HBW 6 - Family text: Coliidae (Mousebirds)
Family COLIIDAE (MOUSEBIRDS)
- Medium-sized arboreal birds resembling passerines, with dull grey or brown plumage, very long tail, erectile crest, and toes which can all be directed for.
- 29-38 cm.
- All bushy or wooded habitats, except dense forest.
- 1 genus, 1 species, 1 taxon.
- 2 genera, 6 species, 36 taxa.
A tiny group of only half a dozen species, the mousebirds, often referred to alternatively as colies, possess a considerable array of very peculiar features. Given their small size and short bill, together with the short neck and short legs, they could easily be taken at first sight for very long-tailed passerines. Indeed, the very earliest classifications of birds included the mousebirds in the order Passeriformes. Their creeping movements through vegetation, often recalling those of small rodents, are responsible for their having been given the name of mousebirds. This behaviour attracts attention, as does their unusual habit of perching with the body vertically suspended between widely splayed feet, held apart at the level of the upper breast. The morphological peculiarities of the Coliidae are no less evident, comprising, for example, a desmognathous palate with very small vomers, an unusually broad pygostyle, and an ulna which is short in relation to the humerus. In addition, they have a pamprodactyl foot, an arrangement whereby all four toes may be directed forwards.
As long ago as 1872, J. Murie, after studying their osteology, proposed placing the mousebirds in a separate order. Since then, there have been several, largely unsuccessful, attempts to establish their relationship to other birds. Classifications have tended to place the Coliidae in a discrete order located among the "higher" non-passerines, wherein they exhibit various affinities with groups such as the rollers (Coraciidae), the swifts (Apodidae), the turacos (Musophagidae), the honeyguides (Indicatoridae), the parrots (Psittacidae) and the trogons (Trogonidae), among others. The DNA-DNA hybridization studies carried out by C. G. Sibley and J. E. Ahlquist not only support the group’s independent status at order level, but also led those authors to propose that the mousebirds be included in a separate "Parvclass", Coliae, one of only seven comprising the Class Aves. It is quite clear, therefore, that the colies are an ancient group which, having diverged from others an extremely long time ago, have no known living close relatives.
The present distribution of the mousebirds is exclusively African. The Coliiformes is, in fact, the sole order of birds that is found nowhere else but in the Afrotropical Region; furthermore, the Coliidae is one of only five avian families that are restricted to that region, the others being the Balaenicipitidae, the Scopidae and the Sagittariidae, each with just a single species, and the Musophagidae, with its 23 species of turaco. Nevertheless, where the mousebirds are concerned, the present-day distribution seems to bear no relationship to the evolutionary origins of the group. The oldest known remains of mousebird-like birds are assigned to the family Sandcoleidae, described by P. Houde and S. Olson in 1992 from the Lower Eocene of North America, and encompassing half a dozen genera, among them the type genus, Sandcoleus. Those scientists placed the Sandcoleidae in its own order, but, in view of the large number of skeletal peculiarities which it shares with the Coliidae, it seems best to include the Sandcoleidae in the Coliiformes for the time being. Members of the Sandcoleidae have subsequently been found in two places in Europe: in the London Clay of the Lower Eocene, and in deposits from the Middle Eocene of Grube Messel, in Germany. The oldest known representative of the Coliidae, Masillacolius brevidactylus, was described as recently as 1998, by G. Mayr and D. S. Peters, from the oil-shales of Grube Messel. This species must have existed some 43-49 million years ago, in the Lutetian of the Middle Eocene, contemporaneously with at least one sandcoleid species of the genus Eoglaucidium.
Although sandcoleids are not known to have survived beyond the Eocene, the coliids seem to have persisted for a long time in Eurasia. This is evidenced by French and German fossils assigned to the Upper Eocene of Quercy, from where the genus Primocolius is already quite similar to living forms, to the Oligocene of Frauenweiler, from where Oligocolius brevitarsus was described by Mayr in the year 2000, and to the Miocene of Grive-Saint-Alban. On the other hand, the only known African fossils are relatively recent, from the Pliocene, a period which began only some five million years ago. These were found in phosphate mines at Langebaanweg, in Cape Province, and are of a species so similar to living forms that it has been included in the genus Colius, and named Colius hendeyi. The limited amount of paleontological evidence currently available may, therefore, support a hypothetical origin for the mousebirds in the northern continents, when these were extensively interconnected at the beginning of the Tertiary, and a subsequent penetration of Africa during the Miocene, when that continent and Eurasia drew together and finally met.
The six species of the Coliidae are currently placed in two genera, Colius and Urocolius, which differ substantially in skeletal and other aspects. In Urocolius, the bones of the wing and pectoral girdle are relatively more robust, and those of the legs and pelvic girdle relatively weaker, than those of Colius. This reflects the relative locomotory capacities of the two genera, Urocolius being stronger fliers and Colius more adept at creeping. The mandibles are relatively straight in Colius, but in Urocolius the distal half is decurved by some 20° in relation to the proximal half. Urocolius has a narrower tail, with five pairs of rectrices, as opposed to six pairs in Colius. In addition, Urocolius lays patterned eggs, whereas those of Colius are unmarked, and the pulli differ in the shape of the bill, which in Urocolius has a curious bulbous swelling at the base. These distinctions, among many others, have been considered by some authorities sufficient to justify the recognition not just of two genera, but of two subfamilies, Coliinae and Urocoliinae, a viewpoint supported by DNA-DNA hybridization studies. R. Verheyen proposed this division into subfamilies as long ago as 1951, but numerous subsequent authors have, nevertheless, regarded Urocolius as no more than a subgenus of Colius.
Four species are distinguishable in the genus Colius. The Speckled Mousebird (Colius striatus) is the most widespread of these, occupying much of the centre, east and south of the African continent. It completes a ring of species together with the allopatric Red-backed Mousebird (Colius castanotus), which is confined to western Angola, and the White-backed Mousebird (Colius colius), which extends from Namibia through western and central South Africa. It is only in the latter country that the Speckled and the White-backed Mousebirds show a marginal overlap in distribution, although even there they still remain largely separated by habitat preferences. Finally, East Africa, and specifically parts of Kenya, southern Somalia and the extreme north-east of Tanzania, is inhabited by the distinctively marked White-headed Mousebird (Colius leucocephalus), which is sympatric with the Speckled Mousebird but associated with more arid regions than those occupied by the latter species.
In contrast, the two species of Urocolius are allopatric, and may be regarded as forming a single superspecies. The Blue-naped Mousebird (Urocolius macrourus) occupies a broad belt of the Sahelian and Sudanese regions, from Mauretania and Senegambia across to Ethiopia and Somalia and southwards in East Africa to Tanzania. The Red-faced Mousebird (Urocolius indicus) is found in the southern third of the continent, extending north to the Angolan coast, south-eastern Zaire and Tanzania.
The complexity of subspecific differentiation within the Coliidae bears some positive relationship to the geographical extent of each species’ range, although it is also influenced by the degree of sedentariness of each species (see Movements) and by the degree of habitat fragmentation. Whereas the Speckled Mousebird has some twenty subspecies, well differentiated by plumage and by bill, leg and iris colours, and the Blue-naped and Red-faced Mousebirds have seven and five respectively, the White-backed and the White-headed Mousebirds each have only two subspecies, while the Red-backed Mousebird is monotypic.
H. Schifter, in his 1985 review of the Coliidae, recognized 19 subspecies of the Speckled Mousebird. He grouped these into three allopatric assemblages, which he regarded as "semi-species". The "striatus group", which comprises five subspecies, including the nominate, and which covers the extreme south-east of the continent from southern Malawi to the Cape, is distinguished by, among other features, an entirely black upper mandible, other races having whitish or bluish marks on the culmen. The "leucotis group" exhibits strikingly contrasting white ear-coverts, as the name suggests, and includes the greatest number of races, twelve in all, distributed across much of East Africa. The third and final group, the "nigricollis group", with only two subspecies distributed through central and western Africa, from Ghana and Angola to Zaire, exhibits the pale culmen marks, but with dull, non-contrasting ear-coverts.
The small body, long tail and dull brown or grey coloration are mousebird features which reinforce the group’s vernacular name. The tail takes up about two-thirds of the total body length of some 30-35 cm. It is longest in the genus Urocolius, with the rectrices of the Blue-naped Mousebird being up to 28 cm long, making that species’ scientific name of macrourus clearly appropriate. Besides being long, the tail is slender and graduated, and has particularly rigid shafts. The short, rounded wings have ten primaries and ten secondaries. Other noteworthy structural attributes include a short, robust and slightly decurved bill, a usually fanned but erectile crest, short legs with relatively large toes, and strong, sharp, hooked claws. The six species are fairly similar in their measurements and masses. These are smallest in the White-headed and White-backed Mousebirds, both of which are species of arid zones and weigh some 35-40 g, and greatest in the Red-backed and Red-faced Mousebirds, weighing about 60 g.
Male and female mousebirds are alike, having a dun appearance, but the plumage generally includes some clear species-specific features. The two Urocolius species have a patch of bare red skin on the face and a fleshy base of the bill, while the Blue-naped Mousebird has, in addition, a conspicuous turquoise-blue nape mark. Both the White-backed and the Red-backed Mousebirds are distinguished by the markings on the rump and lower back, these being white and maroon in the former and an intense chestnut colour in the latter. The White-headed Mousebird, as the name implies, has much of the head and crest white. By contrast, the most soberly attired species, the Speckled Mousebird, has head markings which may be black, white or rufous, according to subspecies. The legs and feet of all the coliids are more or less reddish, tending towards coral-pink in Colius and purplish in Urocolius. Similarly, the adult bill colour shows generic distinctions, the ramphotheca being black and red in Urocolius, whereas in Colius it is black on the upper mandible, at least at the tip, and grey or silvery on the lower mandible.
Mousebirds are essentially frugivorous birds (see Food and Feeding). They spend most of their time in the dense foliage of trees and shrubs, through which they move rapidly and with surprising agility, continually demonstrating their acrobatic prowess. They scurry rapidly lengthwise along horizontal branch surfaces, supporting themselves with the tarsi, tail and bill. The highly flexible foot structure, which allows them to oppose one or two toes, or to turn all four forwards, makes them equivalent to species having anisodactyl, zygodactyl or pamprodactyl feet. Such feet are a special adaptation as much to their foraging style as to food-handling, being used both to help the birds gain access to food and to transfer food to the bill. The toe positions not only are continually varied, but may even differ simultaneously between the left foot and the right one. This capacity to rotate the outer and inner digits at will is made possible by a special arrangement of muscles and tendons which includes two small inner muscles peculiar to the group, as well as an extension to the hallux of the extensor digitorum longus, a muscle which in other bird groups, with the exception of the cockatoos and parrots (Psittaciformes), inserts solely on the anterior digits.
The unusually forward-placed and laterally displaced legs of the mousebirds perhaps enable them to rotate these limbs more widely and effectively. Nevertheless, their adaptations to arboreal creeping do not seem to inhibit their ability to move on the ground, where mousebirds show themselves to be reasonably nimble in walking, running or jumping, which they do generally with the hallux and the fourth toe directed backwards.
Very probably, the strange perching style of mousebirds is related to the forward position of the legs themselves. Although mousebirds can perch briefly in the same manner as that of other birds, their usual habit is to hang with the belly down between the legs and with the feet at upper-breast level. In this position, they generally use the tail or lower abdomen to prop themselves against some support, frequently a small branch but also very often the body of some neighbouring flock-member. When thus suspended, they are able to engage an anatomical device, such as that possessed by bats, which permits them to hang without additional energy expenditure, a feature which explains instances of dead birds having been found still perched. The flexor tendons of the toes pass through a grooved sheath, which is also present in other birds and which serves to restrain slippage, but which is particularly effective in the Coliidae, given that these have particularly thick tendons enclosed by a striated epithelium. It is also the case that these tendons do not insert at the bases of the outer phalanges but, instead, do so more distally so that, when the leg is flexed, the claws automatically move downwards.
Mousebird flocks typically move in line from bush to bush and by means of short flights in which glides are alternated with brief bursts of vigorous flapping. The body and tail shapes and the flight styles of these birds have prompted comparison with parakeets or miniature pheasants (Phasianidae), or even with "arrows flying feathers-foremost". They generally descend from the apex of a shrub to the base or middle portion of another, in which they land rather boisterously. The short, rounded wings, typical of species which inhabit dense cover, allow considerable bursts of speed, the Red-faced Mousebird having been timed at 74 km/h, but they probably do not permit particularly lengthy or sustained flights.
The plumage of mousebirds also displays some peculiar features. The contour feathers cover the body almost uniformly, leaving only one or two apteria on the head. There is no down, but on the other hand the aftershafts are unusually long, each one being up to four-fifths the length of the main shaft. In addition, the contour feathers have loose distal barbs owing to the incomplete development of the barbules, which may be an interesting adaptation to moving unobtrusively through dense scrub, and which confers a soft, hair-like and, indeed, mouse-like quality to the plumage.
As with so many other tropical bird species, the moult occurs throughout the year and is apparently not influenced by the demands of reproduction or migration. Reproduction is not particularly demanding energetically, given the small clutch sizes (see Breeding), while migration is virtually non-existent (see Movements). A seasonal pattern of primary moult has been reported only from South Africa, where the climate is more temperate. In that region, primary moult was apparent in 80% of individuals of the Speckled and the Red-faced Mousebirds examined between November and April, in contrast to only 25% of the Speckled and no Red-faced at any other times of the year. Also in South Africa, there is a tendency for nesting to be to concentrated between August and October, so that the main moult period becomes post-nuptial, as is generally the case among species living in temperate and cold countries.
Plumage replacement by coliids is so slow that some individuals, such as those of the Speckled Mousebird in Tanzania, have been described as being in a nearly permanent state of moult, or even as having an overlap between two successive moult cycles. The moult patterns, too, are very irregular. Although replacement of the flight-feathers seems to follow the pattern most commonly seen in birds, with the primaries replaced descendantly and the moult of the secondaries beginning at both extremities, the mousebirds exhibit irregularities and exceptions of all kinds. The lack of any regular moult sequence is the norm where the rectrices are concerned, where the longest feathers are subject to much abrasion and may even show worn tips before they are fully grown.
Mousebirds of one or another species can be encountered in an extremely broad range of Afrotropical habitats, avoiding only dense forest, extreme desert regions and mountain peaks. In effect, these birds occupy virtually any type of scrub or light woodland, from semi-desert to forest edge and second-growth forest. In addition, they adapt readily to habitats modified by human activity, being frequent or abundant in cultivated land, in areas colonized by exotic flora, and also in suburban or urban parks and gardens. All this apart, interspecific differences in habitat selection exist which are often related to climatic factors, and which become most apparent where the ranges of different species overlap.
Most of sub-Saharan Africa is covered by the combined geographical ranges of the members of this family. Nevertheless, there are at least three extensive regions from which the mousebirds seem to be totally absent. One of these is the great expanse of lowland evergreen forest in the Congo Basin. A second region, their absence from which is hard to explain, extends across the countries to the north of the Gulf of Guinea, from southern Senegambia to eastern Nigeria, within which coliids have been reported only from a small part of Ghana, the Mole Game Park, which has an isolated population of Speckled Mousebirds. The third region covers most of eastern and central Angola, a region dominated by Brachystegia woodland; this is also a habitat which mousebirds avoid, perhaps because of a lack of adequate food during the dry season. At the other extreme, three species overlap in just two areas, both of limited extent, one around Kenya and the other in the centre and south of southern Africa. Hence, it is not possible to find more than one or two species at a time over most parts of the Afrotropical Region. Even where three species occur, they tend to be segregated by habitat and are unlikely to be seen together in a single locality.
The species which is most often found with other members of the family is the Speckled Mousebird, the most widespread of the Coliidae and one which seems to favour more mesic or even humid climatic regimes. Where such overlaps involve only one other species, the latter is generally of the genus Urocolius, the Blue-naped Mousebird in the north and the Red-faced Mousebird in the south. Both Urocolius species appear to tolerate a wide range of climatic conditions and, given their superior flying ability, they may exploit the habitat in different ways. Where three species co-occur, they include a second Colius species with an affinity for arid zones, this being the White-headed Mousebird in East Africa and the White-backed Mousebird in southern Africa. There seems to be a greater overlap in habitat between the Blue-naped and the White-headed Mousebirds in Kenya, but the latter’s range there is fragmented and its population densities are low.
In southern Africa, the three species which may share similar habitats nevertheless display a considerable degree of flexibility in habitat selection, although with one or other species being numerically dominant in any given region. Here, the White-backed Mousebird is most abundant in the west; tolerating very arid conditions, it flourishes in the Karoo and the Kalahari and it penetrates the Namib Desert. In contrast, to the south and east, the Red-faced Mousebird seems to thrive best in various types of thorn-woodland, and the Speckled Mousebird in denser vegetation such as euphorbiaceous bush or macchia, where it may find a more humid micro-climate.
In mountain regions, the Speckled Mousebird has been reported at an altitude of 1800 m in Zimbabwe, at 2300 m in Cameroon and above 2500 m in Kenya. Nevertheless, in the southern highveld of, for example, Lesotho, it soon becomes rare or absent, its limits being marked by the -7°C isotherm, corresponding to the average minimum temperature of the coldest month, July. Other species are more restricted to lower altitudes: in Kenya, for instance, the Blue-naped Mousebird does not normally range above 1600 m, nor the White-headed Mousebird above 1400 m. In arid lowland regions, on the other hand, even the most tolerant species tend to seek out the most vegetated zones, such as those along watercourses or, very frequently, in irrigated farmland.
Mousebirds occur in flocks throughout the year, even when breeding. These are usually small groups, of about half a dozen individuals, but larger gatherings of 20-30 or more birds occur where food is abundant, or at roosts. Isolated pairs or individuals are only occasionally encountered. For the Speckled Mousebird, studies carried out in Gabon, Congo and Cameroon have revealed mean flock sizes of, respectively, 7·0, 8·4 and 8·5 birds. These tend to be family groups, comprising both adults and immature birds, apparently centred on related males. The groups show notably strong social cohesiveness. All daily activities, including foraging, resting and grooming, are carried out communally, with constant vocal communication being maintained. In addition, flock-members very often make direct physical contact with one another, without showing the respect for individual distance demonstrated by other gregarious bird species. Perched mousebirds often prop themselves against each other, belly to belly. Furthermore, at various times during the day, and invariably when roosting, all members of the flock huddle closely together. Allopreening is seen much more frequently than it is among other avian species, and it has an obvious social function, together with food-offering, perhaps reflecting group hierarchies.
This mutual attraction between conspecifics seems to allow mousebirds to accept newcomers into their flocks relatively willingly. M. K. Rowan, who studied these birds in South Africa over many years, relates how wild mousebirds used to visit captives in her outdoor aviaries, attracted by their calls, and how they would perch on the cages and even preen the inmates. Similar observations have often been made elsewhere. There is even an instance of captive Speckled Mousebirds passing food to wild visitors. Despite such behaviour, however, and in contrast, violent territorial conflicts between flocks of that same species have been reported, both in Gabon and in Congo, as well as instances where captive groups have killed individuals which have been newly added to the cage.
Feeding activity, which occurs at widely spaced intervals throughout the daylight hours, seems to take up a relatively small proportion of the daily routine of mousebirds (see Food and Feeding). Much more time is devoted to resting and to plumage maintenance. The latter involves frequent dust-bathing on the ground, water-bathing or the use of dew being relatively rare. Such baths may help to reduce ectoparasite loads, which seem to be high in mousebirds, probably as a result of their propensity for frequent shared body contact. Observations on captives held in aviaries suggest that dust-bathing groups always post a sentry, a duty which is rotated among flock-members. Sun-bathing is frequent, too, especially in the early morning, when it may serve to dry the plumage, and just before sunset.
Groups rest regularly, and their members then often form clusters, especially during cold or wet weather. For Speckled Mousebirds in Congo, S. Yamagishi and G. Kabango recorded such behaviour twelve times a day on average, for up to 39 minutes at a time, the mean duration of rest periods being 7·6 minutes. It is unsurprising, therefore, that these birds tend to cover little ground each day: groups of Speckled Mousebirds may travel less than 500 m per day, and their average home ranges have been reported as only 3·3 ha in Congo and 3·5 ha in Gabon. The Gabon study additionally revealed that there is a core territory of less than 1 ha where roosts and nests are located, and that the birds may range annually over an area of between 10 ha and 15 ha.
Sleeping mousebirds form clusters in trees or shrubs, accommodating between half a dozen and a dozen individuals, sometimes more, irrespective of whether the weather is warm or cold. Captive mousebirds do the same. Clustered individuals hang in their customary posture, not head-down as in the manner of bats or hanging-parrots (Loriculus) as was long thought to be the case, although this erroneous belief is still sometimes repeated in print. They sleep with the head hunched between the shoulders, as if to minimize the body surface area. Cluster formation seems to involve competition for the innermost places, late arrivals often trying to push in. Mousebirds spend relatively more time sleeping than do other birds, gathering at roosts before sunset and not leaving until 15 minutes or half an hour after sunrise, even on fine days. As a result, they sleep for over twelve hours a day in equatorial latitudes, and for around 14 hours a day during the winter months in South Africa.
The rather indolent behaviour of mousebirds, coupled with their frequent sun-bathing and their habit of clustering together when resting or sleeping, suggested to earlier ornithologists that these birds’ thermoregulatory strategies might be unusual, or even that the Coliidae might be "imperfectly endothermic". Without going that far, it is certainly the case that in this respect, too, the mousebirds are quite original. Various authors, from A. Brehm in the early twentieth century onwards, reported observations of captive individuals which showed that the mousebirds can enter into torpidity. Thus, in the 1950’s, R. B. Cowles, after noting how a Speckled Mousebird that was kept in the dark exhibited significant falls in body temperature, from 38°C to 24°C, wrote that these birds "can and do experience cold torpor probably as a fairly regular and normal physiological phenomenon". This possibility was over a long period regarded with a certain scepticism, not least because mousebirds did not appear to be particularly cold-sensitive and could withstand low nocturnal temperatures without displaying any signs of lethargy. In addition, cases of extreme hypothermia were reported in which birds had been accidentally soaked through by heavy downpours of rain and the affected individuals had quite often died. In 1970, G. A. Bartholomew and C. H. Trost finally succeeded in inducing torpor in captive Speckled Mousebirds, not by altering the ambient temperature or humidity, but by limiting the birds’ food intake until the body mass of each was reduced by between 10% and 15%. The underweight birds entered a state of lethargy each night, during which their temperature fell to less than half the normal level and their oxygen consumption was much diminished, indicating reduced metabolic activity. The birds were able to raise their body temperature to normal unaided, in gradual stages, shortly before first light. It was apparent, therefore, that they possessed physiological mechanisms enabling them to save energy at night.
This interesting process has been studied in depth by R. Prinzinger and his collaborators, lately using transmitting sensors implanted in the peritoneal cavity which allow body temperature and other interesting parameters, such as heart rate, to be monitored continuously. These studies have revealed, among other findings, that nocturnal torpor occurs in at least four species of mousebird, and that it is particularly associated with a decline in body mass below a certain minimum. Those individuals which have access to unlimited food and have a normal body mass show a modest regular drop in body temperature at night, from approximately 42°C to 40°C in the Blue-naped Mousebird, and reductions in heart rate by about 20% and in metabolic rate from 120-140 J/g·h to around 80 J/g·h, following a circadian cycle comparable to that of many other endotherms, both mammals and birds. In contrast, those subjected to a restricted diet show an exaggerated response: their body temperature falls to 20-25°C, the heart rate declines from 250-300 to some 200 beats a minute and the stroke volume to less than half the normal, with the metabolic rate falling to scarcely 20 J/g·h. By these means, the mousebirds undoubtedly achieve significant energy savings, of the order of 90% when torpid and some 30% over a whole day.
Such strategies do, however, have their costs. Torpid birds are practically incapable of normal reactions, and so they may fall easy prey to nocturnal predators. In addition, if they are caught unawares by a rainstorm and become thoroughly drenched, with consequent loss or severe impairment of the insulating properties of the plumage, then they are at risk of irreversible hypothermia, bearing in mind that spontaneous arousal seems to be no longer possible once the body temperature falls below 18°C. Because the mousebirds lack down and the distal portions of their contour feathers have loose barbs (see Morphological Aspects), they would appear especially prone to such drenching. As a result, instances in which mousebirds are found dead on their perches, "drowned" by downpours, are relatively frequent. This risk further explains the clustering behaviour described above, as well as the tendency for roosts to be in sites affording particular shelter from rain.
It may seem surprising that torpor should be displayed by birds which are not particularly tiny, as are the hummingbirds (Trochilidae), nor dependent upon such a fluctuating and seasonally variable food as aerial insects, as is the case with the swifts or the nightjars (Caprimulgidae). The explanation may, nonetheless, revolve around dietary considerations, the basically frugivorous diet of the Coliidae being of very low calorific value and food itself being subject to periods of shortage in certain geographical areas (see Food and Feeding). Several other aspects of mousebird behaviour accord well with the consequences of energy shortage that results from the specialized diet of these birds. These include the frequency of sun-bathing and the habit of clustering. Laboratory studies have shown that the latter enables significant energy savings: individuals of the Speckled Mousebird grouped in clusters of four birds show basal metabolic rates about 20-30% lower, depending on the ambient temperature, than those of isolated birds. The employment of solar energy must also be important, given the high frequency of sun-bathing and also the manner in which it is performed: the birds expose the ventral surface, wings opened in an arc, in which posture the sparse plumage and the heavily pigmented skin no doubt assist in the absorption of solar radiation.
The complex social organization of the mousebirds, and perhaps also the fact that they live in dense habitats where visibility is often restricted, may together explain their possession of a considerably rich repertoire of vocalizations. For some species, field observations have been supplemented by aviary-based studies, which have detected low-intensity calls that are sometimes unnoticed in the field. These studies of captives have also made it possible to relate specific calls to particular aspects of behaviour with a greater precision. In this manner, a repertoire of 21 calls has been revealed for the Blue-naped Mousebird. Of these, five are related to group cohesion, two concern cluster formation, five involve various aspects of agonistic behaviour, three are associated with courtship, one is linked with incubation, and the remaining five occur during the earliest stages of the mousebird’s life; two of these last occur within the egg, and three are specific to nestlings or juveniles.
Mousebird flocks maintain vocal contact continuously, with muted chattering when the birds are in close proximity. When perched atop a tree or shrub and about to take flight, or when flying from one spot to another, they use characteristic high-pitched contact calls. In the latter context, the two genera differ substantially. Whereas in Colius these calls are short and have a harsh or buzzy quality, for example "chew-chew" in the Speckled Mousebird or "tsik-tsik-tsik" in the White-headed Mousebird, the two Urocolius species emit long, clear and melodious whistles, often far-reaching. Those of the Red-faced Mousebird have been transcribed as "tree-ree-ree" or "ti-wi-wi-wi", and those of the Blue-naped as "peeee, peeeeeeeeee", such whistles being accompanied by obvious throat movements. The contrast in call types between the two genera has been said to be due to their different mandible structures, the lower mandible being straight in Colius and angled in Urocolius, as described above (see Systematics). It may also be related to differences in flying ability between the two, the superior flying powers and consequent wider-ranging behaviour of Urocolius requiring more powerful contact calls in that genus. It is certainly the case that adults of the Blue-naped Mousebird have two types of contact call, one for short-distance and the other for long-distance communication.
Various alarm calls are uttered on the approach of potential predators. In the case of the Speckled Mousebird, at least, a distinction seems to be made between terrestrial threats, when the call is a strident "shriek", and flying raptors, when an explosive "pit" is used. Alarm calls vary in intensity, and very often are uttered in quick succession, during which the bird’s crest is alternately raised and lowered.
Crest movements and those of the bill and other parts of the body, along with vocalizations, are frequently involved in other contexts, together comprising an extensive repertoire of ritualized signals. Similarly, ritual presentation of fruit or leaves is often observed.
Food and Feeding
Mousebirds feed mainly on fruit, in various states of ripeness, but they also take other plant material such as leaves, shoots, buds, flowers and nectar. In South Africa, Rowan studied the stomach contents of a total of 63 individuals of three coliid species, collected throughout the year in different areas. She found that, apart from a few birds with empty stomachs, 50% had eaten fruits alone, 30% a mixture of fruits and leaves, and 20% only leaves, these proportions being similar for all three species. Observations on Speckled Mousebirds in Gabon show that leaves are eaten more often in the afternoons, a leaf "dinner" preceding sunset. Nevertheless, the diet of captive mousebirds consists almost entirely of fruit.
The range of plant species exploited is very broad. For example, and considering fruit consumption alone, no fewer than 40 species have been recorded as being taken by the Speckled Mousebird in South Africa, with 27 fruit species consumed in Cameroon and 22 in Gabon. Nevertheless, there are very often specific plants which, because of their local abundance, or for some other reason, seem to be especially appreciated by one mousebird species or another. The Blue-naped Mousebird, for instance, appears to depend on Salvadora persica in various parts of the Sahel, this plant also being very important to Red-faced and White-backed Mousebirds in the Namib Desert. Similarly, Speckled Mousebirds in Gabon depend chiefly on Solanum torvum. Plant genera which are cited as particularly important in the diet of mousebirds include Lycium, Solanum, Ficus, Rhus, Phoenix, Balanites, Tamarindus and Diospyros, among many others.
The above details apply to native plant species, but nowadays there are large areas where mousebirds rely more and more on exotics. These include those introduced as human food, such as mangoes, pawpaws, peaches, tomatoes, figs, strawberries, grapes, peas and almond flowers, or as ornamentals, including Jacaranda, Azadirachta, Cotoneaster and others. Even non-native weeds can be important foods of these birds, as is the case in South Africa with the American Opuntia, the European Rubus or the Australian Acacia cyclops.
All coliid species seem to have similar diets. Of a long list of food types taken in South Africa, for example, 80% were shared by at least two species and 30% by all three mousebirds present.
A surprising feature of mousebird diets is that they include, in good measure, many plants which are toxic to other animals. Among these, Rowan records for South Africa the syringa (Melia azderach), the pepper tree (Schinus molle), the bugweed (Solanum auriculatum) and even, as an extreme example, the bushman’s poison (Acokanthera spectabilis), used by bushmen and other peoples for preparing poison-arrows.
Given the wide range of plants used by mousebirds, and the birds’ lack of strict dependence on fruits alone, food availability might be thought to be fairly uniform throughout the year. This does, indeed, appear to be the case in South Africa’s Cape Province, with its Mediterranean climate, where fruiting native plants are always available and where even arid years seem to pose no dietary problems for mousebirds. Farther north, however, in Gabon, a detailed study by J.-P. Decoux showed that the fruiting period of berry-bearing shrubs is very irregular there, and that this, together with the effects of slash-and-burn farming, leads to substantial local variation in food availability for the Speckled Mousebird.
Mousebirds have a short, wide gut, lacking caeca, as might be expected of frugivores, and food transit through this is very rapid. In the Blue-naped Mousebird, the intestine of which averages 19 cm in length, the faeces are voided between 6 and 18 minutes after ingestion of fruits. The transit is much slower when leaves are consumed, which may explain why leaves are often chosen as the final meal of the day. Stomach contents have been found to average 2·5 g in weight for South African species. All this results in feeding bouts being brief and regularly spaced throughout the day. In captivity, and with food available ad libitum, mousebirds visit the feeders at a rate of about three times an hour and consume around 5 g of fruit in that time; over a whole day, this amounts to a substantial intake of food, the equivalent of the individual bird’s body weight. Each meal is very rapid, its consumption taking barely half a minute in aviary studies. Digestive efficiency is low, measured at 71% in the Blue-naped Mousebird in laboratory studies, although this compares favourably with other frugivores, where the usual range is between 30% and 70%. Sugars are, in the main, are metabolized, cellulose being egested.
Food of animal origin is noted from time to time in the coliid diet. There are numerous records of mousebirds capturing insects such as winged termites, as well as what seems tobe an exceptional observation of several Speckled Mousebirds at Mountain Lodge, on Mount Kenya, which were attracted to both raw and cooked meat put out to entice carnivorous mammals. Mousebirds have also been accused of taking the nestlings of other birds on occasions. Furthermore, it has been pointed out that the high levels of infestation with tapeworms (Cyclophyllidae) which mousebirds sometimes exhibit are difficult to explain in the absence of an animal component in the diet, although it has been suggested that the birds may become infested by taking foods contaminated by the faeces of other individuals of their own or another species. Certainly, captive mousebirds appear to show no interest in meat, mealworms or other material of animal origin, apart from ant pupae which they sometimes feed to their young.
It may be that the animal component in the diet is very rare, and that it corresponds with very specific and transient nutritional requirements. This may apply also to observations of mousebirds eating earth, such as those made by J. P. Chapin in Zaire. There, groups of Speckled Mousebirds were seen regularly to visit a particular cave, where they filled their stomachs with a red lateritic soil of significant salt content. Similarly, in Gabon, Decoux observed the tendency by the same species to take clay-rich soil at the time of the evening leaf meals, as was evident from faecal deposits below roosts.
Under normal conditions, the high water content of the diet makes drinking unnecessary, but this activity has been observed in various coliids. Both White-backed and Red-faced Mousebirds have been seen at water-holes in the Namib Desert, although only during periods when supplies of ripe Salvadora berries have been exhausted and when only small, underdeveloped, bitter ones are available. Speckled Mousebirds in Gabon often take drops of dew or rain from leaves. It is possible that the various species may differ in their need for water. As an example, the Speckled Mousebird seems to require water more than does the White-backed Mousebird, this being reflected in the latter’s tendency to frequent more arid habitats and to produce much drier, more powdery faeces than those of the former species.
When they do drink, the mousebirds reveal a further peculiarity. They do not raise the head to swallow each mouthful, but are able to suck up water in the manner of pigeons (Columbidae).
The gregariousness of mousebirds is maintained during the breeding period, when nests are frequently found close together in loose colonies which, at least on some occasions, are clearly associated with high local availability of fruit. Nevertheless, nests are more widely dispersed in many cases. Pairs are essentially monogamous and long-lasting, although there are exceptions. It is also frequently the case, although not invariably so, that mousebird pairs rely on helpers when nest-building, incubating and caring for the young, both within the nest and subsequently. Precise data on this latter phenomenon are lacking for most species, but the intensive study of the Speckled Mousebird in Gabon, carried out by Decoux, revealed the regular presence of between one and three male helpers, usually offspring of the breeding pair, as well as a similar number of satellite females. These females appear from elsewhere, and they occasionally lay eggs in the nest of the principal pair, this having been recorded in 2% of cases. Rowan also gives evidence of communal or co-operative breeding of mousebirds in southern Africa, where up to a third of nests may hold eggs of two or more females.
Although breeding attempts take place throughout the year, peak periods occur. These differ between regions and are more or less related to cycles of food availability. In the case of the Speckled Mousebird in Gabon, clutches are laid in all months but are most frequent towards the end of each of the two dry seasons, thus coinciding with the periods of maximum availability of the fruits of Solanum torvum, the principal food item there. On the other hand, in the south-east of Cape Province, in South Africa, 70% of breeding attempts by this same species fall within just three months, August, September and October, when rising temperatures following the winter rains lead to a rapid growth of vegetation. In areas where rainfall and food supply are unpredictable, the ability to nest at any time of the year may be regarded as a useful adaptation, as seems to be the case with the White-backed Mousebird in the arid regions of the Karoo and Namibia.
The complex social life of these birds must provide many opportunities for synchronizing the reproductive cycle of pairs. Mousebirds have no songs as such, but they do have various calls which may be attributed to courtship, as well as associated behaviour such as allopreening and courtship feeding. In addition, there is a peculiar pre-copulatory display, first reported for the Red-faced Mousebird and subsequently for the other species, with the exceptions of the little-studied Red-backed and White-headed Mousebirds. In this display, known as "jumping" or "bouncing", an individual sits erect on a solid branch, or even on the ground, and moves rhythmically up and down for some minutes without leaving its perch or, more often, leaps up to four centimetres in the air. The display involves both males and females, as evidenced by their final roles, and terminates when one individual approaches the other and copulation occurs, accompanied by billing and allopreening.
Mousebirds build their nests in trees and bushes. The nests themselves are similar to those of many passerines: an open-bowl structure with a basal platform and fine lining. Both sexes take part in nest construction, in some species the males bringing the materials and the females doing the actual building. The nest platform of the two species of Urocolius consists of dry, branched and often thorny twigs, but at least two of the four Colius species, the Speckled and the White-backed Mousebirds, more often include green stems and other relatively flexible plant material in this structure. Occasionally, old mousebird nests, or those of other birds, are dismantled to enable new ones to be constructed. The nest lining can include a surprising variety of materials: grasses, leaves, mosses, lichens, hair, wool, cotton wool, cobwebs and, near towns or villages, bits of cloth, paper or string. In addition, various species decorate the nest externally with flowering sprays, and furthermore, for unknown reasons, green leaves are added to the lining once eggs or chicks are present. The external decoration may serve to camouflage the nest, which is generally well hidden in the foliage, the leaves of creeping plants sometimes being made use of to aid concealment.
Other forms of nest protection include the selection of sites that are difficult of access, or in positions at some height from the ground. Nest-sites within thorny trees or shrubs are preferred by southern African species. Others elsewhere are located near wasp nests, as with Speckled and Red-faced Mousebirds in Namibia which chose to build near nests of the aggressive wasp Belanogaster rufipennis. Mousebird nests have been found from 1 m to 7 m above the ground, although a range of 2-3 m seems most usual. In southern Africa, nest heights are determined partly by the height of vegetation in particular zones and also by species-specific preferences, the Red-faced Mousebird selecting the highest sites. It has been demonstrated that rates of nest predation are, as might be expected, inversely proportional to nest height. Thus, the Red-faced Mousebird loses about one-third of nests built at a height of 2·5 m or less, one-fifth of those situated between 2·7 m and 3·7 m and only one-sixth of those placed at about 5 m or more above ground. The question arises as to why the Speckled Mousebird, which suffers significantly more nest losses than does the Red-faced Mousebird, should regularly locate its nests at lower heights. Perhaps energetics are involved, the former species being a weaker flier. The use of thorny shrubs also seems to be an effective strategy: a study of Speckled Mousebirds in Gabon found that 70% of nests in such sites were successful, as opposed to an average success rate for all sites combined of 44%.
The eggs, which are oval in shape, noticeably rough-textured and whitish, with some brownish-red markings in Urocolius but unmarked in Colius, are surprisingly small. They average 21-22 mm long and 16-17 mm wide, and weigh less than 3 g. This is only 5% or less of the female mousebird’s weight, a situation paralleled in the avian world only by the parasitic cuckoos (Cuculidae). Clutch sizes are small, generally two or three eggs, provided that only one female is involved, which, as already mentioned, is not always the case. The eggs are laid at intervals of at least 24 hours. Incubation starts with the first egg and involves both parents, and sometimes helpers as well. It is not unusual to see two birds incubating at once, or several sleeping together on the nest at night. In the Speckled Mousebird, the incubating bird is relieved frequently, every 45 minutes on average, this undoubtedly being related to the customary feeding pattern (see General Habits, Food and Feeding). The change-over is accompanied by ritual gaping and tongue-showing or by presentation of a leaf by the male. Incubation periods are very brief, around 12 days.
On hatching, the altricial young weigh 2 g or less, are blind and, especially in Urocolius, are covered with a sparse down which leaves the head, neck and much of the back bare. Chicks of the Speckled and White-backed Mousebirds, and possibly of the two other Colius species, have a brilliant yellow tongue which contrasts with the gape. Nestlings of the two Urocolius species have curious bulbous swellings at the base and on both sides of the lower mandible, giving them a strange frog-like appearance when they beg for food. The young are brooded continuously, even when they are already well feathered, and with considerable tenacity, as is also the case with incubation of the eggs. Indeed, the sitting adult sometimes has to be forcibly lifted off the nest in order to inspect its contents.
The mousebird nestlings are fed by regurgitation. Their faeces, which are soft and not encapsulated in sacs, are swallowed by the parents. This behaviour serves to maintain nest hygiene and may also be a way of maximizing food resources, being perhaps a form of refection comparable to that of such animals as lagomorphs and koalas (Phascolarctos). In fact, the Speckled Mousebird in Gabon usually feeds its chicks on a mixture of fresh material and droppings.
Fledging periods of the Coliidae are brief, lasting some two and a half weeks. Sometimes they are even shorter, given that, after ten days, the young are capable of creeping out of the nest, which they may do at times; indeed, they may even leave the nest permanently at this age if they feel seriously threatened by a predator. Beforehand, the first quills appear at around four days of age, and the eyes open on the sixth day, when the first vanes of the remiges begin to emerge from their sheaths. Under normal circumstances, the young fledge at scarcely half the weight of the adults, with a very short tail but with almost full-size wings, which allow them to take short flights. They have a very short crest and a peculiar triangular bald patch on the nape. Full body mass and plumage development are not attained until two months of age, at which time the moult of the flight-feathers begins. A further month elapses before the voice and the soft-part coloration typical of adults are acquired.
In the Speckled Mousebird, the young continue to be fed by regurgitation for a month or six weeks after fledging. Food is provided by both parents and helpers, and also, in a significant proportion of cases, by strangers. Juvenile and immature birds spend a lot of time playing in various ways, at times with other individuals, and otherwise with objects such as leaves or twigs. They remain with the parental group for some time, taking part in territory defence and helping with new breeding attempts, but, sooner or later, they usually depart. Dispersive tendencies are clearly greater in females than in males. The former experience a systematic harassment within the group which soon leads to their expulsion, but there is a possibility that some of the young males, perhaps one out of every two or three, remain with the parents for some considerable time and may come to inherit their territory.
Reproductive output among mousebirds is quite low, partly because of the small clutch sizes, but also because of losses from a variety of causes. The noticeable size differences among brood-members, the result of asynchronous hatching, make it more likely that the smallest will die. Many nests are destroyed by wind or rain, with thunderstorms accounting for the loss of about 11% of nests in Gabon. Many others are destroyed by predators, including birds such as coucals (Centropus), and reptiles such as certain arboreal snakes; in southern Africa, the predation rate on nests is 23% for Red-faced Mousebirds and 35% for Speckled Mousebirds. The latter species in South Africa has been found to fledge an average of 0·58 young per nest from a mean clutch size of 3·0 eggs, and in Gabon 0·49 young per nest from a mean clutch size of 1·9 eggs. These figures are tantamount to two breeding attempts being necessary, on average, for each young bird which fledges successfully.
On the other hand, mousebirds seem not to be particularly long-lived. Recoveries of ringed birds indicate maximum ages of little more than ten years for the Speckled Mousebird and eight years for the Red-faced Mousebird, while captive individuals have not survived longer than twelve years, figures which are more typical of passerines than they are of non-passerines. The studies of Speckled Mousebirds made by Decoux suggest that population levels of that species are maintained by the relatively rapid succession of breeding attempts. Decoux was able to follow three females over a period of about seven months. He found that two of them made three breeding attempts and the third no fewer than seven, four of those successful, from which he considers that, in the study population, each adult female may lay between four and eight clutches annually. The small size of the eggs and the low number laid in a single clutch imply a relatively modest energetic investment, thereby allowing females to lay replacement clutches only five or six days after a clutch is lost. It also enables a female to lay again some ten to 15 days after successfully fledging young, leaving other individuals of the breeding group to attend to the first brood.
The mousebirds, as a group, are undoubtedly highly sedentary birds. Nevertheless, they do exhibit a degree of dispersal or nomadic wandering and, in the case of the genus Urocolius, both members of which are superior fliers, even some well-defined seasonal movements. In the austral winter, the Red-faced Mousebird undertakes movements from the dry interior of South Africa to the more humid eastern regions, and there are recovery distances of ringed birds of 31 km and 54 km. Similarly, the Blue-naped Mousebird, in response to clear variations in food availability in Senegal, largely abandons the savannas during the driest months, from December to June, in favour of valley bottoms, where it occupies riverine woodland and gardens. Short-distance altitudinal movements also occur. For example, in Natal, the Red-faced Mousebird moves from interior uplands down to the coast.
In the genus Colius, nomadism appears to be more frequent among the two species of the driest habitats than it is among those typical of forest edges, although the available information is sparse. Thus, the White-backed and White-headed Mousebirds perhaps wander somewhat more often than do the Red-backed and Speckled Mousebirds. Observations in Gabon, however, have revealed that transient vagrant or nomadic individuals of the Speckled Mousebird, many of them yearlings, appear among established, territorial breeding groups at the beginning of each rainy season.
Relationship with Man
Mousebirds tend to be well known to the human inhabitants of the regions which they occupy. This is partly because of the general abundance of these birds and partly because of the frequency with which they visit orchards and gardens. They often receive colloquial names, some of which are onomatopoeic: for example, the Red-faced Mousebird is called "tsivovo" in South Africa and "ohivivi" in Angola, after its characteristic whistling contact call.
The members of the family have a poor reputation, in general, because of the harm which they cause by eating or damaging fruits and vegetables, as well as the buds and flowers of fruiting trees. This damage does not, however, appear to be serious in intensively cultivated areas, since the flocks stay close to woodland and field edges and seldom range far into extensive plantations. In fact, mousebirds pose a greater threat to smallholdings and to ornamental plants. In any event, they are often persecuted directly by farmers, who shoot and poison them, often in large numbers. Mousebirds have also been accidental victims of pesticide applications (see Status and Conservation).
Mousebirds are not very often encountered in captivity. They were first brought to Europe at the end of the nineteenth century, and by 1912 the Speckled Mousebird had been bred in England. Captives reproduce freely, provided they have large aviaries where they can remain in their groups, and so long as they are given suitable plants for perching, climbing and, eventually, nesting. According to several authors, hand-reared mousebirds become very tame and entertaining, given their inquisitive character, their permanent need for company, and their propensity to play with all types of objects. They survive for up to twelve years in captivity.
Status and Conservation
As a group, the mousebirds are common or very common over much of Africa, and none of the six species is declining or in any way threatened. On the contrary, all are favoured by a diversity of human activities which compensate for the mortality caused by direct persecution, pesticides and roadkills. Man, in effect, continually creates suitable habitats for these birds, as much by his destruction and fragmentation of primary evergreen forest as by his irrigating of previously desertic regions. Indeed, secondary growth, cultivation, especially orchards and fruit plantations, and gardens are ideal mousebird habitats. They are also habitats in which lower predator densities favour improved breeding success. This has been noted in Gabon, where, for the Speckled Mousebird, 58% of nests within villages are successful, compared with 50% on the outskirts and only 36% away from human habitation.
Moreover, the introduction of exotic plants has been advantageous to the Coliidae, by increasing the variety and temporal availability of their food supplies. In Senegal, for example, the recent introduction of the neem tree (Azadirachta indica) appears to be responsible for the increase and spread of the Blue-naped Mousebird in that country.
Precise data on population densities are lacking for all but one species. This is the Speckled Mousebird, which occurs at one to two individuals per hectare in Cameroon and two to three birds per hectare in Gabon. Nevertheless, the abundance levels of nearly all coliids are described as high or very high in the countries which they inhabit. The scarcest species seems to be the White-headed Mousebird, which is evidently local and rather uncommon in Kenya, the country which spans the central part of its comparatively limited range. The range of the Red-backed Mousebird, which is confined to the Angolan scarp, is more restricted still, but that species is said to be one of the commonest birds there.
In general, the geographical ranges of the mousebirds seem to be stable or expanding. The recent Atlas of Southern African Birds, published in 1997, records, for example, various cases of range expansion by coliids which are more or less clearly related to the spread of agriculture and irrigation, and the same seems to be occurring elsewhere in Africa. Thus, the colonization of new sites by the Speckled Mousebird has been reported from the Karoo, Namaqualand, Lesotho, the southern Transvaal, Zimbabwe, northern Angola, Tanzania and Kenya. Paradoxically, these range extensions could ultimately prove unfortunate from the point of view of the conservation of biodiversity, since they may, by rejoining formerly separate populations, result in the disappearance through hybridization of some of the interesting, well-defined subspecies that currently exist.
Apart from the direct persecution which they suffer because of their alleged damage to commercial crops (see Relationship with Man), the mousebirds do not appear to be subject to any major threats from humans. They have, however, been the victims of large-scale pesticide applications aimed at other species. In Senegal, the Red-faced Mousebird is the most frequent non-target species affected by control operations directed against Red-billed Queleas (Quelea quelea), the methods employed involving the terrestrial or aerial spraying of fenthion on roosts.
Another common cause of death among mousebirds is collisions with road vehicles. This often happens in the most populated regions of southern Africa, and such mishaps are exacerbated by the birds’ tendency to fly in file.
General Bibliography Abt (1995), Ballmann (1969), Bartholomew & Trost (1970), Beddard (1898), Bennett et al. (1993), Berman (1980), Berman & Raikow (1982), Bock (1994), Brehm (1911), Brodkorb (1971), Brown & Foster (1992), Cade & Greenwald (1966), Clancey (1964c), Cowles (1959), Cracraft (1981), Diamond (1985), Eiselt (1988), Espinosa de los Monteros (2000), Friedmann (1930b), Garrod (1896), Gaud (1983), Haarhoff (1994), Hanmer (1985, 1999), Hoffmann & Prinzinger (1984), Houde & Olson (1992), Korzun (1986c), Ledger (1968), Lint (1962), Maclean (1990), Manzano et al. (1998), Markus (1965), Mayr (2000), Mayr & Peters (1998), McAtee (1947), Moreau (1966), Moreau et al. (1947), Mourer-Chauviré (1988a), Murie (1872a), Peters, D.S. (1997), Peters, J.L. (1945), Pocock (1966), Prinzinger (1982b), Prinzinger & Schleucher (1996), Prinzinger et al. (1991), Pycraft (1907), Rich & Haarhoff (1985), Rowan (1967a), Schaub & Prinzinger (1999), Schifter (1967a, 1972a, 1972b, 1985, 1988, 1989, 1994), Schoonees (1963), Shelley (1885), Sibley (1996), Sibley & Ahlquist (1972, 1990), Sibley & Monroe (1990, 1993), Sibley et al. (1988), van Someren (1956), Starck (1960), Steyn (1996b), Stresemann & Stresemann (1966), Stuart & Stuart (1999), Verheyen (1956b), Winterbottom (1972b), Woodall (1974).
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