Do thermal tolerances and rapid thermal responses contribute to the invasion potential of Bactrocera dorsalis (Diptera: Tephritidae)?

Abstract

Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) has shown remarkable range expansion over the past 10 years and invaded several new continents including Africa. Here we report results of a detailed assessment of acute high and low temperature survival ability and the plasticity thereof, to test the hypothesis that traits of the thermal niche have contributed to the species’ invasion ability. We also assess life-stage-related variation of thermal tolerances to determine potential stage-related environmental sensitivity. The temperatures at which c. 20% of the population survived of B. dorsalis were determined to be −6.5 °C and 42.7 °C, respectively, when using 2 h exposures. Further, four life stages of B. dorsalis (egg, 3rd instar larvae, pupae and adults) were exposed to high and low discriminating temperatures to compare their thermal survival rates. The egg stage was found to be the most resistant life stage to both high and low temperatures, since 44 ± 2.3% survived the low and 60 ± 4.2% survived the high discriminating temperature treatments respectively. Finally, the potential for adult hardening responses to mediate tolerance of extremes was also considered using a diverse range of acute conditions (using 2 h exposures to 15 °C, 10 °C and 5 °C and 30 °C, 35 °C, 37 °C and 39 °C as hardening temperatures, and some treatments with and without recovery periods between hardening and discriminating temperature treatment). These showed that although some significant hardening responses could be detected in certain treatments (e.g. after exposure to 37 °C and 39 °C), the magnitude of this plasticity was generally low compared to two other wide-spread and more geographically-range-restricted con-familial species, Ceratitis capitata and C. rosa. In other words, Bactrocera dorsalis adults were unable to rapidly heat- or cold-harden to the same extent as the other Ceratitis species examined to date. These results suggest a narrower thermal niche in B. dorsalis compared to these Ceratitis species – in both basal and plastic terms – and suggests that its geographic distribution might be more restricted in consequence.

Introduction

The true fruit flies (Tephritidae) are destructive pests of many fruits and vegetables and are of quarantine importance for the export market (Ekesi et al., 2007). The invasive oriental fruit fly Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) is of Asian origin and was first detected in Kenya in 2003 (Lux et al., 2003). It has showed a remarkably rapid invasion of the African continent (Drew et al., 2005) raising questions surrounding its environmental niche breadth (De Villiers et al., 2015) and possible climate change responses (Hill et al., 2016). First described as B. invadens when it arrived on the African continent in 2005 (Drew et al., 2005), it was subsequently synonymized with B. dorsalis (Hendel) (Schutze et al., 2015a) and re-described by Schutze et al. (2015b).

Currently Bactrocera dorsalis occurs in the northern and eastern parts of South Africa, with the Western Cape Province still free of B. dorsalis (Manrakhan et al., 2015) and therefore poses a significant risk to this large, productive deciduous fruit growing region. The presence of B. dorsalis in this province will have a serious impact on the export of fruit, as well as hamper fruit fly management strategies.

Extreme temperatures can be detrimental to insect (and other ectotherm) populations either through indirect effects such as activity constraints, or through direct effects including, for example temperature-induced sterility and cellular or tissue injury, resulting in functional limits or mortality (discussed in e.g. Sinclair et al., 2012, Andrew and Terblanche, 2013). For insects, extreme temperatures can be a significant factor determining population dynamics (reviewed in Terblanche et al., 2011, Terblanche et al., 2015) but understanding when and where such constraints might exist requires foregoing knowledge of a species’ thermal tolerances, with due consideration of life-stage-related variation (Bowler and Terblanche, 2008). Given that insect populations may cope with thermal extremes using a diverse array of mechanisms and strategies (Andrew and Terblanche, 2013), it is also critical that some understanding of phenotypic plasticity of these acute tolerances is obtained (Sgrò et al., 2016).

The temperature tolerances for B. dorsalis adults and immature stages have been explored previously (e.g. Vargas et al., 1996, Vargas et al., 1997, Ekesi et al., 2006, Chen et al., 2006, Rwomushana et al., 2008, Ye and Liu, 2005). Survival, reproduction and longevity under different temperature regimes are important factors to consider when fruit flies are accidentally introduced into new areas and likely form a critical part of the invasion process (i.e. overcoming a key population establishment barrier). For example, extreme high temperatures (minimum temperature of 24 °C and maximum temperature of 35 °C) reduced the population growth of C. capitata, B. dorsalis and B. cucurbitae and was more limiting for establishment than lower temperatures (Vargas et al., 2000). The ability to rapidly alter tolerance and survival through phenotypic plasticity (physiological adjustments) may also improve the survival capacity of a species introduced to a novel environment, as illustrated for Tephritidae by Nyamukondiwa et al. (2010) with C. capitata relative to C. rosa. The ability to survive low temperatures was markedly improved after pre-treating C. capitata and C. rosa for 2 h at 5 °C and 10 °C. The survival of C. capitata increased after pre-treatment at 0 °C and 35 °C, but a full (100% survival) hardening response was not achieved (Nyamukondiwa et al., 2010). There was a marked difference in the speed and duration of the low temperature plastic responses of these two species which could manifest as an improvement in population survival upon exposure to fluctuating low temperatures in which the opportunities to harden occur intermittently. However, the importance of plastic hardening responses across a wider range of Tephritidae has generally been poorly examined (Nyamukondiwa et al., 2010). Hu et al. (2014) showed that B. dorsalis possess a heat hardening response at 35 °C, 37 °C, 39 °C and 41 °C; and has a wider distribution range as well as a higher thermal plasticity than B. correcta. However, B. dorsalis’ thermal responses relative to other economically-important Tephritidae in South Africa has been poorly explored to date and is essential to understand the relative risks of establishment and population persistence if accidentally introduced in this growing region.

Various niche or distribution models (Stephens et al., 2007, Hill and Terblanche, 2014, De Villiers et al., 2015) predict the spread of B. dorsalis to areas further south within South Africa. This region (specifically, the Western Cape Province of South Africa) has a warm, temperate climate, with cool, wet winters and hot, dry summers. According to De Meyer et al. (2010), B. dorsalis prefers hot and humid environments, but can survive dry seasons. Bactrocera dorsalis was observed in areas of West Africa, the Sudan and Zambia where the climate has longer dry periods and hot conditions prevail during part of the year (De Meyer et al., 2010). Physiological traits and genetic adaptation to new host plants might also influence the ability of B. dorsalis to establish in areas predicted to be suitable and thus alter its fundamental niche during invasion (Hill and Terblanche, 2014). Climate change might not increase the possibility of B. dorsalis to establish in the Western Cape (Hill et al., 2016), but the adaptive capacity of traits of the flies’ thermal performance and survival will likely influence its ability to invade a new environment (Sinclair et al., 2012, Sgrò et al., 2016).

The aims of this study were therefore to determine acute temperature survival rates for several key life-stages of B. dorsalis, and to determine whether B. dorsalis have acute plasticity (i.e. can rapidly cold- or heat-harden (RCH or RHH, respectively)) that might aid their survival and population establishment in this geographic region, which is generally considered less favorable (De Meyer et al., 2010, De Villiers et al., 2015). The colony of flies we used for our experiments came from the recently invaded sub-tropical Limpopo Province in South Africa and the experiments were conducted after 11 months in the laboratory. Limpopo Province was first invaded during 2008, and then declared fully established in 2015 (Manrakhan et al., 2015). Most other experiments on the thermal survival rates of B. dorsalis were conducted using flies that originated from the tropics (Vargas et al., 1996, Vargas et al., 1997, Ekesi et al., 2006, Rwomushana et al., 2008) and being maintained for extended time periods in laboratory colonies. We were also interested in determining which life stage(s) are most resistant to thermal extremes to gain a better understanding of the species invasion ability to aid pest management or eradication efforts. To further understand the relative invasion risk we make use of comparisons with similar data presently available on con-familial species that possess both broader and narrower geographic distributions, but can be readily found in the region.