Biology, images, analysis, design...
|"It has long been an axiom of mine that the little things are infinitely the most important" |
Silver birch aphidOn this page: Identification & Distribution Biology & Ecology: Taxonomy Life cycle Distribution & Behaviour Leaf colour and senescence Competition and coexistence Natural enemies Plant defenses Climate change Other aphids on the same host
Identification & Distribution
Adult winged viviparae of Euceraphis betulae have the head and thorax black above and below, and a pale green to pale yellow abdomen with or without transverse black bands or black patches. They are covered with bluish-white wax, but recently moulted specimens may lack wax. The species is difficult to separate from Euceraphis punctipennis. The only reliable character to separate all forms is that the base of antennal segment VI is usually 0.8-1.32 times longer than the second hind tarsal segment (cf. Euceraphis punctipennis, which has the base of antennal segment VI usually 1.33-1.75 times longer than the second hind tarsal segment). Particular stages in the life cycle can be more readily distinguished. The fundatrix (see first picture below), which is only present in spring (mid-April to mid-May), always has multiple dark cross bands (cf. Euceraphis punctipennis, whose fundatrix has dark bands or patches on abdominal tergites IV & V).
The identity of the adult fundatrigeniae (see second picture above) which are present from mid-May to June can be determined by examining the pigmentation of the legs and antennae. Euceraphis betulae has the basal part of its fore tibia pigmented & scabrous for at least one third of its length (cf. Euceraphis punctipennis, which has the basal part of the fore-tibia pigmented and scabrous for never more than quarter of total length). Euceraphis betulae has the basal parts of antennal segments III and IV pigmented (cf. Euceraphis punctipennis, which has the basal parts of antennal segments III and IV pale). After June these species cannot be discriminated on the basis of extent of their pigmentation. The body length of Euceraphis betulae alates is 3.0-4.2 mm. Immature Euceraphis betulae are green with conspicuous short black-tipped siphunculi.
The silver birch aphid lives on the undersides of leaves of silver birch (Betula pendula). Sexual forms (see below) occur from September to November. Euceraphis betulae occurs throughout Europe and has been introduced to North America and Australia.
Biology & Ecology:
Blackman (1977) distinguished aphids formerly regarded as Euceraphis punctipennis as two species, Euceraphis punctipennis and Euceraphis betulae, on the basis of cytological and morphological differences. Euceraphis punctipennis is primarily associated with downy birch (Betula pubescens) and Euceraphis betulae with silver birch (Betula pendula). Seasonal variations in morphometrics, pigmentation and development of wax glands in the two species are described and compared, and a key to European and North American species of Euceraphis provided.
Blackman & de Boise (2002) measured and analysed samples of birch-feeding and alder-feeding aphids of genus Euceraphis using multiple discriminant analysis (canonical variates) to find out if morphological variation correlated with previously reported differences of karyotype and host association. The dataset comprised groups of specimens defined solely by locality and collection date. Mean scores on the first two canonical variates clustered the samples fully in accordance with their karyotypes and host plants, confirming the existence of a number of morphologically similar but distinct host-specific taxa within the Euceraphis betulae group.
Some of the information given below on the life cycle of the birch aphid is extracted from Blackman & Holopainen a year in the life of a birch aphid. The overwintering eggs hatch in early April and the young nymphs feed on the breaking buds and the expanding leaves. The picture below shows a fourth instar immature fundatrix on birch in late April.
By late April/early May they have developed into adult fundatrices (see first picture below) and start to produce offspring (see second picture below).
Colonization of trees by the alate fundatrices (and subsequent alate generations?), and possibly by dispersal of immature apterae, seems remarkably haphazard as regards host. We have found nymphs of Euceraphis betulae on many different hosts including sycamore, sweet chestnut (see first picture below), and even bamboo (see second picture below - note the nymphs are bamboo-feeding Takecallis). We have no evidence that Euceraphis betulae can reach maturity on such abnormal hosts.
By June the offspring of the fundatrices on birch are themselves producing young (see picture below), so by the time the tree is fully in leaf there may be very large numbers of aphids.
When the leaves are mature they are less nutritious, so during July and August Euceraphis betulae alatae go into reproductive diapause and stop producing young. The picture below shows an alate in late July.
In September, when the food accumulated in the leaves throughout the summer starts to be broken down and translocated to the roots of the tree prior to leaf-fall, the sap becomes full of nutrients again and a new generation of winged adults develops. These prefer to feed on the most nutritious, yellowing, leaves.
The next generation of Euceraphis betulae, becoming adult in October-November, is the sexuales, consisting of winged males (see picture below) and wingless brown egg-laying females (oviparae).
The mature wingless ovipara (see picture below) is orange-brown with dark body markings.
When the female has mature eggs inside her, mating occurs and she then lays her eggs on the birch twigs, usually packed in between a bud and the adjacent stems (see picture below).
The eggs are bright orange-yellow when first laid, but soon become shiny black, and are then resistant to the cold of winter. The winter is passed as an egg, and in spring the life cycle of the birch aphid starts afresh.
Distribution & Behaviour
Hajek & Dahlsten (1986) looked at factors affecting the distribution of aphids on European white birch, (Betula pendula) in northern California. Birches were characterized according to tree vigour, microclimate, isolation from other birches, and homeowner maintenance practices. Discriminant analysis was used to distinguish between trees that developed large aphid populations and those that did not. The resulting discriminant function correctly predicted aphid population load for 91.3% of all study trees. Shading of the tree canopy was the single most important variable discriminating between tree groups.
Hopkins & Dixon (2000) looked at the cues used by birch-feeding aphids to select a resting site. Alate aphids were given access to leaves that were either orientated normally or inverted. Euceraphis betulae used gravity and/or light as the main cue, and settled on the surface that was orientated down.
Leaf colour and senescence
Deciduous trees remobilize the nitrogen in senescing leaves during the process of autumn colouration with reds and yellows, which in many species is associated with increased concentrations of anthocyanins. Archetti et al. (2000)observed that autumn colouration is stronger in tree species facing a high diversity of specialist aphids. They proposed a coevolution theory (actually a hypothesis) that the bright colours in autumn might provide an honest signal of defence commitment, thus deterring migrant aphids from settling on the leaves. Holopainen et al. (2008) pointed out that there had been very few experimental results to support the coevolution hypothesis, and tree commitment to phenolics-based defences has not shown direct protection against aphids. Predators and parasitoids have been found to be the major controllers of arboreal aphids. Indirect defences involve the emission of attractive volatile compounds that enhance the effectiveness of carnivorous enemies. The indirect defence hypothesis was presented to explain low aphid diversity on tree species that are green during autumn. This hypothesis suggests that green foliage can continue to produce herbivore-inducible plant volatiles and maintain volatile-based indirect plant defences against aphids until leaf abscission.
Holopainen et al. (2009) examined the nutrient-translocation hypothesis that yellowing tree leaves are colonized by aphids at the end of the growing season owing to improved availability of nutrients in the phloem sap after chlorophyll degradation. They measured aphid densities on potted Betula pendula seedlings in a field site where a small proportion of foliage rapidly turned yellow before normal autumn coloration as a consequence of root anoxia. Aphids were detected on 19 per cent of green leaves and on 41 per cent of yellow leaves. There was no indication of aphid avoidance of yellow leaves, and the number of winged viviparous Euceraphis betulae adults and their nymphs were significantly higher on yellow leaves than on green leaves. The numbers of apterous Betulaphis brevipilosa and Callipterinella tuberculata did not differ between the leaf colour types. The result suggested that only aphid species with an alate generation during colour change can take advantage of yellowing leaves. This may explain the exceptional abundance of Euceraphis betulae compared with other aphid species on birches. Their observation of nearly fivefold greater Euceraphis betulae density on yellow leaves compared with green leaves gives numerical evidence of aphid preference for yellowing leaves. This confirms the earlier anecdotal evidence that aphids prefer yellow over green leaves in late-season birch, strongly suggesting that yellow is not a warning signal for aphids. The results with Euceraphis betulae indicate that it is not only host alternating aphid species that respond to yellow leaves. A specialist aphid species, that is able to colonize leaves rapidly during the yellowing process, can take advantage of the improved amino-acid composition of leaf phloem sap.
Sinkonnen et al (2012) sought evidence of genetic variation in autumn leaf colours in natural tree populations and investigated whether there was a link between the genetic variation and aphid abundance. They measured the size of the whole aphid community and the development of green-yellow leaf colours in six replicate trees of 19 silver birch (Betula pendula) genotypes at the beginning, in the middle and at the end of autumn colouration. They also calculated the difference between green leaf and leaf litter nitrogen and estimated the changes in phloem sap nitrogen loading. Autumn leaf colouration was found to have significant genetic variation. During the last survey, genotypes that expressed the strongest leaf reflectance 2-4 weeks earlier had an abundance of egg-laying Euceraphis betulae females. Surprisingly, the aphid community size during the first surveys was related to leaf litter nitrogen loss by the litter of different birch genotypes. The authors suggested that their results were the first evidence at the tree intrapopulation genotypic level that autumn-migrating pests have the potential to drive the evolution of autumn leaf colours. They also stressed the importance of recognizing the role of late-season tree-insect interactions in the evolution of herbivory resistance.
The spatial and temporal abundance of Euceraphis betulae was investigated by Johnson et al. (2003) in relation to heterogeneity in host plant (Betula pendula) vigour and pathogenic stress. The performance of aphids feeding on vigorous and stressed foliage was also examined. The "plant stress" and "plant vigour" hypotheses have been suggested as opposing ways in which foliage quality influences herbivore abundance. In many plants, however, vigorously growing foliage co-exists with stressed or damaged foliage. There was a negative correlation between branch growth (vigour) and branch stress (leaf chlorosis), with the most vigorous branches displaying little or no stress, and the most stressed branches achieving poor growth. There was a similar negative correlation between vigour and stress at the level of individual trees. At the beginning of the season, Euceraphis betulae were intermittently more abundant on vigorous branches than on branches destined to become stressed, but aphids became significantly more abundant on stressed branches later in the season, when symptoms of stress became apparent. Similar patterns of aphid abundance were seen on vigorous and stressed trees in the following year. Euceraphis betulae performance was generally enhanced when feeding on naturally stressed Betula pendula leaves, but there was some evidence for elevated potential reproduction when feeding on vigorous leaves too. Overall, plant stress probably influences Euceraphis betulae distribution more than plant vigour, but the temporal and spatial variability in plant quality suggests that plant vigour could play a role in aphid distribution early in the season.
Competition and coexistence
Hajek & Dahlsten (1986) studied resource partitioning by the three introduced species. Resources were partitioned by plant part, feeding sites within leaves and leaf phenological state. Overall niche overlap between species reached a maximum of 50% between Betulaphis brevipilosa and Callipterinella calliptera. Co-occurrence of Euceraphis betulae with both other species on leaves was random while Callipterinella calliptera and Betulaphis brevipilosa were more likely to occur together. California populations of Euceraphis betulae and Betulaphis brevipilosa appeared to utilize resources in a fashion similar to endemic Danish populations. This was not the case for Callipterinella calliptera because Danish (? European) populations usually feed inside leaves silked together by spiders or Lepidoptera whilst in California Callipterinella calliptera also commonly feed on exposed leaf surfaces. Hajek & Dahlsten concluded that Callipterinella calliptera had expanded its endemic niche, and by doing so occupied the most generalized niche of the three species studied.
We have found the black banded birch aphid (Callipterinella calliptera) in Britain (see picture below), but feeding on exposed leaf surfaces as in California rather than inside leaves silked together by spiders or Lepidoptera as in Danish populations.
Johnson et al. (2002) examined the indirect impacts of leaf-mining insects on Euceraphis betulae. While many insect herbivores affect one another through changes to host plant chemical composition, Eriocrania also has the potential to affect Euceraphis betulae through structural modification of a shared leaf. Euceraphis betulae mortality was higher when caged on leaves with Eriocrania leaf-miners. Mortality was not affected by the amount of leaf mined or elevated phenolic compound concentrations in mined leaves, but leaf-miner induced damage to the midrib was strongly correlated with poor aphid survival. In field surveys, Euceraphis betulae was significantly less abundant on mined leaves with midrib damage than on mined leaves with just lamina damage, or mine-free leaves. Experiments simulating leaf-miner damage on Betula pendula leaves pinpointed midrib damage as being associated with higher Euceraphis betulae mortality, whereas lamina damage had no effect on aphid mortality. Disruption of phloem hydraulics is proposed as the mechanism underpinning the negative impacts on the aphid. Eriocrania larvae mining leaves with manually damaged midribs weighed more than those in which the midrib was intact. There was also a trend towards higher nitrogen concentrations in leaves in which Eriocrania had damaged the midrib. There could therefore be a selective advantage to leaf-miners that damage the midrib if severance improves leaf nutritional quality, in addition to rendering the leaves unsuitable to potential competitors.
The role of indirect interactions in structuring communities is becoming increasingly recognised. Plant fungi can bring about changes in plant chemistry which may affect insect herbivores that share the same plant, and hence the two may interact indirectly. Johnson et al. (2003) investigated the indirect effects of a fungal pathogen Marssonina betulae (see pictures below) of silver birch (Betula pendula) on an aphid (Euceraphis betulae), and the processes underpinning the interaction.
Marssonina betulae leaf spot symptoms & fruiting bodies. Pictures: Bruce Watt, University of Maine, Bugwood.org Licensed under a Creative Commons Attribution-Noncommercial 3.0 License.
There was a strong positive association between natural populations of the aphid and leaves bearing high fungal infection. In choice tests, significantly more aphids settled on leaves inoculated with the fungus than on asymptomatic leaves. Individual aphids reared on inoculated leaves were heavier, possessed longer hind tibiae and displayed enhanced embryo development compared with aphids reared on asymptomatic leaves; population growth rate was also positively correlated with fungal infection when groups of aphids were reared on inoculated branches. Changes in leaf chemistry were associated with fungal infection with inoculated leaves containing higher concentrations of free-amino acids. This may reflect a plant-initiated response to fungal attack in which free amino acids from the degradation of mesophyll cells are translocated out of infected leaves via the phloem. These changes in plant chemistry are similar to those occurring during leaf senescence, and are proposed as the mechanistic basis for the positive interaction between the fungus and aphid.
Mahdi & Whittaker (1993) studied populations of insect herbivores in three main guilds on experimental saplings and natural birch (Betula pendula) trees which were either foraged or not foraged by wood ants (Formica rufa) in Lancashire. Of the seven aphid species feeding on Betula pendula, two had mutualistic relationships with the ants and were increased in numbers by them. The remaining five species including Euceraphis betulaewere decreased in numbers presumably as a result of predation. The net effect of the ants on all aphids was to decrease them at the beginning of the season, but to increase them in summer and autumn. Other sap-feeding insects and the leaf-chewing guild were all decreased in numbers in the presence of ants.
Hajek & Dahlsten (1987) looked at predation of birch aphids by the coccinellid Adalia bipunctata (see picture below), the most common aphid predator on silver birch in northern California.
Active escape behaviour was more effective for aphids than passive avoidance of detection. Fourth instars of Callipterinella calliptera escaped from coccinellid larvae more frequently when approached from the front, apparently using vision for pre-contact detection of the coccinellid. Level of predation on three aphid species was dependent upon types of aphid defense. Callipterinella calliptera was not as efficient at avoiding capture as Euceraphis betulae. Callipterinella calliptera seldom kicked predators or dropped from leaves, although predators were often sensed by aphids without contact and aphids usually just walked away from them. Nevertheless, both aphid instars were readily captured by fourth instar larval coccinellids.
Hajek & Dahlsten (1987) looked at the defensive behavior of different aphid species on birch against coccinellid larvae. Euceraphis betulae was the most successful escapee. It was highly mobile and frequently walked away from coccinellid larvae. Active escape behavior was much safer for aphids than passive avoidance of detection. Euceraphis betulae escaped from coccinellid larvae more frequently when approached from the front, apparently using vision for pre-contact detection of Adalia bipunctata. These aphids avoided physical contact with larger predators more often than with smaller predators.
Plant-emitted semi-volatile compounds have low vaporization rates at 20-25°C and may therefore persist on surfaces such as plant foliage. The passive adsorption of arthropod-repellent semi-volatiles to neighbouring foliage could convey associational resistance, whereby a plant's neighbours reduce damage caused by herbivores. Himanen et al. (2010) found that birch (Betula spp.) leaves adsorb and re-release the specific arthropod-repelling C15 semi-volatiles ledene, ledol and palustrol produced by Rhododendron tomentosum when grown in mixed association in a field setup.
Rhododendron tomentosum By Wouter Hagens (Own work) [GFDL or CC BY-SA 3.0], via Wikimedia Commons.
In a natural habitat, a higher concentration of ledene was released from birches neighbouring Rhododendron tomentosum than from birches situated more than 5 meters from Rhododendron tomentosum. Emission of a-humulene, a sesquiterpene synthesized by both Betula pendula and Rhododendron tomentosum, was also increased in Rhododendron tomentosum-neighbouring Betula pendula. In assessments for associational resistance, they found that the polyphagous green leaf weevils (Polydrusus flavipes) and autumnal moth (Epirrita autumnata) larvae both preferred Betula pendula to Rhododendron tomentosum. The green leaf weevils also preferred birch leaves not exposed to rhododendron to leaves from mixed associations. In the field, a reduction in Euceraphis betulae aphid density occurred in mixed associations. Their results suggest that plant species may be protected by semi-volatile compounds emitted by a more herbivore-resistant heterospecific neighbour.
Neuvonen & Lindgren (1987) studied the effect of artificial acid rain on the reproduction and survival of the aphid Euceraphis betulae on silver birch in Turku, southern Finland. Results were variable but an index of aphid reproduction pooled over the whole study was significantly higher on acid-treated than on control birches. The reproduction of aphids on acid-treated birches was enhanced when precipitation was below long term average, suggesting an interaction between the stress caused by acid treatment and dry periods.
Peltonen (2006) examined the effects of elevated carbon dioxide and ozone on aphid oviposition preference and birch bud exudate phenolics. Two genotypes of field-growing silver birch (Betula pendula) trees, which were exposed to doubled ambient concentration of CO2 and O3, singly and in combination, were used in an aphid oviposition preference test. It was found that elevated CO2, irrespective of ozone concentration, increased the number of aphid eggs laid one clone, but not in the other. Although elevated CO2 and O3 affected the level of phenolic compounds in one clone, the effects did not correlate with the observed changes in aphid oviposition. It is suggested that neither bud length, which was not affected by the treatments, nor surface exudate phenolics mediate birch aphid oviposition preference.
Other aphids on same host:
Euceraphis betulae has been recorded from 18 Betula species (including Betula pubescens), albeit 10 of those Betula species were exotic hosts in botanic gardens.
Blackman & Eastop list 17 species of aphid as feeding on silver birch (Betula pendula) worldwide, and provide formal identification keys (Show World list). Of those aphid species, Baker (2015) lists 14 as occurring in Britain (Show British list).