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Hormaphidinae : Nipponaphidini : Neonipponaphis shiiae
 

 

Neonipponaphis shiiae

Japanese chinquapin aphid

On this page: Identification Biology & Ecology Hosts Other aphids on the same host

Identification

Adult apterae of Neonipponaphis shiiae on their secondary host are small, sessile and aleyrodiform (=whitefly larva shaped). They are blackish-brown to almost black, with a reddish tinge, and many long fine dorsal hairs (see first image below). There appear to be several small distinct areas of wax production in both immatures and adults, albeit there is little wax on the adult apterae (possibly due to ant-attendance). The body is circular, a little depressed, and flattened on the dorsum. The antennae are slender, nearly as long as the distance between them, but do not reach fore-coxae. Antennal segment III is fused with segment IV, and not well defined from segment II (but distinct in early instars). The eyes consist of triommatidia. The apical rostral segment is 1.8 times the second hind tarsal segment. The cephalic, thoracic, and first abdominal tergites are fused to form a prosoma (=cephalothorax), which has many fine hairs scattered on the dorsum, about 3 or 4 times as long as the middle diameter of antennal segment III. There are also many subcircular or oval pustules on the prosoma, those around the anterior thoracic spiracles being much smaller, conical, pointed and dark. (cf. Neonipponaphis pustulosis, where those around the anterior thoracic spiracles are oval or rounded). Posterior abdominal tergites II–VII are fused, forming an abdominal plate, but distinctly separated from the (much larger) prosoma by a pale membranous furrow (cf. Nipponaphis spp., where they are not distinctly separated, at least in the medial area). The abdominal plate has about 5 submarginal hairs in a row along each lateral margin, a pair of hairs near the hind margin, and about 17 scattered hairs. Siphunculi are small. The cauda is dusky, constricted basally and broadly rounded at the hind margin. The anal plate is dusky and bilobed. The body length of adult Neonipponaphis shiiae apterae is 1.3-1.7 mm.

The images below show (1) a live adult aptera on its secondary host, (2) a clarified mount thereof, and (3) live mid-instar immatures - one bearing, what appears to be, a cecidomyiid egg.

First and third images above by permission copyright Aoki & Kurosu (2022);
Second image copyright Chen & Qiao (2012), Creative Commons Attribution 3.0.

Neonipponaphis shiiae on their secondary host produce alatae in May. Originally assumed to be secondary migrants, these are now believed to be sexuparae (Aoki & Kurosu, 2022) - viviparous alate secondary migrants are perforce unknown. The body and wings of sexuparae are dark metallic blue in life (see first picture below). In clarified slide mounts they are black, with dusky wings and a dark pterostigma. The head has 12-15 large hairs scattered on the posterior dorsum. The antennae are stout, shorter than half the body length. Secondary rhinaria are distributed 27 on antennal segment III, 13 on segment IV, and 5-6 on segment V. The apical rostral segment is about as long as the second hind tarsal segment, with very long apical primary hairs as in Nipponaphis. The wings are reticulated. On the forewing the pterostigma is broadly rounded at the hind margin, the anal vein (Cu1b) is much thicker than the cubitus, and the media is once branched. The hind wing has two obliques. The abdomen has many dorsal hairs. The siphunculi are small at the apex, but have a much-expanded base, with distinct minute papillae. Tergite VII has 2-4 rather large sclerites and 4 hairs, and tergite VIII is sclerotized on the dorsum and bears 10 long hairs. The cauda is very short, constricted basally, and has 4 or 5 long hairs on each side. The anal plate is divided, with 7 long hairs on each lobe. Body length of the Neonipponaphis shiiae sexupara is about 2 mm.

The images below show an adult alate sexupara, and a fourth-instar nymph thereof.

Both images by permission copyright Aoki & Kurosu (2022).

In first-instar nymphs of apterous viviparae (see first picture below) the tergites have long, stout setae, but no distinct wax plates. (cf. Metanipponaphis spp., where tergites have short thin setae and well-developed wax plates). The first-instar nymphs of sexuales (see second picture for male, third picture for ovipara) have 4-segmented antennae with four short apical setae, a short rostrum (compared to a normal nymph), spinal and marginal rows of small wax plates on the tergites, and a pair of small siphunculi on abdominal tergite VI (normal first instars have more distinct siphunculi). Neonipponaphis shiiae males can develop to adulthood without taking food, after only two moults.

First image by permission copyright Aoki & Kurosu,
Second and third by permission copyright Aoki & Kurosu (2022).

The adult male has a slender body, 0.54 mm long. The antennae are 4-segmented. Antennal segment III is clearly longer than IV, and bears 4–6 small ellipsoid secondary rhinaria. Antennal segment IV has 5 or 6 secondary rhinaria of similar shape, with 4 short hairs at the apex, but without basal hairs. The rostrum is short, not reaching the mid-coxae. The tibiae have 2 apical setae, one of which is short and spine-like on the hind leg. The tarsi are 2-segmented; segment I has a pair of long pointed hairs and, on fore and mid legs, a shorter sense peg between the hairs; segment II has 3 pairs of hairs apically and a pair of hairs mid-dorsally. On the hind leg empodial setae are capitate, extending beyond the apices of the claws. The tergites are without wax plates. The siphunculi are ring-like. The cauda is spinose, with a pair of short hairs. The anal plate is bilobed, with 5 pairs of short hairs.

The adult ovipara has not yet been described, but is probably quite small. None of the immatures obtained by Aoki & Kurosu moulted to second instar - perhaps because, unlike the males, they needed to feed. If so, they may require a suitable primary hostplant.

Neonipponaphis shiiae is thought to be a host-alternating aphid, albeit only known from its secondary hosts, chinquapin (Castanopsis spp.). Colonies occur on twigs, are usually ant attended, earth-tented and persist year-round. Sexuales (males and immature oviparae) are only known via culture of alate sexuparae. The Japanese chinquapin aphid has only been recorded from Japan and some of its islands.

 

Biology & Ecology:

Hosts

The primary host of Neonipponaphis shiiae is unknown, but circumstantial evidence suggests Distylium racemosum as the most plausible.

It is assumed that, like other host-alternating Nipponaphidini whose primary hosts are known, Neonipponaphis shiiae produce pouch galls on Distylium or on a closely-related genus in the Hamamelidaceae (presumably tribe Fothergilleae). Its closest known relative, Neonipponaphis pustulosis (Chen & Qiao, 2012), is also known only from a secondary host, Castanopsis eyrei - an evergreen tree of late successional forests between 300 and 1700 m, common across southeast China and Taiwan.

DNA analysis by Aoki et al. (2021) supports Nipponaphis as being the most closely related genus to Neonipponaphis. On their primary host Nipponaphis galls are mainly formed from the axillary buds of twigs, and are closed, large, globular, cigar or fig-shaped. Five of the seven Nipponaphis whose primary hosts are known use Distylium racemosum, the remaining two use Sycopsis sinensis (=Distylium formosanum) (Yeh, 2009; Wang et al., 2021).

Neonipponaphis shiiae is native to Japan & its southern islands but unrecorded elsewhere, and all but one Distylium species are native to China. Of the Distylium relatives in tribe Fothergilleae, Sycopsis spp. are native to mainland China and Taiwan, but not Japan or its islands. Yeh (2009) recorded an unidentified Nipponaphidini species on Distyliopsis dunnii, but Distyliopsis have a more southerly distribution, excluding Japan or its islands. Neither genus Fothergilla nor Parrotiopsis are known from Asia. Genus Hamamelis only hosts Hamamelistes and Hormaphis, and the only aphid recorded from a Parrotia species is Aphis gossypii (an extremely polyphagous species).

In contrast, 15 of the 17 aphids known from Distylium racemosum are Nipponaphidini species. The distribution of Distylium racemosum includes Japan, its southern islands, Taiwan, southernmost Korea and eastern China but, like Neonipponaphis shiiae, most records are from the southern Japan. Distylium racemosum (first image below) typically grows in evergreen oak forests and, in the south-western half of Japan, was one of the dominant tree species of the lowland forests, now largely replaced by plantations of Cryptomeria japonica (=Japanese cedar, a commercial softwood). Distylium racemosum also occurs on Mount Wuyi (China), which is where Neonipponaphis pustulosis was recorded.

Both images copyright Siebold & Zuccarini (1870) public domain.

The main secondary host of Neonipponaphis shiiae seems to be Castanopsis cuspidata (=Shiia cuspidata, Quercus cuspidata, second image above), but it is also known from Castanopsis sieboldii (both Fagaceae). On these hosts it persists throughout the year, often under ant shelters, on branches and shoots (cf. Metanipponaphis rotunda, which feeds on leaves).

Castanopsis cuspidata has a similar geographic distribution to Distylium racemosum, but forms part of the climax vegetation in laurel forests - rather than the evergreen oak forests which host Distylium racemosum. Castanopsis sieboldii (=Castanopsis cuspidata var. sieboldii, Shiia sieboldii) is native to Japan, its islands, and southernmost Korea. At elevations up to 2100 m in the southern Japanese islands to as low as 200 m in the north Castanopsis sieboldii is a common, often dominant, canopy tree of climax evergreen broadleaved warm temperate rainforest.

The detailed Japanese distribution, genetics, varieties and hybrids of these two closely-related and sometimes-conflated Castanopsis are disentangled by Aoki et al. (2014). Castanopsis cuspidata var. cuspidata is restricted to interior upland terrain around the Seto Inland Sea (Castanopsis cuspidata in Taiwan is var carlesii). Castanopsis sieboldii var. sieboldii has a larger range, comprising the coastal regions of southern Japan including the Ryukyu Islands north of Amami. Castanopsis sieboldii var. lutchuensis occurs in the southern Ryukyu Islands - including Amami where Sugimoto (2019) found Neonipponaphis shiiae.

 

Other aphids on the same host

Primary host

The most likely primary host for Neonipponaphis shiiae appears to be a winter hazel, Distylium racemosum (see above).

Secondary hosts

Neonipponaphis shiiae has been recorded from 2 chinquapin species (Castanopsis cuspidata, Castanopsis sieboldii).

Acknowledgements

We especially thank Shigeyuki Aoki for sending us most of the images used on this page, and for his comments on the draft. We also thank Chen & Qiao for making their paper available under a creative commons licence.

We have used the species accounts of Takahashi (1962) and Aoki & Kurosu (2022), together with those of Roger Blackman & Victor Eastop in Aphids on Worlds Plants. We fully acknowledge these authors and those listed in the reference sections 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

  • Aoki, K., Ueno, S., Kamijo, T., Setoguchi, H., Murakami, N., Kato and M., Tsumura, Y. (2014). Genetic Differentiation and Genetic Diversity of Castanopsis (Fagaceae), the Dominant Tree Species in Japanese Broadleaved Evergreen Forests, Revealed by Analysis of EST-Associated Microsatellites. PLoS ONE 9, (1) Full text

  • Aoki, S., Kutsuake, M. Kurosu, U., Yeh, H.-T., Sano, M. & Fukatsu, T., (2015). Nipponaphis species (Aphididae: Hormaphidinae) that form green galls on Distylium racemosum in Japan. Entomological Science 18, 420–434. Abstract

  • Aoki, S., Kurosu, U., Fukatsu, T., Yeh, H.-T. & Kutsuake, M. (2021). Revision of the Japanese species of Metanipponaphis (Hemiptera: Aphididae) and its allied genera. Entomological Science 24, 302–319. Abstract

  • Aoki, S., & Kurosu, U., (2022). Sexuparae of the aphid Neonipponaphis shiiae (Hemiptera). Rostria 67, 133-136. Full text

  • Chen, J. & Qiao, G.-X. (2012). First record of the aphid genus Neonipponaphis Takahashi (Hemiptera, Aphididae, Hormaphidinae) from China, with a description of one new species. ZooKeys 236, 81–89. Full text

  • Sugimoto, S. (2019). Aphididae of Ôshima Island (Munakata) and Ainoshima Island (Kita-Kyûshû) in the northern part of Fukuoka Prefecture, Kyûshû. Rostria 63, 25-44.

  • Takahashi, R. (1962). Aphids causing galls on Distylium racemosum in Japan, with descriptions of two new related species (Aphididae, Homoptera). Bulletin of the University of Osaka Prefecture, Series B 13, 1–11. Full text

  • Yeh, H.-T. (2009). Biosystematics and molecular phylogeny of the Hormaphidinae (Hemiptera: Aphididae) in Taiwan, Ph.D. thesis, National Taiwan University. Abstract

  • Wang, W., Cui, Y., Chen, X. Bashir, N.H. & Chen, H. (2021). A new species of aphid of the genus Nipponaphis (Hemiptera: Aphididae: Hormaphidinae) from China, inducing galls on the trunk of a witch-hazel (Hamamelidaceae) Zoologia 38, 1-9. Full text