Aedes albopictus (Skuse) (Diptera: Culicidae), or the Asian tiger mosquito, is one of the most invasive vector mosquito species globally. Aedes albopictus bites are both a nuisance and a potential transmitter of arboviruses, such as dengue, Chikungunya, Zika, and dog heartworm (Dirofilaria immitis). Local transmission of dengue in Japan was first recorded during the 1940s (Hotta 1998) with no local transmission occurring since 1945. Between 1999 and 2010, 868 imported cases of dengue were reported in Japan with no local transmission (Takasaki 2011). In 2014, Japan experienced its first dengue outbreak after 70 yr in the Tokyo Metropolis, consisting of 160 locally transmitted cases between August and October, transmitted exclusively by Ae. albopictus (Kutsuna et al. 2015, Tsuda et al. 2016).

Ae. albopictus was previously limited to areas such as Southeast Asia and the islands of the Western Pacific and the Indian Ocean. Over the past 30–40 yr, the species has spread globally to areas that include North, Central, and South America, parts of Africa, northern Australia, and several countries in Europe (Moore 1999, Benedict et al. 2007, Paupy et al. 2009, Roiz et al. 2011). Ae. albopictus is a typical ‘container mosquito’ and prefers artificial environments (Hawley et al. 1987). In Japan, it can be found in various habitats, including, but not limited to, flower vases and wash basins in shrines, the graveyards of Buddhist temples, used tires, used cans, plastic containers, buckets, and bamboo stumps (Kobayashi et al. 2002). Rainwater drainage pits, which are scattered around public roads, parks, public spaces, and private land, are an important larval habitat in urban areas. These pits maintain a suitable depth of water throughout much of the year, even in the dry season, because they are often nonpermeable (Hata and Kurihara 1982, Ogata 2013).

Similar to most other invasive aedine species, the eggs of Ae. albopictus are desiccation resistant. The eggs often overwinter under dry conditions in temperate areas (Makiya 1968). They also can be laid inside water holding cargo that is shipped globally, such as used car tires (Knudsen 1995) or houseplant pots such as ‘lucky bamboo (Madon et al. 2003, Deblauwe et al. 2015).’ The ability of the eggs to survive for long periods without flooding has facilitated their rapid spread globally (Gratz 2004, Sebesta et al. 2012). Eggs can survive in the field for several months over winter (Ishii et al. 1954, Toma and Miyagi 1990). When exposed to a temperature of -10°C for 24 h, the survival rate of dormant eggs from temperate Asia and the United States was 70% (Hawley et al. 1987); however, the survival rate depends on the conditions during embryonation, as well as chemical and physiological changes to the overwintering eggs. After overwintering in temperate areas, such as Japan, the eggs begin to hatch in late March or early April. The temperature is particularly important for terminating the dormancy of the eggs because Ae. albopictus is poikilothermic.

To date, no reports regarding the season in which the eggs hatch after overwintering in the field have been created. Ae. albopictus biting activity occurs in Japan from late April to mid-June in areas of infestation with different annual mean temperatures and altitudes. This study was undertaken to predict the date when Ae. albopictus female adults start to bite in temperate regions of Japan using high-resolution temperature analysis. Japan was a suitable location for this study for two main reasons: first, Ae. albopictus is a native species and is widely distributed throughout Japan, within a large population where most people come into contact with Ae. albopictus; second, Japan covers a range of climates. The country extends north to south, ranging from tropical to subarctic zones, with most of the country located within the temperate zone. The seasonal variation of temperature is also very marked. In this study, we used high-quality and high-resolution meteorological data from weather observation stations throughout Japan.

Materials and Methods

Results

The Ae. albopictus field surveillance results are shown in Table 1. The dates at which Ae. albopictus adults started to bite in the field ranged from late April (Nagasaki) to the middle of June (Morioka, Ueda). Nagasaki was the most southerly and warmest of the surveillance locations; Morioka is located near the northern limit of the Ae. albopictus habitat boundary in Japan (Kobayashi et al. 2002); and Ueda is located inland with an altitude of approximately 500 m. In Nagasaki and Ueda, the monthly mean temperatures from April to June are similar to the mean temperature of March in Morioka. At other locations, the start of the biting season is usually in May.

Table 1.

The date on which the first Ae. albopictus adult was captured using human-baited insect net sweeping

Although geographically there was a difference of up to 2 mo between the first Ae. albopictus biting day, the GDDs were almost the same. The mean GDD value was 269.2 GDDs (95% confidence interval [CI], 245.2 - 292.9). The appearance of the first adults was observed at a daily mean temperature of approximately 20°C. Since the developmental zero temperature of Ae. albopictus was 10°C, the difference was 25°C × d/(20 - 10°C) = 2.5 days.

A correlation was found between the field surveillance data and the climatological data (Fig. 1). The most important factor in determining the dates when Ae. albopictus adults first started to bite in the field was the temperature during larval development. There were high correlations between the monthly mean temperatures from March to June and the date at which the first mosquitoes were captured. The correlation coefficient was highest in April (Pearson product–moment correlation coefficient: r = -0.900), followed by March (-0.8750), May (-0.821), and June (-0.693), respectively.

The dates could be forecasted using a linear regression formula that showed the relationship between the April mean temperature and the number of successive days from April 1. The date was estimated using the following equation: (Days from April 1st (=1 d) to the date) = 123.48 - 5.65 × (April monthly mean temperature). A forecast map created using climatological data is shown in Fig. 2. The climatological data were standardized based on the data over 30 yr (from 1981 through 2010) by the Japan Meteorological Agency. The first forecast map ranges from April to June (Fig. 1). April applies to the part of the southwestern Kyushu districts (i.e., Nagasaki) that face the Pacific Ocean; May 1–15 applies to the southern areas facing the Pacific Ocean (i.e., Kyushu), parts of Chugoku, and 164 Shikoku (Uwajima), which face the inland sea, and Kinki (Nishinomiya), Kanto (Oiso, Ebina, Yokohama, Kasukabe), and the Chubu district; May 15–31 applies to part of Chugoku and Hokuriku district (Toyama, Niigata), which face the Sea of Japan, and Chubu, and the northern Kanto Districts; and June applies to the areas of Tohoku (Morioka) and the inland area of Chubu district (the altitude of Ueda is approximately 500 m). A second map, which was derived from a typical hot spring year (1998) and a third map from a cold spring year (1996) were also created (Fig. 3). In Japan, the spring season occurs from March to May. The Japan Meteorological Agency provided the criteria for hot and cold seasons based on the historical climate data; their definitions were used in the present study. Almost all of the locations found a difference of approximately 20 d in the first biting day (Fig. 3).

Fig. 1.

The correlation between the mean monthly temperature and the days until the first Ae. albopictus female adult was captured from April 1 (= 1). Each circle shows the surveillance results for each field and year. The correlation coefficient is highest in April (Pearson product-moment correlation coefficient: r = -0.900), followed by March (-0.875), May (-0.821), and June (-0.693), respectively.

Fig. 2.

The forecast of the Ae. albopictus first adult biting day. The date was forecast based on the mean April temperature (normal values in 1981–2010; approved by the Japan Meteorological Agency). The base map of Japan and the April mean temperature data were obtained from National Land Numerical Information download service (National Land Information Division, National Spatial Planning and Regional Policy Bureau, MLIT of Japan,  http://nlftp.mlit.go.jp/ksj/). The first biting day was predicted from the temperature. Refer to the results section for details of the forecast calculation formula.

Discussion

We discovered that the timing of seasonal initiation of biting by female Ae. albopictus could be estimated using the monthly mean temperature (Fig. 1). The April mean temperature showed the highest correlation with date of first captured female adults, whereas the mean March temperature showed a moderate correlation. The difference in the correlation coefficient between April and March seems to be derived from the number of cold days below development zero (10°C) in March. From our experience in the field, it seems that the hatching of dormant eggs and the start of larval development occur in early April rather than early or mid-March. The correlation coefficient between the first biting days from April 1 and the May mean temperature was clearly low because, in contrast to March and April, there were no distinct differences in the daily mean temperature. No contradiction was found between the estimation of the Ae. albopictus first biting day and comparisons of the GDDs that theoretically allow for larval development in field or laboratory conditions (Matsuzawa and Kitahara 1966).

There are several reports on egg dormancy and the termination of overwintering of Ae. albopictus in laboratory experiments as well as a small amount of observational data from the field. Several complex factors, such as the age of the eggs, desiccation, the duration of colonization in the laboratory, temperature changes, and the oxygen concentration, determine whether or not Ae. albopictus eggs will hatch upon flooding by spring rain. There are several reports on the number of days from Ae. albopictus ovipositing to hatching, where the duration of embryonation was found to be dependent on the temperature (Hawley 1988). In a strain of Ae. albopictus from China, the period from ovipositing to hatching was 2 d at 25°C, whereas a strain from Japan took 6 d at 17°C and 3 days at 24° °C (Sheng and Wu 1951, Udaka 1959). Laboratory studies found that the mean duration (in days) of the larval stage of Ae. albopictus varies with temperature: 19 d at 14°C, 7 d at 20°C, 8 d at 25°C (Udaka 1959), 5–6 d at 26–30°C (Livingstone and Krishnamoorthy 1985), and 5–7 days at 30°C (Galliard 1968). Unfortunately, detailed experiments have not been performed using field collected eggs or the early instar larvae of Ae. albopictus. It is not clear whether minor meteorological differences influence the termination of egg dormancy or the duration of larval development in spring in countries such as Japan, the United States, European countries, Korea, and China. However, in Japan, the timing depends strongly on the April temperature. A strong correlation was observed between the first Ae. albopictus biting day and the April mean temperature in southern to northern Japan (Table 1). This finding was supported by field observations.

Fig. 3.

The difference in the start of the Ae. albopictus biting season during a typically cold (1996) and hot (1998) spring. The cold and hot springs were defined based on the mean spring (March to May) temperatures in Japan. These were forecast using the mean April temperature for each year.The base map of Japan was obtained from the National Land Numerical Information download service (National Land Information Division, National Spatial Planning and Regional Policy Bureau, MLIT of Japan,  http://nlftp.mlit.go.jp/ksj/). The April mean temperature data in 1996 and 1998 were obtained from Dr. Yasushi Ishigooka (National Institute for Agro-Environmental Sciences, Japan). The first biting day was predicted from the temperature.

Conversely, in some locations, first adult female biting day did not depend on mean April temperature. These locations included the warmer Nansei island regions (around Okinawa), the colder regions of northern Japan (Hokkaido), and mountainous areas (highlands and unpopulated areas). In the warmer regions of Japan, such as the subtropical southern island of Okinawa, Ae. albopictus neither deposits overwintering eggs (Hawley 1988) nor has an annual dormant overwintering period (Toma and Miyagi 1990). Furthermore, Ae. albopictus is not found in the cold or mountainous parts of Japan as they cannot survive the winter in areas where the annual mean temperature is less than 11°C (Kobayashi et al. 2002). In areas in which the first biting day was predicted to be after July, we hypothesized that Ae. albopictus would not survive the winter. This hypothesis was based on two factors: first, there are no reports to indicate that dormant eggs can survive for more than half a year, and therefore, we excluded these locations from this study; second, the northern edge of the area in which the first biting day is predicted to be late June, corresponds with the northern limits of the distribution of Ae. albopictus, indicating that the dormant eggs of Ae. albopictus fail to survive the winter as the dormancy period under the winter low temperatures may be too long.

We predicted that there would be multiple factors affecting the timing of the initiation of spring biting activity in Ae. albopictus. However, in this study, we clearly demonstrated that there is a strong correlation between the April mean temperature and the duration of larval development in the temperate regions of Japan. It is possible that a simple formula can be used to predict the first Ae. albopictus biting day at various geographic locations in Japan, as well as the start date in other temperate countries such as the United States and in European. Due to a variation in temperature from year to year, the first Ae. albopictus biting day changes, meaning the start date can vary up to approximately 20 d (Fig. 3) in Japan. Thus, it is necessary to make the prediction based on the April temperature for the current year. This prediction will be helpful in the implementation of programs to control the populations of Ae. albopictus larvae and adult mosquitoes in potential risk areas such as Japan for the mosquito-borne diseases in temperate regions.