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Autohaemorrhaging

Autohaemorrhaging, also known as reflex bleeding, is a defensive behavior in which certain animals deliberately eject haemolymph or blood from their bodies to ward off predators, often rendering the fluid noxious or toxic through chemical additives.^[1] This phenomenon has been documented across diverse taxa, primarily in insects and reptiles, where it serves as a last-resort antipredator strategy triggered by stress or physical provocation.^[1] In insects, autohaemorrhaging typically involves the release of haemolymph from specialized body regions, such as leg joints, antennal sockets, or the mouth, and is prevalent in families like Coccinellidae (ladybird beetles) and Meloidae (blister beetles).^[1] For instance, in the harlequin ladybird (Harmonia axyridis), repeated reflex bleeding over three weeks significantly reduces haemocyte concentration, protein content, and antimicrobial activity in the haemolymph, thereby weakening the immune system and delaying reproduction by approximately two days without affecting overall egg production or body mass.^[1] In blister beetles such as Lydus trimaculatus and Mylabris variabilis, the ejected haemolymph contains high levels of cantharidin (0.03–0.79 mg/g), a potent toxin produced in the fat body, stored in male accessory glands, and transferred during mating to enhance offspring defense, causing irritation or poisoning in predators.^[2] Among reptiles, autohaemorrhaging is observed in various snakes and lizards, often involving ocular or oral discharge of blood during threat responses like death feigning.^[3] In dice snakes (Natrix tessellata), about 10.6% of individuals (higher in adults at 12.4% than juveniles at 2.1%) release blood from the mouth during death feigning, which, when combined with musking and fecal smearing, shortens the feigning duration by roughly two seconds, potentially signaling unpalatability more effectively.^[4] A notable example occurs in the Bahamian pygmy boa (Tropidophis curtus barbouri), where gentle head pressure induces rapid blood exudation from the eyes (within 0.7 seconds) and mouth (0.8 seconds later), clearing in about 1.6 seconds as part of a multi-component defense including defecation and musk release, though the exact antipredator efficacy remains unconfirmed. Despite its spectacular nature, autohaemorrhaging incurs physiological costs, such as increased pathogen susceptibility in insects, and its prevalence varies by age, sex, and environmental factors across species.^[1]

Definition and Purpose

Definition

Autohaemorrhaging, also known as reflex bleeding, is the deliberate release or ejection of haemolymph or blood from an animal's body as a last-resort antipredator defense mechanism when threatened or attacked.^[5] This behavior involves externalizing body fluids, often containing toxins or distasteful compounds, to deter predators by making the prey unpalatable, startling them visually, or signaling unprofitability.^[5] It is a costly strategy, as it can lead to significant physiological losses for the animal.^[2] In insects, autohaemorrhaging specifically entails the expulsion of haemolymph—the open circulatory fluid analogous to blood in vertebrates but lacking hemoglobin and red blood cells—from specialized body sites such as leg joints or integumental ruptures.^[2] This contrasts with vertebrates like certain reptiles, where true blood is ejected, typically carrying oxygen via hemoglobin.^[5] The phenomenon is widespread in various insect orders, including Coleoptera and Hemiptera, and occurs in some reptile taxa, though detailed mechanisms vary by group.^[5] Autohaemorrhaging manifests in two primary variations: active squirting, where the fluid is forcefully directed toward the predator, often laced with toxic or distasteful chemicals to enhance deterrence; and passive slow emission, involving a gradual oozing that serves as a visual or olfactory warning signal, sometimes without strong toxicity but relying on aposematic cues.^[2] In active forms, such as in some blister beetles, haemolymph is deliberately expelled under pressure from joints, while passive release may occur through minor physical damage or reflexive rupture.^[2] This defense has fascinated biologists for centuries, with reflex bleeding noted as a response to disturbance in insects like ladybugs.^[5]

Evolutionary Significance

Autohaemorrhaging represents a convergent defensive trait that has evolved independently in insects and reptiles, distantly related taxa facing similar predation pressures, underscoring its adaptive value as an antipredator strategy.^[5]^[6] This behavior likely emerged under strong selective forces in environments where rapid, chemical-based deterrence provided survival benefits without necessitating elaborate morphological structures, though it incurs physiological costs such as hemolymph loss and immune compromise.^[5] In insects, autohaemorrhaging has arisen multiple times across at least four orders, including Coleoptera, Hemiptera, Plecoptera, and Orthoptera, with particular prevalence in beetle families like Coccinellidae and Meloidae.^[5]^[7] The trait's distribution suggests independent evolution in response to diverse predators, including birds, mammals, and lizards, where the release of noxious hemolymph exploits aversion to bitter or toxic compounds, enhancing escape probabilities despite associated fitness trade-offs like delayed reproduction.^[5] Comparative studies indicate it functions as a secondary defense, complementing other tactics in resource-limited settings.^[7] Among reptiles, autohaemorrhaging is documented in select lineages, notably the horned lizard genus Phrynosoma, where it is plesiomorphic and retained in six of 13 species, with losses in specific clades such as P. mcallii-modestum-platyrhinos.^[6] This ocular blood ejection targets mammalian predators like canids, delivering irritant chemicals that induce learned avoidance, thereby increasing survival rates in encounters.^[6] Observations in snake families, including Tropidophiidae, further highlight its sporadic occurrence, often integrated with behaviors like death feigning.^[3] Phylogenetic analyses infer multiple independent origins of autohaemorrhaging from extant distributions, with no direct fossil evidence available.^[5]^[6]

Physiological Mechanisms

In Insects

In insects, autohaemorrhaging, also known as reflex bleeding, involves the deliberate rupture of thin membranes at exoskeletal joints, such as the femorotibial or intersegmental areas, to release haemolymph under internal pressure as a defensive response to threats.^[8] This process allows haemolymph to exude from sites like leg joints or under the pronotum, where the softer, thinner integument facilitates controlled leakage without compromising the insect's overall structural integrity.^[9] The release is triggered by mechanical stress, such as grasping or attack, leading to the haemolymph emerging as droplets or jets that deter predators through distastefulness or entanglement.^[10] Pressure for haemolymph ejection is generated primarily through muscle contractions that elevate hydrostatic pressure within the open circulatory system, often supplemented by body deformation or abdominal compression, enabling expulsion over distances of up to several centimeters. The primary force typically arises from localized skeletal muscle activity around the release sites. This mechanism leverages the insect's haemocoel, where haemolymph bathes internal organs, to rapidly mobilize the fluid without requiring specialized vascular rupture.^[11] The released haemolymph frequently contains defensive chemicals, such as alkaloids or phenolics, which impart toxicity or repellency; for instance, in ladybugs (Coccinellidae), coccinellins like coccinelline are present at concentrations that make the fluid unpalatable to predators.^[10] These compounds are biosynthesized via pathways involving acetate precursors, accumulating in the haemolymph to reinforce its role in chemical defense.^[12] In other groups, such as crickets, the haemolymph exhibits an acrid odor due to similar phenolic constituents.^[9] Certain insects exhibit directional control over haemolymph ejection, adjusting the angle and force based on the threat's position through neural reflexes that coordinate muscle responses.^[9] For example, in armoured ground crickets (Gryllidae), side-directed attacks prompt greater projection distances (up to 10 cm) from leg seams compared to overhead threats, optimizing coverage toward the predator via proprioceptive feedback.^[9] This reflexive modulation enhances the defense's efficacy by targeting the assailant more precisely.^[9]

In Reptiles

Autohaemorrhaging in reptiles involves the deliberate rupture of specific vascular structures, such as the circumocular sinuses in lizards or mucosal linings in the oral cavity and nasal passages of snakes, as a reflexive defense mechanism triggered by activation of the autonomic nervous system. This process is elicited during perceived threats, where neural signals prompt rapid physiological changes leading to blood ejection from weak points in the vascular system. Unlike the open circulatory systems of invertebrates, reptiles possess a closed circulatory system that enables precise control over blood pressure and distribution, allowing for targeted release of true blood containing hemoglobin and defensive compounds.^[13]^[14] The buildup of pressure necessary for autohaemorrhaging is achieved through cardiac acceleration and vasoconstriction, which elevate blood pressure in the head and ocular regions, forcing blood through fragile vascular sites. In lizards, specialized muscles encircling the major veins around the eyes contract to restrict outflow, causing the circumocular sinuses—capillary beds near the ocular orbits—to swell and rupture, propelling blood outward. This can result in ejection distances of up to 1.5 meters, depending on the species and intensity of the stimulus.^[15] In snakes, similar pressure increases lead to tears in mucosal linings of the mouth, nostrils, or cloacal vasculature, with blood emerging without the need for extreme propulsion.^[13]^[3] Reflex triggers for autohaemorrhaging are primarily mediated by stress hormones, such as adrenaline (epinephrine) and norepinephrine, released in response to handling, predation attempts, or physical restraint. These catecholamines activate the sympathetic branch of the autonomic nervous system, inducing tachycardia and vasoconstriction to amplify intrathoracic and intracranial pressure. The response is highly reflexive, occurring within seconds of stimulation, and serves an evolutionary role in antipredator behavior by startling or repelling assailants through the sudden release of potentially noxious blood. While the exact neural pathways remain under study, the integration of hormonal and muscular components ensures a coordinated ejection that enhances survival without permanent damage in most cases.^[14]^[16]001[1114:BSVIHL]2.0.CO;2/Blood-Squirting-Variability-in-Horned-Lizards-Phrynosoma/10.1643/0045-8511(2001)001[1114:BSVIHL]2.0.CO;2.full)

Examples in Insects

Beetles and Ladybugs

In the family Coccinellidae, commonly known as ladybugs or ladybird beetles, autohaemorrhaging manifests as reflex bleeding, where haemolymph is ejected from the femoro-tibial joints of the legs in response to predator contact or disturbance. This defensive response releases droplets of orange or yellow fluid containing alkaloids such as coccinelline and adaline, along with methoxypyrazines like 2-isopropyl-3-methoxypyrazine, which produce a bitter taste and pungent odor to repel attackers. These chemicals effectively deter a range of predators, including ants, birds, and lizards, as demonstrated in observational studies where vertebrates rejected ladybirds after initial contact with the reflex fluid.^[10]^[17]^[5] The behavioral trigger for this ejection is typically mechanical stimulation, such as grasping by a predator, leading to rapid haemolymph discharge that can project several millimeters from the body. In some species, a single event may involve the loss of 10–12% of the beetle's fresh body weight, highlighting the trade-off between immediate survival benefits and potential dehydration or nutritional depletion. Seminal research, including early experiments with birds and lizards, has confirmed the efficacy of these alkaloids in reducing predation rates, with ladybirds often surviving encounters that would otherwise be fatal.^[18]^[19] Autohaemorrhaging also occurs in other beetle families within Coleoptera, often integrated with additional defenses. For instance, in blister beetles of the family Meloidae, such as Lydus trimaculatus and Mylabris variabilis, haemolymph containing high levels of cantharidin (0.03–0.79 mg/g) is ejected, acting as a potent irritant or toxin to predators. Cantharidin is biosynthesized in male accessory glands and transferred to females during mating for offspring defense. In darkling beetles of the family Tenebrionidae, such as the blue death-feigning beetle Asbolus verrucosus, larvae release haemolymph during tonic immobility when threatened, using the viscous fluid as an adhesive to bind environmental debris like sand particles for crypsis and camouflage against visual predators. Adults in this family complement reflex bleeding with noxious quinone sprays ejected from pygidial glands, creating a synergistic chemical barrier that enhances overall deterrence.^[2]^[20]^[21]

Other Insect Orders

Autohaemorrhaging manifests in diverse forms across several insect orders beyond Coleoptera, often tailored to the species' ecology and predators, though generally involving smaller volumes of haemolymph compared to the copious releases seen in many beetles. In the order Hemiptera, particularly within the family Cercopidae (froghoppers or spittlebugs), adults exhibit reflex bleeding by exuding haemolymph from specialized rupture lines in the pretarsal membranes of their legs when disturbed. This behavior is closely linked to aposematic coloration, signaling unpalatability, and the released haemolymph is typically odoriferous and distasteful, deterring predators such as ants and birds; for instance, in species like Prosapia bicincta, the haemolymph can inhibit predation without fully preventing attacks but often combined with evasive actions.^[22]^[23] Within the order Orthoptera, autohaemorrhaging is prominently featured in armoured crickets of the family Tettigoniidae, such as Acanthoplus discoidalis. These insects actively squirt haemolymph from pores along their pronotal margins and leg articulations, achieving directional propulsion with projection distances averaging about 4 cm (up to approximately 10 cm) to target approaching threats like spiders or mantises. The ejected fluid is toxic, containing defensive chemicals that cause irritation or toxicity upon contact, enhancing its efficacy as a standoff weapon; this squirting is integrated with other defenses like loud stridulation and feigning death, observed in field encounters where it successfully repels predators.^[24] In Hymenoptera, a related passive defense known as "easy bleeding" occurs in certain sawflies (Tenthredinidae), where larvae release haemolymph from easily ruptured integumental points across the body upon contact with predators. This slow seepage exposes plant-derived alkaloids sequestered in the haemolymph to deter ants and other arthropod predators, entangling attackers with coagulating fluid and providing time for escape; unlike active ejection, it involves low mechanical resistance of the integument. Studies on species like Athalia rosae demonstrate its role in reducing ant foraging, though it incurs physiological costs similar to more vigorous forms.^[25]^[26] Overall, these instances across Hemiptera, Hymenoptera, and Orthoptera highlight autohaemorrhaging's convergent evolution, with less voluminous discharges than in beetles but frequently augmented by pheromones or toxins.^[22]

Examples in Reptiles

Lizards

Horned lizards in the genus Phrynosoma employ autohaemorrhaging as a striking antipredator strategy, rupturing specialized blood vessels in their circumorbital sinuses to eject streams of blood from the eyes toward threats. This behavior is particularly effective against canine predators, such as coyotes and foxes, which are common in their arid habitats. The defensive display often follows initial attempts at camouflage or flight, escalating when the lizard is grasped or closely approached.^[27] At least eight species of Phrynosoma have been confirmed to perform blood-squirting, including P. cornutum (Texas horned lizard) and P. solare (regal horned lizard), out of the 17 recognized in the genus.^[28] The ejection can reach distances of up to 1.5 meters and is remarkably accurate, often directed at the predator's face or mouth. In experimental trials simulating predation, larger individuals squirted more frequently and expelled greater blood volumes, suggesting a correlation with body size that enhances defensive efficacy. Vascular rupture in the ocular region allows for rapid release under increased intraocular pressure, a physiological adaptation unique among vertebrates to this form of autohaemorrhaging.^[27]^[29]^[15] This autohaemorrhagic response integrates with other behaviors, such as body inflation to appear larger, erection of cranial spines for passive defense, and adoption of a rigid, immobile posture to mimic a non-prey item. The squirted blood deters attackers due to its foul taste and irritating properties, primarily attributed to elevated formic acid concentrations derived from the lizards' diet of harvester ants (Pogonomyrmex spp.). These chemical defenses exploit the predators' aversion to the ants' venom, turning the lizard's own blood into an unpalatable deterrent.^[27]^[30]^[15] Field studies in North American desert ecosystems, including the Chihuahuan and Sonoran Deserts, document this behavior in natural encounters, where lizards deploy it against native predators. Observations indicate that individuals can repeat the blood ejection up to five times during a single predatory event before depleting reserves, allowing temporary escape while the threat is repelled. Such repeatability underscores the mechanism's reliability, though it incurs costs like blood loss and potential dehydration in harsh environments.^[31]^[13]

Snakes

Autohaemorrhaging in snakes primarily occurs among colubrid species, where it serves as a defensive response to predation threats. The European grass snake (Natrix natrix) secretes blood from the lining of the mouth during thanatosis, or death feigning, to mimic a diseased or unpalatable carcass.^[32] Similarly, the dice snake (Natrix tessellata), another colubrid, releases blood around the mouth while exhibiting tonic immobility, often inverting its body and gaping to enhance the display.^[32]^[33] Other snake genera demonstrate varied ejection sites for autohaemorrhaging. Hognose snakes (Heterodon spp.) emit blood from the mouth and nostrils as part of an elaborate bluff, combining it with hissing, flattening the head, and rolling onto the back.^[32] The West Indian wood snake (Tropidophis spp.), a dwarf boa, expels blood from the eyes, mouth, and nostrils when stressed, with observations showing rapid filling of the eyes followed by drops from the mouth after gentle head pressure.^[32] In contrast to the specialized ocular squirting in certain lizards, snakes exhibit more flexible multi-site bleeding to broadly deter predators.^[33] This behavior in snakes is frequently paired with other defenses, such as musking—releasing foul cloacal secretions—and defecation, which coat the body and amplify the illusion of decay.^[33] The ejected blood may contribute to deterrence through visual cues or chemical properties, with some studies indicating it can be distasteful or irritating to predators, including mammals, potentially due to bitter compounds.^[33] Recent research highlights the synergistic effects of autohaemorrhaging with these behaviors; in dice snakes, individuals combining mouth bleeding during death feigning with prior musking and fecal smearing spent significantly less time immobilized—approximately 2 seconds shorter—allowing quicker escape from simulated predator handling.^[33]

Defensive Functions and Consequences

Defensive Benefits

Autohaemorrhaging serves as a potent antipredator strategy by releasing haemolymph or blood laden with noxious compounds, thereby deterring assailants through chemical means. In insects, particularly ladybird beetles (Coccinellidae), the haemolymph expelled via reflex bleeding is rich in alkaloids such as coccinellins, including coccinelline, which impart toxicity and bitterness that cause aversion or illness in predators ranging from ants to birds and small mammals.^[10] These chemicals trigger immediate rejection behaviors, such as grooming or retreat, effectively halting predation attempts.^[34] In reptiles, such as horned lizards (Phrynosoma spp.), the blood contains small peptides derived from metabolized ant venom, which elicit profound revulsion and distaste in mammalian predators like coyotes and dogs.^[13] The abrupt ejection of fluids during autohaemorrhaging also exploits visual and startle responses, surprising predators and creating a brief window for escape, particularly against visually hunting species such as birds or diurnal mammals.^[13] This sudden display amplifies the chemical signal by drawing attention to the distasteful release, enhancing its deterrent impact. Laboratory and field studies provide empirical support for these benefits, demonstrating substantial reductions in attack persistence. For instance, in interactions between ants and ladybird larvae, contact with reflex blood causes predators to invariably abort attacks and engage in self-cleaning, achieving near-complete deterrence.^[35] Similarly, in horned lizards, blood-squirting elicits aversion in approximately 85% of encounters with dogs, significantly lowering the likelihood of continued assault.^[13] These outcomes underscore substantial reductions in predation success across tested scenarios involving insects and reptiles.^[36] Autohaemorrhaging often integrates synergistically with complementary defenses, amplifying survival probabilities. In horned lizards, it bolsters cryptic camouflage and spiny cranial projections, forming a multi-layered strategy that confounds predators before chemical ejection becomes necessary.^[13] In insects like ladybirds, reflex bleeding complements aposematic coloration, where the sudden bleed reinforces warning signals and facilitates evasion. For example, the horned lizard's targeted squirting deters approaching dogs by combining startle with chemical repulsion in a single act.^[37]

Physiological Costs

Autohaemorrhaging entails substantial physiological burdens for the organisms that utilize it, stemming from the expulsion of hemolymph in insects or blood in reptiles, which depletes vital fluids containing nutrients, proteins, and immune cells. In ladybird beetles (Harmonia axyridis), a typical reflex bleeding episode results in the loss of 0.44–0.52 µl of hemolymph, while extreme cases can reach up to 2.2 µl, approximating 5% of the adult's live body mass.^[5] This volume reduction induces hypovolemia, impairing hemolymph circulation and nutrient distribution, which can lead to decreased mobility and functional equivalents of anemia through diminished oxygen-carrying capacity. In reptiles, such as the Texas horned lizard (Phrynosoma cornutum), a single blood-squirting event may expel 0.5–53% of total blood volume, causing acute hemodynamic instability, reduced cardiovascular performance, and heightened risk of circulatory collapse.^[6] Frequent autohaemorrhaging episodes compound these effects by compromising immune competence. In a 2020 experimental study on ladybird beetles, individuals subjected to reflex bleeding twice weekly exhibited significantly lower hemocyte concentrations (P < 0.05), reduced hemolymph protein levels (P < 0.05), and diminished antimicrobial activity against the bacterium Micrococcus luteus (P < 0.05), with a near-significant decline against Escherichia coli (P = 0.073).^[5] Such suppression weakens overall hemocyte function, elevating susceptibility to bacterial infections and parasitoids, thereby increasing disease vulnerability in the post-bleeding period. Reproductive fitness also suffers due to the energetic demands of hemolymph replenishment and fluid homeostasis. The same study found that repeated bleeding delayed the age at first reproduction in female ladybirds by approximately 2 days (P = 0.037), with greater hemolymph loss correlating to later onset of oviposition (P = 0.047), though cumulative egg output over 30 days was unchanged.^[5] Concurrently, the loss of water and electrolytes disrupts osmoregulation, promoting dehydration and osmotic stress that diverts metabolic resources from gamete production. The resultant physiological debilitation post-autohaemorrhaging amplifies predation risks by rendering the animal more susceptible to secondary attacks or conspecific cannibalism owing to impaired locomotion and vitality.^[5]

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