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Chaitophorus populicola

American poplar leaf aphid, Smoky-winged poplar aphid

On this page: Identification & Distribution Biology & Ecology Life cycle Ant attendance Natural enemies Other aphids on the same host Damage & Control

Identification & Distribution

Adult apterae of Chaitophorus populicola are yellow brown (see first picture below) to shiny black (see second picture below). Their antennal terminal process is normally longer than the base of antennal segment VI. The longest hair on antennal segment III is about twice as long as the basal diameter of that segment. The fused apical rostral segment (RIV+V) is 0.15 mm long with 2-6 accessory hairs. Abdominal tergites II-VII are wholly sclerotised and fused into a dorsal plate. There is no pale median line on the sclerotic pronotum nor on the abdominal segments, but the metanotum and abdominal tergite I-III may be partly or wholly pale. Abdominal tergites II-VII each have pleural as well as spinal and marginal hairs (cf. Chaitophorus nudus which has no pleural hairs on these tergites). There are no evident spinules or nodules on the dorsum (cf. Chaitophorus nodulosus, which has the abdominal tergum evenly spinulose or nodulose). Part or most of the dorsal hairs on the abdomen are tapered to points, blunt, or with chisel-shaped, often forked apices (cf. Chaitophorus populicola ssp. patchae which has all hairs fine and pointed). Their legs are dark brown to black. The siphunculi are small pale truncate cylinders. The cauda is rounded without any trace of a constriction. The body length of adult apterae is 2.0-2.5 mm. Immature Chaitophorus populicola are reddish brown or dark brown, with a distinctive pattern of dark and pale areas (see pictures of immatures with adults below).

Note: For more information on this species see Richards (1972). Also Blackman notes Chaitophorus populicola is more likely a 'species complex' than a single species.

First image above copyright Kenneth Frank under a Creative Commons License
Second & third images above by permission, copyright Claude Pilon, all rights reserved.

Chaitophorus populicola alatae (see pictures below) have dorsal abdominal cross bars or bands. Their forewings have dark veins with conspicuous brown-borders.

First image above by permission, copyright Claude Pilon, all rights reserved.
Second image above copyright Her Majesty the Queen in Right of Canada, Agriculture and Agri-Food Canada.

Chaitophorus populicola has been recorded from many different poplar (Populus) species. It feeds and forms colonies only in association with the apical meristem. Dense colonies may develop on young shoots, developing leaves, and leaf petioles (cf. Chaitophorus nudus, which is only found around the trunks of poplar saplings, and probably on the branches of more mature trees). Feeding by Chaitophorus populicola on young leaves induces part of the leaf to fold over, thus partially enclosing the colony. This species is nearly always attended by ants (see third picture above), which remove their honeydew and protect the aphids from predators. Chaitophorus populicola is distributed throughout most of North America, but has not so far been invasive outside America, neither in Europe nor Asia. This may be because, in the Palearctic zone, its niche (ant-attended feeding on the apical meristem of Populus) is taken by the poplar shoot aphid, Chaitophorus populeti, which is widely distributed and simarly common.

 

Biology & Ecology

Life cycle

The first picture below shows an apterous female Chaitophorus populicola on balsam poplar (Populus balsamifera) in spring (22nd May).

Image above by permission, copyright Claude Pilon, all rights reserved.

The early date, combined with the shorter body hairs and reduced sclerotization (see Stroyan, 1977) suggest that this is a fundatrix, or 'stem mother' as they are also known. The fundatrices hatch from the overwintering eggs in early spring, and they viviparously produce large numbers of similarly parthenogenetic offspring.

The immatures feed on the young shoots or along the main veins of the leaves, early in the year these develop to apterous viviparae.

Both images above by permission, copyright Claude Pilon, all rights reserved.

In late spring and summer some of the immatures develop to alatae (see picture below) most of which disperse to colonise new hosts.

Image above by permission, copyright Claude Pilon, all rights reserved.

Sexual forms - large pale oviparae (see picture below) and alate males - develop in autumn.

Image above by permission, copyright Claude Pilon, all rights reserved.

Ant attendance

The poplar leaf aphid Chaitophorus populicola has never been recorded without ant-attendents. The tending is done by many different species including Camponotus herculeanus, Camponotus novaeboracensis, Camponotus pennsylvanicus, Formica argentea, Formica dakotensis, Formica montana, Formica oreas, Formica propinqua, Linepithima humile, Myrmica incompleta and Tapinoma sessile (see Siddiqui et al., 2019 and photos shown here). These ants protect their aphids from natural enemies while collecting carbohydrate-rich honeydew. Carl Barrentine has a couple of videos showing the ant Formica oreas tending aphids and protecting the aphids from a potential predator at the Turtle River State Park, North Dakota, USA in June 2012.

Formica oreas tending Popular Leaf Aphids

Formica oreas defending Popular Leaf Aphids

Wimp & Whitham (2001) looked at how the ants, predators, and host plant quality act together to determine the distribution and abundance of the aphid, Chaitophorus populicola. This aphid was found only in association with ants. As a consequence, aphid abundance declined by 88% on host plants located more than 6 m from an ant mound. Differences in host plant quality resulted in aphid fecundity being greatest on narrowleaf cottonwoods and least on Fremont cottonwoods. Due to the combined effects of these factors, they found that the 'realized aphid habitat' was only 21% of their potential habitat. On trees where aphids and tending ants were present, aphids and ants greatly outnumbered any other arthropod species. On a per-tree basis, observational data showed that arthropod species richness was 51% greater and abundance was 67% greater on trees where aphid-ant mutualists were absent relative to trees where they were present. When aphids were experimentally removed and ants abandoned the tree, they found the same pattern. On a per-tree basis, arthropod species richness increased by 57%, and abundance increased by 80% where aphid-ant mutualists were removed, relative to control trees. The aphid-ant mutualism had a negative effect on herbivores, generalist predators, and other species of tending ants, and a positive effect on specialist enemies of aphids.

The picture below shows Chaitophorus populicola being attended by carpenter ants (Camponotus).

Image copyright David Cappaert under a Creative Commons Attribution-Noncommercial 3.0 License.

In southern California in riparian habitats Chaitophorus populicola is commonly tended by the invasive Argentine ant (Linepithema humile). Mondor & Addicott (2007) investigated the potential impact of invasive ants on the native ant mutualisms. To facilitate the ant-aphid interaction, ants have evolved aggressive responses to aphid alarm pheromone emissions. But as invasive and native mutualists have not evolved together, it was unclear if this form of cross-species communication exists between these two parties thereby facilitating these novel interactions. Mondor & Addicott assessed whether Linepithema humile responds to alarm signals of the native poplar aphid, Chaitophorus populicola. They showed that interspecific signalling does exist in this newly established mutualistic interaction. Argentine ant workers exhibit increased aggression and double the number of visits to an aphid colony after an aphid alarm signal is emitted. It seems that pre-adaptations may facilitate the emergence of mutualistic associations between many invasive and native species.

Image above copyright Ashley Bradford under a Creative Commons License.

In ant-aphid mutualisms, ants receive carbohydrates in the form of honeydew, while aphids receive protection from natural enemies. In the absence of natural enemies, however, the direct effects of tending are generally less well known. Yoo & Holway (2011) hypothesized that with increasing tending intensity (ant to aphid ratio), aphid performance would increase initially, then decrease at high tending levels due to the metabolic cost of producing high quality honeydew. They tested their hypothesis in a greenhouse experiment by manipulating Argentine ant (Linepithema humile) colony size while holding constant the initial size of aphid (Chaitophorus populicola) aggregations. The two parameters associated with survival, aphid survivorship to maturity and longevity, declined with increasing tending intensity, whereas per capita birth rate and time to first reproduction showed no relationship to attendance. The intrinsic rate of increase declined only at relatively high tending levels.

Note:
Whilst we fully accept their results, and agree with their predictions, we doubt their proposed mode of action. Since honeydew volume is limited by the aphids' food supply, if the authors were correct, the aphids would have to produce more of the metabolically-expensive ant-attractive melizitose. But why increase melizitose production if they already have more ants than they need - you could equally-well argue the converse? A simpler explanation would be an excessive ants unintentionally damage and harass their aphids, for example by their sharp tarsae when clambering over such soft-bodied insects.

Natural enemies

The orange mites on the aphids above and below are immature velvet mites. Adult velvet mites (= red velvet mites, true velvet mites, rain bugs, Trombididiidae) predate a variety of soil organisms - and their larvae are parasitic on various arthropods, including aphids. Three genera (Allothrombium, Podothrombium and Monothrombium), are aphid specialists.

Image copyright David Cappaert under a Creative Commons Attribution-Noncommercial 3.0 License.

Zhang (1998) reviewed the impact of mites upon their aphid hosts. The effect of larval trombidium mites on an individual aphid depends on the parasitic mite load and the age/size of the aphid. The larvae of Allothrombium pulvinum can kill an adult black bean aphid (Aphis fabae) in 3 days when the mite load is two or more. With one mite per aphid the reproductive rate of adult aphids is decreased and the development of nymphs is arrested. For larger hosts such as the pea aphid, Acyrthosiphon pisum, five Allothrombium pulvinum larvae per aphid kill about 50% of their adult hosts in 4 days.

Allothrombium larvae have been shown to be important early-season natural enemies of the cotton aphid (Aphis gossypii) in cotton fields. We give more information on aphid predation and parasitism by mites on this page: Mites parasitizing and predating aphids.

 

Other aphids on the same host

Chaitophorus populicola has been recorded on 9 species of Populus (Populus acuminata, Populus angustifolia, Populus balsamifera, Populus deltoides ssp. deltoides, Populus deltoides var. occidentalis, Populus euphratica, Populus fremontii, Populus nigra and Populus tremuloides.

 

Damage and control

Some species of poplar, such as Eastern cottonwood (Populus deltoides), are grown commercially in plantations for timber, veneer, pulp, fuelwood and fodder/animal feed - as well as being planted for shade and windbreaks. Chaitophorus populicola can be a serious pest on such trees. Solomon (1999) described a very heavy infestation of the aphid Chaitophorus populicola which developed primarily on growing shoots in commercial cottonwood plantations in lssaquena County, Mississippi and caused serious injury to terminal shoots. Terminal mortality in heavily infested fields averaged 92.5 percent, and shoot dieback averaged 4.3 inches. Many of the surviving terminals were weakened to the extent that slow growth allowed lateral bud growth to become dominant. After one growing season, trees in heavily infested fields generally had more stem deformities, in the form of heavy branches and forks, than did those in lightly infested fields. Four insecticides, acephate, carbaryl, chlorpyrifos, and diazinon, gave excellent control of the aphids.

Coleman & Jones (1988) assessed whether acute ozone stress on Populus deltoides affected the pest potential of the aphid Chaitophorus populicola. Cottonwoods were exposed to ozone (0.20 ppm) or charcoal-filtered air and infested with aphids. Aphid performance was not significantly different on plants exposed to ozone compared with charcoal-filtered air-treated control plants, so the data did not support the notion that aphid performance directly increased on air pollution-stressed plants. They also examined settling and feeding preference of aphids for cottonwood leaves of different developmental ages. Aphids significantly preferred leaf plastochron index 5 to all other leaf ages. (The plastochron index being the time interval between forming one leaf primordium, the group of cells that will form a new leaf, and initiating the next). Although ozone stress did not affect aphid populations directly, the authors noted that reproduction of some other pests (the cottonwood leaf rust fungus, Melampsora medusae, and the invasive willow leaf beetle, Plagiodera versicolora) is reduced on ozone-fumigated plants (reported elsewhere), so if aphid populations are affected by competition with these cottonwood pests, then aphid pest potential may increase in areas characterized by episodic ozone concentrations.

Acknowledgements

We are especially grateful to Claude Pilon for pictures of Chaitophorus populicola (for more of her excellent pictures see, and, and, and, and, and, and).

We have made provisional identifications from high resolution photos of living specimens, along with host plant identity. In the great majority of cases, identifications have been confirmed by microscopic examination of preserved specimens. We have used the keys and species accounts of Blackman & Eastop (1994) and Blackman & Eastop (2006) supplemented with Blackman (1974), Stroyan (1977), Stroyan (1984), Blackman & Eastop (1984), Heie (1980-1995), Dixon & Thieme (2007) and Blackman (2010). We fully acknowledge these authors as the source for the (summarized) taxonomic information we have presented. Any errors in identification or information are ours alone, and we would be very grateful for any corrections. For assistance on the terms used for aphid morphology we suggest the figure provided by Blackman & Eastop (2006).

Useful weblinks

References

  • Coleman, J.S. & Jones, C.G. (1988). Acute ozone stress on Eastern Cottonwood (Populus deltoides Bartr.) and the pest potential of the aphid, Chaitophorus populicola Thomas (Homoptera: Aphididae). Environmental Entomology 17(2), 207-212. Full text

  • Mondor, E.B. & Addicott, J.F. (2007). Do exaptations facilitate mutualistic associations between invasive and native species? Biological Invasions 9, 623-628. Full text

  • Richards, W.R. (1972). The Chaitophorinae of Canada (Homoptera: Aphididae). The Memoirs of the Entomological Society of Canada 104 Supplement S87, 1-109. Abstract

  • Siddiqui, J.A. et al. (2019). Meta-analysis of the global diversity and spatial patterns of aphid-ant mutualistic relationships. Applied Ecology and Environmental Research 17(3), 5471-5524. Full text

  • Solomon, J.D. (1999). Early impact and control of aphid (Chaitophorus populicola Thomas) infestations on young cottonwood plantations in the Mississippi Delta. USDA Southern Forest Research Note SO-326, August 1999 Full text

  • Stroyan, H.L.G. (1977). Homoptera: Aphidoidea (Part) - Chaitophoridae and Callaphidae. Handbooks for the identification of British insects. 2 (4a) Royal Entomological Society of London. Full text

  • Wimp, G.A. & Whitham, T.G. (2001). Ecology 82(2), 440-452. Full text

  • Yoo, H.J. S. & Holway, D.A. (2011). Context-dependence in an ant-aphid mutualism: direct effects of tending intensity on aphid performance. Ecological Entomology, 36(4). Full text

  • Zhang, Z. (1991). Parasitism of Acyrthosiphon pisum by Allothrombium pulvinum (Acariformes: Trombidiidae): Host attachment site, host size selection, superparasitism and effect on host. Experimental & Applied Acarology 11, 137-147. Abstract