Aphid flight trends follow climate change: a fifty years long analysis!

ResearchBlogging.orgI started to find now on different crops near Modena the first aphid populations… it is not too early neither too late… in respect to the last years. However, it seems that in Italy we started to have aphids earlier on our plants in the last years.

Interestingly, a recent papers clearly assessed this trend at an European level using the suction trap network, a valuable tool for monitoring invasive aphid species.

39277227.AphidiuscolemaniAccording to the paper published by the Richard Harrington network in the Journal of Animal Ecology, five decades of data have shown that the first flights of all 55 aphid species studied were found to be occurring earlier and 85% of aphids showed increased duration of their flight season. The seasonal timing of these migrations was shown to be statistically linked to a changing temperature – an indication of the impact of a changing climate on pests. Quite surprisingly, aphid abundances generally has been not increasing dramatically with years. Instead, numbers fluctuate widely between years indicating that that there are strong within-season processes that regulate the overall population size.

However, even if the general trend is clear… there are also controversial effects. For example, as also Simon R. Leather wrote in his paper in The Journal of Animal Ecology, aphids Hyalopterus pruni and Aulacorthum solani seem to be becoming less common, and as such, their pest status may change for the better.

Aphids are able to adapt to climate change faster than many other insect groups studied because of their low developmental threshold temperature and high intrinsic rate of increase, but it seems that also their natural enemies adapted to the climate changes or that these trends can be explained by the effect of climate, particularly that related to winter conditions that are still sufficiently cold to overcome the aphid cryodefence.

A further element of interest is related to the frequencies of alata aphids since some aphid species produce few (or none!) alata specimens so that their identification in suction traps scould be difficult. It could be therefore very important to set up plant-based monitoring sites where aphid occurrence on key host plants is run in parallel with existing suction traps.

I read the paper with great interest, but I have not found any data about emerging pests, such as Myzus persicae nicotianae. This subspecies seems to be spreading in some countries (such as Greece) and this particularly concerning for the economic importance of these aphids. Unfortunately, the paper published by Bell and colleagues did not verified this subspecies that can be identified mainly using molecular tools (actually… what about morphometric analyses?). According to an interview to James Bell, these data will be available in the next future….

We’re watching out for new, potentially damaging aphids such as Myzus persicae nicotianae, Diuraphis noxia and Schizaphis graminum sensu stricto, which are important vectors of plant viruses to UK crops.

… in the meanwhile I will continue to check its presece in Italy, where some surprises seems to be present. Stay tuned!

 

 


 

Bell, J., Alderson, L., Izera, D., Kruger, T., Parker, S., Pickup, J., Shortall, C., Taylor, M., Verrier, P., & Harrington, R. (2015). Long-term phenological trends, species accumulation rates, aphid traits and climate: five decades of change in migrating aphids Journal of Animal Ecology, 84 (1), 21-34 DOI: 10.1111/1365-2656.12282

Kati, A., Mandrioli, M., Skouras, P., Malloch, G., Voudouris, C., Venturelli, M., Manicardi, G., Tsitsipis, J., Fenton, B., & Margaritopoulos, J. (2014). Recent changes in the distribution of carboxylesterase genes and associated chromosomal rearrangements in Greek populations of the tobacco aphid. Biological Journal of the Linnean Society, 113 (2), 455-470 DOI: 10.1111/bij.12357

Leather, S. (2015). Onwards and upwards – aphid flight trends follow climate change Journal of Animal Ecology, 84 (1), 1-3 DOI: 10.1111/1365-2656.12314

Aphid vampires!!! When aphids decide to suck ant larvae!!!

I read a lot of papers about aphids (including recent ones about cannibalism in aphids), but the last paper published by David Martinez-Torres surprised me since it reported an unprecedented and absolutely unusual (!) ant–aphid relationship.

Aphids and ants interact frequently in nature and probably their relationship in one of the most studied example of symbiosis. Even if generally ants take care of aphids on plants, it is not so uncommon to find aphids also within the ant nests since some ant species bring aphids or even aphid eggs into their nests in winter, ensuring the continuity of their symbiotic relationship.

Martinez-Torres and his colleagues, decided to study the aphid Paracletus cimiciformis (a species widely distributed across Europe and also has been recorded in Asia and North Africa, in the left photo from Virtual Insectarium) since it possesses two wingless clonal morphs: a trophobiotic morph (called round morph) and an alternative morph (named flat morph). Interestingly, each of these two morphs of P. cimiciformis is able to produce both morphs through parthenogenesis making this a further example of plasticity/polyphenism in aphids.

Looking at the interactions that these two morphs established with ants, Authors observed that ants played a typical behaviour of “solicitation” on aphids of the round morph in order to induce them to excrete honeydew. According to literature data, this is a typical example of trophobiotic association so that aphids produce honey dew and ants protect them from enemies. Differently, they observed antennation and licking toward flat aphids. This is unusual since antennation is involved in many aspects of ant social life such as kin recognition, brood discrimination, and enemy specification whereas licking is a grooming behaviour performed by ants on their larvae and other nest mates. Furthermore, aphids of the flat morph, although able to feed on plants, are brought inside the ant brood chamber where they are cared for by the ants suggesting that the flat morph is successfully mimicking ant larvae. What????

According to chemical analyses, flat morph aphids are brought inside the ant brood chamber since their cuticular “has a typical ant smell”, so that they use a sort of chemical mimicry deceive worker ants and infiltrate their brood chamber. Ok… this is quite (or actually absolutely unusual for aphids), but why aphids should infiltrate in the brood chamber?

Aphids seem to be able to make few actions and probably their most successful one is sucking and… indeed… in the brood chamber flat aphids actively suck hemolymph from ant larvae!

This is an example of aggressive mimicry, but it is unusual since P. cimiciformis can give birth to two alternative morphs with distinct shape, different “smell” and diverse behavioural strategies!

As Authors wrote in their paper published in PNAS at the end of January 2015:

Conventional trophobiotic relationships may provide protection against fungi, excessive moisture, the low temperatures of winter, or the summer droughts, without the need for aphids to evolve complex adaptations to infiltrate the most heavily defended place of an ant nest (the brood chamber). In fact, trophobiosis is widespread among other Fordini species, in which their single wingless root-dwelling morph has been repeatedly reported to overwinter inside ant nests. (…) The results of this study show that the flat morph in P. cimiciformis mimics the cuticular profile of T. semilaeve ant larvae to gain access to its host’s resources in the form of hemolymph of ant larvae. (…) This strategy likely evolved from a pre-existing trophobiotic relationship that has been retained in the alternative round morph. This evolutionary process could have been favored both by a prolonged close association of aphids and their future prey and by a morphological preadaptation for piercing and sucking shared by all aphids, which would have been exapted to feed on larvae.

The flat aphid morphs and the ants can be expected to be engaged in an arms race, with selection favouring improved deceiving abilities in the aphid and increasingly finer discrimination abilities to detect noncolony members in the ants. However, it is also possible that aphid predation is not so costly for ants since a non-destructive larval hemolymph feeding occurs so that, even if flat aphids may represent an additional cost for ants, it seems that it is still an affordable price for ants in view of the supplies of sugar-rich honeydew supplied by the round morph.

It seems therefore that a single aphid species may adopt two evolutionary strategies at disparate points in the mutualism– antagonism continuum since it change from a classical trophobiosis to larval hemolymph feeding making aphids not always the ant’s cows but also “wolf in sheep’s clothing” or better wolf in ant’s clothing!

A new aphid species arrived in Europe

As Carlos Hernández-Castellano and Nicolás Pérez Hidalgo reported in the journal Redia, it seems that a new invasive aphid species arrived in Europe. This aphid, called Sipha flava, is native to North America, although it has achieved to expand throughout South and Central America, where it is known as “the yellow sugarcane aphid,” and is an important pest of this crop leading to yield reduction (photo source here).

The yellow sugarcane aphid is usually lemon yellow, but under some conditions is pale green, it is 2 mm long, covered with short, black spines, and has two double rows of dark spots on its back. Cornicles are very short. Winged and wingless forms live in the colony.

Sugarcane is rather marginal in European continent, so Sipha flava is not expected to become a sugarcane pest in Europe, however, it could be important to map its spread since it may feed on several species from the same family and it is unknown to what extent this aphid species could represent a threat to some crops in Europe, such as rice or corn.

As stated by Authors:

We found four colonies of Sipha on four different plants of the common thatching grass Hyparrhenia hirta (L.) Stapf in Oliver in an organic citrus grove located in La Selva del Camp (Tarragona, NE Spain 41º13’07’’N, 01º08’35’’E) during a sampling campaign (17th June, 2014) in the context of a scientific project about arthropod trophic webs, and two colonies on the same host-plant in Blanes (Gerona 41º40’40’’N, 2º48’22’’E) on 28th June, 2014. The colonies of aphids were attended by the ants Pheidole pallidula Nylander and Plagiolepis pygmaea Latreille in La Selva del Camp and Blanes, respectively.

Interestingly, many predators feed on the yellow sugarcane aphid, but they are rarely parasitized so that ants could protect them from natural enemies.

Few days ago I was at a workshop about the defence of honey bees against the increasing threat of invasive species, a booming phenomenon caused by globalisation, leading not only to agricultural issues but also rising as the second cause of biodiversity loss in the world, just after habitat destruction in importance. It seems that also aphids would like to have a chance for invading new countries!!

The Scent of Fear – the aphid alarm pheromone

Originally posted on Don't Forget the Roundabouts:

We are all familiar with the effects of epinephrine (adrenaline) and norepinephrine (noradrenaline) on us when placed in a position of stress, such as public speaking or even worse danger.  We flush, shake, our heart rate accelerates and many of us we begin to sweat profusely, thus visibly advertising our distress; sometimes embarrassingly so

Sweating nervously

if we have an antiperspirant  fail and happen to be wearing a dark shirt.

man_giving_speech

http://www.silkyskin.co.uk/blog/wp-content/uploads/2012/07/man_giving_speech.jpg

Those seeing these symptoms may feel a degree of sympathy for the victim, but do not usually flee the scene, although they may sometimes feel tempted to do so.

The case with aphids is very different.   Aphids, when perceiving a threat to their neighbours by a predator or parasite, flee the scene rapidly, by flight, if winged, on foot if not, or even by leaping from their host-plant to the ground below.  The pea aphid, Acyrthosiphon pisum walks away or drops from their…

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Transferring primary symbionts: a missed link?

figure 1_Mandrioli_ManicardiOne of the most studied example of symbiotic interaction is related to aphids and their symbiont Buchnera aphidicola  that they host in specialized cells called bacteriocytes. Each aphid may host about 6 millions of Buchnera cells that are involved in the continuous overproduction of tryptophan and other amino acids.

In addition to obligate symbionts, exemplified by Buchnera, aphids contain several facultative bacterial symbionts that are mostly maternally transmitted and that may be readily transferred between hosts in laboratory experiments, since they can also have an independent life in view of their genome that still contain all the genes necessary for growth and replication. In contrast, exclusively maternally transmitted and obligate symbionts, such as Buchnera, have never faced with the challenge of invading new insects since they possess a reduced genome that lost several genes required, for example, for anaerobic respiration, synthesis of amino sugars, fatty acids, phospholipids and complex carbohydrates. As a consequence, Buchnera has resulted in one of the smallest known genomes of any living organism.

Up till now, an unanswered question is related to the extent of the reciprocal coadaptation of host and symbiont lineages and this why I found an intriguing reading the recent paper of Nancy Moran in PNAS related to the chance of transferring Buchnera symbionts between two different aphid lineages. Indeed as Moran and You wrote in their paper:

Potentially, the rapid evolution of symbiont genes and genomes is tracked by adaptive compensatory changes in host genes, accelerating the establishment of incompatibilities between symbiont and host genotypes from different host matrilines. If so, intimate symbioses might facilitate reproductive isolation and speciation. If beneficial symbionts such as Buchnera are generally interchangeable among related host species, this would suggest the lack of an evolutionary “arms race in these mutualistic relationships.

In order to better understand the state-of-art of this symbiotic relationship in aphids, Moran and Yun planned to exchange Buchnera bacteria between two aphid lineages. In parthenogenetic aphid generations, embryos begin development before their mothers are mature, so embryos ready for colonization are present in the injected juvenile aphids. The success of the transfers indicates an ability of the donor Buchnera to invade the posterior syncytium of these developing embryos and to be packaged normally during subsequent development and inherited stably in subsequent generations. In view of this intimate link, Buchnera and aphid matrilines are always strongly dependent.

Immagine 1In order to face this topics, Moran and Yun used two matrilines of the pea aphid Acyrthosiphon pisum, where the recipient line (the clone LSR1) contains a heat-sensitive Buchnera genotype, and the donor (clone 5AY) contains a heat-tolerant Buchnera genotype. In their study, they depleted native Buchnera by heat in the recipient line and donor Buchnera have been microinjected in the hemocoel of the recipient line in order to observe the results (as schematized at left in the image from the Moran paper in PNAS).

As reported in the paper, most embryos have been successfully colonized by the donor symbionts and in some cases, a complete replacement occurs in the progeny of injected females. In other cases, progeny have a mixed Buchnera population, which can be shifted completely to the donor type through further heat exposure. These results are very intriguing this Moran and Yun disrupted 100 million years (∼1 billion aphid generations) of continuous maternal transmission of Buchnera in its specific host aphid lineage showing that symbiotic relationship seems to occur between Buchnera and A. pisum as a whole without any specific genetic difference between aphid lineage genomes and/or in the Buchnera genomes. Lastly, aphids with the Buchnera replacement showed a strong increase in their heat tolerance demonstrating an effect of symbiont genotype on host ecology and the presence of a cross talk between aphids and their new Buchnera cells.

 

ResearchBlogging.orgMoran NA, & Yun Y (2015). Experimental replacement of an obligate insect symbiont. Proceedings of the National Academy of Sciences of the United States of America PMID: 25561531

 

Fertilizers and aphid growth

ResearchBlogging.org Plant vigour, health and growth rate are intensively managed by farmers to maximize production through the application of nitrogen fertilizers that also influence the growth of phytophagous insect populations because nitrogen is a macronutrient known to be limiting for them.

The effects of fertilizers reported in literature are quite controversial since fertilizers can make faster insect population growth, but they can also have detrimental effects to some phytophagous insects possibly as a result of nutrient imbalance. Indeed, most insects actively maintain close to optimal levels of macronutrients in their tissues, so that changing the ratio of macronutrients in plants can affect insect feeding and performance affecting herbivore abundance.

Aphids are important agricultural pests in many crops and, based on observations from both natural and agricultural systems, they seem to be positively affected by the nitrogen amount in the nutritionally poor phloem sap that they consume. Differently to what reported in aphids, chewing insects, such as grasshoppers and moths, are more likely to be negatively affected by increased defensive compounds that they ingest with leaf tissue. The diversity of insect responses to nitrogen that have been observed suggested that additional research in this area is needed to improve crop management.

B74gTdSCUAAhExRAn interesting set of data has been recently published by Kevi C. Mace and Nicholas J. Mills in the journal Agricultural and Forest Entomology studying the response of walnut aphid Chromaphis juglandicola populations to different levels of nitrogen application to walnut seedlings and the relationship between aphid density and chlorophyll content index (CCI), a non-invasive measure of foliar nitrogen.

Although added nitrogen significantly increased soluble nitrogen content, there was no effect on walnut aphid population growth suggesting that walnut aphid population growth on potted seedlings is limited by factors other than soluble nitrogen, such as amino acids. This suggestion is also supported by data assessing that there wasn’t any difference not only in the population growth, but also in aphid weights and in the age structure of the populations. This is an unusual finding because aphids, including some tree aphids, generally show a positive or dome-shaped response (measured either as increased life-history performance in laboratory studies or as greater abundance in field studies) to nitrogen fertilizer.

A relevant role in the regulation of the C. juglandicola growth could be played also by the production of plant defensive compounds so that it is possible that plant defence, rather than plant nutrition, was responsible for the apparent absence of bottom-up effects on walnut aphid populations in the present study because it has been shown that plant defence can vary with level of nitrogen fertilizer. Walnut foliage, for instance, is known to contain juglone, which is toxic to many insects. Being specialists, walnut aphids may even benefit from juglone or possess a sort of resistance so that a further study of defensive compounds and their relationship to fertilizer application and insect populations is needed to determine whether plant defences could drive the dynamics of walnut aphid populations.

The absence of beneficial effects of fertilizers in aphids is also accompanied by the absence of negative effects so that fertilizer management appears unlikely to effectively contribute to the control of C. juglandicola in commercial walnut orchards.

Mace, K., & Mills, N. (2015). Response of walnut aphid populations to increasing foliar nitrogen content Agricultural and Forest Entomology DOI: 10.1111/afe.12103

A Winter’s Tale – aphid overwintering

Originally posted on Don't Forget the Roundabouts:

Aphids that live in temperate or boreal regions have to be able to survive overwinter. Aphids, depending on species, are able to pass winter in two ways. If they are holocyclic i.e. possess an egg-laying stage, they usually overwinter as eggs. Aphid eggs are extremely cold-hardy; they have been reported to have super-cooling points of about -42oC (Somme ). If laid on a woody host, eggs are usually laid in the bud axils as in the case of the apple aphid, Aphis pomi, the black bean aphid Aphis fabae and the bird cherry aphid, Rhopaloishum padi.

aphid eggs

In some instances, such as the sycamore aphid, Drepanosiphum platanoidis, eggs are laid directly on the tree bark or in crevices in the bark or even in lichen growing on the bark.  See if you can spot the eggs in the picture below.

ovipsyc

If however, the aphid in question lives on an herbaceous host, the eggs…

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