White plant shoots , wax-producing insects and other white structures made by arthropods : A mimicry complex ?

Many insects masquerade as parts of plants, such as bark or leaves, or mimic poisonous organisms in order to defend themselves against predators. However, recent studies indicate that plants may mimic insects and other arthropods to deter herbivores. Here, I report visually similar white structures of plants and arthropods in Japan and suggest they are part of a mimicry complex. Young shoots covered with white trichomes or waxy substances may mimic wax-producing insects, such as woolly aphids, coccids and caterpillars, potentially resulting in reduced herbivory. Since wax-producing insects would reduce plant quality and quantity, be distasteful and attract natural enemies, herbivorous insects and mammals may avoid such white shoots. Furthermore, fungus-infected insects, gregarious braconid cocoons, spider egg sacs and froth made by froghopper nymphs or blasticotomid sawfl y larvae are also conspicuously white and impose risks for herbivorous insects. Thus, these white structures may be mimicry models for white shoots and are likely to be part of a defensive mimicry complex. Although this study focuses on defence against herbivores, there are simultaneous physiological roles for white colouration that will not be discussed in depth here.

Visual mimicry of arthropods or their structures by plants is attained primarily by pigments (e.g.anthocyanin, betalain) and occasionally by trichomes and internal,

White plant shoots
The terminal parts of young shoots, including the buds, stems, and young leaves of some herbaceous plants, shrubs and trees, were visually similar to the human eye to colonies of wax-producing insects (Table 1a).These were caused by a dense covering of white trichomes on the stems of Artemisia indica Willd.var.maximowiczii (Nakai) H. Hara (Asteraceae) (Fig. 1a), Achyranthes bidentata Blume var.faurieri (H.Lév.et Vaniot) (Amaranthaceae) (Fig. 1b), Macleaya cordata (Willd.)R. Br. (Papaveraceae) (Fig. 1c), Lespedeza thunbergii Nakai (Fabaceae), Rubus phoenicolasius Maxim.(Rosaceae) (Fig. 1d) and Clerodendrum trichotomum Thunb.(Lamiaceae) (Fig. 1e), or by whitish waxy substances on buds and young leaves of Chenopodium album L. (Amaranthaceae) (Fig. 1f) and Melia azedarach L. (Meliaceae) (Fig. 1g).Peduncles of Sonchus oleraceus L. (Asteraceae) (Fig. 1h) are covered with white wax, which resembles woolly aphid colonies.Most of these white structures are abundant in spring and early summer (from March to June on A. indica var.maximowiczii, M. cordata, R. phoenicolasius, C. trichotomum, M. azedarach, S. oleraceus), but are also found in mid summer and autumn (July to November on A. bidentata var.faurieri, L. thunbergii, C. album).Although A. bidentata var.faurieri and M. azedarach are restricted to grasslands and forest edges in the lowlands and R. phoenicolasius grew only in mountainous regions, other species are found commonly from lowlands to montane areas.There is variation in the density of white trichomes and amount of wax on individual plants, and mature shoots mainly lack trichomes and wax.
White surfaces scatter-refl ect all spectra of visible light.Because white is striking against dark backgrounds, such as soil, bark, or foliage, many animals use white patterns for communication among conspecifi cs or with other animals.White colouration is also useful for thermoregulation, and may provide camoufl age in snowy or icy environments or in deserts with light-coloured sand (e.g.Cloudsley-Thompson, 1979;Caro, 2005Caro, , 2009;;Lev-Yadun, 2016).In insects, various taxa produce white waxes that are mixtures of long-chain esters, straight-chain hydrocarbons and free fatty acids (Brown, 1975) as a defence against natural enemies, UV radiation and desiccation (Pope, 1979(Pope, , 1983;;Eisner et al., 2005;Yamazaki, 2012).On the other hand, plants use white colouration primarily to attract pollinators, although most white fl owers have at least some dark parts when viewed under UV radiation, which usually serve the pollinating insects as nectar guides (Eisner et al., 1969;Tanaka, 1982).In addition, the vegetative parts of many plants have white patterns caused by trichomes, waxy substances and various mechanisms that cause visual variegation (Lee, 2007;Lev-Yadun, 2014a).These whitish parts have physiological functions such as increasing UV refl ection and desiccation tolerance (Lee, 2007), but may also play a role in visual mimicry (Lev-Yadun, 2014a, 2016).
Here, I discuss white plant structures occurring in Japan that have the potential to visually mimic wax-producing insects, and propose a possible white mimicry complex involving plants and insects.

STUDY SITES AND METHODS
I searched for possible instances of defensive animal mimicry by plants as a pilot study in Japan from March to November in 2010 to 2016.Various types of plants, including herbaceous plants, climbers, shrubs and trees, were carefully examined in urban parks, botanical gardens, arable lands, along riverbanks and in forests in Osaka, Kyoto, Nara, Hyogo, Wakayama, and Yamanashi Prefectures in central Japan.Primary study sites were Tsurumi-ryokuchi Park (34°42´N, 135°34´E, 4 m above sea level), Osaka Castle Park (34°41´E, 135°31´E, 30 m a.s.l.), Nagai Botanical Garden (34°36´N, 135°31´E, 9 m a.s.l.), Kyoto Botani-  bacher spp.), on various plant taxa (Table 1b).These waxproducing insects occurred intermittently from spring to autumn commonly in lowland and mountainous areas, and were found on buds (C.yasushii), stems (C.clematis, lepidopteran caterpillars) or the undersides of leaves (S. celti, A. mori, P. morimotoi, Eriocampa spp., E. hainesii hainesii).White colonies of woolly aphids and jumping plant lice on the underside of leaves looked like trichome-covered leaves (Fig. 2a).Stems covered with wax-producing fl atid nymphs, which resembled white plant stems, were abundant in spring and early summer (Fig. 2b).

Other white structures produced by insects and plants
Furthermore, fungus-infected insects [e.g.caterpillars (Fig. 3a), cicadas] covered with white fungal hyphae and conidia, were found in rainy summers and autumns and were visually similar to wax-producing caterpillars or homopteran colonies.Other structures made by various terrestrial arthropods resemble wax-producing insects or white plant structures: gregarious braconid cocoons (Fig. 3b), spider egg sacs and webs (Fig. 3c), froth made by froghopper nymphs (Fig. 3d) or blasticotomid sawfl y  larvae (Fig. 3e) and cotton-like galls induced by the gall midge Rhopalomyia giraldii Kieffer & Trotter (Fig. 3f).These white structures were commonly found from spring to autumn in lowland to mountainous areas (Table 1c).Other plant parts, including asteraceous pappi (Fig. 3g) and salicaceous comae (Fig. 3h), also look like wax-producing insect colonies (Table 1c), but such plant structures were seen only during a limited period in spring.

White shoots may mimic wax-producing insects
White plant shoots and wax-producing insects are visually similar (i.e., cylindrical, sheet like or patchy in appearance) and can be commonly found from spring to autumn and in both lowlands and mountainous regions (Table 1).Therefore, I propose that white young shoots may visually mimic wax-producing insects, potentially leading to a decrease in herbivory for the following reasons.
It is very important for plants to protect their young shoots, as they contain soft, nutritious meristems and growing tissues that are essential for vegetative growth and reproduction, and they are thus more vulnerable to herbivory than older shoots.Although mature plant tissues are sometimes also attacked by herbivores, physical toughness and chemical defences generally make them less vulnerable to herbivory (e.g., Feeny, 1970;Lev-Yadun & Ne'eman, 2007).Young shoots covered with white trichomes and waxy substances are found coincidentally with wax-producing insects at a variety of sites and in different seasons.This white colouration is visually striking against dark backgrounds (Lev-Yadun, 2014b).Wax-producing herbivorous insects reduce food plant quality or quantity by sucking plant sap, consuming leaves and transmitting pathogens (Eastop, 1977).Wax or wax-producing insects are distasteful or a deterrent to many other arthropods, including ants and spiders, and possibly also to vertebrates (Eisner et al., 2005;Moss et al., 2006;Schwartzberg et al., 2010;Yamazaki, 2012).Although a waxy cover deters predation by ants and spiders, certain wax-producing homopterans are tended by ants and attacked by predators and parasitoids (Delabie, 2001;Eisner et al., 2005), rendering shoots with wax-producing insects dangerous or less palatable to other herbivores.
Based on these facts and observations, such white-coloured shoots are proposed here to visually mimic waxproducing insects, resulting in reduced herbivory.Simultaneously, white coatings on new shoots may mimic phytopathogenic fungal infections (Lev-Yadun, 2006b, 2016;Yamazaki & Lev-Yadun, 2015) or wounded shoots oozing white toxic latex (Lev-Yadun, 2014b) and in addition, probably protect plant tissues from UV light and desiccation (Lee, 2007), as well as from attack by herbivorous insects (Levin, 1973).

White mimicry complex across plants, fungi and arthropods
Moreover, other white structures produced by arthropods, including fungal-infected insects (though their white colour is derived from fungal hyphae and spores), parasitoid cocoons, spider egg sacs and webs, froghopper froth and some plant galls that resemble wax-producing insects and each other, can be found in various habitats throughout the vegetative season (Table 1).Thus, Müllerian and Batesian white mimicry complexes and rings may extend beyond young white shoots mimicking wax-producing insects.
White structures other than wax produced by arthropods are harmful to herbivores.For example, fungal-infected insects are lethal for other herbivorous insects because of the possibility of horizontal transmission, and because they may contain toxic substances (Roy et al., 2006).Froth produced by spittlebugs and blasticotomid sawfl ies contains a detergent (Mello et al., 1987;Cooper & Kennedy, 2010) and small arthropods may drown in the foam.Because spider egg sacs and webs indicate the presence of mature spiders, herbivores are likely to avoid them, as suggested by recent studies of non-consumptive negative effects of spiders on herbivores (Hlivko & Rypstra, 2003;Rypstra & Buddle, 2013;Yamazaki & Lev-Yadun, 2015).Parasitoid cocoons indicate that parasitoids are present in the vicinity.Owing to their conspicuous white colour, these structures, as well as wax produced by arthropods, may provide herbivores with obvious cues of hazards.Consequently, they may function in a manner similar to Müllerian mimicry, if several such taxa occur together.
It is also possible and probable that these white arthropod structures have simultaneous physical and physiological functions, and that they only secondarily serve as a defensive mimicry complex.Parasitoid cocoons, spider egg sacs and froghoppers are in fact attacked by specialist predators and parasitoids (Tagawa & Fukushima, 1993;Sullivan & Völkl, 1999;Finch, 2005;Tanaka & Ohsaki, 2006); however, many generalist predators and parasitoids may fi nd it diffi cult to handle wax, cocoons, egg sacs and froth (Whittaker, 1970;Austin, 1985;Akiyama & Matsumoto, 1986;Hieber, 1992;Eisner et al., 2005).White cotton-like galls may mimic these white arthropod structures and reduce herbivory on galls and surrounding plant tissues, resulting in higher survival rates for galling insects and their host plants.Because galls are attractive food sources for certain herbivores they are vulnerable to herbivory if not well-defended and as a consequence may be protected by aposematism and mimicry in addition to chemical and physical defences (Inbar et al., 2010;Rostás et al., 2013;Yamazaki, 2016).Plant pappi and comae are white and abundant, but also temporal.Therefore, these plant structures do not seem to be an important part of the white mimicry complex.
To investigate this mimicry hypothesis further, the optical characteristics (e.g.under both visible and UV spectra) of white shoots and insect-produced wax should be compared.Future studies should also investigate the effects on herbivory of removing white trichomes or waxy substances from shoots, or adding white coatings to normal shoots.Furthermore, herbivore damage, and rates of visitation by predators and parasitoids should be compared between related plants bearing normal shoots versus white shoots.Patterns in the occurrence of such white structures should be examined in relation to the intensity of herbivory using phylogenetically controlled methods.
In conclusion, because white is a prominent colour in forests and grasslands, white structures often serve as warning signals.In some plant species, young shoots may mimic wax-producing insects, probably leading to reduced herbivory.In addition, fungus-infected insects, spider egg sacs, parasitoid cocoons and froghopper froth are also likely to be mimicry models for white shoots, and together constitute a white mimicry complex along with wax-producing insects.Further observations on other organisms using optical analyses and fi eld experiments are required to confi rm the existence and elucidate the mechanisms of this putative defensive mimicry complex.

Table 1 .
White structures on plants and of arthropods recorded in central Japan.