Ecological consequences of climate stress

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Ecological consequences of climate stress

Increased temperature and thermal fluctuations

To improve predictions of species responses to climate change, thermal fluctuations should be taken into account (Thompson et al. 2013; Vasseur et al. 2014). Predicted increases in the amplitude of thermal fluctuations elevate the risk of detrimental effects of temperature stress on animals, as the risk of experiencing temperatures close to, or even above, their CT max increases (Hansen, Sato, and Ruedy 2012; IPCC 2014; Stillman 2019). Furthermore, studies have found that a period of extreme heat can have a larger impact than a moderate increase in mean daily temperatures (Vasseur et al. 2014).
Theoretically, it has been shown that insects developing in a fluctuating environment live at temperatures lower than that of their thermal optima, which greatly limit the risks of deleterious temperature effects when thermal fluctuations occur at high amplitudes (Sunday et al. 2014). Therefore, the fitness of these insects could be expected to increase with the mean temperature of the environment. Insects developing in environments having relatively constant temperatures should have a thermal optimum close to the environmental temperature, due to the reduced risk of occurrences of detrimental thermal fluctuations; for these organisms, increasing temperature should thus result in steep fitness decline. This is why tropical species have long been considered as being more sensitive to climate change than their temperate relatives (Deutsch et al. 2008). However, recent research has also reported that some temperate insects may also live in thermal niches with temperatures close to their thermal optima, meaning that their fitness and/or current distribution could also be affected by climate change (Johansson, Orizaola, and Nilsson-Örtman 2020).
Finally, changes in humidity can be a direct effect of increased temperatures that should increase desiccation risks for small animals like insects. Moreover, predicted shifts in entire weather systems should reduce rainfall in certain areas (Trenberth 2011). In turn, desiccation can further affect insects’ ability to cope with temperature stress owing to the physiological costs incurred by desiccation stress (Kleynhans, Clusella-Trullas, and Terblanche 2014). Meanwhile, positive effects have also been reported when physiological responses to climate change overlap with desiccation (particularly tolerance to freezing temperatures, Sinclair et al., 2013). The latter effect is based on what is called cross tolerance, which is when increased tolerance to one stressor induces tolerance to another (Gotcha, Terblanche, and Nyamukondiwa 2018).

Invasive species

One of the currently well-characterized effects of increasing temperatures is the range expansion (movement) of species (Hickling et al. 2006), and displacement of populations to avoid being exposed to unfavourable conditions. In particular, movements of populations towards the north (in the northern hemisphere), or movement uphill, have been reported. This is thought to occur either to mitigate temperature change, or because the warming climate makes a wider area suitable for species that were normally living in habitats at lower altitude or latitude (I. C. Chen et al. 2011; Parmesan and Yohe 2003; Sunday, Bates, and Dulvy 2012). In sum, warming may open new niches for ectotherms. Increase in average temperatures can facilitate the spread of certain species, previously limited in their range by thermal limits (Battisti et al. 2005). Such range changes have been well documented in butterflies. For example, Parmesan et al. (1999) found that over half of 35 non-migratory European butterfly species had shifted their range northward during the 20th century.
In addition, invasion of species by human transportation may increase a species’ range (Ward and Masters 2007). Insular ecosystems, including (relatively) small islands, where ecological niches can be poorly diversified, are prone to invasion. The high level of endemism and total of few species means island communities often evolved at a low biotic pressure, which also renders them vulnerable to effects of invasive species (Case 1990). Large scale changes in species range can cause new biotic interactions to occur, such as increased competition or predation, which could decrease the ability of vulnerable species to persist (Tylianakis et al. 2008). Furthermore, habitat disturbance by human activity is associated with invasion success (Gonzalez, Lambert, and Ricciardi 2008; Lozon and MacIsaac 1997). By consequence, with the increasing ease of movement of goods and people over the last decades, invasive species are establishing populations in far reaching places of the world. As range-shifting and invasive species adapt to local thermal conditions, it has been shown that thermal ranges are increased at expansion fronts (Hillaert et al. 2015), and several examples of changes in traits that follow a pattern of the residence time of individuals at a locality have been described (Fronhofer and Altermatt 2015; Ochocki and Miller 2017; Renault et al. 2018). Such adaptations could further increase the possible range of an invading species.

Mild winters

Insect development often requires thermal seasonality, with life cycles being completed in the periods where it is most favourable. In many habitats, winter temperatures result in the need for either migration or entering diapause in the form of eggs, larva, or more rarely, as adults in order to survive (Yang and Rudolf 2010). Diapause is a dynamic state of low metabolic activity, characterized by inactivity, morphogenesis and a pause in reproductive function, regulated by different environmental signals preceding the occurrence of unfavourable conditions (Tauber, Tauber, and Masaki 1986). Diapause can also refer to aestivation, or summer diapause, commonly triggered by arid conditions (Storey and Storey 2012). Animals cannot break diapause immediately, even if favourable conditions appear, and it should be seen more as a process rather than a status (Koštál 2006). During the diapause period, survival is directly linked to environmental temperatures, warmer winter temperatures usually being associated with increased mortality (Marshall and Sinclair 2012; Sobek-Swant et al. 2012; Stuhldreher, Hermann, and Fartmann 2014). A shorter winter has been shown to reduce emergence and increase time to emergence in insects (Bosch and Kemp 2004; Stålhandske, Gotthard, and Leimar 2017). At the same time, it has been shown that the return of favourable temperatures earlier in the season should trigger continued development sooner, which has been observed in several species, and can lead to a de-synchronization of life cycles of interacting species, be it host and parasite or plant and insect, with possible additional detrimental consequences (Yang and Rudolf 2010).
In addition, shorter and milder winters, giving longer and warmer summers, can decrease ectotherms’ cold tolerance. For example, exposure to winter (extreme) warm spells reduced cold tolerance in emerald ash borer (Agrilus planipennis) even after they had been returned to low temperatures (Sobek-Swant et al. 2012). Furthermore, it has been shown that summer acclimated or acclimatized insects will generally show more cold sensitivity (Block 1990; Košťál and Šimek 1996). Nonetheless, increase in average winter temperatures has been shown to increase the average number of species in terrestrial communities, possibly due to range expansion of many species (Bowler et al. 2017).

Climate stress tolerance strategies

Adaptation or acclimatization to stressful conditions/extreme temperatures include morphological, behavioural, ecological and/or physiological changes. Insects can change morphologically by for example reducing body size or melanism or increase pubescence. Changes in body size has been observed in several species as a response to climate change, but the direction of change varies as well as suggested causes, from changes in food availability to temperature (Gardner et al. 2011; Sheridan and Bickford 2011). In a review of studies on morphological changes associated with recent climate change (temperature or precipitation), only changes in coloration often had a strong association to climate change (MacLean et al. 2019). A very specialized example of morphological adaptation are desert beetles with a body shape specially capable of collecting water droplets from fog or morning dew at the mouth for ingestion (Guadarrama-Cetina et al. 2014; Hamilton and Seely 1976).
Behavioural changes include, for example, habitat selection and changes in activity patterns (Hutchison and Maness 1979). General behaviour to cope with stressful situations include sit-and wait strategy, where the animals reduce activity to an absolute minimum in hopes of surviving until the environment is suitable again (Renault, Hervant, and Vernon 2003; Renault and Coray 2004). This greatly contribute to reduce energy expenditure, water loss and potential exposure to environmental pollution, making it a possible solution to endure a wide range of stressors. Oppositely, an individual might increase activity for foraging or looking for a more suitable habitat (Lorenzo and Lazzari 1998; Yu et al. 2010). When experiencing stress, animals might also burrow into the ground awaiting better conditions (Bayley et al. 2010). Research is still needed to try to develop a universal framework for standardized behavioural tests, in order to determine if a stressor is above a critical level. As behavioural observations are often less stressful and invasive for the experimental animals, recognizing general and easily observed behavioural responses could improve ethical and economical implication of risk assessment of environmental factors, and is therefore of great interest. Recently, methods for large-scale phenotyping of the behavioural responses of insects to thermal stress have been proposed (Laursen et al. 2021).
When animals go through so called ecological changes, it can have detrimental effects on the function of an ecosystem, because for example changes in timing of phenology can cause mismatches with interacting species, with potential detrimental outcomes (Parmesan and Yohe 2003; Yang and Rudolf 2010). Over the last decades, a trend of advancement of phenological traits in the spring and summer have been described for plants and animals, but with a stronger effect in insects than plant, which could lead to a decoupling of plant-insect interactions (Gordo and Sanz 2005).
Tenebrionid beetles can serve as a clear example of insects adapted behaviourally, morphologically, and physiologically to their environment. They can be found naturally in areas like the African dry savanna, where they spend the hot dry season as adults rather than larvae like most other insects (Zachariassen and Einarson 1993). As the name Tenebrionid (also called darkling beetle) indicates, these insects spend their lives in darkness, to avoid the hot and dry surface of their natural habitat. They have an extremely impermeable cuticle which reduces their transpiratory water loss, in combination with fused elytra which reduces respiratory water loss from abdominal spiracles (Ahearn 1970; Zachariassen 1991). In addition, their metabolic rate is so low that respiratory water loss from breathing is minimized and they can reabsorb almost all water in the gut, producing extremely dry faeces (Zachariassen et al. 1987).
Physiological changes can involve several other responses, such as increased production of certain proteins or changing metabolite composition in the haemolymph, described in more detail below. Some of the more important responses, such as heat shock protein regulation and freeze tolerance, are described below because of their high relevance in the field of thermal tolerance, despite not being included in the work of this thesis.

Heat shock proteins and chaperones

Heat shock proteins (hsps) were first discovered in 1973 after subjecting Drosophila cells to heat shock (Tissieres, Mitchell, and Tracy 1973). Because this category of proteins was highly induced by the high temperature treatment, they were given the name heat shock proteins (hsps). Since then, hsps have been observed in most living organisms and the production of these proteins is elicited by a variety of stress (Parsell and Lindquist 1993). In the process of uncovering their functions, several groups of hsps have been discovered, and they have been grouped in families named after their molecular weights (for example Hsp70 constitutes proteins weighing approximately 70 kilodaltons) (Brocchieri, Conway de Macardio, and Macario 2008; Hoffmann, Sørensen, and Loeschcke 2003). These proteins can protect the cell either by ensuring the function of other proteins in the cell, increasing degradation of dysfunctional proteins and/or inhibiting stress induced apoptosis (cell death) (Parsell and Lindquist 1993; Samali and Cotter 1996). Because they prevent improper protein associations, they are also called protein chaperones. Hsps are both inducible (only expressed following stress), constitutive (always expressed) and forms that are always present and yet can be induced following stress. The main trigger for heat shock protein induction is thought to be the presence of abnormal (denatured or unfolded) proteins, themselves resulting from the stressful conditions (Ananthan, Goldberg, and Voellmy 1986; Lepock, Frey, and Ritchie 1993).
During heat stress, small sections of a denatured protein can bind to a hsp. It is the binding of only a small section of the substrates that allows many hsps to be so versatile, because it means that they are not limited by substrate size. Low levels of ATP are typical in heat stress, and this causes the hsp binding site to be kept closed until it can bind ATP again. This sustained binding keeps proteins from aggregating during heat stress (Vollemy and Boellmann 2007). In addition to preventing aggregation of denatured proteins, hsps can untangle proteins that have already aggregated. In this process, alternating cycles of hsp binding, protein unfolding and hsp release, converts proteins in a stable misfolded aggregated state to a temporarily unstable state, which can then allow the spontaneous correct folding of individual proteins (Ben-Zvi et al. 2004). Hsps’ role in degradation of damaged proteins largely entails contributing in the ubiquitin-proteosome pathway, which is also one of the cells main degradation pathways under normal conditions. When a hsp is bound to an unfolded protein, it can recruit Ubiquitin, which is also a hsp, which functions as the tag, marking substrates for proteasomal degradation.
Apoptosis inhibition is another function of hsps, which not only improves the integrity of cell proteins, but the entire cell. Hsps can either reduce cell damage and thereby prevent the death, or they can inhibit the activation or activity of sensor or effector molecules, and thereby inhibit stress induced apoptosis (Mosser et al. 1997). In fact, several points of function for hsps are being identified in the apoptosis pathways, making them important apoptosis regulators (Lanneau et al. 2008). This is a role of hsps that has been given a lot of attention, because it seems that these protective mechanisms can also stabilize mutant proteins, and thus enables tumour cells to function. Furthermore, the anti-apoptotic system appears to protect these cells from dying, and thus could be major carcinogens.
Because several types of stress result in the induction and activation of a common set of stress proteins, hsp induction can be associated with increased tolerance to subsequent stress conditions. The molecular basis of this cross tolerance is that these proteins remain active and their expression remains elevated. This occurs for a period of time dependent on several factors such as species, cell-type, prior stress exposure (history), interactions between genes and the environment during development and the stress severity (Kültz 2005). This is advantageous for organisms thriving in unstable environments, where they can be exposed to more than one type of stress over a short time period, or even at the same time.
The many beneficial effects of the hsps suggest that it would be advantageous to always have a high level of hsp expression. However, their gene expression is usually not maximized but highly regulated, suggesting a cost related to expression of these proteins, as is the case for many hsps (and other stress responses). When hsps are induced, a large reduction in other protein synthesis has been observed, meaning these proteins are built at the expense of others (Feder et al. 1992). This means that normal cell function is shut down during the stress response, clearly demonstrating that such protein expression cannot persist (Sørensen, Kristensen, and Loeschcke 2003). Furthermore, Krebs and Feder (1997) showed that overexpression of hsp70 reduced growth, development and survival in transgenic Drosophila melanogaster larvae, even though it increased protection, and thus survival, during heat stress exposure. Feder and Hofmann (1999) suggested that the underlying cause of these effects could be that hsp production is associated with a significant consumption of cell nutrients and/or too much pressure on the anabolic/catabolic apparatus for proper processing of other important substances. Thus, the regulation of hsps (as many other stress responses) is a consequence of apparent cost/benefit trade-offs, but the mechanisms behind the deleterious effects are unclear. Yancey (2001) illustrated that reduction in cell content of an hsp (hsp70) coincided with increased levels of other chaperones and cryoprotectants, most of which are molecules with a relatively small production cost. This can help explain why the cell can keep increasing survival while downregulating stress proteins (Dahlgaard et al. 1998).
In conclusion, hsps are important in relation to stress resistance, as they ensure the proper function of proteins, contribute to degradation of damaged polypeptides and increase cell survival. These benefits come at a cost, which is why they are carefully up- and downregulated in the cell.

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Oxidative stress

Oxygen is an essential substance for all animals, but it is also the cause of many pathological conditions and associated with the natural aging process, due to its biotransformation into reactive oxygen species (ROS) (Hermes-Lima and Zenteno-Savın 2002). Additionally, stressful conditions can cause overproduction of ROS, which can damage important cellular molecules, leading to, for example, lipid peroxidation, protein oxidation and DNA damage. This is why mechanisms to limit ROS formation, repair damage and detoxify damage products are of vital essence for all organisms (Fridovich 1998). In response to ROS stress, antioxidant defences include metabolites such as ascorbate and vitamin E, peptides such as glutathione and thioredoxin, and enzymes such as superoxide dismutase (SOD), catalase (CAT), thioredoxin peroxidase and selenium-dependent glutathione peroxidase (Se-GPX) (Felton and Summers 1995; Storey and Storey 2010). It has been shown that animals that experience oxidative stress regularly maintain high constitutive levels of antioxidants, whereas others demonstrate inducible defences (Hermes-Lima and Zenteno-Savın 2002).
Measurements of the total antioxidant capacity (TAC) describe the cumulative action of all antioxidants in an organism, which account for the actions of known (and measurable) and unknown antioxidants, as well as their interactions affecting productivity (Ghiselli et al. 2000). Measuring important antioxidant enzyme activities as well as TAC, Zhang et al. (2015) found increased antioxidant capacity in the ladybeetle Propylaea japonica at high, but not lethal, temperatures. Furthermore, low temperature has been shown to increase antioxidant activity in Alphitobius diaperinus (Lalouette et al. 2011). This indicates that thermal stressors lead to oxidative stress in insects, for which antioxidant activity is increased to limit oxidative damage.


There is considerable variation in the level of dehydration that insect species can endure. Studies have shown that the tolerable body water loss is only 20% in the beetle Callosobruchus maculatus (Yoder, Christensen, and Keeney 2010), while it can reach 90% in the semiaquatic beetle Peltodytes muticus (Arlian and Staiger 1978). Water loss tolerance does not only vary between species, but also between developmental stage, sex, or age (Hadley 1994). It is generally important in stress research to consider all such factors when executing experiments, in order to reduce variance and increase validity of results. As mentioned earlier, some animals have adapted to dry conditions by reducing water loss, for example by having very low cuticular water permeability (Zachariassen 1991) or by absorbing a very large amount of water from faecal material before excretion (O’Donnell and Machin 1991). An alternative solution to tolerating dry conditions and high water loss is the ability developed by some organisms who can absorb water from the surrounding air by accumulation of sugars and polyols in the body fluids, so that it creates hyperosmoticity, causing water to enter through a permeable cuticle. This phenomenon has been described for the springtail Folsomia candida (Bayley and Holmstrup 1999), which seems to be the coping strategy for mild water stress for the springtail. When water stress increases, the animal then dehydrates to a state resembling anhydrobiosis (Sjursen, Bayley, and Holmstrup 2001). Tenebrionid larvae can also absorb vapor from the surrounding air, down to 88% relative humidity (L. L. Hansen, Ramløv, and Westh 2004).

Table of contents :

Chapter 1
Thermal performance curve
What is stress?
Ecological consequences of climate stress
Increased temperature and thermal fluctuations
Invasive species
Mild winters
Climate stress tolerance strategies
Heat shock proteins and chaperones
Oxidative stress
Other extreme temperature tolerance strategies
Metabolomics – finding the players of physiological responses to stress exposure
Measuring toxicity
Types of insecticides
Pathways of uptake and excretion
Ecological consequences of pesticides in the environment
Pesticide and temperature interactions in insects
Effect of temperature on pesticide sensitivity in insects
Pesticide effect on temperature sensitivity in insects
This thesis
Aims and hypotheses
Biological models
Merizodus soledadinus
Alphitobius diaperinus
Chapter 2
Thermal tolerance patterns of a carabid beetle sampled along invasion and altitudinal gradients at a sub-Antarctic island
1 Introduction
2 Methods
2. 1 Insect collection
2. 1. 1 Invasion gradient
2. 1. 2 Altitudinal and lowland gradients
2. 2 Measurement of the duration of recovery from cold and heat exposures
2. 3 Statistical analysis
3 Results
3. 1 Recovery of adult M. soledadinus sampled along an invasion gradient transect
3. 2 Recovery of adult M. soledadinus sampled along an altitudinal gradient
3. 3 Duration of recovery of adult M. soledadinus exposed for different time periods
3. 4 Duration of recovery of adult M. soledadinus sampled along a seashore-inland transect
4 Discussion
4. 1 Thermal sensitivity of M. soledadinus adults sampled along an invasion gradient
4. 2 Adult M. soledadinus sampled along an altitudinal gradient
4. 3 Adult M. soledadinus sampled along a seashore-inland transect and exposed for different time periods
5 Conclusions
Supplementary material
Chapter 3
Thermal plasticity and sensitivity to insecticides in populations of an invasive beetle: Cyfluthrin increases vulnerability to extreme temperature
1. Introduction
2. Materials and methods
2.1. Rearing of the insects
2.2 Experimental design
2.2.1. Characterization of the thermal tolerance of the insects from different populations
2.2.2. Effect of daily heat spikes and cyfluthrin exposure
2.2.3. Effect of daily heat spikes and cyfluthrin exposure on recovery from exposure to extreme temperatures
2.3. Data treatment
3. Results
3.1. Characterization of the thermal tolerance of the insects from different populations
3.2. Effect of daily heat spikes and cyfluthrin exposure
3.3. Effect of daily heat spikes and cyfluthrin exposure on recovery from exposure to extreme temperatures
4. Discussion
4.1 Characterization of the thermal tolerance of the insects from different populations
4.2. Effect of daily heat spikes and cyfluthrin exposure
4.3. Effect of daily heat spikes and cyfluthrin exposure on recovery from exposure to extreme temperatures
5. Conclusion
Supplementary File 1
Supplementary File 2
Supplementary File 3
Effect of heat and pesticide exposure on Alphitobius diaperinus
1 Introduction
2 Methods
2.1. Rearing of the insects
2.2 Experimental chamber preparation
2.3 Exposure treatment
2.4 Physiological Analyses
2.5 Reproduction
3 Results
4 Discussion
Chapter 4
Desiccation in the lesser mealworm Alphitobius diaperinus
1 Introduction
2 Methods
2.1 Collection and rearing of insects
2.2 Effects of desiccating conditions on the survival and physiology of the insects
2.2.1 Survival of the insects exposed to desiccating conditions
2.2.2 Measurements of body water and sugar content
2.2.3 Metabolomics
2.3 Effects of desiccating conditions on activity and reproductive capacities of the insects .. 136
2.3.1 Measurement of locomotor activity
2.3.2 Measurement of the reproduction capacities of the beetles
2.4 Statistics
3 Results
3.1 Survival of the insects exposed to desiccating conditions
3.2 Effects of desiccating conditions on sugar content and metabolic profiles
3.3 Locomotor activity of the beetles
3.4 Reproductive capacities
4 Discussion
Supplementary Material
Chapter 5
General discussion on the scientific contributions of the thesis’ results and future perspectives
Warming and geographic expansion of alien species
Thermal tolerance breadth
Effects of climate change and pesticides on A. diaperinus


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