Differential rates of invasion in three related alien oak gall wasps (Cynipidae: Hymenoptera)

Abstract. Three related species of oak gall wasps, Andricus corruptrix (Schlechtendal), A. kollari (Hartig) and A. lignicola (Hartig) have entered Britain since the introduction of Turkey oak, Quercus cerris L. in 1735. Their lifecycles involve alternating generations between an agamic generation on the native oak species (Q. petraea, Q. robur and their hybrid Q. x. rosacea), and a smaller, sexual generation on the alien Q. cerris. In examining the distributions of these insects and Q. cerris, we hypothesized that: (1) the invasion will spread more rapidly in places where both host trees are equally abundant than through regions where one of the tree species is substantially less common than the other; (2) interspecific competition between these bud‐galling species will lead to a negative correlation between their abundances at a particular site; (3) differential recruitment of natural enemies from the native hymenopteran fauna will slow the rate of spread in a species‐specific manner. A. kollari arrived nearly 200 years ago and is now found throughout the British Isles, wherever Turkey oak is grown. A. lignicola and A. corruptrix have been here for 30 years, after establishing in S.E. England. A. lignicola is in its final rapid stages of range expansion across England, southern Scotland and N.E. Scotland. A. corruptrix is just beginning to spread through Central and S.W. England. It has occupied proportionally fewer sites behind its invasion front than have the other two species, but is no less abundant at these sites. Nevertheless, distance leaps of up to 50 km were identified in A. lignicola in N.E. Scotland, and the possibility of long‐distance transport of infected trees through the horticulture and forestry trades remains. The co‐occurrence of mature individuals of both host Quercus species does appear to have increased their rates of colonization in A. lignicola and A. corruptrix. There is no evidence, however, to suggest that interspecific competition between the three alien gall formers is an important factor in determining their distributions and abundance within their invaded ranges. All three species have recruited parasitoids and inquilines rapidly from the native fauna; attack rates were highly variable, but showed no evidence of density dependence across sites.     

The protein content of tissues in cynipid galls (Hymenoptera: Cynipidae): Similarities between cynipid galls and seeds

Cynipid galls are examples of induced plant development, where the gall inducer is in control of cell differentiation and morphogenesis of a new plant organ. This study concentrates on the tissues of the larval chamber common to all cynipid galls. The protein content of the inner gall tissue was compared to that of non‐gall plant tissues. We investigated three oak and two rose galls and their respective host plants. Total protein signatures of inner gall tissues were different from those of non‐gall plant tissues, and among the five galls. N‐terminal sequences were obtained for two abundant proteins from the inner gall tissues of D. spinosa and A. quercuscalicis, which were common to all galls, at 62 and 43 kDa. Database queries suggest the 62 kDa protein to be homologous to a protein disulphide isomerase (PDI), and the 43 kDa protein to be homologous to NAD‐dependent formate dehydrogenase (FDH). A naturally biotinylated protein was detected at 33 kDa during Western analyses with streptavidin. Western analyses revealed the presence of the biotinylated protein and PDI in the inner gall tissues of all five galls, while FDH was only detected in A. quercuscalicis and A. fecundator. PDI was also common to all non‐gall tissues, while FDH was not detected in non‐gall tissues, and the biotinylated protein was only detected in seeds. The proteins identified in the inner gall tissue suggest that (a) inner gall tissues in some galls are under respiratory stress, and (b) cynipid gall formation might involve the ectopic expression of seed‐specific proteins.     

Skewed sex ratios and multiple founding in galls of the oak apple gall wasp Biorhiza pallida

Abstract. 1. The gall wasp Biorhiza pallida (Hymenoptera: Cynipidae) reproduces by cyclical parthenogenesis. The adults of the sexual generation develop within galls (oak apples) that contain many larval cells.
2. Folliot [(1964) Annales Des Sciences Naturelles: Zoologie, 12, 407–564] found asexual generation females to be of three reproductive types. Androphores produce only sons, gynophores produce only daughters, and gynandrophores produce both sons and daughters. In nature, most oak apples give rise to either only males or only females but a proportion produces both sexes. These mixed‐sex galls could result either from eggs laid by one or more gynandrophores or from eggs laid by androphores and gynophores developing within a single gall (multiple founding).
3. Here the frequency of mixed‐ and single‐sex galls was quantified, and morphological and genetic analyses were carried out on the adults emerging from 10 galls to determine the frequency of multiple founding in B. pallida .
4. Seventy-five per cent of 627 galls yielded only one sex. The majority of the remaining 25% had a highly skewed sex ratio. Low genetic variation in B. pallida limited the application of allozyme-based genetic techniques, however seven of the 10 galls analysed in detail, including mixed-sex galls, appeared to have been multiply founded. Contributions by the different foundresses in multiply founded galls were highly skewed.
5. The significance of multiple founding is discussed in the light of possible adaptive scenarios (reduction of parasitoid-induced mortality, avoidance of local stochastic extinction and inbreeding) and possible competition for oviposition sites.     

Brood sex ratios of the solitary parasitoid wasp, Coccophagus atratus

Abstract.

• 1 Female eggs of Coccophagus atratus are deposited within the haemolymph of coccoid scale insects. Male eggs are deposited on to late larval and prepupal stages of parasitoids of scale insects, including conspecifics.
• 2 When presented with either one host type or a combination of both host types, female C.atratus deposit all their available eggs, assigning the appropriate sex egg to each host encountered. Brood sizes are not adjusted for different combinations of hosts.
• 3 Behavioural observations show that females do not move away from patches of hosts until all their eggs are laid, regardless of the host type.
• 4 Brood sex ratios varied with changes in the relative availability of hosts for males and hosts for females. When both host-types were present in equal numbers, male biased sex ratios resulted (mean ±SEM =0.71 ± 0.009) and when 70% of hosts provided were suitable for female eggs, mostly female-biased sex ratios resulted (mean ± SEM = 0.37±0.01).
• 5 Our results do not fit predictions based on the assumption that a sex ratio of 0.5 should be expected in C.atratus. Observed sex ratios indicate that the unusual life histories of these parasitoids need to be taken into account in explanations of their sex ratios.

     

Red galls: the different stories of two gall types on the same host

• Several studies have suggested reasons why galls have conspicuous colours, but none of the ideas have been confirmed. However, what if the vibrant colours of some galls are explained simply by the effect of light exposure? This may lead to anthocyanin accumulation, functioning as a defence mechanism against the effects of high light.
• We studied the globoid galls induced by Cecidomyiidae (Diptera) on Qualea parviflora (Vochysiaceae), relating anthocyanin accumulation and chlorophyll fluorescence parameters to light incidence in abaxial and adaxial galls. We also tested if the anthocyanin accumulation patterns apply to another Cecidomyiidae‐induced gall morphotype (intralaminar) within the same plant.
• Adaxial galls are exposed to higher incident light, with more anthocyanin accumulation and therefore red coloration. In galls from angled leaves, the greater the angle of the leaf, the higher the difference between anthocyanins on the sun and shade sides of galls. Photosynthetic pigment concentrations did not differ between abaxial and adaxial galls. However, we found higher (F_m′ ? F′)/F_m′ and F_v/F_m in the abaxial galls. Conversely, NPQ and R_fd were higher in adaxial galls. Finally, the pattern of anthocyanin accumulation was not found in the intralaminar gall.
• Anthocyanin accumulation in galls functions as a photoprotective strategy, maintaining tissue vitality in regions exposed to high light conditions. However, this mechanism may vary even among galls within the same host, indicating idiosyncrasy when it comes to coloration in galls. To date, this is the first study to demonstrate quantitatively why the galls of a specific species may be coloured: the variation in light regimes creates differential anthocyanin accumulation, influencing coloration.

     

Invaders on the move: parasitism in the sexual galls of four alien gall wasps in Britain (Hymenoptera: Cynipidae)

Four alien, host-alternating cynipid gall wasps are established in the British Isles: Andricus kollari, A. lignicola, A. quercuscalicis and A. corruptrix. Their current distributions divide Britain into four zones; all four invaders are present in the south and south-east of Britain, whereas only A. kollari is present in the far north of Scotland. The rank order, according to how far north the distributions of the four invading cynipid species reach, is: A. corruptrix→ A. quercuscalicis→ A. lignicola→ A. kollari. The life cycles of all four cynipid species involve a sexual generation in spring on Quercus cerris, and an agamic generation in autumn on Q. robur. Here we studied the parasitoid attack by four pteromalid species on the sexual generations of the invaders. We collected and reared the galls of all four species at eight sites from the south to the north of the country (two sites per zone). The geographical locations of the sites reflect the invasion history and thus the residence time of the alien species in the four zones. At each site we measured the densities of all host galls on Q. cerris and of both obligatory host-tree species. We also took a series of measures, such as host-tree density and mean host-tree size, to further characterize the tree stands. These measures are referred to as local parameters. Host densities varied between sites and between years. In A. kollari, galling rates were highest in the middle of the country (zone 2) in 1994, whereas in 1995 they increased from the south to the north. In A. lignicola, galling rates in both years were lowest at the sites in zone 3 (closest to its distribution boundary). In A. quercuscalicis, galling rates were found to be lowest at the site most to the north-west in both years, again the one furthest away from the area where this species was first recorded. Mortality caused by parasitoid attack differed from less than 10% to as high as 70% and varied between host species, sites and years. In four out of six cases the historical/regional variables (north/south and east/west) correlated significantly with parasitoid attack rates that were characteristically lowest at sites close to the distribution boundaries. Of the local factors, we found parasitoid attack rates correlated negatively in one case with host density, whereas they correlated positively in four cases with the density of alternative hosts of the parasitoids. In one of the models the local density of Q. cerris trees correlated negatively with parasitoid attack on A. quercuscalicis. For all three host species the terms retained in the minimal adequate models obtained for 1994 and 1995 differed, which might indicate that these communities of native parasitoids and invading host have not yet settled in any definite structure.     

Maternal control of offspring sex and male morphology in the Otitesella fig wasps

Models concerning the evolution of alternative mating tactics commonly assume that individuals determine their own strategies. Here we develop a computer-based ESS model that allows mothers, ovipositing in discrete patches, to choose both the sex and the male mating tactics (natal-patch mating or dispersing) of their offspring based only on how many other mothers have used the specific patch before them. Data for three species of nonpollinating fig wasps from the Otitesella genus agree quantitatively with the model's assumptions and predictions. This suggests that females respond to population densities at the level of individual figs. The alternative male tactics in the species we studied are probably a result of a conditional strategy exercised by the mother that laid them. In addition, as females were only allowed to lay one egg per patch, our results suggest a new mechanism that can skew population sex ratios towards a female bias.     

Dioecy and the evolution of sex ratios in ants

Split sex ratios, when some colonies produce only male and others only female reproductives, is a common feature of social insects, especially ants. The most widely accepted explanation for split sex ratios was proposed by Boomsma and Grafen, and is driven by conflicts of interest among colonies that vary in relatedness. The predictions of the Boomsma–Grafen model have been confirmed in many cases, but contradicted in several others. We adapt a model for the evolution of dioecy in plants to make predictions about the evolution of split sex ratios in social insects. Reproductive specialization results from the instability of the evolutionarily stable strategy (ESS) sex ratio, and is independent of variation in relatedness. We test predictions of the model with data from a long-term study of harvester ants, and show that it correctly predicts the intermediate sex ratios we observe in our study species. The dioecy model provides a comprehensive framework for sex allocation that is based on the pay-offs to the colony via production of males and females, and is independent of the genetic variation among colonies. However, in populations where the conditions for the Boomsma–Grafen model hold, kin selection will still lead to an association between sex ratio and relatedness.     

Population ecology and spatial synchrony in the abundance of leaf gall wasps within and among populations of valley oak (Quercus lobata)

What factors drive population variability through space and time? Here we assess patterns of abundance of seven species of gall wasps in three genera occurring on the leaves of valley oaks (Quercus lobata) at 10 sites throughout this species' statewide range in California, from 2000 to 2006. Our primary goals were to understand the factors driving variability in gall abundance and to assess the extent of spatial synchrony in gall wasp communities at both large and small geographic scales. On the large, statewide scale, there was significant site-to-site variation in gall abundance, driven in all cases primarily by differences in mean maximum seasonal temperatures, and lesser year-to-year variation. In contrast, on the small, local scale, differences were more pronounced from year to year than from tree to tree, and were to some extent correlated with differences in acorn production, suggesting an interaction with the reproductive effort of hosts. Significant spatial synchrony was detected, particularly at the statewide scale, but in no case did synchrony decline significantly with distance, despite sites being up to 741 km apart. Variation in spatial synchrony was correlated with a number of exogenous factors, including seasonal weather conditions, the acorn crop at the statewide scale and soil phosphorus availability at the local scale; however, most variation in spatial synchrony in our analyses remained unexplained.     

The influence of host size on sex ratios in the parasitoid Diglyphus begini (Hymenoptera: Eulophidae)

Abstract. 1. Sex ratio in the ectoparasitoid, Diglyphus begini (Ashmead), attacking larvae of the dipterous leafminer Liriomyza trifolii (Burgess) in glasshouse marigolds, is best depicted by a model where sex ratio varies as a function of host size.
2. Male D. begini progeny are produced in hosts significantly smaller in size than those producing female progeny.
3. Female wasps attack and oviposit on the largest leafminer larvae available and whether a host is large or small depends upon the size of the other hosts attacked.
4. Diglyphus begini females adjust the thre:shold size for the change-over in sex allocation relative to the size of hosts attacked; however, the sex ratio is maintained at between 60% and 70% males.
5. The patterns observed in these glasshouse studies are not due to sex-specific differential mortality or superparasitism.     

Partial local mate competition and the sex ratio: A study on non-pollinating fig wasps

In many species, mating takes place in temporary patches where only a small number of females produce offspring. In this situation Local Mate Competition (LMC) theory predicts that the optimal sex ratio (defined as proportion males) should become increasingly female biased as the number of females contributing offspring to a patch decreases. However, in a large number of these species, some mating is also likely to occur away from the natal patch (termed partial LMC). In this case the degree of LMC is reduced, and theory predicts a relatively less female biased sex ratio. We tested these two predictions with field data from 17 species of New World non-pollinating fig wasps representing three genera. We present a model which suggests that the average number of females ovipositing in a fruit (i.e. patch) is positively correlated with the proportion of fruit of a given tree species in which that species of wasp occurs. Across species, the overall sex ratio was positively correlated with the proportion of fruit in which that species occurs. Furthermore, the males of some species are wingless, and in these species all mating must take place before females disperse from their natal fruit. In contrast, the males of other species are winged, and in these species mating may also take place away from the natal fruit. Species with winged males had less female biased sex ratios than species with wingless males that occurred in a similar proportion of fruit. Finally, the correlation between sex ratio and the proportion of fruit in which a species occurs was also observed within species when comparing between the fruit crops of different trees. This suggests that individual females facultatively adjust the sex ratio of their offspring in response to variable LMC.     

Extremely female-biased sex ratio and lethal male-male combat in a parasitoid wasp, Melittobia australica (Eulophidae)

Melittobia australica (Hymenoptera: Eulophidae) is a gregariousectoparasitoid of the prepupae and pupae of solitary wasps andbees. The males never disperse from their natal patch, and matingtakes place only on the host from which they emerged. We measuredthe offspring sex ratio of M. australica with differing foundressnumbers and examined combat between emerged males. The offspringsex ratios were extremely female biased and almost independentof foundress number in all cases. The population of M. australicaused in the experiment was infected with the cytoplasmicallyinherited symbiotic bacterium Wolbachia. However, although Wolbachiais a potential sex-ratio distorter, noninfected individualsshowed the same sex ratio patterns as the Wolbachia-infectedindividuals. An arena experiment showed that younger males werealmost always killed by older males that had eclosed earlier.These results suggested that lethal male–male combat isan additional factor distorting the sex ratio toward a morefemale-biased sex ratio. This provides a new perspective oncurrent local mate competition models.     

母代雌蜂数、进果时间及非传粉小蜂对传粉榕小蜂后代数量及性比的影响

【目的】对性比的研究有助于我们理解自然界生物的选择压力及其所产生的原因和结果,榕树和榕小蜂之间的互惠共生关系以及生物学和生态学特性使其成为研究性比和局域配偶竞争模型（local mate competition）的理想材料。本研究旨在探明榕小蜂性比调节和进化机制。【方法】对分布于西双版纳地区的鸡嗉子榕Ficus semicordata进行了人工控制性放蜂实验。测定了母代雌蜂数量及其进果时间间隔、非传粉小蜂Sycoscapter trifemmensis数量对传粉榕小蜂Ceratosolen gravelyi后代数量（成蜂数量）和性比的影响,并分析了小蜂后代数量和性比的相关性。【结果】在榕果发育期一致的前提下,随着母代雌蜂数量的增加,每头雌蜂的平均后代数量明显下降(P<0.001),后代性比显著升高(P<0.001),后代数量和性比呈显著负相关(P<0.05);随着雌蜂进果间隔的延长,后代数量亦呈现下降趋势,且性比增大,放2头雌蜂和3头雌蜂的处理呈同样趋势,但差异均不显著(P=0.87; P=0.49),小蜂后代数量与性比无显著相关性(P=0.86)。此外,非传粉小蜂数量与传粉小蜂后代数量呈显著负相关(P<0.001),与传粉小蜂性比呈正相关(P<0.001),小蜂后代数量和性比同样呈现显著负相关(P<0.001)。【结论】本实验模拟了自然界中榕 蜂的相互作用,所得结果有助于我们理解自然状态下榕小蜂性比调节模式和机制,以及榕 蜂互利共生系统的进化机制。     

Alien herbivores and native parasitoids: rapid developments and structure of the parasitoid and inquiline complex in an invading gall wasp Andricus quercuscalicis (Hymenoptera: Cynipidae)

Abstract.

• 1 Rapid and substantial changes have occurred in the parasitoid and inquiline community associated with the agamic galls of Andricus quercuscalicis since it invaded Britain in the late 1950s. The number of parasitoid and inquiline species has risen from one to thirteen over a 15-year period. Although the number of species has been relatively consistent over the last 8 years, the species composition has changed considerably and in a highly characteristic way during this period.
• 2 The parasitoid complex can be divided into two broadly distinct sets of parasitoid species; one set attacks only the gall former whereas the other set concentrates on the inquilines living in the wall of the gall.
• 3 The most dramatic change, however, is in the abundance of inquilines which were reported to be virtually absent in earlier studies on this community in Britain. Over a period of only 5 years, between 1988 and 1993, inquiline attack rose from less than 0.01 to an average of 0.26 inquilines per gall. The intensity of inquiline attack is geographically heterogenous, with high inquiline numbers restricted to south-east England. Because of the relatively high specificity of the parasitoids, high inquiline abundance is positively correlated with parasitoid species richness in knopper galls.
• 4 Parasitism rates, particularly on the gall former, were generally low (<10%). Over the last 5 years, however, seven parasitoid species have been consistently recorded and the mortality caused by these species has increased continuously. The species composition of the community associated with this alien gall wasp in Britain has quickly converged to the community known from its native range in continental Europe. Parasitoid species known to attack the galls of A.quercuscalisis on the continent have been recorded from it in Britain for the first time mainly in areas where inquilines have recently become abundant.
• 5 Since rates of parasitism of the gall former are still low, parasitoids are unlikely to play a major role in the population dynamics of this invading gall wasp at present, but the rapidly increasing inquiline and parasitoid attack could be a source of increased mortality for native cynipid species which are the alternative hosts of those parasitoid species.

     

Beyond sex allocation: the role of mating systems in sexual selection in parasitoid wasps

Despite the diverse array of mating systems and life histories which characterise the parasitic Hymenoptera, sexual selection and sexual conflict in this taxon have been somewhat overlooked. For instance, parasitoid mating systems have typically been studied in terms of how mating structure affects sex allocation. In the past decade, however, some studies have sought to address sexual selection in the parasitoid wasps more explicitly and found that, despite the lack of obvious secondary sexual traits, sexual selection has the potential to shape a range of aspects of parasitoid reproductive behaviour and ecology. Moreover, various characteristics fundamental to the parasitoid way of life may provide innovative new ways to investigate different processes of sexual selection. The overall aim of this review therefore is to re‐examine parasitoid biology with sexual selection in mind, for both parasitoid biologists and also researchers interested in sexual selection and the evolution of mating systems more generally. We will consider aspects of particular relevance that have already been well studied including local mating structure, sex allocation and sperm depletion. We go on to review what we already know about sexual selection in the parasitoid wasps and highlight areas which may prove fruitful for further investigation. In particular, sperm depletion and the costs of inbreeding under chromosomal sex determination provide novel opportunities for testing the role of direct and indirect benefits for the evolution of mate choice.     

Resource utilization and sex allocation in response to host size in two ectoparasitoid wasps on subcortical beetles

Patterns of host resource utilization and sex ratio manipulation in relation to host size were investigated for two solitary ectoparasitoid wasps,Atanycolus initiator andSpathius brevicaudis (Hymenoptera Braconidae). Both species parasitize subcortical beetles on the trunks of Japanese pine trees.A. initiator is on average 8 times larger in body weight and has an ovipositor that is 3.7 times longer than that ofS. brevicaudis. In both parasitoids, the size of emerging wasps was positively correlated with host size, but the host/wasp size regressions were linear for all three major host species inA. initiator, whereas inS. brevicaudis the regression was logarithmic for a relatively large host species. The sex ratios (proportion of males) of both parasitoids emerging from different host species decreased with increasing host size, but the overall sex ratio on each host species was male-biased inA. initiator, while female-biased inS. brevicaudis. How the proportion of host consumed changed in response to host size, differed between the two parasitoids for the same host species. In the field survey, the size and sex ratio of the emerging two parasitoids from a dead tree were closely related to host size. However, the spatial distribution of the two parasitoids depended on the bark thickness of the trunk. The data suggest that differences in the relative evaluation of host size and in ovipositor length may enable the coexistence of the two parasitoid wasps.     

The effect of interspecific mating on sex ratios in the twospotted spider mite and the Banks grass mite (Acarina: Tetranychidae)

Mixed populations of the twospotted spider mite (TSM),Tetranychus urticae (Koch), and the Banks grass mite (BGM),Oligonychus pratensis (Banks), occur on corn and sorghum plants in late summer in the Great Plains. Interspecific matings between these arrhenotokous species occur readily in the laboratory but yield no female offspring. The effect of interspecific mating on female: male sex ratios was measured by examining the F₁ progeny of females that mated with both heterospecific and conspecific males in no-choice situations. TSM females that mated first with BGM males and then with TSM males produced a smaller percentage of female offspring than TSM females that mated only with TSM males (43.1±5.8 and 78.9±2.8% females, respectively). Similarly, BGM females mated with heterospecific males and then with conspecific males produced fewer female offspring than females mated only with BGM males (55.7±5.2 and 77.5±2.5%, respectively). Lower female: male sex ratios were produced also by BGM females that mated with TSM males after first mating with conspecifics (62.4±3.4%). In mixed populations containing males of both species, females also produced lower female: male sex ratios, but these ratios were not as low as expected based on mating propensities and progeny sex ratios observed in no-choice tests. These data suggest that interspecific mating may substantially reduce female fitness in both mite species by reducing the output of female offspring, but in mixed populations this effect is mitigated by unidentified behavioral mechanisms.     

The impact of an exotic social wasp (Vespula germanica) on the native arthropod community of north-west Patagonia, Argentina: an experimental study

Abstract 1. Biological invasions are usually thought to have a negative impact on native communities. However, data supporting this idea are often based on comparative studies between invaded and non‐invaded areas, and are spatially and temporally limited. 2. The present study experimentally assessed the impact of an exotic wasp, Vespula germanica, on the native arthropod community of north‐west Patagonia during 3 years in an area of 80 ha. Vespula germanica is an exotic social vespid that invaded north‐west Patagonia 20 years ago. It has been suggested that its populations affect native arthropods because of its broad diet and also because Patagonia lacks natural enemies and potential competitors for these wasps. 3. Using wasp‐specific toxic baits, V. germanica abundance was reduced in five sites of native woodlands during 3 consecutive years. The abundance, species richness, and composition of arthropods between non‐poisoned (control) and poisoned sites was then compared, both before and after the wasps were poisoned. 4. Wasp abundance represented 6% of the total arthropod catches in non‐poisoned sites and was reduced, on average, by 50% in the treated areas. The abundance, species richness, and composition of the arthropod community (305 species, 24 600 individuals) did not differ between control areas and areas where the abundance of V. germanica was reduced. Significant differences in response variables were found only before wasp poisoning had begun and were related to variations among sites. 5. These results suggest that V. germanica is not affecting the local arthropod assemblages, contradicting past work in other regions. The low relative abundance of wasps in Patagonia, when compared with other invaded regions, might explain the findings. 6. The present study provides further evidence for the importance of large‐scale experimental work with before/after comparisons to fully understand the impact of invaders on natural communities.