Identification of molecular markers for DNA barcoding in the Aphidiinae (Hym. Braconidae)

Reliable identification of Aphidiinae species (Braconidae) is a prerequisite for conducting studies on aphid–parasitoid interactions at the community level. However, morphological identification of Aphidiinae species remains problematic even for specialists and is almost impossible with larval stages. Here, we compared the efficiency of two molecular markers [mitochondrial cytochrome c oxydase I (COI) and nuclear long wavelength rhodopsin (LWRh)] that could be used to accurately identify about 50 species of Aphidiinae that commonly occur in aphid–parasitoid networks in northwestern Europe. We first identified species on a morphological basis and then assessed the consistency of genetic and morphological data. Probably because of mitochondrial introgression, Aphidius ervi and A. microlophii were indistinguishable on the basis of their COI sequences, whereas LWRh sequences discriminated these species. Conversely, because of its lower variability, LWRh failed to discriminate two pairs of species (Aphidius aquilus, Aphidius salicis, Lysiphlebus confusus and Lysiphlebus fabarum). Our study showed that no unique locus but a combination of two genes should be used to accurately identify members of Aphidiinae.     

The prospect of using sub-lethal imidacloprid or pirimicarb and a parasitoid wasp, Lysiphlebus fabarum, simultaneously,to control Aphis gossypii on cucumber plants

The broad-spectrum insecticides greatly influence the control of cotton aphids; however, due to frequent chemical control, Aphis gossypii (Hemiptera: Aphididae) has developed resistance against several classes of synthetic insecticides. In this study, we explored the sub-lethal effects of imidacloprid and pirimicarb, two commonly used insecticides for aphid control, on a parasitoid wasp, Lysiphlebus fabarum (Marshall) (Braconidae: Aphidiinae), when simultaneously used to control melon aphid on cucumber plants, as part of a comprehensive study for integrated pest management. Bioassays of imidacloprid and pirimicarb were performed to calculate LC₅₀ with third instars of A. gossypii. The LC₅₀ of these insecticides (110.55 and 250.89 μg/lit, respectively) were used to expose the wasp larvae, pupae, and adult parasitoids on a cucumber leaf. The percent mortality, percent adult emergence, and sex ratio were calculated during each exposure test. Moreover, the body size, egg load, and mature egg size of wasps surviving the insecticide treatments, as well as the sex ratio of the second generation was evaluated. Regardless of the host aphid mortality, none of the insecticides caused mortality of larval stage of the parasitoid. The insecticide application on pupal stage revealed that the percentage of mortality, sex ratio, body size, and egg load of surviving wasps, as well as the sex ratio of their offspring was adversely affected by imidacloprid, but not by pirimicarb. The present study suggests pirimicarb as a preferred insecticide, with less harmful effects on the fitness components of L. fabarum, for integrated pest management of cotton aphids.     

Host genotype affects the relative success of competing lines of aphid parasitoids under superparasitism

1. In solitary parasitoids, only one individual can complete development in a given host. Therefore, solitary parasitoids tend to prefer unparasitised hosts for oviposition, yet under high parasitoid densities, superparasitism is frequent and results in fierce competition for the host's limited resources. This may lead to selection for the best intra‐host competitors. 2. Increased intra‐host competitive ability may evolve under a high risk of superparasitism if this trait exhibits genetic variation, and if competitive differences among parasitoid genotypes are consistent across environments, e.g. different host genotypes. 3. These assumptions were addressed in the aphid parasitoid Lysiphlebus fabarum (Hymenoptera: Braconidae: Aphidiinae) and its main host, the black bean aphid, Aphis fabae (Scopoli) (Hemiptera: Aphididae). Three parthenogenetic lines of L. fabarum were allowed to parasitise three aphid clones singly and in all pairwise combinations (superparasitism). The winning parasitoid in superparasitised aphids was determined by microsatellite analysis. 4. The proportions of singly parasitised aphids that were mummified were similar for the three parasitoid lines and did not differ significantly among host clones. 5. Under superparasitism, significant biases in favour of one parasitoid line were observed for some combinations, indicating that there is genetic variation for intra‐host competitive ability. However, the outcome of superparasitism was inconsistent across aphid clones and thus influenced significantly by the host clone in which parasitoids competed. 6. Overall, this study shows that the fitness of aphid parasitoids under superparasitism is determined by complex interactions with competitors as well as hosts, possibly hampering the evolution of improved intra‐host competitive ability.     

Density-dependent parasitism of cowpea aphid,Aphis craccivora by Lysiphlebus fabarum,Binodoxys acalephae,and Aphidius matricariae (Hymenoptera: Braconidae: Aphidiinae)

Biological control, as a major component of pest management strategies, uses natural biological agents to reduce pest populations. Studying the interaction among Aphis craccivora and its parasitoids including, Lysiphlebus fabarum, Binodoxys acalephae, and Aphidius matricariae in 2016 and 2017 in Tehran Parke-Shahr, showed positive, significant correlations in all cases between the densities of three parasitoid species and that of aphid nymphs and adults. The density of the parasitoids increased by increasing the density of the aphids. The parasitoids showed aggregative behavior in response to different densities of the host. There was a positive density-dependent correlation between the density of A. craccivora and rate of parasitism. Parasitism rates of nymphs and adult aphids by L. fabarum, B. acalephae, and A. matricariae increased or decreased along with decline or increase in the population of the aphid host. In 2016 spring, the highest rates of parasitism on aphid nymphs by L. fabarum, B. acalephae, and A. matricariae were 46.82, 23.09, and 17.16%, respectively. In 2017 spring, the highest rates of parasitism on aphid nymphs by L. fabarum, B. acalephae, and A. matricariae were 48.97, 21.77, and 15.06%, respectively. So, given the accordance between changes in aphid population and that of parasitoids, and parasitoids’ efficacy in Tehran’s polluted air, they can be used as biological agents in the management of A. craccivora population.     

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.

     

Effect of Bt maize on the plant-aphid–parasitoid tritrophic relationships

The effect of Bt maize on aphid parasitism and the aphid–parasitoid complex was measured in field conditions on three transgenic varieties, two derived from Event MON810 and one from Bt176, and their near-isogenics in a two-year study. No differences in aphid abundance were found between Bt maize varieties and their near-isogenics. Differences within Bt and within near-isogenic varieties were found, but only in one year. Differences in aphid abundance were probably better accounted for the variety background and year conditions than by the transgenesis or Event. Lysiphlebus testaceipes (Cresson), Lipolexis gracilis Förster (Hymenoptera, Braconidae, Aphidiinae) and Aphelinus sp. (Hymenoptera, Aphelinidae) were the prevalent parasitoids. Bt maize did not alter the aphid–parasitoid associations and had no effect on the aphid parasitism and hyperparasitism rates. The results suggest that Bt maize has no negative impact on second, third and fourth levels of the trophic relationships studied.     

The potential host ranges in Australia of some imported aphid parasites [Hym: Ichneumonoidea: Aphidiidae]

Host selection trials on restricted populations of the aphidiid parasites,Lysiphlebus fabarum (Marshall) andL. testaceipes (Cresson), imported into Australia as biological control agents ofAphis craccivora Koch, the cowpea aphid, have shown that these imported parasites are not widely polyphagous, and thus support a view that the 2 species, as presently recognized, each represent a complex of host-restricted biotypes or of sibling species. Whereas both of the importedLysiphlebus readily oviposited in species ofAphis andToxoptera, and developed successfully to adulthood inA. craccivora, A. gossypii Glover andT. aurantii (Boyer de Fonscolombe), they failed to complete development inA. citricola van der Goot, one of the most common aphid species in Australia, and only a small number completed development inT. citricidus (Kirkaldy). Both of these hosts, then, act as “egg traps” for theLysiphlebus. A. nerii Boyer de Fonscolombe was a suitable host forL. testaceipes but not forL. fabarum. NeitherL. fabarum notL. testaceipes oviposited inCavariella aegopodii (Scopoli),Brevicoryne brassicae (L.),Brachycaudus helichrysi (Kaltenbach),B. persicae (Passerini),Hyperomyzus lactucae (L.),Acyrthosiphon kondoi Shinji,A. pisum (Harris),Macrosiphum euphorbiae (Thomas) orM. rosae (L.); andL. fabarum did not oviposit inRhopalosiphum padi (L.) orMyzus persicae (Sulzer). The prognosis for the effective establishment in Australia of these 2 parasites is therefore not good In contrast, another purportedly polyphagous aphidiid,Praon volucre (Haliday), imported into Australia to help effect control ofH. lactucae, the sowthistle aphid, successfully and effectively parasitizedMacrosiphum euphorbiae, M. rosae, Acyrthosiphon pisum, A. kondoi, Aulacorthum solani (Kaltenbach),Myzus persicae andAphis craccivora, in addition toH. lactucae.     

Intraguild predators and the spatial distribution of a parasitoid

An experimental plot of the aphid Aphis fabae on various host plant species was colonized by natural populations of the aphidiine parasitoid Lysiphlebus fabarum and insect predators, especially coccinellids. Parasitism of A. fabae by L. fabarum was significantly depressed on plants bearing coccinellids. The number of parasitized aphids increased with aphid abundance on three plant species (Papaver dubium, Rumex obtusifolius, Vicia faba), but not on the plant species (Chenopodium album) which bore very high numbers of coccinellids. In complementary laboratory experiments, L. fabarum offered a choice between odours of plants infested with A. fabae and/or coccinellids selected the odour fields from coccinellid treatments at significantly lower frequency than the odour fields of other treatments. It is concluded that avoidance of coccinellids by L. fabarum contributes to the negative association between the abundance of coccinellids and parasitoids in the field. Received: 22 March 1999 / Accepted: 22 March 2000     

Aphids on ornamental plants from Córdoba, Argentina (Hemiptera: Aphididae)

The quality of the ornamental plants is closely related to their phytosanitary state, that, in turn, is affected by the activity of some insect groups. Aphids are common pests of nearly all kinds of plants, ornamental plants among them. The fauna associated with aphids that colonize ornamental plants includes honey ants (Hymenoptera: Formicidae) that establish mutualistic relations, and some parasitoids (Hymenoptera: Braconidae, Aphidiinae) that contribute to the control of the aphid population. Very little is known about the aphids and their associated fauna living on ornamental plants of Cordoba, Argentina. The goal of this work was to identify the aphids that colonize ornamental plants, as well as their associated honey ants and parasitoids. Samples of sprouts, leaves and/or flowers of aphid-colonized ornamental plants of the Jardín Botánico Municipal of Cordoba city were collected weekly, from October 2003 to November 2004. Whenever found, the associated honey ants and "mummies" of aphids attacked by parasitoids were also collected. One hundred and thirty two aphid-plant associations were registered, 64.4% of which were unknown in the country. In 33.3% of these associations, the aphids were tended by honey ants whereas the presence of aphid parasitoids was registered in 16.7%. Ninety five species of ornamental plants were colonized by 41 aphid species, whereas six ant species tended 10 aphid species. Aphid parasitoids were represented by four species related to 11 aphid species.     

Success of aphid parasitoids and their hosts varies with ant attendance: A field study

Aphid–ant associations are often described as mutually beneficial interactions in which honeydew is traded for protection from predators and parasitoids. The aim of the present study was to determine parasitization avoidance in ant‐tended aphid colonies. Field experiments were carried out on two host plants: hoary cress Lepidium draba (Brassicaceae) and Canadian teasel Cirsium arvense (Asteraceae). Lepidium was host to Acyrthosiphon gossypii (Aphididae) tended by the ant Lasius turcicus (Formicidae) and attacked by two parasitoids, Trioxys asiaticus (Braconidae) and Lysiphlebus fabarum (Braconidae). Cirsium was host to Brachycaudus cardui tended by Crematogaster sordidula and attacked by L. fabarum and Aphidius colemani (Braconidae). The per capita population growth rate of A. gossypii was significantly higher in the presence of ants, while B. cardui was negatively affected, albeit non‐significantly. The parasitism rate of A. gossypii decreased significantly when tended by Lasius turcicus, but the presence of Crematogaster sordidula in colonies of B. cardui significantly increased parasitism. Our results indicate that the effects of ant attendance vary between different aphid–ant interactions. Moreover, parasitoids can benefit from the presence of ants under some conditions.     

In vitro rearing ofLysiphlebus fabarum [Hym.: Braconidae]

In vitro rearing of the aphid endoparasitoidLysiphlebus fabarum (Marshall) (Hymenoptera, Braconidae) was attempted. Successful permanent cultures ofAphis fabae Sc. andMyzus persicae Sulz. cells were not obtained. Therefore, parasitoid larvae were reared in 2 unnatural media rone of which included cells ofCeratitis capitata Wied. (Diptera, Trypetidae). A group of larvae was reared in a substrate to which parasitoid teratocytes had been added. SinceLysiphlebus fabarum females did not oviposit into paraffin droplets including the substrates, the larvae were directly transferred from parasitized aphids into the rearing media. Several larvae reached the final instar, but only 2 out of the 48 tested in the 3 substrates became adults. The meaning of teratocytes inin vitro rearing of Aphidiine, Braconids is discussed. This work was supported by a grant from the italian Ministry of Education (M.P.I. 40%).     

Bidirectional movement of aphid parasitoids (Braconidae: Aphidiinae) between crops and non-crop plants in agroecosystems of central Argentina

The movement of predators and parasitoids between natural and cultivated habitats is a common process in agroecosystems, which may be affected by different biotic and abiotic factors, mostly related to the availability of resources. Here, through a broad approach, we aimed to obtain an overview of factors affecting the bidirectional movement of aphid parasitoids (Braconidae: Aphidiinae) across cultivated habitats and their natural vegetated borders. Using bidirectional flight traps, we measured the number of parasitoids moving from borders to crops and vice versa, in fields of three common crop species (alfalfa, oat and wheat) in the Pampean region, Santa Fe, Argentina. The effects of the abundance of aphid prey, abundance and richness of flowers in both habitats, as well as temperature and wind speed on parasitoid movement, were assessed through generalized mixed models, considering sampling date and field as random factors. The relationship between parasitism percentages and parasitoid movement from the borders to the crops was explored separately for three pest aphid species: Aphis craccivora Koch, Rhopalosiphum padi (L.) and Schizaphis graminum (Rondani). Overall, we found a prevalence of parasitoids moving in the border-crop direction, mainly in wheat and alfalfa crops. Aphid abundance in the arrival habitat affected parasitoid movement in both directions. A link between parasitoid movement and parasitism percentages was observed for the aphid species S. graminum in wheat, suggesting a beneficial role of natural vegetation in pest control.     

Occurrence of Macrosiphum hellebori Theobald & Walton (Hemiptera: Aphididae) in Australia

The European aphid species, Macrosiphum hellebori , the hellebore aphid, is recorded from Australia, having been found in Melbourne, Victoria and in Canberra, Australian Capital Territory, colonising ornamental hellebores, Helleborus species (Ranunculaceae). Insect associates of M. hellebori are recorded, including the hymenopterous primary parasite Lysiphlebus testaceipes (Cresson) (Braconidae: Aphidiinae). Keys are provided for the identification of the three species of Macrosiphum Passerini known from Australia.     

The parasitoid complex [Hym.: Ichneumonoidea] ofToxoptera aurantii [Hom.: Aphidoidea] in the Mediterranean area

The parasitoid complex of the Black Citrus Aphid,Toxoptera aurantii (B.d.F.) in the Mediterranean area has been complemented on the basis of samples collected in South Italy and Lebanon. To the complex presently belong 10 Ichneumonoid species of the generaAphidius Nees,Diaeretiella Staryý,Ephedrus Haliday,Lipolexis Förster,Lysiphlebus Förster,Praon Haliday andTrioxys Haliday. Of these,Aphidius colemani Viereck, in spite of its wide distribution in the Mediterranean region, seems to be restricted to Near East (Israel and Lebanon) asT. aurantii parasitoid. The nearctic speicesLysiphlebus testaceipes (Cresson) is localized in Spain, South France, Corsica, Central and South Italy, including Sicily. In Italy, this endoparasitoid has heavily interfered with the local dominant congeneric speciesLysiphlebus confusus Tremblay & Eady andLysiphlebus fabarum (Marshall). The possible associative relationships betweenLysiphlebus testaceipes andL. fabarum have been examined in the samples collected in South Italy. The results of the examination suggest that the 2 species are negatively associated with each other, i.e. the abundance of 1 of the 2 species makes it more likely that the other will decrease in numbers. Moreover, the data concerning the relative abundance of both species in the same area indicate that a shift may have occurred in favour ofL. testaceipes between 1977 and 1978. The nearctic parasitoid seems to be able to displace the 2 congeneric species by a competitive biological mechanism which is still in course of investigation.     

Foraging efficiency of Lysiphlebus fabarum Marshall (Hymenoptera: Aphidiidae) parasitizing the black bean aphid,Aphis fabae Scopoli (Hemiptera: Aphididae), under laboratory conditions

Foraging efficiency of Lysiphlebus fabarum Marshall, the most abundant and effective parasitoid of the black bean aphid, Aphis fabae Scopoli, in terms of functional and numerical responses and mutual interference, was studied on broad bean plants in a growth chamber at 21 °C, 70 ± 5% RH and a photoperiod of 16:8 (L:D) h. Using logistic regression, a type II functional response was determined for L. fabarum. Nonlinear least-square regression was used to estimate the searching efficiency (a') and handling time (T_h). Numerical response of L. fabarum to cumulative host densities was partially linearly increasing. Nicholson's model and linear regression were used to determine the per capita searching efficiency and interference coefficient, respectively. In general, the per capita parasitism and, consequently, the per capita searching efficiency decreased significantly as parasitoid density increased. Mutual interference and quest constants were ? 0.508 and ? 0.697, respectively. The results of this study suggest that both the host and parasitoid densities have no significant impact on the progeny sex ratio. The information provided here will be useful in assessing the efficiency of L. fabarum as a biological control agent of A. fabae, devising mass-rearing protocols and implementing release programs for this parasitoid.     

A comparison of life history traits of sexual and asexual strains of the parasitoid wasp,Lysiphlebus fabarum (Braconidae: Aphidiinae)

1. This study examined biological characteristics of sexual and asexual strains of the parasitoid wasp, Lysiphlebus fabarum (Marshall) (Hymenoptera: Braconidae). 2. Strains were reared in different instar hosts (the black bean aphid, Aphis fabae Scopoli) under identical environmental conditions (21 °C, 65–75% RH, and LD 16:8 h). 3. Results showed that the second instar of the aphid is the most suitable growth stage for both strains, as the wasps that emerged from the second instar hosts were larger, more fecund, and had larger egg size. Trade‐offs between the fitness components of the parasitoid were clearer when the parasitoids were reared in suboptimal instars. 4. According to the results, sexual females emerged around 1 day earlier and lived around 0.5 day less than asexual females. Also, sexual females emerged with a lower initial egg load, although these wasps tend to have larger eggs than asexual females. Asexual females may enjoy greater longevity and higher developmental plasticity which suggests a higher degree of synchronization with pest population dynamism. 5. The results suggest that sexual wasps, in contrast to asexual wasps, invest more in egg size than in egg load. This study suggests strain‐specific adaptations of L. fabarum to different instars of the black bean aphid by which the allocation of nutritional resources to various functions differs between strains. 6. Furthermore, differences in life history traits between strains can greatly influence the population dynamics of each strain, and hence their effectiveness in suppressing pest populations.     

Parasitoids associated with the common pistachio psylla, Agonoscena pistaciae, in Iran

The parasitoids associated with the common pistachio psylla, Agonoscena pistaciae Burckhardt and Lauterer, were investigated at three pistachio plantations in Rafsanjan, Iran. Of the 6504 wasps emerging from mummified psyllids, 46% were the primary parasitoid Psyllaephagus pistaciae Ferrière, and the remaining 54% represented six species of hymenopterous hyperparasitoids, including Chartocerus kurdjumovi (Nikol’skaja), Marietta picta (André), Pachyneuron aphidis (Bouché), Pachyneuron muscarum (Linnaeus), Psyllaphycus diaphorinae (Hayat), and Syrphophagus aphidivorus (Mayr). Lysiphlebus fabarum Marshall, the parasitoid of Aphis gossypii Glover and Aphis craccivora Koch present on weeds, was found to be an alternative host for three major hyperparasitoids of A. pistaciae. The most abundant hyperparasitoid was S. aphidivorus, appearing during the growing season in all trial locations on psyllids and aphids in pistachio orchards. The weed-infesting aphids, along with their primary parasitoid, can act as a reservoir of A. pistaciae secondary parasitoids. Therefore, parasitized aphids allow populations of secondary parasitoids to increase and consequently to apply higher pressure on P. pistaciae. We detected that two primary parasitoid species, including P. pistaciae and L. fabarum, attacking different species of hosts interact indirectly through shared secondary parasitism. It is suggested that the community structure of A. pistaciae may be influenced by apparent competition, although more work is needed to provide firm evidence.     

Nonhost diversity and density reduce the strength of parasitoid–host interactions

The presence of nonprey or nonhosts is known to reduce the strength of consumer– resource interactions by increasing the consumer's effort needed to find its resource. These interference effects can have a stabilizing effect on consumer–resource dynamics, but have also been invoked to explain parasitoid extinctions. To understand how nonhosts affect parasitoids, we manipulated the density and diversity of nonhost aphids using experimental host–parasitoid communities and tested how this affects parasitation efficiency of two aphid parasitoid species. To further study the behavioral response of parasitoids to nonhosts, we tested for changes in parasitoid time allocation in relation to their host‐finding strategies. The proportion of successful attacks (attack rate) in both parasitoid species was reduced by the presence of nonhosts. The parasitoid Aphidius megourae was strongly affected by increasing nonhost diversity with the attack rate dropping from 0.39 without nonhosts to 0.05 with high diversity of nonhosts, while Lysiphlebus fabarum responded less strongly, but in a more pronounced way to an increase in nonhost density. Our experiments further showed that increasing nonhost diversity caused host searching and attacking activity levels to fall in A. megourae, but not in L. fabarum, and that A. megourae changed its behavior after a period of time in the presence of nonhosts by increasing its time spent resting. This study shows that nonhost density and diversity in the environment are crucial determinants for the strength of consumer–resource interactions. Their impact upon a consumer's efficiency strongly depends on its host/prey finding strategy as demonstrated by the different responses for the two parasitoid species. We discuss that these trait‐mediated indirect interactions between host and nonhost species are important for community stability, acting either stabilizing or destabilizing depending on the level of nonhost density or diversity present.     

Use of plants by Myzus persicae in agroecosystems: Potential applications in conservation biological control

Myzus persicae (Sulzer) is a highly polyphagous aphid species that attacks several economically important crop plants. Here, trophic webs involving M. persicae, its host plants and its parasitoids were described and quantified in wheat, oat and alfalfa agroecosystems from central Argentina, with special emphasis on the sub-habitats where interactions occur: crops and adjacent field margins. Three fields cultivated with each crop species and their margins were sampled during three years; aphid abundance and mummification percentage were compared among crop plants and the diverse natural vegetation in the borders. Interactions were described using a quantitative food web approach, and abundance and mummification percentage e data were analysed using a generalized linear model. Four plant species present in the borders (Capsella bursa-pastori, Rapistrum sp., Melilotus sp. and Trifolium repens) hosted M. persicae and its parasitoids. The alfalfa agroecosystem produced a significantly higher number of aphids than oat and wheat; however, in all cases, crops and borders sustained similar aphid abundance. A total of six Aphidiinae species attacked M. persicae, with no significant differences in the richness of parasitoid species between the borders and the crops, but with significant differences in parasitoid abundance, being higher in the crops. Mummification percentage were higher in crops than in the borders, with Lysiphlebus testaceipes, Aphidius colemani and A. ervi being the most abundant species. Almost 70% of M. persicae individuals were collected from fields borders, which highlights the importance of including these sites in studies of trophic interactions in crop fields.     

Cheaper is not always worse: strongly protective isolates of a defensive symbiont are less costly to the aphid host

Defences against parasites are typically associated with costs to the host that contribute to the maintenance of variation in resistance. This also applies to the defence provided by the facultative bacterial endosymbiont Hamiltonella defensa, which protects its aphid hosts against parasitoid wasps while imposing life-history costs. To investigate the cost–benefit relationship within protected hosts, we introduced multiple isolates of H. defensa to the same genetic backgrounds of black bean aphids, Aphis fabae, and we quantified the protection against their parasitoid Lysiphlebus fabarum as well as the costs to the host (reduced lifespan and reproduction) in the absence of parasitoids. Surprisingly, we observed the opposite of a trade-off. Strongly protective isolates of H. defensa reduced lifespan and lifetime reproduction of unparasitized aphids to a lesser extent than weakly protective isolates. This finding has important implications for the evolution of defensive symbiosis and highlights the need for a better understanding of how strain variation in protective symbionts is maintained.