Host plant intraspecific variation determines gall traits

• Galls display a multiplicity of traits, including colours, which are driven by pigment accumulation. Their conspicuousness has attracted researchers' attention and several hypotheses have been raised. However, plants themselves vary intra-specifically, including in their pigment concentrations. As galls are a result of host tissue development, colours may be a by-product of the host's own traits, being more conspicuous simply because the sites where galls develop already have the predisposition to accumulate more pigment. Here, we call this the host variation hypothesis.
• We test this hypothesis using the system of galls induced by Palaeomystella oligophaga on Macairea radula host plant. Using spectrophotometry, we calculated the Anthocyanin Reflectance Index (ARI) of gall projections, which are responsible for their characteristic colours. We tested the influence of occupant identity (galling insect or any natural enemy), gall volume, parenchyma thickness, height from the ground, ARI of leaf, ARI of gall surface and ARI of the respective stem.
• We corroborated the host variation hypothesis since the anthocyanin content in stems and in galls' projections were positively related. Moreover, anthocyanin in galls' projections was positively related to anthocyanin in the gall surface and negatively related to gall volume and parenchyma thickness. This shows that, besides the host specificities, galls' own traits may also be responsible for pigment accumulation, influencing their colours.
• In this study, using colour as an example, we show that although galls tend to be considered complex expressions of galling insects' stimuli, their traits may be simply influenced by previous and specific attributes of the host organs.

     

Synchronization of gallers with host plant phenology

In addition to various bottom-up effects, the synchronization of herbivores with their host plant phenology determines quality and quantity of food resources and affects the preference–performance linkage and abundance of herbivores. The synchronization has a more critical meaning for such short-lived galling insects as cecidomyiid adults and young aphid stem mothers than for other insects. This review, first, presents general information about gall midges and gall aphids, together with their life history patterns and some ecological attributes. Second, some important topics of galling insect–host plant relation are briefly reviewed. Then, synchronization patterns between gall midge emergence and host plant phenology are analyzed to discuss the adaptive strategies of gall midges and to show how the amount of available food resources is affected by the time lag in synchronization. The spatial distribution pattern and the preference–performance linkage of aphid stem mothers is also discussed in relation to synchronization. Received: October 2, 1998 / Accepted: July 3, 2000     

The life history of a gall‐inducing mite: summer phenology,predation and influence of gall morphology in a sugar maple canopy

• 1 Eriophyoid mites are among the most ubiquitous gall‐inducing arthropods, and are adapted species‐specifically to a broad diversity of plants, although their life histories remain poorly studied outside agricultural systems.
• 2 We examined the seasonal phenology of a leaf‐galling eriophyid mite, the maple spindle gall mite Vasates aceriscrumena (MSGM), in naturally occurring stands of sugar maple Acer saccharum in south‐central Ontario in 2007 and 2008.
• 3 Galls were first induced in spring (mid‐May) and were devoid of mites by late August. In the study region, MSGM appears to have at least two generations, with overwintering, deutogyne females that initiate galls in spring (mid‐May) after leaf flush, giving rise to a generation of protogyne (primary) females and a few morphologically similar males (<1 for every 10 females) and, subsequently, to a new generation of deutogyne females in mid‐July to early August. In July, some galls can be highly crowded, with 50–200 individuals per gall.
• 4 In addition, a tarsonemid mite, Tarsonemus acerbilis, was found in approximately 40% of MSGM galls examined. As much as 95.4% of galls in 2007 and 97.4% in 2008 that contained tarsonemid larvae did not contain MSGM eggs (by contrast, only 2.3% of tarsonemid‐free galls contained no MSGM eggs), suggesting that these juveniles feed, at least opportunistically, on MSGM eggs.
• 5 Gall ostiole morphology appeared to influence both MSGM and Tarsonemus densities within galls, with ‘open’ ostioles (versus ‘closed’) being much more susceptible to invasion by the tarsonemid. The latter is likely to be an important regulator of MSGM populations. We hypothesize that the two ostiole types are the result of selection pressures on the gall inducer, favouring closed gall entrances for increased protection, and possibly also on the host tree, favouring open galls to increase predator access.

     

Bottom‐up manipulations alter the community structures of galling insects and gall morphs on Neoboutonia macrocalyx trees in a moist tropical rainforest

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Bottom-up effects shift top-down community structure of the parasitoid guild that attacks Asphondylia borrichiae (Diptera: Cecidomyiidae) on Borrichia frutescens (Asteraceae)

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Modification of tree architecture by a gall-forming aphid

Herbivory may substantially alter the architectural structure of plants. Among insects, gall-formers that substantially manipulate host traits may have a profound effect on the plants even at low densities. The aphid, Baizongia pistaciae induces banana-like large galls on the terminal buds of Pistacia palaestina. We hypothesized that these large galls are associated with the shape of the plant which may grow as a tree or a bush. In the natural Mediterranean forest, we monitored the effects of the galls on infested branches. In the year of gall formation, usually (~95%) there is neither elongation nor branching beyond the position of the gall. However, in the following years, galled branches produced more lateral branches (branching) than ungalled branches. This effect persists for at least 2 years. Consequently, galled branches carried more leaves and tended to gain more biomass than ungalled branches. Galling did not affect fruit yield. We suggest that repeated galling by B. pistaciae may promote bush-like architecture in P. palaestina.     

Reproductive phenology of two Mimusops species in relation to climate,tree diameter and canopy position in Benin (West Africa)

Assessing species phenology provides useful understanding about their autecology, to contribute to management strategies. We monitored reproductive phenology of Mimusops andongensis and Mimusops kummel, and its relationship with climate, tree diameter and canopy position. We sampled trees in six diameter classes and noted their canopy position. For both species flowering began in the dry season through to the rainy season, but peaked in the dry season, whilst fruiting occurred in the rainy season and peaked during the most humid period. Flowering was positively correlated with temperature. Conversely, fruiting was negatively correlated with temperature and positively with rainfall, only in the Guineo‐Sudanian zone. For M. andongensis, flowering and fruiting prevalences were positively linked to stem diameter, while only flowering was significantly related to canopy position. For M. kummel, the relationship with stem diameter was significant for flowering prevalence only and in the Guineo‐Sudanian zone. Results suggest that phylogenetic membership is an important factor restricting Mimusops species phenology. Flowering and fruiting of both species are influenced by climate, and consequently climate change might shift their phenological patterns. Long‐term investigations, considering flowering and fruiting abortion, will help to better understand the species phenology and perhaps predict demographic dynamics.     

Phenotypic plasticity and similarity among gall morphotypes on a superhost,Baccharis reticularia (Asteraceae)

Understanding factors that modulate plant development is still a challenging task in plant biology. Although research has highlighted the role of abiotic and biotic factors in determining final plant structure, we know little of how these factors combine to produce specific developmental patterns. Here, we studied patterns of cell and tissue organisation in galled and non‐galled organs of Baccharis reticularia, a Neotropical shrub that hosts over ten species of galling insects. We employed qualitative and quantitative approaches to understand patterns of growth and differentiation in its four most abundant gall morphotypes. We compared two leaf galls induced by sap‐sucking Hemiptera and stem galls induced by a Lepidopteran and a Dipteran, Cecidomyiidae. The hypotheses tested were: (i) the more complex the galls, the more distinct they are from their non‐galled host; (ii) galls induced on less plastic host organs, e.g. stems, develop under more morphogenetic constraints and, therefore, should be more similar among themselves than galls induced on more plastic organs. We also evaluated the plant sex preference of gall‐inducing insects for oviposition. Simple galls were qualitative and quantitatively more similar to non‐galled organs than complex galls, thereby supporting the first hypothesis. Unexpectedly, stem galls had more similarities between them than to their host organ, hence only partially supporting the second hypothesis. Similarity among stem galls may be caused by the restrictive pattern of host stems. The opposite trend was observed for host leaves, which generate either similar or distinct gall morphotypes due to their higher phenotypic plasticity. The Relative Distance of Plasticity Index for non‐galled stems and stem galls ranged from 0.02 to 0.42. Our results strongly suggest that both tissue plasticity and gall inducer identity interact to determine plant developmental patterns, and therefore, final gall structure.     

Mechanisms of hydraulic conductivity in the leaf galls of Meunieriella sp. (Cecidomyiidae) in Avicennia schaueriana (Acanthaceae): does vascularization explain the preferred sites of induction?

• Intralaminar galls of Meunieriella result from ground tissue proliferation in leaves of Avicennia schaueriana, a typical halophytic mangrove. We tested if the preferred sites of gall induction were the midribs and secondary veins (SV) at the basal leaf portion, where the galls were expected to be largest; and if the vascular system in galls and adjacent regions was altered to favour water supply in galls, thus increasing their growth.
• Gall induction sites and gall sizes were quantified according to leaf portions and regions. Anatomical and histometric analyses in vascular and ground tissues of galls and adjacent regions were compared to equivalent regions of non-galled leaves.
• The galls were largest at basal sites on leaves, the midrib and SV. More galls occurred on the apical portion of the leaf, and on the leaf blade and secondary vein regions. Changes in shape and vascular system area, number and diameter of vessel elements were detected in both galls and adjacent regions. Fewer and smaller-sized vessel elements were observed in regions proximal to the galls and inside them.
• Gall size is not related with preferred induction sites, which could be explained by factors such as thermal balance. Alterations in the vascular system indicate reduced hydraulic conductivity in the xylem in the proximal region and inside galls, leading to water leakage to gall parenchyma cells. This compensatory mechanism explains the expansion and proliferation of water storage and spongy parenchyma cells in the galls, explaining the higher growth in more vascularized regions.

     

Control of gall morphology: tephritid gallformers (Aciurina spp.) on rabbitbrush (Chrysothamnus)

Abstract.

• 1 Sibling species of tephritid flies occumng on separate subspecies of Chrysofhamizus nauseosus Hall and Clements have distinct gall moiphologies (smooth and cotton).
• 2 Cross matings of and subsequent confinement of the flies to particular host plants demonstrated that the insect's and not the plant's genotype dictated the morphology of the gall, although the plant genotype may determine whether or not a gall is produced.
• 3 The results implicate a possible single gene control mechanism for external gall morphology.

     

Evolutionary radiation of Asteromyia carbonifera (Diptera: Cecidomyiidae) gall morphotypes on the goldenrod Solidago altissima (Asteraceae)

Population divergence of phytophagous insects is often coupled to host‐plant shifts and is frequently attributed to the divergent selective environments associated with alternative host‐plants. In some cases, however, divergence is associated with the use of alternative host‐plant organs of a single host species. The basis of within‐host radiations such as these remains poorly understood. In the present stusy, we analysed the radiation of Asteromyia gall midges occurring both within one host plant species and within a single organ on that host. In this system, four morphologically distinct Asteromyia gall forms (morphs) coexist on the leaves of goldenrod Solidago altissima. Our analyses of amplified fragment length polymorphism and DNA sequence data confirm the genetic differentiation among midges from three gall morphs and reveal evidence of a genetically distinct fourth gall morph. The absence of clear gall morph related clades in the mitochondrial DNA derived phylogenies is indicative of incomplete lineage sorting or recent gene flow, suggesting that population divergence among gall forms is recent. We assess the likely history of this radiation and use the results of phylogenetic analyses along with ecological data on phenology and parasitism rates to evaluate potential hypotheses for the mode of differentiation. These preliminary analyses suggest that diversification of the Asteromyia gall morphs is likely shaped by interactions between the midge, a symbiotic fungus, and parasitoid enemies. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 840–858.     

Hypersensitivity of Fagus sylvatica L. against leaf galling insects

Hypersensitivity is known as a localized resistance of plants against pathogens. It also can be detected in response to galling insects, i.e., in the area immediately adjacent to the site of oviposition and attempted penetration by the galling larva. This host response includes morphological and histological changes that cause the death of the attacked tissue. It is observed as a rounded dark brown halo around the gall induction site. We provide the first observation on the occurrence and possible relevance of this induced mechanism by which one of the most common tree species in Germany, Fagus sylvatica L., resists attack by two of its most common galling insects, Mikiola fagi and Hartigiola annulipes (Diptera: Cecidomyiidae). Galls induced by these cecidomyiids were extremely common in the studied area in beech forests around Darmstadt, Germany. The availability of resources (leaves on a stem) was a poor predictor of attack by the galling insects as well as for gall abundance (galls successfully formed). Hypersensitive reaction was the most important factor acting against the galling population studied. More than 77% of the attempts of the insects to induce galls on F. sylvatica resulted in failure and consequently the death of the galling larvae. Therefore, few live galls remained to be found and destroyed by natural enemies. This corroborates the view that in galling insect–host plant system interactions plant-driven factors may play a major role in determining herbivore failure and success, and perhaps the resulting community structure.     

An emerging example of tritrophic coevolution between flies (Diptera: Fergusoninidae) and nematodes (Nematoda: Neotylenchidae) on Myrtaceae host plants

A unique obligate mutualism occurs between species of Fergusonina Malloch flies (Diptera: Fergusoninidae) and nematodes of the genus Fergusobia Currie (Nematoda: Neotylenchidae). These mutualists together form different types of galls on Myrtaceae, mainly in Australia. The galling association is species‐specific, and each mutualism in turn displays host specificity. This tritrophic system represents a compelling arena to test hypotheses about coevolution between the host plants, parasitic nematodes and the fergusoninid flies, and the evolution of these intimate mutualisms. We have a basic knowledge of the interactions between the host plant, fly and nematode in this system, but a more sophisticated understanding will require a much more intensive and coordinated research effort. Summaries of the known Fergusonina/Fergusobia species associations and gall type terminology are presented. This paper identifies the key advantages of the system and questions to be addressed, and proposes a number of predictions about the evolutionary dynamics of the system given our understanding of the biology of the mutualists. Future research will profitably focus on (1) gall cecidogenesis and phenology, (2) the interaction between the fly larva and the nematode in the gall, and between the adult female fly and the parasitic nematode, (3) the means by which the fly and nematode life cycles are coordinated, (4) a targeted search of groups in the plant family Myrtaceae that have not yet been identified as gall hosts, and (5) establishment and comparison of the phylogenetic relationships of the host plants, fly species and nematodes. Recently derived phylogenies and divergence time estimation studies of the Diptera and the Myrtaceae show that the fly family Fergusoninidae is less than half the age of the Myrtaceae, discounting the hypothesis of cospeciation and coradiation of the fly/nematode mutualism and the plants at the broadest levels. However, cospeciation may have occurred at shallower levels in the phylogeny, following the establishment of the fly/nematode mutualism on the Myrtaceae. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 699–718.     

Species‐specific responses to combined water stress and increasing temperatures in two bee‐pollinated congeners (Echium,Boraginaceae)

1. Water stress and increasing temperatures are two main constraints faced by plants in the context of climate change. These constraints affect plant physiology and morphology, including phenology, floral traits, and nectar rewards, thus altering plant–pollinator interactions.
2. We compared the abiotic stress responses of two bee‐pollinated Boraginaceae species, Echium plantagineum, an annual, and Echium vulgare, a biennial. Plants were grown for 5 weeks during their flowering period under two watering regimes (well‐watered and water‐stressed) and three temperature regimes (21, 24, 27°C).
3. We measured physiological traits linked to photosynthesis (chlorophyll content, stomatal conductance, and water use efficiency), and vegetative (leaf number and growth rate) and floral (e.g., flower number, phenology, floral morphology, and nectar production) traits.
4. The physiological and morphological traits of both species were affected by the water and temperature stresses, although the effects were greater for the annual species. Both stresses negatively affected floral traits, accelerating flower phenology, decreasing flower size, and, for the annual species, decreasing nectar rewards. In both species, the number of flowers was reduced by 22%–45% under water stress, limiting the total amount of floral rewards.
5. Under water stress and increasing temperatures, which mimic the effects of climate change, floral traits and resources of bee‐pollinated species are affected and can lead to disruptions of pollination and reproductive success.

     

Length–weight relationship of Hyporthodus haifensis and Mycteroperca rubra (Pisces; Serranidae) from the North‐Eastern Mediterranean Sea,Turkey

Length–weight relationships (LWRs) for Hyporthodus haifensis and Mycteroperca rubra were studied using longlines at depths of 5–150 m, in the Gulf of Antalya, northeastern Mediterranean Sea. Fishing operations were carried out daily with 15 fishing boats. A total of 170 individuals were sampled. The LWR relationships of Hyporthodus haifensis and Mycteroperca rubra were calculated as W = 0.009L^3.142 (r²) = 0.996 and W = 0.0081L^3.0652 (r²) = 0.989 P < 0.05, respectively.     

Dormancy cycles in buried seeds of three perennial Xyris (Xyridaceae) species from the Brazilian campo rupestre

• Dormancy cycles are an important mechanism for avoiding seed germination under unfavourable periods for seedling establishment. This mechanism has been scarcely studied in tropical species. Here, we studied three tropical and perennial species of Xyris, X. asperula, X. subsetigera and X. trachyphylla, to investigate in situ longevity and the existence of seasonal seed dormancy cycles.
• Seeds of three species of Xyris were buried in their natural habitat, with samples exhumed bimonthly for 18 months. Germination of exhumed seeds was assessed under a 12‐h photoperiod over a broad range of temperatures. Seeds of X. trachyphylla were also subjected to treatments to overcome secondary dormancy.
• Seeds of all species are able to form a persistent seed bank and exhibit seasonal changes in germinability. Secondary dormancy was acquired during the rainy summer and was overcome during the subsequent dry season (autumn/winter). Desiccation partially overcomes secondary dormancy in X. trachyphylla seeds.
• Soil seed bank persistence and synchronisation of seed germination under favourable conditions for seedling establishment contribute to the persistence and regeneration of X. asperula, X. subsetigera and X. trachyphylla in their natural environment.

     

Identifying the abiotic and biotic drivers behind the elevational distribution shift of a parasitic plant

• Climate change will alter the biotic and abiotic environment and dissipate ecological barriers, reorganising maps of current distribution of parasites and their hosts. In this study, we analyse the population dynamics of the parasitic plant Viscum album subsp. austriacum and explore key biotic (host availability and seed dispersal) as well as abiotic (temperature) factors influencing elevational distribution.
• The study was conducted along an elevational gradient of a Mediterranean mountain, covering the distribution belts of three potential pine hosts: Pinus halepensis (1300–1500 m), P. nigra (1300–1900 m) and P. sylvestris var. nevadensis (1600–2000 m). Along this gradient, we measured multiple variables of mistletoe population (prevalence, abundance and demographic profile) and different factors that might define the current mistletoe distribution (host suitability and availability, temperature and seed dispersal services).
• We found a decline in mistletoe prevalence and abundance with increasing elevation, detecting larger values of both variables at lower elevations of the most suitable host (Pinus nigra). Pinus sylvestris var. nevadensis was a suboptimal but suitable host for the parasite at high elevations. Mistletoe found suitable temperatures and seed dispersal services all along the gradient, being able to recruit at any site.
• With warming temperatures, the presence of suitable vectors for parasite dispersion, and the presence of a sub‐optimal host (P. sylvestris var. nevadensis) at the mountain top, mistletoe currently has a window of opportunity to expand its present geographic distribution to the summits.

     

Climate warming effects on grape and grapevine moth (Lobesia botrana) in the Palearctic region

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Taxonomic identity of a galling adelgid (Hemiptera: Adelgidae) from three spruce species in Central Japan

Gall‐forming insects are commonly highly host‐specific, and galling species once thought to be oligo‐ or polyphagous are often found to represent a complex of host‐specific races or cryptic species. A recent DNA barcoding study documented that an unidentified species of the genus Adelges is a gall‐former associated with four spruce species (Picea bicolor, P. koyamai, P. maximowiczii, P. polita) as the primary hosts, with little genetic differentiation among insects on different host species. In this study, we investigated the morphology of this galling adelgid to determine its taxonomic identity. Morphological inspection of insects collected from three of the spruce species confirmed that this adelgid is a single galling species, and is identified as Adelges (Sacchiphantes) kitamiensis, which was previously known only from the secondary host. We described the gallicola adults of this species, as well as the first‐instar exules which are the offspring of gallicolae. Finally, we verified the taxonomic identity of this species and discuss its life cycle and host distribution.     

Phenology of the black bean aphid,Aphis fabae,on organic crops and effect of parasitoid communities

1. Parasitoids represent the third trophic level in plant-insect food webs. They develop in or on herbivorous insects at the second trophic level, which in turn feed on plants that constitute the first trophic level. This food web system might be affected by agricultural landscape and practices.
2. We studied the phenology and population density of Aphis fabae (Hemiptera: Aphididae) and determined the impact of parasitoids in organic fields of beans and beet plants.
3. Twenty leaves per field were collected weekly. For each leaf, the total number of aphids, apterous and alate morphs, the number of mummies, and mortality of aphids were recorded.
4. Our results showed that the phenology of A. fabae varied throughout the season with maximal numbers observed at the beginning of summer. In addition, the production of alate morphs and the proportion of parasitism were positively correlated to an increase in aphid densities.
5. Six parasitoid species were recorded attacking A. fabae in the field, with Lysiphlebus fabarum and Binodoxys angelicae (Hymenoptera: Aphidiinae) being the most abundant parasitoids.
6. Field characteristics and availability of host plants in the surroundings affected A. fabae density. Lysiphlebus fabarum and B. angelicae appeared to be good biocontrol candidates against A. fabae.