Animal Functional Traits Associated with Fire Sensitivity: History
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Eugênia K. L. Batista
,
José E. C. Figueira
,
Ricardo R. C. Solar
,
Cristiano S. de Azevedo
,
Marina V. Beirão
,
Christian N. Berlinck
,
Reuber A. Brandão
,
Flávio S. de Castro
,
Henrique C. Costa
,
Lílian M. Costa
,
Rodrigo M. Feitosa
,
André V. L. Freitas
,
Guilherme H. S. Freitas
,
Conrado A. B. Galdino
,
José E. Santos Júnior
,
Felipe S. Leite
,
Leonardo Lopes
,
Sandra Ludwig
,
Maria C. do Nascimento
,
Daniel Negreiros
,
Yumi Oki
,
Henrique Paprocki
,
Lucas N. Perillo
,
Fernando A. Perini
,
Fernando M. Resende
,
Augusto H. B. Rosa
,
Luiz F. Salvador
,
Larissa M. Silva
,
Luis F. Silveira
,
Og DeSouza
,
Emerson M. Vieira
,
Geraldo Wilson Fernandes

Changes in fire regimes in the 21st century are posing a major threat to global biodiversity. In this scenario, incorporating species’ physiological, ecological, and evolutionary traits with their local fire exposure might facilitate accurate identification of species most at risk from fire. 

  • fire ecology
  • resilience
  • sensitivity
  • functional traits
  • savanna ecosystems
  • species vulnerability
  • fauna
  • fire exposure

1. Introduction

Natural fire has shaped species evolution in savanna ecosystems worldwide [1][2]. In these ecosystems, animal species are relatively tolerant to low-severity and patchy fires. Natural fires usually allow individuals to survive or reestablish populations from adjacent preserved ecosystems after burning. However, extreme wildfires have resulted from a synergy between severe droughts, high temperatures, low air humidity, windy days, and increased human ignitions, which increase the flammability of terrestrial ecosystems and expand fire’s niche around the world [3][4][5][6]. Recent studies show alarming prospects, suggesting that under different future climate scenarios, changes in fire regimes are expected in the 21st century in terms of a meaningful increase, variability, and frequency of extreme events posing a major threat to global biodiversity [6][7].

2. Animal Functional Traits Associated with Fire Sensitivity

Researchers compiled 14 species traits that can increase the vulnerability of the species to the direct and indirect effects of fire. These traits are explained in detail below and are summarized in Table 1.
Table 1. Animal functional traits associated with fire sensitivity or fire resistance/resilience.
  Trait Group Increase Vulnerability Decrease Vulnerability
DURING FIRE Dormancy Species that often express deep torpor on flammable surfaces in the flame zone. Non-hibernators; species that rapidly arouse from shallow torpor when exposed to smoke or flame noises; species that remain in torpor in places protected from fire, such as in deeper soil layers
Escape decision Animals that run away randomly when frightened; fossorial species with shallow burrowing behavior; species that take shelter in flammable or suffocating places, such as plants in the lower layers, litter, or cavities in small trees. Animals that run toward nearby refuges when frightened; fossorial species with deep burrowing behavior; scansorial animals that seek refuge on top of tall trees during surface fires, in water, in termite mounds, or on rocky surfaces with little flammable material.
Habitat use Leaf litter-dwelling fauna in the o-horizon and other species that live or build nests in the lower strata of vegetation on flammable substrates, such as shrubs, grasses, dry and/or fallen trunks and branches, and small trees. Soil-dwelling species that can burrow deeper into the ground; species that live or build nests close to perennial wetlands or water sources (semi-aquatic habits), below-ground, on rocky substrates, termite mounds with low flammability, and deep cavities inside massive tree trunks or in the upper strata of vegetation (on the top of tall trees).
Mobility Limited movement capability: slow-moving animals, weak flyers, ground-dwelling species that fail to climb trees, smaller jumpers with reduced effective jump height. Good or excellent movement capability: fast runners, strong flyers, skilled climbers, larger jumpers with great effective jump height, and other jumping specialists that use catapult mechanisms.
Morphology Medium-bodied animals that may have difficulty fleeing or finding refuge; species whose bodies are covered with long, coarse fur or feathers. Small-bodied animals that can find refuge more easily during a fire, while larger ones can flee or move away from affected areas; species with short fur, smooth skin, or covered with scales.
Nest substrate Species using flammable materials to build nests: thatched mounds, moss and lichen, fine grass or mammalian hair, and plant material such as bark, fiber, leaves, twigs, grasses, tussocks, and branches. Species that use thermally insulating building materials: great amounts of soil in hard, protective clay mounds; species with deliberate behavior for modifying their surrounding environment causally reducing flammability; species that build subterranean nests without thatched mounds.
Reproductive cycles Synchronous reproduction, usually at the end of the dry season, exposing fragile life stages, pregnant, lactating, nesting, and brooding females to high-intensity fire. Year-round breeders or species that reproduce during the wet season but decrease reproduction during the dry season.
Sensory detection of fire cues Species that spend most of their time in complex vegetation and rely primarily on the visual detection of fire (small-bodied animals could be even more vulnerable, as they usually have lower visual acuity). Species that are able to detect olfactory and/or acoustic fire cues; species that can detect fire cues at lower thresholds; species that have thermoreceptors that can detect infrared radiation from fires; species relying primarily on the visual detection of fire, but that spend most of their time in the top of tall trees or open, low-stature vegetation and topographically simple landscapes.
Social organization Solitary animals or those that live in small family groups (parents and young); species with poorly developed social relationships (e.g., groups with weak connections) and whose individuals or groups lack effective communication skills. Gregarious animals living in large groups; social species or those residing in more connected, reciprocal, and socially homogeneous groups.
  Behavioral plasticity Late-successional species that require more structured habitats for nest sites and foraging, which take several years to recover. Generalists that can temporarily adapt their diet and/or habitat preferences to the conditions and food resources available across the post-fire landscape; species that may benefit from fire-induced changes include early or mid-successional species.
POST-FIRE Dormancy Species that express multi-day torpor but need to rewarm frequently; species that use daily torpor, which is not as deep as hibernation, lasts only some hours rather than days or weeks, and is usually—but not always—interrupted by daily foraging and feeding. Invertebrates that remain inactive after a fire, allowing their tissues to become desiccated (anhydrobiosis); invertebrates that express aestivation and remain in an inactive stage remarkably resistant to water loss; species that use multi-day torpor for weeks or even months after a fire or during fire season without the need to rewarm.
Endogenous circadian rhythms Diurnal ectotherms that depend on thermoregulation opportunities afforded by habitat structure; strictly diurnal prey species. Nocturnal or crepuscular species; cathemeral or diurnal prey that can adjust their daily activity patterns.
Mobility Species with restricted home range; species with high site fidelity or territorial species; Migratory species (highly mobile), but with strong site fidelity. Highly mobile species that travel long distances or show metapopulation dynamics; species with low site fidelity or non-territorial species.
Morphology Large ectotherms; invertebrates with thinner cuticles. Large mammals; species capable of camouflaging in the scorched substrate; invertebrates with higher cuticle thickness.

2.1. During Fire

High environmental temperatures predispose animals to heat stress, including physiological and behavioral disturbances such as hyperventilation and loss of coordination. For any species, there is a body temperature threshold beyond which cells undergo denaturation of proteins and membrane structures degrade, causing the individual’s death [8][9]. Beyond the heat from flames, reduced oxygen and exposure to toxic compounds following smoke inhalation may be critical factors that increase animal mortality during a fire [10]. The longer an animal is exposed to high temperatures, anoxia, or smoke inhalation, the greater the chances of mortality; therefore, detecting and avoiding fire are essential behaviors for survival, especially for less mobile animals [11]. It is also important to mention the increased vulnerability of prey to opportunistic predators while trying to escape fires. The physical and behavioral traits that can increase or decrease a species’ sensitivity to the direct effects of a fire are described in detail below and illustrated in Figure 1.
Figure 1. Fire vulnerability traits of species during wildfires. In green are animals that are most likely to survive the burning (decreased sensitivity). In black are animals whose traits increase their probability of death (increased sensitivity).

Dormancy

Being in a torpor during a wildfire may increase or decrease the chances of survival, depending on shelter security and depth of torpor. Low body temperatures are associated with decreased responsiveness (both sensory and locomotor function remains limited) and torpid animals might therefore face an increased mortality risk during fires due to inhalation of toxic smoke, oxygen depletion, and heat exposure [12]. Even though torpid animals can respond to fire stimuli, they may be slow in doing so; therefore, when in deep torpor animals are at risk of not responding to fire cues quickly enough to survive [13].
Increased sensitivity: Species that often present deep torpor on flammable surfaces in the flame zone [14].
Decreased sensitivity: Non-hibernators; species that rapidly arouse from shallow torpor when exposed to fire cues [13][15]; species that remain in torpor in places protected from fire, such as in deeper soil layers.

Escape Decision

When an animal becomes aware of approaching fire, it has two possible escape options: it can move away or find shelter. In the first approach, complex physiological adjustments, which include increases in oxygen consumption, body temperature, heart rate, and blood flow to skeletal muscle prepare the animal for prolonged strenuous activity [11]. As a result, the animal tends to move away from the threat. The alternative behavioral response involves stopping moving, bradycardia, and depression of metabolism [16]. As a result, the animal tends to hide in nearby refuges. Each decision will have different implications for the individual’s survival.
Increased sensitivity: Species that run randomly when frightened can become disoriented when surrounded by fire [10]. In this case, animal survival depends on speed, agility, spatial memory, and a good navigation capacity, which can be compromised when in panic (or under severe stress). However, not only extreme heat but also smoke can affect the animal’s ability to navigate, causing disorientation while trying to escape [17][18][19]. Fossorial species with shallow burrowing behavior may also die, as fire can induce advective flows in soils (e.g., shallow-nesting mining bees) [20][21][22][23]. Species that take shelter in flammable or suffocating places, such as plants in the lower layers, litter, or cavities in small trees [23].
Decreased sensitivity: Species that run toward nearby refuges when frightened. In this case, animal survival depends on how protected refuges are. Small animals using deep burrows or termite mounds as main shelters (e.g., lizards that flee to termite mounds and soil burrows) [24]. Scansorial species that seek refuge on top of tall trees during surface fires, in water, or on rocky surfaces with little flammable material.

Habitat Use

Typically, savanna fires produce flames of 1–2 m in height, which consume all the herbaceous and most of the woody vegetation of about this height [25][26]. Depending on how the species uses the habitat for nesting, foraging, or shelter, it may be more or less exposed to fire. More vulnerable and less mobile stages (e.g., eggs, offspring, larvae, pupae, and pre-emergent adults found in nests) are particularly susceptible to burning. Nest residents may die from lethal substrate heating unless the nests are adequately insulated.
Increased sensitivity: Leaf litter-dwelling fauna in the O-horizon [27][28] and other species that live or build nests in the lower strata of vegetation on flammable substrates, such as shrubs, grasses, dry and/or fallen trunks and branches, and small trees. For example, macroinvertebrate detritivores such as millipedes (Diplopoda), woodlice (Isopoda), and fly larvae (Diptera: Nematocera); fungivorous such as fungus gnats (Diptera: Sciaridae), and predators such as spiders (Araneae), centipedes (Chilopoda), and ground beetles (Coleoptera: Carabidae) [28]; leaf-litter herpetofauna [29][30]. Above-ground nesters that use pre-existing cavities made by other organisms in the thinner branches and smaller trees [31]; species nesting in soil deposits in cracks and crevices of soil-limited landscapes that occur in rock outcrops [32].
Decreased sensitivity: Soil-dwelling species, such as earthworms and worm lizards, that are able to burrow deeper into the ground (10–20 cm deep) [33][34]; species that excavate, use pre-existing holes or natural cavities underground to take shelter, or build nests (below-ground nesters) [35]; species that live or build nests close to perennial wetlands or water sources (aquatic or semi-aquatic habits), on rocky substrates, termite mounds with low flammability, and deep cavities inside massive tree trunks or in the upper strata of vegetation (on the top of tall trees) [36][37][38][39][40].

Mobility

This trait is associated with the species’ ability to flee from the flame zone. Species that exhibit more powerful and flexible movement capabilities should be better able to escape fires.
Increased sensitivity: Nonvolant species of relatively low vagility, including amphibians, snakes, small lizards with short limbs (slow-running animals), and slow-moving animals such as sloths, turtles, and molluscs in general [34][41][42][43][44]; larger arboreal animals that are expected to attach less well to surfaces and have more difficulty distributing loads uniformly across large contact areas [45]; ground-dwelling species that fail to climb trees [7][46]; smaller jumpers with reduced effective jump height [47][48]; weak flyers with shorter wings and smaller flight muscles that usually can only fly a short distance at lower strata of vegetation on the flame zone [49][50].
Decreased sensitivity: Fast runners that can reach higher maximum speeds and escape the flames or travel greater distances, increasing the chances of finding safe shelter away from the fire [51]; birds that can fly higher and avoid the rising column of gasses, smoke, ash, particulates, and other debris produced by a fire [52][53]; lizards with longer limbs, larger toe pads, and more lamellae can run faster, exert stronger cling forces, and perch higher [54]; skilled climbers able to reach the tops of taller trees (at least 4–5 m above) [7][9]; larger jumpers with great effective jump height and other jumping specialists (e.g., arthropods that use catapult mechanisms [47][48].

Morphology

Body size can influence the animal’s ability to find shelter or flee during a fire.
Increased sensitivity: Medium-bodied species may have difficulty fleeing or finding refuge and are more susceptible to direct mortality during the fire or increased chances of predation following a fire [55]. Terrestrial mammals whose bodies are covered with long, coarse fur may be more affected by fire due to the greater flammability of their bodies [56].
Decreased sensitivity: Small-bodied species can find and move into safe micro-refugia (e.g., frogs) [57]; large-bodied species are able to flee or move readily away from the affected areas to avoid direct mortality [55].

Nest Substrate

Beyond location, the substrate used to build nests can increase or decrease the chances of fire spreading.
Increased sensitivity: Species that build nests with thatched mounds [58]; moss and lichen (dry out rapidly because they lack developed root systems) [32][59]; fine grass or mammalian hair (capable of trapping a great deal of air) [60]; plant material such as bark, vegetal fiber, leaves, twigs, grasses, tussocks, and branches [61][62].
Decreased sensitivity: Species that use a great amount of soil in the nests [63][64] to build hard, protective clay mounds (e.g., some termites, wasps, ants, and birds) [65]; species with a deliberate behavior for modifying their surrounding environment, thus reducing flammability (e.g., birds that reduce litter around their nests—‘fuel management’) [66][67]; species that build subterranean nests without thatched mounds [58].

Reproductive Cycles

Pregnant females may experience reduced speed, maneuverability, and endurance [68][69]. This likely occurs due to the additional physical load of the eggs or embryos, which makes the body broader and heavier [70][71][72] and decreases muscle strength [73]. Because they are slower and heavier, pregnant females tend not to endure long runs [74], which increases the likelihood of dying from fire injuries before finding shelter. In addition, pregnant and lactating females tend to spend most of their time stationary and sleeping, avoiding energetically costly behaviors such as running or climbing [75][76][77]. The longer vulnerable life stages are exposed to fire, the greater the risk of individual mortality and population decline.
Increased sensitivity: Species with synchronous reproduction at the end of the dry season, exposing pregnant, lactating, nesting, and brooding females to high-intensity fire (e.g., holometabolous insects whose larvae are restricted to dry-season) [78]. In species with a higher allocation of parental care, females may be burned in an attempt to protect the offspring or by delaying their decision to flee the fire [79]. K-strategists would be particularly disadvantaged because, in addition to longer pregnancies, parental care is more pronounced and offspring tend to depend on their parents for longer [80].
Decreased sensitivity: Species in which the majority of individuals are able to reproduce at any month of the year (year-round breeders); species that reproduce during the wet season but stop reproducing during the dry season. R-strategists would benefit because, in addition to a shorter pregnancy, they generally produce more offspring, which tend to grow at a faster rate to fully utilize the window of favorable environmental conditions with minimal (or no) parental care [80].

Sensory Detection of Fire Cues

Some animals are able to detect fire cues, either through olfactory (chemo-reception of smoke), visual (smoke plumes and flames), or acoustic (crackling sounds) means. Others may rely on thermoreceptors that can detect infrared radiation [11][81][82][83][84]. The greater the detection distance of fire cues, the greater the chance of an animal escaping and surviving. In general, olfactory cues can reach the farthest, followed by auditory and visual cues, which often signal immediate danger [7]. However, the value of fire cues as an early warning signal likely depends on an animal’s sensory sensitivity, an individual’s perceptual range, the fire behavior, and the environmental context [85][86].
Increased sensitivity: Species that spend most of their time surrounded by dense vegetation and rely primarily on the visual detection of fire may be particularly vulnerable, as the visual cues of fire might not enter an animal’s perceptual range until it is very close [85][87][88]. Based on these terms, small-bodied animals could be even more vulnerable, as they usually have lower visual acuity [89].
Decreased sensitivity: Species that are able to detect olfactory and/or acoustic fire cues may have more time to make good escape decisions because they can detect fire at greater distances regardless of vegetation structure [13][15][81][90][91][92]. Species that are able to detect fire cues at lower thresholds (e.g., lower concentrations and from greater distances). Species that rely on thermoreceptors can detect infrared radiation from fires [82][93][94]. Species that spend most of their time on top of tall trees, in open or low-stature vegetation, and in topographically simple landscapes may have some escape advantage as the rising smoke plumes could enter the animal’s perceptual range from a considerable distance (tens of kilometers), providing ample warning of fire risk [85][95].

Social Organization

Vigilance allows animals to monitor their surroundings and detect threats before it is too late to escape; however, it represents an allocation of time and energy that could be devoted to foraging and other fitness-enhancing activities [96]. In that case, sociality seems to be a good strategy because group members can reduce their investment in vigilance at no significant increased risk to themselves. As group size increases, individual vigilance decreases, and yet overall group vigilance and detection ability increases (effect of many eyes scanning for threats) [97]. However, for collective detection to work, it is important that at least one individual is vigilant and detects a threat (in this case, fire), upon which it alerts other group members, whether seeking shelter, fleeing, or emitting alarm calls. The fear responses may be socially transmitted by a cascade effect or contagious alertness [98][99][100]. Therefore, individuals who have not detected the threat by themselves can use this information and still escape before it is too late [101][102]. Therefore, aspects of social organization, such as group size, relationship structure, and communication system can determine the effectiveness of collective detection of fire signals.
Increased sensitivity: Solitary species or those that live in small family groups (parents and young) rely on fewer individuals to detect approaching fire [103]. Species with poorly developed social relationships (e.g., groups with weak connections) and whose individuals or groups lack effective communication skills.
Decreased sensitivity: Gregarious species living in large groups [104][105][106]. Social species residing in more connected, reciprocal, and socially homogeneous groups [107][108][109][110].

2.2. Post Fire

Animals may be indirectly negatively affected after fire by the simplified habitat structure with greater microclimate extremes (e.g., temperature, humidity, and greater exposure to predators), diminished food resources (e.g., less food, lowered nutritional status, or decreased palatability), or interactions with other organisms (e.g., increased competition, predation, or parasitism) [111]. The physical and behavioral traits that can increase or decrease a species’ sensitivity to the indirect effects of fire are described in detail below and illustrated in Figure 2.
Figure 2. Fire vulnerability traits of species after a fire. In green are the animals most likely to survive in the post-fire landscape (decreased sensitivity). In black are the animals whose traits increase the probability of death after a fire (increased sensitivity).

Behavioral Plasticity

Population recovery depends on the species’ behavioral plasticity with respect to habitat structure and diet.
Increased sensitivity: Late-successional species that require more structured habitats for nest sites and/or foraging, which take several years to recover [112]: canopy and upper-middle strata insectivores that forage in thicker bark or denser canopies [113][114]; small arboreal animals that depend on late successional resources (e.g., leaf litter and thick branches); tree cavity-nesters that rely on highly-decayed wood or large living trees that provide both long-lasting cavities (e.g., in the main stem) and a series of single-use cavities (e.g., in dead branches) [114][115][116]; pollinators, nectarivores, and frugivores that benefit, respectively, from specific late-successional flowers, fruits and seeds of trees and shrubs [113][117][118][119][120]; low mesic insectivores that forage in thick litter [113]; saproxylic insects typically associated with large old trees and the decaying wood they generate [121]; invertebrates that have biological stages of their development inside fungal fruiting bodies [122].
Decreased sensitivity: Generalists that can temporarily adapt their diet and/or habitat preferences to the conditions and food resources available across the post-fire landscape [113]; species that may benefit from fire-induced changes such as predators (birds of prey) [123] and early or mid-successional species: open grassland species [124], aerial insectivores that benefit from the increased availability of flying insects [116][125][126]; nectarivores, frugivores, and granivores that forage on (or close to) the ground and benefit from the greater abundance of small herbaceous plants producing flowers, fruits, and seeds after fire [127][128][129][130][131]; deadwood-associated species [93].

Dormancy

Dormancy allows species to cope with the scorched post-fire environment, avoiding risky foraging movements within the simplified post-fire landscape and reducing the chances of starving or being captured by a predator [132][133][134].
Increased sensitivity: Species that express multi-day torpor but need to rewarm frequently. These species may deplete energy reserves and starve before their preferred habitat and resources recover since active rewarming from torpor requires a substantial increase in energy expenditure and can compromise energy savings gained from using torpor. On the other hand, passive rewarming from torpor involves basking in the sun and, consequently, being more exposed to predators [91][135]. Species that use daily torpor, which lasts only some hours rather than days or weeks, and is usually, but not always, interrupted by daily foraging and feeding. In this case, individuals will have to deal with the lack of food resources, which may impair the ability to rewarm after daily torpor [136]. Additionally, since torpid animals move slower than when normothermic and during foraging, they may be captured by a predator or exposed to altered environmental conditions [92].
Decreased sensitivity: Invertebrates that express aestivation and remain in an inactive stage that is remarkably resistant to water loss (e.g., mucus cocoon to resist desiccation) or that can afford the loss of water and sustain a dry form without compromising on revival upon rehydration (e.g., all anhydrobiotes) [137]; species that use multi-day torpor for weeks or even months after a fire or during fire season without the need to rewarm [14][133][134][136].

Endogenous Circadian Rhythms

Fire-induced changes may affect diurnal, crepuscular, and nocturnal species differently.
Increased sensitivity: Diurnal ectotherms that depend on thermoregulation opportunities [138][139]; strictly diurnal prey species, which become more vulnerable to increased predation rates [133][140][141][142].
Decreased sensitivity: For nocturnal or crepuscular animals, nighttime environmental temperatures are often lower than preferred temperatures. For this reason, individuals seek out warmer places within (or closer to) their preferred temperature range (e.g., deep bark fissures, hollow branches, warm rocks, trees, or inside retreat sites during the day), which are typically more protected from predators [143]. Cathemeral or diurnal prey that can adjust their daily activity patterns [133].

Mobility

Finding new habitat beyond the fire perimeter is likely to be a major determinant of population persistence because if individuals do not disperse they risk reduced fitness or increased mortality due to predation or starvation [133].
Increased sensitivity: Species with restricted home range (e.g., burrows or rock crevices); territorial species with high site fidelity that may perceive the risk of leaving their territory or home range to locate unburned patches to be greater than that of remaining in a familiar area with little or no food resource [18][144][145]. Migratory species (highly mobile) but with strong site fidelity to a limited number of stopover locations and travel routes can have adverse demographic results if traditional sites are completely scorched [146].
Decreased sensitivity: Highly mobile species that travel long distances (e.g., migratory or high-flying birds) or show metapopulation dynamics [84]; nomadic or non-territorial species with low site fidelity [144][145].

Morphology

Increased sensitivity: Large ectotherms. The body size–environment interaction is profound in ectotherms because they rely on external heat [147][148]. Since heat is dissipated more slowly in large-bodied animals (lower surface-to-volume ratio), being large in a post-fire environment may be particularly disadvantageous for an ectotherm as it can be more sensitive to overheating. Invertebrates with thinner cuticles are expected to desiccate faster [137].
Decreased sensitivity: Large mammals [149][150]; species with black morphs or that can change their color after a fire, likely diminishing predator detectability while foraging after a fire [151]; invertebrates with higher cuticle thickness, which gives the animal the advantage of reducing water loss (desiccation resistance) [152].

This entry is adapted from the peer-reviewed paper 10.3390/fire6060242

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