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Keywords:

  • life cycle;
  • Nipponaphidini;
  • overwintering;
  • social aphids;
  • social insects

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

This paper examines the life history of a generation of galls created by the aphid Quadrartus yoshinomiyai (Hormaphidinae: Nipponaphidini) on its primary host plant, Distylium racemosum. First-instar fundatrix nymphs of Q. yoshinomiyai initiated galls on stems of developing shoots in early April and incipient enclosed galls were found from later the same month. The galls lasted for up to 14 months, during which they grew to maturity, opened in early or mid-April of the following year and dried up by the end of June. First-instar fundatrix nymphs were found on winter buds, indicating that they hatched from eggs in autumn and overwintered as nymphs. These results suggest that Q. yoshinomiyai has a three-year life cycle.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

Gall-forming aphids have shown to develop sociality multiple times independently (Aoki 1987; Stern & Foster 1996; Pike & Foster 2008; Aoki & Kurosu 2010). The tribe Nipponaphidini, which forms galls on Distylium trees and contains several unique social species, provides an important clade for understanding the evolution of sociality in aphids. The presence of defensive nymphs has been reported in the gall-inhabiting generation of six species (Kurosu et al. 1995, 2003; Aoki et al. 1998; Fukatsu & Antonius 1998; Fukatsu et al. 2000; Uematsu et al. 2007), one of which produces a morphologically specialized, sterile caste (Fukatsu & Antonius 1998; Fukatsu et al. 2005). In addition, self-sacrificial gall repair and post-reproductive colony defense, previously unknown social behaviors in aphids, have recently been reported (Kurosu et al. 2003; Kutsukake et al. 2009; Uematsu et al. 2010).

Although life cycles of nipponaphidine aphids are poorly known, their galling phase on the primary host has been studied to some extent (Sorin 1960, 1997; Nishitani & Ito 1991; Ngakan & Yukawa 1996; Kurosu & Aoki 1998, 2009; Fukatsu et al. 2005). Galls of nipponaphidine aphids are completely closed until they grow to maturity, and then develop exit holes, allowing winged adults to fly to their secondary hosts, mainly evergreen trees such as Quercus, Castanopsis, or Neolitsea (Blackman & Eastop 1994), where their progeny form open colonies. The galls of Nipponaphis monzeni and Nipponaphis distyliicola last for over a year and attain a large colony size (Kurosu & Aoki 1998, 2009). Galls of N. monzeni, in particular, can survive for four and a half years (Kurosu & Aoki 2009). Water absorption through the gall inner surface facilitates such a long life in such completely enclosed galls (Kutsukake et al. 2012).

The nipponaphidine aphid Quadrartus yoshinomiyai forms conspicuous large galls on the evergreen Distylium racemosum, its primary host plant. A single fundatrix (gall founder) forms a closed gall. In the gall the fundatrix parthenogenetically produces offspring, which then develop into wingless adults. The gall gradually matures and forms an exit hole in early or mid-April, before drying up at the end of June. Winged adults disperse to the deciduous Quercus acutissima, their secondary host, and found colonies on the young shoots (Sorin 2001). In the galling generation, first-instar nymphs attack intruding predators with their stylets and wingless adults sacrifice themselves to defend the gall by sticking to predators (Uematsu et al. 2007, 2010, 2013). The colony size of a mature gall can reach over 4000, suggesting that the gall may last for over a year. However, the details of gall formation by a fundatrix have not been previously studied in Q. yoshinomiyai. In this study, we report that a fundatrix of Q. yoshinomiyai overwinters as a nymph and forms a gall from the beginning of April. It is revealed that this species has a long galling phase that lasts for 14 months until terminating in June of the second year.

Materials and Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

Study sites

Galls of Q. yoshinomiyai were found on trees of Distylium racemosum at Shinkiba and Wakasu, Tokyo, Japan. Field observations were carried out at these sites from February 2007 to December 2010. To identify the gall-forming fundatrix nymphs of Q. yoshinomiyai, some twigs of D. racemosum were collected for examination in the laboratory. If fundatrix nymphs were found, then their behavior was observed under a dissecting microscope and the stage and size of the incipient gall were recorded.

Morphological examination

Insects were preserved in 70% ethanol, cleared in 10% KOH, stained with acid fuchsin, mounted in balsam and examined under a light microscope.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

Development of Q. yoshinomiyai galls

From late April to early May, some tiny closed galls were found on the stems of developing shoots of D. racemosum (Fig. 1a). The size and shape of the galls remained almost constant (about 2–5 mm in height) during summer. From autumn, the galls gradually expanded and, in winter, formed protuberances on their outer surface (Fig. 1b,c). The height of the galls collected on 2 November 2010 were 6.4 ± 1.1 mm (range 5–10, n = 19) and those collected on 2 December 2010 were 12.0 ± 3.3 mm (range 5–16, n = 19). In early spring, the galls began rapidly expanding and became reddish and mature. An exit hole, through which winged aphids dispersed, appeared in mid-April (Fig. 1d). All mature galls dried up before mid-June.

figure

Figure 1. Galls of Quadrartus yoshinomiyai. (A) An incipient gall (on 9 May, 2009). (B) An immature gall (on 2 November, 2010). (C) A growing gall (on 2 December, 2010). (D) A mature gall (on 7 May, 2010). Scale bars, 10 mm.

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Fundatrices on winter buds of D. racemosum

On 5 February 2007, 28 December 2009, and 2 December 2010, first-instar fundatrix nymphs were found on winter buds of D. racemosum (Fig. 2a). These nymphs remained motionless in the space between the bud scales. When tapped with an insect pin, they moved away sluggishly from their feeding sites.

figure

Figure 2. Gall formation by fundatrix nymph. (A) Two fundatrix nymphs on winter buds (on 5 February, 2007). (B) A fundatrix nymph forming a gall (on 7 April, 2010). (C) Morphology of a gall-forming fundatrix nymph. (D) Morphology of an adult fundatrix. Fundatrix nymphs are shown by yellow arrows. Scale bars, 200 μm.

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Gall formation by fundatrices

On 10 April 2009 and 7 April 2010, first-instar fundatrix nymphs were forming galls on stems of developing shoots (Fig. 2b). The morphology of the nymphs (Fig. 2b) was identical to that of the overwintering nymphs mentioned above (Fig. 2a). Gall formation was not complete on those dates, with the surrounding plant tissues bulging but not yet enclosing the nymphs (Fig. 2b).

Three and four already closed incipient galls were sampled on 28 April and 7 May 2008, respectively. All galls contained an adult fundatrix, and three out of four galls collected on 7 May also contained one or two first-instar nymphs of the next generation. The size and morphological characters of a small, sclerotized shed skin found inside each of the galls were identical to the exoskeleton of the gall-forming fundatrix nymphs (see the next section).

Morphology of fundatrices

Gall-forming fundatrix nymphs had sclerotized exoskeletons (Fig. 2c), whereas older fundatrix nymphs and adults were soft-bodied (Fig. 2d). In addition, the gall-forming nymphs had thick and long setae on their back (Fig. 2c).

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

In the present study, the first-instar fundatrix nymphs of Q. yoshinomiyai were found on or inside winter buds from December to March, and initiated galls in April. This indicates that the fundatrix nymphs hatched by winter, probably in autumn, overwintered on the buds and initiated galls in early spring. This is consistent with a previous report that winged sexuparae of Q. yoshinomiyai emerged from late-July to early October (Sorin 2001). Overwintering by a fundatrix nymph has hitherto been unknown in the tribe Nipponaphidini. The sclerotized exoskeleton and long setae of the first-instar fundatrix nymph might be an adaptation to survive cold winter conditions.

Sorin (2001) seems to have thought that galls of Q. yoshinomiyai last for only two months. Through his transfer experiments, Sorin (2001) found that offspring of winged aphids of Q. yoshinomiyai grew on Quercus acutissima, and he obtained presumed winged sexuparae, not within the year, but in the following year. From these observations he concluded that the species has a two-year life cycle. Our results, however, showed that galls of Q. yoshinomiyai were initiated in April, grew mature and open in early or mid-April of the second year, and dried up in June, indicating that the galls last for about 14 months. Thus this species probably has a three-year life cycle.

Like Q. yoshinomiyai, the galls of two Nipponaphis species, N. distyliicola and N. monzeni, also last for over a year (Kurosu & Aoki 1998, 2009). The galls of the above three species are among the largest in Nipponaphidini, and all of them have young defenders or gall-repairers. Q. yoshinomiyai also has adult defenders that exhibit a unique self-sacrificing behavior (Uematsu et al. 2010). Larger galls can attain larger colony sizes composed of a single genotype, which would facilitate the development of altruistic behavior (Aoki & Kurosu 2004; Aoki & Imai 2005). A long galling phase might also allow the aphids to perform more elaborate social behavior at the expense of many altruistic individuals.

Acknowledgments

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

We thank Ed Turner and two anonymous reviewers for comments on the manuscript. K.U. was supported by a Research Fellowship of the Japan Society for the Promotion of Science for Young Scientists.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References
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