Tuberolachnus salignus

Tuberolachnus salignus
	Tuberolachnus salignus, showing dorsal tubercle
Scientific classification
Kingdom:	Animalia
Phylum:	Arthropoda
Class:	Insecta
Order:	Hemiptera
Suborder:	Sternorrhyncha
Superfamily:	Aphidoidea
Family:	Aphididae
Genus:	Tuberolachnus
Species:	T. salignus
Binomial name
	Tuberolachnus salignus; Gmelin, 1790

Tuberolachnus salignus (Gmelin, 1790), known as the giant willow aphid, is a large aphid that belongs in the genus Tuberolachnus. It feeds upon many species of willow (Salix spp.) causing significant damage to the tree.^[1], and produces honeydew has major effects on the honeybees^[2]

Description

Morphology

The adult giant willow aphid is the largest aphid of the 120 species that feed on willow.^[3] with having a body length ranging from 5.0-5.8mm^[4]. The giant willow aphid, as the main suggests, is mainly associated with the branches of willow^[5], particularly the Salix spp. However, it can be found on Populus as well^[6]. The aphid has two forms: apterae (wingless) and alates (winged)^[2]. There is some differentiation between the two forms. Apterae individuals are mid-brown to dark-brown^[6] with several rows of black sclerotic patches^[2] and a large dark brown tubercle in the centre of the dorsum^[6]. The tubercle is in front of the siphunculi that is on dark cones^[2]. Alates individuals have the forewing membrane unpigmented^[6] while the pterostigma (wing markings) are dark brown. The costal margins are also dark brown^[2]. However, both of forms have antennae that are just less than half the body length, and numerous fine hairs on the abdomen to give it a greyish-golden shine^[2]

Feeding

Like most aphids, the giant willow aphid uses their stylet tips to penetrate into the phloem sieve-tubes of their host (willow), where multiple cells are pierced.^[1]. The phloem sap has an increased concentration of sugars and small amounts of amino acids^[7]. The sap also is under turgor pressure, which allows for the aphid to be supplied with large amounts of sap that is swallowed regularly^[1]. Therefore, the aphid would not feed upon dormant willows but will seek out the young willow trees, in which have new phloem sieve-tubes next to the cambium of the secondarily thickened willow stems^[1].

As a result of excess carbohydrates in the aphid from the sugar ingested, they excrete honeydew^[7]. The honeydew from the giant willow aphid contains melezitose^[7]. The production of honeydew does depend upon the season for the aphid due to the monthly changes of sap in the willow tree. As a result, there would be different calorific equivalents of honeydew made^[8].

Genetics

The Tuberolachnus genus contains three species, that all possess a large conical tubercle on the dorsum. However, the species in the genus appear to be more physically similar than genetically similar. Those two species have been placed in a sub-genus of Tuberolachniella^[4]. There is a suggestion that other Asian Salix-feeding species, in the Lachnus genus, are more closely related to the giant willow aphid^[4].

The genetic diversity of the giant willow aphid is low through it being an obligate parthenogen^[9]. There has been only 16 genotypes found in 27 populations in five different countries^[2]; however, a singular colony would have two genotypes, suggesting that once colonizing in an area, the aphid might aggregate^[9]. In the aphid population, there is also no known male individuals found around the world^[2]. The genotypes of the North American population of giant willow aphid dramatically differ from the genotypes of the populations that are found Sweden and Spain^[9]. There appear to be two clusters of genotypes in the populations in the United Kingdom for the individual genotypes^[9]. It is believed, in 2014, that there has only been one genotype that has colonized New Zealand^[2].

Distribution

The giant willow aphid originated in Asia and spread all across the world where willow trees are found^[7], in parks, natural sites, and plantations^[10]. The aphid can be dated back being on continental Europe, Poland, in 1868^[10]. In the United Kingdom, the aphid is found to be on the SCR willow clones in commercial plantings^[3]. The aphid has been said to be everywhere but Australasia^[6], but in 2013 it arrived in New Zealand and Australia in 2014^[11].

The first detection in New Zealand was in Central Auckland on a Crack Willow (Salix fragilis) in December 2013^[12]. The Ministry for Primary Industries High Risk Surveillance Program, from southeast Auckland, picked up a different specimen in Northland that had been detected^[12]. The aphid has now spread throughout the North and South Island^[4]. The first detection in Australia happened in early 2014 in Tasmania. The aphid, shortly after, was detected in Australian Capital Territory, New South Wales, and Victoria^[4]. However, there has been some speculation that the aphid could have been present in New South Wales four to five years prior to this detection^[4]

The aphid has been recorded to be a mobile species^[9], through the alates individuals able to fly to new areas if the colony gets overcrowded to find a new host^[10]. Additionally, it is suggested that the aphid has had help from trading of timber^[13]

Life Cycle

The giant willow aphid is completely asexual species, known as parthenogen, with no sexual morphs known to be present anywhere.^[6]. The aphid does not have overwinter eggs^[3] or the inability to hibernate^[14], through the lack of sexual forms^[3]. Overwinter, the aphid will survive on two species of willow (S. lasiandra and S. schwerinii) in small clusters behind the stems and petioles^[14]. However, the population will deplete virtually to zero^[14]. The aphids have been seen active in the United Kingdom through the frosts and heavy snow^[4]

As the days get warmer, the adults will give birth to nymphs.^[2]. The development of the nymph takes around 196 degree days with a threshold temperature of 5.5°C to reach maturity^[3]. The optimal temperature for development is 20°C^[4]. At a temperature at 17.5°C to 22.5°C, there is a two to three week generation time for the species^[4]. At the start of summer, it is possible to find the aphids at the base of the tree trunk and move up the stems^[2]. Once on the stems, the population in that cluster will rise rapidly to form dense colonies on the branches until autumn, even through the willow being a poor host^[3]. The aphid population can deplete the host of its resources based upon the size and how early the colony develops; therefore, affecting the quality later on in the season^[14]. The aphid colonies will persist throughout autumn^[2] with the population slowly reducing^[14]

The alate individuals have been more likely to form with insufficient nutrients from the food supply.^[10]. These forms are less fecund than the apterous individuals^[3], where the alate individuals produce around 34 nymphs^[2] while the apterous individuals produce 70-80 nymphs^[10]. The reproductive period of the alate individuals are 30% shorter than the apterous individuals^[10]. However, the alate colonies are found higher in the trees, around 3.5 meters above the ground^[2]

Ecology

Effects on Willow

The giant willow aphid is a pest species that affect willow trees.^[7]. Willow trees are used for biomass production, bioremediation, erosion, and soil nutrient management^[15]. Many farmers have been using willow as it is easily planted, and can be used for slope protection and an additional feed source, especially during drought events^[4]

The aphid is found to be 50 species of willow.^[7] and one species of poplar species^[14]. However, there are some species of willow (Salix alba, S. fragilis, S. viminalis, S. schwerinii, S. miyabeana, S. matsudana) that the aphid grow faster on than others^[2], but is known to colonies both tree and osier willows^[4]. The aphid, in 2016, has been the cause of death for a shrub willow species at a New Zealand nursery plantation^[4]

The main affect the aphid has on the willows is lowering their health. An infested willow will increase their photosynthetic rate, leaf nitrogen, their water use, and reduce their shoot and root biomass, and growth the following year. However, this can cause stress to the tree^[2]; therefore, allowing secondary pathogens to infect the tree^[4]. An example, is the finding of fungi, Botryospaeria parva (Pennycook & Samuels), on a S. caprea that had been previous infestation of the aphid in New Zealand. As a result, the tree had many dead stems, including the main stem, within the next two months^[4]. The aphid is also known to be the cause for a large scale mortality in the Himachal Pradesh State (North India) plantation in 2001–2002, with infestation on the willows ranging from 40 to 100% of the plantation^[2].

The root biomass of the willow is commonly used for the rural stabilization of the soil terrestrially and along the riverbanks.^[16]. A lot of river systems in New Zealand are dependent on willows to prevent erosion from the banks. With successive defoliations, there will be major affects upon the riverbanks. The early 2000s in New Zealand saw the willow sawfly, Nematus oligospilus, which caused disruption to the rivers previously mentioned^[2]. The roots do not establish from the infestation through the inability of the sugars able to get to the roots, resulting in the roots unable to grow^[2]. The inability to grow roots affect the survival of an infested tree^[9], as well as post-planting survival rate if nursery willows^[4]

Another major affect the aphid has on the willow tree is delaying flowering in the flowers. The willow tree flowers are used as a source of protein for honey-bees in early spring. However, the aphids affected the flowering of the trees through delaying the flowering, extending the time that they flowered, decreased the size of the catkin, but increased the number of catkins and total floral output.^[15]

There are some species of willow that are resistant to the giant willow aphid (S. eriocephala and S. lasiolepis x S. viminalis).^[7]

Economic Effects

Honeydew

Through the production of honeydew, the giant willow aphid is affecting the production of honey and health of the honeybee. The aphid's honeydew has melezitose sugar that crystallizes the honey (cement honey) more readily, meaning that the comb would need to be heated for it to be extracted^[2]. Therefore, the honeydew is increased economic impacts^[7] on the honey collecting process, as well as causing a problem with the taste of the honey from increased phenol levels^[2].

The honeybees (Apis mellifera) cannot utilise the melezitose sugar.^[2] and is considered to be a poor feed quality for them^[7]. The sugar produced in the honeydew is linked to dysentery, abdominal swelling, reduced mobility, and low overwintering survival in the honeybees^[7]. As mentioned previously, the aphids effect the willows pollen and nectar production, which is the main source for the honey-bees in spring; therefore, affecting the ability of making quality and cost of the honey lower^[7]

The vespid wasp feed upon the honeydew of the aphids.^[2], resulting in there being an increased wasp population in the rural and urban areas, creating an increase nuisance and public health risk^[16]. The wasps can reduce the population of bees through competition for food and attacking bees^[7], and other beneficial insects^[2], as well as being a risk to livestock and humans being stung^[4]

The main concern that farmers would have is the black sooty mould that is produced from the excess honeydew. The mould grows on the leaves, stems, and soil surface below the aphid colonies.^[15]. For the soil microbes, an energy-rich source is provided from the aphid's honeydew. The increase in the microbes, leads to increased soil enzyme activities and effects the meso-fauna microbivores and those predators^[15]. The black sooty mould, however, reduces the commercial value of orchard's fruit if the fruit gets stained by the honeydew^[10]. The honeydew is also a problem to livestock through it getting stuck in the wool and causing the wool to stick together, as well as debris sticking to it^[10]; therefore, causing the price of the wool to go down^[4]

Control

Biological Control

Fungi

A major pathogen to the giant willow aphid is a fungus, Neozygites turbinata (Kenneth), that is found in the United Kingdom, central Europe, Israel, and North America.^[4] (In California, United States and British Columbia, Canada)^[4]. N. turbinata is an entomopathogenic fungus that has caused significant to the populations of the giant willow aphid^[9]. An outbreak of the fungus occurred in Slovakia in 2001 where the populations of the aphid eliminated almost all of them^[4]. The fungus attack the aphid internally^[2] through the proboscis, where their bodies will be filled with black spores and are released years later from the liquefied aphid cadavers^[10]

Parasitoids and Predators

Throughout the world, there are many parasitoids that attack the giant willow aphid. In Japan, the aphid is parasitized by the Braconid Wasp, Aphidius salignae^[2]. In India, the generalist parasitoid Lipolexis oregmae (Gahan), feed upon the giant willow aphid but is an uncommon association^[4].

There are a few predators that feed upon the aphid. In Israel, the maggots of the predaceous midge, Aphidoletes aphidimyza, feed on the aphid and are commonly used to defend greenhouse crops in Europe.^[4]. Only one bird, Australian Silvereye (Zosterops lateralis Latham) has been shown to feed upon the aphid^[10]. However, there has been reports of the New Zealand Tūī (Prosthemadera novaeseelandiae (Gmelin)) and Bellbird (Anthornis melanura (Sparman)) have feed on the honeydew of the aphid resulting in some casualties of the aphid^[4]. The aphid has also been found in the stomachs in one bat species, Pipistrellus pygmaeus (Leach), within riparian areas^[10]

Pauesia

There are two parasitoid wasps that host specific to the giant willow aphid. One of these wasps is Pauesia salignae (Watanabe). P. salignae is found in Japan.^[2], India, Korea, Taiwan, and the United States^[4]. P. salignae is also predated on by two other hyperparasites called Dendrocerus carpenteri and D. ramicornis^[2]

The other parasitoid wasp is P. nigrovaria (Provancher) and this species has been approved to be released in New Zealand to combat the giant willow aphid outbreak^[17]. This wasp is found from British Columbia to Canada, which have a similar climate and latitudinal range as found in New Zealand, a contributing reason for the decision of the release to the country^[16].

Ladybirds

Several generalist ladybirds have been observed feeding upon the giant willow aphid. However, these ladybirds are generalist species that will feed on a larger range than just the giant willow aphid.^[16]. The tortoise shelled-ladybird (Harmonia testudinaria Mulsant) feeds upon the aphid in Australia^[4]. In New Zealand, there are a few known species to feed upon the aphid, including the two-spot ladybird (Adalia bipunctata Linnaeus), the eleven-spot ladybird (Coccinella undecimpunctata L.), and the large spotted ladybird (Harminia conformis Boisduval)^[4]

Another ladybird that feeds on the giant willow aphid is the harlequin ladybird (Harmonia axyridis Pallas)^[16]. The harlequin ladybird is native to east Asia but does not have an overlapping range in both of their natural range. However, there is an association in populations in Europe^[11]. The ladybird, however, has become a pest overseas through it displacing the native ladybirds and can build up large populations quickly and being a generalist feeder^[4]. The harlequin ladybird does feed upon the giant willow aphid, but it results in the ladybirds having low weights and survival rate through the likelihood of committing cannibalism if they have too low of aphids to feed upon^[11]. Additionally, the ladybird prefers to feed on other soft-body insects, such as the green peach aphid (Myzus persicae Sulzer)^[11].

Chemical Controls

Using chemicals to control the giant willow aphid should only be used as a short-term solution in specific locations, through build-up of honeydew attracting wasps, thus leading to a human-health risk. The insecticides that kill the aphids, would not work on the wide-scale and can potentially affect the non-target insects, such as honey-bees, that use the willow tree^[4]. The best chemical approach to the aphids would be to use systemic insecticides that are friendly towards the bees; however, they could be difficult for the effectiveness of the sprays to be established on the willow^[2].

References

↑ ^1.0 ^1.1 ^1.2 ^1.3 Mittler, T. E. (1957-09-01). "Studies on the Feeding and Nutrition of Tuberolachnus Salignus (Gmelin) (Homoptera, Aphididae): : 1. the Uptake of Phloem Sap". Journal of Experimental Biology. 34 (3): 334–341. doi:10.1242/jeb.34.3.334. ISSN 0022-0949.
↑ ^2.00 ^2.01 ^2.02 ^2.03 ^2.04 ^2.05 ^2.06 ^2.07 ^2.08 ^2.09 ^2.10 ^2.11 ^2.12 ^2.13 ^2.14 ^2.15 ^2.16 ^2.17 ^2.18 ^2.19 ^2.20 ^2.21 ^2.22 ^2.23 ^2.24 ^2.25 ^2.26 ^2.27 ^2.28 McIvor. I. (2014, March). Tuberolachnus salignus the great willow aphid. Plant and Food Research. https://www.giantwillowaphid.co.nz/__data/assets/pdf_file/0005/62591/McIvor_Tuberolachnus_salignus.pdf
↑ ^3.0 ^3.1 ^3.2 ^3.3 ^3.4 ^3.5 ^3.6 Collins, C.; Leather, Simon R. (2013-01-01). "Effect of temperature on fecundity and development of the Giant Willow Aphid, Tuberolachnus salignus (Sternorrhyncha: Aphididae)". EJE. 98 (2): 177–182. doi:10.14411/eje.2001.033. ISSN 1210-5759.
↑ ^4.00 ^4.01 ^4.02 ^4.03 ^4.04 ^4.05 ^4.06 ^4.07 ^4.08 ^4.09 ^4.10 ^4.11 ^4.12 ^4.13 ^4.14 ^4.15 ^4.16 ^4.17 ^4.18 ^4.19 ^4.20 ^4.21 ^4.22 ^4.23 ^4.24 ^4.25 ^4.26 ^4.27 Sopow, Stephanie L.; Jones, Trevor; McIvor, Ian; McLean, John A.; Pawson, Stephen M. (2017). "Potential impacts of Tuberolachnus salignus (giant willow aphid) in New Zealand and options for control". Agricultural and Forest Entomology. 19 (3): 225–234. doi:10.1111/afe.12211. ISSN 1461-9563. Unknown parameter |s2cid= ignored (help)
↑ Cranshaw, Whitney (2018). Garden insects of North America : the ultimate guide to backyard bugs. David J. Shetlar, Whitney Preceded by: Cranshaw (Second ed.). Princeton, N.J. ISBN 978-1-4008-8894-8. OCLC 1002303962. Search this book on
↑ ^6.0 ^6.1 ^6.2 ^6.3 ^6.4 ^6.5 Blackman, R. L. (1994). Aphids on the world's trees : an identification and information guide. V. F. Eastop, C.A.B. International, Natural History Museum. Wallingford: CAB International in association with the Natural History Museum. ISBN 0-85198-877-6. OCLC 30971263. Search this book on
↑ ^7.00 ^7.01 ^7.02 ^7.03 ^7.04 ^7.05 ^7.06 ^7.07 ^7.08 ^7.09 ^7.10 ^7.11 Tun, Kyaw Min; Minor, Maria; Jones, Trevor; Clavijo McCormick, Andrea (2020-12-12). "Effect of willow cultivar and plant age on the melezitose content of giant willow aphid ( Tuberolachnus salignus ) honeydew". Agricultural and Forest Entomology. 23 (3): 261–268. doi:10.1111/afe.12428. ISSN 1461-9555. Unknown parameter |s2cid= ignored (help)
↑ Llewellyn, M.; Rashid, R.; Leckstein, P. (1974). "The Ecological Energetics of the Willow Aphid Tuberolachnus salignus (Gmelin); Honeydew Production". Journal of Animal Ecology. 43 (1): 19–29. doi:10.2307/3155. ISSN 0021-8790. JSTOR 3155.
↑ ^9.0 ^9.1 ^9.2 ^9.3 ^9.4 ^9.5 ^9.6 Aradottir, Gudbjorg I.; Hanley, Steven J.; Collins, C. Matilda; Dawson, Kevin J.; Karp, Angela; Leather, Simon R.; Shield, Ian; Harrington, Richard (May 2012). "Population genetics of Tuberolachnus salignus, an obligate parthenogenetic aphid". Agricultural and Forest Entomology. 14 (2): 197–205. doi:10.1111/j.1461-9563.2011.00559.x. Unknown parameter |s2cid= ignored (help)
↑ ^10.00 ^10.01 ^10.02 ^10.03 ^10.04 ^10.05 ^10.06 ^10.07 ^10.08 ^10.09 ^10.10 Bochniarz, Alina (2020). "Giant willow aphid (Tuberolachnus salignus Gmelin, 1790) - a literature review". Polish Journal of Agronomy. 43: 113–124. doi:10.26114/pja.iung.449.2020.43.11.
↑ ^11.0 ^11.1 ^11.2 ^11.3 Tun, Kyaw Min; Clavijo McCormick, Andrea; Jones, Trevor; Minor, Maria (2020-06-01). "The potential of harlequin ladybird beetle Harmonia axyridis as a predator of the giant willow aphid Tuberolachnus salignus: voracity, life history and prey preference". BioControl. 65 (3): 313–321. doi:10.1007/s10526-020-10010-5. ISSN 1573-8248. Unknown parameter |s2cid= ignored (help)
↑ ^12.0 ^12.1 Gunawardana, D; Flynn, A; Pearson, H; Sopow, S (December 2014). "Giant willow aphid: a new aphid on willows in New Zealand". Surveillance (Wellington). 41 (4): 29–30 – via Ministry for Primary Industries.
↑ Fang, Fang; Chen, Jing; Jiang, Li-Yun; Chen, Rui; Qiao, Ge-Xia (2017). "Biological traits yield divergent phylogeographical patterns between two aphids living on the same host plants". Journal of Biogeography. 44 (2): 348–360. doi:10.1111/jbi.12818. ISSN 1365-2699. Unknown parameter |s2cid= ignored (help)
↑ ^14.0 ^14.1 ^14.2 ^14.3 ^14.4 ^14.5 Tun, Kyaw Min; McCormick, Andrea Clavijo; Jones, Trevor; Minor, Maria (2021). "Seasonal abundance of Tuberolachnus salignus and its effect on flowering of host willows of varying susceptibility". Journal of Applied Entomology. 145 (6): 543–552. doi:10.1111/jen.12866. ISSN 1439-0418. Unknown parameter |s2cid= ignored (help)
↑ ^15.0 ^15.1 ^15.2 ^15.3 Tun, Kyaw Min; Clavijo McCormick, Andrea; Jones, Trevor; Garbuz, Stanislav; Minor, Maria (August 2020). "Honeydew Deposition by the Giant Willow Aphid (Tuberolachnus salignus) Affects Soil Biota and Soil Biochemical Properties". Insects. 11 (8): 460. doi:10.3390/insects11080460. PMC 7469182 Check |pmc= value (help). PMID 32707954 Check |pmid= value (help).
↑ ^16.0 ^16.1 ^16.2 ^16.3 ^16.4 New Zealand Forest Research Institute Limited. (2019, June 28). To obtain approval to release new organisms (APP203853). Retrieved from Ministry for Primary Industries https://www.epa.govt.nz/assets/FileAPI/hsno-ar/APP203853/66e04c0700/APP203853-Application.pdf
↑ Environment Protection Authority. (2019, November 29). APP203853 Decision [Report]. Ministry for Primary Industries. https://www.epa.govt.nz/assets/FileAPI/hsno-ar/APP203853/APP203853_Decision.pdf