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Issues in Aphid Biology
- May 2022

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It is probably not what you imagine

Currently, if you Google 'honeydew', you will mainly get reviews of the American horror movie 'Honeydew', (we will make no further comment on this 'epic'). Those reviews are interspersed with pictures of 'honeydew melons', a smooth-skinned musky-smelling sweet-fleshed fruit of one cultivar of muskmelon (Cucumis melo) (called honeydew melons as more appealing to American buyers than their original name of 'white Antibes winter melon'). If you're lucky, there may also be a page on honeydew as a sugar-rich sticky liquid 'secreted' by aphids and scale insects. In biology honeydew usually (but not always) refers to the liquid faeces of insects (especially aphids) that specialize in feeding on phloem-sap (and, no, honeydew is not milk).

First image: a yellow honeydew melon cut to show its seeds and sweet flesh (parenchyma). ©Tobias, GNU 1.2.
Second image: a wax-covered larch adelgid, Adelges laricis, producing honeydew.; ©InfluentialPoints.

Although we now know its composition and sources (most honeydew is produced by certain species of insects and fungi), the word's use remains somewhat inconsistent. For example, sweet-tasting plant saps (even those which only taste sweet post-evaporation) are sometimes described as honeydew, but dry honeydew is seldom called such. The excrement of xylem-feeding insects (such as the cuckoo-spit of spittlebug cercopids) is occasionally described as honeydew. Even among scientists, some things are described as nectar or honeydew. When referring to the spore-laden sweet liquid produced by ergot-infected grass flowers, the distinction is understandably blurred. While honeydew, nectar, honey and most saps can be regarded as sugar solutions (as is syrup), there are important differences...

The meaning of honeydew, nectar, and mildew

Honeydew is one of those outwardly simple terms that entrap the uninitiated - partly because its original, purely-descriptive, meaning has changed and diversified. Whilst honeydew and mildew have distinct meanings now, they originally referred to the same thing: a wet sweet often sticky substance found on or under vegetation. (Mould or mold, as in mouldy, may have arisen similarly: from proto-Germanic indicating wetness, slipperiness - from proto-Indo-European indicating mucus, slimy, sneezing and sneeze-causing.)

The term honeydew (or honey-dew) dates from the mid-1500's, but mildew dates from the mid-1200's (mildeu was from the Old English 'meledeaw', where 'mele' meant honey, and 'deaw' meant dew). As plant growers know all too well, honeydew readily becomes mouldy. The resulting sooty moulds (Ascomycete fungi, commonly Cladosporium and Alternaria), grow on fences and stones and taint (from tint, =stain) plants and fruit (which does them no good). By the mid-1300's mildew also referred to any kind of mould or taint, especially if it was sticky - including those which were not honeydew-fed (those plant-dwelling mildews are either species of Erysiphales fungus, or fungus-like Peronosporaceae).

We now know that most honeydew is the excrement of certain sap-feeding insects, but for many years its origin was unknown - and this was variously assumed to be honey, nectar, or plant sap. That certain bee species produced honey was self-evident, but whether it was simply nectar, and whether nectar was sweet plant sap, was unknown. Aristotle may have distinguished honey and nectar in the 4th century BC, but in the 1200-1500's the terms were often conflated - not least since observational and experimental biology were considered near-blasphemous.

Image above: Winged adult maple aphid (Drepanosiphum aceris,) excreting honeydew.; ©InfluentialPoints.

Incidentally, the English word nectar came in to use during the 1550's, from nek (=death) + tar (=overcoming) meaning 'the drink of the gods'; its modern meaning regarding something pleasant or sweet arose 50 years later.

Linnaeus described floral and extrafloral nectaries in the mid-1700's, but suggested nectar was a waste product. The function of nectar and nectaries only became clear in the late-1800's. A full understanding of how and why those substances differ being recent, in the interim the terms tended to get conflated (even in current scientific literature - whether nectar was merely exuded phloem was only recently resolved). Eventually it became clear that insects feeding on phloem sap produced sweet honeydew (as detected by the human tongue), whereas xylem sap feeders produced tasteless liquids - which were not seen as honeydew. Sweet exudates from insects (other than bees) and certain phloem-feeding fungi (such as Claviceps) were described as either honeydew or nectar - or neither. Then again, where honeydew was only observed dry it was accorded different names - such as manna, or lerps:

  • Excrement of the Tamarisk manna scale (Trabutina mannipara) feeding on Tamarisk trees (particularly Tamarix gallica) has been suggested as the most likely source of biblical manna - and was once marketed as such. Another manna, known as "kudret helvasi", is honeydew from various species of aphids feeding on turkey oak (Quercus cerris) which has dried in the sun - and traditionally used in Turkey to make cakes. Manna also refers to dried sugary fluid exudate from damaged plants, especially following insect attack.

  • Lerps are structures of crystallized honeydew produced by immature psyllids as a protective cover (e.g. red lerps, Austrochardia acaciae, on mulga trees, Acacia aneura). Many Australian psyllid species produce lerps of various physical forms, and the species tend to be highly host-specific. Lerps produced by Australian psyllids are mainly sugars - except for those produced by Eucalyptolyma maidenii which are glucose polymers, and those of Cardiaspina densitexta which are starch.

Why honeydew is important

Moderately dilute honeydew is excellent food for moulds, notably sooty mould - which can damage both plants and vehicles. Sooty mould make plants unsightly, unpalatable, and reduce growth by blocking photosynthesis (they can also stain paintwork). Like many other sugars, dry honeydew does not easily dissolve in cool water so is hard to remove from cars. Warm water combined with prolonged non-abrasive rubbing works, but detergents do not (they are intended for greasy non-polar hydrophobic compounds, and proteins, not sugars).

Sweet honeydew is much liked by animals including birds, flies, mosquitoes, ants and wasps. It is occasionally eaten by both humans and honeybees, but for some animals it is an important part of their diet. As a result a few ant and aphid species have evolved very close mutually-beneficial relationships. Whilst this reduces the aphids' honeydew problems, including sooty mould, it does cause others. To ensure ants attend rather than consume them, these aphids must produce ant-attractive honeydew and ingest extra phloem-sap. This can reduce the aphids' nutrient-intake whilst increasing damage to, and nutrient loss by, their host plants.

Image above: Paton (1980) described the importance of manna, honeydew and lerps in the diets of birds such as the New Holland honeyeater (Phylidonyris novaehollandiae). The yellow forehead is flower pollen. ©JJ Harrison, CC-BY-SA-2.5.

Ant-attractive honeydew contains large proportions of an unusual sugar, melizitose - which, whilst highly attractive to a few ant species, is indigestible to honeybees. Bees tend to partake of honeydew towards the end-of flowering season when alternative food sources get scarce. If honeydew-honey is left in the hive overwinter, being their food reserve, it can cause colony die-off (melezitose has a laxative effect upon bees and is poorly digested by them). Melizitose honey tends to crystallize in the honeycomb, especially in dry conditions, which complicates beekeepers' honey-extraction procedures. Thus, although honeydew-rich melizitose honeys are highly-prized by some people and correspondingly pricey, their production entails careful hive maintenance.

It has been suggested that honeydew may assist root mycorrhizae (these are often crucial for many plant's nutrient and water intake). Soil sugar availability is an important growth-limiter in these symbiotic arboreal-root fungi. To date, studies aimed at confirming honeydew-improved growth are conflicting. Honeydew aside, rainfall leaches substantial quantities of soluble nutrients from plants, again this sugar solution is too dilute to be detectable by human taste buds.

What makes honeydew

Aside from plant saps, which generally only ooze following an injury and are comparatively uncommon, honeydew-like secretions are produced by relatively few fungal and insect species.

Fungi

A few fungi, such as ergot (Claviceps purpurea, Claviceps africana on grasses), produce small droplets of sweetish spore-rich liquid that attract insects (including honeybees) and so propagate the fungi. Fungi in the genus Claviceps cause disease symptoms (ergot) on plants and infect the flowers of various plants, inducing them to produce honeydew (Mower & Hancock, 1975). Ergot honeydew is a viscous fluid matrix containing high concentrations of sugars and massive amounts of sexual spores. The sugary matrix of ergot nectar / honeydew is a nutritional resource for many insects, which spread the spores. Sugar analysis of honeydews from infected hosts indicates that synthesis of the major sugars is controlled by the parasite, and that sugar composition is distinct for each fungus.

First image: honeydew drops from early stage ergot (Claviceps purpurea) on ryegrass (Lolium) flower. ©, Howard F. Schwartz, Colorado State University, Bugwood.org, CC-by-4.0. Second image: fruiting body on leaves of common barberry (Berberis vulgaris) of stem rust (Puccinia graminis), a pest species and close relative of Puccinia arrhenatheri. Both species alternate between Berberis spp. and cereals/grasses. ©Krzysztof Ziarnek CC-by-4.0.

Naef et. al (2002) found Puccinia arrhenatheri (a rust fungus which cause witches' brooms on Berberis vulgaris) produces a similar liquid for very much the same purpose. The witches' brooms bear yellow discolored leaves on which the fungus exposes its gametes in a sugary nectar. During the spermatial stage of the fungus the infected leaves emit a strong, flowery scent. Together these attract insects by floral mimicry.

Cypress spurge (Euphorbia cyparissias) is commonly infected by rust fungi of the species complex Uromyces pisi. When infected, the spurge is unable to flower, but instead is induced by the fungus to form pseudoflowers, which are rosettes of yellow leaves upon which the fungus presents its gametes in a sweet-smelling sugary fungal nectar. Funder & Roy (2000) showed insects thus-attracted aid the reproduction of these fungi.

Image above: Euphorbia cyparissias, normal flowers left, Uromyces pisi-sativi infected plant right. ©Stefan Lefnaer (CC-SA-4.0).

Hemiptera

Many organisms consume phloem sap as part of a mixed diet, but only one group obtain most of their food thus. Copious amounts of sweet-tasting honeydew are only produced by one group of insects, various phloem-feeding species among the Hemiptera. These insects neither store their honeydew nor feed it to their young (unlike honeybees). They excrete honeydew because their liquid diet is extremely rich in sugar, but has a low concentration of the nitrogen compounds they need to make protein. Symbiotic gut-organisms enable such insects to make best use of whatever nitrogen they ingest, so their honeydew contains little else but sugar and water. That said, the honeydew of some species are avidly collected by ants, and only becomes excessive when the phloem feeders attain large dense colonies. Small solitary phloem feeders seldom produce sufficient honeydew to be noticeable. The most common phloem-feeders are aphids (specifically the Aphididae & Adelgidae) and coccids (scale insects, Coccoidea).

Images above: Ant collecting honeydew from cottony camellia scale (Pulvinaria floccifera) on Holly (Ilex aquifolium); ©InfluentialPoints.

Phloem-feeding has evolved multiple times among the Hemiptera, but phloem honeydew is mainly produced by species within two of its four orders: the Sternorrhyncha and Auchenorrhyncha. For some examples of the latter see Piotr Naskrecki's pages on flying honeydew.

  • Most Sternorrhyncha are specialized phloem feeders, including the aphids (Aphidoidea), white flies (Aleyrodoidea), scale insects & mealy bugs (Coccoidea), and jumping plant lice (Psylloidea). These phloem-feeders mainly feed when their stylet tips are within phloem sieve elements. The stylet is pushed between the cells, during which it periodically probes cells. Having found a suitable phloem sieve cell only the stylet tip enters. Prior to feeding, watery saliva is injected into the sieve cell to counteract the plant's defense mechanisms.

    A few Hemiptera have lost this ability. For example one aphid group, the Phylloxeridae (Aphidoidea) feed on cell sap.

  • Phloem-feeding Auchenorrhyncha include most planthoppers (Cercopoidea, except spittlebugs); and many leafhoppers (Cicadellidae), plus most plant-feeding Heteroptera, such as the seed bugs (lygaeids), shield bugs (pentatomids), and leaf-footed bugs (coreids). The Cicadomorpha initially evolved to feed on xylem (Cercopidae, Cicadidae, Cicadellidae: Cicadellinae), but has radiated to phloem (Membracidae, Cicadellidae: Deltocephalinae) and parenchyma (Cicadellidae: Typhlocybinae) as neoniches, presumably after the development of these plant tissues (Sorensen et. al, 1995). Phloem feeding is probably universal in Fulgoroidea, and in Cicadelloidea other than Cicadellini and Typhlocybinae, but firm evidence is lacking for several tribes of Cicadellidae and some families of Fulgoroidea (Novotny and Wilson, 1997). Planthoppers (Fulgoromorpha) probably initially fed on roots and fungal hyphae, as many of their immatures still do, and subsequently became phloem-feeders. The Heteroptera evolved into predation, but a few groups subsequently became parenchyma, seed and pollen-feeders (the Pentatomomorpha are the only others where phytophagy became common).

    Cicadomorpha and Fulgoromorpha feed with less precision than sternorrhynchans: The insect pushes its stylets through the intervening cells to the phloem sieve element from which it eventually feeds.

Xylem feeding appears universal in Cercopoidea and in Cicadoidea. In Cicadelloidea, only members of Cicadellini sensu Hamilton have been shown to be xylem feeders. Reports on xylem feeding of species other than cercopoids, cicadoids (cicadas) and cicadellines refer to facultative rather than obligatory xylem feeding, or the evidence is equivocal. Dedicated xylem-feeders produce what is, in effect, a highly dilute form of honeydew - hence seldom described as such. Insects whose feeding damages phloem ducts, such as large cicadas, may cause the sugar rich sap to bleed after the insect has moved on - which may dry to a white sugar crust called manna, but in some cases that exudate is a mixture of sweet honeydew and sap.

Lepidoptera and wasps

Caterpillars of some Lycaenidae butterflies and some moths produce honeydew. Maschwitz et. al (1986) observed various ant species of the subfamilies Formicinae, Dolichoderinae and Myrmicinae feeding on anal exudate from tortricid larvae of a hitherto unknown genus and species in Malaysia. These larvae live in silken shelters fixed to the leaves of bamboo. In response to mechanical stimuli from the ants, they discharge from the anus a liquid containing sugar and amino acids and/or protein.

More than half of lycaenid species associate with ants during their larval stage, and some are obligate myrmecophiles which require specific ants for their survival, as protectors against enemies, or as a food source. These interactions are mediated by several glandular organs. For closely ant-associated, non-parasitic lycaenid caterpillars the dorsal nectar organ (on the seventh abdominal segment) is most important. Upon tactile stimulation around this gland by attendant ants, the larvae secrete droplets of an attractive clear fluid. Unlike aphid honeydew (which, being a variably-modified waste product its discharge is under limited control), this secretion is controlled by the lycaenid larvae, and only minute amounts are produced.

The nectar of myrmecophilous lycaenid species contains about 5-10% sugar, with the possible exception of the Australian obligate ant mutualist Paralucia aurifera. In all lycaenid and riodinid species analyzed thus far, the main sugar components are uniformly either sucrose or glucose. The amino acid content of their secretions, in contrast, seems to be determined by the intimacy of associations with attendant ants, more strongly myrmecophilous species providing a richer and more diverse mixture. Daniels et. al (2005) analysed the nutrient composition of this larval secretion from three unspecifically and facultatively ant-attended lycaenid butterfly species (Polyommatus coridon, P. icarus, and Zizeeria knysna). Its composition was very different from the caterpillar's haemolymph: 0.03-1% (w/v) of the secretion was amino acids, of which half was leucine, but also phenylalanine (another 'essential' amino acid). The amino acid content of P. coridon secretion was greater than in almost any other alternative source, be it honeydew, floral or extrafloral nectars. The total sugar content was 4.4-7.4% (w/v), of which sucrose was the main component - which is less than aphid honeydew or plant nectar. In P. icarus, and Z. knysna melezitose was the second-most important component, followed by fructose and glucose. Melezitose is commonly found in aphid honeydew, especially when ant-attended, but these two lycaenids clearly do not produce it for osmoregulation. P. coridon, which is strongly facultative myrmecophilous, sometimes also produced a little glucose, but very small amounts of other sugars.

First image: a Lankan large oakblue butterfly larva (Arhopala amantes) with Asian weaver ants (Oecophylla smaragdina); Second image: Oecophylla smaragdina taking honeydew from larval Redspot butterfly (Zesius chrysomallus). Both ©Kalesh Sadasivan, via antwikki, CC-by-SA.

Owing to their thin waists, adult ants, bees, and wasps cannot readily process large food items, and pass these to the larvae (Schultner et.al, 2017). In wasps these larvae produce saliva of similar sugar and amino acid composition to nectar (including essential amino acids not produced by the adults) which is consumed by attendant adult workers. Eusocial ant and wasp nests fare poorly if adults are denied access to these larval secretions. When prey are in short supply the larvae starve and, if possible, the adults switch to alternative food sources (which may include the larvae).

Gall wasps (Cynipidae: genera Andricus, Disholcaspis and Dryocosmus) can induce the host tree (oaks, Quercus) to secrete a sugary liquid from their galls. Nicholls et. al (2017) found this trait appears to have evolved a number of times within the Cynipini, and is exhibited by at least 13 species. Oak trees lack floral or extrafloral nectar, and ants consuming the sugary gall secretion reduce mortality of the gall wasp larvae due to parasitoid attack. This secretion occurred from gall eruption until the gall wasps emerged. It was dispersed randomly across the gall surface, and there was no nectary structure. The sugar concentration was 73%, of which 94% was sucrose, 2% was glucose, 1% fructose and 3% oligosaccharides.

Image above: Ants collecting honeydew from gall produced by larval Disholcaspis eldoradensis (honeydew gall wasp). ©Edward Rooks, CC BY-NC.

Saps that give honeydew

To the uninitiated, honeydew appears much like syrup, nectar, or honey - all of which are generally derived from plant 'sap'.

Crude sap is produced by gross tissue damage of live or fresh plant material in bulk (= flesh + skin + fibrous material). Cane syrup for instance is filtered crushed whole sugarcane stems, concentrated by boiling; further boiling yields crystals of raw dark sugar, or it may be refined to white sugar. Crude sap is a variable combination of xylem sap, phloem sap and cell sap, plus resins, tannins, pectins, oils and other plant material. Resins and latexes, unlike other sap components, are produced 'intentionally' by plants such as conifers and euphorbias following injury to ward off microbial, insect, or animal attack to the site of injury. Note: (a) Resins can trap biological material and prevent microbial breakdown very effectively: amber (a fossilized resin) has preserved insects for many millions of years. (b) The latex of some euphorbias contain prussic acid.

A function common to all saps it their pressure maintains plant turgor (fluid pressure which provides rigidity) which is why thirsty plants droop.

Cell sap is derived from cell vacuoles within the plant tissues. Cell sap extraction, contents, and properties depend upon the particular tissue and its function (whether as dermal, vascular, or ground tissue). Parenchyma ground tissue, for instance, is commonly used by plants for storage in roots, stems and fruits (including honeydew melons - their flesh is 9% sugars). Parenchyma is an important sugar store in sugarcane and sugarbeet, from which table sugar is made. (Refined white table sugar is largely sucrose, a disaccharide of glucose & fructose, plus fructose, a monosaccharide common in fruits.) Ground tissue, and its sap, often has a rich mixture of the nutrients required by insects, but may also contain toxins, gums, and various anti-feedants. Vascular tissue saps, by contrast, have fewer such deterrents, but pose nutritional challenges to committed consumers.

Image above: Cross-section of a herb stem (flax, Linum usitatissimum), showing the parenchyma, xylem, and phloem cells - surrounded by strengthening sclerenchyma and cuticle. Photo Ryan R. McKenzie, CC0.

Xylem vascular tissue is primarily a set of sap-filled tubes that passively conduct water from the roots to replace the plant's evaporative losses (hence suck the water up). The roots assist that transport to some extent by actively pumping inorganic ions into the xylem lumen. As a result, water enters the xylem sap by osmosis and exerts what is known as 'root pressure'. The xylem sap contains varying amounts of dissolved minerals (including inorganic nitrogen), sugars (mainly monosaccharides =simple sugars), amino acids (both essential and nonessential), 'sugar alcohols' (such as xylitol, but not xylol) and plant hormones.

Xylem sap is usually very dilute (sugars 1 mM, amino acids 3-10 mM) and does not taste sweet to humans unless dried - except for when 'sap rises' in spring, when xylem sap may transport sugars stored in the roots or stem. Maple sugar is dehydrated xylem spring-sap from the sugar maple (Acer saccharum), the black maple (A. nigrum), or the red maple (A. rubrum). This xylem sap may contain 2-5% of sugar (w/v) of which 90% is sucrose, plus variable amounts of fructose and glucose. At the other extreme, guttation (an overflow of xylem sap expelled from leaves when root pressure exceeds leaf suction) is generally tasteless to humans. Goatley & Lewis (1966) found guttation of rye, wheat and barley seedlings contained 0.003-0.005% sugars, 0.0003-0.0014% amino acids (non-essential), and 0.003-0.005% inorganic ions (w/v). Dried guttation can be sweet enough to attract insects or, if there is excess inorganic soil nitrogen, to 'burn' tender plants. Neonicotinoids in guttation may harm pollinators.

First image: maple syrup tapping, Photo Oven Fresh. Second image: guttation from a strawberry (Fragaria) leaf. Photo Noah Elhardt. Both images CC0.

Xylem sap, whilst having few toxins and relatively balanced nutrients for insects, is nearly always very dilute - and in most of the plant is under negative pressure (so must be actively sucked out). Xylem feeders therefore require suitable feeding equipment and large amounts of xylem sap (0.1-0.8 ml per milligram of insect per day). The resulting liquid excrement, whilst very large (xylem feeders tend to be larger than phloem feeders), is nearly always extremely nutrient poor (and unsweet). In most cases the result approximates distilled water and can evaporate without much trace. Spittlebugs are an exception because they add a foaming agent to their faeces and use their legs to whip it into a mass of sticky protective bubbles (cuckoo spit). Whilst some predominately phloem sap feeders will also take xylem sap, virtually all insects that wholly feed on xylem sap are Auchenorrhyncha. Many Auchenorrhyncha feed on parenchyma, or on a mixture of parenchyma, phloem sap and xylem sap.

Phloem sap conveys nutrients, rather than water, gases or waste products. Unlike xylem, which has inert tubes providing unidirectional transport, phloem transport is bidirectional via a series of living tubular cells known as sieve elements. Phloem sap is a strong solution of sugars (especially disaccharides), but a rather weaker solution of amino acids (largely the non-essential ones), plus various organic compounds being transported from where they are synthesised (or are being recovered) to where they are needed for growth (or storage). In a few plants (such as cucurbits) phloem sap may also contain appreciable quantities of protein. At least some aphids are able to digest proteins within the sieve-tubes - and presumably ingest the results. Most vascular plants use specific proteins to block attacked or damaged sieve tubes.

Whilst glucose (a monosaccharide) is the primary product of photosynthesis, phloem sap sugar is primarily sucrose, plus some fructose (another monosaccharide). Phloem sap is, on average 15-25% dry matter, 90% of which is sucrose. With a few exceptions (glucosinolates in crucifers and other Capparales, cardenolides in the Asclepiadaceae, and pyrrolizidine alkaloids in various groups) phloem sap contains few toxins. It has low viscosity but high osmolarity (=moles dissolved per litre). Unlike xylem sap, phloem sap is usually under some positive pressure.

Image above: Sap run on birch (Betula) presumably made and maintained by European hornet (Vespa crabro); ©InfluentialPoints.

Owing to its contents, phloem is a tempting target to many animals, especially in spring. Ants and wasps for example will strip the cuticle to feed on phloem as it oozes out. Since plants actively react to phloem damage by sealing the affected vessels, ants and wasps have to strip progressively more cuticle to maintain the desired flow. Many insects that feed primarily on phloem have surprisingly-flexible fine-piercing tubular mouthparts. Their saliva not only lubricates the mouthparts entry and exit between cells, it actively inhibits the plants phloem-sealing mechanism. Relatively few insects can cope with a sustained diet of such unbalanced nutrients and high osmotic pressure (its net concentration, of 1000 mM, is several times that of the insects' haemolymph), and only certain Hemiptera can do so. Aside from their feeding equipment, dedicated phloem feeders have specialized symbiotic bacteria or fungi to produce essential amino acids.

Recent research shows phloem-feeders (including aphids) also sometimes feed from xylem, presumably in order to replenish water-loss. Ullman & McLean (1988) found pear psyllid, Psylla pyri, ingest from a variety of vascular and non-vascular tissues (but did not quantify what proportion was taken from each).

Nectar, Honey & Honeydew

Nectars are produced by plants so as to attract insects (and some animals). Although nectar is derived from phloem, it has rather different components - according to the plant's needs. Floral nectar contains a variety of monosaccharides, plus attractants (such as perfumes) to attract pollinators, but may also contain toxins to deter unwanted visitors or to limit the amount of honey per pollinator (such as the nicotine in Nicotiana nectar taken by hummingbirds). Extra-floral nectaries attract ants to protect the plant from herbivores or, in the case of some carnivorous plants, they attract victims. The unpalatability of unripe fruit and the sugar+toxin content of ripe fruit act in similar fashion - they deter frugivores until seeds are ready, and encourage desirable seed-dispersers thereafter. Note: Whilst plants commonly convert the acids in fruit to sugars upon ripening, many ripe fruits, such as those of Datura stramonium, contain human-toxic alkaloids, others contain oils.

First image, flower damaged by ant nectar larceny. Second image, ant at extrafloral nectary at blossom base; both images ©InfluentialPoints.

Many plants produce nectar that is toxic or repellent to unwanted floral visitors. Lohaus & Schwerdtfeger (2014) analysed nectar and phloem (via severed aphid stylet) of angels trumpet (Maurandya barclayana), Mexican twist (Lophospermum erubescens), and rape (Brassica napus). For all 3, phloem sap had 1000-1500 mM sugars, mainly sucrose. The amino acid concentrations varied between 81 and 315 mM, mainly nonessential. Their nectar contained similar amounts of sugars, but rape nectar was mainly glucose and fructose, whereas M. barclayana and L. erubescens were mainly sucrose. Nectar contained just 0.2–2 mM amino acids.

The sugar concentration of floral nectar is 8-80% (w/v), and varies between nearly all sucrose to all hexoses (fructose, glucose), but is fairly consistent within a given species given their preferred pollinators (hummingbirds prefer dilute, sucrose-rich nectars, whereas short-tongued bees and flies favour more concentrated hexose-rich nectars). Rarer sugars identified in nectars of some flowers can be toxic to potential pollinators (Roy et. al, 2017). The main nutrients found in extrafloral nectar are similar to floral nectar, but their micronutrients can differ. Similarly, some ants rely on hexose-rich extrafloral nectar because they cannot digest sucrose. Amino acids are found in all nectars, and whilst important for the protein manufacture in pollinators and ant attendants (although pollen is protein rich, honey bees prefer nectars high in essential amino acids), they can have other roles. Some bees favour nectars with high concentrations of proline, perhaps due to its importance in energy production by their flight muscles. Floral and extrafloral nectar also contains proteins (nectarins) that tailor the nectar for their animal mutualists and prevent microbial growth.

Honey (and most types of honeydew, see below), is made by insects. About 8 Apis species (known as honeybees) produce honey. Humans collect honey from all 8 species, but commercially from just 2 (Apis mellifera & Apis cerana). Honeybees feed primarily upon nectar supplemented by pollen, and convert surplus nectar to honey - an energy rich storage product. (Bees make honey for their benefit, not ours!) Honey is a spore-free supersaturated solution, primarily of the sugars sucrose and fructose in water. Whilst its high osmotic pressure inhibits microbial growth, the bees use a variety of other means to improve its storage properties, such as sealing it in small waterproof (wax) compartments. Being supersaturated, the sugars in honey tend to crystallize, which causes problems for bees - and they try to avoid it. Since the high osmotic pressure of nectar also dehydrates them, bees must drink water - and in hot dry conditions, quite a lot. When nectar is in short supply, bees will sometimes consume honeydew instead. This is not their regular diet, honeybees have problems digesting it - especially the oligosaccharides. Some of the oligosaccharides in honeydew (notably melezitose, see below) are relatively unsweet, exert comparatively low osmotic pressure, but are less soluble than sucrose or fructose, and tend to nucleate crystals in honey.

Honeydew varies from being virtually sugar-free water (when excreted by xylem-feeders), through to the sun-dried solid sugar lumps (known as lerps) which protect some Australian psyllids (there are 300 species thereof, and various distinct lerp-forms). Effects of drying aside, the composition of honeydew, both sugars and otherwise, depends upon its origin. The crucial difference, for many honeydews, is the presence of short-chain sugar molecules (trisaccharides, tetrasaccharides, etc.) known as oligosaccharides - which are often less sweet than mono- / disaccharides, and tend to be more sticky / less soluble. Viewed as a food, fresh honeydew is generally less 'extreme' than phloem. Honeydew is more dilute, and has a more balanced amino acid composition than phloem. To many ants, honeydew amino acid composition is very important.

Image above: Meat ants (Iridomyrmex purpureus) on red lerps (produced by larval Austrochardia acaciae) on mulga (Acacia aneura). ©Mark Marathon, CC-BY-SA-4.0.

All dedicated phloem-feeders have gut-dwelling endosymbionts, either bacterial or fungal but never both. Buchnera has been the primary bacterial endosymbiont of aphid for 160 to 280 million years. Whilst originally derived from bacteria similar to Escherichia coli, it now has a much-reduced genome, lives inside the gut cells, and cannot survive outside its host. The fungal symbionts of Hemiptera are extracellular and yeast-like. They seem to have originated, much more recently, from entomopathogenic fungi of genera Cordyceps and Ophiocordyceps (Douglas, 2022). These bacterial and fungal symbionts modify the amino acid composition by producing essential amino acids. Some of these are absorbed by the insect, the remainder pass into the excreted honeydew.

Honeydew contains a number of oligosaccharides absent from sap. Converting monosaccharides (especially glucose) and disaccharides (especially sucrose) in phloem sap to oligosaccharides requires energy. Doing so reduces the osmotic pressure (which otherwise dehydrates sap-feeding insects), and improves ant attendance (albeit why is unclear). The same conversion is used to create the nutrient sink by which fungal phloem-feeders produce more honeydew (aphid colonies also produce nutrient sinks simply by taking lots of phloem from one place).

Melezitose is often the predominant honeydew oligosaccharide (up to 40% w/v). This trisaccharide is produced by enzymes from sucrose and glucose. It is less sweet than sucrose and crystallizes more readily. Originally isolated from dried larch 'sap', it was assumed to be a plant sugar much like melitose (=Raffinose), so was named melezitose: From French meleze (=larch). In fact, melezitose is not produced by plants (or, if so, in minute amounts), but is produced by a number of honeydew-producers. Nonetheless, for some time it was believed to be component of tree sap following insect attack.

Why produce honeydew

The answers to this depend upon what precisely is being described as honeydew.

  1. Where 'honeydew' refers to plant sap:

    Plant sap is generally only released following injury to the plant. (The exception being guttation, where xylem sap is exuded via specialized leaf pores in very damp conditions when water taken up by the roots exceeds evaporation via the leaves.) Loosing plant sap is a waste of water and valuable nutrients, it risks pathogen invasion, and encourages unwanted herbivores. Thus plants attempt to seal-off the damage, and discourage unwanted visitors by exuding resin or latex, or by having toxins in their cell sap. Both phloem and xylem sap are relatively toxin-free, but phloem vessels have self-sealing properties which phloem feeders have to overcome.

    Where phloem or xylem sap-feeders have been active, drops of the sap may ooze for a short time thereafter, yielding droplets of 'honeydew'.

  2. Where 'honeydew' refers to plant nectar:

    Plants produce nectar for three very different reasons: pollination, protection, or predation. Floral nectar is produced from phloem via specialized glands within the flowers in order to attract pollinating insects, and deter nectar thieves - so both the flowers and the nectar composition are highly optimized towards that end.

    Note: Not all plant 'flowers' produce nectar: primitive wetland-dwelling plants produce motile sperm, or rely on passive waterborne transport, and many land dwellers use windborne transport. A few supply blooms or pollen in return for insect pollination, but floral nectar is a recent innovation. That said, ants in particular engage in 'nectar larceny' from flowers - albeit their presence may also help protect the surviving flowers from herbivores.

    Grass flowers, although wind-pollinated, have been found to produce sugar-rich fluid (known as nectar) due to ergot fungus - which possibly acts as a 'nutrient sink'. The composition of this 'nectar' varies with, and is modified by, the fungus to produce ergot honeydew rich in conidiospores and attractive to insects which disperse the spores.

    Many plants develop extra-floral nectaries in order to reward, in particular, herbivore-discouraging ants - although that is not their only method of obtaining such protection. For example some plants produce ant-friendly galls or nodules, but others encourage ant attended phloem-fed aphids. (e.g. Aphis jacobaeae-friendly ragwort strains put less toxin in their phloem.)

    A number of carnivorous, 'pitcher plant' species have insect-attractive extra-floral nectaries around the entrance of their pitfall traps. The nectar of the yellow pitcherplant (Sarracenia flava) also contains the same nerve-paralysing toxin (coniine) as found in hemlock and fools-parsley.

    Image above: Muscid on a carnivorous yellow pitcherplant (Sarracenia flava) pitfall trap, the lip-roll (peristome) of which is studded with extra-floral nectaries. ©Stefano Zucchinali, cc3.0.

    Whilst extra-floral nectaries produce very small amounts of nectar, some floral nectaries can produce enough nectar to yield visible droplets on plants - especially species which are bird or bat-pollinated.

  3. Where 'honeydew' refers to insect honeydew:

    Insects produce honeydew as a waste-product, for protection, to feed their carers, or a combination thereof. Most honeydew observed as sweet droplets on plants are the faeces of specialized phloem feeders.

    Xylem sap, whilst an abundant and generally reliable low-toxin low-osmolarity food source with a good nutrient balance, is normally very dilute (the exception being some plant species in spring, where the sucrose + fructose content may be 3 or even 7%). Moreover xylem sap (being in part sucked up by evaporative loss from the leaves) is often under negative pressure so has to be actively pumped out, which requires energy and specialized pumping equipment (other than low on the plant). As a result the faeces of xylem feeders are both highly-copious and very, very, dilute (and unsweet). Being of correspondingly limited food value, they are simply discarded. Spittlebugs are an exception since they add foam-stabilizing chemicals to their watery waste and whip it into an unsightly but concealing, mass of protective foam.

    Phloem sap is more concentrated than xylem sap but relatively poor in 'vital' amino acids. Non-specialists get around this by, for example, switching between sap sources. Relatively few species can subsist entirely on this extremely unbalanced diet - not least since phloem sap, being hyper-osmotic, tends to dehydrate the feeder. Taking more phloem to obtain an adequate supply of vital amino acids exacerbates the problem, so a number of species reduce the osmotic pressure by converting the phloem's mono- and disaccharides to short-chain polymers (=oligosaccharides). For example, fructose being the principal sugar metabolised by aphids, their gut enzymes break down disaccharides such as sucrose and maltose, and synthesize the trisacharide melezitose, erlose, raffinose, and the disaccharide trehalose often using glucose as a substrate. The resulting honeydew ranges from nearly all oligosaccharides, to virtually untouched phloem sugars. Insects that largely subsist on phloem, such as aphids, use gut symbionts to improve the amino-acid balance, but in order to obtain enough amino acids, they still have to consume and then excrete the excess sugar.

A waste disposal problem

Honeydew: Late 19th century slang for the muck, or raw sewage, in a cesspool. Late Victorian euphemism. [As in] "It's time to empty the cesspool, the honeydew is nearing the top."
 
Source: The Urban Dictionary

If you think honeydew is a problem on your car, or on your plants, imagine a life producing copious quantities of liquid excrement. It may sound like a joke, but honeydew can pose a serious problem to its producers. Firstly, being sticky, it can seriously damage and disable delicate insects such as aphids. Secondly, being nutritious, honeydew attracts unwanted visitors such as mould (which damages the aphids' food plants), predators (such as wasps, syrphids & birds) and parasitoids - all of which can cause mass mortality to an aphid colony.

First image, European wasp (Vespula germanica) gleaning honeydew from bird cherry-oat aphids (Rhopalosiphum padi); second image, adult syrphid taking honeydew from Cooley spruce gall adelgid (Adelges cooleyi); ©InfluentialPoints.

So, what are the options? - bearing in mind these may not be mutually exclusive. (What follows is largely about aphids since most is known of that group, but doubtless applies to other phloem feeders.)

  1. Ignore it

    Setting aside comments about Derek and Clive Live, doing nothing may be the best option if your population is sparse or solitary, or you are not producing much honeydew - for instance, if you are aestivating, or if your host's phloem is transporting little of use. Adult coccids being generally immobile, find drying honeydew less of an entrapment risk - they also have a dorsal anus.

  2. Move elsewhere

    The do-nothing method has obvious limits - especially for fast-growing large dense colonies - and most especially where usable space is limited. In that situation, once matters become too appalling some or all of the colony can disperse - assuming a suitable alternative is in close proximity. Sometimes the apterae disperse on foot, but more often the viviparae switch to producing nymphs that mature to alates, which then fly to a new host. Since weather is fickle, some species have a fall-back option - if circumstances do not require emigration, the wings may never develop (and the adult functions as an ordinary aptera).

  3. Dump it

    For aphids atop a growing shoot any honeydew may simply drop off, albeit this is less fun for those below. Being on the underside of a leaf allows honeydew to fall away and shields the aphids from direct hits from above (or indeed from rain drops) but a sticky shiny leaf upperside is still an advertisement to unwelcome visitors. Some aphids kick their honeydew away with the back leg, other flick it away with their cauda, whilst others expel the droplet by contracting their abdomen or rectum (Way, 1963). Some gall-dwelling aphid species have nymphs that specialize in gall defence and/or cleaning. These nymphs (for example Pemphigus populitransversus) collect the colony's honeydew as balls, and push them out of the gall's entrance. Aphids living within closed galls for an extended period sometimes have another option, their plant may resorb the honeydew - and thus recoup some of its losses. This latter option is only likely to evolve in for plants where the gall-dwellers are very longstanding routine lodgers - such as Paracolopha morrisoni.

    Image above: Sometimes someone else will clean up the unwanted honeydew, as this tree bumblebee (Bombus hypnorum) is doing for a colony of rosy apple aphid (Dysaphis plantaginea) in their leaf-roll; ©InfluentialPoints.

  4. Use protective material

    Wax is water-repellent. Moreover whilst wax-making is energy-intensive, it uses little or no precious nitrogen. Small wax particles do stick to honeydew, but cause it to ball-up - which either roll away, or readily drop off. Wax fibres and flakes break-off readily, so any honeydew which does stick is a smaller problem to the aphid. In addition, wax tends to get transferred to the aphid's immediate surroundings which helps prevent them becoming honeydew-coated. Furthermore wax is unpalatable to many predators, and can provide visual camouflage, or make it harder for unspecialized predators to find an individual aphid's precise location.

    Image above: Gall on black poplar (Populus nigra) cut open to show the colony of poplar-cudweed pouch gall aphid (Pemphigus populinigrae). The aphid wax coats the honeydew droplets preventing the winged adults from becoming fouled and unable to fly; ©InfluentialPoints.

  5. Poison it

    The high sugar content of honeydew frequently attracts unwelcome visitors - such as parasitoids wanting a feed prior to laying eggs in the aphid. Poisoning unwanted visitors may seem outwardly attractive, but making poison is apt to prove expensive (metabolically speaking). Many aphids of course feed on poisonous plants, and those plant poisons are available, if not always in the plant's phloem. This of course assumes the aphids can cope with said poison. Aphids such as Aphis sambuci & Aphis jacobaeae sequester the plant poison safely within their own sensitive tissues - which provides a nasty lesson for uneducated consumers thereof. An alternative option is to 'weaponize' their waste. Oligosaccharides such as melezitose are one such possibility (especially given they reduce water loss). Some parasitoids and probably some predators cannot metabolize melezitose, which when consumed in quantity makes them ill, so could function as an antifeedant. It seems, with continued use over thousands of generations, specialized predators and parasitoids develop immunity.

  6. Use as bribery

    An alternative approach is to pay off the enemy in return for a services rendered. Ants can be serious aphid predators, but at the same time they can keep away other predators. Ants, despite their reputation, do not like the honeydew produced by many aphid species. Yet some aphids produce honeydew that is highly attractive to certain ant species, and a few aphid species have developed extremely close mutually-beneficial relationships with certain ant species. Such aphids often have behaviour and morphology modified to facilitate this relationship (for example some aphids have honeydew-retaining baskets of hairs, termed trophobiotic organs, around their anus). Close observation indicates just a very few individual ants remain with the colony for extended periods of time. These dedicated individuals pass the regurgitated honeydew to their nest mates and display a fierce loyalty towards their precious aphids, even post mortem - suggesting melezitose could be an addictive ant narcotic.

Image above: black garden ants (Lasius niger) attending lime leaf-nest aphid (Patchiella reaumuri) are devoted but comparatively non-aggressive - unlike the 'crazed killer ants' (Lasius fuliginosus) attending the variable clematis aphid (Aphis vitalbae); ©InfluentialPoints.

Acknowledgements

We are grateful to the photographers named above for making some of their pictures available for use under Creative Commons licences.

The information in this page was drawn from a wide variety of sources, but we are particularly indebted to Douglas (2006), Nicholls et. al (2017), Novotny & Wilson (1997), Roy et. al (2017), Sorensen et. al (1995) and Will et. al (2013). Any errors in quoting their work are ours alone.

Useful weblinks

References

  • Aranda-Rickert, A. et al. (2017). Sugary secretions of wasp galls: a want-to-be extrafloral nectar? Annals of Botany 120, 765–774. Full text

  • Daniels, H., Gottsberger, G. and Fiedler, K. (2005). Nutrient composition of larval nectar secretions from three species of myrmecophilous butterflies. Journal of Chemical Ecology 31(12). Full text

  • Douglas, A. E. (2006). Phloem-sap feeding by animals: problems and solutions. Journal of Experimental Botany 57(4), 747–754. Full text

  • Douglas, A. E. (2022). Insects and their beneficial microbes. Princeton University Press.

  • Funder, M. & Roy, B.A. (2000). Pollinator-mediated interactions between a pathogenic fungus Uromyces pisi (Pucciniaceae) and its host plant, Euphorbia cyparissias (Euphorbiaceae). American Journal of Botany. 87(1), 48–55. Full text

  • Goatley, J.L. & Lewis, R.W. (1966). Composition of guttation fluid from rye, wheat, and barley seedlings. Plant. Physiol. 41, 373-375. Full text

  • Lohaus, G. & Schwerdtfeger, M. (2014). Comparison of sugars, iridoid glycosides and amino acids in nectar and phloem sap of Maurandya barclayana, Lophospermum erubescens, and Brassica napus. PLoS ONE 9 (1): e87689. Full text

  • Maschwitz U, Dumpert K, Tuck KR (1986). Ants feeding on anal exudate from tortricid larvae: a new type of trophobiosis. Journal of Natural History 20 (5), 1041-1050.

  • Mower, R. L. and Hancock, J. G. (1975). Sugar composition of ergot honeydews. Canadian Journal of Botany 53(23), 2813-2825. Abstract

  • Naef, A., Roy, B.A., Kaiser, R. and Honegger, R. (2002). Insect-mediated reproduction of systemic infections by Puccinia arrhenatheri on Berberis vulgaris. New Phytologist 154 717–730. Full text

  • Nicholls, J.A., Melika, G. and Stone, G.N. (2017). Sweet tetra-trophic interactions: Multiple evolution of nectar secretion, a defensive extended phenotype in cynipid gall wasps. The American Naturalist 189 (1), 66-77. Full text

  • Novotny, V. & Wilson, M.R. (1997). Why are there no small species among xylem-sucking insects? Evolutionary Ecology. 11, 419-437. Abstract

  • Paton, D.C. (1980). The importance of manna, honeydew and lerp in the diets of honeyeaters. Emu 80, 213-226. Abstract

  • Roy, R., Schmitt, A.J, Thomas, J.B., Carter, C.J. (2017). Nectar biology: From molecules to ecosystems. Plant Science. 262, 148–164. Abstract

  • Schultner E, Oettler J, Helanterä H. (2017). The role of brood in eusocial hymenoptera. Q. Rev Biol. 92 (1), 39-78. Full text

  • Sorensen, J.T. et. al (1995). Non-monopoly of Auchenorrhyncha (‘Homoptera’) based upon 18S rDNA phylogeny. The Pan-Pacific Entomologist. 71(1) p. 31-60. Full text

  • Ullman, D.E. & McLean, D.L. (1988). Feeding behavior of the winter-form pear psylla, Psylla pyricola (Homoptera: Psyllidae), on reproductive and transitory host plants. Environ. Entomol., 17 675-678. Full text

  • Wäckers, F.L. (2000). Do oligosaccharides reduce the suitability of honeydew for predators and parasitoids? A further facet to the function of insect-synthesized honeydew sugars. Oikos 90(1), 197-201. Full text

  • Way, M.J. (1963). Mutualism between ants and honeydew-producing Homoptera. Annual Review of Entomology 8, 307-344. Abstract

  • Will, T., Furch, A.C.U. and Zimmermann, M.A. (2013). How phloem-feeding insects face the challenge of phloem-located defences. Frontiers in Plant Science 4 (336), 1-12. Full text

  • Will, T. & Vilcinskas, A. (2015). The structural sheath protein of aphids is required for phloem feeding. Insect Biochemistry and Molecular Biology. 57, 34-40. Full text