exotic plants do not reach saturation within a time scale of few hundred years. This contrasts with previous findings for crop plants.     

Comparison of invertebrate herbivores on native and non‐native Senecio species: Implications for the enemy release hypothesis

The enemy release hypothesis posits that non‐native plant species may gain a competitive advantage over their native counterparts because they are liberated from co‐evolved natural enemies from their native area. The phylogenetic relationship between a non‐native plant and the native community may be important for understanding the success of some non‐native plants, because host switching by insect herbivores is more likely to occur between closely related species. We tested the enemy release hypothesis by comparing leaf damage and herbivorous insect assemblages on the invasive species Senecio madagascariensis Poir. to that on nine congeneric species, of which five are native to the study area, and four are non‐native but considered non‐invasive. Non‐native species had less leaf damage than natives overall, but we found no significant differences in the abundance, richness and Shannon diversity of herbivores between native and non‐native Senecio L. species. The herbivore assemblage and percentage abundance of herbivore guilds differed among all Senecio species, but patterns were not related to whether the species was native or not. Species‐level differences indicate that S. madagascariensis may have a greater proportion of generalist insect damage (represented by phytophagous leaf chewers) than the other Senecio species. Within a plant genus, escape from natural enemies may not be a sufficient explanation for why some non‐native species become more invasive than others.     

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.     

Influence of feeding guild on insect response to host plant fertilization

Abstract.

• 1 The densities of insect herbivores in fertilized and unfertilized field plots of goldenrods, Solidago altissima (Compositae), were monitored over a period of 4 years.
• 2 A total of seventeen insect taxa occurred on the plots over the course of the study, including sap feeders, leaf chewers, leaf miners, leaf gallers and stem gallers with multiple representatives in each of these feeding guilds.
• 3 Nine of the seventeen taxa significantly increased in density on fertilized plots in at least one year of the study, two taxa showed marginally significant increases on fertilized plots, two significantly decreased in density on fertilized plots in at least one year, and the remaining taxa were unaffected by the fertilizer treatment.
• 4 The effects of fertilization on the insects were not strongly related to feeding guild; the group of insects that increased on fertilized plots was functionally diverse, and for the most part members of the same guild did not respond to the fertilizer treatment in consistent ways.
• 5 Differences between fertilized and unfertilized plots were greatest in the fourth year. The insects that showed delayed responses to fertilizer treatment may have been affected by changes in microclimate that developed slowly over the course of the study, suggesting that long-term studies may be necessary to detect effects of host plant stress on insect herbivores.

     

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.