InfluentialPoints.com
Biology, images, analysis, design...
Aphids Find them How to ID AphidBlog
"It has long been an axiom of mine that the little things are infinitely the most important" (Sherlock Holmes)

 

 

Aphis (Toxoptera) aurantii

Camellia aphid, Black citrus aphid, Tea aphid

On this page: Identification & Distribution  Biology & Ecology  Damage & Control 

Identification & Distribution:

Adult apterae of Aphis (Toxoptera) aurantii are oval, shiny black, brownish-black or reddish brown in colour with rather short black-and-white banded antennae. The antennal terminal process is more than 3.5 times the length of the base of the last antennal segment (cf. Aphis gossypii  which has the terminal process less than 3.5 times longer than the base of the last antennal segment). The cauda and siphunculi are black, and the siphunculi are 1.0-1.5 times the length of the cauda. The cauda usually has less than 20 hairs (cf. Aphis (Toxoptera) citricidus which usually has more than 20 hairs on the cauda). A stridulatory apparatus is present below and in front of the siphunculi. The body length of Aphis (Toxoptera) aurantii apterae is about 2 mm long.

Alates (see second picture above) have the head and pterothorax blackish. The abdomen has dusky paired marginal sclerites on segments 2-5 inclusive, a pair of large postsiphuncular sclerites, and transverse dark bands across tergites 7-8 and sometimes also on tergite 6. Their siphunculi are 1.25-1.65 times as long as the cauda.

The clarified slide mounts below are of adult viviparous female Aphis (Toxoptera) aurantii : wingless, and winged.

Micrograph of clarified mounted  aptera (first image) courtesy PaDIL.  Copyright Simon Hinkley & Ken Walker (Museum Victoria) under Commons Attribution 3.0 Australian License.  Alate micrograph (second image) courtesy Favret, C. & G.L. Miller, AphID.  Identification Technology Program, CPHST, PPQ, APHIS, USDA; Fort Collins, CO.

The black citrus aphid is found on the underside of leaves of Citrus, as well as tea (Camellia), coffee (Coffea) and mango (Mangifera). Infestation in spring can be very harmful to citrus crops. In temperate countries Aphis (Toxoptera) aurantii is a pest of ornamental Camellia bushes. Sexual forms are unknown, and aphids overwinter as viviparae. Adults stridulate by rubbing tibial spines on abdominal striae. Their distribution is now cosmopolitan.

Biology & Ecology

Life cycle

Wang & Tsai (2001)  looked at development, survival and reproduction of black citrus aphid in relation to temperature. Lower and upper temperature thresholds were 4 and 35°C. Between 7 and 32°C, developmental periods of immature stages varied from 44.2 days at 7°C to 5.3 days at 28°C. Overall immature development required 129.9 degree-days above 3.8°C. Immature survivorship varied from 82.1 to 97.7% within the temperature range of 10-30°C. However, immature survivorship was reduced to 26.3% at 7°C and 33.1% at 32°C. Mean adult longevity was the longest (44.2 days) at 15°C and the shortest (6.2 days) at 32°C. The predicted upper temperature limit for adult survivorship was at 32.3°C.

Total nymph production increased from 16.3 nymphs per female at 10°C to 58.7 nymphs per female at 20°C, declining to 6.1 nymphs per female at 32°C. The estimation of lower and upper temperature limits for reproduction was at 8.2 and 32.5°C, respectively. The population reared at 28°C had the highest intrinsic rate of increase (0.394), the shortest population doubling time (1.8 days), and shortest mean generation time (9.5 days) compared with the populations reared at six other temperatures. The population reared at 20°C had the highest net reproductive rate (54.6). The theoretical lower and upper temperature limits for population development, survival and reproduction were estimated at 9.4 and 30.4°C, respectively.

Behaviour

Han & Chen (2012)  investigated the attraction of Aphis (Toxoptera) aurantii to different colours and volatile compounds from tea shoots. Fourteen compounds were identified using gas chromatography-mass spectrometry from headspace samples of intact tea shoot volatiles. Electrophysiological and behavioural responses of winged tea aphids to intact tea shoot volatiles as well as to the full blend of 14 synthetic compounds, to a partial mixture of green leaf volatiles included in the 14 compounds, and to individual synthetic compounds were studied by using electroantennography and a Y-tube olfactometer. The various tea volatiles and blends were strongly active, with intact tea shoot volatiles being the strongest. In the greenhouse and in tea plantations, sticky boards of six different colours strongly attracted tea aphids in flight, with "rape-flower yellow" and "Chinese olive-yellow-green" being the most attractive. Furthermore, the two boards in combination with intact tea shoot volatiles attracted winged tea aphids more strongly than their corresponding collared sticky boards alone. In the greenhouse, plastic models of tea seedlings baited with Z-3-hexen-1-ol or the green leaf volatiles mixture significantly attracted winged tea aphids in flight. This study demonstrates that green leaf volatiles from tea shoots are attractive to the tea aphid. The combination of these volatiles with the color light yellow or green, and the shape of tender tea shoots, result in orientation flight and landing of winged tea aphids on host tea shoot

The black citrus aphid is the only species of aphid known to produce audible sound. Broughton & Harris, 1971  report that it produces a distinct scraping sound by rhythmic movements of whole colonies. During one recording the aphids stridulated 15 times in 21 seconds, giving an average period of 1-4 seconds between emissions. This rate remained virtually constant for at least an hour. Analysis of the recording established a clear peak frequency band at about 4-6 kHz with another around 800 Hz-1 kHz and possibly another in the ultra-sonic range above 18 kHz. Stridulation may function as a defence mechanism or as a means of intraspecific communication.

Ant attendance

Rosen (1967)  looked at the relationships between ants and parasites of coccids (=scale insects) and aphids on citrus. A total of eight ant species were recorded attending Aphis (Toxoptera) aurantii. However, no especially aggressive species of ants were recorded, and natural enemies usually exterminated ant-attended colonies of the aphid (see picture above).

We have found Aphis (Toxoptera) aurantii colonies on Camellia in East Sussex, England, to be closely attended by the black garden ant Lasius niger (see picture above).

Natural enemies
Firempong & Kumar (1975)  studied the natural enemies of the black citrus aphid on cocoa in Ghana. The aphid was found to be attacked by the parasite Pseudendaphis, the syrphid predators, Paragus tibialis and Paragus sp., the coccinellids Platynuspsis ferrugineus and Scymnus scapuliferus and a larval chrysopid Chrysops [Note: some of these seem to have changed their names over the years]. The syrphid and coccinellid predators were found to be more active during the day than at night, and their searching paths were concentrated along the veins of the undersurface of leaves where the aphids tend to aggregate. A close synchronization between the appearance of the predators and the inception of aphid colonies was observed. Syrphids were found to appear earlier in aphid colonies than the coccinellids. It was found that syrphids tended to lay more eggs in aphid colonies with higher numbers of individuals. It was also found that the three groups of predators could occur simultaneously in one aphid colony, in which case their predatory action occurred in concert. The aphids exhibit no defensive mechanism against the syrphids but against the coccinellids they avoid captures - mainly by moving away from the predators. A brown sticky secretion exuded from the cornicles (=siphunculi) of the aphid when it was pinched or grabbed by a predator, although the secretion was not thought to have any offensive or defensive functions.

Tremblay (1967)  examined the natural parasitoid complex of Aphis (Toxoptera) aurantii in the Mediterranean area on the basis of samples collected in South Italy and Lebanon. Ten Ichneumonoid species of the genera Aphidius, Diaeretiella, Ephedrus, Lipolexis, Lysiphlebus, Praon and Trioxys presently belong to the complex. Of these, Aphidius colemani, in spite of its wide distribution in the Mediterranean region, seems to be restricted to Israel and Lebanon as a Toxoptera aurantii parasitoid. The nearctic species Lysiphlebus testaceipes is localized in Spain, South France, Corsica, Central and South Italy, including Sicily. In Italy, this endoparasitoid has heavily interfered with the local dominant congeneric species Lysiphlebus confusus and Lysiphlebus fabarum.

The possible associative relationships between Lysiphlebus testaceipes and Lysiphlebus fabarum have been examined in the samples collected in South Italy. The results of the examination suggest that the 2 species are negatively associated with each other. Moreover, the data concerning the relative abundance of both species in the same area indicate that a shift may have occurred in favour of Lysiphlebus testaceipes between 1977 and 1978, with the nearctic parasitoid seemingly able to displace the two local Lysiphlebus species.

 

Damage and control

In tropical regions, Aphis (Toxoptera) aurantii is polyphagous, attacking tea (Camellia), coffee (Coffea), mango (Mangifera) and anone (Annona) plants. In countries with a Mediterranean climate, Aphis (Toxoptera) aurantii is virtually monophagous, attacking virtually only citrus (although sometimes Pittosporum). In the spring, the black citrus aphid is very harmful to citrus fruits, causing flower buds to drop off. The abundant honeydew it produces attracts ants and allows the development of sooty moulds.

In temperate climates, colonies of Aphis (Toxoptera) aurantii causes severe curling of the leaves of ornamental Camellia plants (see picture below).

Stary et al (1988).   discussed the biocontrol of aphids by the introduced Lysiphlebus testaceipes in Mediterranean France. The parasitoid was introduced from Cuba (via Czechoslovakia) to Southern France in 1973/74 to control the exotic aphids Aphis (Toxoptera) aurantii and Aphis citricola on citrus. Research until 1986 showed that Lysiphlebus testaceipes had established over the whole of Mediterranean France (as well as Spain, Portugal, and most of Italy to Sicily). Apart from high effectiveness upon the target species (albeit incomplete parasitism on Aphis citricola) Lysiphlebus testaceipes has become the predominant parasitoid of a number of indigenous pest aphids and indifferent species in all environments from agroecosystems to climax ecosystems (forests). Oligophagy of the species is considered rather useful due to the phenology (=seasonal variation) of its particular host species that manifest considerable seasonal succession. The effectiveness of Lysiphlebus testaceipes as well as the value of the biocontrol project for the whole Mediterranean area are discussed.

Acknowledgements

We have made provisional identifications from high resolution photos of living specimens, along with host plant identity. In the great majority of cases, identifications have been confirmed by microscopic examination of preserved specimens. We have used the keys and species accounts of Blackman & Eastop (1994)  and Blackman & Eastop (2006)  supplemented with Blackman (1974) , Stroyan (1977) , Stroyan (1984) , Blackman & Eastop (1984) , Heie (1980-1995) , Dixon & Thieme (2007)  and Blackman (2010) . We fully acknowledge these authors as the source for the (summarized) taxonomic information we have presented. Any errors in identification or information are ours alone, and we would be very grateful for any corrections. For assistance on the terms used for aphid morphology we suggest the figure  provided by Blackman & Eastop (2006).

Useful weblinks 

References

  •  Broughton, W.B. & Harris, K. M. (1971). First recording of the sound produced by the black citrus aphid, Toxoptera aurantii (Boy.). Bulletin of Entomological Research 60(4), 559-563. Abstract 

  •  Firempong, S. & Kumar, R. (1975). Natural enemies of Toxoptera aurantii (Boy.) (Homoptera: Aphididae) on cocoa in Ghana. Biological Journal of the Linnean Society 7, 261-292.  Full text 

  •  Han, B. & Chen, Z. (2012). Attraction of the tea aphid, Toxoptera aurantii, to combinations of volatiles and colours related to tea plants. Entomologia Experimentalis et Applicata 144(3), 258-269. Full text 

  •  Rosen, D. (1967). On the relationship between ants and parasites of coccids and aphids on citrus. Beitr. Ent. 17(6), 281-286. Full text 

  •  Stary et al. (1988). Biocontrol of aphids by the introduced Lysiphlebus testaceipes (Cress.) (Hym., Aphidiidae) in Mediterranean France. Journal of Applied Entomology 105 (1-5), 74-87. Abstract 

  •  Tremblay, E. (1984). The parasitoid complex [Hym.: Ichneumonoidea] of Toxoptera aurantii [Hom.: Aphidoidea] in the Mediterranean area. Entomophaga 29(2), 203-209. Abstract 

  •  Wang, J.J. & Tsai, J.H. (2001). Development, survival and reproduction of black citrus aphid, Toxoptera aurantii (Hemiptera: Aphididae), as a function of temperature. Bulletin of entomological Research 91(6), 477-487. Abstract