Uroleucon Research Articles

Chemodiversity affects preference for Tanacetum vulgare chemotypes in two aphid species

Plants of the same species can strongly differ in their specialized metabolite profiles, which can affect insect presence and abundance in the field. However, how specialized chemistry shapes plant attractiveness to herbivorous insects is not fully understood. Here, we used common tansy Tanacetum vulgare, Asteraceae) – a perennial plant that is highly diverse in terpenoid composition and is known to have variable chemotypes – to test whether 1) plants with different chemotype profiles differ in attractiveness to two specialist aphid species, Macrosiphoniella tanacetaria and Uroleucon tanaceti, in pairwise choice assays; 2) the diversity of the terpenoid blend affects plant attractiveness to aphids; 3) how plant chemical traits relate to plant morphological traits and which traits best explain aphid preference. We found that M. tanacetaria preferred two out of five chemotypes, dominated by α‐thujone/β‐thujone and β‐trans‐chrysanthenyl acetate, while avoiding a chemotype dominated by α‐pinene/sabinene. Uroleucon tanaceti showed no clear preference towards chemotypes, but when given a choice between chemotypes dominated by α‐thujone/β‐thujone and by α‐pinene/sabinene, they preferred the former. Importantly, plant attractiveness to aphids was marginally negatively correlated with chemodiversity, i.e. the number of terpenoid compounds, in M. tanacetaria, but not in U. tanaceti. Interestingly, the relative concentration and number of terpenoids were generally higher in larger and bushier plants. Hence, we did not observe a tradeoff between plant growth and defence. We conclude that plant chemical composition affects plant attractiveness to aphids and hence may contribute to variation in natural aphid colonization patterns on plants of the same species.

Intraspecific chemodiversity provides plant individual- and neighbourhood-mediated associational resistance towards aphids.

Some plant species express an extraordinarily high intraspecific diversity in phytochemicals (= chemodiversity). As discussed for biodiversity, higher chemodiversity may provide better protection against environmental stress, including herbivory. However, little is known about whether the resistance of a plant individual towards herbivores is mostly governed by its own chemodiversity or by associational resistance provided by conspecific neighbours. To investigate the role of chemodiversity in plant-aphid interactions, we used the Asteraceae Tanacetum vulgare, whose individuals differ pronouncedly in the composition of leaf terpenoids, forming distinct chemotypes. Plants were set up in a field consisting of plots containing five individuals of either the same or different chemotypes. Presence of winged aphids, indicating attraction, and abundance of winged and unwinged aphids, indicating fitness, were counted weekly on each plant. During the peak abundance of aphids, leaf samples were taken from all plants for re-analyses of the terpenoid composition and quantification of terpenoid chemodiversity, calculated on an individual plant (Shannon index, Hsind, also considered as α-chemodiversity) and plot level (Hsplot, = β-chemodiversity). Aphid attraction was neither influenced by chemotype nor plot-type. The real-time odour environment may be very complex in this setting, impeding clear preferences. In contrast, the abundance was affected by both chemotype and plot-type. On average, more Uroleucon tanaceti aphids were found on plants of two of the chemotypes growing in homogenous compared to heterogenous plots, supporting the associational resistance hypothesis. For Macrosiphoniella tanacetaria aphids, the probability of presence differed between plot-types on one chemotype. Terpenoid chemodiversity expressed as a gradient revealed negative Hsplot effects on U. tanaceti, but a positive correlation of Hsind with M. tanacetaria abundance. Aphids of M. fuscoviride were not affected by any level of chemodiversity. In conclusion, this study shows that not only the chemotype and chemodiversity of individual plants but also that of conspecific neighbours can influence certain plant-herbivore interactions. These effects are highly specific with regard to the plant chemotype and differ between aphid species and their morphs (winged vs. unwinged). Furthermore, our results highlight the importance of analysing chemodiversity at different levels.

Invertebrate fauna associated with the cultivation of Vernonia calvoana calvoana (Asteraceae) in Yaound (Center-Cameroon)

Vernonia calvoana is a culture spread across the world and prized for its culinary and medicinal virtues. The data was collected in Yaounde, Central Cameroon region through manual harvesting at two stations from 2017 to 2019. A total of 168 species or morphospecies belonging to 47 families and 12 orders from two phyla were collected. The most abundant phylum was Arthropoda which represented 99.96% of the total number of all species, while Mollusca represented the rest. Within arthropoda, insecta class was found the most dominant. In Insecta, Formicidae and Aphididae were the most frequent families. At Nkolbisson, Hymenoptera and Hemiptera are more abundant on the purple variety than on the white variety. However, both are less abundant compared to those at Nlong-mvolye. The species Uroleucon compositae (37.01%), Hilda cameroonensis (4.67%) and Sphaerocoris annulus (2.71%) were the most abundant species recorded in all the three variants. Depending on the preference with the host plant, some orders have a distribution according to the site, but also, the variety. Key words: Manual harvest, insecta, hymenoptera, hemiptera, Nkolbisson, Nlong-mvolye.

Lady Beetle Oviposition Site Choices: Maternal Effects on Offspring Performance

Maternal effects can result in adaptive phenotypic responses of offspring that increase their fitness. Several recent studies report a positive relationship between maternal choices and offspring fitness. However, few studies have assessed the associations between aphidophagous lady beetle oviposition site selection, the adequacy of food resources for their offspring, and offspring performance. To clarify these issues, we explored whether aphidophagous lady beetle oviposition site selection can influence offspring performance, thereby reflecting adaptive maternal behavior. To assess the effect of food resources on offspring performance, we fed the larvae of 3 lady beetle species: Cycloneda sanguinea (L.), Harmonia axyridis (Pallas), and Hippodamia convergens (Guerin-Meneville) (all Coleoptera: Coccinellidae), with different types of aphids (Uroleucon and Brevicoryne) (both Hemiptera: Aphididae) then measured development time, survival, adult body mass, brightness, and chromatic coloration of the adult beetles. We found that Ha. axyridis larvae fed Brevicoryne exhibited a higher survival rate than those fed Uroleucon. Also more adults emerged from C. sanguinea larvae fed Uroleucon aphids, and these adults were heavier, shinier, with more chroma, and developed faster than those fed on Brevicoryne. Overall, lady beetles performed better when fed aphids commonly found near their respective oviposition sites. We conclude that aphidophagous lady beetle oviposition site selection reflects adaptive maternal choices associated with an adequate food resource positively affecting offspring fitness. Elucidating the links between lady beetle oviposition site choice and optimal resource for their offspring enhances our understanding of habitat use and co-existence of aphidophagous lady beetle communities in Brazilian agroecosystems. Resumo Os efeitos maternos podem resultar em respostas fenotipicas adaptativas da prole que aumentam sua aptidao. Varios estudos recentes relatam uma relacao positiva entre escolhas maternas e aptidao dos filhos. No entanto, poucos estudos avaliaram as associacoes entre a selecao do local de oviposicao de besouros afidofagos, a adequacao dos recursos alimentares para a prole e o desempenho da prole. Para esclarecer essas questoes, avaliamos se a selecao do local de oviposicao de besouros afidofagos pode influenciar o desempenho da prole, refletindo assim o comportamento materno adaptativo. Para avaliar o efeito dos recursos alimentares no desempenho da prole, alimentamos as larvas de tres especies de besouros: Cycloneda sanguinea (L.), Harmonia axyridis (Pallas), e Hippodamia convergens (Guerin-Meneville) (todos Coleoptera: Coccinellidae), com diferentes tipos de pulgoes (Uroleucon e Brevicoryne) (ambos Hemiptera: Aphididae), medimos o tempo de desenvolvimento, a sobrevivencia, a massa corporal adulta, o brilho e a coloracao cromatica dos besouros adultos. Foi observado que larvas de Ha. axyridis alimentadas com Brevicoryne exibiram uma taxa de sobrevivencia mais alta do que aquelas alimentadas com Uroleucon. Tambem emergiram mais adultos de larvas de C. sanguinea quando alimentadas com pulgoes Uroleucone e esses adultos eram mais pesados, mais brilhantes, com mais croma e se desenvolveram mais rapidamente do que aqueles alimentados com Brevicoryne. No geral, as joaninhas tiveram melhor desempenho quando alimentados com pulgoes comumente encontrados perto de suas respectivas posturas. Concluimos que a selecao do local de oviposicao de besouros afidofagos reflete escolhas maternas adaptativas associadas a um recurso alimentar adequado que afeta positivamente a aptidao da prole. A elucidacao dos vinculos entre a escolha do local de oviposicao do besouro e o recurso ideal para seus filhotes aprimora nossa compreensao do uso do habitat e a coexistencia de comunidades de besouros afidofagos nos agroecossistemas brasileiros. Key Words: Cycloneda sanguinea; Harmonia axyridis; Hippodamia convergens; Uroleucon; Brevicoryne; adaptative maternal behavior View this article in BioOne

Near-regular distribution of adult crimson tansy aphids,Uroleucon tanaceti(L.), increases aposematic signal honesty on different tansy plant chemotypes

Near-regular distribution of adult crimson tansy aphids,<i>Uroleucon tanaceti</i>(L.), increases aposematic signal honesty on different tansy plant chemotypes

Volatile, stored and phloem exudate-located compounds represent different appearance levels affecting aphid niche choice

Intraspecific and intra-individual differences in emitted volatile compounds and in surface and phloem sap-related metabolites do not only affect host plant choice of monophagous aphids but may also guide them to the plant part that provides their ideal niche by maximising their fitness. However, little is known about the variation at these different plant appearance levels. We investigated the preferences of the monophagous aphid species Macrosiphoniella tancetaria and Uroleucon tanaceti for different plant parts (inflorescence stems, young and old leaves) of Tanacetum vulgare plants from two chemotypes, testing their reactions towards volatile, surface and phloem sap-related cues. Furthermore, we studied the variation in leaf glandular trichome density as well as in the composition of volatile, stored and phloem exudate-located specialised (secondary) plant compounds from the different plant parts of these chemotypes. Aphid species showed differences in their preferences. Aphids of M. tanacetaria had to assess the entire plant to choose the stem, whereas U. tanaceti only needed volatile cues to locate the old leaves, which are the plant parts representing their respective niches. Volatiles and stored metabolites varied in their composition and concentration between chemotypes. Stored metabolites additionally differed among plant parts, which was reflected in distinct trichome densities. The composition of phloem exudate-located specialised compounds mostly varied among plant parts. These pronounced differences in plant chemistry on multiple levels provide distinct perception levels for aphids probably driving their niche choice. This study demonstrates the importance to consider these multiple levels to elucidate plant-herbivore interactions with high resolution.

Aphid infestation leads to plant part-specific changes in phloem sap chemistry, which may indicate niche construction.

Phloem sap quality can differ between and within plants, and affect the performance of aphids. In turn, aphid infestation may change the chemical composition and nutritional value of phloem sap. However, the effects of different aphid species on the overall phloem sap composition of distinct parts within plant individuals in relation to aphid performance remain unclear. To test the specificity of plant responses to aphids, we used two chemotypes of Tanacetum vulgare plants and placed the monophagous aphids Macrosiphoniella tanacetaria and Uroleucon tanaceti on different plant parts (stems close to the inflorescence, young and old leaves). Aphid population growth was determined and sugars, organic acids, amino acids and metabolic fingerprints of phloem exudates were analysed. Macrosiphoniella tanacetaria performed best on stems, whereas U.tanaceti performed best on old leaves, indicating differences in niche conformance. Aphid infestation led to distinct changes in the phloem exudate composition of distinct metabolite classes, differing particularly between plant parts but less between chemotypes. In summary, plant responses to aphids are highly specific for the chemotype, plant part, metabolite class and aphid species. These changes may indicate that aphids construct their own niche, optimizing the food quality on the plant parts they prefer.

Coexistence through mutualist-dependent reversal of competitive hierarchies.

Mechanisms that allow for the coexistence of two competing species that share a trophic level can be broadly divided into those that prevent competitive exclusion of one species within a local area, and those that allow for coexistence only at a regional level. While the presence of aphid‐tending ants can change the distribution of aphids among host plants, the role of mutualistic ants has not been fully explored to understand coexistence of multiple aphid species in a community. The tansy plant (Tanacetum vulgare) hosts three common and specialized aphid species, with only one being tended by ants. Often, these aphids species will not coexist on the same plant but will coexist across multiple plant hosts in a field. In this study, we aim to understand how interactions with mutualistic ants and predators affect the coexistence of multiple species of aphid herbivores on tansy. We show that the presence of ants drives community assembly at the level of individual plant, that is, the local community, by favoring one ant‐tended species, Metopeurum fuscoviride, while preying on the untended Macrosiphoniella tanacetaria and, to a lesser extent, Uroleucon tanaceti. Competitive hierarchies without ants were very different from those with ants. At the regional level, multiple tansy plants provide a habitat across which all aphid species can coexist at the larger spatial scale, while being competitively excluded at the local scale. In this case, ant mutualist‐dependent reversal of the competitive hierarchy can drive community dynamics in a plant–aphid system.

Effects of intraspecific and intra-individual differences in plant quality on preference and performance of monophagous aphid species.

Plant chemistry is one of the main drivers of herbivore distribution. Monophagous herbivore species are highly specialized, but even within their only host species the chemistry varies. The herbivore's choice is initially mainly guided by volatile plant compounds. Once on the plant, particularly for aphids the phloem quality affects their performance. However, little is known about the intraspecific and intra-individual variation in phloem sap and their influences on monophagous aphids. To determine potential mechanisms involved in aphid colonization, we tested the effects of intraspecific chemical variation in Tanacetum vulgare, which produces different chemotypes, on the preference of two monophagous aphid species. Moreover, we measured the performance of the aphids on different plant parts (stem close to the inflorescence, young and old leaves) of these chemotypes and analyzed their phloem sap composition. Both species preferred the β-thujone (THU) over the trans-carvyl acetate (CAR) chemotype in dual-choice assays. Survival of Macrosiphoniella tanacetaria was neither affected by intraspecific nor intra-individual variation, whereas the reproduction was highest on stems. In contrast, Uroleucon tanaceti survived and reproduced best on old leaves of the preferred chemotype. The sugar, organic acid and amino acid composition pronouncedly differed between phloem exudates of different plant parts, but less between chemotypes. Unexpectedly, high concentrations of amino acids did not necessarily enhance aphid performance. These different performance optima may cause niche differentiation and, therefore, enable co-existence. In conclusion, the tremendous variation in plant chemistry even within one species can affect the distribution of highly specialized aphids at various scales aphid species-specifically.

Mechanisms of species‐sorting: effect of habitat occupancy on aphids' host plant selection

Interspecific interactions such as competition are important factors affecting insect herbivore fitness. Host choice in herbivorous insects including aphids has largely been studied with respect to host plant condition, while the role of competition is also very important. Tansy (Tanacetum vulgare L.) hosts three specialised aphids, Macrosiphoniella tanacetaria (Kaltenbach), Metopeurum fuscoviride Stroyan and Uroleucon tanaceti (L.) (Hemiptera: Aphididae). In this study, a set of greenhouse and field experiments were carried out to investigate whether aphid host plant choice was affected by the presence of the other aphid species. When winged individuals were given the choice between unoccupied plants and plants occupied by the same or another aphid species, choices generally reflected the outcome of competitive interactions among aphids. Colonisation of plants by winged individuals was influenced not only by the presence of other aphids on the host plant but also by previous infestation. The host choice of winged individuals basically reflected competitive hierarchies, i.e. aphids in most cases selected plants where future competition was less likely. By contrast, unwinged aphids did not show any host plant preference. For M. tanacetaria previously infested plants promoted the production of winged offspring. Our results show that competitive interactions could affect host selection behaviour by aphids. In a metacommunity context, such preferences in colonising different habitats leads to species‐sorting through habitat heterogeneity.

Diet-mediated effects of specialized tansy aphids on survival and development of their predators: Is there any benefit of dietary mixing?

Some predators have a broad prey range, but not all prey are equally suitable for a predator. We tested the suitability of three specialized tansy (Tanacetum vulgare) aphids, Macrosiphoniella tanacetaria, Metopeurum fuscoviride and Uroleucon tanaceti, on biological parameters of their major predators, Coccinella septempunctata and Chrysoperla carnea, when aphid species were offered either alone, or as a mixed diet of all the three aphid species. For the lacewing C. carnea, a diet consisting only of the generally ant-tended M. fuscoviride resulted in the shortest larval and total developmental time, in highest larval survival and pupation success. For the ladybird C. septempunctata, a pure diet of the non-tended M. tanacetaria was most suitable, resulting in the shortest total developmental time, heaviest fresh and dry weight. Larvae of both predator species had low survival and none of them developed to pupal stage when offered only U. tanaceti that has a bright red colour, is not ant-tended and feeds on the underside of lower leaves. The mixed diet of all three aphid species was worse than the best single-aphid diet for both predators, for almost all fitness parameters. Thus, while diet mixing may allow predators to avoid the negative impact of unsuitable prey, diet mixing does not necessarily result in the highest fitness of predators.

How aphids decide what is good for them: experiments to test aphid feeding behaviour on Tanacetum vulgare (L.) using different nitrogen regimes

Leaf-chewing herbivores select food with a protein/carbohydrate ratio of 0.8-1.5, whereas phloem sap, which aphids feed on, has a ratio of approximately 0.1. Enhanced N fertilization increases the amino acid concentration in phloem sap and elevates the N/C ratio. The study examines: (1) whether aphids select between plants of different N nutrition, (2) whether feeding time correlates with the amino acid composition of phloem sap, and (3) at which stage of probing aphids identify the quality of the plant. Uroleucon tanaceti (Mordvilko) and Macrosiphoniella tanacetaria (Kaltenbach), specialist aphids feeding on tansy (Tanacetum vulgare L.), were reared on this host plant grown essentially hydroponically (in Vermiculite) in the greenhouse on 1, 3, 6, or 12 mM NH(4)NO(3). One and 3 mM NH(4)NO(3) corresponds to the situation found in natural tansy stands. Aphid stylet penetration was monitored by electrical penetration graphs whilst phloem sap was sampled by stylectomy. Both aphid species settled 2-3 times more frequently on plants fertilized with 6 or 12 mM NH(4)NO(3). The phloem sap of these plants contained up to threefold higher amino acid concentrations, without a change in the proportion of essential amino acids. No time differences were observed before stylet penetration of plant tissue. After the first symplast contact, most aphids penetrated further, except M. tanacetaria on low-N plants, where 50% withdrew the stylet after the first probing. The duration of phloem feeding was 2-3 times longer in N-rich plants and the time spent in individual sieve tubes was up to tenfold longer. Aphids identified the nutritional quality of the host plant mainly by the amino acid concentration of phloem sap, not by leaf surface cues nor the proportion of essential amino acids. However, U. tanaceti infestation increased the percentage of methionine plus tryptophan in phloem tenfold, thus manipulating the plants nutritional quality, and causing premature leaf senescence.

New records and a new subspecies of aphids (Homoptera) from India

Abstract Uroleucon tanaceti indica, subsp. nov. is described from Nefa, India. Apterous oviparous females Amphorophora ampullata Buckton and alate male of Macrosiphum (Sitobion) ? fragariae (Walker) are also recorded for the first time from India.