Pareuchaetes Insulata (Walker) (Lepidoptera: Erebidae), to Low Temperatures
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Bulletin of Entomological Research (2017) 107, 448–457 doi:10.1017/S0007485316001103 © Cambridge University Press 2016 Reduced mobility but high survival: thermal tolerance and locomotor response of the specialist herbivore, Pareuchaetes insulata (Walker) (Lepidoptera: Erebidae), to low temperatures O.O. Uyi1,2*, C. Zachariades3,4, E. Marais5 and M.P. Hill2 1Department of Animal and Environmental Biology, University of Benin, P.M.B. 1154, Benin City, Nigeria: 2Department of Zoology and Entomology, Rhodes University, P.O. Box 94, Grahamstown 6140, South Africa: 3ARC – Plant Protection Research Institute, Private Bag X6006, Hilton 3245, South Africa: 4School of Life Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville 3209, South Africa: 5Centre for Invasion Biology, Stellenbosch University, Private Bag X01, Matieland 7602, South Africa Abstract Disentangling the responses of insects to variations in their thermal environment is central to our understanding of the evolution of temperature-dependent performance in thesespecies.Here,wereportresultsofexperimentsexaminingtheeffectsofhigh(upper lethal temperature = ULT) and low (lower lethal temperature = LLT) temperature and exposure time onthe survival of larvae and adults ofa multivoltine,nocturnal moth spe- cies, Pareuchaetes insulata, a biological control agent whose impact on an invasive weed, Chromolaena odorata has been variable in South Africa. The influence of temperature and acclimation onlocomotion performance ofthe moth wasalsoinvestigated. Temperature and duration of exposure significantly affected survival of both adults and larvae of P. insulata with more extreme temperatures and/or longer durations proving to be more lethal. Third instar larvae and adults are both freeze intolerant and had LT50 of −5.9 and −4.7°C, respectively, after a 2 h exposure. Although cold acclimation was beneficial to the nocturnal larvae, temperatures below 10°C significantly reduce their locomotion activities. The average daily minimum temperatures in the coldest months at three locations in South Africa are over 5°C lower than those of Fort Lauderdale, Florida, USA, where P. insulata was originally collected. Our results suggest that lethal high or low temperatures at short timescales are trivial in explaining the variable per- formance of P. insulata, but reduced locomotion at sub-lethal temperatures may be an importantdriverofthepopulationdynamicsofthebiocontrolagent (especiallyinwinter months) and may consequentlyexplain the low population levels of the moth because of possible reduced feeding by larvae during night-time low temperatures. Keywords: Pareuchaetes insulata, locomotion performance, acclimation, lethal temperatures, biological control agent, Chromolaena odorata (Accepted 18 October 2016; First published online 15 December 2016) Introduction *Author for correspondence Phone: +234 80380 130 12 Ambient temperature is a key environmental factor Fax: +234 052 602370 influencing a variety of aspects of animal ecology and E-mail: [email protected] evolution, especially for ectotherms due to their limited Downloaded from https://www.cambridge.org/core. Stellenbosch University, on 22 Aug 2017 at 06:55:11, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0007485316001103 Reduced mobility but high survival 449 thermoregulatory capacity. For example, insect performance P. insulata could also be due to temperature incompatibility traits such as development rates, fecundity, longevity, and (Uyi et al., 2016a) or their response to lethal or sub-lethal tem- mobility (Bale et al., 2002; Hughes et al., 2004; Tamiru et al., peratures over long periods or at short time scales. To our 2012; Ferrer et al., 2014;Wattet al., 2016) coupled with physio- knowledge there are no published studies on the thermal tol- logical and biochemical processes (Hochachka & Somero, erance and the effect of temperature on the locomotion ability 2002; Denlinger & Lee, 2010; Terblanche, 2013) are strongly af- of P. insulata. Therefore, knowledge of the effects of tempera- fected by ambient temperatures. Insect response to tempera- ture on the activity of P. insulata can assist in determining the ture extremes is thought to be a key driver of life cycle effects of sub-lethal temperatures on biological activities such events, species geographic distribution and population dy- as feeding by the larvae of the moth. Such a study may be help- namics in time and space (Terblanche, 2013). At longer time ful in terms of (i) understanding the establishment failure of scales, temperature not only influences survival but also sea- the moth at some release sites, (ii) understanding the poor per- sonal and evolutionary processes (Denlinger & Lee, 2010) re- formance of the moth, (iii) predicting the potential distribution sulting in variation of life history traits and the development of of and the impact of the moth in relation to the South African phenotypic plasticity (Chown et al., 2007; Régnière et al., 2012; climate and (iv) predicting more suitable release sites. Ferrer et al., 2014). The ability of temperature to influence sur- Because temperatures that are lethal to insects are a func- vival and activities (e.g., locomotion, feeding) at short time tion of both the degree of the temperature variation and the scales is also of critical importance (e.g., Li et al., 2011; duration of exposure (Chown & Nicholson, 2004;Liet al., Esterhuizen et al., 2014). Empirical evidence suggests that in- 2011), this study investigated a range of time-temperature sect species have an optimal temperature range (where per- combinations, which may be lethal at short time scales in lar- formance reaches a maximum); outside of this range, vae and adults of P. insulata. A further objective of this study performance rapidly decreases (e.g., development is slowed, was to investigate the effect of acclimation (thermal history) on mobility is reduced, see Wu et al., 2013; Esterhuizen et al., the locomotion performance of the larvae of P. insulata, 2014; Hough-Goldstein et al., 2016) and mortality may occur because the relationship between ambient temperatures and due to alterations in physiological and metabolic activities insect performance has been previously reported to be de- (Angilletta et al., 2002; Martin & Huey, 2008; Angilletta, 2009). pendent on thermal history at several timescales in some in- Understanding variation in insect thermal tolerance is im- sects (e.g., Deere & Chown, 2006; Esterhuizen et al., 2014). portant in the applied context (e.g., Terblanche, 2014; Zhao Similarities or differences in seasonal temperature patterns be- et al., 2015). The predictions of biological response to tempera- tween the collection and release sites (introduced range) can ture variation are used in population forecasting models help explain the success or poor performance of biological con- (Terblanche et al., 2008; Zhao et al., 2015; Hough-Goldstein trol agents (Hopper & Roush, 1993; Byrne et al., 2003). In order et al., 2016), which influence pest management decisions to determine whether climate incompatibility is a primary fac- such as whether to release certain biological control agents tor responsible for the poor establishment success or variable or to integrate conventional control methods with biological performance of P. insulata in South Africa, we compared cli- control. About 40% of weed biological control agents (usually mate data (daily minimum and maximum temperatures aver- insects) fail to establish while a number of others perform aged per month) between Fort Lauderdale, Florida, USA, poorly in their introduced ranges (McEvoy & Coombs, where P. insulata was collected and locations (Durban South, 2001). Some of these failures can be attributed to climate in- Umkomaas, and Thohoyandou) in South Africa where the compatibility, especially with low temperatures (McClay, host plant of the moth is invasive. 1996; Byrne et al., 2002, 2003; May & Coetzee, 2013). Therefore studies on thermal tolerance and locomotion per- formance of the specialist herbivore, Pareuchaetes insulata Materials and methods (Walker) (Lepidoptera: Erebidae: Arctiinae) [released in Study organisms South Africa (between 2001 and 2009 for the biological control of the invasive alien weed, Chromolaena odorata (L.) King and Chromolaena odorata is an invasive perennial shrub native to Robinson (Asteraceae)] are not inconsequential. the Americas from southern USA to northern Argentina Following the release of over 1.9 million individuals of dif- (Gautier, 1992). In its invasive range, C. odorata grows in a ferent life stages of the moth (from Florida – USA, Cuba and wide range of vegetation types such as forest margins, grass- Jamaica), only the Floridian population is thought to have lands, roadsides, agricultural lands, and disturbed forests established (880 000 individuals of different life stages), posing a significant threat to agriculture, biodiversity and liveli- at only one site, after it was released at some 21 sites in hoods(seereviewsinZachariades etal.,2009;Uyietal.,2014aand KwaZulu-Natal province (north-eastern South Africa), South references therein). The shrub can grow 2–3 m in height. Prolific Africa (Zachariades et al., 2011). flowering peaks in December to January in the northern hemi- Prior to the release of P. insulata, two related species, sphere and June to July in the southern hemisphere. Pareuchaetes pseudoinsulata Rego Barros and Pareuchaetes aurata