Many birds stand on one leg when resting on the ground (Clark 1973, Stiefel 1979; Necker 2010; see Liste). This behavior can best be observed in long-legged birds like storks, flamingos and herons but species with short legs, e.g. pigeons and ducks and some songbirds do it the same way. When standing on one leg birds may either rest, sleep or preen their plumage. Standing or resting on one leg requires contrived mechanisms to keep balance. The main issue of the present review is to find out how birds manage to keep equilibrium when standing on one leg (Functional Anatomy). Furthermore possible functions of this behavior are discussed (Meaning).

Functional Anatomy

Keeping balance in a biped vertebrate

Bipedal locomotion is found in humans and in birds. In humans the body is oriented vertically, i.e. in line with the line of gravity, and the center of gravity is located near the insertion of the legs. In birds the body is oriented more horizontally and the center of gravity is located rostral to the insertion of the hindlimbs (Fig. 1). This imposes special demands on keeping balance.

Birds standing on one leg: mechanisms and meaning

The legs of birds are different from bipedal humans in that they walk on their toes and there is an ankle joint which looks like the human knee but with a reversed angle. There is an upper leg with a femur and a lower leg with a tibia and a fibula. Upper leg and lower leg are connected by a knee joint (Fig. 2). The distal end of the tibia includes parts of tarsal bones. Therefore the lower leg is called tibiotarsus. The remaining tarsal elements fuse with metatarsal bones to make up the tarsometatarsus or tarsus (Baumel & Witmer 1993). The tarsus looks like a lower leg and this impression is furthered by the fact that upper and lower legs are normally hidden in the plumage. Tibiotarsus and tarsometatarsus are connected by the intertarsal joint (Fig. 2).

To keep balance when standing on both legs, the knees are flexed, which puts the knee joint near the center of gravity (Fig. 1). The antitrochanter (Fig. 2), a structure unique to birds, forms a joint with the neck of the femur which serves to prevent abduction of the femur and to absorb stresses which would otherwise act on the head of the femur (Hertel and Campbell 2007). The feet are positioned under the center of gravity which results in a stable balance of the body.

When resting on both legs, the femur is oriented nearly horizontally. A further unintended upward movement of the femur is prevented mechanically by the antitrochanter and the ligaments of the hip joint. The hip joint is now in a fixed position. Because of the high position of the knee, the center of gravity may shift to below the knee. This means that the body is suspended at the knee joint, which results in a very stable position that does not need much muscle activity to keep balance.

Standing on one leg

When resting the supporting foot is set below the center of gravity (Figs. 3, 4). This position stresses the lateral ligaments of both knee and intertarsal joints (see arrows) but these ligaments are well developed in birds. In a recent study in flamingo cadavers (Chang & Ting 2017) it was found that standing on one leg as shown in Fig. 3 (adduction of about 20 degrees from the vertical) results in a very stable support of the body. A vertically aligned leg as is the case during bipedal standing is followed by an instable body. This means that the unipedal stance of birds should not need much muscular energy expenditure.

Long-legged birds: is there a “locking” or “snapping” mechanism?

In long-legged birds like storks, herons and flamingos (to cite well-known species) the center of gravity is far from the ground. The question arises whether these birds have specialized elements in their legs to avoid overbalance. It is said that flamingos are able to "lock" their intertarsal joint in the extended position by a snapping mechanism. This should prevent unintended flexion of this joint and thus overbalance, e.g. during sleep. An early description of a stiffening of the joint is found in the book "A familiar history of birds" (Stanley 1835; see Fig. 5) but details of the construction are lacking.

There are other specializations in the intertarsal joint of long-legged birds. As shown in Fig. 8 by dashed lines, in the mid-sagittal plane there is a flexion hook of the tarsometatarsus which fits into a flexion groove of the tibiotarsus. These structures have been described already by Langer (1859) in flamingos (Fig. 9) and marabus. Langer (1859) states that these elements prevent rotation of the intertarsal joint and that this works even in the fully extended condition. However, these structures are not able to prevent the intertarsal joint from unintended flexion. Normally there are menisci and cross-ligaments in the intertarsal joint. Both structures lack in the flamingo, which means that this joint is completely unable to rotate (Stolpe 1932). Herons neither have the specialization of the trochanter nor any specializations in the intertarsal joint.

According to Stolpe (1932) there are specializations in the hip joint of long-legged birds which support a stable position when resting on one leg. There is a lateral comb in the trochanter with a deepening. When standing the body lowers in between the upper legs and the antitrochanter is lodged in the deepening of the trochanter comb. This prevents the body from forward overbalance and stabilizes the body against rotation towards the non-supported side when standing on one leg. This seems to be an important mechanism to stabilize the body of long-legged birds and to reduce muscle activity.

Conclusions

Most birds stand or sleep on one leg without having specializations in their legs. The leg is positioned in such a way that the body is well balanced without much additional muscle activity. Most long-legged birds like flamingos and storks have specializations in the hip joint and intertarsal joint which help stabilizing a body which is far from the ground. So far an often cited snapping mechanism has been demonstrated convincingly only in the ostrich, a long-legged bird who does not stand on one leg. Whether there is a similar mechanism in long-legged birds standing on one leg is unclear.  It seems that the extra-labyrinthine sense organ of equilibrium in the lumbosacral vertebral canal plays an important role in keeping balance when standing on one leg. This sense organ may even be a prerequisite for easily standing on one leg.

A useful function of standing on one foot with hiding the non-feathered part in the plumage is to reduce heat loss. Such a function is supported by recent quantitative behavioral observations. As to standing on one foot while preening or without hiding one foot in the plumage one might argue that the ability to stand easily on one foot is used even when there is no need for a reduction in heat loss, i.e. thermoregulation is probably an important but perhaps not the only function of standing on one leg. For another possible function discussed in detail, the reduction of muscle fatigue, there is so far no experimental support. The recent discovery in flamingos that standing on one leg results in a more stable body position than standing on both legs (see above: Functional anatomy/Standing on one leg) seems to be an attractive explanation why most birds prefer to rest on one leg independent of other functional implications like e.g. a role in temperature regulation.

Literature:

Anderson MJ (2016) Flamingo resting behavior: a general description and sampling of findings. In: Flamingos. Behavior, Biology and Relationship with Humans. Nova Science publishers 2016.

Anderson MJ, Williams SA (2009) Why do flamingos stand on one leg? Zoo Biology 28.:1-10.

Anderson MJ, Laughlin CP (2014) Investigating laterality, social behavior, and temperature effects in captive Chilean flamingos, Phoenicopterus chilensis. Avian Ecol. Behav. 25:3-19

Baumel JJ, Witmer LM (1993) Osteologia. In: Handbook of avian anatomy: Nomina anatomica avium. 2nd edition: 45-132. Nuttal Ornithol Club, Cambridge, Massachusetts.

Bell C (1847) Die Hand und ihre Eigenschaften (translated from the English by F Kottenkamp; original: The hand, its mechanism and vital endowment as evincing design). Expedition der Wochenbände, Stuttgart

Berndt R, Meise W (1959) Naturgeschichte der Vögel. Band 1. Allgemeine Vogelkunde. Kosmos, Stuttgart.

Bouchard LC, Anderson MJ (2011) Caribbean Flamingo resting behavior and the influence of weather variables. J Ornithol 152: 307-312.

Chang Y-H, Ting LH (2017) Mechanical evidence that flamingos con support their body on one leg with little active muscular force. Biology Letters 13: 20160948

Clark GA 1973 Unipedal postures in birds. Bird Banding 44: 22-26.

Dawson WR, Whittow GC (2000) Regulation of body temperature. In: Whittow GC (Hrsg) Sturkies´s Avian Physiology: 343-390. Academic Press, San Diego.

Flamingo file (1991): New Scientist Nr. 1782 vom 17. August 1991, Letters: Flamingo file. URL: http://www.newscientist.com/search?doSearch=true&query=Flamingo+file.

Harker TD, Harker FR (2010) Why do birds stand on on leg? - A pilot study of exotic and native New Zealand birds. Noturnis 57: 173-177.

Hertel F, Campbell KE Jr (2007) The antitrochanter of birds: form and function in balance. Auk 124: 789-805.

Kahl MP Jr (1963) Thermoregulation of the wood stork, with special reference to the role of the legs. Physiol Zool 36: 141-151.

Herzog K (1968) Anatomie und Flugbiologie der Vögel. Fischer, Stuttgart.

Langer K (1859) Über die Fussgelenke der Vögel. Zweiter Bericht. Zur vergleichenden Anatomie und Mechanik der Gelenke. Denkschriften der kaiserlichen Akademie der Wissenschaften, mathematisch-naturwissenschaftliche Klasse. Vol 16: 93-130 (plus 4 tables)

McFarland JC, Meyers RA (2008) Anatomy and histochemistry of hindlimb flight posture in birds. I. The extended hindlimb posture of shorebirds. J Morphol 269:967-979.

Midtgård U (1989) Circulatory adaptations to cold in birds. In: Bech C, Reinertsen RE (Hrsg) Physiology of Cold Adaptations in Birds: pp 211-222. Plenum, New York.

Necker R (2006) Specializations in the lumbosacral vertebral canal and spinal cord of birds: evidence of a function as a sense organ which is involved in the control of walking. J Comp Physiol A: 439-448.

Necker R (2010) Stehen der Vögel auf einem Bein: Mechanismen und mögliche Funktionen - eine Übersicht (Birds standing on one leg: mechanisms and possible functions - a review). Vogelwarte 48: 43-49

Randler C (2007) Foot preferences during resting in wildfowl and waders. Laterality 12: 191-197.

Schaller NU, Herkner B, Villa R, Aerts P (2009) The intertarsal joint of the ostrich (Struthio camalus): Anatomical examination and function of passive structures in  locomotion. J Anat 214: 830-847.

Stanley E (1835) A familiar history of birds. Their nature, habits, and instincts. Parker, London.

Steen I, Steen JB (1965) The importance of the legs in the thermoregulation of birds. Acta physiol. scand. 63: 285-291.

Stiefel A (1979) Ruhe und Schlaf bei Vögeln. Neue Brehm-Bücherei. Ziemsen, Wittenberg

Stolpe M (1932) Physiologisch-anatomische Untersuchungen über die hintere Extremität der Vögel. J Ornithol 80: 161-247.

Stresemann E (1934) Sauropsida: Aves. W Kükenthal, Th Krumbach (eds) Handbuch der         Zoologie. Band 7, 2. Hälfte. Gruyter, Berlin.

Fig. 4: Gray goose standing on one leg

Bell (1847) described in detail a snapping motion in the ostrich intertarsal joint (for explanation see Fig. 6). Bell (1847) claims that the mechanism described by him explains the peculiar "springy" gait of ostriches. However, the ostrich does not rest on one leg and Bell (1847) does not mention that the snapping mechanism might be useful when standing on one leg.

Fig. 6: Snapping mechanism in the intertarsal joint of the ostrich. On the left: extended leg; on the right: flexed leg. In the extended state the lateral ligament B rests relaxed in a groove caudal to an elevation A of the condylus of the tibiotarsus. During flexion the ligament is stretched when gliding over the elevation and relaxes again in the rostral position. An additional effect is a stretching of muscle C which improves the force exerted on the leg when pushing the body forward during walking. After Bell (1847)

Langer (1859) cites Bell (1847) but describes a somewhat different snapping mechanism in the ostrich. Due to the geometry of the tibiotarsal condylus, coming from an extended state, flexion has to overcome a point of resistance, which involves a stretching of the lateral ligament (Fig. 7). The point of resistance is at an angle of about 125° and amounts to about 3°. Langer (1859) did observe the elevation in the ostrich described by Bell (1847) but argues that it cannot be the only source of a snapping mechanism since he observed such a mechanism and hence a springy gait in bustards, storks and flamingos all of which do not have such an elevation. Cutting the lateral ligaments eliminated the snapping mechanism.

Fig. 7: Scheme to show the elongation of the lateral ligament during flexion as described by Langer (1859). Filled circles represent points of fixation of the ligament. These points are fixed in the scheme while the length of the ligament is adapted to the state of flexion (constructed by copying the tarsus to different positions). Inset on the lower right compares the lengths of the ligament according to the three states of flexion (copied from the corresponding schemes). Scheme of the intertarsal joint redrawn from Fig. 6 (Corel Draw 11®).

Stresemann (1934) refers in detail to Langer (1859) and compares the snapping mechanism to a pocket knife. Furthermore, Stresemann (1934) mentions that the snapping mechanism helps long-legged birds to stand on one leg nearly without muscle activity.

In a recent study of the intertarsal joint of the ostrich (Schaller et al. 2009) a snapping mechanism which involves ligaments and bony structures of the tibiotarsus has been described with fresh material. Coming from a fully  extended state of the joint (168°) there is an increase in resistance (measured as joint moment in Nm) up to 140° and a transition point to relaxation at 115°. It seems that this mechanism (named “engage-disengage mechanism”, EDM) makes sense to avoid unintended flexion in the ostrich regarding the always slightly flexed intertarsal joint and the body mass of about 100 kg. Whereas a snapping motion of the intertarsal joint of the ostrich seems to be proven it is not clear whether there are similar mechanisms in the much lighter long-legged birds standing on one leg with the intertarsal joint usually fully extended.

The most detailed study on the functional organization of hindlimbs of birds, which also deals with the problem of standing on one leg is by Stolpe (1932). Fig. 8 shows a parasagittal section through the lateral condylus of the intertarsal joint of the flamingo (Phoenicopterus ruber). There is a process in the tarsometatarsus which fits into a groove of the condylus of the tibiotarsus in the fully extended joint (see arrows in Fig. 8). Although this looks like a locking mechanism, Stolpe (1932) claims that it only prevents the joint from overstretching. Similar specializations are found in cranes and storks but not in herons (Stolpe 1932).

Stolpe (1932) mentions that Langer (1859) described a snapping mechanism in long-legged birds but Stolpe himself could not find such a snapping mechanism in flamingos nor in a demoiselle crane or a purple heron. Stolpe mentions that Prof. R. Hesse found a snapping mechanism in storks but Stolpe himself could not verify this because of the lack of a suitable preparation. Berndt and Meise (1959) followed the study of Stolpe (1932) in that there is probably no special mechanism in  long-legged birds.

The possible function of standing on one leg

There are many speculations but few experimental studies or quantitative behavioral observations why birds stand on one leg. A couple of possible functions are published in Flamingo file (1991).  Two possible functions which have been tested by quantitative observations in recent publications (Anderson & Williams 2009; Bouchard & Anderson 2011; Anderson & Laughlin 2014) will be dealt with in detail: a thermoregulatory function and relaxation of muscle fatigue in the retracted leg.

Thermoregulatory function. Sleeping positions and the occurrence of sleeping on one leg among many orders of birds are described in detail by Stiefel (1979). When sleeping while standing on one leg the head is often hidden in the plumage on the back (Fig. 11). The head is usually positioned on the side of the ground foot or above the center of gravity. This supports a stable balance. The retracted leg is hidden in the breast feathers or under the wing. Hiding non-feathered parts of the body (mainly lower legs and the beak) in the plumage is a useful mechanism to reduce heat loss when sleeping. Reduction of heat loss applies also to, e.g. ducks when standing on ice on one foot.

Reduction of muscle fatigue of the retracted leg. Humans tend to put the body weight on one leg when standing for longer times. This serves to reduce muscle fatigue in one leg. Accordingly, Clark (1973) suggested that standing on one leg in birds may serve a similar function. However, retraction of one leg needs muscle activity.  This is confirmed by an own observation of a resting nile goose (Alopochen aegyptiacus) whose retracted leg dropped again and again. However, when sleeping with its head on the back and with closed eyes, the leg was continuously hidden in the plumage. That leg retraction needs energy is supported by the casual own observation of a woolly-necked stork who fixed his retracted foot to the intertarsal joint of the stance leg (Fig. 14). There is no indication of structural or physiological mechanisms which may reduce muscle activity in the retracted leg as already noted by Clark (1973). During flight legs are retracted in a similar way as one leg during the unipedal stance. In a biochemical study it is shown that leg muscles involved in flight posture do not have specializations (McFarland & Meyers 2008).  However, one has to consider that hindlimb muscles of birds are close to the body (normally hidden in the plumage) which reduces the energy to lift the leg.

Humans of some tribes which use to rest on one leg (e.g. Australian Aborigines or African Bushmen) the retracted leg rests on the supporting leg  and equilibrium may be stabilized by leaning on a stick. A casual own obervation shows that storks may use the same technique (Fig. 14).

The question of reduction of muscle fatigue was addressed by Anderson & Williams (2009) in flamingos by measuring the latency of initiating a forward movement. This latency was longer following resting on one leg as compared to the latency when resting on two legs. The authors conclude that this result discounts the possible function of reducing muscle fatigue or enhancing predatory escape.

In most bird species there is no preference of the side (left/right) they use for standing on one leg (Randler 2007; Anderson & Williams 2009; Anderson & Laughlin 2014) and there is an about equal use of left and right leg in individual flamingos (Anderson & Williams 2009). However, it would be interesting to know whether there is a regular shift from one leg to the other leg in order to reduce muscle fatigue in both legs. However, it is not clear whether a reduction of muscle fatigue of the supporting leg or the retracted leg is intended. Given that retracting a leg is energy consuming (see above) one might assume that changing the retracted leg may serve reduction of muscle fatigue of the retracted leg.

Fig 12B: Mute swan on the water with left leg stretched backwards

Fig. 14: Woolly-necked stork fixing the lifted leg to the intertarsal joint of the stance leg

The legs of birds are an important site of heat exchange (Steen & Steen 1965; Dawson & Whittow 2000). In a warm environment heat of the body is dissipated via the legs. In cold ambient temperature blood supply to the legs is reduced and there is a counter-current heat exchange of the blood vessels leaving or entering the body: cold venous blood coming from the legs is warmed up by the warm arterial blood running to the legs which itself is cooled down (Kahl 1963; Mitgard 1989). This means that in the cold heat loss via the legs is strongly reduced (amounting to 10 per cent at -10° C; Steen & Steen 1965).

In recent investigations it was shown that flamingos spend more time standing on one leg in the water (facilitates heat loss) as compared to standing on one leg on the ground. Furthermore, flamingos stand more often on one leg at cool temperatures.(Anderson & Williams 2009; Bouchard & Anderson 2011; Anderson & Laughlin 2014). These quantitative behavioral observations support a thermoregulatory function of standing on one leg. There are, however, observations which show that in the range of 8 to 19 °C, i.e. at low temperatures, the incidence of standing on one leg is reduced (Harker and Harker 2010). This is supported by a casual own observation of flamingos at 2 °C. The authors argue, that the birds tend to rest/sleep only at higher temperatures. For a detailed discussion of the temperature/rest/sleep topic on standing on one leg see Anderson 2016.

Standing or resting on one leg does not necessarily mean an inactive state. Birds may practice intense preening while standing on one leg (Fig. 12A). Even aggressive behavior to neighbors was seen in flamingos while standing on one leg (own observations). Often resting birds just lift one leg partially without hiding it in the plumage (see Fotos). In preliminary own observations at the zoo of Dortmund it is shown that lifting one leg partially occurs more often at higher temperatures (27 C) than at lower temperatures (20 C). On the other hand complete retraction  of one leg was observed more often at the lower temperatures (Fig. 13). This supports the assumption of a thermoregulatory function of standing on one leg: an only partially retracted leg means less heat conservation.

Fig. 13A: Sleeping flamingos: Occurence of standing on both legs, with one leg retracted partially and one leg retracted completely.  Blue column: 20 °C (observed in 2008); red column. 27 °C (observed in 2013).

Fig. 13B: Percentage of standing on one leg with the leg retracted only partiallly. Left column: two observations (20 and 23 °C); right column: two observations (27 and 31 °C)