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Bed Bug Activity During Heat Treatments, and Physiological Effects Among Surviving Individuals Master’s Thesis 2018 60 ECTS Faculty of Environmental Sciences and Natural Resource Management Tone Birkemoe Bed bug activity during heat treatments, and physiological effects among surviving individuals Marius Saunders Biology Faculty of Biosciences 1 Table of contents Preface and acknowledgments 3 Abstract 3 1 Introduction 4 1.1 Bed bugs 4 1.2 Temperature limits for insects 4 1.3 Thermal tolerance for bed bugs 6 1.4 Pest control 6 1.5 Objective of the thesis 7 2 Materials and methods 7 2.1 Experimental animals and feeding 7 2.2 Bioassay 8 2.3 Experimental protocol 10 2.4 Experimental heat treatments 10 2.5 Response variables and collection of data 13 2.6 Statistical analysis 13 3 Results 15 3.1 Behavioral responses to heat 15 3.2 Long-term physiological damage caused to bed bugs by a short heat treatment 19 4 Discussion 21 4.0 Key results for discussion 21 4.1 Bed bugs responses to heat, activity and dispersal during a heat treatment 21 4.2 Possible mechanisms behind the physiological damage 24 4.3 Relevance to bed bug control 25 5 Conclusion and future directions 26 6 References 28 7 Appendix 33 2 Preface and acknowledgments This thesis was written as a part of an ongoing research program on bed bugs at the Department of Pest Control at the Norwegian Institute of Public Health (NIPH). Thanks to NIPH for use of laboratories, experimental animals and equipment. Especially thanks to my supervisors at NIPH Anders Aak and Bjørn Arne Rukke for guidance throughout the whole thesis, with topic for the thesis, creation of the bioassay, execution of the experiments, and helpful advices on the thesis structure and contents. I also thank my supervisor at NMBU Tone Birkemoe, and students Martin Paliocha and Kristian Seres for helpful comments on the thesis. Lastly, thanks to Ingunn Ruud for help with grammar and orthography. Abstract Simulated heat treatments with different heating rates were performed in experimental climate chambers to study bed bug behavior during rising heat. In addition, detrimental effects of these short time exposures to sub-lethal heat were recorded. On average, the bed bugs started to move as a reaction to the heat at 40°C. Some bed bugs reacted as early as 37°C, and others as late as 42°C. Heating rate did not affect the temperature that caused the initial movement response to the heat. Activity, measured as number of bed bugs walking at the same time increased from 37 to 42°C, and lower rate of temperature increase in the heat treatments reduced activity. As a consequence of the heat treatment, the bed bugs had a reduction in eggs per female, a reduction in hatching success of the eggs and reduced feeding abilities. The results from my thesis show that during heat treatments, pest controllers should be aware of bed bug activity when the temperature in the harborages passes 38°C, and increasing activity from this point. Figure 0: Thesis word cloud. Keywords: Bed bugs; Cimex lectularius; heat treatment; sub-lethal heat; behavioral response; heat avoidance; physiological heat response; pest control 3 Introduction Bed bugs can affect people in many negative ways. These include discomfort, mental health 1.1 Bed bugs issues (Doggett et al., 2012), and both public The common bed bug (Cimex lectularius) (Hwang et al., 2005) and private expenditure (Hemiptera: Cimicidae) is a flightless (Reinhardt and Siva-Jothy, 2007). Serious nocturnal insect, and an ectoparasite that feeds mental health issues as insomnia, anxiety, and on human blood (Usinger, 1966). Bed bugs are post-traumatic stress disorder can occur during an increasing problem all over the developed or after a bed bug infestation (Goddard and de world (Doggett et al., 2012). Norway has had Shazo, 2012, Susser et al., 2012). Pathogen a six-fold increase in treated infestations the transmission by bed bugs has been last ten years, with 500 in 2006 and 3000 demonstrated in laboratory experiments treated infestations in 2016 (Norwegian (Goddard and deShazo, 2009, Salazar et al., Institute of Public Health, 2017). The cryptic 2015, Leulmi et al., 2015), however, public nature of bed bugs makes control harder, as health reports have not found any evidence of bed bugs can hide in places that are difficult to bed bugs being responsible for any outbreak of get to during a treatment of the infestation infectious diseases (Lai et al., 2016, Delaunay (Doggett et al., 2012). Bed bugs have evolved et al., 2011). both behavioral and physiological resistance to Like most other mobile animals, activity in bed insecticides (Romero et al., 2007, Dang et al., bugs is controlled by many biotic and abiotic 2017), which has made bed bug control more factors, such as mate location, foraging, and difficult. Infestations also have increased due circadian rhythms. Mate location in bed bugs to more international and local travel; bed bugs occurs generally over a short range, as bed can disperse passively through human clothing bugs live in clusters (Usinger, 1966). Foraging (Hentley et al., 2017) and luggage (Reinhardt and host location is short range, compared to and Siva-Jothy, 2007). As bed bugs can live in other ectoparasites such as the tsetse fly furniture, acquisition of second hand items (Glossina pallidipes) (Voskamp et al., 1998). such as beds or upholstered furniture can Bed bugs are nocturnal, and is much more contribute to bed bug dispersal (Potter, 2006). active in the night than the day (Romero et al., Bed bugs are wingless, but can also disperse 2010), and human stimulus increase the bed actively through walking (Cooper et al., 2015). bugs activity (Aak et al., 2014). Abiotic factors Walking may be the most important form of as temperature has a big impact on activity for dispersal between rooms in the same building insects (Chown and Nicolson, 2004). (Reinhardt and Siva-Jothy, 2007). Bed bug infestations often start with only a few 1.2 Temperature limitations for insects individuals (Saenz et al., 2012, Fountain et al., Temperature affects biochemical reactions, 2014), and due to swift population growth, a protein structure, metabolism, and other small bed bug infestation can increase physiological traits in all living organisms exponentially to a huge bed bug population, (Garrity et al., 2010). In insects, temperature with a 35-fold increase per generation, which also controls important life-history traits, such is just three months (Polanco et al., 2011). as development time (Regniere et al., 2012, Campbell et al., 1974). Three general temperature ranges are used to describe the insect’s performance over a range of 4 temperatures. These are the optimal range, the (Moseley, 1997). The critical maximum sub-optimal range and the lethal range (Fields, temperature for Cataglyphis bicolor is 55°C 1992). The optimal temperature range is in the (Gehring and Wehner, 1995), 8°C higher than middle, were the insects have the best the average reported for other insects (Addo- performance, with sub-optimal- and lethal Bediako et al., 2000). The temperature range temperature ranges for both colder and hotter an insect can tolerate generally increases with temperatures on each side. The general ranges latitude, (Deutsch et al., 2008), consequently can be divided further; the sub-lethal range is the tropical bed bug (Cimex hemipterus) has a in the end of the sub-optimal range, just before shorter temperature range than the closely the lethal range starts. related common bed bug (Benoit, 2011). Behavior related to optimization of body Too high temperatures can decrease the fitness temperature is called behavioral of the insects by reducing the number of thermoregulation. Air temperature has a huge offsprings (Silbermann and Tatar, 2000) and impact on an insects body temperature as heat stress may increase the resources needed insects are poikilothermic (Gullan and to survive. The heat can be fatal by Cranston, 2010). Because the lack of internal denaturizing proteins, by causing cellular or regulation of body temperature, insects must tissue damage, and by destabilizing control their body temperature by other means. phospholipid membranes, which are central Body temperature of ectotherms is mainly components in stable functioning of the controlled by seasonal and daily temperature nervous system (Stevenson, 1985, Gullan and change, habitat choice, selection of Cranston, 2010, Fields, 1992). microhabitat (sun/shade, burrowing, climbing, Heat shock proteins (HSPs) can increase the and grouping), postural adjustments and thermal tolerance of insects (Gullan and physiological adaptions (muscle activity, Cranston, 2010, Moseley, 1997). Production of panting, urination, etc.) (Stevenson, 1985). In heat shock proteins are induced by several addition, some insects use behavioral stress-factors, among them heat, cold, and thermoregulation, such as the bumblebee starvation (King and MacRae, 2015), and a (Bombus spp.) uses flight muscles to increase few heat specialist insects can produce heat body temperature (Heinrich, 1975). shock proteins even prior to heat exposure The temperature range an insect species can (Gehring and Wehner, 1995). Heat shock tolerate varies with species. Insects have proteins increase thermal tolerance because it smaller variance in upper temperature limits, prevents denaturation of other proteins, and compared to lower limits (Neven, 2000). contributes to protein refolding (King and However, smaller variance in upper lethal MacRae, 2015, Denlinger and Yocum, 1998, temperatures does not mean that certain insects Tatar, 1999). Generally, for insects, Hsp70 is cannot survive in extremely high temperatures. the most important heat shock protein Ants in the genus Cataglyphis can tolerate associated with thermal protection (Chown extremely high temperatures, both because of and Nicolson, 2004, Denlinger and Yocum, physiological and behavioral adaptions; 1998); for bed bugs, both Hsp70 and Hsp90 are species in this genus can tolerate body highly produced during heat exposure, and temperatures around 53-55°C during associated with thermal protection (Benoit et scavenging mid-day in the Saharan desert al., 2009).
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