Dehydration dynamics in terrestrial arthropods: from water sensing to trophic interactions

Abstract

Since transition from water to land, maintaining water balance has been a key challenge for terrestrial arthropods. We explore factors that allow terrestrial arthropods to survive within a variably dry world and how these aspects shape ecological interactions. Detection of water and hydration is critical for maintaining water content. Efficient regulation of internal water content is accomplished by excretory and osmoregulatory systems that balance water intake and loss. Biochemical and physiological responses are necessary as water content declines to prevent and repair the damage that occurs during dehydration. Desiccation avoidance can occur seasonally or daily by a move to more favorable areas. Dehydration and its avoidance have ecological impacts that extend beyond a single species to alter trophic interactions. As climate changes, evolutionary and ecological processes will be critical to species survival during drought.

1. Importance of dehydration

1.1. Transition from water to land: coping with a new dry world

As arthropods made the transition from water to land, they went from living in a surplus of water to the frequent pressure of preventing the negative effects of dehydration (Fig. 1). While arthropods that reside in water sources with a high salt content (=higher osmolarity) also experience challenges in maintaining water balance, terrestrial environments typically pose more severe challenges than aquatic ones.

Figure 1 -.

Summary of the transition from water to land. As arthropods move from within water there are a variety of factors that must be overcome, where most involve losing the protection and support within an aqueous environment. A summary of factors that underlie the transition from water to land has been reviewed by Little (81) and Dunlop et al. (41). Figure illustrated with biorender.com.

The terrestrialization of arthropods did not occur as one specific transition, but rather multiple lineages transitioned from water to land starting at the Cambrian–Ordovician boundary onwards (ca. 488 Ma) with direct evidence of chelicerates in the Silurian (ca. 416-443 Ma) and hexapods in the Devonian (ca. 398-416 Ma (41, 81)). The process of moving to the terrestrial environment was accompanied by physiological changes including altered gas exchange, reproduction, osmoregulation, responses to exposure to ultraviolet radiation without the protection of water, and modifications of sensory organs to function in a dry environment (41, 81, 121). Details of these adaptations have been previously reviewed (41, 81). Following the transition to land, terrestrial arthropod species were able to diversify, with over 1 million extant species, representing a major component of the biodiversity of Earth. This review will focus on water homeostasis in terrestrial arthropods, ranging from how individuals detect water sources, to how organisms respond to varying internal levels of water, and to the impact of drought on ecological interactions.

1.2. Water is a critical resource

A great deal of research is devoted to the ability of insects to locate food sources or mates, but these activities are less urgent than maintaining water balance. During hot and arid periods, a terrestrial arthropod can die in as little as an hour if water stores cannot be replenished (12). Arthropods have particularly high water loss rates because they are small, and smaller organisms have a higher surface area to volume ratios that promote water loss across a surface (141). Oxygen represents the only factor that is more critical to survival, where death can occur within minutes. But oxygen consumption and gas exchange also result in water loss and this too scales with body size, such that smaller animals have higher water loss rates relative to gas flux (~metabolic) rates (88). Water can be acquired from imbibing liquid water, ingestion of food, or from the metabolic breakdown of specific nutrients. Metabolic water production likely occurs in most systems but is typically only a major water source for those with extremely suppressed water loss (10, 16). A few taxa can also obtain water directly from subsaturated air through uptake systems (4, 8, 17).

As water is not always available, the prevention of water loss represents a critical factor for survival. In general, species that reside in wet environments tend to have higher water loss rates compared to those that reside in drier habitats (12, 70, 148). The reduction of water loss is predominantly accomplished through behavioral shifts, direct changes in the cuticle (shifts in cuticular hydrocarbon types or abundance, different cuticle proteins, or changes in spiracle size (12)), or through a reduction in breathing, suppressing transpiration through the cuticle and respiratory water loss, respectively (28). A balance in obtaining water and preventing water loss allows terrestrial arthropods to maintain water homeostasis and survive. As climate change progresses, drought is expected to increase in duration, frequency, and intensity, (34), thus establishing how terrestrial arthropods respond to potential or actual dehydration will be critical for understanding changes in populations of these species and their impacts on humans.

2. How arthropods sense water and water vapor

The ability to locate water relies on a combination of visual and chemosensation cues to find water or wet materials (Fig. 2). Visual cues rely on light polarization to distinguish large bodies of water, which are mostly associated with aquatic insects, and those that deposit eggs in bodies of water (20, 61, 62). Humidity detection and contact with a moist surface represent the critical methods for the location of water (12, 44). This is accomplished through two distinct mechanisms; 1. contact that likely operates through the gustatory system and 2. detection of varying humidity levels in the air by the olfactory system. Humidity and water detection studies have been limited to Drosophila and mosquitoes (29, 44, 77, 86), however, electrophysiological surveys have identified humidity sensitive sensilla in other arthropods (128, 129).

Figure 2 -.

Humidity detection localization on terrestrial arthropods. There is a combination of vision, humidity, and contact detection that allows insects to visualize large bodies of water, locate water or moist substrate for water ingestion, and contact with liquid water based on osmolarity levels. Lastly, an internal detection system allows for the regulation of water content within the individual arthropod. A combination of these factors allows for the terrestrial arthropods to maintain water balance. Figure illustrated with biorender.com.

2.1. Humidity detection

Few studies have directly addressed specific receptors associated with humidity detection with nearly all studies on Drosophila (44, 76). Ionotropic Receptors (IRs) have been identified as the major humidity detectors in insects. IRs have been linked to the detection of temperature, taste, and humidity, where there are even overlapping roles in specific IRs for multiple cues (19, 134). Multiple IRs have been identified in the sacculus of Drosophila antenna, which directly is linked to water sensing in flies. The IRs found in Drosophila have closely-related orthologs, indicating that IR-based humidity detection likely occurs in most insect systems and related arthropods such as mites (19, 65, 127). The co-expression of IR21a, IR25a, and IR93a are involved in the detection of water and cool temperatures (76). For mosquitoes, IR21a is involved in heat sensing (53), further highlighting the dynamics between thermal and humidity sensing in insects. For mosquitoes, IR8a has been linked to altered water detection (105). The association between IRs that sense thermal changes and humidity suggest that there is neural integration of these cues. This is not surprising; vapor pressure deficits directly link humidity and temperature to water loss (60).

Along with the role of IRs, odorant binding proteins (Obps, low-molecular weight soluble proteins that may act as carriers for specific chemicals) have been tied to humidity detection. As with IRs, this has only been examined in Drosophila. One specific obp, Obp59a, is highly conserved and is necessary for hygroreception in Drosophila (122). Mutants for Obp59a have an impaired ability to detect water and increased survival during desiccation (122). The specific mechanism of how this Obp is involved in humidity detection is unknown, but the abundance of Obps in arthropod systems presents the possibility that others will have similar roles in humidity detection and helps clarify how receptors in aqueous solution can detect changes in humidity in the external environment (127, 136).

2.2. Contact detection of water and drinking

Liquid water is not only in water bodies, but can be accessed from saturated soil or other moist materials, and contact detection of moisture is necessary. This specifically involves channel proteins that respond to the osmolarity levels of the water. The pickpocket (ppk) gene has been tied to the cellular and behavioral responses to water osmolarity in mosquitoes and Drosophila (26, 27, 86). In Drosophila, PPK28 has been linked to response to osmolality changes and potentially serves a role in gustatory water detection (27). In mosquitoes, ppk301 is expressed in legs and acts in the mechanical response to water and salt (86), likely playing a critical role in the decision where oviposition occurs.

Insects need to know when to drink water and this likely involves the integration of both external cues like humidity and internal cues such as osmolality. Nanchung, a transient receptor channel, acts to restrict water consumption in Drosophila (66). Nanchung expressing neurons in the taste center of the brain work to regulate both water and sugar consumption responding to cues from the hemolymph. Mechanosensation of water and osmolarity detection needs further investigation to establish the mechanisms used to identify water sources and maintain hydration in arthropods. Studies in genetically accessible insects such as Drosophila and the yellow fever mosquito, Aedes aegypti, may point the way to common mechanisms across taxa.

3. Behavioral dynamics of arthropods in humid and dry environments

3.1. How does humidity alter insect behavior?

Most terrestrial arthropods are more active during more humid periods. There are a few exceptions and extended periods of water levels near saturation can yield overhydration and increase the likelihood of fungal growth (146). During periods of rest, such as during the night and hot periods during the day, most species will search for or move into the area of the microhabitat with the highest relative humidity (73). This ability to move between varying relative humidity can occur since it is likely that most terrestrial arthropods can sense humidity gradients with variations as low as 20% RH (44). Movement into reprieves during periods of low humidity, movement within these reprieves into the most favorable location, and subsequent emergence when conditions are more favorable are critical for survival in dry areas.

3.2. How does hydration status impact behavioral changes across daily and seasonal cycles?

There are distinct changes in insect behavior and distribution associated with daily and seasonal cycles. Many insects undergo periods of inactivity in refugia and this occurs in both the winter, to avoid cold and dryness, and as aestivation during hot and arid periods (8). Most species have decreased water loss rates in their diapause stage, usually due to a combination of reduced respiration and increased cuticle waterproofing, along with retreating into protected areas (8, 11). An alternative is a movement to more favorable regions, from short distances (e.g. to permanent water bodies or within hibernacula) to migrations across hundreds of kilometers (36, 63). Long-distance movement was thought to be limited to a few species, but wind-borne migration at higher altitudes has been demonstrated to move insects long distances (63, 64).

Daily variation in the potential for dehydration is common. In general, warm dry periods during mid-day represent the period when most insects are most susceptible to desiccation, due to the highest vapor pressure deficit. As such, few terrestrial arthropods are active during this time, with most insects active at dusk, night, and dawn, but a few taxa, such as bees, are active during the photophase (18, 131). If factors such as humidity directly impact daily activity, this has not been well-established. Reliance on humidity cues would be unreliable to set circadian changes, as precipitation could supersede daily humidity changes.

3.3. Food vs. water: eat to rehydrate

A few organisms do not directly drink water, but rather have unique mechanisms to obtain water from the air (discussed below) or their water budget is obtained from a meal (13, 75). Feeding to hydrate is limited, where most feed on water-rich foods, such as blood and plant-based fluids. To survive this lifestyle, an organism will need to ensure that feeding occurs regularly (tsetse flies, which feed every two to three days (9)) or have the ability to withstand long periods without water, common in beds bugs and other members of Cimicidae (10). Of interest, when in environments that are extremely dry, such as sub-Saharan Africa or in many human dwellings (85), obtaining water from a large bag of fluid (e.g. human or livestock) may be more likely than obtaining free water. Most arthropods obtain water by drinking liquid water and by eating. In these situations, changes in water availability may lead to changes in consumption of moist food (88) or altered intake of macronutrients (5, 23, 47), to maintain water balance through dietary intake of water or metabolic water production, respectively.

4. Molecular and biochemical responses to dehydration

4.1. Transcriptional shifts genomic changes prevent dehydration-induced damage

Molecular and biochemical responses to dehydration stress have been studied in multiple systems, which has expanded with new technologies that allow for the assessment of complete transcriptional, metabolite, and proteomic shifts (57, 112, 140) (Fig. 3). Changes include increases in ubiquitin-dependent proteolysis, heat shock proteins, and oxidative stress proteins (12, 125, 126). These changes are most likely to prevent, scavenge, and repair cellular damage during dehydration. Expressional changes in aquaporins or other transmembrane genes do not usually occur during dehydration stress in most terrestrial arthropods (12, 125, 126), even though these are critical to water homeostasis, but play critical roles in water and ion regulation. A reduction in metabolism commonly occurs during dehydration and reduces water loss through respiration, which has been supported by RNA-seq and functional studies in several systems (12, 125, 126). Cytoskeletal changes have been noted in both transcriptional and proteomic levels (79, 82) to support cell structure as the insect encounters conditions that would threaten internal homeostasis. Lastly, transcriptional changes involved in amino acid and carbohydrate metabolism have been associated with dehydration in multiple insect systems (57, 126), where the increase in these metabolites play a critical role during dehydration stress in providing energy and acting as a buffer (discussed in metabolite section below) or could be involved in the production of metabolic water. More lineage-specific differences occur, such as increased levels of autophagic-associated genes during extreme dehydration in the Antarctic midge (124) and changes that allow for post-dehydration responses, such as increased water vapor uptake in ticks when humidity increases (112).

Figure 3 -.

Molecular and biochemical aspects that occur when terrestrial arthropods are exposed to dehydration. Figure illustrated with biorender.com.

Specific genomic changes have been linked with dehydration resistance (51, 68, 107, 108). One factor that has been identified is specific chromosomal inversions associated with increased dehydration resistance in mosquitoes (51, 108, 140). Other aspects have been identified through genome sequencing following prolonged selection for increased dehydration resistance in Drosophila (68). Specific genes with positive selection following artificial selection included those involved in cuticle structure and development (cuticle proteins) along with a multitude of other specific genes (68). Importantly, many of the genomic factors that underlie the increased dehydration resistance following selection are not aspects typically known to increase during dehydration, suggesting the potential evolutionary changes that increase dehydration resistance may vary from those that are directly critical for survival during acute exposure to dry periods.

4.2. Metabolite shifts preventing dehydration-induced damage

A suite of other metabolite shifts is critical to allow for rapid survival and recovery from desiccation stress. Importantly, many of the processes to increase metabolites are not without cost, where each bout of dehydration/rehydration will result in a metabolic breakdown of nutrient reserves (15, 110). If the life stage feeds, replenishing nutrient reserves is relatively easy, but for species that rarely feed (ticks or diapausing adults) or stages incapable of feeding (pupae) these bouts of dehydration can eventually exhaust nutrient reserves. Glycerol represents one of the most common metabolites increased, which acts to protect unwanted biochemical interactions (7, 147). Trehalose is commonly noted to be increased during dehydration stress in multiple systems (113), which likely acts similarly to glycerol and protects cells from potentially damaging biochemical interactions or serves in osmolyte balance. Increased trehalose and other sugars within the hemolymph likely act as an immediate energy source to restart metabolic processes to repair the damage. Multiple amino acids are increased during dehydration stress, with proline and alanine being most common (57, 84, 112, 142). These metabolites are not likely only colligative and fully interchangeable during dehydration stress (132), rather there may be overlapping and specific roles for each metabolite.

4.3. Population differences in the response to dehydration

Dehydration resistance varies both between species and among populations of the same species (31, 71, 107). Most studies of differences among populations have focused on insect eggs, e.g. Aedes or Drosophila (31, 70, 71, 107). In Drosophila, species with the strongest basal desiccation resistance show the least plasticity, and that basal resistance is higher in drier locations (70), but does not vary with latitude unlike thermal tolerance (2). A variety of differences between populations related to desiccation resistance have been identified, including distinct genomic variation, shifts in gene expression profiles, altered structural aspects (e.g. cuticle changes), and distinct variation in survival under dry conditions (31, 70, 71, 107). In general, populations collected from drier environments display increased dehydration resistance. This suggests that inferences related to drought tolerance for a species as a whole should be made only after examining the dehydration response in multiple populations of that species, but that species-level basal desiccation resistance may be important for understanding sensitivity to climate change (71).

5. Physiological responses to dehydration

5.1. Malpighian tubules and hindgut in water regulation

Internal water regulation is predominantly accomplished by generation of primary urine by the Malpighian tubules (MT) and selective reabsorption by the hindgut . The MT open into the gut at the junction of midgut and hindgut, allowing the latter to act both on waste food and urine. The main function of the hindgut is to allow water and other key ions and other compounds to be re-absorbed, allowing defecation of dry waste such as non-toxic uric acid and other products.

The mechanisms underlying the MTs role as the kidney equivalent has been extensively examined and studies have begun to elucidate cellular differences that may be underlying functional differences in this organ (25, 80, 96, 100, 115, 144). A general synopsis of MT factors that underlie the function of this organ in relation to water balance can be found in Figure 4. For Drosophila, and likely other systems, there are filtration nephrocytes (garland cell nephrocytes and pericardial nephrocytes) that occur outside the MT involved renal process, but these are mainly involved in filtration, rather than osmoregulation (96), as such aren’t discussed in this review. The adult MT are functionally analogous to renal tubular systems and, in Drosophila, develop from the ectodermal hindgut primordium and visceral mesoderm (67). The MT directly attaches to the hindgut at the posterior midgut and consists of a varying number of epithelial tubes depending on the lineages (21, 40, 115). Single-cell RNA-seq studies in Drosophila have established that there are nine distinct cell types associated with the MT, which consist of two types of stellate cells, six types of principal cells, and stem cells (80, 144). The differences in the cell types suggest that PC and SC likely have functional differences depending on their location in the MT, specifically whether in the upper, main, or lower tubules or as part of the ureter. Similar cell type differences based on transcript level variation are likely to occur in other terrestrial arthropods as cell shapes vary throughout the length of the MT (43, 138).

Figure 4 -.

Function of the Malpighian tubules in relation to hormonal control during dehydration based on mosquito and Drosophila studies. Top, location of the Malpighian tubules. Middle, specific factors in the principal (left) and stellate (right) cells that are involved in the movement of water and ions from the hemolymph to the tubule lumen for removal within the urine (25, 96, 115). Bottom, an image of the Malpighian tubules from Drosophila showing the principal and stellate cells. Tubule photomicrograph courtesy of Dr. Anthony Dornan. Figure illustrated with biorender.com. *, occurs in only mosquitoes.

The function of the MT relies on a combination of specific proteins that transport water and other small molecules from the hemolymph into the MT lumen for diuresis (Fig. 4). A specific combination of aquaporins is critical to the transport of water, glycerol, and urea in both the PC and SC. A combination of ion channels allows for the movement of specific factors such as chloride and potassium and specific pumps act in the movement of hydrogen, potassium, and sodium ions (25, 80, 96, 100, 115, 144). The specific activity of these factors relies on the dynamics between the relative abundance of the specific channels and pumps along with factors that regulate their activity, such as hormonal cues discussed below.

5.2. Internal control of water homeostasis - diuretic and anti-diuretic hormones

Factors that regulate the internal water content consist of a suite of hormones that regulate water release (diuretic) and retention (anti-diuretic) (99). Specific hormones that underlie the processes of water regulation have been examined extensively in Drosophila due to genetic tools available, and in mosquito and kissing bug systems, as blood gluttony yields unique water balance requirements (25, 100, 115). Outside of insect systems, there is some focus on factors that act in the regulation of diuresis in ticks (145), but little is known about this process in other terrestrial arthropods. In Drosophila, active cation transport is stimulated by three peptides: DH₃₁ and DH₄₄ (acting through cAMP) and CAPA (acting though calcium/cGMP). In Rhodnius, DH₃₁ acts as a natriuretic agent, prompting sodium release and diuresis, 5-HT serves as a kaliuretic, prompting the release of potassium and diuresis, and DH₄₄ serves as a general diuretic factor (24, 25, 72, 100, 115). Kinin-like peptides act as diuretic factors on the stellate cells, acting though calcium to stimulate chloride conductance, and the biogenic amine tyramine acts similarly.

5.3. Alternative mechanisms for hydration - water vapor uptake

Hydration can occur by routes other than the ingestion of liquid water and food. One of the most unique processes is the ability to utilize water from subsaturated air (water vapor absorption), which occurs in at least 60 species and has evolved independently at least eight times (98). The specific site where this occurs varies between species, such as oral routes in ticks and some cockroaches, rectal-based mechanisms which have been noted in fleas, thysanurans, and some beetles and lice, or directly through the cuticle or some specific cuticle-associated structure (4, 98). Some mechanisms are extremely efficient and allow replenishment of water near 40% RH and others can only accomplish this process near saturation between 98-99% RH. The process that allows this to occur is the presence of hygroscopic material or fluid in or on a specific tissue or organ, which allows water to be drawn from the air and moved into the arthropod. The properties of this material vary, but most are a variety of salts, carbohydrates, amino acids, and polyhydric alcohols (e.g. glycerol) that promote water absorption (4, 98). Water vapor absorption is an active process that is energy-depleting. This has been demonstrated in ticks, where the process of generating hygroscopic materials and hydration will drastically reduce survival between the rare blood meals (74, 110). More details on this process have been previously reviewed by O’Donnell and Machin (98), but little is still known about the molecular mechanism during the processes, except that gamma-Aminobutyric acid (GABA) likely drives secretion by tick salivary glands to promote water uptake (112).

5.4. Impact of dehydration on other physiological aspects (reproduction and cross-tolerance)

Cross tolerance between dehydration and other stress types has been documented in multiple terrestrial arthropod systems (111, 119, 120). The most common type is where slight bouts of dehydration increase the cold tolerance in many species (14, 119). This is most likely since cellular dehydration is a common component associated with cold stress (95, 102, 119). Dehydration in the presence of ice (cryoprotective dehydration) occurs in many terrestrial arthropods, specifically small species that reside within the soil that have higher water loss rates (30, 42, 69). The impact of short bouts of dehydration on other stress types is not as conclusive.

Bouts of dehydration seem to lead to decreased growth rates (58) and a general reduction in reproductive output (1, 15, 46), which is likely due to issues in metabolism and stress. Prolonged selection for dehydration yields a general reduction in reproductive output in Drosophila (1). The specific role of dehydration in relation to immune responses in insect systems has been understudied, where dehydration may increase or suppress immune responses (146, 149).

SIDEBAR - Extreme dehydration – Anhydrobiosis

A few terrestrial arthropods can lose nearly all of their water content, and is almost exclusively midges and collembolans. A model for this process is the sleeping chironomid, Polypedilum vanderplanki, which resides in dry regions of Africa. The larvae are present at the bottom of temporary water pools that commonly dry. To survive, larval stages will lose 97% of their water content and resume activity following subsequent hydration, even after 17 years in the dehydrated state. While in this dehydrated state, these larvae can tolerate extreme heat, cold, and even exposure to the vacuum of space (59). Importantly, many of the mechanisms that are utilized by this system to prevent dehydration damage are similar to other insects but are more extensive (12, 14, 126). Metabolome and transcriptome studies have revealed that there is a massive increase of trehalose, accumulation of components of the citric acid cycle, and mechanisms to accumulate stable waste products (113). Genomics studies have revealed that distinct paralogous stress-associated gene clusters are highly expressed in desiccating larvae (55, 113).

6. Role of dehydration in ecological interactions

6.1. Connecting behavioral responses to dehydration and trophic interactions

Insects and other arthropods employ a variety of behavioral approaches to avoid or cope with dehydration and these activities have profound impacts on trophic interactions. Under desiccating conditions, arthropods may either seek out additional water sources, e.g. (6, 45, 91, 139), or seek refugia that lower water loss rates (32, 88). When terrestrial arthropods seek water sources, sometimes the only available water is within food, resulting in increases in consumption of vegetation by herbivores or prey by predators (88). For instance, studies have documented increases in consumption of moist leaves by crickets (Gryllus alogus) and increases in consumption of crickets by spiders (Hogna antelucana) in response to limited drinking water (78, 92). Other studies show similar patterns for parasites and plant-arthropod interactions (see 6.2 and 6.3). On the other hand, although arthropod-based examples are lacking, when animals seek refugia to prevent water loss, their rates of consumption should decline, reducing the strength of species interactions (vertebrates examples, e.g. (37, 52)). A complex set of tradeoffs likely influences whether dehydration results in increased consumption and stronger trophic interactions versus increased time in refugia and weakened trophic interactions. The availability of refugia, the need for reproductive activities, the longevity of the animal, the degree of predation risk, the water loss rate relative to metabolic rate, and the water content of food items, all likely influence when and where animals seek refuge versus increase consumption as a response to desiccating conditions.

6.2. Impact of dehydration on parasite-host interactions

Dehydration has been demonstrated to impact arthropod disease vector interactions with their host and dynamics between parasitoid wasps and their fly host (22, 57, 112) (Fig. 5). For mosquitoes, dehydration increases host landing and blood feeding in multiple species, which is likely to have a significant impact on disease transmission by mosquitoes (57). Importantly, this only occurs during actual dehydration and not only exposure to dry conditions. Similarly, dry periods have been demonstrated to both increase and decrease tick activity, suggesting that questing for hosts and subsequent tick-borne disease transmission is impacted by dry periods (17, 106). Along with vertebrate-disease vector interactions, dehydration drives increased parasitism by wasps (22). These studies provide evidence that host-parasitism dynamics are impacted by both dry conditions and dehydration.

Figure 5 -.

Specific interactions between species in relation to dehydration stress based upon studies that have assessed the impact of dehydration on ecological interactions of terrestrial arthropods. In order from top to bottom, plant-arthropod pest interactions (49, 87, 89, 123), parasitoid-host dynamics (22), predation of aphids by beetles (2), mosquito-host-drought impacts on blood feeding (57, 60), arachnid predation or questing is suppressed by arid periods (17, 88, 112), and wolf spider predation is shifted from small conspecifics to crickets when water is not available (92). Figure illustrated with biorender.com.

6.3. Plant-arthropod interactions under dry conditions

The effects of plant water deficits on the interactions between plants and arthropod pests have been examined, with most studies focusing on pestiferous insects and mites (49, 87, 89, 123). These effects are inconsistent across studies, possibly because water-stressed plants may have higher nutrient levels, likely due to increased foliar nitrogen in relation to total mass, but other aspects, such as leaf water potential, may limit feeding in specific species (49, 116). These effects may differ with the duration or periodicity of drought (49). Hydration of plant-feeding arthropods can also impact plant-arthropod interactions, altering feeding rates and the ability of arthropods to reduce the toxicity of plant defensive compounds (109). In general, specialist pests seem to be more negatively impacted by severe drought, while benefiting under mild/moderate stress, and generalist pests may proliferate most under more severe dehydration stress (35, 49) (Fig. 5). Importantly, few studies have addressed the impact of variable drought stress (mild to severe) on both plants and arthropods during their interactions (49), suggesting that the full extent of plant-arthropod interactions under drought are not yet understood.

6.4. Dehydration, food webs, and ecosystems: how do changes in species interactions alter entire food webs and ecosystems?

The responses of entire food webs and ecosystems to desiccating conditions often depend on trophic interactions, with arthropods frequently playing an important role (97). For example, in experimental mesocosms, large wolf spiders (H. antelucana) have been shown to switch between consuming energy-rich small spiders (Pardosa spp.) under wetter conditions and water-laden crickets (G. alogus) under drier conditions (78). Similar patterns have been seen in large open-air manipulations, with large spiders causing trophic cascades under dry conditions (large spiders suppress crickets, reducing their effect on leaf material), but not causing these trophic cascades under wetter conditions (93).

Although sometimes trophic interactions dominate ecosystem responses to drought, in other cases bottom-up effects of water on plants may dominate or at least complicate predictions (3, 89, 94). Animals may experience water stress when plants do not, e.g. when plants can access groundwater (114), or plants may experience water stress when animals do not, e.g. when herbivores can still obtain enough water from water-stressed plants or locate surface water sources (83), or both plants and animals may simultaneously experience water stress (but explicit examinations of both are scarce). In situations where animals experience water stress, but plants do not, arthropod trophic interactions likely play a key role in understanding the dynamics of the system (top-down effects are important, e.g. (93)). Alternatively, when plants experience water stress, but animals do not, food web and ecosystem dynamics may be governed by the responses of the plants themselves, whether mediated by changes in plant nutrient content (49), plant defensive compounds, or simply changes in primary productivity (94). When both plants and animals experience water stress, predictions are complicated. Although arthropod examples are limited, some studies suggest that bottom-up effects on primary productivity may predominate in these situations (3), while other studies suggest that direct effects on trophic interactions are most important (38). It may be that this depends on traits of the specific members of the food web or that systems oscillate between bottom-up and top-down effects over time (94). Continued research on the effects of altered plant and animal water balance on food webs and ecosystems is needed, especially in light of climate change.

7. Long-term adaptations and recent evolution to survive in dry environments

7.1. Wet and dry environments shape insect diversity.

Terrestrial arthropods have expanded into nearly all environments. Although exceptions exist (e.g. bees, which are most diverse in temperate regions, (101)), there is a general trend where species diversity and abundances of terrestrial arthropods are higher in wet, warm tropical habitats (33). Temperate regions usually represent a middle ground with temperate dry regions generally having less species (130, 143). Elevational changes in tropical areas can lead to similar patterns, where higher elevations are usually drier and colder, leading to reduced abundances in terrestrial arthropod diversity and abundances (33). Desert regions are sometimes limited to a few species (e.g. ants, specific beetles, firebrats, and spiders) with extremely low water loss rates and other traits that enable their survival in these inhospitable environments (32, 56). Similarly, polar regions are limited to specific species, which can be locally abundant, that can tolerate the extreme cold and dryness of these regions (104). Along with general trends, the stability of water availability (and the environment in general), leads to larger and more diverse terrestrial arthropod communities in complex environments (33, 117, 143). Regions with extended and severe dry seasons (or dry, winter periods) will be dominated by species that can decline and rebound during growing seasons following dormancy or migration to survive the inhospitable periods (39).

7.2. Climate change, drought, and insect distribution.

Climate predictions suggest that the duration and periodicity of extreme weather will increase, including droughts (34, 133). These climate changes, along with urbanization (see 7.3) and other factors, have led to significant reductions in terrestrial arthropods during the Anthropocene (135, 137). The effects of climatic shifts in water availability and vapor pressure deficit on insects have been understudied relative to thermal shifts, which is surprising given the direct relationship between relative humidity and temperature in relation to water vapor deficits (60). Moreover, dry periods impact, and even increase, arbovirus transmission by mosquitoes, alter tick questing, and impact the survival and proliferation of many critical insect pests (57, 88, 112, 116, 118).

Directly assessing the impact of drought is much more difficult than thermal stress, as exposure to dehydrating conditions does not always yield actual dehydration. Additionally, experimental dehydration is sometimes hard to achieve when food must be provided, and can be more challenging to measure than body temperature. Thus, careful studies of the effects of dehydration have rarely been conducted (57). Selection-based studies to determine how species may respond to an increasing period of drought have been limited to Drosophila (48, 50), which limits our predictions of how terrestrial arthropods might adapt to increasing drought prevalence. Importantly, future studies will need to examine population differences (dry-adapted vs. wet-adapted lines) or focus on prolonged selection to both thermal and dehydration stress to determine how specific species may adapt to climate change.

7.3. Cities and indoor habitats are dry or wet islands

Human development has created substantial changes to the environment (Fig. 6), and nowhere is that more apparent than in cities and within buildings. Cities and indoor locations have unique biophysical characteristics and the impact of humans in creating these environments varies based on the natural local environment and social systems (85). Residential parts of cities and indoor environments tend to be drier in mesic regions and wetter in xeric regions (54, 85). Urbanization has been shown to influence the hydration of arthropods (90). Hydration of arthropods in cities can influence their demand for macronutrients (5) and the relative abundance of arboreal species (91). The numerous potential impacts of these human-created dry or wet islands on insects need further study, particularly given the direct effects on humans living in these environments.

Figure 6 -.

General factors that will impact terrestrial arthropods during drought and urbanization. A. Increasing periods of drought will reduce water availability both as free resources (e.g. water pools) and within food sources (plants and other animals). B. Specific factors are necessary to survive immediate and prolonged exposure to arid conditions. The mechanisms that increase dehydration resistance long-term (permanently increased in dehydration resistance) do not necessarily overlap with the factors that allow survival during acute, severe dehydration stress. C. Urbanization will have varying impacts where urbanization will see a general decline in species diversity, urbanization will have varying impacts on water availability depending if a city is in a wet or dry environment. Lastly, as buildings become larger the indoor biome space increases significantly in size (85). Figure illustrated with biorender.com.

8. Conclusions and future directions

Dehydration has been a continual pressure on arthropods since their movement into the terrestrial environment. The ability to resist dehydration has been critical to the proliferation of terrestrial arthropods, especially insects and mites, which has allowed their domination in most, if not all biomes. Climate change is leading to rapid changes in water availability (34) and increases in temperature that create increasing vapor pressure deficits that desiccate insects. Human development can also alter water availability and vapor pressure deficits, across cities, and within buildings (85, 103). These factors will have a major impact on the proliferation of both beneficial and pestiferous species. To fully understand these impacts, more in-depth studies will be needed to measure how drought and dehydration directly alter terrestrial arthropods, how drought impacts interactions between terrestrial arthropods and their food sources, and how climate change and urbanization interact with water deficits to impact the proliferation of terrestrial arthropods.