The analysis showed advances in the bud break and full bloom dates for both apple cultivars. Fujisawa and Kobayashi12 found negative correlations between bud break date and mean air temperature in March as well as between flowering date and mean air temperature in March–April in the main apple-producing district in Japan. By comparing the phenological response to the long-term trend in air temperatures with the response to year-to-year fluctuations in air temperatures, they revealed that long-term changes in the phenology of apples are attributable to long-term changes in temperature.

In our study, the mean air temperatures in March and in March–April increased (Supplementary Table S1). Strong negative correlations (P < 0.001) were found between temperature and the phenological events (Fig. 4; Supplementary Table S5). These results were similar to the findings by Fujisawa and Kobayashi12, suggesting that the phenological advances in our study were caused by recent warming in the experimental orchard.

Figure 4 Phenological responses to temperature. Relationship between (a) bud break date and mean air temperature in March and (b) full bloom date and mean air temperature in March–April. Lines represent linear regressions. Full size image

The precipitation in March and in December–April and the sunshine duration in March–April exhibited a significant increase in Nagano (Supplementary Table S1), but a significant correlation with phenological dates was recorded only in precipitation in December–April (Supplementary Table S5). Total rainfall in winter–early-spring, as opposed to temperature, is positively correlated with full bloom dates of apple trees in South Africa15. In our study, total precipitation in December–April exhibited a significant increase in Nagano (Supplementary Table S1) and the full bloom date was negatively correlated with rainfall; this finding was not consistent with the results in South Africa. The relationship between precipitation and blooming may not be simple in heavy-snow regions such as Nagano.

Our results showed that the taste and textural attributes of apples harvested on 1 November (‘Fuji’) or on 1 September (‘Tsugaru’) changed during the long-term observation period (Fig. 3; Table 1). The acid concentration, firmness and watercore rating all decreased, whereas the soluble-solids concentration increased. Here, it should be noted that the acid concentration of fruit is strongly correlated with the sensorial perception of sourness34 and that watercore rating is linked to storage stability35. The correlations between firmness and hardness36 and between soluble-solids concentration and sweetness34 are weaker than that between acid concentration and sourness; nevertheless, firmness and soluble-solids concentration have generally been used as the respective indicators of hardness and sweetness. Because the soluble-solids concentration increased and the acid concentration decreased, the soluble-solids to acid ratio, another indicator of sweetness34, significantly increased (‘Fuji’ in Nagano, P = 0.001; ‘Fuji’ in Aomori, P = 0.000; ‘Tsugaru’, P = 0.017).

With advancing maturity, apples show gradual decreases in acid concentration and firmness and increases in soluble-solids concentration. The observed trends in fruit taste and textural attributes on the benchmark calendar date seemed to be partly ascribable to the earlier fruit maturity derived from the earlier blooming dates, except in the case of watercore rating, because apples grown under high temperatures seldom exhibit watercore disorder37. Instead, Yamada et al25. demonstrated that low temperature directly causes watercore disorder in apples without influencing the level of fruit maturity.

The mean air temperatures during the maturation periods of ‘Fuji’, exhibited a significantly increasing trend (P < 0.05) and that for ‘Tsugaru’ showed an increasing trend (P < 0.1, Supplementary Table S2). Previous studies using temperature-controlled chambers have indicated that high temperatures during the maturation (pre-harvest) period can reduce the acid content24,25, firmness24 and watercore rating25,26. Therefore, the increase in temperatures during the maturation period is probably another reason for the observed decrease in the acid concentration, firmness and watercore rating of fruits harvested on the benchmark calendar date. In contrast, previous studies have shown that the soluble-solids concentration is unaffected by temperature24,25,27.

Because determination of harvest date on the basis of the number of days after full bloom may cancel out the effect of the advancement of fruit maturity by earlier blooming, the effects of air temperature during the maturation periods on the taste and textural attributes of fruit judged by the number of days after full bloom can be detected more clearly than those judged by calendar date. Both acid concentration and watercore rating in fruit, as judged by the number of days after full bloom, showed significant decreasing temporal trends and firmness also exhibited a significant decreasing trend for the two cultivars in Nagano (Table 1). The relationship between these attributes and air temperature during the maturation period is shown in Figure 5 and Supplementary Table S6. Acid concentration, fruit firmness of ‘Fuji’ in Nagano and watercore rating were significantly negatively correlated with mean temperature during the maturation period. These relationships were in agreement with those shown in previous experiments in temperature-controlled chambers24,26. Therefore, the temporal trends of these attributes assessed by the number of days after full bloom (Table 1) were probably a result of increasing air temperature during the maturation period (Supplementary Table S2).

Figure 5 Responses of taste and textural attributes or maturity indexes in apples to mean temperatures during the maturation period, which is 110–180 (‘Fuji’ in Nagano), 100–170 (‘Fuji’ in Aomori) or 90–120 (‘Tsugaru’) days after full bloom. Relationships between mean temperature during the maturation period and (a) acid concentration, (b) firmness in Nagano and (c) watercore rating of fruit on 180 (‘Fuji’ in Nagano), 170 (‘Fuji’ in Aomori) and 120 (‘Tsugaru’) days after full bloom, all of which showed significant temporal trends (Table 1). Lines represent linear regressions with regression formulae. Full size image

The residual errors of the regression formulas shown in Figure 5 were further analyzed by separately comparing those from before 1990 with those after 1991. No significant differences between the mean values of the residual errors from before 1990 and after 1991 were found in any parameters of fruit quality (Supplementary Table S6). This result suggests that factors other than air temperature have little effect on the long-term trends.

A strong correlation (P < 0.001) between watercore rating and temperature during the maturation period was found (Fig. 5, Supplementary Table S6).Watercore is characterized by water-soaked and translucent flesh tissues and is prevalent in cultivars such as ‘Fuji’ but absent in ‘Tsugaru’. To avoid the development of watercore, which causes internal browning during storage35, ‘Fuji’ apples for storage must be harvested before being fully ripe. If the harvest time of ‘Fuji’ could be delayed because of decreased watercore development by warming, this could contribute to a decrease in the acid concentration and an increase in the soluble-solids concentration of stored apples.

Our findings suggested that harvest date, as judged by four (blush, ground colour, starch concentration and calendar date) of the five maturity indices, did not show significant temporal trends (Supplementary Table S4). These results support the findings of a study conducted in the Mediterranean region8, which reported an advance in the unfolding time of apple leaves but no significant change in fruiting date.

It is well known that anthocyanin levels, which are responsible for the redness in apple peel blush, are inversely related to field temperature38; anthocyanin accumulation in ‘Fuji’ decreases at temperatures greater than 25°C39. Starch degradation is also inhibited by high temperatures during maturation25. Our results were in accordance with these findings; temperatures during maturation were positively correlated with number of days from full bloom to the dates when the blush or starch concentration ratings reached the benchmark values (Supplementary Table S7).

However, no significant temporal trends were found in the blush ratings or starch concentration (Supplementary Table S4). This may be because a slower advance toward the benchmark maturity index values caused by warming offset the advance in fruit maturity induced by the earlier blooming. Menzel6 previously reported that higher spring temperatures advanced leaf colouring as a result of earlier leafing, whereas warmer temperatures in autumn could delay it. This may be true for the apple peel as well: high temperatures during spring could advance the peel blush rating as a result of earlier blooming, but warmer temperatures in autumn could have the opposite effect. The long-term trends in taste and textural attributes, as judged by peel colour rating and starch concentration, were similar to those derived from calendar date (Table 1). This may be because there was little change in the dates upon which the peel colour ratings and starch concentration reached the benchmark values over the study period.

In conclusion, we identified changes in attributes of the taste and textural attributes of apples in response to recent climate warming. These changing quality attributes are likely to be caused by earlier blooming and higher temperatures during the maturation period. Regardless of the maturity index used to determine harvest date, reductions in acid concentration, fruit firmness and watercore development were observed, whereas the soluble-solids concentration increased in some cases. These results suggest that the taste and textural attributes of apples in the market are undergoing change from a long-term perspective, even though consumers might not perceive these subtle changes. If global warming continues to progress, the changes in the taste and textural attributes of apples could be more striking as blooming dates become even earlier and temperatures increase during the fruit maturation period.