Morphological abnormalities in gall-forming aphids in a radiation-contaminated area near Fukushima Daiichi: selective impact of fallout?

Abstract

To evaluate the impact of fallout from the Fukushima Daiichi Nuclear Power Plant accident on organisms, this study compared the morphology and viability of gall-forming aphids between the Fukushima population and control populations from noncontaminated areas. This study, in particular, focused on the morphology of first-instar gall formers derived from the first sexual reproduction after the accident. Of 164 first instars from Tetraneura sorini galls collected 32 km from Fukushima Daiichi in spring 2012, 13.2% exhibited morphological abnormalities, including four conspicuously malformed individuals (2.4%). In contrast, in seven control areas, first instars with abnormal morphology accounted for 0.0-5.1% (on average, 3.8%). The proportions of abnormalities and mortality were significantly higher in Fukushima than in the control areas. Similarly, of 134 first instars from T. nigriabdominalis galls, 5.9% exhibited morphological abnormalities, with one highly malformed individual. However, of 543 second-generation larvae produced in T. sorini galls, only 0.37% had abnormalities, suggesting that abnormalities found in the first generation were not inherited by the next generation. Although investigation is limited to one study site, this result suggests that radioactive contamination had deleterious effects on embryogenesis in eggs deposited on the bark surface, but a negligible influence on the second generation produced in closed galls. Furthermore, analysis of both species samples collected in spring 2013 indicated that the viability and healthiness of the aphids were significantly improved compared to those in the 2012 samples. Thus, the results of this study suggest the possibility that a reduced level of radiation and/or selection for radiation tolerance may have led to the improved viability and healthiness of the Fukushima population.

Keywords: Tetraneura; malformation; morphology; radiation; viability.

Figure 1

Percentage abnormal morphologies in Tetraneura sorini first-instar gall formers from eight populations. Asterisks in sample sizes indicate that first instars were collected from buds, whereas nonasterisked figures indicate that first-instars' cast-off skins were collected from galls. Level 1, slight abnormalities included the atrophy or bending of one leg (Fig. S2A,B), small ganglia on the ventral surface (Fig. S2C), partial fusion of adjacent abdominal tergites (Fig. S2D), and tissue necrosis in one leg or antenna (Fig. S3A,B). Level 2, abnormalities included the atrophy or bending of two legs and tissue necrosis in two or more appendages. I categorized the complete or partial loss of one appendage of first instars as level 2 (Fig. S3C,D). Level 3, intense abnormalities included the loss of two or more appendages, the loss of one leg and atrophy of another leg, the appearance of new features, and conspicuous asymmetry in bilateral characters.

Figure 2

Cast-off skins of first-instar gall formers of T. sorini from Fukushima. (A) normal morphology, (B) level-3 malformation with a bifurcated abdomen.

Figure 3

Two level-3 malformed T. sorini first instars from Fukushima. (A) a dead first instar having a distended abdomen (arrowed) and a projection on the joint of the mid-femur and tibia (arrowed). (B) projection having a seta (arrowed), (C) a dead first instar having protuberances on the abdomen (arrowed) and the base of a mid-leg (arrowed). The mid-leg was transposed from the original position. (D) protuberance on the base of the trochanter.

Figure 4

Two level-3 malformed first instars from Fukushima. (A) dead T. sorini first instar with a hind tibia missing due to tissue necrosis (arrowed) and the other hind leg atrophied (arrowed). (B) cast-off skin of a T. nigriabdominalis first instar with a hind leg, a mid-leg, and an antenna missing (arrowed).

Figure 5

T. sorini first-instar gall former with a trifurcated tarsus (arrowed) collected from Bibai, Hokkaido in 1987.

Figure 6

Percentage abnormal morphologies in T. nigriabdominalis first-instar gall formers from seven populations. Asterisks in sample sizes indicate that first instars were collected from buds, whereas nonasterisked figures indicate that first-instars' cast-off skins were collected from galls. The definitions of three levels of abnormality are the same as in Fig. 1.

Figure 7

Comparison of the fates of gall formers collected from one elm tree in the Fukushima area between 2012 and 2013. Gall formers in the galls were categorized into three groups: healthy, morphological abnormal, and dead aphids (fundatrices).