Tag Archives: mutualism

Sloth Moths – moving faster than their hosts

One of the minor downsides of our Biology and Taxonomy of Insects module on the MSc course is, that we do have to review a lot of families within some of the groups, Lepidoptera being a prime example.  Current estimates range from 250 000 to 500 000 species in 124 families (Kristensen et al., 2007). Going through the basic biology of each family can be pretty dry stuff, even if I have a personal anecdote or two to help lighten information overload.  I am, for example, able to wax lyrical for several minutes about small ermine moths and their incredible silk-production activities, but even after more than 40 years of playing around with insects I don’t have a personal story for every family of Lepidoptera 🙂 so I am always on the lookout for an extra interesting or mind-blowing fact to help leaven the student’s knowledge diet.

Imagine my delight then when I came across a clip* from a BBC One Wildlife programme, Ingenious Animals, describing an obligate association between sloths and moths and not just because of the rhyming opportunity** 🙂

Sloth with moths – BBC One Ingenious Animals

The earliest record of a moth associated with a sloth that I have been able to find is in 1877 (Westwood, 1877) which merely records that the unidentified moth was “parasitic on the three-toed sloth”. In 1908 a Mr August Busck on a visit to Panama saw a two-toed sloth, Choloepus hoffmanni fall from a tree and noticed several moths flying out of the sloth’s fur.  He caught these and on his return to the United States presented them to Dr Harrison Dyar (Dyar, 1908a).  If the name seems familiar to you that is because Harrison Dyar is better known in connection with Dyar’s Law, the observation that larval growth in arthropods is predictable and follows a geometric progression (Dyar, 1890). The moths were identified by Dyar as a new species which he named Cryptoses choloepi.  Dyar hypothesised that the moths and their larvae lived in the fur of the sloth and it was this that caused the sloth’s matted hair.

Cryptoses choloepi (Lepidoptera, Chrysauginae)

http://nmnh.typepad.com/department_of_entomology/2014/03/sloths-moths-and-algae-whos-eating-whom.html

Shortly after publishing the first note Dyar came across two more moth specimens, this time collected from a sloth in Costa Rica.  He felt that these were another species, possibly Bradipodicola hahneli (Dyar, 1908b).  The next mention of a sloth moth that I could fine is in a marvellously titled paper (Tate, 1931) who refers to a moth shot in western Ecuador whose fur was “literally alive with a small species of moth, whose larvae possibly fed on the greenish algae which grew in the hair”.  The idea that sloth moths fed on the fur of living sloths was further reinforced by Brues (1936) although this was not based on any personal observations.  It was only in 1976 that it was discovered that the larvae of the sloth moth Cryptoses choloepi were actually coprophagous (Waage & Montgomery, 1976), the female moths waiting for the three-toes sloth B. infuscatus to descend from the trees to relive their bowels, which they do about once a week.  As an aside, I have known Jeff Waage for many years in his role as a biological control expert but until I discovered this paper about a month ago, had no idea that he had ever spent time inspecting sloth faeces 🙂  Jeff and his co-author Gene Montgomery, described the association between the moths and the sloths as phoretic, rather than parasitic, as they saw no harm being caused to the sloths, but a number of benefits accruing to the moths, namely oviposition-site location being simplified, the fur of the sloth acting as refuge from avian predators and diet enhancement from sloth secretions (Waage, 1980).  It turns out however, that some species of sloth moth do spend their whole life cycle on the sloth, B. hahneli lose their wings once a sloth host is found and their eggs are laid in the fur of the sloth (Greenfield, 1981).  The algae that these moths presumably feed on is considered to be in a symbiotic association with the sloths, providing camouflage and possibly nutrition in the form of trace elements (Gilmore et al., 2001).  Hereby lies a tale.  The two-toed sloths have a much wider diet and home range than three-toed sloths and also defecate from the trees, unlike the three-toed sloths which have a very narrow diet (entirely leaves) and narrow home ranges, yet descend from the relative safety of the forest canopy to defecate, albeit only once a week, but still a risky undertaking (Pauli et al., 2017).  Rather than a phoretic relationship Pauli and colleagues see the relationship between sloths, algae and moths as a three-way mutualism, beautifully summarised in their Figure 3.

Postulated linked mutualisms (þ) among sloths, moths and algae: (a) sloths descend their tree to defecate, and deliver gravid female sloth moths (þ) to oviposition sites in their dung; (b) larval moths are copraphagous and as adults seek sloths in the canopy; (c) moths represent portals for nutrients, and via decomposition and mineralization by detritivores increase inorganic nitrogen levels in sloth fur, which fuels algal (þ) growth, and (d ) sloths (þ) then consume these algae-gardens, presumably to augment their limited diet. This figure brazenly ‘borrowed’ from Pauli et al. 2014).

The sloths take the risk of increased predation by descending to ground level, because by helping the moths they improve their own nutrition and hence their fitness.  Yet another great example of the wonders of the natural world.

 

Post script

Although not as exotic as the sloth moth, we in the UK can also lay claim to a coprophagous moth, Aglossa pinguinalis, the Large Tabby which feeds on, among other things, sheep dung.  In Spain it is recorded as a cave dweller feeding almost entirely on animal dung, apparently not being too fussy as to the source.

 

References

Bradley, J.D. (1982) Two new species of moths (Lepidoptera, Pyralidae, Chrysauginae) associated with the three-toed sloth (Bradypus spp.) in South America.  Acta Amazonica, 12, 649-656.

Brues, C.T. (1936) Aberrant feeding behaviour among insects and its bearing on the development of specialized food habits.  Quarterly Review of Biology, 11, 305-319.

Dyar, H.G. (1890) The number of molts of lepidopterous larvae. Psyche, 5, 420–422.

Dyar, H.G. (1908a) A pyralid inhabiting the fur of the living sloth.  Proceedings of the Entomological Society of Washington, 9, 169-170.

Dyar, H.H. (1908b) A further note on the sloth moth. Proceedings of the Entomological Society of Washington, 10, 81-82.

Dyar, H.G. (1912) More about the sloth moth. Proceedings of the Entomological Society of Washington, 14, 142-144.

Gilmore, D.PP., Da Costa, C.P. & Duarte, D.P.F. (2001) Sloth biology: an update on their physiological ecology, behaviour and role as vectors of arthropods and arboviruses.  Brazilian Journal of Medical and Biological Research, 34, 9-25.

Greenfield, M.D. (1981) Moth sex pheromones: an evolutionary perspective.  The Florida Entomologist, 64, 4-17.

Kristensen, N., Scoble, M.J. & Karsholt, O. (2007)  Lepidoptera phylogeny and systematics: the state of inventorying moth and butterfly diversity.  Zootaxa, 1668, 699-747.

Pauli, J.N., Mendoza, J.E., Steffan, S.A., Carey, C.C., Weimer, P.J. & Peery, M.Z. (2014) A syndrome of mutualism reinfocrs the lifestyle of a sloth.  Proceedings of the Royal Society B, 281, 20133006. http://dx.doi.org/10.1098/rspb.2013.3006.

Pinero, F.S. & Lopez, F.J.P. (1998) Coprophagy in Lepidoptera: observational and experimental evidence in the pyralid moth Aglossa pinguinalisJournal of Zoology London, 244, 357-362.

Tate, G.H.H. (1931) Random observations on habits of South American mammals.  Journal of Mammalogy, 12, 248-256.

Waage, J.K. (1980) Sloth moths and other zoophilous Lepidoptera.  Proceedings of the British Entomological and Natural History Society, 13, 73-74.

Waage, J.K. & Montgomery, G.G. (1976) Crytopses choloepi: a coprophagous moth that lives on a sloth.  Science, 193, 157-158.

Westwood, J.O. (1877) XXVIII. Entomological Notes.  Transactions of the Entomological Society, 25, 431-439.

 

*For the clip about the sloth moth see here http://www.bbc.co.uk/programmes/p04840xn

**Now, when I see a sloth,

My first thought is for the moth,

That has to make that desperate jump

When the sloth decides to take a dump!

 

 

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Not all aphids are farmed by ants

One of the great things about working with aphids is that it gave me the chance to go back to my childhood entomological roots of playing with ants.  Most gardeners have had the experience when cruelly* running their finger and thumb down an aphid covered plant stem of finding their hand suddenly covered with ants.   As someone who has a very relaxed approach to aphids, I find the presence of ants on a plant a handy way of finding aphids, although sometimes the ants are there because of extra-floral nectaries.  So what exactly is going on when you find ants and aphids together?

It has long been known that some aphids are farmed or tended by some ant species.  According to Jones (1927) Goedart** was the first to describe the relationship scientifically (Goedart & Lister, 1685) and by the latter half of the 19th Century you can find illustrations such as the one below that appeared in Van Bruyssel’s fantastic foray into early science-communication.

antsaphids-1

An ant dairy maid coming to milk her aphids – their siphunculi and anuses are just visible if you look closely: cleverly made to look like cow heads (From Van Bruyssel, 1870)

The ant-aphid association is usually defined as a mutualism as the two species exist in a relationship in which each individual benefits from the activity of the other.  Just to confuse people however, the association is also sometimes termed trophobiosis*** (e.g. Oliver et al., 2008) which is a more symbiotic relationship.

The degree of dependence of the aphid on the ants varies from species to species.  Some aphids, especially those that live underground on plant roots, are unable to survive without their ant attendants (Pontin, 1978).   Pontin (1960) also reports seeing Lasius flavus workers licking aphid eggs which he suggests stops them from going mouldy as the licking removes fungal spores.  He also noted that those eggs that were not cared for in this way did not hatch.  Other aphids have a more facultative relationship, and are able to survive quite successfully without the help of their friendly neighbourhood ants.

We tend to think of aphids as soft squidgy defenceless things that are easy to squash.  To other insects however, they present a bit more of a challenge.  Aphids have structural and behavioural defences to keep them safe in the dangerous world of bug eat bug.  Alarm pheromones and dropping behaviour are commonly used by aphids to avoid meeting predators face to face (Dixon, 1958a).    Aphis also have a number of physical defences.  Their spihunculi (cornicles) can produce a quickly hardening wax to gum up ladybird jaws (Dixon, 1958b).  Other aphid species cover themselves with dense waxy coats that make them less palatable or accessible to natural enemies (Mueller et al., 1992).  Other aphids have thick skins (heavily sclerotized) and what entomologists term saltatorial leg modification; long legs to you and me, and so able to give a ladybird or other opportunistic insect predator a good kicking (Villagra et al., 2002).  These characteristics, which are all costly, are reduced or absent in aphids that are frequently associated with ants (Way, 1963) as presumably with ant bodyguards in attendance, there is no need for the aphids to invest in extra anti-predator defences.

antsaphids-2

Note also the shortened siphunculi in Periphyllus testudinaceus and the hairier bottom, when compared with the leggy, and arguably, prettier Drepanosihpum platanoidis.

Apart from reducing their defensive armoury, those aphids that are obligately ant attended have a specially adapted rear end, essentially a hairy bottom.  This is more scientifically known as the trophobiotic organ.   The trophobiotic organ is an enlarged anal plate surrounded by special hairs that acts as a collection and storage device that allows the aphid to accumulate honeydew ready for the ants to remove at their leisure.

antsaphids3

Three different trophobiotic organs, some hairier than others – after Heie (1980)

antsaphids4

A real live view of the “trophobiotic organ” of Tetraneura ulmi (from the fantastic Influential Points website – http://influentialpoints.com/Images/Tetraneura_ulmi_aptera_on_grass_roots_c2015-09-04_14-53-13ew.jpg

Non-ant attended aphids without the trophobiotic organ, deposit their honeydew directly on to the leaf surface or on the ground, or if you are unlucky enough to park under an aphid infested tree, on to your car 🙂  Ants lick and collect sycamore aphid, Drepanosiphum platanoidis honeydew from leaves, but not directly from the aphids, which they do do from the maple aphid, Periphyllus testudinaceus, which also lives on sycamore trees P. testudinaceus (Pontin, 1958).

So what’s in it for the ants?  Why should they bother looking after aphids, even in some cases, keeping aphid eggs in their nests over the winter (Pontin, 1960)? The obvious answer is the honeydew that the aphids produce as a by-product of feeding on phloem sap. The amount of material that an aphid can remove from a plant is quite astounding.  A large willow aphid (Tuberolacnhus salignus) adult can sucks up the equivalent of 4 mg sucrose per day Mittler (1958) , which is equivalent to the photosynthetic product of one to two leaves per day.  Admittedly, they are large aphids and not ant attended****, but even an aphid half their size passes a lot of plant sap through their digestive systems.  Honeydew is not just sugar but is a mixture of free amino acids and amides, proteins, mineral and B-vitamins, so all in all, quite a useful food source for the ants (Way, 1963).  All aphids produce honeydew but not all aphids are ant attended and as I pointed out earlier, not all ants attend aphids.  Our research suggests that 41% of ant genera have trophobiotic species, but these are not equally distributed among ant families.  Some ant sub-families, for example the Fomicinae,  specilaise in ant attendance,  whereas in other ant families such as the Ecitoninae, aphids are used only as prey and the honeydew is gathered from plant and ground surfaces (Oliver et al., 2008).  The ant species that are most likely to develop mutualistic relationship with aphids appear to be those that live in trees, have large colonies, are able to exploit disturbed habitats and are dominant or invasive species (Oliver et al., 2008).

Those ants that do tend aphids don’t just protect them from predators and other natural enemies. They want to maximise the return for their investment. The black bean aphid, Aphis fabae, which is often tended by Lasius niger, has its tendency to produced forms reduced by the ants, thus making sure that the aphids are around longer to provide food for them (El-Ziady & Kennedy, 1956).  The ant Lasius fuliginosus transports young Stomaphis quercus aphids to parts of the tree with the best honeydew production (Goidanich, 1959) and Lasius niger goes one step further, moving individuals of the aphid Pterocomma salicis, to better quality willow trees (Collins & Leather, 2002).  Lasius niger seems to have a propensity for moving bugs about, they have also been seen moving coccids from dying clover roots to nearby living ones (Hough, 1922).

In the mid-1970s John Whittaker and his student, Gary Skinner, set up a study to examine the interactions between the wood ant, Formica rufa and the various insect herbivores feeding on the sycamore trees in Cringlebarrow Wood, Lancashire.  They excluded some ants from some of the aphid infested branches and allowed them access to others on the same trees and also looked at trees that were foraged by ants and those that weren’t.  They found that F. rufa was a heavy predator of the sycamore aphid, D. platanoidis, but tended the maple aphid,  P. testudinaceus (a novel observation for that particular ant-aphid interaction).  Ant excluded colonies of P. testudinaceus decreased, whereas D. platanoidis did not, but on those branches where ants were able to access the aphids, the reverse pattern was seen (Skinner & Whittaker, 1981).

The presence of thriving aphid colonies in the neighbourhood of ant nests and in some cases aphid colonies only exist where there are ant nests nearby (Hopkins & Thacker, 1999), has made some people wonder if aphids actively look for ant partners (Fischer et al., 2015).  There is, however, no evidence that aphids look for ant partners, rather the fact that wing production is reduced in the presence of tending ants, means that aphid colonies can accumulate around and close to ant nests (Fischer et al., 2015a).

That doesn’t mean that the aphids only rely on honeydew production to guarantee the presence of their ant bodyguards. The aphid Stomaphis yanonis, which like other

antsaphids5

Stomaphis aceris, also ant attended.  Imagine trying to drag that mouth part out of a tree trunk quickly 🙂

Stomaphis species, has giant mouthparts, and so needs plenty of time to remove its mouthparts safely definitely needs ant protection to cover its back when involved in the delicate operation of stylet unplugging. In this case, it turns out that the aphids smell like that ants, they have cuticular hydrocarbons that resemble those of their ant protector Lasius fuji and thus encourages the ants to treat them as their own (Endo & Itino (2013).  Earlier work on the ant-attended tree-dwelling aphids, Lachnus tropicalis and Myzocallis kuricola, in Japan showed that the ant Lasius niger preyed on aphids that had not been attended by nest mates, but tended those that had been previously tended (Sakata 1994).  This too would indicate the presence of some sort of chemical marker or brand.

To add support to this, just over twenty years ago (1996), I supervised an undergraduate student Arran Frood*****.   He worked with the maple aphid, and the ants L. niger and L. fulginosus.  Aphids on ant-attended sycamore trees were washed with diluted acetone or water.   Those that had been washed with acetone were predated more than unwashed aphids suggesting that It was like washing off the colony specific pheromone marker. In support of this hypothesis, Arran found that predation would also increase if he swapped a twig full of aphids between colonies, but not from one part of the colony to another. It also worked between the two ant species, Lasius niger and L. fuliginosus, so it seems like the ants have a colony specific marker on their aphids.  We should really have written this up for publication.

Although aphids do not actively seek ant partners, they may compete with each other to retain the services of their ant bodyguards by producing more honeydew (Addicott, 1978).  There is evidence that ants make their decisions of whether to predate or tend aphids by monitoring honeydew production and choose to prey on aphids in colonies that produce less honeydew (Sakata, 1995).  Recent work has also shown that the honeydew of the black bean aphid, Aphis fabae is often colonised by the bacterium Staphylococcus xylosus. Honeydew so infected produces a bouquet of volatile compounds that are attractive to the ant L. niger thus increasing the cahnces of the aphids being ant-attended (Fischer et al., 2015b).  This adds yet another layer of complexity to the already complicated mutualistic life style that aphids have adopted.

And finally, you may remember me writing about the wonderful colour variations seen in some aphid species and how this could be modified by their symbionts. In another twist, it seems that ants may have a say in this too, albeit at a colony level rather than at the clonal level.  The improbably named Mugwort aphid, Macrosiphoniella yomogicola  which is obligately ant-attended by the ant L. japonicus, is found in  colonies that are typically 65% green 35% red (Watanabe et al. 2016).  The question Watanabe and his colleagues asked is why do ants like this colour balance? One possibility is that red and green aphids have slightly different effects on the mugwort plants where they feed. Though green aphids produce more honeydew, red aphids seem to prevent the mugwort from flowering. Given that aphid colonies on a flowering mugwort go extinct, ants looking to maintain an aphid herd for more than a year might see an advantage to keeping reds around to guarantee a long-term food supply from their green sisters.

Aren’t insects wonderful?

 

References

Addicott, J.F. (1978) Competition for mutualists: aphids and ants.  Canadian Journal of Zoology, 56, 2093-2096.

Carroll, C.R. & Janzen, D.H. (1973) Ecology of foraging by ants.  Annual Review of Ecology & Systematics, 4, 231-257

Collins, C.M. & Leather, S.R. (2002) Ant-mediated dispersal of the black willow aphid Pterocomma salicis L.; does the ant Lasius niger L. judge aphid-host quality?  Ecological Entomology, 27, 238-241.

Dixon, A.F.G. (1958a) The escape responses shown by certain aphids to the presence of the coccinellid Adalia decempunctata (L.). Transactions of the Royal Entomological Society London, 110, 319-334.

Dixon, A.F.G. (1958b) The protective function of the siphunculi of the nettle aphid, Microlophium evansi (Theob.). Entomologist’s Monthly Magazine, 94, 8.

El-Ziady, S. & Kenendy, J.S. (1956) Beneficial effects of the common garden ant, Lasius niger L., on the black bean aphid, Aphis fabae Scopoli.  Proceedings of the Royal Entomological Society London (A), 31, 61-65

Endo, S. & Itino, T. (2012) The aphid-tending ant Lasius fuji exhibits reduced aggression toward aphids marked with ant cuticular hydrocarbons.  Research on Population Ecology, 54, 405-410.

Endo, S. & Itino, T. (2013) Myrmecophilus aphids produce cuticular hydrocarbons that resemble those of their tending ants.  Population Ecology, 55, 27-34.

Fischer, C.Y., Vanderplanck, M., Lognay, G.C., Detrain, C. & Verheggen, F.J. (2015a) Do aphids actively search for ant partner?  Insect Science, 22, 283-288.

Fischer, C.Y., Lognay, G.C., Detrain, C., Heil, M., Sabri, A., Thonart, P., Haubruge, E., & Verheggen, F.J. (2015) Bacteria may enhance species-association in an ant-aphid mutualistic relationship. Chemoecology, 25, 223-232.

Goidanich, A.  (1959) Le migrazioni coatte mirmecogene dello Stomaphis quercus Linnaeus, afido olociciclio monoico omotopo. Bollettino dell’Istituto di Entomologia della Università degli Studi di Bologna, 23, 93-131.

Goedart, J. & Lister, M. (1685) De Insectis, in Methodum Redactus; cum Notularum Additione. [Metamorphosis Naturalis] Smith, London.

Heie, O. (1980)  The Aphdioidea (Hemiptera) of Fennoscandia and Denmark. 1. Fauna Entomologica Scandinavica 9.Scandinavian Science Press, Klampenborg, Denmark.

Hough, W.S (1922) Observations on two mealy bugs Trionymus tritolii Forbes and Pseudococcus maritimus Ehrh. Entomologist’s News, 33, 1 7 1-76.

Hopkins, G.W. & Thacker, J.I. (1999) Ants and habitat specificity in aphids. Journal of Insect Conservation, 3, 25-31.

Jones, C.R. (1927) Ants and Their Relation to Aphids.  PhD Thesis, Iowa State College, USA.

Mittler, T.E. (1958a) Studies on the feeding and nutrition of Tuberolachnus salignus (Gmelin) (Homoptera, Aphididae).  II. The nitrogen and sugar composition of ingested phloem sap and excreted honeydew.  Journal of Experimental Biology, 35, 74-84.

Mueller, T.F., Blommers, L.H.M. & Mols, P.J.M. (1992) Woolly apple aphid (Eriosoma lanigerum Hausm., Hom., Aphidae) parasitism by Aphelinus mali Hal. (Hym., Aphelinidae) in relation to host stage and host colony size, shape and location.  Journal of Applied Entomology, 114, 143-154.

Oliver, T.H., Leather, S.R. & Cook, J.M. (2008)  Macroevolutionary patterns in the origin of mutualisms,  Journal of Evolutionary Biology, 21, 1597-1608.

Pontin, A.J. (1958)  A preliminary note on the eating of aphids by ants of the genus Lasius. Entomologist’s Monthly Magazine, 94, 9-11.

Pontin, A.J. (1960)  Some records of predators and parasites adapted to attack aphids attended by ants.  Entomologist’s Monthly Magazine, 95, 154-155.

Pontin, A.J. (1960)  Observations on the keeping of aphid eggs by ants of the genus LasiusEntomologist’s Monthly Magazine, 96, 198-199.

Pontin, A.J. (1978) The numbers and distributions of subterranean aphids and their exploitation by the ant Lasius flavus (Fabr.). Ecological Entomology, 3, 203-207.

Sakata, H. (1994) How an ant decides to prey on or to attend aphids.  Research on Population Ecology, 36, 45-51.

Sakata, H. (1995) Density-dependent predation of the ant Lasius niger (Hymenoptera: Formicidae) on two attendant aphids Lachnus tropicalis and Myzocallis kuricola (Homoptera: Aphidae). Research on Population Ecology, 37, 159-164.

Skinner, G.J. & Whittaker, J.B. (1981) An Experimental investigation of inter-relationships between the wood-ant (Formica rufa) and some tree-canopy herbivores.  Journal of Applied Ecology, 50, 313-326.

Stadler, B. & Dixon, A.F.G. (1999)  Ant attendance in aphids: why different degrees of myrmecophily? Ecological Entomology, 24, 363-369.

Van Bruyssel, E. (1870) The Population of an Old Pear Tree.  MacMillan & Co, London

Vilagra, C.A., Ramirez, C.C. & Niemeyer, H.M. (2002) Antipredator responses of aphids to parasitoids change as a function of aphid physiological state.  Animal Behaviour, 64, 677-683.

Watanabe, S., Murakami, T., Yoshimura, J. & Hasegawa, E. (2016) Color piolymorphism in an aphid is maintained by attending ants.  Science Advances, 2, e1600606

Way, M.J. (1963) Mutualism between ants and honeydew-producing Homoptera.  Annual Review of Entomology, 3, 307-344.

*in my opinion at any rate 🙂

**I have had to take this on faith as have not been able to get hold of the original reference and read it myself

***Trophobiosis is a symbiotic association between organisms where food is obtained or provided. The provider of food in the association is referred to as a trophobiont. The name is derived from the Greek τροφή trophē, meaning “nourishment” and -βίωσις -biosis which is short for the English symbiosis

****Perhaps they are too big for ants to mess with?  They are, however, very often surrounded by Vespid wasps who do appreciate the huge amount of honeydew deposited on the willow leaves and stems.

***** He must have enjoyed it because he also did his MSc project with me the following year 🙂

 

Post script

I began this post with an illustration from Van Bruyssel.  I finish it with this illustration from another early attempt to get children interested in entomology.  Unfortunately in this case the  ant attended aphids are the very opposite of what they should look like and he further compounds his error by telling his youthful audience that the aphids milk the aphids via their siphunculi 😦

antsaphids-holdrich

The very opposite of what an ant-attend aphid looks like – from Half hours in the tiny world; wonders of insect life by C.F. Holder (1905)

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Ten Papers that Shook My World – Owen & Weigert (1976) – The things that eat you are good for you

Journal clubs have been around a long time, but as a new PhD student in 1977 it was a new experience for me.  I was thus somewhat uncertain about what was expected from me when my supervisor presented me with a copy of Owen, D.F. & Wiegert, R.G. (1976) Do consumers maximise plant fitness? Oikos, 27, 488-492, and informed me that I was going to present my views on the paper the following month.  In those days organised PhD training programmes in the UK did not exist. Nowadays, PhD students in the UK follow a programme of lectures and workshops ranging from statistics, presentation skills, paper writing, ethics, use of social media, how to run tutorials, IPR, critical appraisal,  etc. etc. Given my lack of experience,  I was a little apprehensive to say the least.  Luckily I had the chance to see how the older members of our research group dealt with their papers in the preceding weeks and was somewhat moe confident about what was expected of me.  I duly read the paper and highlighted the areas that I wanted to critique.

O&W1O&W2O&W3

Parts of the Owen & Weigert (1976) paper showing the bits that I highlighted for my critique.

Owen & Weigert’s hypothesis was, that contrary to accepted doctrine, consumers, especially those feeding on trees, were beneficial to their host plants and not harmful.  Coming fresh from an agriculture department where I had been taught that anything that ate a plant was a pest, this was a startling and heretical concept for me to digest!  I remember at the time that I was not particularly convinced by the arguments and that within the group the general consensus was that Denis Owen was a bit of an eccentric.  In fact, the senior members of the group entered into a printed debate in the popular scientific press (McLean et al., 1977; Owen, 1977) which resulted in what I still consider to be the best ever front cover of New Scientist 😉

New Scientist cover

Arguably the best ever front cover of New Scientist

 We were not the only ones who expressed scepticism about Owen’s hypothesis, although experimental rebuttals of Owen’s claim that aphids and trees were in a mutualistic relationship via honeydew production did not appear until some years later (Petelle, 1980; Choudhury, 1984, 1985).  These papers resulted in a series of spirited responses from Owen (Owen & Wiegert, 1982a, b, 1985, 1987).  Some years later, however, Joy Belsky provided further evidence against Owen’s hypothesis (Belsky, 1986,1987; Belsky et al., 1993) and I too entered the fray (Leather, 1988,2000).

Thus by the end of the last century it appeared that all the evidence indicated that if you were a plant, being eaten was not good for you.  On the other hand, if Owen had posed his hypothesis at a population or group level, he might have been able to make a better case for herbivores increasing plant fitness. In an earlier post, in which I wrote about the plant immune response and how plants communicate with each other when attacked and warn their neighbours of potential attack, one could definitely make a stronger case for plants benefitting from being eaten.  Induced resistance can even work at an individual level, some recent work (McArt et al., 2013) has shown that evening primroses (Oenothera biennis) attacked early in the season by the Japanese beetle, Popillia japnonica, become more resistant to attack from seed predators than those that escape early season defoliation. As a result the beetle attacked plants produce more seed than those that escaped attack.  Given that a general measure of fitness is reproductive success (i.e. how many seeds are produced) then in this case, consumers do maximise plant fitness and Denis Owen can have the last word.

References

Belsky, A.J. (1986) Does herbivory benefit plants? A review of the evidence. American Naturalist 127, 870-892

Belsky, A.J. (1987) The effects of grazing: confounding of ecosystem, community and organism scales. American Naturalist, 129, 777-783.

Belsky, A.J., Carson, W.P., Jensen, C.L. & Fox, G.A, (1993) Overcompensation by plants – herbivore optimization or red herring. Evolutionary Ecology, 7, 109-121.

Choudhury, D. (1984) Aphids and plant fitness – a test of Owen and Wiegert’s hypothesis. Oikos, 43, 401-402.

Choudhury, D. (1985) Aphid honeydew – a re-appraisal of Owen and Wiegert’s hypothesis. Oikos, 45, 287-289.

Leather, S.R. (1988) Consumers and plant fitness: coevolution or competition ? Oikos, 53, 285-288.

Leather, S.R. (2000) Herbivory, phenology, morphology and the expression of sex in trees: who is in the driver’s seat? Oikos, 90, 194-196.

McArt, S.H., Halitschke, R., Salminen, J.P. & Thaler, J.S. (2013)  Leaf herbivory increases plant fitness via induced resistance to seed predators.  Ecology, 94, 966-975.

McLean, I., Carter, N., & Watt, A. (1977) Pests out of Control. New Scientist, 76, 74-75.

Owen, D.F. (1977) Are aphids really plant pests? New Scientist, 76, 76-77.

Owen, D. F. (1980). How plants may benefit from the animals that eat them. Oikos 35: 230-235.

Owen, D.F. & Wiegert, R.G. (1976) Do consumers maximise plant fitness? Oikos, 27, 488-492

Owen, D.F. & Wiegert, R.G. (1982) Beating the walnut tree: more on grass/grazer mutualism. Oikos, 39, 115-116.

Owen, D.F. & Wiegert, R.G. (1982) Grasses and grazers: is there a mutualism ? Oikos, 38, 258-259.

Owen, D.F. & Wiegert, R.G. (1984) Aphids and plant fitness. Oikos, 43, 403.

Owen, D.F. & Wiegert, R.G. (1987). Leaf eating as mutualism. In Insect Outbreaks (ed. by P. Barbosa & J.C. Schultz), pp. 81-95. Academic Press, New York.

Petelle, M. (1980) Aphids and melezitose: a test of Owen’s 1978 hypothesis. Oikos, 35, 127-128.

 

Post script

Denis Owen died at a relatively young age and for those interested in his career and life, his obituary can be found here.

 

 

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Not all aphids live on leaves

I haven’t written about aphids for a while, so I thought I would indulge myself and tell you about a few of my favourite aphids.  Most people’s perceptions of aphids (assuming that they know what  aphids are of course) is that they live on leaves.  They will I think, also possibly know that they are usually found on the undersides of leaves, although I may be assuming too much here.  In fact, many species of aphid do not live on leaves; a number of species feed on shoots, twigs and branches and some actually feed on the main trunks of trees.  Yet other species live on the roots of trees and herbaceous plants, such as the apple-grass aphid, Rhopalosiphum insertum which can be a pest of apples and cereals, feeding on the leaves and buds of apples and the roots of grasses and cereals.   Another root-feeding aphid that is a double pest, is Pachypappa tremulae, the spruce root aphid, which host alternates between the aerial parts of aspen trees and the roots of Norway spruce; easily visible when infesting the roots of young potted plants due to the presence of white waxy tufts on its rear end.

Some aphids not only live underground feeding on roots, but are entirely dependent on being farmed by ants e.g.  Tetraneura ulmi, which host-alternates between elm and grass roots, and  Forda formicaria, which host-alternates between Pistachio trees and grass roots.

Forda_formicaria_hirsuta_root_aphid_03-03-13_3

http://www.aphotofauna.com/images/bugs_homoptera/bug_forda_formicaria_hirsuta_root_aphid_03-03-13_3.jpg

Both these aphids are looked after or ‘farmed’ by the yellow meadow ant Lasius flavus in exchange for donations of honeydew.

Lasius%20flavus%202

These two aphid species, along with a number of others, have an enlarged anal plate surrounded by special hairs that form the so-called trophobiotic organ.  This acts as a storage device that allows the aphid to accumulate honeydew ready for the ants to remove.  Those aphids that have a more casual (facultative) relationship with ants, do not have this organ which is the basis of this remarkable mutualism.

Another aphid that is farmed by ants, but in a somewhat different way, is the rather larger rose root aphid, Maculolachnus submacaula, which as its name suggests, feeds on rose roots.  In this case, the ants allow the aphids above ground but only in an ant tunnel, similar to those produced by termites when they are infesting a building.  I have only ever been lucky enough to see this aphid once, some 35 years ago in Norwich when I was doing my PhD and noticed things that looked like termite trails running up the main stem of one of my rose bushes.  On breaking them open, well I am a curious entomologist, I found to my surprise not only ants but large brown aphids.

Maculolachnus submacula nest

http://jardiweb-floralbum.forumsactifs.com/t1797-colonie-de-pucerons

for a better view of the aphid see http://www.afripics.co.za/home/products/product.php?ProductID=1301564582

But of course the really spectacular ones are those that feed on branches of trees such as the giant willow aphid Tuberolachnus salignus (famous for its sharks fin) and those from the genus Stomaphis which feed through the bark of trees such as oak and

Tuberolachnus

sycamore and are possessed of truly enormous mouthparts such as those of Stomaphis aceris which feeds on sycamore

Stomaphis query aceris

This one, despite its enormous mouthparts, is quite difficult to find as it hides underneath the bark, but luckily it is ant attended so if you see ants scurrying around on the bark of sycamore and disappearing underneath loose flaking bits, it is a good bet that if you gently lever off the loose bark you will find yourself in the presence of this weird-looking creature.

The more I learn about aphids the more I find to marvel at.  Aphids really are remarkable and we know so little about so many of them and their weird and wonderful life styles.

Useful References

Blackman, R.L. & Eastop, V.F. (19 94) Aphids on the World’s TreesAn  Identification and Information Guide.  CABI Publishing. http://www.aphidsonworldsplants.info/index.htm

Evenhuis, H.H. (1968)  The natural control of the apple grass aphid,  Rhopalosiphum insertum, with remarks on the control of apple aphids in general in The Netherlands. Netherlands Journal of Plant Pathology, 74, 106-117  http://link.springer.com/article/10.1007/BF02309501#page-1

Farrell, J.A. & Stufkens, M.W. (1989) Flight activity and cereal host relationships of Rhopalosiphum spp. (Homoptera: Aphididae) in Canterbury New Zealand Journal of Journal of Crop and Horticultural Science, 17, 1-7  http://www.tandfonline.com/doi/abs/10.1080/01140671.1989.10428003

Ivens, A.B.F., Kronauer, D.J.C., Pen, I., Weissing, F.J. & Boomsma, J.J. (2012)  Ants farm subterranean aphids mostly in single clone groups – an example of prudent husbandry for carbohydrates and proteins?  BMC Evolutionary Biology, 12:106 http://link.springer.com/article/10.1186%2F1471-2148-12-106

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