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Pseudoregma bambucicolaBamboo woolly aphidOn this page: Identification Background On primary host On secondary host Summary & distribution Biology & Ecology On primary host On secondary host Colony growth Ants & soldiers Natural enemies Other aphids on the same hostIdentificationBackgroundPseudoregma bambucicola is a member of the bambucicola / carolinensis group of aphids, which typically host alternate from galls on Styrax to bamboo. The Styrax gall-dwelling Pseudoregma bambucicola was originally named Astegopteryx swinhoei, whilst the secondary host dwellers were named Oregma bambucicola. When they were recognised as different life stages of the same species, these were renamed Pseudoregma bambucicola. The two species within the group, Pseudoregma bambucicola and Pseudoregma carolinensis were differentiated using molecular techniques by Fukatsu et al. (2001). Since then several extremely similar species feeding on bamboo have been synonomized with Pseudoregma bambucicola. These include Pseudoregma albostriata, in Taiwan, described as having four longitudinal wax stripes in life, not three as in Pseudoregma bambucicola. Aphids which have in the past identified as P. bambucicola also occur in India, Sri Lanka and Fiji. Fukatsu et al. (2001) suggest they are Pseudoregma carolinensis, but Blackman thinks they may represent a third (unidentified) species - which we shall refer to as (putative) Pseudoregma bambucicola. Other closely related Pseudoregma species are Pseudoregma koshunensis, which also host alternates to bamboo, and Pseudoregma sundanica, which has ginger (Zingiberaceae) as its secondary host. Species in other closely related genera which gall Styrax and host alternate to bamboo include Astegopteryx bambusae and Cerataphis bambusifoliae. On primary hostPseudoregma bambucicola induce galls from developing flower buds on their primary host, Styrax suberifolius. A mature gall consists of a small central gall from which extend clusters of brown, elongate pod-shaped subgalls (see first picture above) (cf. subgalls of Pseudoregma sundanica on Styrax paralleloneura, which are velvety-white with green internal projections). The subgalls have petiolate bases and osteoles (apical openings) (cf. subgalls of Pseudoregma koshunensis on Styrax suberifolius, which lack a distinct petiole). Also their walls are thinner and softer than those of Pseudoregma koshunensis. The subgalls do not have a clearly marked longitudinal suture (cf. Pseudoregma carolinensis subgalls on Styrax benzoides, which have a conspicuous longitudinal suture, and are smaller). Field-collected Pseudoregma bambucicola galls have 1-15 subgalls, depending upon how many are lost. Each subgall is 24-43 mm long and 5.5-8.9 mm wide. Image above by permission, copyright Aoki & Kurosu, all rights reserved.
The first-instar fundatrix, hatched from sexually produced eggs, feeds on a developing flower bud. It has well-sclerotized tergites with long setae, well-developed hairs on the tarsi and a long slender ultimate rostral segment. The second instar fundatrix, enclosed by the developing gall, has membranous tergites and a shortened rostrum. The adult fundatrix is apterous, with membranous tergites and no siphunculi. Adults maturing after the second generation are generally larger and have siphuncular pores.
Whilst the galls (see above) and emigrant alatae (see below) are readily distinguishable from those of other Pseudoregma species which also form galls on trees of the Styrax genus (series Benzoin), the gall-dwelling adults of these species being 'very similar' are usually ignored. For example Tao (1969) showed an antenna but the aptera was not otherwise described. This is frustrating since alatae are only produced when the gall matures - which is by no means assured for galls once collected from the field!
Image above copyright Tao (1969).
The colour of live gall-dwelling Pseudoregma bambucicola apterae is unknown, albeit presumably waxy. The adult aptera (hitherto undescribed, but described here from a single clarified mount, see picture below) has 4-segmented antennae which are 0.18 times the body length and have a terminal process that is 0.44 times the base of the last antennal segment (cf. Pseudoregma carolinensis, which has 5-segmented antennae and a terminal process 0.35 times the base of the last antennal segment). The eyes of apterae and young nymphs have only 3 ommatidia.
Image above by permission, copyright Aoki & Kurosu, all rights reserved.
There is a pair of forward-pointing horn-like processes on the front of the head, much smaller than on the secondary host apterae. The apical rostral segment (RIV+V) is 0.067 mm, and 0.75 times the second hind tarsal segment (HTII) (cf. Pseudoregma carolinensis, where RIV+V is 0.09 mm and 0.89 times HTII). The abdominal segments appear unsclerotized (cf. Pseudoregma carolinensis, where areas around the siphuncular pores are distinctly sclerotized). The cauda is knobbed, and the anal plate bilobed (both are upturned in the image above). The body length of the adult aptera is 1.37 mm (cf. Pseudoregma carolinensis, where it is 1.20 mm). Please note that for each species these measurements are currently from the clarified mount of one specimen (see above).
First instar nymphs have the front femora stouter than other femora, and setae on the basal tarsal segments which are similar to those of the adults. They have 2 pairs of spines on the frons, which are shorter in later instars. Normal first-instars which develop to adult apterae have 4-segmented antennae, those destined to become soldiers in their second instar have 5-segmented antennae. Soldier morphs do not progress beyond their second instar, and are hence sterile. Unlike normal second-instars, these soldier forms have thickened forelegs, sclerotized tergites with longer setae, longer claws, protruded siphunculi, and pairs of spine-like setae on the frons. Second instar soldiers attack via their stylets (cf. first instar sterile soldiers on the secondary host, which use their horns).
The emigrant alatae (and nymphs) of Pseudoregma bambucicola were described by Takahashi (1936) (as Astegopteryx swinhoei) and shown by Aoki & Kurosu (1992) to be the gall-dwelling stage of Pseudoregma bambucicola. Winged viviparae from the primary host (emigrant alatae) have the head broadly rounded on the hind margin, with about 40 rather short dorsal hairs. The antennae are long, with 23-27 annular secondary rhinaria on segment III, 13-15 on segment IV and 8-11 on segment V. The rostrum reaches beyond the first coxae. The wing veins are stout, the first and second obliques on the front wing a little curved, united basally, the third oblique nearly as stout as the second. The legs are slender with many hairs; the hind tarsi have two very long hairs on the basal segment. The abdomen is thickened and dusky on tergites VII & VIII, and around the bases of hairs on tergite VI. The siphunculi are small, and surrounded by 3-5 hairs. The cauda is broadly rounded , not constricted basally, much wider than long, and with about 18 long bristles. The anal plate is divided (bilobed), the lobes as wide as the cauda. The alate body length is about 2.0 mm.
Viviparous emigrant alatae of Pseudoregma bambucicola migrate to the secondary host, bamboo, where they deposit nymphs. These first generation nymphs are all of the 'normal' type (not soldier forms). The head is completely fused with the prothorax. They have well-developed sharp frontal horns, bearing a number of minute hairs. Their antennae are 4-segmented, and the rostrum reaches the hind coxae. There are large granular sclerites on the thoracic and anterior abdominal tergites, and smaller sclerites on the posterior abdominal segments. Siphunculi are absent. The cauda and anal plate have one and two pairs of hairs respectively.
Subsequent secondary-host generations have 2 types of nymph, normal and soldiers (plus, rarely, an intermediate form).
Image above by permission, copyright Sunil Joshi & Poorani, J. Aphids of Karnataka (accessed 12/2/20).
The adult viviparous aptera of (putative) Pseudoregma bambucicola from Sri Lanka on bamboo is described by Doncaster (1966) (as Oregma bambusicola). In life they are grey-brown or dark purplish to greenish-brown or black, dusted with granular wax (see picture below of apterae of bambucicola / carolinensis group from India). Individuals in young colonies have three longitudinal rows (two marginal, one spinal) of white wax tufts, but in older colonies these are less developed and adults have a thick cushion of wax posterior to the siphunculi. The second picture below is a clarified mount of a confirmed Pseudoregma bambucicola adult aptera from bamboo.
First image above by permission, copyright Sunil Joshi & Poorani, J. Aphids of Karnataka (accessed 12/2/20). The vertex of the aptera is covered with small denticles and the frontal horns are quite small, conical and sharp. Their antennae are 4-segmented, but with segment III showing an incomplete division about 0.67 of the length from the base. The rostrum is short, not reaching the second coxae. The pronotum is fused with the head and has two low swellings on each side of the median line also bearing denticles. The mesonotum has a pair of larger, more heavily sclerotized but less prominent denticulate (=small toothlike) swellings. The metanotum is almost covered by irregularly broken sclerotic areas covered with denticles. The abdominal tergites are more or less evenly covered with denticles, and bearing numerous small dark scleroites each bearing 1 or 2 hairs. The siphunculi are circular, slightly elevated on narrow sclerotic cones. Tergite VIII has a median transverse sclerotic patch. The cauda has 20 hairs and the anal plate is bilobed. The body length of the adult aptera is 1.5-2.6 mm.
The alate Pseudoregma bambucicola / carolinensis (see picture below of alate of bambucicola / carolinensis group from India) is greenish black, and the pterostigma of the forewing on the side of the subcosta is bordered with black. All alatae of Pseudoregma bambucicola from the secondary host described to date appear to be sexuparae, with no secondary migrants (alate viviparae) having been recorded. Instead first instar nymphs of this species often wander about, and can be dispersed via the wind to found new colonies or join existing ones.
Image above by permission, copyright Sunil Joshi & Poorani, J. Aphids of Karnataka (accessed 12/2/20). Summary & distributionPseudoregma bambucicola may host alternate between Styrax suberifolius and bamboo, or it may persist anholocyclically on bamboos whether or not the primary host is present. Colonies are usually formed on the culms or twigs. Pseudoregma bambucicola sexuales are produced on the primary host where it is available, but over much of their range it is not. Sexuales are tiny, wingless, with a short rostrum and are produced by sexuparae originating from the secondary host. After mating, oviparae lay a single egg. Studies have indicated that Pseudoregma bambucicola is found in Japan (anholocyclic populations only), China (Guizhou Province, Zhou et al., 2020), Taiwan, Hong Kong and northern Vietnam. This contrasts with the more southerly distribution of Pseudoregma carolinensis, which is found in Thailand, Malay Peninsula, Java, Irian Jaya and Micronesia. The identity of those in India, Sri Lanka and Fiji is unconfirmed. Biology & Ecology:On primary hostOn the primary host in Taiwan, in May newly-hatched Pseudoregma bambucicola fundatrices transform axillary flower buds of newly-developed shoots into very young galls. By the second instar each fundatrix is usually enclosed by plant tissues. The early-stage gall surrounding the fundatrix develops subgalls (see below) which her first-generation nymphs (but not her) move into, mature and reproduce for a number of generations.
Image copyright Aoki & Kurosu (2010) under the Creative Commons Attribution License. The subgalls are then sealed off, and the main gall may open revealing the fundatrix. Any further first-generation nymphs cannot enter the sealed subgalls, and presumably do not survive to maturity, but may defend the gall. As subgalls develop further, they open at their distal end to permit egress of soldiers which eject honeydew balls and exuviae and repel some but not all uninvited guests. Some first instars leave their parent gall and move to others. At maturity each gall contains 280-1500 aphids, 23-41% of which are soldiers. It is not known to what extent Pseudoregma bambucicola galls on the primary host are ant attended. Pseudoregma carolinensis can be ant-attended on their primary host, but the relationship is more one of gleaning - cleaning ejected honeydew from around the gall - than of actively 'attending'; the ants are not attacked by their soldier aphids. Whilst Pseudoregma bambucicola galls may or may not be defended by gleaning ants, they are protected by soldier nymphs. These gall-dwelling second-instar soldiers clasp an insect predator and pierce it with their stylets, but non-soldier immatures will also do this. Being bitten by the soldiers causes moderate irritation if they pierce one's hands, and may deter vertebrate predators. Curiously enough, these soldiers allow conspecific soldiers (such as those of Astegopteryx bambusae) to join their colonies, but not other aphids. No parasitoid wasps been found in the galls, and syrphid larvae only rarely. Predacious beetle larvae (and sometimes adults) of genus Aethina have also been found in the subgalls. Oriental species of Assara pyralid moths, whilst one of the most commonest predators of cerataphidine galls, are as yet unreported from Pseudoregma bambucicola. Provided they can avoid any soldiers protecting the gall-outside, their larvae bore into the galls where they protect themselves from soldier attack under a mesh of silk threads - leaving only their chitinized heads exposed. In Taiwan, from July to September, emigrant alates (distinguishable by their horned embryos) appear in the galls then fly to their secondary hosts. Pseudoregma bambucicola have not been found to persist on their primary host beyond their fundatrix initiated gall-dwelling generations. Some galls remain occupied until May, but all their alatae have horned nymphs. On secondary hostColony establishment & growthSeasonal migrants arriving from the primary host (alatae bearing horned embryos, described by Noordam, 1991) deposit their nymphs on the lower side at the base of a bamboo leaf, where they form colonies. As these colonies mature they migrate to stem internodes. Our understanding of what follows comes from studies of anholocyclic populations in Kagoshima, extreme Southern Japan, about 1200 km northeast of Taiwan. Normal first instar nymphs on the secondary host are especially mobile. Sunose et al. (1991) found they walked about on the shoot of bamboo and often dispersed on the wind to new shoots or uninhabited culms, or joined other colonies. These nymphs appear to be the primary dispersive form. No secondary migrants (viviparous alatae that fly between bamboo hosts) have been observed, but Shibao (1997) obtained brachypterous functional viviparae from colonies on bamboo in late winter and spring. These 'wing-padded' adults produced apparently normal horned embryos and nymphs, but had a mixture of the features of alate sexupara and parthenogenetic aptera. Although unable to discount these were "phenotypic mosaics" his results suggest Pseudoregma bambucicola has the potential, albeit normally suppressed, of producing secondary migrants. As the stem-feeding colonies grow in size they produce daughter colonies on other stem internodes. In Japan, where their primary host is absent, and reproduction appears to be entirely parthenogenetic and clonal, colonies are presumably extremely closely related and nymphs are readily admitted to alien colonies. (Under these circumstances the term 'colony' is somewhat arbitrary, some authors term them borderless colonies and may define them on a plant-by-plant basis - or by the internode they inhabit, and call them clusters or subcolonies.) Shibao et al. (2009) found fewest Pseudoregma bambucicola in July. New shoots of Bambusa multiplex, their usual secondary host in Japan, appear from late July to September which is when most seasonal arrivals would be expected to establish colonies. Apterae arising from overwintering parthenogenetic colonies on bamboo colonize young growing shoots, or sometimes young branches in spring. As the shoot grows, and the colony sizes increase, each newly-established colony divides into subcolonies. Sunose et al. (1991) found the number of aphids per subcolony was lowest in June-July, but otherwise fairly constant. Presumably as a subcolony became crowded the rate of emigration increased. The overall population was lowest in June-July, but peaked in September / October. The establishment of new subcolonies was greatest from May to September, and least from October to March. The highest proportion of new subcolonies were founded when the populations were growing most rapidly, which occurred before they peaked - as the production of normal (reproductively-able) nymphs was reduced. Nearly 80% of clusters disappeared within two months of their foundation. Ant attendance & soldier productionPseudoregma bambucicola colonies on the secondary host are variably ant attended. Shibao et al. (2009) (assuming 1 colony per infested plant studied) found 42% of colonies were initially attended by the ants Crematogaster osakensis (first image below) or Lasius japonicus but after 1 month just 14.3% were continuously and closely attended. Such colonies are generally earth-tented by the ants and very different from unattended ones, albeit ants may opportunistically glean honeydew from unattended aphids. Ant attended colonies survived longer than unattended ones, lasting until around July, but contained far fewer aphids, and normally lacked soldier-nymphs. Like other closely attended species, these aphids produced few if any alates (in this case, sexuparae). Since they produced nymphs at the same rate as unattended colonies, but produced few if any soldier nymphs, it was concluded the ants were removing and eating some of the nymphs (see second image below).
Images by permission, copyright Shibao et al. (2009). Yet soldiers do not attack attending ants. Soldier production is evidently curtailed because attendant ants provide more effective protection against predators. When ant attendance became unusually low in winter, or when ants were experimentally removed from ant attendance, soldier nymphs were produced - and in the latter instance sexuparae resulted. All of which suggests the embryo type is under maternal control. Presumably ant attendance is costly, and attended colonies, being unable to produce many sexuparae, continue to produce normal nymphs and persist longer. Unattended colonies, including those abandoned by ants, often achieve a larger colony size and, since larger colonies tend to attract more predators, they tend to produce numerous soldiers. Shibao, 1998 showed the primary role of soldiers is defence against predators. In soldier-producing colonies, apterae gave birth to more soldiers than normal nymphs. The graph below illustrates how, in 30 colonies, the proportion of soldiers was related to colony size.
Whole-plant colonies collected Oct.-Nov., Dec & May. Data Shibao (1998). The findings of Shibao et al. (2009) suggested soldier production is increased by predator attack. In September-December the predators Eupeodes confrater (=Metasyrphus confrater, a syrphid) and Dipha aphidivora (a pyralid moth) became common, and any colonies with fewer than 5% of soldiers unable to react quickly enough were wiped out. Colonies with 5-22% of soldiers tended to be larger and, despite the predator prevalence, remained constant until crashing in May as Eupeodes confrater numbers peaked.
Image by permission, copyright Shibao et al. (2009). In Taiwan, from November to February, colonies of Pseudoregma bambucicola on bamboo produce alate sexuparae (each of which usually contains male and female embryos, both hornless) that fly to Styrax suberifolius. In Japan, Shibao et al. (2009) recorded alates in October-December. Sunose et al. (1991) found the populations and their predators peaked in September-October, and the highest proportion of nymphs with wing pads (developing sexuparae) in October-November. - Shortly thereafter, the number of predators, proportion of soldiers, and number of alate nymphs peaked more-or-less together. As the colony-density peaked the apterae switched to producing sexupara nymphs, which contributed no new nymphs to the colony. Reduced fecundity, predators, and possibly host-damage from the larger colonies, caused a rapid population decline. From late summer to autumn 86.4% of colonies were destroyed. Two years later Shibao et al. (2009) found the population size of colonies with more than 5% soldiers remained fairly constant after they had peaked in October-December, through to their sudden decline in April. The soldiers (being relatively long-lived) slowly declined from around 22% in November, to 2% in February, before rising to about 5% in March as Eupeodes confrater numbers began to rise, thence fell as the colonies collapsed. Natural enemies on bambooIn Southern Japan Shibao et al. (2009) found the most common predators were specialists of the soldier-producing Pseudoregma alexanderi, Pseudoregma bambucicola and Pseudoregma koshunensis. The most significant predator was the syrphid, Eupeodes confrater (see picture below). Their adults and larvae were almost always present, but were most common in June and in October. A single second instar larva was found able to rapidly demolish a colony.
Image by permission, copyright Shibao et al. (2009). Nevertheless the soldier defense was to some extent effective against Eupeodes. Like those of most generalist predators Eupeodes confrater egg shells are not very hard and the soldiers easily pierce and kill them, so this syrphid adjusts its oviposition behaviour accordingly. When soldiers are active in autumn and early winter, its eggs are laid on spider's webs or the tips of sheath blades. When there are few soldiers present in mid-winter to spring the eggs are laid close to the colony, or in it. A newly-hatched Eupeodes confrater larva can be lifted by a single soldier, and both may fall from the colony, but consuming one adult aphid makes it too heavy. Mature syrphid larvae survived any attacks - and their saliva was lethal to the aphids or attending ants. Also, when a soldier clasps the posterior part of the syrphid body, the soldier dies and is detached from it in a few minutes. This is presumably due to toxins secreted by the larva as this occurs without it being counterattacked by the syrphid with its mouth hook. Another specialist predator is Synonycha grandis, a large coccinellid (see pictures below). An adult female lays approx 60 eggs, on the culms or leaves, in the vicinity of aphid colonies but at enough distance to avoid attack. The cuticle of larvae and adults is too hard for the soldiers to penetrate, and they prey on aphids both in and around the colony. Adults and immatures can consume very large numbers of aphids (a single larva can eat more than 1000) and they frequently exterminate colonies. Larvae and adults occur from May to November, but their abundance is highly variable - and soldiers may clasp or push the legs of the larvae and force them to fall off the bamboo.
Images by permission, copyright Shibao et al. (2009). Dipha aphidivora, a pyralid moth, is also a specialist predator (see picture below). The adults, which are probably nocturnal, produce eggs too flat for the aphids to attack. Their larvae produce silk tunnels / mats soon after hatching, and live on the surface of the bamboo culm near to or within the aphid colonies. They occasionally poke out their head to catch an aphid, and move swiftly enough to avoid soldiers or ants. If they leave their shelter to capture an aphid, they rapidly return to consume it in safety. Whilst hiding under their silk they are largely ignored but, if removed, are strongly attacked - so are presumably toxin free. These larvae are abundant from September to December, when the aphids have numerous developing sexuparae. Their mats may cover most of the culm surface, leaving little space for the aphids.
Images by permission, copyright Shibao et al. (2009). We have found no record of cecidomyiids or aphelinids attacking Pseudoregma bambucicola. Generalist predators, whilst attracted to the colonies, are seldom observed and cause little damage - presumably owing to the soldiers harassing, killing, or ejecting them. Episyrphus balteatus, is a relatively small (9-12 mm) syrphid widespread throughout the Palaearctic. It often forms dense migratory swarms, and the larvae feed on many aphid species. Early-instar larvae of two moths, Taraka hamada (Lycaenidae) and Atkinsonia ignipicta (Stathmopodidae) avoid unwanted attention by hiding under silk mats - but in Japan their main prey is Ceratovacuna japonica. The brown lacewing, Micromus numerosus (Neuroptera) is a common generalist predator in Japan (see picture below), and their females can lay very large numbers of eggs (up to 1500). The larvae feed on the brown citrus aphid, Toxoptera citricidus, mainly in citrus groves. As they move quickly aphids cannot usually escape or, given their comparatively large mandibles, resist their attack. Pseudoregma bambucicola soldiers may be able to throw small larvae from a twig, but they are mostly ignored. Although ubiquitous, they are not numerous, and cause Pseudoregma bambucicola comparatively little damage.
Image by permission, copyright Shibao et al. (2009). Rodents sometimes eat Pseudoregma bambucicola on bamboo, and we assume birds and herbivores could seriously damage unprotected colonies. If viewed as a warning, this may explain their 'leg waving' behaviour (see image below): In Pseudoregma bambucicola colonies without attending ants, many soldiers, and to a lesser extent normal nymphs and adults, wave their legs when disturbed. Whilst their fore and mid legs remain in situ, the aphids lift their hind legs (and sometimes their abdomens) and move them up and down - and many honeydew droplets fall from the colony. This is presumably derived from honeydew-discarding kicks. Pseudoregma alexanderi (which also forms colonies on bamboo shoots or twigs), but only a few non-soldiers of Pseudoregma sundanica (on ginger) exhibit this behaviour - as do certain Aphidinae, (e.g. Aphis nerii) Lachninae (e.g. Lachnus roboris) and Eriosomatinae (e.g. Grylloprociphilus imbricator, the boogie-woogie aphid).
Image by permission, copyright Shibao et al. (2009). Other aphids on the same hostPrimary hostThe only recorded primary host of Pseudoregma bambucicola is Styrax suberifolius.
Secondary hosts
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