Aphid Nymphs, Instars, Moults & Metamorphosis:

The first image below shows a young nymph of Symydobius oblongus (Shiny birch aphid) mid-way through her moult. The second image shows a similar nymph completing her moult.

Since insects generally undergo a number of moults prior to adulthood it must be important to them. Nontheless, moulting (=ecdysis) has downsides.

Moulting is an expensive, risky and exhausting business for insects. Casting-off their skins (as exuviae) costs precious materials and energy, it immobilizes the insect, can result in serious injury, and renders insects soft & vulnerable immediately thereafter.

• For instance the first image below shows a newly-moulted 'teneral' adult Clethrobius comes (brown hairy birch aphid) shortly after it's final moult, climbing over its slightly younger (pre-moult) fellows. The second shows an adult after it's cuticle has sclerotized (hardened off, and darkened).

The colour variation among these (wingless) nymphs and (winged) adult Drepanosiphum platanoidis (common sycamore aphids) are because many moulted recently.

Air-breathing insects face a further difficulty. During moulting, respiration is seriously limited because their trachae are blocked whilst the linings are pulled out (Camp, et al., 2014).

• Below is a ventral view of the exuvia from a mature nymph of Macrosiphoniella millefolii (yarrow aphid) which has moulted to become an adult sexual female. The white 'threads' around the head-end (top-right) are trachael linings.

So why moult?

There are several reasons why insects, like other arthropods, moult.

1. Moulting enables them to recover from minor cuticular damage such as lost sensory hairs, bristles & scales - and to shed adhering matter, including some hitch-hikers.

2. Moulting enables insects to grow - unavoidably so, since their cuticule provides skeletal support. Immature insects moult a genetically-predefined number of times prior to adulthood - few species moult thereafter. All insects have to moult in order to grow even if there is is no metamorphosis.
   • For example silverfish (Lepisma saccharina, Thysanura) are 'primitive' and wingless insects. They are ametabolous: they do not undergo metamorphosis. The newly-hatched (first-instar) nymphs look very like small adults. After six or seven moults these nymphs become adults, which can reproduce, but continue to moult throughout their life.

3. Moulting enables insects to change form (=metamorphose).

Furthermore, since aphid exuviae smell like aphids, Muratori et. al (2008) found they can act as decoys for parasitoids.

So what is meant by complete and incomplete metamorphosis?

• Butterflies & moths (=Lepidoptera), for example, are holometabolous: They undergo complete metamorphosis, and have 4 distinct life stages: eggs, larvae, pupae & adults - all of which are markedly different. Their larvae undergo a series of moults as they grow, but show little change in form until they moult to become pupae, and moult again to become adults.

• Odonata (e.g. Dragonflies), an 'ancient' insect group, are paurometabolous: They undergo incomplete metamorphosis, and have 3 distinct life stages: eggs, nymphs & adults. They have no pupal stage, but their larvae and adults may be very different. Their larvae are aquatic, the adults agile fliers.

Mayflies (=Ephemoptera), another 'ancient' insect group, do not pupate. Shown below, an adult mayfly completes its final nymphal moult, leaving behind the exuvia. Adult mayflies do not feed, they disperse, mate, and reproduce.

• Aphids (and other Hemiptera) are hemimetabolous. They undergo incomplete metamorphosis, with 3 distinct life stages. Their nymphs and adults are of comparatively similar form.

Below are the eggs, young nymphs, and an adult Cinara pinea (large pine aphid).

• A few aphids, such as Myzus ascalonicus (shallot aphid) and Tuberolachnus salignus (giant willow aphid), have never been known to lay eggs - so their incomplete-life cycle has just 2 distict life stages (nymphs & adults).

Having different body forms enables juveniles and adults to specialize in different tasks, to occupy different niches - and to avoid different predators.

Nymphs often have a quite different defensive strategy to the parents. The adults of Cinara confinis have strong dark green aposematic (warning) coloration to discourage predators. Their nymphs tend to cluster together and rely upon their cryptic coloration for concealment.

Pterocomma pilosum, (hairy bark aphid) nymphs are wonderfully cryptic, but their wingless adults are strongly striped and very conspicuous - perhaps because it takes time for the aphid to sequester enough chemicals from their host-plant to deter would-be predators.

Metamorphosis is, of course, an ancient trait among arthropods.

• Crab larvae, for instance, live planktonically and are dispersive - a very different lifestile to their reproductive, relatively immobile, heavily-armoured adults.

• Insects tend to do the opposite. Mayfly (=Ephemoptera) adults disperse, mate and reproduce but, unlike their young, do not feed or grow.

  Many aphids species go a step further because, via different (body-forms), they can produce adults best fitted to reproduction, or dispersal, or mating, or waiting, or some combination thereof. (To distinguish these body-forms from developmental stages, they are known as morphs.)

Holometabolous insects arose from hemimetabolous insects monophyletically, around 285 million years ago, by retaining (or repeating) embryonic features in the juvenile stages (Erezyilmaz, 2006). Holometabolous larvae are often grouped according to how they resemble embryonic segmental development stages (Richards, 2013), but holometabolous larvae are not merely prematurely hatched embryos. Holometabolous & hemimetabolous insect embryos both undergo three moults (known as cuticular depositions) - and holometabolous larval forms have evolved to serve their current lifestyles.

• Since insect embryos moult, in nearly all species they become "first instars" following their third embryonic moult. In aphid eggs this moult occurs prior to hatching. In viviparae, aphid embryos moult about 24 hours prior to birth.

For insects that undergo incomplete metamorphosis, young nymphs, mature nymphs and adults can still look quite different.

The images below show a group of first-instar nymphs, a second instar with its cast-off cuticle, a third, and fourth instar, and a wingless, parthenogenetic adult Macrosiphum euphorbiae (Potato aphid) - with her first-instar nymphs.

• First-instar aphid nymphs differ in a number of ways from their adult forms. For example their antennae are short, and usually have fewer segments than adults (4 or 5, rather than 5 or 6). Nymphs have no cauda, and their rostrum is comparatively long.

• Later instars resemble their adult forms progressively more closely - which makes life hard if you need wingless adults to key the species out.

Below are fourth-instar nymphs of Lachnus roboris (variegated oak aphid), attended by ants, and a winged vivaparous adult. In this species vivaparous adults may be winged or wingless. Wingless morphs are produced by supressing wing development (Braendle, et al. 2006), but only nymphs destined to become winged adults have visible wing-buds. The fourth-instar nymph wing buds only become wings after moulting to adult.

Immature oviparae may be noticeably spindle-shaped, whereas fourth-instar nymphs destined to become alates have wing buds and longer antennae.

The first image below shows developing and adult oviparae of Rhopalosiphum padi (bird cherry aphid). The red aphids in the second image are immature males of Macrosiphoniella millefolii (yarrow aphid) - in this species only the males are red.

Acknowledgements We are grateful to The Amateur Entomologists' Society for permission to reproduce abstracts from their website's glossary. 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 Braendle, C., Davis G.K., Brisson,J.A. & Stern, D.L. (2006). Wing dimorphism in aphids. Heredity 97, 192-199 Full text Camp, A.A., Funk, D.H. & Buchwalter, D.B. (2014). A stressful shortness of breath: molting disrupts breathing in the mayfly Cloeon dipterum. Freshwater Science 33 (3), 695-699. Abstract Erezyilmaz, D.F. (2006). Imperfect eggs and oviform nymphs: a history of ideas about the origins of insect metamorphosis. Integr Comp Biol. 46(6) 795-807. Full text Muratori, F.B., Damiens, D., Hance, T. & Boivin, G. (2008). Bad housekeeping: why do aphids leave their exuviae inside the colony? BMC Evolutionary Biology 8:338. Full text Richards, O.W. (2013). Development and metamorphosis. In: Imms' outlines of entomology. Imms, A.D., Springer. 254 pp.