Information

Is the birds' decision to fly away congenital or learned behaviour?

Is the birds' decision to fly away congenital or learned behaviour?


We are searching data for your request:

Forums and discussions:
Manuals and reference books:
Data from registers:
Wait the end of the search in all databases.
Upon completion, a link will appear to access the found materials.

I see two possibilities how could the birds know what to do every fall:

  • The birds' migrations are driven entirely by the vertical memetics and today it is just a custom transferred from parents to offsprings.
  • There is a gene that causes birds to decide to fly to the warmer areas every fall, activated when it is appropriate time

Which of these hypothesis is closer to the truth?


This example proves IMHO that migration is largely nature and not nurture:
In the Netherlands, white storks were bred / reintroduced. A large part (about one third?) of the reintroduced birds do not migrate, but their offspring usually does migrate see. They couldn't have learned it from their parents, that's for sure.


Is the birds' decision to fly away congenital or learned behaviour? - Biology

S40.1: Migratory orientation: Learning rules for a complex behaviour

Kenneth P. Able 1 & Mary A. Able 1

1 Department of Biological Sciences, University at Albany, State University of New York, Albany, New York 12222, USA, fax 518 442 4767, e-mail [email protected]

Able, K.P. & Able, M.A. 1999. Migratory orientation: Learning rules for a complex behaviour. In: Adams, N.J. & Slotow, R.H. (eds) Proc. 22 Int. Ornithol. Congr., Durban: 2356-2365 . Johannesburg: BirdLife South Africa.

The ability to orient movements in the correct directions is an essential component of a successful migration. Development of the necessary compass mechanisms involves an intricate interplay of innate information and learning that is programmed and constrained by a variety of rules. Young songbirds are born with apparently innate information about the direction they should fly on their first migration. Captive breeding experiments have revealed a high degree of genetic control over many of the details of this vector-navigation. The general migration direction of the species is coded with respect to celestial rotation, monitored by stars at night and patterns of polarised skylight during the day. Population-specific details of the migration direction and changes in direction seem to be coded only with respect to the magnetic field. Innate learning rules define the ways in which birds interpret celestial rotation such that they can extract information about true compass directions. Once learned, the star pattern and polarised light compasses are apparently immune to further modification. The magnetic direction of migration may be adjusted by information about true compass directions, thus effecting a compensation for magnetic declination. Various sorts of plasticity in these orientation mechanisms provide migrants with the ability to respond in apparently adaptive ways to spatial and temporal variability in the quality or availability of orientation information encountered during migration. These points are illustrated with data from our experiments with the North American night migrant Savannah Sparrow Passerculus sandwichensis and studies performed with other migrants.

Long-distance migration is one of the most complex and risk-prone tasks performed by birds. For most passerine birds, especially those that migrate at night, the first migration apparently takes place without the aid of other individuals. To be successful, the young bird must combine a variety of congenital information with experience during the first few months of life to obtain all of the skills necessary to reach an appropriate locale in which to spend the winter. The bird must migrate at the proper time of year, it must fly in an appropriate direction for an approximately correct distance, know where or when to cease migrating, and be able to find its way back to the breeding range of its population. In this paper we will focus on the orientation component of migration: how does the bird know which direction to migrate and what mechanisms does it employ to identify those directions? We will illustrate the points with data from our experiments performed with the North American Savannah Sparrow Passerculus sandwichensis (Able & Able 1996), a typical nocturnal migrant, and with the results of experiments performed on a variety of other species.

Orientation in nocturnal migrants is based upon three known compass mechanisms: a magnetic compass, star pattern compass and a compass based on patterns of polarised skylight. One can only speculate about the selection pressures that favoured the evolution of multiple compasses (Terrill 1991), but their existence provides birds with a potentially useful redundancy of orientation machinery and with the possibility of pooling information from the different sources (Wiltschko & Wiltschko 1994). The development of functional compasses in young migrants is based upon the interplay of apparently genetically-programmed information with a suite of innate learning rules. The congenital information becomes combined, via these learning rules, with relevant environmental stimuli to produce functional compasses that not only confer effective orientation ability, but also provide a degree of plasticity in orientation behaviour that enables the birds to respond to spatial and temporal variability in orientation information in ways that may provide a survival advantage.

Direction of the first migration

A considerable volume of work has shown that hand-raised migrants held in captivity exhibit migratory behaviour characterised by orientation directions and timing characteristic of free-living conspecifics from the same populations (summarised by Berthold 1996). Hypothesising that migratory behaviour was based on endogenous time and directional programmes, Schmidt-Koenig (1973) termed the phenomenon vector-navigation. Experiments performed with Blackcaps Sylvia atricapilla showed that hand-raised birds from eastern Europe showed population-typical southeastward directions in orientation cages, whereas those from farther west showed the expected southwestward direction (Helbig 1991). Captive-bred hybrids between the two populations oriented in nearly intermediate directions. A similar degree of genetic control was demonstrated in the orientation directions selected by Blackcaps that migrate from central Europe to the British Isles for the winter (Helbig et al. 1994). Several European migrants also exhibit characteristic changes in direction during the course of migration (e.g. those that migrate to Africa around the western end of the Mediterranean Sea first fly southwestward and later turn to more southward or southeastward directions). These changes in direction also appear to be under genetic control (Gwinner & Wiltschko 1978 Helbig et al. 1989).

D eveloping a compass to serve vector-navigation

The information that comprises the directional programme of vector-navigation appears to be genetically coded in at least two ways in newborn migratory songbirds. The direction of the first migration is represented with respect to the magnetic field and with respect to the axis of celestial rotation (Wiltschko et al. 1987), but the information coded seems to be somewhat different for the two sets of cues. The development of functional compass capabilities is known to involve several complex interactions among these information systems and experience during the first three or so months of the bird’s life.

Young birds that grow up isolated from any exposure to visual orientation information (daytime or night sky) still develop a magnetic compass capability sufficient to enable them to orient in the appropriate migration direction with respect to the magnetic field (summary in Wiltschko & Wiltschko 1995). Population-specific migration directions are coded with respect to the magnetic field (Weindler et al. 1996). In several European and one Australian species in which migration routes include large changes in direction, the vector-navigation programme also contains the necessary information to enable the birds to execute those changes in orientation when raised and tested only in the presence of the magnetic field (Gwinner & Wiltschko 1978 Helbig et al. 1989 Munro et al. 1993). Studies of the Pied Flycatcher Ficedula hypoleuca, which shows a shift in the direction of autumn migration from southwestward early in the season to southeastward later, indicated that the expected change in direction occurred only if the birds experienced a change in the ambient magnetic field that would have been experienced as they migrated to lower latitudes (Beck 1984 Beck & Wiltschko 1988). These data suggest a complex interaction between the endogenous temporal programme and some parameter of the magnetic field: only when the 'expected' magnetic field condition is experienced at the proper time does appropriate orientation occur.

The data available indicate that a quite substantial amount of ecologically appropriate orientation behaviour can develop in birds whose experience is limited to growing up in a magnetic field with properties similar to that of the earth. Development of a functional magnetic compass capability might be restricted to a range of magnetic field intensities similar to those found on the earth (Wiltschko 1978), and the inclination or dip angle of the field may also affect the resultant magnetic orientation (Weindler et al. 1995, 1998).

The migratory compasses based on visual information also develop during the months prior to the first migration. Many species of nocturnally migrating songbirds possess compasses based on star patterns and patterns of polarised skylight at dawn and dusk. Classic experiments by Emlen (1970 Wiltschko et al. 1987) showed that configurational star patterns acquire learned directional meaning from the axis of stellar rotation. Once this learning process has been completed, rotational information is no longer required, and the static relationships between stars are sufficient for meaningful orientation: birds that have reached migratory age and been exposed to stellar rotation when young can orient under stationary planetarium skies. This process seems to be guided by some innate rules. Birds are apparently predisposed to pay attention to the movement of celestial objects and to identify the center of celestial rotation (true north). This information is then interpreted in light of a rule that translates the genetically coded migration direction into this frame of reference, e.g. fly away from the center of rotation.

Visual information at sunset provides important compass information for many species of nocturnal migrants (Moore 1987 Able 1993 Wiltschko et al. 1997). Polarised skylight patterns, rather than the sun itself, seem to provide the relevant directional information (Helbig 1990a, 1991). During daytime, these patterns of polarised skylight apparently provide the relevant stimulus from which celestial rotation is assessed, but it is not yet clear whether the birds directly observe the dynamics of rotation or locate the pole point by observing static patterns of polarised light, e.g. at dawn or dusk (Phillips & Waldvogel 1988 Able & Able 1990a, 1995a). Similar to the star pattern compass, once the pattern of celestial rotation has been learned, birds are able to determine orientation directions essentially instantaneously from static polarised skylight patterns just after sunset (Able 1989).

These visual compasses appear to develop to an extent at least sufficient to enable a bird to identify its general migration direction even if the birds never have experience with the visual orientation cues in the presence of magnetic information (but see Katz et al. 1988). Savannah Sparrows reared outdoors in a vertical magnetic field (no directional information) oriented southwestward when tested just after sunset (also in a vertical magnetic field) (Able & Able unpublished data), and Pied Flycatchers reared under similar conditions oriented in the same direction as controls under stars (Bingman 1984). Further evidence of the general independence of the development of visual compasses from magnetic influence comes from experiments in which birds have been raised with exposure to natural and artificial visual orientation cues only within shifted magnetic fields. In all such cases, stellar or sunset orientation was unaffected by rearing in the shifted field (Bingman 1984 Wiltschko 1982 Wiltschko et al 1987 Able & Able 1997). Whereas the evidence indicates that at a coarse level, the ontogeny of visual compasses is immune to magnetic influence, recent experiments have shown that more subtle interactions are occurring in at least one species (see below).

I nteractions during development

Two types of interactions of cue systems and innate information have been identified during the development of compass capabilities. The first involves the transfer of information about the population-specific details of migration direction from one cue system to another. As noted above, Weindler et al (1996) found that in hand-raised Garden Warblers Sylvia borin, the innate information indicating that southwest is the initial direction of autumn migration seems to be coded only with respect to the magnetic field. Birds exposed to rotating artificial stars in a vertical magnetic field hopped toward south those exposed to the same sky in the presence of the magnetic field oriented in the expected southwestward direction typical of the population. This result suggests that the migration direction coded with respect to celestial rotation may be only a general one, e.g. away from the centre of rotation. The more specific directional information exists initially only with respect to the magnetic field, but under normal conditions is transferred to visual cues during the learning of stellar rotation. Additional experiments indicated that for this transfer of information to occur, the sense of stellar rotation must be that of the natural sky (Weindler et al. 1997). Whether similar complex and subtle processes are going on in other species is not known. In Savannah Sparrows, sunset orientation was identical in sparrows raised outdoors in a normal magnetic field and in those raised outdoors in a vertical magnetic field (Able & Able unpublished data). This suggests that in this species, no additional information not coded with respect to celestial rotation was available via the magnetic field.

The second interaction involves a transfer of information between celestial rotation (which reveals true compass directions) and the preferred magnetic direction of migration, a process referred to as calibration of magnetic orientation. In experiments with Savannah Sparrows and Pied Flycatchers, it has been found that if hand-raised birds experience celestial rotation only in a situation in which magnetic compass directions are different from true compass directions (magnetic declination), the magnetic orientation expressed during the first autumn will be altered (Bingman 1983 Bingman et al 1985 Prinz & Wiltschko 1992). The birds raised in a large magnetic declination will orient in the magnetic direction that corresponded to the appropriate true migration direction (e.g. if the expected migration direction is south and the bird’s experience was that magnetic east corresponded to true south, it will orient toward magnetic east when tested in the magnetic field without visual cues).

Experiments have shown that the visual information responsible for this calibration of magnetic orientation is celestial rotation. Stellar rotation at night (Able & Able 1990b) and polarised skylight in the daytime (Able & Able 1993, 1995a Weindler et al. 1998) provide the necessary information about true compass directions employed in the calibration. Such primacy of true compass directions over magnetic ones provides birds that might grow up in a region of large magnetic declination with a means of bringing their various orientation mechanisms into conformity. This makes adaptive sense inasmuch as true compass directions are the ones most relevant to a migrant required to move from high to low latitudes on its first migration, and many Savannah Sparrows are born in areas with large magnetic declination wherein such developmental plasticity might be advantageous.

Plasticity in the system

Varying degrees of openness and plasticity characterise migrant bird orientation mechanisms, both during early development and as functional components of an adult bird’s migratory compasses. During development, transfers of information take place, in both directions, between orientation based on visual cues and that based on the magnetic field. Based as they are upon celestial rotation, an invariant source of true compass directions, there might be no advantage in having the visual compasses remain susceptible to modification later in life. The only experimental evidence relevant to this question comes from an experiment on Indigo Buntings Passerina cyanea. An incorrect star pattern compass learned during the first summer of life was not subsequently modified when the birds were exposed to a different (and normal) stellar rotation during their second summer (Emlen 1972). More study of the time course of learning of these behaviours is needed, but this one experiments suggests the existence of a finite sensitive period for learning that may end prior to the first migration.

Of course, the potential advantages of possessing a somewhat flexible orientation system do not end with the onset of the first migration. During migration, birds may experience substantial spatial and temporal variability in the environmental information that forms the bases of their compasses (Table 1). We have tended to assume that most plasticity in orientation systems ended by the time the first migration began, but few experiments have tested this assumption. Adult as well as first-summer Savannah Sparrows, exposed to clear day and night skies within a shifted magnetic field for four days during the migration season, exhibited the same type of recalibration of magnetic orientation found in young birds during their first summer (Able & Able 1995b). By alternating the birds’ exposure between shifted and unshifted fields, we found that this calibration process may occur repeatedly over the course of a single migration season. For a species like the Savannah Sparrow that calibrates magnetic orientation in response to declination on the breeding ground, such an open-ended plasticity makes sense. Magnetic orientation calibrated to a particular value of declination in the natal area would result in orientation errors when the bird migrated into an area where declination was markedly different: the calibrated magnetic preference would no longer correspond to the correct true compass direction.

Other species do not seem to respond in the same way. For example, in the Australian Silvereye Zosterops lateralis and several European species, magnetic orientation remained unchanged following exposure to visual cues in a shifted magnetic field during the migration season. In fact, in some cases the orientation direction with respect to visual cues was altered, i.e. magnetic information appeared to calibrate orientation based on visual information (Wiltschko, et al. 1997). There may be many reasons for such differences in results and they confound our desire for generality of orientation mechanisms across species. Indeed, in terms of the basic mechanisms of compass orientation, there does seem to be broad similarity that spans a diversity of taxa and little compelling evidence for interspecies differences (Helbig 1990b). On the other hand, if birds have evolved flexible, interactive orientation behaviour as an adaptation enabling them to cope with various sorts of environmental variability, we should probably expect to discover species-specific differences as we explore ever finer details of the orientation mechanisms. All migratory birds may possess the same suite of compasses, but the details of their workings and relationships may differ in ways that reflect the evolutionary histories of the different lineages. In this particular case, Savannah Sparrows occupy a breeding range that encompasses a wide range of magnetic declination, inclination and total intensity. In contrast, across western Europe, Africa, and the small range of the Tasmanian population of the Australian Silvereye, magnetic variation is slight. The migration route of the silvereye encompasses only about 2 o of declination, and birds migrating between western Europe and Africa are unlikely to encounter magnetic declination values greater than about 10 o (versus Savannah Sparrows born at high latitudes, which might experience declination values of 50-60 o ). It is perhaps not surprising that individuals of these species seem not to have evolved means of coping with conditions that neither they nor their recent ancestors has experienced.

Innate information and learning rules

The foregoing examples illustrate the sorts of complex interactions of innate information and programmed learning that characterise the development of compass orientation mechanisms in migratory birds. Experimental data reveal a substantial amount of apparently genetically programmed information (Table 2) and canalisation of development through a series of rules by which that information interacts with experience with stimuli to which the animals are to some degree predisposed to respond (Table 3). At the same time, the richness of the system, with its multiple compasses and susceptibility to open-ended calibration, imbues migratory orientation with a remarkable flexibility.

There are many obvious parallels between the development of migratory orientation and the ontogeny of passerine song. Although the history of experimental work in the two areas is of similar duration, the song system is much more thoroughly understood. There are a number of reasons for this. Song is a more robust and tractable behavioural assay than is migratory orientation and this facilitates behavioural studies. Secondly, major portions of the neural circuitry involved in the learning and control of bird song are known. In the case of migratory orientation, almost nothing beyond the level of the sensory receptors is known, and in the case of the magnetic field, even the receptor(s) are not fully characterised (e.g.Walker et al. 1997). In the brain itself, there is evidence that melatonin is necessary for the expression of magnetic migratory orientation, perhaps required for the transfer of the innate migratory direction into a direction with respect to the magnetic field (Schneider et al. 1994) and that the hippocampus may be somehow involved in sun compass orientation in homing pigeons (Bingman et al. 1996). There must exist dedicated brain regions in which the innate components of vector-navigation are integrated with sensory information acquired during early experience with the relevant orientation cues, analogous to the well-known centres associated with the song system. Identifying the neural substrates of migratory orientation is the route to the next major breakthrough in our understanding of this behaviour, but much work will be required to chart that path.

Our work on migratory orientation has been generously supported over the years by the National Science Foundation (grants BNS7923711, BNS 8217633, BNS 8608653, BNS 8909886, IBN 9119508, and IBN 9419644).

Able, K.P. 1989. Skylight polarization patterns and the orientation of migratory birds. J. Exper. Biol. 141: 241-256.

Able, K.P. 1993. Orientation cues used by migratory birds: A review of cue-conflict experiments. Trends Ecol. Evol. 8: 367-371.

Able, K.P. & Able, M.A. 1990a. Ontogeny of migratory orientation in the Savannah Sparrow, Passerculus sandwichensis: mechanisms at sunset. Anim. Behav. 39: 1189-1198.

Able, K.P. & Able, M.A. 1990b. Calibration of the magnetic compass of a migratory bird by celestial rotation. Nature 347: 378-380.

Able, K.P. & Able, M.A. 1993. Daytime calibration of magnetic orientation in a migratory birds requires a view of skylight polarization. Nature 364: 523-525.

Able, K.P. & Able, M.A. 1995a. Manipulations of polarized skylight calibrate magnetic orientation in a migratory bird. J. Comp. Physiol. A 177: 351-356.

Able, K.P. & Able, M.A. 1995b. Interactions in the flexible orientation system of a migratory bird. Nature 375: 230-232.

Able, K.P. & Able, M.A. 1996. The flexible migratory orientation system of the Savannah Sparrow (Passerculus sandwichensis). J. Exper. Biol. 199: 3-8.

Able, K.P. & Able, M.A. 1997. Development of sunset orientation in a migratory bird: No calibration by the magnetic field. Anim. Behav. 53: 363-368.

Beck, W. 1984. The influence of the earth magnetic field to the migratory behavior of Pied Flycatchers (Ficedula hypoleuca Pallas). In: Varju, D. & Schnitzler, H.-U. (eds) Localization and orientation in biology and engineering. Berlin Springer-Verlag: 357-359.

Beck, W. & Wiltschko, W. 1988. Magnetic factors control the migratory direction of Pied Flycatchers (Ficedula hypoleuca Pallas). In: Ouellet, H. (ed.) Acta XIX congr. intern. ornithol. Ottawa Univ. of Ottawa Press: 1955-1962.

Berthold, P. 1996. Control of bird migration. London Chapman & Hall: 355pp.

Bingman, V.P. 1983. Magnetic field orientation of migratory naive Savannah Sparrows with different first summer experience. Behaviour 87: 43-53.

Bingman, V.P. 1984. Night sky orientation of migratory Pied Flycatchers raised in different magnetic fields. Behav. Ecol. Sociobiol. 15: 77-80.

Bingman, V.P., Beck, W. & Wiltschko, W. 1985. Ontogeny of migratory orientation: A look at the Pied Flycatcher, Ficedula hypoleuca. In: Rankin, M.A. (ed.) Migration: Mechanisms and adaptive significance. Austin Univ. of Texas Press: 543-552.

Bingman, V.P., Gagliardo, A. & Ioale, P. 1996. Hippocampal participation in the sun compass orientation of phase-shifted homing pigeons. J. Comp. Physiol. A 179: 695-702.

Emlen, S.T. 1970. Celestial rotation: Its importance in the development of migratory orientation. Science 170: 1198-1201.

Emlen, S.T. 1972. The ontogenetic development of orientation capabilities. In: Galler, S.R., Schmidt-Koenig, K., Jacobs, G.J. & Belleville, R.E. (eds) Animal orientation and navigation. NASA SP-262 Washington, D.C. U.S. Government Printing Office: 191-210.

Gwinner, E. & Wiltschko, W. 1978. Endogenously controlled change in the migratory direction of the Garden Warbler, Sylvia borin. J. Comp. Physiol. A 125: 267-273.

Helbig, A.J. 1990a. Depolarization of natural skylight disrupts orientation of an avian nocturnal migrant. Experientia 46: 755-758.

Helbig, A.J. 1990b. Are orientation mechanisms among migratory birds species-specific? Trends Ecol. Evol. 5: 365-366.

Helbig, A.J. 1991. Inheritance of migratory direction in a bird species: A cross-breeding experiment with SE- and SW-migrating Blackcaps (Sylvia atricapilla). Behav. Ecol. Sociobiol. 28: 9-12.

Helbig, A.J., Berthold, P. & Wiltschko, W. 1989. Migratory orientation of Blackcaps (Sylvia atricapilla): Population-specific shifts of direction during the autumn. Ethology 82: 307-315.

Helbig, A.J., Berthold, P., Mohr, G. & Querner, U. 1994. Inheritance of a novel migratory direction in central European Blackcaps. Naturwissen. 81: 184-186.

Katz, Y., Liepa, V. & Viksne, J. 1988. Orientation research in the Latvian SSR in 1982-1985. In: Ouellet, H. (ed.) Acta XIX congr. intern. ornithol. Ottawa Univ. of Ottawa Press: 1919-1931.

Moore, F.R. 1987. Sunset and the orientation behavior of migrating birds. Biol. Rev. 62: 65-86.

Munro, U.H., Wiltschko, W. & Ford, H.A. 1993. Changes in the migratory direction of Yellow-faced Honeyeaters, Lichenostomus chrysops (Meliphagidae) during autumn migration. Emu 93: 59-62.

Phillips, J.B. & Waldvogel, J.A. 1988. Celestial polarized light patterns as a calibration reference for sun compass of homing pigeons. J. Theoret. Biol. 131: 55-67.

Prinz, K. & Wiltschko, W. 1992. Migratory orientation of Pied Flycatchers: Interaction of stellar and magnetic information during ontogeny. Anim. Behav. 44: 539-545.

Schmidt-Koenig, K. 1973. Uber die Navigation der Vogel. Naturwissen. 60: 88-94.

Schneider, T., Thalau, H.-P., Semm, P. & Wiltschko, W. 1994. Melatonin is crucial for the migratory orientation of Pied Flycatchers (Ficedula hypoleuca Pallas). J. Exper. Biol. 194: 255-262.

Terrill, S.B. 1991. Evolutionary aspects of orientation and migration in birds. In: Berthold, P. (ed) Orientation in birds. Basel Birkhauser Verlag: 180-201.

Walker, M.M., Diebel, C.E., Haugh, C.V., Pankhurst, P.M., Montgomery, J.C. & Green, C.R. 1997. Structure and function of the vertebrate magnetic sense. Nature 390: 371-376.

Weindler, P., Beck, W., Liepa, V. & Wiltschko, W. 1995. Development of migratory orientation in Pied Flycatchers in different magnetic inclinations. Anim. Behav. 49: 227-234.

Weindler, P., Wiltschko, R. & Wiltschko, W. 1996. Magnetic information affects the stellar orientation of young bird migrants. Nature 383: 158-160.

Weindler, P., Baumetz, M. & Wiltschko, W. 1997. The direction of celestial rotation influences the development of stellar orientation in young Garden Warblers (Sylvia borin). J. Exper. Biol. 200: 2107-2113.

Weindler, P., Bohme, F. & Wiltschko, W. 1998. The role of daytime cues in the development of magnetic orientation in a night-migrating bird. Behav. Ecol. Sociobiol. 42: 289-294.

Wiltschko, R., Wiltschko, W. & Munro, U. 1997. Migratory orientation in birds: The effects and after-effects of exposure to conflicting celestial and magnetic cues. In: Orientation and navigation - birds, humans and other animals. London Royal Inst. of Navigation: 6-1 - 6-14.

Wiltschko, R. & Wiltschko, W. 1994. Avian orientation: Multiple sensory cues and the advantage of redundancy. In: Davies, M.N.O. & Green, P.R. (eds) Perception and motor control in birds. Berlin Springer-Verlag: 95-119.

Wiltschko, R. & Wiltschko, W. 1995. Magnetic orientation in animals. Berlin Springer-Verlag: 297pp.

Wiltschko, W. 1978. Further analysis of the magnetic compass of migratory birds. In: Schmidt-Koenig, K. & Keeton, W.T. (eds) Animal migration, navigation, and homing. Berlin Springer-Verlag: 302-310.

Wiltschko, W. 1982. The migratory orientation of Garden Warblers, Sylvia borin. In: Papi, F. & Wallraff, H.G. (Eds) Avian navigation. Berlin Springer-Verlag: 50-58.

Wiltschko, W., Daum, P., & Fergenbauer-Kimmel, A. 1987. The development of the star compass in Garden Warblers, Sylvia borin. Ethology 74:285-292.

Table 1. Types of spatial and temporal variability in the cue information involved in migratory orientation

Table 2. Apparently innate directional information that provides the basis for the development of migratory orientation mechanisms

Table 3. Learning rules underlying the development of migratory orientation mechanisms.


Is the birds' decision to fly away congenital or learned behaviour? - Biology

Training Birds for Husbandry and Medical Behavior to Reduce or Eliminate Stress
By Barbara Heidenreich
First presented at the Association of Avian Veterinarians Conference 2004

Introduction

The history of animal training has evolved tremendously over the past century. What once was considered revolutionary is now expected practice with a variety of animal species in captive situations. Of incredible significance has been the training of animals for basic husbandry needs and medical behaviors. Via the use of operant conditioning with an emphasis on positive reinforcement, animals have been trained to cooperate and/or accept a variety of previously potentially stressful circumstances. Much of the ground breaking work in this field was generated from the marine mammal training community. This has since grown to include primates, elephants, rhinoceros, various hoof stock, bears, large cats and more. However, it is evident that this may be just the beginning of even more training accomplishments to come. There has been a heavy focus on training large mammal species for husbandry and medical behaviors. This is certainly understandable, as previous methods of trying to treat medical conditions or gain cooperation with a large mammal through force, restraint, anesthesia, etc, had the potential to be dangerous and detrimental. As we learn more about the application of operant conditioning with a focus on positive reinforcement and see people and animals benefit from the results, it is a natural progression to see this methodology permeate into other taxa.

Avian species, possibly due to their relatively small size, are still often captured and restrained for husbandry and medical procedures. It is considered standard practice in many cases. It is reasonable to assume that there will always be procedures that will require physical restraint to best serve the health and welfare of the bird. However, as has been demonstrated with large mammals, there is great potential to reduce and/or eliminate the need for the use of restraint to accomplish a variety of husbandry and medical goals. In addition, if restraint is necessary, animals can be conditioned to reduce the potential stress that may accompany restraint procedures. Many bird species respond exceptionally well to positive reinforcement. With an incredible capacity to learn, birds are excellent candidates for husbandry and medical behavior training.

The Value of Training Birds for Husbandry and Medical Behaviors
Training birds using positive reinforcement has been shown to be extremely successful in bird shows. Many people have seen free flighted birds willingly return to a handler/trainer on stage. Usually birds in show situations have also been trained to present a variety of behaviors that facilitate handling and program presentation. These behaviors include stepping up, sitting on a scale, going into travel containers and more. Training these behaviors may involve more hands on contact than is required to meet a specific collection’s training goals. However, examining the training practices of free flight presentations can provide some important insights.

Because a free flighted bird has the option to fly away if the experience is negative, it forces the trainer to learn to be extremely sensitive to bird behavior. A successful trainer will do his or her best to avoid any circumstance that might cause a bird to display fear, nervous or aggressive behavior. In addition, a successful trainer will also provide positive reinforcement as the consequence of the performance of desired behavior. By avoiding aversives and providing positive consequences, birds are more likely to present desired behavior. In addition, these practices can result in a situation in which a bird does not show behavioral (and most likely physiological) signs of stress. This can easily be applied to other training goals and circumstances.

Evidence of reduced stress in husbandry and medical procedures has been demonstrated many times with other animal species. Denver Zoological Gardens measured blood parameters of bongo (Tragelaphus eurycerus) after sedation via a dart or pole syringe. They also measured blood parameters on bongo (T eurycerus) conditioned with positive reinforcement for loading into a crate and a variety of other husbandry and veterinary procedures. Values for these blood parameters, commonly associated with stress, appeared to be lower in crate conditioned animals (Phillips, Grandin, Graffam, Irlbeck and Cambre 1995) By training an animal to cooperate in its own health care, life becomes less stressful for the animal and trainer. (Ramirez, 1999) Some other examples of procedures trained with positive reinforcement include tigers sitting calmly for blood draws, lions allowing their teeth to be brushed, primates presenting their arms for tuberculosis testing, killer whales urinating on cue. Anesthetizing or restraining these animals for procedures seems impractical now. However, this is not yet the case for many birds.

It is not uncommon for birds to be chased in the aviary until exhaustion allows them to be captured. Birds have also been hosed until too wet to fly to facilitate capture. Nets and towels are typical conditioned negative reinforcers to birds that have come to learn these items mean chase and/or restraint. While these methods may be relatively quick and easy for people to use, the effect to the bird may be more detrimental than helpful. Most birds fall into the category of “prey” in the wild. Capture and restraint in the wild usually is a precursor to death. Fight or flight responses most likely are exhibited by birds facing chase, capture and restraint. This can result in elevated corticosterone levels, increased heart rate, rapid breathing, elevated blood pressure and more physiological responses associated in the alarm reaction stage of stress. Some birds, if exposed often enough to capture and restraint, can learn to acquiesce and/or tolerate this practice. However, this occurs after a series of exposures to the stressful process or prolonged exposure to this type of stress. There is considerable research that shows the long term detrimental effects of repeated exposure to uncontrollable aversive events with both animals and people. (Mazur 2002) In one unfortunate incident, an African grey parrot (Psittacus erithacus) was so stressed by procedures utilized for nail and wing trims, the owner requested the bird to be anesthetized. The veterinarian chose not to do so, and as a result the bird expired during the procedure. (Wissman 2003)

Training with positive reinforcement can allow birds to learn to voluntarily participate in husbandry and medical behaviors and potentially avoid the stress associated with capture and restraint. Stress can exasperate an existing medical condition, cause nest or egg abandonment and/or become associated with the individual causing the stress. (Many animals learn to associate veterinarians with negative experiences and show stress responses or aggressive behavior at the sight of the veterinarian) In addition, birds trained with positive reinforcement are more likely to perform the required behaviors more often to earn the reinforcement. This allows more opportunities to monitor birds’ health. Collecting weights, visual and/or tactile exams and other preventative procedures can be much easier to perform. Preventative medicine with birds can be highly effective due to birds’ innate tendency to mask symptoms. Symptoms such as large weight fluctuations can be easily noted and signal caretakers to observe an animal for questionable health. Another interesting phenomenon that can occur from using positive reinforcement training is that sick animals will often still perform behaviors when cued. If a behavior in the past has been positively reinforced, that history of reinforcement may be powerful enough that even though an animal is symptomatic, it will still perform the requested behaviors. Again this can prevent the need to stress an already compromised animal to obtain medical information. Furthermore, as the following examples demonstrate, medical and husbandry behaviors with birds can be trained. Choosing to implement such advances in avian care and management can dramatically effect the quality of care provided to birds and progress aviculture into the future.

Examples of Husbandry Behavior Training
For the purposes of this paper, husbandry behaviors are described as behaviors that facilitate the day to day operation of a facility that manages birds on exhibit and/or in aviaries. These behaviors include, but are not limited to training birds with the use of positive reinforcement to do the following:

Stationing: To stand or sit for a period of time in a designated location.
Targeting: To touch a body part or direct a body part to a specific item (such as a hand, stick, overturned tub, etc.) This can sometimes be similar to stationing. For example if a turkey is trained to target its feet or stand on a rock, it may also be said to be stationing on the rock.
Shifting: To move from one location to another designated location. Typically the subject is prevented from returning to the original location by a physical barrier (such as a door)
A to B: To move from point A to point B.
Crating: To enter into a crate or travel container, allow door to be shut and container to be moved without the bird(s) showing signs of distress.
Recall: To return to a designated area when signaled.

While these behaviors can be useful for a number of different circumstances, they are especially helpful for managing birds that are not handled, display aggressive behaviors, live in large aviaries, and/or live in flock situations. The following examples illustrate the practical application of these husbandry behaviors.

At Disney’s Animal Kingdom Lodge, marabou storks (Leptoptilos crumeniferus) share a large exhibit with a variety of animals. Prior to training, feeding the storks by hand resulted in a keeper being surrounded and harassed by hungry large birds. To address this, the birds were trained to station on overturned rubber tubs. This training resulted in the birds waiting on their stations to be fed and reduced harassment of the keeper.

Also on exhibit at Disney’s Animal Kingdom Lodge are African crowned cranes (Balearica pavonina). The cranes on exhibit were required to shift between the exhibit and nighttime holding enclosures daily. During the shifting process, an imprinted male crane would display aggressive behavior towards the keeper. To reduce the aggression, the bird was trained to station on a series of overturned tubs on its way in or out of its nighttime holding. This gave the bird a place to focus its attention for positive reinforcement, as opposed to presenting aggressive behavior towards the keeper.

At Dallas World Aquarium, two jabiru storks (Jabiru mycteria) would consistently display aggressive behaviors towards keepers that attempted to enter the enclosure. In addition, one stork would drive the other stork away from the food. To remedy this situation, both storks were trained to station on separate wooden discs. This successfully eliminated aggression towards keepers and aggression related to competition for food. It also ensured each bird was receiving adequate food and allowed keepers to better monitor food intake in general for each bird.

At the Houston Zoo, aggressive rhinoceros hornbills (Buceros rhinoceros) were trained to sit or station on a particular perch while the keeper entered the exhibit. Teaching the birds they would be positively reinforced periodically for remaining on the indicated perch reduced aggressive behavior displayed by the birds and allowed the keeper to attend to the exhibit.

Another method to address aggressive behavior is to train an animal to shift from one area to another. This allows an animal caretaker to enter an enclosure without having to interact with an aggressive animal. At Disney’s Discovery Island a small shift cage was built and attached to the larger aviary to address hornbill aggression. The hornbill was then trained to go into the shift cage for its diet and closed in the area.

Training smaller birds in large aviaries for husbandry behaviors may seem to be too great a challenge. However facilities such as Moody Gardens have accomplished this. The Rainforest Pyramid exhibit at Moody Gardens is 10 stories. Sun bittern (Eurypyga helias) and fairy bluebird (Irena puella) have been trained to perform a recall when cued and voluntarily load into crates for transport and periodic weight measurements.

Bell bird (Procnias alba), spangled cotinga (Cotinga amabilis), troupial (Icterus icterus) and green aracari (Pteroglossus viridis) at Dallas World Aquarium also voluntarily load into a small wire cage used to transport birds to different enclosures. This training was completed in anticipation of moving the birds to a new exhibit. Knowing this move was to occur allowed staff the time to incorporate short training sessions daily, well in advance of the actual relocation.

SAIC Biosolutions produces mobile exhibits of 400 birds. These birds include finches (Taeniopygia guttata), cockatiels (Nymphicus hollandicus), budgerigars (Melopsttacus undulates), and rosellas (genus Platycerus). At the Hogle Zoo SAIC Biosolutions exhibit, all 400 birds have been trained to come off exhibit and enter crates. All 400 birds voluntarily load into crates twice a year for veterinary examinations and as needed for travel.

Examples of Medical Behavior Training
For the purposes of this paper, medical behaviors are described as behaviors that involve procedures that monitor or attend to the physical condition or health of the birds. These behaviors include, but are not limited to training birds with positive reinforcement to voluntarily participate in the following:

Sit or stand on a scale
Allow nail filing or trim
Allow trimming of flight feathers
Allow wrapping in a towel
Present foot for exam
Allow general tactile exam
Allow keel and breast muscle to be palpated
Allow preen gland exam
Allow touch with swab
Allow touch with gauze pad of alcohol
Open mouth
Accept medication in liquid delivered with syringe
Allow bandage change
Accept eye drops
Provide fecal on cue
Allow stethoscope exam
Allow body temperature reading
Allow cloacal swab
Inhale medication/anesthesia
Allow radiograph
Allow ultrasound exam
Allow blood draw

Training medical behaviors can be more involved than training husbandry behaviors. In addition many of the examples presented in this paper involve birds that are comfortable with handling. However, some medical behaviors can be accomplished without the need to handle the birds. Creative thought and training most likely will provide impressive progress in the training of medical behaviors in protected contact situations in the future. A few examples of training of medical behaviors without hands on contact will be presented here. The following examples illustrate the practical application of medical behaviors with or without physical contact.

Obtaining a weight on a bird can be a very simple behavior to train. Parrots can be easily trained to step from a hand or perch onto a scale. However, birds not usually handled can also be easily trained to stand on a scale. At Disney’s Animal Kingdom Lodge, the simple behavior of stationing on a tub for cranes and storks was easily modified to standing on a scale. This was done by simply placing a flat scale on top of the tub. This same concept was used to train the jabiru storks (J mycteria) at Dallas World Aquarium to stand on a scale.

Birds on exhibit, held in enclosures, or in aviaries can also learn to stand on a scale. An Andean condor (Vultus gryphus) at the Oregon zoo often preferred to perch by the door to its enclosure. To obtain a weight on this bird, a scale was permanently and securely placed in the enclosure by the door. The condor simply continued to perch in its favorite location. However, this time the perch location had been modified to include the scale. This is also a very effective method for small birds such as finches. Favorite foods or food bowls can be placed to encourage perching on the scale to easily obtain weights on a daily basis.

At Dallas World Aquarium weights are easily obtained on cock of the rock (Rupicola rupicola), bell bird (P alba), spangled cotinga (C amabilis), troupial (I icterus) and green aracari (P viridis) by simply using Velcro to attach a bowl of favorite food items to a scale. The birds land on the bowl and the weight is recorded while the bird eats. This session is usually done just prior to placing the regular diet in the aviary to ensure the birds have an interest in the food items offered.

Training a bird to target to an object can also facilitate obtaining a weight. A bird that learns to follow a specific object, such as a hand, can be lured over a scale. John Ball Zoo used this method to teach a chicken to stand on a simulated scale.

Targeting was utilized to train a sick macaw to inhale medications at Parrots and People, a parrot sanctuary and adoption facility. Sheba, a blue and gold macaw (Ara ararauna), was showing signs of respitory distress. After a trip to Texas A & M University Veterinary Teaching Hospital, the bird was sent home with a prescription for Albutoral, which was to be administered when breathing difficulties were observed. It was recommended to administer the medication by attaching a nebulizer to the spout of container, such as a milk jug, with the bottom cut out. The birds head was to be put into the open bottom end of the container to administer the treatment. The bird, however had never been handled, or separated from it’s mate. Rather than capture and restrain Sheba and potentially further exasperate the problem, the decision was made to train the bird to voluntarily accept the treatment. This was achieved by training the bird to target the end of a stick with its beak. The stick was then inserted through a hole in a container. The stick was gradually pulled into the container to train the bird to put its head farther into the container. Other factors were gradually added to the training sessions. These factors included the nebulizer and a latex covering over the large opening of the container. The latex covering had a slit cut out to allow the bird to insert its head into the container, yet prevent the medication from escaping. Within one week, this bird had learned to voluntarily participate in the treatment. The bird remained in its enclosure during the treatment and handling was not required. In addition, it is possible this behavior can be modified as a way for birds to be trained to voluntarily accept inhaled anesthesia.

Training behaviors that require touching a birds body or introducing unusual objects can be achieved via a process known as conditioning. Positive reinforcement, usually in the form of food, is presented in association with the new circumstance or object. Introducing these new circumstances or objects is done in a manner that does not promote behaviors that indicate fear, nervousness or aggression in the animal. Training birds to accept nail trimming and flight feather clipping are familiar examples of this type of training. However this process can be applied to many medical behavior training goals.

Several parrots at Parrots and People, have been trained to accept various medical behaviors via conditioning. These behaviors include the following: allow nail filing, allow wrapping in a towel, allow foot visual and tactile exam, allow general tactile exam, allow keel and breast muscle to be palpated, allow preen gland exam, allow stethoscope exam. One of the parrots, a Panama Amazon (Ochrocephala panamensis), was trained to allow nail filing, keel palpitation and foot examination while the bird remained in an enclosure. This was to demonstrate how to achieve these behaviors with a parrot that is not comfortable with handling. The bird was trained to target its beak to an object in order to obtain a body position that facilitated the procedures, and then conditioned to accept the medical procedures.

Some other examples of utilizing conditioning to train medical behaviors include the following: Moody Gardens trained parrots to accept being touched with a swab and a gauze pad to facilitate application of medications. Staff also trained parrots to accept liquid oral medications through a syringe. SeaWorld of San Diego used conditioning to treat a chronic bumble foot problem on an African fish eagle (Haliaetus vocifer). Training the bird to accept the application of topical medication and bandage changes allowed the staff to avoid the difficult and stressful task of capturing and restraining the eagle on a daily basis. This bird was also conditioned to accept an intramuscular injection without restraint. Staff at the Taronga Zoo in Australia conditioned an Andean condor (V gryphus) to accept eye drops without the use of restraint. Staff at the Utica Zoo conditioned a hyacinth macaw (Anodorhynchus hyacinthinus) to accept cloacal insertion of a thermometer to monitor this bird’s health. This became especially important when the bird did become ill. Although the bird was symptomatic, a solid positive reinforcement history with this behavior allowed keeper staff to obtain a temperature from this bird without incident.

Dolphin Discovery in Mexico has taken the training of husbandry and medical behaviors to new levels. In addition to the behaviors mentioned above, their collection of ten macaws will voluntarily participate in blood draws and are also being conditioned to accept radiographs and ultrasound examinations. Most of the staff at Dolphin Discovery learned animal training skills by working with marine mammals. By applying the same training skills and structured training program to their bird collection, they achieved unheard of goals in the bird training community. By exploring options outside the constraints of traditional bird care practices, incredible progress can be made in the care and management of avian species.

Developing a Training Program
The previous examples demonstrate training birds for husbandry and medical behaviors can be accomplished. It may be surprising to learn that achieving some of these training goals can be relatively easy.

It is often stated that facilities find it difficult to invest time in training. However, facilities are training all the time. Although it may not be a structured training program, any time a bird is aware and reacts to a caretaker’s action, training is occurring. For example: a frightened bird that flys to the back of an enclosure because a caretaker has picked up a broom, may have learned to associate aversive stimuli with that caretaker. In addition every time the same food bowl is placed in an enclosure, a bird may learn to associate positive reinforcement with that bowl. This can be a highly powerful training tool. An important step towards developing a training program at a facility is to teach staff to be aware of their actions and how it effects bird behavior.

To facilitate efficient use of time, facilities can also keep training sessions short. Sessions can be 5-10 minutes. They can occur whenever birds are being fed. They can also occur several times throughout the day, or just a few times a week. Usually more training sessions in a given time allows training goals to be achieved faster. However, training goals can still be achieved with infrequent sessions over a longer period of time. Sessions can also be relatively passive depending on the desired behavior. For example training birds to go into a crate may be as simple as placing food bowls closer and closer to the crate over a period of days. Facilities with young birds can begin exposing those birds to unfamiliar objects they may encounter later in life. Often young birds are more accepting of new things. Associating items, such as crates, stethoscopes, nail clippers, scissors, etc. with feeding times can help desensitize birds to these objects. Staff can easily turn a feeding session into a training session.

Although training can be easily introduced into a daily routine, the time invested to develop a structured training program has tremendous benefits. Eventually husbandry and medical procedures can be performed quickly, efficiently, and calmly and save time in the long run. Instead of viewing training as an additional luxury to include in daily operations, consider viewing training as essential to the successful operation of a facility. Zoological facilities are beginning to realize not only the benefits to day to day facility operations, but more importantly the benefit to animal health and welfare. Behavior Husbandry programs in zoos are emerging as a requirement for the American Zoo and Aquarium Association (AZA) accreditation. Rather than squeezing in time to train, many zoos are moving towards ensuring staff have time to train and structured training programs are in place.

Any facility or person caring for birds can benefit from training husbandry and medical behaviors. To truly experience these benefits, consider implementing a structured training program. A training program may involve educating staff about behavior modification theory, developing training goals and strategies, implementing training sessions, record keeping, and follow up on progress. While describing the details of developing a structured training program is beyond the scope of this paper, there are resources available to facilitate program development. These include private consultants, organizations such as AZA, The International Association of Avian Trainers and Educators (IAATE), Animal Behavior Management Alliance (ABMA), workshops, literature, websites, listservs, peers, colleagues and more. Please see the resources section of this paper for more specific contact information on these resources.

Conclusion
In the past, the words “bird training” conjured up images of birds on bicycles and roller skates. Today, training is an essential tool we can utilize to provide for the health and welfare of the avian species we steward. It is my hope that the examples presented in this paper will provide inspiration and motivation for bird caretakers to explore ways to reduce stress in husbandry and medical procedures in their avian collections by developing structured training programs. Training has the power to do much more than entertain us. It can facilitate efficient daily operations and improve the quality of life of the creatures that give us so much pleasure. I hope bird training will become a priority in your facility.

Training Credits:
The following people and/or facilities are responsible for the indicated training examples in this paper, accompanying PowerPoint and/or video presentations:

Barbara Heidenreich- Animal Training and Consulting Services www.ATandCS.com and staff members of listed facilities
Parrots and People: www.parrotsandpeople.org
Cockatoo step up onto hand
Macaw step onto scale
Macaw trained to accept inhalant
Conure conditioned to accept towel
Conure conditioned to accept tactile exam (keel, preen gland, feet, wings, vent check, etc)
Conure conditioned to accept stethoscope exam
Conure trained to open mouth
Conure trained to go into a crate
Amazon Parrot conditioned to accept nail filing in protected contact situation
Amazon Parrot conditioned to accept foot examination in protected contact situation
Amazon Parrot conditioned to accept keel and breast muscle palpitation in protected contact situation
Dallas World Aquarium: www.dwazoo.com
Manatee stationing and conditioning for blood draw
Saki Monkey targeting and sit on scale
Jabiru Stork stationing and stand on scale
Cock of the Rock, Bell Bird, Green Aracari, Spangled Cotinga, Troupial stand on scale
Bell Bird, Green Aracari, Spangled Cotinga, Troupial go into transport cage
John Ball Zoo: www.accesskent.com/visiting/zoo/zooindex.htm
Chicken targeting hand to step onto scale

Dr. Renato Lenzi - Dolphin Discovery www.dolphindiscovery.com
Macaws conditioned to accept wing and nail trim
Macaws conditioned to accept tactile exam
Macaws conditioned to accept cloacal swab
Macaws conditioned to accept stethoscope exam
Macaws conditioned to accept blood draw
Macaws conditioned to accept simulated radiograph procedure
Macaws conditioned to accept simulated ultrasound procedure

Peta Clarke -Taronga Zoo www.zoo.nsw.gov.au/index.htm
Condor conditioned to accept eye drops

Cathi Wright -Oregon Zoo www.zooregon.org
Condor stationing on a scale

Matt Schmitt- Houston Zoo http://wild.houstonzoo.org/Public/index.asp
Aggressive Hornbill stationing while keeper enters exhibit

Heather Leeson - Moody Gardens www.moodygardens.org
Conure trained to accept oral medication through a syringe
Cockatoo conditioned to accept swab or gauze pad application
Sun Bittern, Guan, Fairy Bluebird trained to come off exhibit and go into crates

Alison Sinnott- Utica Zoo www.uticazoo.org
Macaw conditioned to accept cloacal thermometer insertion

Jenny Schaefer and Keri Caporale -Seaworld San Diego www.seaworld.com
Fish Eagle conditioned to accept intramuscular injection and bandage change to feet

Bird Keeping Staff - Caldwell Zoo www.caldwellzoo.org
Macaw conditioned to accept wing stretched out
Barn Owl on scale

Animal Care Staff – Disney’s Discovery Island (facility permanently closed)
Hornbill trained to shift to separate holding

Animal Lodge Animal Care Staff - Disney’s Animal Kingdom http://disneyworld.disney.go.com/waltdisneyworld/parksandmore/parkindex?id=TPAnimalKingdomPrk
Storks and cranes trained to station on tubs for feeding, shifting and weighing

Animal Care Staff- John Ball Zoo www.accesskent.com/visiting/zoo/zooindex.htm
Chimps presenting chest for stethoscope exam

Andy Schleis SAIC- Biosolutions www.saic.com/biosolutions
Flock of 400 Finches, Budgerigars, Cockatiels and Rosellas trained to go into crates

Acknowledgements
I would like to thank the following for their support and input in the development of this paper: Parrots and People for the use of their parrots as training subjects (www.parrotsandpeople.org), Dr. Renato Lenzi and his staff at Dolphin Discovery, Peta Clarke and Mathew Kettle at Taronga Zoo, Cathi Wright and Shannon LaMonica at the Oregon Zoo, Matt Schmitt at the Houston Zoo, Heather Leeson and Kat Fowler at Moody Gardens, Jenny Schaefer at Seaworld San Diego, Andy Schleis and Scott Klappenback of SAIC- Biosolutions and Christine Barth of Disney’s Animal Kingdom Lodge.

Bibliography

Barth, C. (2003) Stepping up the Training Process: The Benefits of Stationing East African Crowned Cranes and Marabou Storks. International Association of Avian Trainers and Educators Proceedings. Portland, OR.

Canoine, V., Hayden, T., Rowe, K., Goymann, W. (2002) The Stress Response of European Stonechats Depends on the Type of Stressor. Behaviour 139, 1303-1311.

Caporale, K., Schafer, J. (2003) Focused Behavioral Plan for African Fish Eagles. International Association of Avian Trainers and Educators Proceedings. Portland, OR.

Friedman, S. (2002) Alternatives to Breaking Parrots: Reducing Aggression and Fear through Learning. Stop PDD Virtual Conference: PsittaScene.

Lacinek, T., Scarpuzzi, M., Force, D., & McHugh, M. Sea World’s Husbandry Program Update (1999). Animal Training. Successful Animal Management through Positive Reinforcement. Chicago: Shedd Aquarium. 160-163.

Selye, Hans (1978, 1976) The Stress of Life. New York: McGraw-Hill.

Silervin, B. (1998) Behavioural and Hormonal Responses of the Pied Flycatcher to Environmental Stressors. Animal Behaviour. Volume 55. 1411-1420.

Mazur, J. E. (2002) Learning and Behavior. Prentice Hall.

Phillips, M., Grandin, T., Graffam, W., Irlbeck, N., Cambre, R. (1998)
Crate Conditioning of Bongo (Tragelaphus eurycerus) for Veterinary and Husbandry Procedures at the Denver Zoological Gardens. Zoo Biology, 17, 25-32.

Ramirez, K. (1999) Animal Training. Successful Animal Management through Positive Reinforcement. Chicago: Shedd Aquarium.

Wissman, M. (2003) Causes and Cures: Anesthetizing During Grooming. Bird Talk. January, 2003.


Contents

In the Pacific, traditional landfinding techniques used by Micronesians and Polynesians suggest that bird migration was observed and interpreted for more than 3000 years. In Samoan tradition, for example, Tagaloa sent his daughter Sina to Earth in the form of a bird, Tuli, to find dry land, the word tuli referring specifically to landfinding waders, often to the Pacific golden plover. [1] Bird migrations were recorded in Europe from at least 3,000 years ago by the Ancient Greek writers Hesiod, Homer, Herodotus and Aristotle. The Bible, as in the Book of Job, [2] notes migrations with the inquiry: "Is it by your insight that the hawk hovers, spreads its wings southward?" The author of Jeremiah [3] wrote: "Even the stork in the heavens know its seasons, and the turtle dove, the swift and the crane keep the time of their arrival."

Aristotle recorded that cranes traveled from the steppes of Scythia to marshes at the headwaters of the Nile. Pliny the Elder, in his Historia Naturalis, repeats Aristotle's observations. [4]

Swallow migration versus hibernation Edit

Aristotle, however, suggested that swallows and other birds hibernated. This belief persisted as late as 1878, when Elliott Coues listed the titles of no less than 182 papers dealing with the hibernation of swallows. Even the "highly observant" [5] Gilbert White, in his posthumously published 1789 The Natural History of Selborne, quoted a man's story about swallows being found in a chalk cliff collapse "while he was a schoolboy at Brighthelmstone", though the man denied being an eyewitness. [6] However, he writes that "as to swallows being found in a torpid state during the winter in the Isle of Wight or any part of this country, I never heard any such account worth attending to", [6] and that if early swallows "happen to find frost and snow they immediately withdraw for a time—a circumstance this much more in favour of hiding than migration", since he doubts they would "return for a week or two to warmer latitudes". [7]

It was not until the end of the eighteenth century that migration as an explanation for the winter disappearance of birds from northern climes was accepted. [4] Thomas Bewick's A History of British Birds (Volume 1, 1797) mentions a report from "a very intelligent master of a vessel" who, "between the islands of Menorca and Majorca, saw great numbers of Swallows flying northward", [8] and states the situation in Britain as follows:

Swallows frequently roost at night, after they begin to congregate, by the sides of rivers and pools, from which circumstance it has been erroneously supposed that they retire into the water.

Bewick then describes an experiment which succeeded in keeping swallows alive in Britain for several years, where they remained warm and dry through the winters. He concludes:

These experiments have since been amply confirmed by . M. Natterer, of Vienna . and the result clearly proves, what is in fact now admitted on all hands, that Swallows do not in any material instance differ from other birds in their nature and propensities [for life in the air] but that they leave us when this country can no longer furnish them with a supply of their proper and natural food .

Pfeilstörche Edit

In 1822, a white stork was found in the German state of Mecklenburg with an arrow made from central African hardwood, which provided some of the earliest evidence of long-distance stork migration. [11] [12] [13] This bird was referred to as a Pfeilstorch, German for "Arrow stork". Since then, around 25 Pfeilstörche have been documented.

Migration is the regular seasonal movement, often north and south, undertaken by many species of birds. Bird movements include those made in response to changes in food availability, habitat, or weather. Sometimes, journeys are not termed "true migration" because they are irregular (nomadism, invasions, irruptions) or in only one direction (dispersal, movement of young away from natal area). Migration is marked by its annual seasonality. [14] Non-migratory birds are said to be resident or sedentary. Approximately 1800 of the world's 10,000 bird species are long-distance migrants. [15] [16]

Many bird populations migrate long distances along a flyway. The most common pattern involves flying north in the spring to breed in the temperate or Arctic summer and returning in the autumn to wintering grounds in warmer regions to the south. Of course, in the southern hemisphere the directions are reversed, but there is less land area in the far south to support long-distance migration. [17]

The primary motivation for migration appears to be food for example, some hummingbirds choose not to migrate if fed through the winter. [18] In addition, the longer days of the northern summer provide extended time for breeding birds to feed their young. This helps diurnal birds to produce larger clutches than related non-migratory species that remain in the tropics. As the days shorten in autumn, the birds return to warmer regions where the available food supply varies little with the season. [19]

These advantages offset the high stress, physical exertion costs, and other risks of the migration. Predation can be heightened during migration: Eleonora's falcon Falco eleonorae, which breeds on Mediterranean islands, has a very late breeding season, coordinated with the autumn passage of southbound passerine migrants, which it feeds to its young. A similar strategy is adopted by the greater noctule bat, which preys on nocturnal passerine migrants. [20] [21] [22] The higher concentrations of migrating birds at stopover sites make them prone to parasites and pathogens, which require a heightened immune response. [17]

Within a species not all populations may be migratory this is known as "partial migration". Partial migration is very common in the southern continents in Australia, 44% of non-passerine birds and 32% of passerine species are partially migratory. [23] In some species, the population at higher latitudes tends to be migratory and will often winter at lower latitude. The migrating birds bypass the latitudes where other populations may be sedentary, where suitable wintering habitats may already be occupied. This is an example of leap-frog migration. [24] Many fully migratory species show leap-frog migration (birds that nest at higher latitudes spend the winter at lower latitudes), and many show the alternative, chain migration, where populations 'slide' more evenly north and south without reversing order. [25]

Within a population, it is common for different ages and/or sexes to have different patterns of timing and distance. Female chaffinches Fringilla coelebs in Eastern Fennoscandia migrate earlier in the autumn than males do [26] and the European tits of genera Parus and Cyanistes only migrate their first year. [27]

Most migrations begin with the birds starting off in a broad front. Often, this front narrows into one or more preferred routes termed flyways. These routes typically follow mountain ranges or coastlines, sometimes rivers, and may take advantage of updrafts and other wind patterns or avoid geographical barriers such as large stretches of open water. The specific routes may be genetically programmed or learned to varying degrees. The routes taken on forward and return migration are often different. [17] A common pattern in North America is clockwise migration, where birds flying North tend to be further West, and flying South tend to shift Eastwards.

Many, if not most, birds migrate in flocks. For larger birds, flying in flocks reduces the energy cost. Geese in a V-formation may conserve 12–20% of the energy they would need to fly alone. [28] [29] Red knots Calidris canutus and dunlins Calidris alpina were found in radar studies to fly 5 km/h (3.1 mph) faster in flocks than when they were flying alone. [17]

Birds fly at varying altitudes during migration. An expedition to Mt. Everest found skeletons of northern pintail Anas acuta and black-tailed godwit Limosa limosa at 5,000 m (16,000 ft) on the Khumbu Glacier. [30] Bar-headed geese Anser indicus have been recorded by GPS flying at up to 6,540 metres (21,460 ft) while crossing the Himalayas, at the same time engaging in the highest rates of climb to altitude for any bird. Anecdotal reports of them flying much higher have yet to be corroborated with any direct evidence. [31] Seabirds fly low over water but gain altitude when crossing land, and the reverse pattern is seen in landbirds. [32] [33] However most bird migration is in the range of 150 to 600 m (490 to 1,970 ft). Bird strike aviation records from the United States show most collisions occur below 600 m (2,000 ft) and almost none above 1,800 m (5,900 ft). [34]

Bird migration is not limited to birds that can fly. Most species of penguin (Spheniscidae) migrate by swimming. These routes can cover over 1,000 km (620 mi). Dusky grouse Dendragapus obscurus perform altitudinal migration mostly by walking. Emus Dromaius novaehollandiae in Australia have been observed to undertake long-distance movements on foot during droughts. [17]

During nocturnal migration, many birds give nocturnal flight calls, which are short, contact-type calls. [35] These likely serve to maintain the composition of a migrating flock, and can sometimes encode the gender of a migrating individual, [36] and to avoid collision in the air. [35] Nocturnal migration can be monitored using weather radar data, [37] allowing ornithologists to estimate the number of birds migrating on a given night, and the direction of the migration. [38] Future research includes the automatic detection and identification of nocturnally calling migrant birds. [39]

Nocturnal migrants land in the morning and may feed for a few days before resuming their migration. These birds are referred to as passage migrants in the regions where they occur for a short period between the origin and destination. [40]

Nocturnal migrants minimize depredation, avoid overheating, and can feed during the day. [4] One cost of nocturnal migration is the loss of sleep. Migrants may be able to alter their quality of sleep to compensate for the loss. [41]

The typical image of migration is of northern landbirds, such as swallows (Hirundinidae) and birds of prey, making long flights to the tropics. However, many Holarctic wildfowl and finch (Fringillidae) species winter in the North Temperate Zone, in regions with milder winters than their summer breeding grounds. For example, the pink-footed goose migrates from Iceland to Britain and neighbouring countries, whilst the dark-eyed junco migrates from subarctic and arctic climates to the contiguous United States [42] and the American goldfinch from taiga to wintering grounds extending from the American South northwestward to Western Oregon. [43] Some ducks, such as the garganey Anas querquedula, move completely or partially into the tropics. The European pied flycatcher Ficedula hypoleuca follows this migratory trend, breeding in Asia and Europe and wintering in Africa.

Migration routes and wintering grounds are both genetically and traditionally determined depending on the social system of the species. In long-lived, social species such as white storks (Ciconia ciconia), flocks are often led by the oldest members and young storks learn the route on their first journey. [44] In short-lived species that migrate alone, such as the Eurasian blackcap Sylvia atricapilla or the yellow-billed cuckoo Coccyzus americanus, first-year migrants follow a genetically determined route that is alterable with selective breeding. [45] [46]

Often, the migration route of a long-distance migratory bird doesn't follow a straight line between breeding and wintering grounds. Rather, it could follow a hooked or arched line, with detours around geographical barriers or towards suitable stopover habitat. For most land-birds, such barriers could consist of large water bodies or high mountain ranges, a lack of stopover or feeding sites, or a lack of thermal columns (important for broad-winged birds). [14] Additionally, many migration routes are circuitous due to evolutionary history: the breeding range of Northern wheatears Oenanthe oenanthe has expanded to cover the entire Northern Hemisphere, but the species still migrates up to 14,500 km to reach ancestral wintering grounds in sub-Saharan Africa rather than establish new wintering grounds closer to breeding areas. [47]

The same considerations about barriers and detours that apply to long-distance land-bird migration apply to water birds, but in reverse: a large area of land without bodies of water that offer feeding sites may present a barrier to birds that feeds in coastal waters. Detours avoiding such barriers are observed: for example, brent geese Branta bernicla migrating from the Taymyr Peninsula to the Wadden Sea travel via the White Sea coast and the Baltic Sea rather than directly across the Arctic Ocean and northern Scandinavia. [48]

In waders Edit

A similar situation occurs with waders (called shorebirds in North America). Many species, such as dunlin Calidris alpina [49] and western sandpiper Calidris mauri, [50] undertake long movements from their Arctic breeding grounds to warmer locations in the same hemisphere, but others such as semipalmated sandpiper C. pusilla travel longer distances to the tropics in the Southern Hemisphere. [51]

For some species of waders, migration success depends on the availability of certain key food resources at stopover points along the migration route. This gives the migrants an opportunity to refuel for the next leg of the voyage. Some examples of important stopover locations are the Bay of Fundy and Delaware Bay. [52] [53]

Some bar-tailed godwits Limosa lapponica have the longest known non-stop flight of any migrant, flying 11,000 km from Alaska to their New Zealand non-breeding areas. [54] Prior to migration, 55 percent of their bodyweight is stored as fat to fuel this uninterrupted journey.

In seabirds Edit

Seabird migration is similar in pattern to those of the waders and waterfowl. Some, such as the black guillemot Cepphus grylle and some gulls, are quite sedentary others, such as most terns and auks breeding in the temperate northern hemisphere, move varying distances south in the northern winter. The Arctic tern Sterna paradisaea has the longest-distance migration of any bird, and sees more daylight than any other, moving from its Arctic breeding grounds to the Antarctic non-breeding areas. [55] One Arctic tern, ringed (banded) as a chick on the Farne Islands off the British east coast, reached Melbourne, Australia in just three months from fledging, a sea journey of over 22,000 km (14,000 mi). Many tubenosed birds breed in the southern hemisphere and migrate north in the southern winter. [56]

The most pelagic species, mainly in the 'tubenose' order Procellariiformes, are great wanderers, and the albatrosses of the southern oceans may circle the globe as they ride the "roaring forties" outside the breeding season. The tubenoses spread widely over large areas of open ocean, but congregate when food becomes available. Many are among the longest-distance migrants sooty shearwaters Puffinus griseus nesting on the Falkland Islands migrate 14,000 km (8,700 mi) between the breeding colony and the North Atlantic Ocean off Norway. Some Manx shearwaters Puffinus puffinus do this same journey in reverse. As they are long-lived birds, they may cover enormous distances during their lives one record-breaking Manx shearwater is calculated to have flown 8 million kilometres (5 million miles) during its over-50-year lifespan. [57]

Diurnal migration in large birds using thermals Edit

Some large broad-winged birds rely on thermal columns of rising hot air to enable them to soar. These include many birds of prey such as vultures, eagles, and buzzards, but also storks. These birds migrate in the daytime. Migratory species in these groups have great difficulty crossing large bodies of water, since thermals only form over land, and these birds cannot maintain active flight for long distances. Mediterranean and other seas present a major obstacle to soaring birds, which must cross at the narrowest points. Massive numbers of large raptors and storks pass through areas such as the Strait of Messina, [58] Gibraltar, Falsterbo, and the Bosphorus at migration times. More common species, such as the European honey buzzard Pernis apivorus, can be counted in hundreds of thousands in autumn. Other barriers, such as mountain ranges, can cause funnelling, particularly of large diurnal migrants, as in the Central American migratory bottleneck. The Batumi bottleneck in the Caucasus is one of the heaviest migratory funnels on earth, created when hundreds of thousands of soaring birds avoid flying over the Black Sea surface and across high mountains. [59] Birds of prey such as honey buzzards which migrate using thermals lose only 10 to 20% of their weight during migration, which may explain why they forage less during migration than do smaller birds of prey with more active flight such as falcons, hawks and harriers. [60]

From observing the migration of eleven soaring bird species over the Strait of Gibraltar, species which did not advance their autumn migration dates were those with declining breeding populations in Europe. [61]

Many long-distance migrants appear to be genetically programmed to respond to changing day length. Species that move short distances, however, may not need such a timing mechanism, instead moving in response to local weather conditions. Thus mountain and moorland breeders, such as wallcreeper Tichodroma muraria and white-throated dipper Cinclus cinclus, may move only altitudinally to escape the cold higher ground. Other species such as merlin Falco columbarius and Eurasian skylark Alauda arvensis move further, to the coast or towards the south. Species like the chaffinch are much less migratory in Britain than those of continental Europe, mostly not moving more than 5 km in their lives. [62]

Short-distance passerine migrants have two evolutionary origins. Those that have long-distance migrants in the same family, such as the common chiffchaff Phylloscopus collybita, are species of southern hemisphere origins that have progressively shortened their return migration to stay in the northern hemisphere. [63]

Species that have no long-distance migratory relatives, such as the waxwings Bombycilla, are effectively moving in response to winter weather and the loss of their usual winter food, rather than enhanced breeding opportunities. [64]

In the tropics there is little variation in the length of day throughout the year, and it is always warm enough for a food supply, but altitudinal migration occurs in some tropical birds. There is evidence that this enables the migrants to obtain more of their preferred foods such as fruits. [65]

Altitudinal migration is common on mountains worldwide, such as in the Himalayas and the Andes. [66]

Many bird species arid regions across southern Australia are nomadic they follow water and food supply around the country in an irregular pattern, unrelated to season but related to rainfall. Several years may pass between visits to an area by a particular species. [67]

Sometimes circumstances such as a good breeding season followed by a food source failure the following year lead to irruptions in which large numbers of a species move far beyond the normal range. Bohemian waxwings Bombycilla garrulus well show this unpredictable variation in annual numbers, with five major arrivals in Britain during the nineteenth century, but 18 between the years 1937 and 2000. [64] Red crossbills Loxia curvirostra too are irruptive, with widespread invasions across England noted in 1251, 1593, 1757, and 1791. [68]

Bird migration is primarily, but not entirely, a Northern Hemisphere phenomenon. [69] This is because continental landmasses of the northern hemisphere are almost entirely temperate and subject to winter food shortages driving bird populations south (including the Southern Hemisphere) to overwinter In contrast, among (pelagic) seabirds, species of the Southern Hemisphere are more likely to migrate. This is because there is a large area of ocean in the Southern Hemisphere, and more islands suitable for seabirds to nest. [70]

The control of migration, its timing and response are genetically controlled and appear to be a primitive trait that is present even in non-migratory species of birds. The ability to navigate and orient themselves during migration is a much more complex phenomenon that may include both endogenous programs as well as learning. [71] [72]

Timing Edit

The primary physiological cue for migration is the changes in the day length. These changes are related to hormonal changes in the birds. In the period before migration, many birds display higher activity or Zugunruhe (German: migratory restlessness), first described by Johann Friedrich Naumann in 1795, as well as physiological changes such as increased fat deposition. The occurrence of Zugunruhe even in cage-raised birds with no environmental cues (e.g. shortening of day and falling temperature) has pointed to the role of circannual endogenous programs in controlling bird migrations. [73] Caged birds display a preferential flight direction that corresponds with the migratory direction they would take in nature, changing their preferential direction at roughly the same time their wild conspecifics change course. [74]

In polygynous species with considerable sexual dimorphism, males tend to return earlier to the breeding sites than their females. This is termed protandry. [75] [76]

Orientation and navigation Edit

Navigation is based on a variety of senses. Many birds have been shown to use a sun compass. Using the sun for direction involves the need for making compensation based on the time. Navigation has been shown to be based on a combination of other abilities including the ability to detect magnetic fields (magnetoreception), use visual landmarks as well as olfactory cues. [77]

Long-distance migrants are believed to disperse as young birds and form attachments to potential breeding sites and to favourite wintering sites. Once the site attachment is made they show high site-fidelity, visiting the same wintering sites year after year. [78]

The ability of birds to navigate during migrations cannot be fully explained by endogenous programming, even with the help of responses to environmental cues. The ability to successfully perform long-distance migrations can probably only be fully explained with an accounting for the cognitive ability of the birds to recognize habitats and form mental maps. Satellite tracking of day migrating raptors such as ospreys and honey buzzards has shown that older individuals are better at making corrections for wind drift. [79] Birds rely for navigation on a combination of innate biological senses and experience, as with the two electromagnetic tools that they use. A young bird on its first migration flies in the correct direction according to the Earth's magnetic field, but does not know how far the journey will be. It does this through a radical pair mechanism whereby chemical reactions in special photo pigments sensitive to short wavelengths are affected by the field. Although this only works during daylight hours, it does not use the position of the sun in any way. At this stage the bird is in the position of a Boy Scout with a compass but no map, until it grows accustomed to the journey and can put its other capabilities to use. With experience it learns various landmarks and this "mapping" is done by magnetites in the trigeminal system, which tell the bird how strong the field is. Because birds migrate between northern and southern regions, the magnetic field strengths at different latitudes let it interpret the radical pair mechanism more accurately and let it know when it has reached its destination. [80] There is a neural connection between the eye and "Cluster N", the part of the forebrain that is active during migrational orientation, suggesting that birds may actually be able to see the magnetic field of the earth. [81] [82]

Vagrancy Edit

Migrating birds can lose their way and appear outside their normal ranges. This can be due to flying past their destinations as in the "spring overshoot" in which birds returning to their breeding areas overshoot and end up further north than intended. Certain areas, because of their location, have become famous as watchpoints for such birds. Examples are the Point Pelee National Park in Canada, and Spurn in England.

Reverse migration, where the genetic programming of young birds fails to work properly, can lead to rarities turning up as vagrants thousands of kilometres out of range. [83]

Drift migration of birds blown off course by the wind can result in "falls" of large numbers of migrants at coastal sites. [84]

A related phenomenon called "abmigration" involves birds from one region joining similar birds from a different breeding region in the common winter grounds and then migrating back along with the new population. This is especially common in some waterfowl, which shift from one flyway to another. [85]

Migration conditioning Edit

It has been possible to teach a migration route to a flock of birds, for example in re-introduction schemes. After a trial with Canada geese Branta canadensis, microlight aircraft were used in the US to teach safe migration routes to reintroduced whooping cranes Grus americana. [86] [87]

Birds need to alter their metabolism to meet the demands of migration. The storage of energy through the accumulation of fat and the control of sleep in nocturnal migrants require special physiological adaptations. In addition, the feathers of a bird suffer from wear-and-tear and require to be moulted. The timing of this moult – usually once a year but sometimes twice – varies with some species moulting prior to moving to their winter grounds and others molting prior to returning to their breeding grounds. [88] [89] Apart from physiological adaptations, migration sometimes requires behavioural changes such as flying in flocks to reduce the energy used in migration or the risk of predation. [90]

Migration in birds is highly labile and is believed to have developed independently in many avian lineages. [91] While it is agreed that the behavioral and physiological adaptations necessary for migration are under genetic control, some authors have argued that no genetic change is necessary for migratory behavior to develop in a sedentary species because the genetic framework for migratory behavior exists in nearly all avian lineages. [92] This explains the rapid appearance of migratory behavior after the most recent glacial maximum. [93]

Theoretical analyses show that detours that increase flight distance by up to 20% will often be adaptive on aerodynamic grounds – a bird that loads itself with food to cross a long barrier flies less efficiently. However some species show circuitous migratory routes that reflect historical range expansions and are far from optimal in ecological terms. An example is the migration of continental populations of Swainson's thrush Catharus ustulatus, which fly far east across North America before turning south via Florida to reach northern South America this route is believed to be the consequence of a range expansion that occurred about 10,000 years ago. Detours may also be caused by differential wind conditions, predation risk, or other factors. [94]

Climate change Edit

Large scale climatic changes are expected to have an effect on the timing of migration. Studies have shown a variety of effects including timing changes in migration, [95] breeding [96] as well as population declines. [97] [98] Many species have been expanding their range as a likely consequence of climate change. This is sometimes in the form of former vagrants becoming established or regular migrants. [99]

The migration of birds also aids the movement of other species, including those of ectoparasites such as ticks and lice, [100] which in turn may carry micro-organisms including those of concern to human health. Due to the global spread of avian influenza, bird migration has been studied as a possible mechanism of disease transmission, but it has been found not to present a special risk import of pet and domestic birds is a greater threat. [101] Some viruses that are maintained in birds without lethal effects, such as the West Nile virus may however be spread by migrating birds. [102] Birds may also have a role in the dispersal of propagules of plants and plankton. [103] [104]

Some predators take advantage of the concentration of birds during migration. Greater noctule bats feed on nocturnal migrating passerines. [21] Some birds of prey specialize on migrating waders. [105]

Early studies on the timing of migration began in 1749 in Finland, with Johannes Leche of Turku collecting the dates of arrivals of spring migrants. [106]

Bird migration routes have been studied by a variety of techniques including the oldest, marking. Swans have been marked with a nick on the beak since about 1560 in England. Scientific ringing was pioneered by Hans Christian Cornelius Mortensen in 1899. [107] Other techniques include radar [108] and satellite tracking. [109] The rate of bird migration over the Alps (up to a height of 150 m) was found to be highly comparable between fixed-beam radar measurements and visual bird counts, highlighting the potential use of this technique as an objective way of quantifying bird migration. [110]

Stable isotopes of hydrogen, oxygen, carbon, nitrogen, and sulphur can establish avian migratory connectivity between wintering sites and breeding grounds. Stable isotopic methods to establish migratory linkage rely on spatial isotopic differences in bird diet that are incorporated into inert tissues like feathers, or into growing tissues such as claws and muscle or blood. [111] [112]

An approach to identify migration intensity makes use of upward pointing microphones to record the nocturnal contact calls of flocks flying overhead. These are then analyzed in a laboratory to measure time, frequency and species. [113]

An older technique developed by George Lowery and others to quantify migration involves observing the face of the full moon with a telescope and counting the silhouettes of flocks of birds as they fly at night. [114] [115]

Orientation behaviour studies have been traditionally carried out using variants of a setup known as the Emlen funnel, which consists of a circular cage with the top covered by glass or wire-screen so that either the sky is visible or the setup is placed in a planetarium or with other controls on environmental cues. The orientation behaviour of the bird inside the cage is studied quantitatively using the distribution of marks that the bird leaves on the walls of the cage. [116] Other approaches used in pigeon homing studies make use of the direction in which the bird vanishes on the horizon. [117]

Human activities have threatened many migratory bird species. The distances involved in bird migration mean that they often cross political boundaries of countries and conservation measures require international cooperation. Several international treaties have been signed to protect migratory species including the Migratory Bird Treaty Act of 1918 of the US. [118] and the African-Eurasian Migratory Waterbird Agreement [119]

The concentration of birds during migration can put species at risk. Some spectacular migrants have already gone extinct during the passenger pigeon's (Ectopistes migratorius) migration the enormous flocks were a mile (1.6 km) wide, darkening the sky and 300 miles (480 km) long, taking several days to pass. [120]

Hunting along migration routes threatens some bird species. The populations of Siberian cranes (Leucogeranus leucogeranus) that wintered in India declined due to hunting along the route, particularly in Afghanistan and Central Asia. Birds were last seen in their favourite wintering grounds in Keoladeo National Park in 2002. [121] Structures such as power lines, wind farms and offshore oil-rigs have also been known to affect migratory birds. [122] Other migration hazards include pollution, storms, wildfires, and habitat destruction along migration routes, denying migrants food at stopover points. [123] For example, in the East Asian–Australasian Flyway, up to 65% of key intertidal habitat at the Yellow Sea migration bottleneck has been destroyed since the 1950s. [124] [125]

Other significant areas include stop-over sites between the wintering and breeding territories. [126] A capture-recapture study of passerine migrants with high fidelity for breeding and wintering sites did not show similar strict association with stop-over sites. [127] Unfortunately, many historic stopover sites have been destroyed or drastically reduced due to human agricultural development, leading to an increased risk of bird extinction, especially in the face of climate change. [128]

Stopover site conservation efforts Edit

California's Central Valley was once a massive stopover site for birds traveling along the Pacific Flyway, before being converted into agricultural land. [128] 90% of North America’s shorebirds utilize this migration path and the destruction of rest stops has had detrimental impacts on bird populations, as they cannot get adequate rest and food and can be unable to complete their migration. [128] As a solution, conservationists and farmers in the United States are now working together to help provide stopover habitats for migrating birds. [129] In the winter, when many of these birds are migrating, farmers are now flooding their fields in order to provide temporary wetlands for birds to rest and feed before continuing their journey. [130] Rice is a major crop produced along this flyway, and flooded rice paddies have shown to be important areas for at least 169 different bird species. [131] For example, in California, legislation changes have made it illegal for farmers to burn excess rice straw, so instead they have begun flooding their fields during the winter. [132] Similar practices are now taking place across the nation, with the Mississippi Alluvial Valley being a primary area of interest due to its agricultural use and its importance for migration. [133]

Plant debris provides food sources for the birds while the newly formed wetland serves as a habitat for bird prey species such as bugs and other invertebrates. [132] In turn, bird foraging assists in breaking down plant matter and droppings then help to fertilize the field helping the farmers, and in turn significantly decreasing their need for artificial fertilizers by at least 13%. [133] [132] Recent studies have shown that the implementation of these temporary wetlands has had significant positive impacts on bird populations, such as the White‐fronted Goose, as well as various species of wading birds. [134] [129] The artificial nature of these temporary wetlands also greatly reduces the threat of predation from other wild animals. [130] This practice requires extremely low investment on behalf of the farmers, and researchers believe that mutually beneficial approaches such as this are key to wildlife conservation moving forward. [132] [133] Economic incentives are key to getting more farmers to participate in this practice. [135] However, issues can arise if bird populations are too high with their large amounts of droppings decreasing water quality and potentially leading to eutrophication. [136] Increasing participation in this practice would allow migratory birds to spread out and rest on a wider variety of locations, decreasing the negative impacts of having too many birds congregated in a small area. [136] Using this practice in areas with close proximity to natural wetlands could also greatly increase their positive impact. [137]


How Do Young Birds Know When To Leave The Nest?

Adult gray-headed junco (Junco hyemalis caniceps) enticing one of its youngsters to leave the nest. . [+] Parents hold food away from nest and tempt the young come out to get it. This picture captures a young bird that was just fed outside of the nest. (Credit: T. E. Martin, doi:10.1126/sciadv.aar1988)

Major life changes can be dangerous, even fatal. Probably the most dangerous life transition is when young animals, such as fledgling birds, begin to move about on their own and to make their own decisions. Predictably, when baby birds -- nestlings -- transition from dependency to their new life as fledglings living outside of the nest, their first few weeks of exploring the landscape and learning to fly are fraught with extraordinary dangers.

When nestlings leave the nest too early, they fly poorly, or not at all, because their wings are small and underdeveloped. Fledging too early is usually a fatal decision: it is in a nestling’s best interests to remain in its nest for as long as possible to allow its wings the time necessary to develop more fully.

But remaining in the nest for “too long” is tremendously dangerous for many bird species because predators are always searching their territories for something to eat, and upon discovering an occupied nest, a predator usually kills all the nestlings in one go. Since bird nests are stationary objects, it’s simply a matter of time -- sometimes just hours or even minutes -- before a nest filled with chicks on the verge of transitioning to fledglings is discovered and transformed into lunch. This is especially true for birds that build open-cup nests on or near the ground.

A young gray-headed junco (Junco hyemalis caniceps) is captured leaving the nest, with its sibling . [+] still in the nest in the background, illustrating the under-developed nature of wings when this species leaves the nest. (Credit: T. E. Martin, doi:10.1126/sciadv.aar1988)

Predictably, predation plays an important role in driving the evolution of optimal fledging times for birds. Songbirds that experience higher daily rates of predation -- species like towhees and juncos that build open-cup nests on the ground or in low bushes -- have evolved younger ages of fledging to deal with this pressure. In contrast, this pressure to fledge early is relaxed for birds that enjoy a relatively low risk of nest predation -- as seen in cavity-nesting birds, like chickadees and bluebirds.

Cavity-nesting birds, like this mountain chickadee (Poecile gambeli), about to feed its young, have . [+] safer nests that allow young to stay in nests longer and develop their wings for improved flight at leaving. (Credit: T. E. Martin, doi:10.1126/sciadv.aar1988)

“Predation pressure has a huge influence on the capacity of birds to fly,” said Bret Tobalske, a professor who works at the intersection of biology and physics to study animal locomotion at the University of Montana, and Director of the Field Research Station at Fort Missoula. Professor Tobalske was a co-author of the recently published study. “Our study shows this for the developmental phase from nestling to fledgling.”

For example, some species of songbirds lose only 12% of their young, mostly to predators, in the first 3 weeks after they leave the nest, whereas other species lose as many as 70% (for example ref and ref). This is typical: similarly high or highly variable mortality rates due to predation in the first weeks of juvenile life are common across a wide variety of other animal species, too (ref).

A research team, headed by avian ecologist Thomas Martin, Assistant Unit Leader and Senior Scientist in the Montana Cooperative Wildlife Research Unit at the University of Montana, investigated how predation influences the transition from nestling to fledgling in different species of songbirds. These songbirds included species that build open-cup nests either on the ground, low down in bushes or higher up in trees, as well as species that nest in cavities. Dr. Martin and his colleagues measured nest predation rates, wing growth rates, fledging ages and they used high-speed videography to record and examine flight performances of newly fledged birds of 11 songbird species to see if this may explain differences in their fledgling mortality rates.

As expected, Dr. Martin and his collaborators found that songbird species with higher nest predation rates produced fledglings that left their nests earlier, and they had smaller, more underdeveloped wings, and poorer flight abilities.

Dr. Martin and his collaborators tested the effect of older fledging age on survival -- what would happen if the researchers delayed fledging time? To do this, they built a small enclosure around the nests of gray-headed juncos, Junco hyemalis, a species that builds open-cup nests on or near the ground, to delay fledging for three days, whilst leaving other junco nests unprotected to serve as experimental controls. The enclosures were high enough to keep predators out, but had an open top to allow the parents access to feed their nestlings.

They found that all young juncos had nearly identical masses (Figure 6A) regardless of experimental treatment, but the wing lengths of the delayed fledging juncos were substantially longer (Figure 6A and B) than controls, as expected. Further -- and most important -- the scientists found that mortality decreased for individual junco fledglings as their wing lengths increased (Figure 6C and D).

Fig. 6. Wing length and mass with respect to fledgling mortality rates. (A) Mass and wing length as . [+] a proportion of adult size in control versus experimentally enclosed nests for gray-headed junco. Control nests fledged at normal age (11 to 12 days), whereas enclosed nests prevented young from leaving for 3 days after fledging naturally to create a delayed fledge age. (B) Photos of typical wings of junco young from control versus experimentally delayed nests on fledging day versus release day, respectively. (C) Daily mortality rate (±1 SE) decreased among fledglings with increasing wing length at fledging in juncos. (D) Mortality rate of junco fledglings for the first week after fledging in nests where fledge age was experimentally delayed had substantially lower mortality rate than fledglings from control (normal fledge age) nests and comparable to other species based on wing length. (E) Daily mortality rate of fledglings and nestlings when based on estimates per offspring versus per brood across eight species. The line represents equal fledgling and nestling mortality rates. (F) Nest predation influences evolution of fledging age and growth rates of offspring with consequences for relative development when young fledge, which thereby influences locomotor performance and fledgling mortality. Fledgling mortality, in turn, feeds back to further influence evolution of the age of fledging and traits that affect performance and mortality, but parents and offspring conflict on the optimal fledging age. (doi:10.1126/sciadv.aar1988)

It is predicted that natural selection should favor fledging at a time when mortality for remaining in the nest is the same as mortality for leaving the nest, but this is not what Dr. Martin and his collaborators found. Instead, they found that daily mortality is higher for junco fledglings (orange balls above the line for equal mortality rate in Figure 6E) than for junco nestlings. Whilst it is true that when nestling juncos leave later, the risk of nest predation increases, but delayed leaving allows greater wing development and thus, reduces overall individual fledgling mortality. This indicates that junco nestlings are leaving the nest sooner than they should.

“Songbird species differ in rates of mortality of young after leaving the nest due to differences in their relative stage of development caused by risk of predation in the nest,” Dr. Martin elaborated in email. “But the age of leaving is a compromise between offspring and parents, where parents want young to leave earlier than young want.”

“It fits into a broader pattern [that] predation pressure has been (and continues to be) a major driver of the evolution of flight,” Dr. Tobalske said in email.

Thomas E. Martin, Bret Tobalske, Margaret M. Riordan, Samuel B. Case, and Kenneth P. Dial (2018). Age and performance at fledging are a cause and consequence of juvenile mortality between life stages, Science Advances, 4(6):eaar1988, published online on 20 June 2018 ahead of print | doi:10.1126/sciadv.aar1988

Susan M. Smith (1967). Seasonal changes in the survival of the Black-capped Chickadee, The Condor, 69(4):344-359 | doi:10.2307/1366198

Kimberley A. Sullivan (1989). Predation and Starvation: Age-Specific Mortality in Juvenile Juncos (Junco phaenotus), Journal of Animal Ecology, 58(1):275-286 | doi:10.2307/5000


Birds orient their heads appropriately in response to functionally referential alarm calls of heterospecifics

Australian magpies obtain information on predator type from noisy miner alarm calls.

Magpie head orientation was higher in response to miner aerial than mobbing calls.

Magpies were vigilant for longer after aerial calls that followed mobbing calls.

Individuals can gain detailed information from heterospecific alarm calls.

Vertebrate alarm calls signal danger and often encode graded or categorical information about predator proximity or type. In addition to allowing communication with conspecifics, alarm calls are a valuable source of information for eavesdropping heterospecifics. However, although eavesdropping has been experimentally demonstrated in over 70 species, we know little about exactly what information eavesdroppers gain from heterospecific alarm calls. Here, we investigated whether Australian magpies, Cracticus tibicen, extract relevant information about the type of threat from functionally referential alarm calls given by noisy miners, Manorina melanocephala. Miner aerial alarm calls signal a predator in flight, whereas mobbing calls signal a terrestrial or perched predator. We therefore tested whether magpies gain information on the elevation of expected danger. We first confirmed, by measuring bill angles on video, that magpie head orientation changes appropriately with differences in the elevation of a conspicuous moving object. We then conducted a field experiment that measured magpie bill angle in response to playback of miner aerial and mobbing alarm calls. The maximum and mean bill angles were higher in response to aerial than to mobbing calls, suggesting that magpies use information from miner alarms to search visually at appropriate elevations for the specific type of danger. Magpies were also vigilant for longer after aerial alarm calls that followed mobbing calls, implying perception of an escalating threat level. Our work shows that individuals can gain information on the type or location of danger from heterospecific alarm calls, which is likely to increase the effectiveness of antipredator responses.


Contents

The ability to perform an effective escape maneuver directly affects the fitness of the animal, because the ability to evade predation enhances an animal’s chance of survival. [3] [6] Those animals that learn to or are simply able to avoid predators have contributed to the wide variety of escape responses seen today. Animals that are able to adapt their responses in ways different from their own species have displayed increased rates of survival. [7] Because of this, it is common for the individual escape response of an animal to vary according to reaction time, environmental conditions, and/or past and present experience. [7]

Arjun et al. (2017) found that it is not necessarily the speed of the response itself, but the greater distance between the targeted individual and the predator when the response is executed. [8] In addition, the escape response of an individual is directly related to the threat of the predator. Predators that pose the biggest risk to the population will evoke the greatest escape response. Therefore, it may be an adaptive trait selected for by natural selection.

Law & Blake (1996) argue that many morphological characteristics could contribute to an individual's efficient escape response, but the escape response has undoubtedly been molded by evolution. In their study, they compared more recent sticklebacks to their ancestral form, the Paxton Lake stickleback, and found that the performance of the ancestral form was significantly lower. [9] Therefore, one may conclude that this response has been ripened by evolution.

How the escape responses are initiated neurologically, and how the movements are coordinated is dependent on the species. The behaviors alone vary widely, so, in a similar manner, the neurobiology of the response can be highly variable between species. [10]

‘Simple’ escape responses are commonly reflex movements that will quickly move the animal away from the potential threat. [3] These neural circuits operate quickly and effectively, rapidly taking in sensory stimuli and initiating the escape behavior through well-defined neuron systems. [11]

Complex escape responses often require a mixture of cognitive processes. This may stem from a difficult environment to escape from, or the animal having multiple potential escape methods. Initially, the animal must recognize the threat of predation, but following the initial recognition the animal might have to quickly determine the best route of escape, based on prior experience. [12] This means rapid integration of incoming information with prior knowledge, and then coordination of motor movements deemed necessary. Complex escape responses generally require a more robust neural network. [3]

Researchers will often evoke an escape response to test the potency of hormones and/or medication and their relationship to stress. As such, the escape response is fundamental to anatomical and pharmacological research. [13]

Habituation Edit

A series of initially threatening encounters that do not lead to any true adverse outcomes for the animal can drive the development of habituation. [3] Habituation is an adaptation strategy that refers to the diminishing response of an animal to a stimulus following repetitive exposures of the animal to that same stimulus. [14] In other words, the animal learns to distinguish between innately threatening situations and may choose to not go through with their escape response. This is a highly variable phenomenon, where the stimulus itself is highly specific, and the experience is highly context dependent. [15] [16] This suggests that there is no one mechanism by which a species will develop habituation to a stimulus, instead habituation may arise from the integration of experiences. [3] A number of cognitive processes may operate during one single threatening experience, but the levels at which these processes are integrated will determine how the individual animal will potentially respond next. [17]

Caenorhabditis elegans, commonly identified as nematodes, have been used as a model species for studies observing their characteristic “tap-withdrawal response”. [18] The tapping on serves as the fear-provoking, mechanical stimulus which C. elegans worms will move away from. If the tapping stimulus continues without any direct effects on the worms, they will gradually stop responding to the stimulus. This response is modulated by a series of mechanosensory neurons (AVM, ALM, PVD, and PLM) which synapse with interneurons (AVD, AVA, AVB, and PVC) transmitting the signal to motor neurons that cause the back-and-forth movements. Habituation to the tapping reduces activity of the initial mechanosensory neurons, seen as decrease in calcium channel activity and neurotransmitter release. [18]

The primary force driving escape habituation is suspected to be energy conservation. [3] If an animal learns that a certain threat will not actively cause harm to it, then the animal can choose to minimize its energy costs by not performing its escape. [19] For example, Zebra danios, also known as Zebrafish, who are habituated to predators are more latent to flee than those who were not habituated to predators. [20] However, habituation did not affect the fish's angle of escape from the predator. [20]

Learned Helplessness Edit

If an animal cannot react via a startle or avoidance response, they will develop learned helplessness as a result of receiving or perceiving repeated threatening stimuli and believing the stimuli is unavoidable. [21] The animal will submit and not react, even if the stimuli previously triggered instinctual responses or if the animal is provided an escape opportunity. In these situations, escape responses are not used because the animal has almost forgotten their innate response systems. [22]

Helplessness is learned through habituation, because the brain is programmed to believe control is not present. In essence, animals operate under the assumption they have the free will to fight, flee or freeze as well as engage in other behaviors. When escape responses fail, they develop helplessness.

A common, theoretical example of learned helplessness is an elephant, trained by humans who condition the elephant to believe it cannot escape punishment. As a young elephant, it would be chained down with a pick to keep it from leaving. As it grows, the elephant would have the ability to easily overpower the tiny pick. Development of learned helplessness keeps the elephant from doing so, believing that it is trapped and the effort is futile.

In a more natural setting, learned helplessness would most often be displayed by animals that live in group settings. If food were scarce and one individual was always overpowered when it came time to get food, it would soon believe that no matter what it did, getting food would be impossible. It would have to find food on its own or submit to the idea it will not eat.

Startle response is an unconscious response to sudden or threatening stimuli. In the wild, common examples would be sharp noises or quick movements. Because these stimuli are so harsh they are connected to a negative effect. This reflex causes a change in body posture, emotional state, or a mental shift to prepare for a specific motor task. [23]

A common example would be cats and how, when startled, their arrector pili muscles contract, making the hair stand up and increase their apparent size. Another example would be excessive blinking due to the contraction of the orbicularis oculi muscle when an object is rapidly moving toward an animal this is often seen in humans.

Halichoerus grypus, or Grey seals, respond to acoustic startle stimuli by fleeing from the noise. The acoustic startle reflex is only activated when the noise is over eighty decibels, which promotes stress and anxiety responses that encourage flight. [24]

Flight Zone Edit

Flight zone and flight distance are interchangeable and refer to the distance needed to keep an animal under the threshold that would trigger a startle response.

A flight zone can be circumstantial, because a threat can vary in size (individually or in group number). Overall, this distance is the measure of an animal's willingness to take on risks. This differentiates a flight zone from personal distance an animal prefers and social distance (how close other species are willing to be). [25]

An applicable analogy would be a reactive dog. When the flight zone is large, the dog will maintain an observant stance, but a startle response will not occur. As the threatening stimuli moves forward and decreases the flight zone, the dog will exhibit behaviors that fall into a startle or avoidance response. [25]

The avoidance response is a form of negative reinforcement which is learned through operant conditioning. This response is usually beneficial, as it reduces risk of injury or death for animals, also because it is an adaptive response and can change as the species evolves. Individuals are able to recognize certain species or environments that need to be avoided, which can allow them to increase the flight distance to ensure safety.

When scared, octopus release ink to distract their predators enough that they can burrow into a safe area. Another example of avoidance is the fast-start response in fish. They are able to relegate musculoskeletal control which allows them to withdraw from the environment with the threatening stimuli. [26] It is believed that the neural circuits have adapted over time to more quickly react to a stimulus. Interestingly, fish that keep to the same groups will be more reactive than those who are not.

In birds Edit

Avian species also display unique escape responses. Birds are uniquely vulnerable to human interference in the form of aircraft, drones, cars, and other technology. [27] [28] There has been a lot of interest in how these structures will and do affect the behaviors of terrestrial and aquatic birds.

One study, Weston et. al., 2020, observed how flight initiation changed according to the distance of the drone from the birds. It was found that as the drone approached the tendency of birds to take flight to escape it increased dramatically. This was positively affected by the altitude at which the birds were exposed to the drone. [28] In another experiment by Devault et al. (1989), brown-headed cowbirds (Molothrus ater) were exposed to a demonstration of traffic traveling at speeds between 60 – 360 km/hr. When approached by a vehicle travelling at 120 km/h, the birds only allotted 0.8s to escape before a possible collision. [27] This study showed that fast traffic speeds may not allow enough time for birds to initiate an escape response.

In fish Edit

In fish and amphibians, the escape response appears to be elicited by Mauthner cells, two giant neurons located in the rhombomere 4 of the hindbrain. [29]

Generally, when faced with a dangerous stimuli, fish will contract their axial muscle, resulting a C-shaped contraction away from the stimulus. [30] This response occurs in two separate stages: a muscle contraction that allows them to speed away from a stimulus (stage 1), and a sequential contralateral movement (stage 2). [30] This escape is also known as a "fast-start response". [31] The majority of the fish respond to an external stimulus (pressure changes) within 5 to 15 milliseconds, while some will exhibit a slower response taking up to 80 milliseconds. [32] While the escape response generally only propels the fish a small distance away, this distance is long enough to prevent predation. While many predators use water pressure to catch their prey, this short distance prevents them from feeding on the fish via suction. [33]

Particularly in the case of fish, it has been hypothesized that the differences in escape response are due to the evolution of neural circuits over time. This can be witnessed by observing the difference in the extent of stage 1 behaviour, and the distinct muscle activity in stage 2 of the C-start or fast-start response. [26]

In larval zebrafish (Danio rerio), they sense predators using their lateral line system. [33] When larvae are positioned lateral to a predator, they will escape in a likewise lateral direction. [33] According to game theory, zebrafish who are positioned lateral and ventral to the predator are more likely to survive, rather than any alternate strategy. [33] Finally, the faster (cm/s) the predator is moving, the faster downward the fish will move to escape predation. [33]

Recent research in guppies has shown that familiarity can affect the reaction time involved in the escape response. [31] Guppies that were placed in familiar groups were more likely to respond than guppies who were assigned to unfamiliar groups. Wolcott et al. (2017) suggest that familiar groups may lead to reduced inspection and aggression among conspecifics. The theory of limited attention states that the brain has a limited amount of information processing, and, as an individual is engaged in more tasks, the less resources it can provide to one given task. [34] As a result, they have more attention that they can devote toward anti-predator behaviour.

In insects Edit

When house flies (Musca domestica) encounter an aversive stimulus, they jump rapidly and fly away from the stimulus. A recent research suggests that the escape response in Musca domestica is controlled by a pair of compound eyes, rather than by the ocelli. When one of the compound eyes was covered, the minimum threshold to elicit an escape response increased. In short, the escape reaction of Musca domestica is evoked by the combination of both motion and light. [35]

Cockroaches are also well known for their escape response. When individuals sense a wind puff, they will turn and escape in the opposite direction. [36] The sensory neurons in the paired caudal cerci (singular: cercus) at the rear of the animal send a message along the ventral nerve cord. Then, one of two responses are elicited: running (through the ventral giant interneurons) or flying/running (through the dorsal giant interneurons). [37]

In mammals Edit

Mammals can display a wide range of escape responses. Some of the most common escape responses include withdrawal reflexes, fleeing, and, in some instances where outright escape is too difficult, freezing behaviors.

Higher-order mammals often display withdrawal reflexes. [38] Exposure to danger, or a painful stimulus (in nociceptor-mediated loops), initiate a spinal reflex loop. Sensory receptors transmit the signal to the spine where it is rapidly integrated by interneurons and consequently an efferent signal is sent down motor neurons. The effect of the motor neurons is to contract the muscles necessary to pull the body, or body part away from the stimulus. [39]

Some mammals, like squirrels and other rodents, have defensive neural networks present in the midbrain that allow for quick adaptation of their defense strategy. [40] If these animals are caught in an area without refuge, they can quickly change their strategy from fleeing to freezing. [41] Freezing behavior allows for the animal to avoid detection by the predator. [3]

In one study, Stankowich & Coss (2007) studied the flight initiation distance of Columbian black-tailed deer. According to the authors, the flight initiation distance is the distance between prey and predator when the prey attempts an escape response. [42] They found that the angle, distance, and speed that the deer escaped was related to the distance between the deer and its predator, a human male in this experiment. [42]

Other examples Edit

Squids have developed a multitude of anti-predator escape responses, including: jet-driven escape, postural displays, inking and camouflage. [1] Inking and jet-driven escape are arguably the most salient responses, in which the individual squirts ink at the predator as it speeds away. These blobs of ink can vary in size and shape larger blobs can distract the predator while smaller blobs can provide a cover under which the squid can disappear. [43] Finally, the released ink also contains hormones such as L-dopa and dopamine that can warn other conspecifics of danger while blocking olfactory receptors in the targeted predator. [44] [1]

Cuttlefish (Sepia officinalis) are also well known for their escape responses. Unlike squids, who may engage more salient escape responses, the cuttlefish has few defences so it relies on more conspicuous means: jet-driven escape and freezing behaviour. [2] However, it appears that the majority of cuttlefish use a freezing escape response when avoiding predation. [2] When the cuttlefish freeze, it minimizes the voltage of their bioelectric field, making them less susceptible to their predators, mainly sharks. [2]


Cost–Benefit Analysis

Assessing the costs and benefits of any animal behaviour relative to the suite of possible behavioural options available is a valuable framework in which to consider its expression, utility and consequences in any given ecological context. Here, we conduct a cost–benefit analysis of distraction displays compared with the use of alternative anti-predator tactics in different situations that prey may encounter.

Benefits

The obvious benefit of anti-predator distraction displays for adult birds is the defence of their young (Gochfeld 1984 , Smith & Wilson 2010 , Gómez-Serrano & López-López 2017 ). Offspring survival translates into increased reproductive success and overall lifetime fitness for the parents. As discussed earlier, the timing of the occurrence and frequency of displays varies between bird species, apparently dependent on how and when the behavioural strategy best maximizes return on parental investment (Barash 1975 ). Distraction displays clearly serve a useful anti-predator function in some bird species, but otherwise it is not common behaviour. The potential costs associated with the behaviour go some way to explain this pattern across taxa, and it is these costs which we consider in more detail.

Costs

For all species that use distraction there will be associated energy costs, particularly where the display is elaborate and continues for a long time through various transitions over long distances as the individual attempts to lead predators away. Time spent distracting predators is also less time spent feeding, incubating and maintaining nest structures, and so individuals may have to expend further energy in the immediate aftermath of distracting predators in order to compensate (Montgomerie & Weatherhead 1988 , Gómez-Serrano & López-López 2017 ). Distraction behaviour may thereby reduce fitness, although such long-term reproduction or survival costs of distraction displays would be difficult to quantify accurately.

The fitness costs if displays inadvertently provide a clue to the location of offspring will be more severe and more easily quantifiable than energetic costs (Gochfeld 1984 ). This cost may not necessarily be associated with the focal predator that the original display was intended to attract. More eye-catching displays, for example, could unintentionally attract other predators, which may then pursue the adult or start searching for their young nearby. Gochfeld ( 1984 ) also drew attention to an observation by Matthiessen ( 1967 ) that the re-entrapment practices by shorebirds after performing a ‘rodent run’ distraction behaviour represent a vulnerability, as predators may recognize from their prey's pauses that they are not in fact dealing with a fleeing rodent. The re-entrapment behaviour essential to responsive and flexible distraction displays may be a weakness in other distraction behaviours, too, and such predator-monitoring pauses may be used as a clue to trigger predators to abandon interest in the parent and return to search the vicinity for young (although we know of no empirical exploration of this suggestion).

Considering the environments in which distraction displays are most common, further costs can arise. Because distraction displays are frequently associated with comparatively open nest locations, with unimpeded views of the surroundings so that predators are detected by parents as they approach (Armstrong 1954 , Gochfeld 1984 , Muir & Colwell 2010 ), birds occupying such locations may experience higher thermoregulatory costs due to factors such as increased wind speeds, particularly in arctic environments. Parents and their offspring at open nest-sites may also be more susceptible to threats that do not respond to distraction displays, such as avian predators.

In the uncommon scenario where predators find themselves responding to distraction displays more commonly than they encounter genuinely injured prey, there is an alternative risk of predators becoming habituated to such displays. Sonerud ( 1988 ) reports two encounters between brood-attending grouse hens (Tetraonidae) – a Black Grouse hen Tetrao tetrix and a Capercaillie hen Tetrao urogallus – and a Red Fox Vulpes vulpes where the fox appeared to ignore the distraction displays of the hens and instead changed its behaviour in a way that was interpreted as enhanced searching for a nest. In circumstances such as this, where local learning may have occurred for a predator with several breeding prey in its territory, the conspicuousness of distraction displays carries the risk of further attracting a predator's attention to offspring.

Beyond potentially informing a predator of offspring presence, distraction displays can also carry a risk of predation for the parent themselves. Self-sacrifice would probably also be fatal to a parent's dependent young, so the fitness cost is likely to be total, but birds exhibiting distraction displays do occasionally get captured during distraction efforts (Gochfeld 1984 , Brunton 1986 , Sordahl 1990b , Amat & Masero 2004 , Gómez-Serrano & López-López 2017 ). Although some of these cases do involve the bird being captured by the predator at which the display was directed (Brunton 1986 , Sordahl 1990b ), there are a couple of observations that have involved displaying birds being preyed upon by raptors, such as a Montagu's Harrier Circus pygargus (Amat & Masero 2004 ) and a Common Kestrel Falco tinnunculus (Gómez-Serrano & López-López 2017 ). In these latter cases, displays were most likely to have been deployed against other predators, but the raptors were able opportunistically to predate the birds while they were engaged in distraction behaviour. The importance of all captures during distraction displays should certainly not be neglected in considering the potential costs of this behaviour (Brunton 1986 , Lima & Dill 1990 , Sordahl 1990b , Gómez-Serrano & López-López 2017 ). For all species that employ distraction display behaviours there is likely to be some risk of capture by the predator to which the display is aimed, as predators are evolutionary disposed to not ignore signals suggesting an easy meal (Ruxton et al. 2018 ). However, many observations suggest that individuals engaged in defence are constantly alert, probably even in a state of hyper-alertness (Gochfeld 1984 ). Fatal outcomes for prey are expected to be rare, otherwise selection would act strongly to eliminate such a high-risk behaviour (Gochfeld 1984 , Gómez-Serrano & López-López 2017 ).

Different levels of risk are likely to be experienced by birds performing different types of display. Although there is little quantitative evidence, some studies suggest that birds performing riskier displays gain a greater reward from the behaviour. For example, Byrkjedal ( 1987 ) found that ground-based distraction displays, which suggest a high degree of incapability but also make the displaying parent relatively vulnerable, were more efficient and had a greater effect on nest survival than were displays performed while flying away from the nest. Furthermore, the findings of Gómez-Serrano and López-López ( 2017 ) also suggest that the longevity of nests can be greater when parents take greater risks as part of their distraction display behaviour. Certainly, investment in anti-predator defence should be proportional to predation risk (Lima & Dill 1990 ) and flexible according to the specific circumstances. We next consider the trade-offs involved in distraction displays and what situations may provoke distraction in preference to alternative anti-predator tactics.


Contents

The ability to perform an effective escape maneuver directly affects the fitness of the animal, because the ability to evade predation enhances an animal’s chance of survival. [3] [6] Those animals that learn to or are simply able to avoid predators have contributed to the wide variety of escape responses seen today. Animals that are able to adapt their responses in ways different from their own species have displayed increased rates of survival. [7] Because of this, it is common for the individual escape response of an animal to vary according to reaction time, environmental conditions, and/or past and present experience. [7]

Arjun et al. (2017) found that it is not necessarily the speed of the response itself, but the greater distance between the targeted individual and the predator when the response is executed. [8] In addition, the escape response of an individual is directly related to the threat of the predator. Predators that pose the biggest risk to the population will evoke the greatest escape response. Therefore, it may be an adaptive trait selected for by natural selection.

Law & Blake (1996) argue that many morphological characteristics could contribute to an individual's efficient escape response, but the escape response has undoubtedly been molded by evolution. In their study, they compared more recent sticklebacks to their ancestral form, the Paxton Lake stickleback, and found that the performance of the ancestral form was significantly lower. [9] Therefore, one may conclude that this response has been ripened by evolution.

How the escape responses are initiated neurologically, and how the movements are coordinated is dependent on the species. The behaviors alone vary widely, so, in a similar manner, the neurobiology of the response can be highly variable between species. [10]

‘Simple’ escape responses are commonly reflex movements that will quickly move the animal away from the potential threat. [3] These neural circuits operate quickly and effectively, rapidly taking in sensory stimuli and initiating the escape behavior through well-defined neuron systems. [11]

Complex escape responses often require a mixture of cognitive processes. This may stem from a difficult environment to escape from, or the animal having multiple potential escape methods. Initially, the animal must recognize the threat of predation, but following the initial recognition the animal might have to quickly determine the best route of escape, based on prior experience. [12] This means rapid integration of incoming information with prior knowledge, and then coordination of motor movements deemed necessary. Complex escape responses generally require a more robust neural network. [3]

Researchers will often evoke an escape response to test the potency of hormones and/or medication and their relationship to stress. As such, the escape response is fundamental to anatomical and pharmacological research. [13]

Habituation Edit

A series of initially threatening encounters that do not lead to any true adverse outcomes for the animal can drive the development of habituation. [3] Habituation is an adaptation strategy that refers to the diminishing response of an animal to a stimulus following repetitive exposures of the animal to that same stimulus. [14] In other words, the animal learns to distinguish between innately threatening situations and may choose to not go through with their escape response. This is a highly variable phenomenon, where the stimulus itself is highly specific, and the experience is highly context dependent. [15] [16] This suggests that there is no one mechanism by which a species will develop habituation to a stimulus, instead habituation may arise from the integration of experiences. [3] A number of cognitive processes may operate during one single threatening experience, but the levels at which these processes are integrated will determine how the individual animal will potentially respond next. [17]

Caenorhabditis elegans, commonly identified as nematodes, have been used as a model species for studies observing their characteristic “tap-withdrawal response”. [18] The tapping on serves as the fear-provoking, mechanical stimulus which C. elegans worms will move away from. If the tapping stimulus continues without any direct effects on the worms, they will gradually stop responding to the stimulus. This response is modulated by a series of mechanosensory neurons (AVM, ALM, PVD, and PLM) which synapse with interneurons (AVD, AVA, AVB, and PVC) transmitting the signal to motor neurons that cause the back-and-forth movements. Habituation to the tapping reduces activity of the initial mechanosensory neurons, seen as decrease in calcium channel activity and neurotransmitter release. [18]

The primary force driving escape habituation is suspected to be energy conservation. [3] If an animal learns that a certain threat will not actively cause harm to it, then the animal can choose to minimize its energy costs by not performing its escape. [19] For example, Zebra danios, also known as Zebrafish, who are habituated to predators are more latent to flee than those who were not habituated to predators. [20] However, habituation did not affect the fish's angle of escape from the predator. [20]

Learned Helplessness Edit

If an animal cannot react via a startle or avoidance response, they will develop learned helplessness as a result of receiving or perceiving repeated threatening stimuli and believing the stimuli is unavoidable. [21] The animal will submit and not react, even if the stimuli previously triggered instinctual responses or if the animal is provided an escape opportunity. In these situations, escape responses are not used because the animal has almost forgotten their innate response systems. [22]

Helplessness is learned through habituation, because the brain is programmed to believe control is not present. In essence, animals operate under the assumption they have the free will to fight, flee or freeze as well as engage in other behaviors. When escape responses fail, they develop helplessness.

A common, theoretical example of learned helplessness is an elephant, trained by humans who condition the elephant to believe it cannot escape punishment. As a young elephant, it would be chained down with a pick to keep it from leaving. As it grows, the elephant would have the ability to easily overpower the tiny pick. Development of learned helplessness keeps the elephant from doing so, believing that it is trapped and the effort is futile.

In a more natural setting, learned helplessness would most often be displayed by animals that live in group settings. If food were scarce and one individual was always overpowered when it came time to get food, it would soon believe that no matter what it did, getting food would be impossible. It would have to find food on its own or submit to the idea it will not eat.

Startle response is an unconscious response to sudden or threatening stimuli. In the wild, common examples would be sharp noises or quick movements. Because these stimuli are so harsh they are connected to a negative effect. This reflex causes a change in body posture, emotional state, or a mental shift to prepare for a specific motor task. [23]

A common example would be cats and how, when startled, their arrector pili muscles contract, making the hair stand up and increase their apparent size. Another example would be excessive blinking due to the contraction of the orbicularis oculi muscle when an object is rapidly moving toward an animal this is often seen in humans.

Halichoerus grypus, or Grey seals, respond to acoustic startle stimuli by fleeing from the noise. The acoustic startle reflex is only activated when the noise is over eighty decibels, which promotes stress and anxiety responses that encourage flight. [24]

Flight Zone Edit

Flight zone and flight distance are interchangeable and refer to the distance needed to keep an animal under the threshold that would trigger a startle response.

A flight zone can be circumstantial, because a threat can vary in size (individually or in group number). Overall, this distance is the measure of an animal's willingness to take on risks. This differentiates a flight zone from personal distance an animal prefers and social distance (how close other species are willing to be). [25]

An applicable analogy would be a reactive dog. When the flight zone is large, the dog will maintain an observant stance, but a startle response will not occur. As the threatening stimuli moves forward and decreases the flight zone, the dog will exhibit behaviors that fall into a startle or avoidance response. [25]

The avoidance response is a form of negative reinforcement which is learned through operant conditioning. This response is usually beneficial, as it reduces risk of injury or death for animals, also because it is an adaptive response and can change as the species evolves. Individuals are able to recognize certain species or environments that need to be avoided, which can allow them to increase the flight distance to ensure safety.

When scared, octopus release ink to distract their predators enough that they can burrow into a safe area. Another example of avoidance is the fast-start response in fish. They are able to relegate musculoskeletal control which allows them to withdraw from the environment with the threatening stimuli. [26] It is believed that the neural circuits have adapted over time to more quickly react to a stimulus. Interestingly, fish that keep to the same groups will be more reactive than those who are not.

In birds Edit

Avian species also display unique escape responses. Birds are uniquely vulnerable to human interference in the form of aircraft, drones, cars, and other technology. [27] [28] There has been a lot of interest in how these structures will and do affect the behaviors of terrestrial and aquatic birds.

One study, Weston et. al., 2020, observed how flight initiation changed according to the distance of the drone from the birds. It was found that as the drone approached the tendency of birds to take flight to escape it increased dramatically. This was positively affected by the altitude at which the birds were exposed to the drone. [28] In another experiment by Devault et al. (1989), brown-headed cowbirds (Molothrus ater) were exposed to a demonstration of traffic traveling at speeds between 60 – 360 km/hr. When approached by a vehicle travelling at 120 km/h, the birds only allotted 0.8s to escape before a possible collision. [27] This study showed that fast traffic speeds may not allow enough time for birds to initiate an escape response.

In fish Edit

In fish and amphibians, the escape response appears to be elicited by Mauthner cells, two giant neurons located in the rhombomere 4 of the hindbrain. [29]

Generally, when faced with a dangerous stimuli, fish will contract their axial muscle, resulting a C-shaped contraction away from the stimulus. [30] This response occurs in two separate stages: a muscle contraction that allows them to speed away from a stimulus (stage 1), and a sequential contralateral movement (stage 2). [30] This escape is also known as a "fast-start response". [31] The majority of the fish respond to an external stimulus (pressure changes) within 5 to 15 milliseconds, while some will exhibit a slower response taking up to 80 milliseconds. [32] While the escape response generally only propels the fish a small distance away, this distance is long enough to prevent predation. While many predators use water pressure to catch their prey, this short distance prevents them from feeding on the fish via suction. [33]

Particularly in the case of fish, it has been hypothesized that the differences in escape response are due to the evolution of neural circuits over time. This can be witnessed by observing the difference in the extent of stage 1 behaviour, and the distinct muscle activity in stage 2 of the C-start or fast-start response. [26]

In larval zebrafish (Danio rerio), they sense predators using their lateral line system. [33] When larvae are positioned lateral to a predator, they will escape in a likewise lateral direction. [33] According to game theory, zebrafish who are positioned lateral and ventral to the predator are more likely to survive, rather than any alternate strategy. [33] Finally, the faster (cm/s) the predator is moving, the faster downward the fish will move to escape predation. [33]

Recent research in guppies has shown that familiarity can affect the reaction time involved in the escape response. [31] Guppies that were placed in familiar groups were more likely to respond than guppies who were assigned to unfamiliar groups. Wolcott et al. (2017) suggest that familiar groups may lead to reduced inspection and aggression among conspecifics. The theory of limited attention states that the brain has a limited amount of information processing, and, as an individual is engaged in more tasks, the less resources it can provide to one given task. [34] As a result, they have more attention that they can devote toward anti-predator behaviour.

In insects Edit

When house flies (Musca domestica) encounter an aversive stimulus, they jump rapidly and fly away from the stimulus. A recent research suggests that the escape response in Musca domestica is controlled by a pair of compound eyes, rather than by the ocelli. When one of the compound eyes was covered, the minimum threshold to elicit an escape response increased. In short, the escape reaction of Musca domestica is evoked by the combination of both motion and light. [35]

Cockroaches are also well known for their escape response. When individuals sense a wind puff, they will turn and escape in the opposite direction. [36] The sensory neurons in the paired caudal cerci (singular: cercus) at the rear of the animal send a message along the ventral nerve cord. Then, one of two responses are elicited: running (through the ventral giant interneurons) or flying/running (through the dorsal giant interneurons). [37]

In mammals Edit

Mammals can display a wide range of escape responses. Some of the most common escape responses include withdrawal reflexes, fleeing, and, in some instances where outright escape is too difficult, freezing behaviors.

Higher-order mammals often display withdrawal reflexes. [38] Exposure to danger, or a painful stimulus (in nociceptor-mediated loops), initiate a spinal reflex loop. Sensory receptors transmit the signal to the spine where it is rapidly integrated by interneurons and consequently an efferent signal is sent down motor neurons. The effect of the motor neurons is to contract the muscles necessary to pull the body, or body part away from the stimulus. [39]

Some mammals, like squirrels and other rodents, have defensive neural networks present in the midbrain that allow for quick adaptation of their defense strategy. [40] If these animals are caught in an area without refuge, they can quickly change their strategy from fleeing to freezing. [41] Freezing behavior allows for the animal to avoid detection by the predator. [3]

In one study, Stankowich & Coss (2007) studied the flight initiation distance of Columbian black-tailed deer. According to the authors, the flight initiation distance is the distance between prey and predator when the prey attempts an escape response. [42] They found that the angle, distance, and speed that the deer escaped was related to the distance between the deer and its predator, a human male in this experiment. [42]

Other examples Edit

Squids have developed a multitude of anti-predator escape responses, including: jet-driven escape, postural displays, inking and camouflage. [1] Inking and jet-driven escape are arguably the most salient responses, in which the individual squirts ink at the predator as it speeds away. These blobs of ink can vary in size and shape larger blobs can distract the predator while smaller blobs can provide a cover under which the squid can disappear. [43] Finally, the released ink also contains hormones such as L-dopa and dopamine that can warn other conspecifics of danger while blocking olfactory receptors in the targeted predator. [44] [1]

Cuttlefish (Sepia officinalis) are also well known for their escape responses. Unlike squids, who may engage more salient escape responses, the cuttlefish has few defences so it relies on more conspicuous means: jet-driven escape and freezing behaviour. [2] However, it appears that the majority of cuttlefish use a freezing escape response when avoiding predation. [2] When the cuttlefish freeze, it minimizes the voltage of their bioelectric field, making them less susceptible to their predators, mainly sharks. [2]


Chullin 140b

We are just two days away from finishing the long tractate called Chullin, which dealt with all manner of questions about kosher meat and poultry. In the final chapter we are studying the details of a rather different issue: the command to frighten away the mother bird if you wish to eat the eggs she is incubating. This commandment is called שילוח הקן – shiluach haken, (lit. “sending away the nest”). We will discuss some ornithological issues and see how they might impact our understanding of the command.

Here are the details in the Torah:

כִּ֣י יִקָּרֵ֣א קַן־צִפּ֣וֹר ׀ לְפָנֶ֡יךָ בַּדֶּ֜רֶךְ בְּכָל־עֵ֣ץ ׀ א֣וֹ עַל־הָאָ֗רֶץ אֶפְרֹחִים֙ א֣וֹ בֵיצִ֔ים וְהָאֵ֤ם רֹבֶ֙צֶת֙ עַל־הָֽאֶפְרֹחִ֔ים א֖וֹ עַל־הַבֵּיצִ֑ים לֹא־תִקַּ֥ח הָאֵ֖ם עַל־הַבָּנִֽים׃ שַׁלֵּ֤חַ תְּשַׁלַּח֙ אֶת־הָאֵ֔ם וְאֶת־הַבָּנִ֖ים תִּֽקַּֽח־לָ֑ךְ לְמַ֙עַן֙ יִ֣יטַב לָ֔ךְ וְהַאֲרַכְתָּ֖ יָמִֽים׃

If, along the road, you chance upon a bird’s nest, in any tree or on the ground, with fledglings or eggs and the mother sitting over the fledglings or on the eggs, do not take the mother together with her young. Let the mother go, and take only the young, in order that you may fare well and have a long life.

That’s it. Two sentences. But have no fear - there are at least twelve pages of discussion about this in the Talmud, which raises all sorts of questions. Like this one, asked by Rabbi Zeira:

בעי ר' זירא יונה על ביצי תסיל מהו תסיל על ביצי יונה מהו

If a yonah (pigeon) is resting upon the eggs of a tasil, [a kosher bird resembling a pigeon,] what is the halakha with regard to sending away the mother bird from the nest? Likewise, if a tasil is resting upon the eggs of a yonah (pigeon), what is the halakha?

אמר אביי ת"ש עוף טמא רובץ על ביצי עוף טהור וטהור רובץ על ביצי עוף טמא פטור משילוח הא טהור וטהור חייב דלמא בקורא

Abaye said: Come and hear that which is taught in the Mishna (on 138b): In a case where a non-kosher bird is resting upon the eggs of a kosher bird, or a kosher bird is resting upon the eggs of a non-kosher bird, one is exempt from sending away the bird. One may infer from the mishna that in a case involving a kosher bird and kosher eggs, [e.g., a tasil resting on the eggs of a pigeon, one is obligated to send away the mother bird. The Gemara rejects this:] Perhaps this inference applies only to the case of a koreh, (? female pheasant) , which normally rests upon the eggs of other birds. Since this is its normal behavior, one is obligated to send it away even if it rests upon the eggs of another kosher bird. This may not be the case with regard to a tasil or pigeon.

Let’s try and figure all this out. First, what are the identities of these three birds mentioned: the yonah, the tasil and the koreh?

Male and Female Bird Plumage

The Yonah is fairly easy to identify there is unanimous agreement that it a dove. Or a pigeon. Confused? They are both members of the species Columbida: The common (or domestic) pigeon is Columba livia domestica, and the mourning dove is Columbidae Zenaida macroura. Moving right along.

The Tasil is a bit more challenging. Rashi declares that it is “a tahor [ie kosher] bird, similar to the yona.” And that’s how it is translated in the Schottenstein Talmud. Marcus Jastrow wrote in his dictionary that is “a species of small dove.” The Koren notes that the tasil might be “a bird similar to a pigeon, or to a laughing dove, a small dove native to Eretz Yisrael.” So a bit of a mystery.

The identity of the Koreh seems to be easy. At least that what it seems from the translations. The Soncino translates it as a partridge, as is does the Schottenstein. The Koren English translation is even more specific: “This bird is identified as the sand partridge, a desert bird of the genus Ammoperdix in the pheasant family Phasiandae.” Wow. That’s some impressive ornithology.

Actually that specific identification is very important, because there is a debate as to whether this whole business of sending away the bird brooding over some eggs applies only to the female bird, and not to a male that is incubating. Here is a photo of a male sand partridge. It is grey with wavy flanks and beautiful white markings over the beak and behind the eyes. The female is a drab sandy brown color.

Male sand partridge. Note the beautiful white markings behind the eyes.

A lady sand partridge. No white facial markings.

According to the Talmud there is agreement that the command of shiluach haken does not apply to male birds. But there is a dispute about this specific bird, the koreh - our sand partridge. Rabbi Eliezer ruled that when it comes to this particular species, the male bird that is brooding must be frightened away before taking the eggs, just like the female.

תניא נמי הכי זכר דעלמא פטור קורא זכר ר"א מחייב וחכמים פוטרין

With regard to a male bird in general, one is exempt from the mitzva of sending it away, but with regard to a male koreh, Rabbi Eliezer deems one obligated to send it away from the nest, and the Rabbis deem one exempt from sending it away.

This requirement only makes sense if the two are readily distinguishable at a distance, and thanks to these nice photos, we now know they are.

By the way, have you wondered why this bird is called the קורא - koreh, which from the hebrew root ק–ר–א, k-r-h which means to call out? Apparently the bird has a prominent call which is heard long before it can be seen. Which perhaps gave its name: “the one that calls out.” (If you want to hear that call, click here. To be honest, to me it sounds like a slower version of the swish of a baby’s heartbeat heard with ultrasound. But that’s just me.)

Who is sitting on the eggs? Mom or dad?

As we noted, the Talmud rules that the commandment of shiluah haken applies only to the female of the species. Should the father be incubating, no such command applies (except for the sand partridge, as we just discussed). Here, for example, is what the great Maimonides wrote in his code, the Mishneh Torah:

רמב’ם משנה תורה הל׳ שחיטה. יג:י

זָכָר שֶׁמְּצָאוֹ רוֹבֵץ עַל הַקֵּן פָּטוּר מִלְּשַׁלֵּחַ

If a male was found incubating in the nest, there is no obligation to send him away [before taking the eggs or chicks].

This is also the ruling of the Shulchan Aruch, the Code of Jewish Law. Which raises the question - just how common is it for the male of the species to incubate the eggs? This is, of course a very challenging question to answer, because it all depends: which birds (European, American, African)? Birds of prey? Backyard birds? But given that, can we make a generalization?

Yale’s Ornithologist-in-Chief to the rescue

For an answer, Talmudology turned to Richard Prum, who is both the William Robertson Coe Professor of Ornithology in the Department of Ecology & Evolutionary Biology at Yale University, and the Curator of Ornithology, (and Head Curator of Vertebrate Zoology,) at Yale’s Peabody Museum of Natural History, in New Haven, Connecticut. And here is what he told us:

This certainly came as a bit of a surprise. It turns out then that you will find a male brooding in the nest a lot of the time! Prof. Prum also noted that these behaviors are not randomly distributed among birds. Closely related species of birds tend to have similar incubation behavior, but higher groups may differ extensively.

In addition, most of the species with substantial eggs have female only incubation. These groups include most game birds and waterfowl like chickens, quail, francolins, guineafowl, ducks, geese, etc. In most of these species, the male takes no part in parental care. That last bit is really important, because it is just these kinds of kosher wild birds that are subject to the law of sending the mother-bird away. In most of these species the male takes no part. So the Talmud was spot on, so to speak, in limiting the commandment to these kinds of fowl. But there is another complication. Prof. Prum also wrote that “in many species with shared incubation, it is impossible to distinguish the male from the female by plumage.”

Reasons For the Commandments

There is a well-known philosophical debate about whether it is appropriate to give reasons behind the 613 mitzvot (commandments) found in the Torah. Much has been written and many fine minds were engaged with this question as it pertains to the commandment of shiluach haken. Perhaps it is an example of imitatio dei:God is kind, so you should be kind to his creatures. Therefore send the mother bird away so she cannot get upset when you remove her eggs. As an example of this train of thought (and there are many) here is the commentary of the famous Moshe ben Nachman, (1194-1270), better known as the Ramban:

הטעם לבלתי היות לנו לב אכזרי ולא נרחם, או שלא יתיר הכתוב לעשות השחתה לעקור המין, אע"פ שהתיר השחיטה במין ההוא. והנה ההורג האם והבנים ביום אחד, או לוקח אותם בהיות להם דרור לעוף, כאלו יכרית המין ההוא

If the nest of a bird chances to be in front of you: Also this commandment is explained by "it and its son do not slaughter on one day" (Leviticus 22:28) since the reason in both of them is that we should not have a cruel heart and [then] not have mercy, or that the verse should not permit us to be destructive to destroy the species, even though it allowed slaughter within that species. And behold, one who kills the mother and the children on one day or takes them when they are 'free to fly' is as if he cuts off that species.

A similar reason is cited by the French French commentator Rashbam Samuel ben Meir (1085 – c. 1158). It it prevents cruelty (שדומה לאכזריות ורעבתנות). So too the Spanish commentator R. Bechayei (1255-1340):

שלח תשלח את האם, טעם המצוה ללמדנו על מדת הרחמנות, ושנתרחק מן האכזריות שהיא תכונה רעה בנפש, וכעניין שאסרה תורה (ויקרא כב) לשחוט אותו ואת בנו ביום אחד, וכעניין שנצטוינו בתורה שבעל פה דרך רחמנות לא דרך אכזריות בשחיטה בצואר ולא מן העורף, והוא דעת הרב בספר המורה, וכבר הזכרתיו למעלה"

The reason for the command is to teach us the quality of mercy, and to distance us from cruelty…just as the Torah prohibited the slaughter of a mother and its calf on the same day…

Maimonides, in his Guide for the Perpexled, also weighed in on the reason for this command, and decided it was all about kindness:

The same reason applies to the law which enjoins that we should let the mother fly away when we take the young. The eggs over which the bird sits, and the young that are in need of their mother, are generally unfit for food, and when the mother is sent away she does not see the taking of her young ones, and does not feel any pain. In most cases, however, this commandment will cause man to leave the whole nest untouched, because [the young or the eggs], which he is allowed to take, are, as a rule, unfit for food. If the Law provides that such grief should not be caused to cattle or birds, how much more careful must we be that we should not cause grief to our fellowmen.

On the other hand…

There are a few sources that criticize the entire enterprise of ascribing reasons for any of the commandments in general, and of shiluach haken in particular. Like this one in the Mishnah itself:

משנה :האומר על קן ציפור יגיעו רחמיך …משתקין אותו

If a person adds in his prayers: “Your mercy is extended to a bird’s nest, so too extend Your mercy to us…he is silenced

Why such drastic action for reciting such a nice prayer? Here is the talmudic discussion:

פליגי בה תרי אמוראי במערבא רבי יוסי בר אבין ורבי יוסי בר זבידא חד אמר מפני שמטיל קנאה במעשה בראשית וחד אמר מפני שעושה מדותיו של הקדוש ברוך הוא רחמים ואינן אלא גזרות

Two amora’im in Eretz Yisrael disputed this question Rabbi Yosei bar Avin and Rabbi Yosei bar Zevida one said that this was because he engenders jealousy among God’s creations, [as it appears as though he is protesting the fact that the Lord favored one creature over all others]. And one said that this was because he transforms the attributes of the Holy One, Blessed be He, into expressions of mercy, when they are nothing but decrees of the King that must be fulfilled without inquiring into the reasons behind them.

So there are two opinions as to why this prayer is forbidden: the first, because it is inherently unfair to single out the incubating bird for a dose of extra divine mercy. What about the rest of the animal kingdom? And the second, because in general, the commands have nothing to do with mercy. They are just the commandments of God. And if they are kind, well that’s an added benefit but even if they were cruel they are there to be obeyed.

Ornithology and today’s daf

Now back to the observations of Prof. Prum, and today’s page of Talmud. If it is indeed the case that:

1) male and female birds are often equally likely to be incubating and

2) in many species with shared incubation, it is impossible to distinguish the male from the female and

3) that male incubators are exempt from commandment of shiluach haken,

then what becomes of the school of thought that ascribes mercy to the reason for it in the first place? Don’t male incubators, who have built the nest and are just as invested in the project as are the females, don’t they deserve some mercy too? And why exempt male birds when male and females are so often indistinguishable?

There is increasing evidence that all kinds of animals experience emotions just like we do. And it’s not only playful chimps and depressed dogs. Elephants mourn. Pigs kept in boring pens show behavior that in humans we would call depression. Rats enjoy being tickled.

And birds? Well, some birds like to surf at the beach, a behaviour that does not “seem to provide any obvious function apart from enjoyment — they look like they are having fun.” And birds have self-control. Really. Remember the Marshmallow test? (We reviewed it back in April 2015 when we learned Ketuvot 83. If you’ve forgotten, read this and then come back….) Well it turns out that when a (particularly smart and cooperative) parrot was given the bird equivalent of the test, he was successful 90% of the time, enduring delays of up to 15 minutes. The researchers noted that to do this “the parrot had to postpone the immediate available reward to gain more desirable future rewards, maintaining the choice to delay, and tolerate the frustration of this self-inflicted delay.” So, yeah, birds have self control. The more we study, the more we realize that animals too, have emotions. So if sending away the mother bird might reduce her grieving, let’s do it.


Media Release

Each homing pigeon embarking on a lengthy homeward journey is following in the wingbeats of the human tradition of pigeon keeping dating back thousands of years. Equipped with internal compasses for guidance, young pigeons gradually build up a picture of the terrain surrounding their loft, which they eventually call on when displaced further. However, Dora Biro and Lucy Taylor, from the University of Oxford, UK, were curious to learn more about how pigeons build confidence as a route becomes more familiar. &lsquoWhen I think about how I move when navigating, I move differently if I am not sure where I am going compared to when I am walking a known route&rsquo, says Taylor, adding, &lsquoWe imagined the same may also be true for birds&rsquo.

Teaming up with biomechanics expert Steven Portugal, from Royal Holloway, University of London, UK, Taylor and Biro attached accelerometers, which detect motion, coupled with GPS sensors to young pigeons to monitor their wingbeat patterns and routes as the aviators became increasingly familiar with the return journey home from two locations, 3.85 and 7.06 km away.

&lsquoThe pigeons were very cooperative&rsquo, says Taylor, recalling that they were content to be held while the motion sensors were secured to their backs before being released individually. However, Taylor had to be prepared for the notoriously unpredictable British summer. High winds, cloud, rain and extreme heat can affect a bird&rsquos ability to navigate home, so Taylor was on standby for much of the season to catch the few days when the conditions were ideal and the team could fit in two homing flights per day. Then, having collected 200 acceleration readings each second during flights lasting 5 min up to several hours, Taylor was faced with the colossal task of synchronising over 48 million data records to build a complete understanding of each homing flight as the birds gained in confidence.

After analysing the immense data set, the trio was able to identify clear patterns in the pigeons&rsquo behaviour. As the birds became more experienced, their routes meandered less and became more direct until they converged on an efficient flight path by the sixth return journey. In addition, the animals flapped their wings
harder (their torsos bobbed up and down more) and increased their speed as they
became more confident of their path.

Summing up their observations, Taylor says, &lsquoPigeons flap their wings differently depending on how well they know a landscape&rsquo, adding that early flights from unfamiliar locations are likely to be more energetically costly as the pigeons fly more slowly and take less direct routes.

Reflecting on the study, Taylor says, &lsquoWe didn&rsquot know at the start whether the birds would flap differently depending on how well they know a terrain&rsquo, and she and her colleagues are now optimistic that their observations could help other scientists investigate how animals navigate. &lsquo[These] flight characteristics may be used as &ldquosignatures&rdquo of birds&rsquo familiarity with a navigational task&hellipthat could be utilised to
provide new insights, through non-invasive methods, into the decision-making and navigational strategies of birds&rsquo, says Taylor.


Watch the video: This tree isnt what it appears to be when the birds decide to fly away (May 2022).