Susan J. Cunningham

The relative importance of olfaction and remote touch in prey detection by North Island brown kiwis

Birds that forage by probing in sand, soil or mud substrates must often use senses other than vision to find their prey. Kiwis (Apterygidae) are nocturnal probing birds inhabiting forested areas in New Zealand. Their visual sense is reduced, but they have a highly developed sense of smell, a bill tip organ similar to that found in Scolopacidae shorebirds, which may be used to detect vibrotactile cues produced by burrowing prey (remote touch), and prominent ear openings. We designed a foraging experiment presenting mealworm prey to eight captive North Island brown kiwis, Apteryx mantelli, under a variety of trial conditions to discover whether they were using hearing, olfaction, remote touch or direct touch (chance alone), singly or together, to find prey. Kiwis were most efficient at finding prey using olfaction alone or in combination with other cues, but switched to locating prey with lower efficiency using remote touch, in the absence of olfactory cues. They did not appear to use auditory cues for foraging. The ability to switch between sensory modalities depending on the quality of the cues available has been documented before in other groups of birds (including thrushes (Turdidae) and sandpipers (Scolopacidae)) and would be of great advantage to wild kiwis foraging under a wide range of environmental conditions.

Temperatures in excess of critical thresholds threaten nestling growth and survival in a rapidly-warming arid savanna: a study of common fiscals.

Frequency, duration, and intensity of hot-weather events are all predicted to increase with climate warming. Despite this, mechanisms by which temperature increases affect individual fitness and drive population-level changes are poorly understood. We investigated the link between daily maximum air temperature (tmax) and breeding success of Kalahari common fiscals (Lanius collaris) in terms of the daily effect on nestling body-mass gain, and the cumulative effect on size and age of fledglings. High tmax reduced mass gain of younger, but not older nestlings and average nestling-period tmax did not affect fledgling size. Instead, the frequency with which tmax exceeded critical thresholds (tcrits) significantly reduced fledging body mass (tcrit = 33°C) and tarsus length (tcrit = 37°C), as well as delaying fledging (tcrit = 35°C). Nest failure risk was 4.2% per day therefore delays reduced fledging probability. Smaller size at fledging often correlates with reduced lifetime fitness and might also underlie documented adult body-size reductions in desert birds in relation to climate warming. Temperature thresholds above which organisms incur fitness costs are probably common, as physiological responses to temperature are non-linear. Understanding the shape of the relationship between temperature and fitness has implications for our ability to predict species’ responses to climate change.

A new prey‐detection mechanism for kiwi (Apteryx spp.) suggests convergent evolution between paleognathous and neognathous birds

Kiwi (Apterygidae: Apteryx spp.) are traditionally assumed to detect their soil‐dwelling invertebrate prey using their sense of smell. The unique position of the nares at the tip of the bill and the enlarged olfactory centres in the brain support this assumption. However, studies designed to show the importance of olfaction in prey‐detection by Apteryx have provided equivocal results. Another family of probing birds, the Scolopacidae, detect their buried prey using specialised vibration and pressure‐sensitive mechanoreceptors embedded in pits in the bill‐tip. We found that aspects of the foraging patterns of Apteryx mantelli are like those of scolopacid shorebirds, suggesting that Apteryx may be using a similar prey‐detection mechanism. We examined specimens of all five Apteryx species and conducted a morphological and histological examination of the bill of A. mantelli. We discovered that Apteryx possess an arrangement of mechanoreceptors within pits similar to that in Scolopacidae species and may therefore be able to localise prey using a similar vibrotactile sense. We suggest that this sense may function in conjunction with, or be dominant over, olfaction during prey‐detection. The Apterygidae and the Scolopacidae are members of the two different super‐orders of birds: the Paleognathae and the Neognathae, respectively. Therefore we cite the similar bill‐tip anatomy of these two families as an example of convergent evolution across a deep taxonomic divide.

Identifying biologically meaningful hot-weather events using threshold temperatures that affect life-history.

Increases in the frequency, duration and intensity of heat waves are frequently evoked in climate change predictions. However, there is no universal definition of a heat wave. Recent, intense hot weather events have caused mass mortalities of birds, bats and even humans, making the definition and prediction of heat wave events that have the potential to impact populations of different species an urgent priority. One possible technique for defining biologically meaningful heat waves is to use threshold temperatures (Tthresh) above which known fitness costs are incurred by species of interest. We set out to test the utility of this technique using Tthresh values that, when exceeded, affect aspects of the fitness of two focal southern African bird species: the southern pied babbler Turdiodes bicolor (Tthresh = 35.5°C) and the common fiscal Lanius collaris (Tthresh = 33°C). We used these Tthresh values to analyse trends in the frequency, duration and intensity of heat waves of magnitude relevant to the focal species, as well as the annual number of hot days (maximum air temperature > Tthresh), in north-western South Africa between 1961 and 2010. Using this technique, we were able to show that, while all heat wave indices increased during the study period, most rapid increases for both species were in the annual number of hot days and in the maximum intensity (and therefore intensity variance) of biologically meaningful heat waves. Importantly, we also showed that warming trends were not uniform across the study area and that geographical patterns in warming allowed both areas of high risk and potential climate refugia to be identified. We discuss the implications of the trends we found for our focal species, and the utility of the Tthresh technique as a conservation tool.

The anatomy of the bill tip of kiwi and associated somatosensory regions of the brain: comparisons with shorebirds

Three families of probe-foraging birds, Scolopacidae (sandpipers and snipes), Apterygidae (kiwi), and Threskiornithidae (ibises, including spoonbills) have independently evolved long, narrow bills containing clusters of vibration-sensitive mechanoreceptors (Herbst corpuscles) within pits in the bill-tip. These ‘bill-tip organs’ allow birds to detect buried or submerged prey via substrate-borne vibrations and/or interstitial pressure gradients. Shorebirds, kiwi and ibises are only distantly related, with the phylogenetic divide between kiwi and the other two taxa being particularly deep. We compared the bill-tip structure and associated somatosensory regions in the brains of kiwi and shorebirds to understand the degree of convergence of these systems between the two taxa. For comparison, we also included data from other taxa including waterfowl (Anatidae) and parrots (Psittaculidae and Cacatuidae), non-apterygid ratites, and other probe-foraging and non probe-foraging birds including non-scolopacid shorebirds (Charadriidae, Haematopodidae, Recurvirostridae and Sternidae). We show that the bill-tip organ structure was broadly similar between the Apterygidae and Scolopacidae, however some inter-specific variation was found in the number, shape and orientation of sensory pits between the two groups. Kiwi, scolopacid shorebirds, waterfowl and parrots all shared hypertrophy or near-hypertrophy of the principal sensory trigeminal nucleus. Hypertrophy of the nucleus basorostralis, however, occurred only in waterfowl, kiwi, three of the scolopacid species examined and a species of oystercatcher (Charadriiformes: Haematopodidae). Hypertrophy of the principal sensory trigeminal nucleus in kiwi, Scolopacidae, and other tactile specialists appears to have co-evolved alongside bill-tip specializations, whereas hypertrophy of nucleus basorostralis may be influenced to a greater extent by other sensory inputs. We suggest that similarities between kiwi and scolopacid bill-tip organs and associated somatosensory brain regions are likely a result of similar ecological selective pressures, with inter-specific variations reflecting finer-scale niche differentiation.

Bill Morphology of Ibises Suggests a Remote-Tactile Sensory System for Prey Detection

ABSTRACT. Birds that forage by probing must often use senses other than vision to find their prey. Remote touch is a sense based on the interception of vibrations produced by moving prey in the substrate or on the evaluation of pressure patterns produced by hard-shelled sessile prey. In probing birds, this system is mediated by an organ made up of clusters of mechanoreceptors housed within pits in the bone of the bill-tips. This bill-tip organ was first described in probing shorebirds (Scolopacidae), and more recently in kiwi (Apterygidae). Here, we describe this bill-tip organ in a third family of probing birds, the ibises (Threskiornithidae). We examined the bill morphology of 11 species of ibis from 8 genera. We found bill-tip organs in species in a wide range of habitat types, from predominantly terrestrial to predominantly aquatic, which suggests that ibises may use remote touch when foraging both in water and in granular substrates. Our data imply a link between bill-tip morphology and habitat use—a pattern that we believe warrants further investigation.

Can behaviour buffer the impacts of climate change on an arid-zone bird?

Behavioural thermoregulation, particularly the use of cool microclimates, is one method by which organisms could avoid the worst effects of climate warming. However, retreat into cool microsites, e.g. shady vegetation or burrows, may carry important lost-opportunity costs. These could include reduced opportunity for foraging, breeding or territorial defence, each carrying implications for fitness. We investigated patterns of microclimate use and foraging behaviour by Southern Fiscals Lanius collaris in the Kalahari. We used Ivlevs electivity index to assess preference of breeding males for perch types with different thermal properties. We found that Southern Fiscals preferred to hunt from high, sunny perches at all times, except on hot afternoons (air temperature >35 °C), when they switched their preference to high, shaded perches. Black-bulb thermometers indicated shaded perches were always cooler than sunny perches, especially on hot afternoons. Therefore, Southern Fiscals could reduce thermoregulatory costs by switching foraging locations. However, Southern Fiscal foraging success rates were highest when hunting from sunny perches, and were reduced by c. 50% when hunting from shaded perches. Our data suggest that Southern Fiscals were making a trade-off on hot afternoons, compromising foraging intake in return for thermal benefits. We discuss potential costs and consequences of this trade-off under climate change.

Regulation of Heat Exchange across the Hornbill Beak: Functional Similarities with Toucans?

Beaks are increasingly recognised as important contributors to avian thermoregulation. Several studies supporting Allen’s rule demonstrate how beak size is under strong selection related to latitude and/or air temperature (Ta). Moreover, active regulation of heat transfer from the beak has recently been demonstrated in a toucan (Ramphastos toco, Ramphastidae), with the large beak acting as an important contributor to heat dissipation. We hypothesised that hornbills (Bucerotidae) likewise use their large beaks for non-evaporative heat dissipation, and used thermal imaging to quantify heat exchange over a range of air temperatures in eighteen desert-living Southern Yellow-billed Hornbills (Tockus leucomelas). We found that hornbills dissipate heat via the beak at air temperatures between 30.7°C and 41.4°C. The difference between beak surface and environmental temperatures abruptly increased when air temperature was within ~10°C below body temperature, indicating active regulation of heat loss. Maximum observed heat loss via the beak was 19.9% of total non-evaporative heat loss across the body surface. Heat loss per unit surface area via the beak more than doubled at Ta > 30.7°C compared to Ta < 30.7°C and at its peak dissipated 25.1 W m-2. Maximum heat flux rate across the beak of toucans under comparable convective conditions was calculated to be as high as 61.4 W m-2. The threshold air temperature at which toucans vasodilated their beak was lower than that of the hornbills, and thus had a larger potential for heat loss at lower air temperatures. Respiratory cooling (panting) thresholds were also lower in toucans compared to hornbills. Both beak vasodilation and panting threshold temperatures are potentially explained by differences in acclimation to environmental conditions and in the efficiency of evaporative cooling under differing environmental conditions. We speculate that non-evaporative heat dissipation may be a particularly important mechanism for animals inhabiting humid regions, such as toucans, and less critical for animals residing in more arid conditions, such as Southern Yellow-billed Hornbills. Alternatively, differences in beak morphology and hardness enforced by different diets may affect the capacity of birds to use the beak for non-evaporative heat loss.

Elevated temperatures drive fine-scale patterns of habitat use in a savanna bird community

Many animals use thermally buffered microhabitats, e.g. patches of shade within trees, to avoid temperature extremes. These ‘thermal refugia’ may mediate the impact of climate change on animals. Predicting how species and communities will respond to rising temperatures therefore requires an understanding of the availability of these refugia and how animals use them. We investigated patterns of tree use by birds in the southern Kalahari across different times of day and days of varying maximum air temperature. On ‘hot’ days (>35 °C) birds showed increased preference for trees that provided the greatest density of shade (Boscia albitrunca), and this effect was particularly pronounced at the hottest times of day. Comparisons of focal bird species with differing foraging niches revealed interspecific differences in tree use. Two arboreally foraging species showed a similar preference for B. albitrunca on both ‘cool’ and ‘hot’ days. In contrast, two ground-foraging species increased their use of B. albitrunca trees on hot days, with one species (Scaly-feathered Finch Sporopipes squamifrons) changing its behaviour from avoiding to preferring this tree. We discuss the role of B. albitrunca trees as thermal refugia and the implications of temperature-driven changes in tree use in the context of rising temperatures due to climate change.

Facial bristle feather histology and morphology in New Zealand birds: implications for function.

Knowledge of structure in biology may help inform hypotheses about function. Little is known about the histological structure or the function of avian facial bristle feathers. Here we provide information on morphology and histology, with inferences for function, of bristles in five predominantly insectivorous birds from New Zealand. We chose species with differing ecologies, including: brown kiwi (Apteryx mantelli), morepork (Ninox novaezealandae), hihi (Notiomystis cincta), New Zealand robin (Petroica australis), and New Zealand fantail (Rhipidura fuliginosa). Average bristle length corrected for body size was similar across species. Bristles occurred in distinct groups on different parts of the head and upper rictal bristles were generally longest. The lower rictal bristles of the fantail were the longest possessed by that species and were long compared to bristles of other species. Kiwi were the only species with forehead bristles, similar in length to the upper rictal bristles of other species, and the lower rictal bristles of fantails. Herbst corpuscles (vibration and pressure sensitive mechanoreceptors) were found in association with bristle follicles in all species. Nocturnal and hole‐nesting birds had more heavily encapsulated corpuscles than diurnal open‐nesting species. Our results suggest that avian facial bristles generally have a tactile function in both nocturnal and diurnal species, perhaps playing a role in prey handling, gathering information during flight, navigating in nest cavities and on the ground at night and possibly in prey‐detection. These differing roles may help explain the observed differences in capsule thickness of the corpuscles. J. Morphol., 2011.