DISCUSSION
We provided quantitative estimates of the frequency of toe amputations in juvenile and adult red-necked nightjars, evaluated the severity of damage to the birds, and identified the body parts of the ants that remained attached to nightjar toes. Less than <1% individuals missed one or more toes. Toe amputations were only observed in adults that had performed at least one round-trip migration from Europe to Africa and, although ant-nightjar encounters also occurred in juveniles, these resulted in minor injuries. The taxonomic analysis of mandible remains identified army-ant bites as the most likely cause of toe amputations in adult nightjars.
Our estimate of the incidence of ant bites is based on the proportion of toe-mutilated birds, but the cause of damage could only be confirmed for those individuals that had remains of ant mandibles or the full head on their toes. None of the nightjars examined in this population (>4,500 captures) exhibited typical poxvirus-like lesions on the eyes, feet or toes, suggesting that poxvirus infection does not play a major role in the observed toe amputations. Besides amputations, over the 15 years of study we have observed structural injuries to the sternum (n=7), tarsus (n=1), mandibles (n=4), and toes (n=5) of nightjars, affecting <1% of all trapped individuals. These injuries are hypothesized to reflect healed fractures based on the presence of bone callus formation and/or angular deformity. Damaged toes due to traumatic fracture differ from confirmed ant-bitten toes in that fractured toes often become distorted in position, pointing obliquely across the other toes, but the skin remains intact. By contrast, army ant bites result in a break in the skin of the affected phalanx and, even though the compressive force applied to the toe is not enough to fracture the bone, prolonged compression might cause ischemia and subsequent necrosis of the bone tissue, ultimately resulting in the excision and loss of one or more of the phalanges or the entire toe. The anatomical similarities of mutilations among birds missing toes and the confirmed ant-bite injuries in birds in the process of loosing a toe suggest that ant bites, rather than laceration from trauma (e.g. road traffic or building collisions) or predator attacks (e.g. carnivores), are the most likely cause of the observed toe amputations in adult nightjars.
No trace of severe damage from ant bites was seen in juveniles despite their sample size being even larger than that of adults (1,145 juvenilesvs. 1,104 adults considering all years of the long-term study). Nevertheless, the total number of injured birds is too small to support the statement that injuries from ant bites are restricted to adults. The observation of the full head of a M. barbarus attached to the pecten of the medial toe of a juvenile demonstrates that they are not entirely free from ant attacks, although ant species occurring in south Spain are likely too small for their mandibles to grasp on the relatively thick toes of a nightjar. M. barbarus is very common on the Mediterranean coast (Lebas et al., 2017), but it may not pose as much a threat to nightjars as army ants because M. barbarus feed mainly on seeds and their mandibles are relatively small in comparison to those of army ants.
The genus Dorylus ranges from sub-Saharan Africa across North Africa and Asia Minor to Borneo in Southeast Asia. The Afrotropics harbour the largest number of species (116 so far described), including subterranean-, leaf litter- and surface-dwelling species. Of these, surface-dwelling species have, among other characteristics, the greatest mandible length and mandibular aperture (Schöning et al., 2005).Dorylus species are generalist predators that take any type of prey, from immature individuals of other insects to vertebrate carrion (Schöning & Moffett, 2007). Unlike leaf litter-dwelling and subterranean species, Dorylus ants spend much of their time foraging on the soil surface, and given their mobile, predatory lifestyle and aggressive behaviour, attacks on the birds they encounter on the ground should be common.
Nineteenth-century naturalists assumed that birds eat army ants but, as evidence accumulated about the foraging patterns of birds, it became clear that birds peck only at ants attacking their feet or plumage (Willis & Oniki, 1978). No mention of army ants is made in the published studies of diet of Afrotropical nightjars (Jackson, 2000). In addition, although army ants are major predators of vertebrates (e.g. birds, sea turtles), most documented cases of predation on birds took place during the nesting stage (Ikaran et al., 2020; Robinson & Robinson, 2001). None of these organisms therefore appear to serve as a trophic resource for the other, suggesting that agonistic ant-nightjars encounters are coincidental and detrimental to both parties.
Missing and damaged toes have also been observed in other migratory and sedentary bird species and, as in the red-necked nightjar, these injuries were hypothesized to result from ant attacks (e.g. Ibáñez et al., 2007; Sugg, 1974). Sugg (1974) reported on the specific bite effects by Dorylus sp. on 10 out of 343 (2.9%) pied kingfishers (Ceryle rudis ) from a breeding colony on the Kenyan shore of Lake Victoria. Toe amputations and damage from ant bites appear to be more common in pied kingfishers (3%) than in red-necked nightjars (<1%) despite the latter spending more time on the ground. The estimated proportion of toe amputations in another population of red-necked nightjars monitored for six years in E Spain is 0.4% (3 cases out of 751 different adults examined in 2017-2022; J.M. Zamora, pers. comm.). The field protocols in this study, as in the first years of our long-term study, did not include routine screening for toe or foot anomalies, and so estimates are based on opportunistic observations made during ringing sessions. The proportions of toe amputations in both populations, as estimated from opportunistic observations, are identical (0.4%) and half the magnitude of that based on systematic examination of both feet (0.8%), suggesting that a routine screening for anomalies is needed to obtain unbiased estimates. Caution is therefore required in extrapolating our results to other populations, species and geographic regions. Different estimates could be obtained if we study nightjars in their wintering area (where ants occur). The frequency of ant-bite damage in breeding nightjars appears almost negligible. However, this might be an underestimate if only birds that manage to survive their injuries migrate successfully from their non-breeding grounds to our study area.
Most injuries observed on nightjars, as in the pied kingfishers, consisted of single-toe amputations that should not necessarily impair the birds’ functional capacities and compromise performance in tasks such as predator avoidance or food acquisition. One of the injured nightjars actually survived from one breeding season to the next. Nonetheless, the loss of the medial toe and, therefore, of the pecten could be detrimental to nightjars because, even though the exact purpose of the pecten remains unclear, it has been suggested that it might be used as a comb for removing parasites during preening, or to straighten out the rictal bristles (Cleere, 2010). Moreover, as evidenced from at least one of the injured nightjars, multiple ant bites on the same bird might cause multiple amputations, potentially compromising locomotion on a chronic basis and, ultimately, long-term survival. Breaks in the skin from ant bites, even if affecting only one toe, might increase the risk of fatal complications, such as severe bleeding and sepsis from opportunistic infections, so it is possible that some individuals die before migrating and being captured on their breeding grounds. That is, only the fraction of birds that are able to survive ant attacks and subsequent damage might be recorded by us. Hence, the true incidence of ant bites on birds could be much higher than it appears to be.
Further research is required to understand the true incidence and eco-evolutionary implications of antagonistic ant-bird interactions. Being accidental, the factors promoting ant-nightjar encounters are difficult to determine, and consequences different from injuries (e.g. a change in behaviour, systemic symptoms) are difficult to assess and require more detailed study. Fortunately, migratory nightjars are becoming popular model organisms in movement ecology studies across the globe, including capture programs conducted in tropical areas during the non-breeding season (e.g. (Cockle et al., 2023; Evens et al., 2023), and so it is possible that studies similar to ours could be attempted in other populations, species, and geographic regions. More of these studies should encompass areas of the distribution range of large, tropical ants and incorporate routine examination and systematic recording of injuries into their protocols in order to increase the chances of encountering clear evidence of the agent of damage and to obtain reliable estimates of the true frequency of injuries and their origin (stochastic or not). Moreover, studies that consider aspects of performance (e.g. mating success, foraging success) and components of fitness (e.g. survival, reproductive success or lifespan) in injured birds relative to uninjured ones are encouraged as a critical step to understand the influence of injuries on natural selection and evolution (Hendry et al., 2022).