Industrial melanism in the spittlebug Philaenus spumarius (L) (Homoptera: Aphrophoridae)*

The visible polymorphism of the spittlebug, Philaenus spumarius, has been investigated in the vicinity of a smokeless fuel factory in the Cynon Valley of south Wales. The factory is a significant source of local particulate air pollution. A striking relationship exists between the combined frequencies of the eight dark (melanic) morphs and proximity to the factory. Maximum melanic phenotype frequencies of over 95“, occur in both sexes immediately adjacent to it and decline to levels normal for south Wales 1.5–6 km away, depending on direction. This relationship is largely confined to sites within the valley; samples from adjacent localities outside it have melanic frequencies within normal limits for the south Wales area. Maximum melanic phenotype frequencies in the Cynon Valley are far higher than any known from elsewhere in the species range in Europe, Asia and North America. No consistent difference is apparent in total melanic frequency between males and females at any of the sites in this study. However, marked differences exist between the sexes in the relative contributions of the eight melanic phenotypes to the overall association with the factory. For females the industrial melanism is entirely attributable to the group flanicollis + gibbus + leucocephalus (mainly leucocephalus) whereas in males both this group and the group quadnmaculatus + albomaculatus + leucopthalmus contribute to the relationship. It is suggested that this relationship is due to the selective effects of the local air pollution from the factory. The exact nature of the selection involved is as yet uncertain; it would appear to be strong since the local adaptation involved has developed in a maximum of 40 generations since the factory was opened. Finally, comparison is made with two other insects, a ladybird and a moth, in which high frequencies of melanic forms are also associated with this pollution source.     

Geographic variation in the colour/ pattern polymorphism of British Philaenus spumarius (L) (Homoptera: Aphrophoridae) populations *

Geographic variation in the frequency of colour/pattern morphs of Philaenus spumarius is described at 48 localities in England and Wales. The sites have been divided into four broad environmental categories, two urban and two rural. There is a distinction between the urban and rural groupings in the relative proportions of the colour morphs; in urban localities there is a higher combined frequency of the eight ‘melanic’ morphs. Differences also exist between locality groupings, and between the sexes, in the relative frequencies of the eight morphs within the ‘melanic’ phenotypic category. Morphs limited to the female sex in some other parts of the species range occur among males in British populations. It is suggested that the different dominance hierarchy between the sexes which exists in Fennoscandian populations may not be characteristic of British populations.     

Population genetics of the spittlebug genus Philaenus (Homoptera: Gercopidae) in Greece

The electrophoretically detectable variability of 18 enzyme loci was studied in three species of the genus Philaenus: P. loukasi, P. spumarius and P. signatus . Four natural populations of P. loukasi , three of P. spumarius and two of P. signatus were analysed. Two loci, aldehyde oxidase-1 and aldehyde oxidase-2 were found to be in strong linkage disequilibrium in both populations of P. signatus . The enzyme loci acid phosphatase, peptidase-2, mannose-phosphate isomerase and aldehyde oxidase-2 proved to be powerful tools for the identification of the species in question. The colour polymorphism is discussed as well as the low average heterozygosities maintained by the three species (0.099 for P. loukasi , 0.027 for P. spumarius and 0.066 for P. signatus) . On the basis of electrophoretic data a phylogenetic tree is constructed.     

Localized industrial melanism in the spittlebug Philaenus spumarius (L.) (Homoptera: Aphrophoridae) in Cardiff docks, south Wales

Twenty-four large adult samples of the meadow spittlebug, Philaenus spumarius , were collected from within a 4 times 3 km area containing Cardiff docks, south Wales. All samples are highly polymorphic for colour and pattern and show marked geographic variation in the combined frequency of the eight melanic morphs (from <15% to > 75%). Maximum melanic phenotype frequencies in both sexes coincide with dock wharfs currently containing large accumulations of pulverized coal and these samples are heavily contaminated with small coal particles. However, interpretation of this association is complicated by the existence, until 1976, of a smokeless fuel factory causing local air pollution immediately adjacent to the area of highest melanic frequency. It is suggested that the association of high levels of melanism in P. spumarius with areas heavily contaminated with particulate pollutants is due to direct selective effects of small particles favouring melanies.     

Mechanical limitations on feeding by meadow spittlebugs Philaenus spumarius (Homoptera: Cercopidae) on wild and cultivated host plants

Abstract. 1. Field observations on the distribution of Philaenus spumarius (L.) on pearly everlasting (Anaphalis margaritacea) and alfalfa (Medicago sativa) showed that the range of feeding sites exploited increased with instar. Development of trichomes, depth of xylem elements, and tissue hardness were measured as possible factors determining the suitability of sites on food plants.
2. Spittlebugs caged outside their normal feeding sites experienced difficulty feeding. Experimental removal of trichomes showed that trichomes prevented younger instars from feeding on the stem. The depth of the xylem elements and tissue hardness were not significant barriers to feeding near the stem apex.
3. By caging fourth and fifth instar nymphs at increasing distances below the terminal bud on A.margaritacea stems, we showed feeding ability declined with distance below the apex, and feeding was more restricted in fourth compared to fifth instars. A similar decline was demonstrated in experiments with fifth instars on M.sativa.
4. On A.margaritacea, this restriction was associated with increasing tissue hardness of the stem with distance from the apex and the presence of trichomes in regions with hard tissues. On M.sativa the associated barriers were a combination of tissue hardness and reduction in the availability of xylem vessels in the penetrable region of the stem. Although the tissues impeding stylet penetration differed in the two hosts, the critical factor in both species was the increase in the amount of lignification of those tissues at increasing distances from the terminal bud.     

Lagged effects of North Atlantic Oscillation on spittlebug Philaenus spumarius (Homoptera) abundance and survival

The North Atlantic Oscillation (NAO) is a large‐scale pattern of climate variability that has been shown to have important ecological effects on a wide spectrum of taxa. Studies on terrestrial invertebrates are, however, lacking. We studied climate‐connected causes of changes in population sizes in island populations of the spittlebug Philaenus spumarius (L.) (Homoptera). Three populations living in meadows on small Baltic Sea islands were investigated during the years 1970–2005 in Tvärminne archipelago, southern Finland. A separate analysis was done on the effects of NAO and local climate variables on spittlebug survival in 1969–1978, for which survival data existed for two islands. We studied survival at two stages of the life cycle: growth rate from females to next year's instars (probably mostly related to overwintering egg survival), and survival from third instar stage to adult. The latter is connected to mortality caused by desiccation of plants and spittle masses. Higher winter NAO values were consistently associated with smaller population sizes on all three islands. Local climate variables entering the most parsimonious autoregressive models of population abundance were April and May mean temperature, May precipitation, an index of May humidity, and mean temperature of the coldest month of the previous winter. High winter NAO values had a clear negative effect on late instar survival in 1969–1978. Even May–June humidity and mean temperature of the coldest month were associated with late instar survival. The climate variables studied (including NAO) had no effect on the growth rate from females to next year's instars. NAO probably affected the populations primarily in late spring. Cold and snowy winters contribute to later snow melt and greater spring humidity in the meadows. We show that winter NAO has a considerable lagged effect on April and May temperature; even this second lagged effect contributes to differences in humidity. The lagged effect of the winter NAO to spring temperatures covers a large area in northern Europe and has been relatively stationary for 100 years at least in the Baltic area.     

Effects of enhanced UVB on populations of the phloem feeding insect Strophingia ericae (Homoptera: Psylloidea) on heather (Calluna vulgaris)

Heather plants (Calluna vulgaris (L.) Hull) were grown for two years (April 1994–October 1996) under ambient or enhanced ultraviolet-B radiation (UVB: 280–315 nm), provided as a modulated treatment simulating a 15% ozone depletion (seasonally adjusted). Populations of the psyllid (Strophingia ericae (Curtis)) were measured before treatment and at yearly intervals thereafter. Before treatment there was no significant difference in the psyllid populations between treatments, or between the experimental and source populations. Enhanced UVB progressively produced a reduction in S. ericae populations compared with controls over 27 months. Analyses of C, N, total water soluble phenolics, total free amino acids and measurements of leaf angles and distances between leaflets demonstrated no effects of UVB treatment. However, concentrations of the amino acid isoleucine were lower (28%) in C. vulgaris exposed to the enhanced UVB treatment. Over the duration of the experiment the psyllid population structure at Lancaster changed from that typical of the upland site of origin (two-year cycle with overlapping cohorts) to a one-year life cycle typical of lowland sites, but this was independent of UVB treatments. Reduced isoleucine might explain the negative effects of elevated UVB on psyllid population numbers, but the precise effects of UVB on host chemistry and morphology are unknown. The problem of interpreting herbivore responses to enhanced UVB treatments in the field is discussed.     

Genetic control of colour /pattern polymorphism in British populations of the spittlebug Philaenus sputnarius (L.) (Homoptera: Aphrophoridae)

The results of breeding experiments designed to determine the genetic control of the colour/pattern polymorphism in Philaenus spumarius in certain British populations are described and contrasted to previously published results for material taken from populations in southern Finland. The 11 principal phenotypes are controlled by seven alleles at a single autosomal locus, with complex patterns of dominance and co-dominance. In Finland, and most of the rest of the species' extensive range, the eight melanic morphs are wholly or substantially limited to the females, in which they are dominant to the typical form. Previously, this sex limitation has been explained in terms of reduced penetrance of melanic alleles in males and/or dominance reversal between the sexes, such that the eight melanic phenotypes (controlled by five alleles which are adjacent in the dominance heirarchy) are dominant to typical in the females but recessive in the males. Published data on morph frequencies in S Finland and on breeding experiments using material collected from these populations are re-examined and it is shown that neither theory accounts adequately for all the evidence. By contrast, in most British populations there is greatly increased penetrance in males of the melanic morphs which are strictly female-limited elsewhere. Breeding experiments, using P. spumarius taken from selected British populations, provide clear evidence that melanics are dominant to typical in both sexes. This difference in genetic control is entirely consistent with the balance of morph frequencies between the sexes in the populations from which the breeding material for the two separate studies was taken. Experimental material for this study was taken from populations in the Cynon Valley in south Wales, which have the highest melanic frequencies in the species' range and show particularly clear expression of melanic phenotypes in males. Both of these features are strongly correlated with severe aerial pollution from a local smokeless fuel factory. Selection for melanism in these populations is clearly strong, which probably accounts for the high level of penetrance and the dominance of melanics to typical in both sexes. Although further experiments are needed, it is suggested that regulatory loci, controlling the penetrance and expression of melanic alleles in males, could account for the observed differences in genetic control between populations in Britain and Finland.     

Temperature and the colour polymorphism of Philaenus spumarius (Homoptera: Aphrophoridae)

ABSTRACT.

• 1 The spittle bug, Philaenus spumarius (L.), has eleven distinct elytral colour pattern morphs in Britain, of which three are designated non-melanic and eight melanic. Frequencies of different morphs vary between populations.
• 2 The role of thermal factors in the maintenance of the balanced polymorphism was investigated by measurements of dorsal reflectance and body temperature when artifically irradiated.
• 3 Non-melanic forms had higher reflectances and showed lower temperature excesses when irradiated. There was considerable variation in reflectance for the populi–typicus morph group, and trilineatus is therefore the only true‘non-melanic’morph.
• 4 For samples along altitudinal transects in three Scottish glens, trilineatus frequencies were found to be negatively and populi-typicus and melanic frequencies positively correlated with altitude.
• 5 Thermal considerations do therefore play some role in the broad and complex selection regime of P.spumarius.

     

Post-embryonic photoreceptor development and dark/light adaptation in the spittle bug Philaenus spumarius (L.) (Homoptera, Cercopidae)

The aims of this paper have been to describe (1) the general structure of the compound eye of the spittle bug Philaenus spumarius, (2) the eye's post-embryonic development, (3) photomechanical changes upon dark/light adaptation in the eye, and (4) how leaving the semi-aquatic foam bubble and turning into an adult affects the organization of the eye. Spittle bugs, irrespective of size or sex, possess apposition type compound eyes. The eye's major components (i.e. facet, cornea, cone and rhabdom) grow rather isometrically from the smallest nymph to the adult. Photomechanical changes can occur during both nymphal and adult phases and manifest themselves through pigment granules and mitochondria migrating to and away from the rhabdom, and rhabdom diameters varying with time of day and ambient light level. When a nymph transforms into an adult, its compound eyes’ dorsoventral axes widen, facet diameters increase, facet shapes turn from circular to pentagonal and hexagonal, the cornea thickens and the rhabdoms become thinner. The agile adults, free from the foam that surrounds the nymphs, can be expected to need their vision more than the nymphs, and the changes in eye structure do, indeed, indicate that the adults have superior visual acuity. A thicker cornea in the adults reduces water loss and protects the compound eye from mechanical and light-induced damage: protection given to the nymphs by their foam bubbles.     

The effect of increased deposition of atmospheric nitrogen on Calluna vulgaris in upland Britain

Regular (monthly) additions of NH₄NO₃ (4–12 g N m⁻² yr⁻¹) were made over a period of 8 yr (1989–98) to areas of moorland in North Wales dominated by the ericaceous shrub Calluna vulgaris . Results from the early stages of the experiment (1990–94) have shown marked and dose-related increases in shoot extension and canopy height in response to the nitrogen treatments, with significantly higher shoot nitrogen contents. The nitrogen-related stimulation in the growth of the C. vulgaris canopy over this period has resulted in large accumulations of litter on the high-nitrogen-treated plots (6.6 kg m⁻² in plots treated with 12 g N m⁻² yr⁻¹, compared with 3.8 kg m⁻² for the water controls). Litter nitrogen concentrations were also significantly increased at the higher rates of nitrogen addition, leading to a doubling of the total return of nitrogen to the litter layer over the experimental period. These changes in vegetation structure were associated with large reductions in the abundance of the bryophyte and lichen species normally present under the untreated canopy. Results since 1994, however, show little increase in shoot extension in response to the nitrogen treatments, with no clear dose response to increasing levels of addition. These findings are associated with a dose-related increase in the susceptibility of the nitrogen-treated areas of the C. vulgaris canopy to late winter injury, characterized as browning of the shoot tips in early to late spring. These results indicate that deleterious effects are now accumulating as a result of the long-term addition of nitrogen to these moorland plots.     

The classification of adult colour forms of Philaenus spumarius (L.) (Homoptera: Insecta)

Philaenus spumarius is an insect of wide geographical distribution which has a number of colour morphs. This is a report of an attempt to provide an objective classification of the morphs by direct measurement of some visual characteristics. Distribution of these within the sample did not follow a normal curve but it was not possible to correlate the observed distribution with the subjectively sorted groups. This throws some doubt on the validity of the traditional subjective classification and on deductions based on this.     

A laboratory assessment of the relative susceptibility of Molinia caerulea (L.) Moench and Calluna vulgaris (L.) Hull to a range of herbicides

There is a concern that Molinia caerulea (L.) Moench may be increasing in upland moorland communities at the expense of Calluna vulgaris (L.) Hull and other ericaceous species. In order to develop a strategy for the control of Molinia, laboratory studies were carried out to determine the dose-response relationships of seven graminicides and glyphosate on both Molinia caerulea and Calluna vulgaris. Plants were grown under laboratory conditions and sprayed with increasing doses of herbicide using a precision sprayer. Results were highly variable, indicating the great morphological plasticity of these two species, making determination of the ED₅₀ difficult. Glyphosate, quizalofop-ethyl and sethoxydim successfully reduced various measures of Molinia growth to 50% of control levels (ED₅₀ estimates ranged from 0.41–0.67 kg a.i. ha^-1, 0.18–1.20 kg a.i. ha^-1and 0.37–0.49 kg a.i. ha^-1respectively). In contrast, only glyphosate reduced Calluna growth significantly (ED₅₀s ranged from 0.025–0.45 kg a.i. ha^-1), whilst selective herbicides left it undamaged. A comparison of the results for Molinia and Calluna suggests that there is no application rate of glyphosate which will reduce Molinia effectively whilst leaving Calluna undamaged. Recommendations for field testing of selective herbicides are discussed.     

The Lepidoptera fauna associated with Calluna vulgaris: effects of plant architecture on abundance and diversity

Abstract .1. The effects of plant architecture on the Lepidoptera assemblage associated with heather Calluna vulgaris were studied at four locations in northern England and southern Scotland in 1992 and 1993. The study areas were Calluna vulgaris – Vaccinium myrtillus heaths, where management by rotational burning had created a mosaic of stands of different-aged Calluna . Lepidoptera were sampled in the larval stage.
2. Larval abundance was considered in relation to Calluna age, height, cover, green shoot density, and flower density. For most study areas and species, multiple regression selected Calluna height as the variable that explained most variation in larval density, although the explanatory variables were intercorrelated.
3. After compensating for the effects of different study locations, the slope of the regression between the logarithm of larval density and the logarithm of Calluna height was common to the macrolepidoptera, microlepidoptera, geometrid, and noctuid larval groups.
4. There was a significant progressive increase in larval diversity with increase in Calluna height, due to the presence of uncommon moth species in the samples from taller Calluna, and a change in the contribution of common species to the community in different height zones.
5. The significance of these results is discussed in relation to other heathland invertebrate studies and management practices.     

The influence of ammonium nitrate on the root growth and ericoid mycorrhizal colonization of Calluna vulgaris (L.) Hull from a Danish heathland

Conversion of European heathlands to grassland has been reported as a response to increased nutrient availability, especially of nitrogen; a direct effect upon mycorrhizal colonization has been proposed as an likely explanation.This hypothesis was tested in a random block experiment with four blocks and four replicates on a Danish inland heath, Hjelm Hede. Ammonium nitrate was applied (0, 35, 50 and 70 kg N ha^–1 year^–1) to a stand of Calluna vulgaris (L.) Hull four times annually for 2 years. Calluna roots were sampled on four occasions in the 2nd year of the nitrogen treatment. The extent of ericoid mycorrhizal colonization was determined by direct observation of the roots using a line-intersection method. The nitrogen content of the current-year shoots of Calluna increased when they were treated with nitrogen. Nitrogen fertilization had no significant effects on ericoid mycorrhizal colonization of Calluna nor on root biomass. The seasonal variation in mycorrhizal colonization of the Calluna roots was highly significant. The spatial variability of mycorrhizal colonization, both in replicated plots and in the two contrasted soil horizons – the mor layer and the bleached sand – within the plots, were considerable. I conclude that heather decline under enhanced nitrogen input is unlikely to be caused by a direct impact on the ericoid mycorrhizae of Calluna. Received: 1 December 1998 / Accepted: 7 December 1999