It has been said that if aphids had their own way and unlimited resources the world as we know it would be 149 km deep in the cute little beasts (Harrington, 1994 ). Last year I wrote about how predators that feed on aphids, although useful, don’t really cut the mustard when it comes to keeping them in check and suggested that their host plants played a major role in keeping aphids from taking over the World. While they do play an important part in keeping aphid populations under control, and are aided and abetted by aphid specific predators, there are, however, some much more efficient aphid-specific natural enemies out there. They may be less conspicuous than the brightly coloured ladybirds that we often see munching their way through aphid colonies; public perception of their name may make people wince, but these beautiful and graceful creatures make sure that our appetite for salads and exotic vegetables out of season is satisfied safely and efficiently. Their life cycles rival that of their prey, or should that be hosts, and entomologists fondly imagine that the film Alien was inspired by them 😊
I am, of course, talking about parasitic wasps, or parasitoids as they are more commonly known. They are called parasitoids because unlike true parasites which generally speaking keep their hosts alive, insect victims of these wasps will, if successfully parasitized, die well before their non-parasitized relatives. In case you were wondering, the term parasitoid was coined by the Finnish Hemipterist, Odo Reuter (1913). Aphids are not the only insects that are attacked by parasitoid wasps. The action of insect parasites has been known about for over two hundred years. Erasmus Darwin, grandfather of the more famous Charles, noted that Ichneumonid wasps parasitised cabbage white butterfly caterpillars and so should be encouraged by gardeners (Darwin, 1800). This is not the only early mention of parasitic insects in this context; Wheeler (1928), points out that back in the 1850s, two Italian entomologists, Camillo Rondani and Vittore Ghiliana also suggested the use of parasitic insects as biological control agents. Aphid pests of glasshouse crops originally controlled mainly by predators (van Lenteren & Woets, 1988) are now routinely controlled by the application of commercially produced Braconid and Chalcid wasps (Boivin et al., 2012; van Lenteren, 2012).
Three commonly used aphid parasitoid biological control agents in action. Images from http://biologicalservices.com.au/products/aphelinus-2.html and https://www6.inra.fr/encyclopedie-pucerons/Especes/Parasitoides/Braconidae-Aphidiinae/Praon-volucre
When people think of Hymenoptera, they tend to think of bees, Vespid wasps and ants as being the most important and abundant. They are very much mistaken. The Parastica, or parasitoid wasps, are, by a huge margin, the most speciose and abundant section of
Parasitoids clearly dominate the Hymenopteran fauna of the British Isles (Many thanks to Natalie Dale-Skey of the NHM for permission to use this).
the Hymenoptera both in the UK and elsewhere
In the tropics the parasitoids are even more dominant. Data from Gaston et al., (1996).
Once parasitized, the egg(s), unless they are encapsulated by the aphid ‘immune’ system, hatch and begin to feed on the internal tissues of their, presumably, unsuspecting aphid host. The parasitoid larvae avoid feeding on vital parts of the aphid, so that it can continue to grow and develop and provide food for the parasitoid, until the parasitoid is ready to pupate. Once the parasitoid is ready to pupate it delivers the coup de grace putting the aphid out of its misery and allowing the formation of the ‘mummy’ in
The three most common types of aphid mummies. Images from http://resources.rothamsted.ac.uk/science-stories/aphids-mummies-and-cadavers, http://biologicalservices.com.au/products/aphelinus-2.html and https://farm1.static.flickr.com/327/18532751584_becc0e56e9_b.jpg respectively.
which the parasitoid completes its development before sawing its way out to emerge as a winged adult ready to seek out new hosts, leaving a characteristic neat circular hole in mummy case. In case you were wondering why the mummy of Praon volucre looks like it is sitting on a plate, this because, unlike the other aphid parasitoids, the final instar cuts its way out of the bottom of the aphid and spins its cocoon externally underneath the remnants of the aphid, hence the ‘plate’ (Beirne, 1942).
And out she comes; emerging parasitoid – http://resources.rothamsted.ac.uk/science-stories/aphids-mummies-and-cadavers
Lysiphelbus testaceipes Photo by J.K.Clark, University of California Statewide IPM Project
Once an aphid, now a hollow mummy; note the neat emergence holes. Aphid parasitoids are very much tidier than the parasitic lifeform in the classic film Alien 🙂
Another aspect of their life style that makes parasitoids a breed apart from true parasites, is that as well as using aphids as egg laying sites for their larvae, the adults like to snack on them every now and then to help mature more eggs and to keep up their energy levels; sometimes quaintly described as predatism (Flanders, 1953). Although the parasitoids can make feeding attacks at any time, they appear to feed first and then start laying their eggs (e.g. Collins et al., 1981).
Parasitoids are widely used as biological control agents in glasshouses and other protected environments as they are generally regarded as being more effective than predators (Debach & Rosen, 1991), although there is some support that generalist predators can play a significant part in biological control in the wider environment (Symondson et al., 2002; Gontijo et al., 2015). That said, aphid parasitoids seem to be fairly host specific in that commercial companies offer specific parasitoid mixtures to control different aphid pest species e.g. https://www.koppert.com/pests/aphids/product-against/aphipar/ [Note this is NOT an endorsement]. In fact it has been suggested that the relationship between aphids and their parasitoids can be used to clarify aphid taxonomic relationships (Mackauer, 1965). On the other hand, there are very few examples of monophagous aphid parasitoids, most being described as oligophagous (Stary & Rejmanek, 1981). So given that there is a fair bit of evidence that the parasitoids attacking aphids do show some discrimination in their choice of hosts, how do they find them?
Parasitoids in general were originally thought to be “possessed of an unerring instinct that guided them in their search for hosts” but Cushman (1926) rebutted this idea pointing out that actually the parasitoids first home in on the habitat or food plant that their host lives in and then search for their host (Laing, 1937). The parasitoids referred to by Cushman and Laing, are however, not parasitoids of aphids, attacking lepidopteran leaf miners and carrion feeding flies respectively, so you might perhaps think that aphid parasitoids could have a different strategy. Although habitat selection by parasitoids of lepidopteran larvae (Thorpe & Caudle, 1938) and sawfly larvae (Monteith, 1955), using olfactory cues of their host’s food plant was confirmed readily easily and early on, the situation with aphids was less clear cut. Manfred Mackauer for example, suggested that aphid parasitoids might be using visual cues, such as leaf deformities or damage to find their aphids hosts (Mackauer, 1965). The breakthrough came when three cabbage loving entomologists from the USA used an olfactometer to first show that the Braconid parasitoid Diaeretiella rapae, responded positively to the odour of collards (what we in the UK call spring greens) and second to show a very strong preference for them to lay their eggs in the aphid Myzus persicae when it was feeding on crucifers rather than other host plants. They attributed this to the presence of mustard oil, the chemical that gives cabbages their distinctive taste and suggested that once the aphid host plant was found then the parasitoids used visual cues to find their aphid victims (Read et al., 1970). Six years later it was firmly established that parasitoids in general used olfactory cues both to locate the habitat of their host (long-range) and then a short-range to find and confirm the identity (contact chemicals) their insect hosts (Vinson, 1976).
It was thought that the aphid parasitoids were chemically ‘conditioned’ during their larval life within the aphid feeding on a host plant and that this influenced their adult host preferences (e.g. Sheehan & Shelton, 1989; Wickremasinghe & Van Emden, 1992). These, and other similar results, seemed to support the Hopkins host selection principle (Hopkins, 1917) which states that adult preferences are learnt as larvae. A very neat experiment by van Emden et al., (1996) proved this hypothesis wrong. They transferred aphid mummies from the plant on which they had been parasitized on to another host plant and this changed the preference of the emerging adult, seeming to suggest that this was how aphid parasitoids developed their host preferences. Now comes the neat, and very tricky part; if however, the parasitoid pupae were removed (very carefully) from the mummy case and reared to adulthood in the absence of a host plant or mummy and kept in a glass tube, the emerging adults showed no preference for particular host plants, clearly showing that adult preferences were not determined during larval development but ‘conditioned’ by exposure to the external skin of the aphid mummy on emergence (van Emden et al., 1996). Using aphids reared on an artificial diet (Douloumpaka & van Emden, 2003) showed that the it was very likely that the mother parasitoid leaves a chemical cue in or around the egg(s) she lays and that this is later incorporated into the silk of the parasitoid pupa, thus inducing the host preference seen as an adult.
An additional twist to the story is that male and female parasitoids differ in their responses to odours. Both sexes of Aphidius uzbekistanicus and A. ervi, parasitoids of cereal aphids in the UK, respond to plant odours, but only females respond to aphids (Powell & Zhi-Li, 1983). Males of both species are, however, attracted to the odours of their respective females, suggesting the existence of a sex pheromone. The existence of a sex pheromone in aphid parasitoids had been suggested a few years earlier when it was shown that male D. rapae attempted to copulate with filter paper that had had female abdomens crushed on them (Askari & Alisha, 1979). The existence of sex pheromones in aphid parasitoids has now been shown in several species (e.g. Decker et al., 1993; McNeil & Broduer, 1995). Strangely, female parasitoids also respond to sex pheromones, but in their case, the sex pheromones of aphids. It turns out that they ‘parasitise’ aphids in more than one way, they home in on their prey using the aphid sex pheromone and this enables them to find a suitable overwintering host (Hardie et al., 1991). At other times of the year they also use other aphid indicators; several studies have shown that parasitoids use the presence of aphid honeydew to help them find their hosts (Budenberg, 1990; Bouchard & Cloutier, 1984; Gardner & Dixon, 1985).
Predators of aphids such as ladybirds use chemical markers to warn other ladybirds that they have laid eggs near aphid colonies, thus reducing the chances of cannibalism and competition (e.g. Oliver et al., 2006). Given that the eggs of aphid parasitoids are laid internally, they are in effect invisible, it would make sense if the parasitoids ‘marked’ their hosts in some way to avoid other parasitoids laying their eggs in an already parasitized aphid, superparasitism. Sure enough, there is some evidence that some adult parasitoids can recognise aphids that already have larval parasitoids developing inside them although they don’t seem to be able to consistently recognise already parasitized aphids until some hours afterward (e.g. Cloutier et al., 1984). In some cases, it seems that it is the aphid herself that prevents superparasitism by reacting more aggressively towards parasitoids after being attacked once (Gardner & Dixon, 1984) and also by the presence of dried siphuncular secretions on the aphid’s skin (Outreman et al., 2001). The waxy secretion had an effect for up to a day or so after which the internal changes caused by the developing parasitoid larvae were enough to deter further oviposition attempts.
It is a good thing for the poor aphids that they have such a high reproductive rate, or they would truly be in dire straits. On the other hand, as exemplified by the words of Jonathan Swift (1733),
“So naturalists observe, a flea
Has smaller fleas that on him prey;
And these have smaller still to bite ’em,
And so proceed ad infinitum”
there are parasites of parasitoids, the hyperparasites, that help keep the numbers of parasitoids under control, and thus, indirectly, help aphids remain relatively abundant.
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*This is how he spelt it; not a mistake on my part J