BIRD ODORS AND OTHER CHEMICAL SUBSTANCES: A DEFENSE MECHANISM OR OVERLOOKED MODE OF INTRASPECIFIC COMMUNICATION?

Birds emit many chemical compounds, though ornithologists rarely consider them. Avian odors, for example, are readily detectable to humans in at least 17 avian orders and 80 genera (Table 1; data from Weldon and Rappole 1997). Scents consist of volatile chemicals, and birds embrace a remarkable diversity of aromas, such as the musky plumage of storm-petrels (Hydrobatidae; Jacob and Zisweiler 1982); the tangerine-like perfume of Crested Auklets (Aethia cristatella; Humphrey and Phillips 1958); the acrid, sour odor of Hooded Pitohuis (Pitohui dichrous) and Variable Pitohuis (P. kirkocephalus; Dumbacher et al. 1992); the sweet and dusty fragrance of the Kakapo (Strigops habroptilus; Butler 1989, J. C. Hagelin pers. obs.); and the foul stench of the Hoatzin (Opisthocomus hoatzin; see Weldon and Rappole 1997). Birds also produce a variety of substances consisting of larger, less volatile compounds. Frequently odorless, these occur in various forms, such as saturated fatty acids of uropygial gland secretions (Jacob and Zisweiler 1982, Sweeney et al. 2004) or toxins sequestered in plumage or skin (e.g., Dumbacher et al. 1992). Some avian orders considered odorous to ornithologists (adapted from Hagelin [2007]; original data collected from Weldon and Rappole [1997]). Some avian orders considered odorous to ornithologists (adapted from Hagelin [2007]; original data collected from Weldon and Rappole [1997]). Human detection of an avian compound clearly does not mean that it is important to a bird, unless this has been verified experimentally. Here, we focus on two major types of adaptive functions that have been proposed for a variety of odors and other chemical substances that birds either produce themselves or sequester from secondary sources. First, avian compounds may serve as a chemical defense. This includes protection against predators, ectoparasites, and microbes and can involve substances that act as an interspecific deterrent or signal (e.g., Cott 1947, Swennen 1968, Dumbacher et al. 1992, Mouritsen and Madsen 1994, Douglas et al. 2001, Shawkey et al. 2003). Alternatively, some authors posit that avian compounds function as an intraspecific chemosignal, similar to those found in other vertebrates, such as mammals (e.g., Balthazart and Schoffeniels 1979; review in Roper 1999, Hagelin 2007). Recently, birds have been shown to recognize conspecific body odor (Hagelin et al. 2003) and personal body odor or mate odor (Bonadonna and Nevitt 2004). Some chemical signatures are even individually specific (e.g., Bonadonna et al. 2003a, b, 2004, 2007). The use of chemical signals in intraspecific communication has the potential to fundamentally alter how we interpret bird behavior. The idea is relatively new and challenges the traditional view that birds predominantly respond to their world through sight and sound. Birds readily respond to chemicals derived from their environment during activities such as foraging, navigation, or nest building (e.g., Wenzel 1968; Hutchison and Wenzel 1980; Clark and Mason 1985; Nevitt et al. 1995; Petit et al. 2002; Wallraff 2004; Nevitt and Bonadonna 2005a, b). Birds also exhibit the three vertebrate chemosenses—olfaction, taste, and a trigeminal system, though ornithologists rarely consider them separately (Roper 1999). A fully functional olfactory system, which detects volatile chemical stimuli, has been found in every bird studied, and it is similar in design to that of other vertebrates (Bang and Wenzel 1985, Roper 1999). Avian species also have taste buds, a sense of taste (e.g., Wenzel 1973, Ganchrow and Ganchrow 1985), and a trigeminal system that processes chemical sensations, such as the burning of a chemical irritant (e.g., Clark et al. 1991, Mora et al. 2004, McKeegan et al. 2005; review in Roper 1999). Consequently, we believe that the use of avian compounds as intraspecific signals is to be expected in birds, just as chemosignals are commonly linked to the senses and behavioral repertoire of other vertebrate groups. To introduce the topic of avian odor and chemical substances, we focus on common sources of scents, secretions, and other compounds, such as those stored in tissues. Next, we discuss the use of avian chemicals as a heterospecific defense mechanism, and then examine in detail the role of intraspecific chemical signals, a topic that is usually overlooked in studies of avian social behavior. For both hypotheses, we define terms and provide a set of testable predictions. We also highlight gaps in our knowledge of avian species, point out productive research topics from other animal systems, and call attention to discussions of birds that we find rather speculative. Future investigations of the chemical senses and signals of birds are promising. Such studies are inherently interdisciplinary, involving responses at the molecular, physiological, developmental, and behavioral levels. Research on any aspect of avian chemosensory biology will lead to informative comparisons with other vertebrates, such as mammals, which are in detail (e.g., and and see also and 2007). substances of birds occur in many forms, such as plumage odor (e.g., 1968, and 1985, and Roper Wenzel and and Birds also have a variety of that produce substances, the uropygial and even and Jacob and Zisweiler 1982, and such as may also secretions and Some compounds have been linked to such as the found in species of the and of as as in of et al. 1992, The in both birds and from those stored in et al. 2004). Alternatively, birds, and compounds similar this that at least species of is considered et al. 2004). of a has been in that produce odorous derived from the and secretions are as a of avian chemical substances, the gland of volatile and compounds in the of that are on as of plumage (Jacob and Zisweiler are to and though the function is Sweeney et al. 2004). Avian uropygial can in and et al. 1991, et al. 1999, et al. et al. 2007). can also (Jacob et al. and and and et al. which that important of to social from studies of the uropygial intraspecific of avian compounds are rarely in the Crested and which exhibit in the chemical substances the of odor of toxins et al. and volatile compounds from plumage (Bonadonna et al. chemical are the et al. Hagelin et al. Bonadonna et al. 2007). for Crested Auklets and also some for Crested Auklets are less odorous and a from at least species (P. with an from the et al. compounds that Crested odor are during the (Hagelin et al. and that odor in and the of Hagelin 2007). Variable and chemical of species have also been to or et al. chemicals from uropygial secretions have been linked to avian such as the of et al. 2004) and and of the species exhibit in the and of uropygial substances, which during the and similar to secretions are also to for the musky plumage of some et al. et al. 2007). The uropygial is not the of avian body bird the gland et al. 2003). in and are in a of birds and Rappole 1997). species have fully functional uropygial produce secretions that are the Crested and Phillips and the Kakapo (Hagelin 2004) emit uropygial secretions that are to with the of C. Hagelin pers. The data that volatile compounds in avian odor may be derived from is of substances in Birds also a diversity of avian microbes on and skin and 1999, et al. and Shawkey et al. which may be in the or of chemical Jacob and Zisweiler that of uropygial secretions from compounds acids and to the musky of Birds may also substances that compounds in Crested odor are similar to those expected during to such in or two major functions of avian compounds defense and intraspecific it is important to a the chemical substances of birds may be the of such as and or other for this is the odor of which has function is to the functional such as to and and a function for avian chemical substances the or does not the Cott the to that respond to chemical substances in Cott that the of some birds less those of to potential or avian species are to produce or substances, during which at and the of and which are an is from the nest studies discuss of avian chemical A common function to uropygial secretions is to and skin of and microbes (Jacob and Zisweiler 1982, Sweeney et al. 2004, et al. compounds a of and (e.g., Jacob et al. and 1999, 2001, et al. Shawkey et al. or have been to a that microbes such as et al. substances that birds may also a similar of as in or in Weldon 2004) or with to (e.g., Clark and Mason 1985, and and Dumbacher and the defense an or or chemical substances that or The authors avian substances as either or those in compounds or a heterospecific is to them at in compounds are substances that in an the in which the chemicals the chemosensory of a The the two types of compounds is not For example, of compounds can also an or in a and for the defense Avian compounds exhibit of a or on predators, or microbes at the an and with less protection themselves with that produce and are to these with the compounds at that are We consider three of chemicals in avian defense. The common and in the for which data are Dumbacher and provide many of species that produce compounds that have been as or to are a many and species have been The genera and of species that compounds et al. 1992, are the to occur in vertebrates and The compounds are and Dumbacher et al. 2004). Hooded and Variable sequester in and and et al. 1992). of animal that are in vertebrate et al. 1992, and can to a in the species, and with a bird can or chemosensory of the trigeminal system, such as and and Dumbacher and Some predators, such as the and also to of the 1999, J. Dumbacher Such that to or skin can an or in at least some vertebrates, which function as an interspecific The two species, Hooded and Variable also emit an or sour odor et al. though the chemical and any function are may from of volatile or from other sources Dumbacher pers. Dumbacher and a of of to for chemical defense and as a signal against vertebrate The two in and plumage which the idea that of plumage may 1994, et al. authors also a of in which two species chemical Dumbacher the of on A of to in that on of Hooded which is with avian compounds a a though the which toxins is The Crested is a that an tangerine-like consisting of and during (Table Douglas et al. 2001, Hagelin et al. 2003). function proposed for the volatile compounds in Crested odor is that ectoparasites, the substances are similar to other found in et al. The is a common with of from to of birds pers. see also Douglas The the and and 2004). has also been in (e.g., Some volatile compounds of Crested plumage odor that exhibit in in et al. the data are from in Hagelin et al. Some volatile compounds of Crested plumage odor that exhibit in in et al. the data are from in Hagelin et al. the of Crested compounds against or other is from of compounds and chemical against both and a Douglas et al. a which the and of a et al. to the of to of with compounds found in Crested a of the of in a et al. which an or also a on two genera of and Douglas et al. which on with chemicals found in Crested Hagelin data on the of Crested plumage Hagelin et al. 2003) to the on and of compounds. Some chemical during to on birds, of at to that of plumage (Hagelin 2007). responses and to are for the Douglas et al. we such the chemical of or on Crested other investigations call the of Crested compounds. First, plumage of not or of et al. to of and in a not plumage (Hagelin 2007). Crested odor is and can in a (Hagelin et al. 2003). The a of it is that odor of plumage have to the of it is to a role to of compounds a Crested in studies of uropygial secretions in et al. 2003). the compounds in Crested against ectoparasites, the is not as is the as as in 1999). or on (e.g., have been et al. Douglas vertebrate have not been though Crested Auklets are and their the and a from their uropygial and in the of and the odor on any it et al. 2004). The behavioral of a stench a chemical defense against vertebrate and and as does the of birds, which of responses or in predators, such as and which in their and have been on predators, though data in et al. that some compounds and the also uropygial secretions, and can which that the two avian may exhibit similar of chemical 17 uropygial compounds in that against and and common avian (e.g., is of chemical substances found on plumage or skin of A from the uropygial gland and 2003) may be for the compounds. the from a uropygial also substances with et al. studies of compounds in chemical defense Dumbacher and that substances have a or on predators, ectoparasites, or of as a chemical defense in the is and of and in some vertebrates, a and the signal of plumage and toxins in plumage can The data for Crested Auklets and are less provide for A of the of chemical defense that predators, or microbes be with of chemical compounds that occur on an The of that are to design and are for of the species and the the of avian chemical defense are also Dumbacher and that chemicals, those of with or social behavior. in birds, in the of in both the Hooded and in the and and 1992, and an chemical defense and a of to of and review in Dumbacher and is that chemical defense the for a or and for other Dumbacher and Roper considered avian odors and other chemical substances in intraspecific to be of the topics in bird biology that has been overlooked is not that intraspecific chemosignals are birds to them et al. Birds commonly which to the chemical compounds of a mate or other (Roper 1999). The a of that a role to chemical substances in both and For example, an odor during the that is to function as a signal and during and of these has been experimentally. to et al. we define chemical communication as the specific or of a chemical The is to as a and is considered to be any chemical compound or that has a social or on the use of social recognize and respond or to the chemical a and the an is important to that the is to any chemical signal (e.g., and 2007). and a as a specific of of in which is similar to the of a or The has been we the original it to testable (e.g., et al. 2003). that ornithologists are just to the of chemical substances in birds, it to any avian as a (Hagelin et al. 2003). we consider the for functions of avian compounds in the intraspecific of birds, to nest and mate signals, and also Hagelin for a of this a to body which is through the of volatile chemical Birds may also chemical the two other taste or trigeminal responses in Roper the to which this is of the have been to studies of individually specific chemical many species produce a musky plumage birds also use to odors (e.g., Nevitt and Bonadonna 2005a, b). The that the function of odor can be two types of responses to a nest odor and odor of and of and from the uropygial and secretions on other in to produce a (Jacob and Zisweiler 1982, et al. 2003). also from the of (Bonadonna et al. 2003a, b). can be and birds to at to which that on chemical that their nest from studies to the that use to their nest 1973, has been to other species (Bonadonna and studies have that of the odor signatures of their and their Bonadonna et al. 2003a, Bonadonna et al. 2004; two Bonadonna et al. Such investigations a the of the two birds the with the of their odorous from at the of of the (Bonadonna et al. and new from which to nest (Bonadonna et al. 2004). Such that to volatile compounds from the rather to with the of the nest of the also volatile chemical for et al. 2003). a to the 1997). can their from that of other et al. which that to the that their odor are to provide protection and are the are et al. 2003). The of the chemical signatures of not that of to their on has a Bonadonna and Nevitt odor in a The a of to use in the bird for a in and plumage odor to the Bonadonna and Nevitt three First, with the of mate odor and that of an to their a which is with the use of body to to a and the of conspecific from an of is in Some chemical of mammals, for example, are the major with which with an chemosignals and and and in and et al. 2005; review in and also occur in birds in and though data in avian are (e.g., et al. et al. 2004, et al. et al. that are and and produce birds to their to with have of compounds on that exhibit chemical signatures that are (Bonadonna et al. 2007). et al. that or in the uropygial secretions of also act as an for birds in the potential for is The chemical of has for such as the in which for and and 1992). or have chemical such or or a to avian and The of an avian linked to a Balthazart and Schoffeniels olfactory and social and Schoffeniels in responses with in the uropygial secretions of (Jacob et al. et al. which that an sense of is for to chemicals and exhibit the which chemical compounds are of this species The social Crested a plumage is with a the in which birds their the of a during The and odor are during in to be a of chemosensory or of other and Hagelin et al. The of Crested Auklets two or Birds their the of a The plumage of this species has a from Hagelin [2007]; and J. C. a Hagelin et al. that Crested Auklets the of plumage and a of compounds from also these and other and not respond to a Hagelin et al. a to Crested the not the social et al. for odor function a similar to that to examine the function of and 1999). Crested Auklets exhibit mate for their and authors to that odor may also serve as an olfactory (e.g., Douglas et al. 2001, Hagelin et al. et al. 2004). Crested with a of two odor compounds and First, both of such with not the of or any other behavior. The at least a social function for Crested odor in which both respond relatively to et al. 2004). of birds also that the of some odor compounds with social C. Hagelin a of the Crested with two compounds found in plumage birds of both such for the from Hagelin [2007]; data from in et al. A of or in the Crested some the role in mate et al. 2004). The chemical clearly not act as a for any of of birds and 1999). may act as a secondary in to or function in with which not Alternatively, odor may not function in and chemical can at Birds in a a at from responses that occur at of on the of such as those et al. odor compounds are to in birds, a for which new are in both and are such as provide new odor body odor or other chemical substances function as a signal during intraspecific of birds, be Mouritsen and Madsen the to the functions of avian chemical defense with intraspecific of to an of a the of chemical protection in et al. chemical in a similar to plumage (e.g., Mouritsen and Madsen that the signal of in be an sour The volatile of uropygial secretions in other avian species, such as and have also been to defense of plumage and skin et al. 2007). the compounds a bird with the of chemical that will be as those with Avian chemical compounds have the potential to signal other of and other substances of birds, as exhibit and Such that compounds provide with an or such as an or social or as in mammals (e.g., and and review in Hagelin 2007). and review of a variety of animal species an point for investigations of avian chemical those to mate substances that such as the odor of avian or have been in intraspecific and 1985, and Roper et al. other vertebrates, compounds with can be of the species, such such as a on and review in 2003). birds, for example, the odors or of or act not as an interspecific defense as an intraspecific that with any adaptive of chemical substances in birds as signals of or of responses to volatile chemicals and other substances that during for example, and to the odor of and 1985, and This is similar to the of to the of their or body odor et al. or to odor a can and a chemical in Roper 1999, Hagelin 2007). studies involve chemical substances, the of can also recognize compounds at the to a of compounds less and et al. also chemical birds have a to or in Roper 1999). to less and in new et al. The of this volatile in a environment et al. responses be expected the compounds an or nest are to or of avian chemosensory are the and of chemical are in other vertebrates (e.g., et al. et al. review in and chemical also in birds, it may how chemical such as odors or other substances with et al. and in Hagelin 2007). of avian compounds have the of the intraspecific body odor or other chemical substances birds are expected to a in investigations have in bird that and to and recognize conspecific with other of volatile chemical during interspecific chemical such as or may also function during intraspecific have not been of avian chemical compounds are and data that of chemical compounds or their are chemical have behavioral in some and in other that birds are and we that it is to that intraspecific compounds will other Avian is and usually on of For example, it is to odor function in Crested Auklets through A may or with other of such as and and odor and other chemical substances be as which birds their environment and other a for studies of avian odor and other chemical any system, compounds in interspecific such as chemical or those as intraspecific signals an of a and a The may involve two or such as and or to of the a on which to Avian chemicals for defense or as an intraspecific signal such as the chemical of the signal it is the and in a the and behavioral or responses of the to the of are to or in the of to either or The of also a A for the of avian odors and other chemical substances (adapted from Hagelin 2007). The can to interspecific signals, such as those in chemical or to intraspecific also of biology through to of chemical any system, can be three the of the signal a of the signal the (e.g., olfactory and and any of the to the signal physiological, of the with the and are to and the of the species are the or in A will common physiological, or to as to the function of avian chemical compounds. that of the data from other vertebrate (e.g., and and and will also provide for studies of are many topics to from studies of Crested has avian compounds can both act as an interspecific of defense against and serve as a intraspecific signal or as proposed Mouritsen and Madsen We also that chemical secretions of some birds we have to find a species that is from predators, or may be informative to chemical provide an or of protection at of the For example, in uropygial secretions have been as a of chemical against in et al. birds may also a of defense to the of et al. or during the The for avian chemical substances as signals or as a are for odor and chemical species to are those that have a chemosensory or produce odors or secretions linked with avian chemosignals as studies have not in which for or and The for example, is a species from in which produce a plumage et al. and a variety of animal studies that investigations of avian chemosignals to mate such as those in species mate and of and other chemical substances may also be to common avian such as or conspecific communication may also occur relatively avian senses and are or sense chemical compounds that birds and the chemical of can be it is to in and function of chemosignals through behavioral similar to those to and other (e.g., et al. in and et al. 2001, and 2007). plumage odor and other avian chemical substances are as an aspect of bird biology that a or adaptive defense and intraspecific communication have attention in though it is to that these are the in which birds use chemical compounds. We with that it is to a for in which avian chemical compounds are research that on and both and promising. For example, the on bird body of odor We that birds have olfactory the of the in volatile chemical and it is such species are to odor is also that birds that have in the of may be to emit odorous substances pers. for example, produce plumage odor and Rappole 1997). of avian chemosensory and are also rarely the three vertebrate taste, and the trigeminal has the data on the other two are Hagelin also out that on the of avian chemosensory are types in the olfactory for example, have been in two and and in to volatile chemical occur in of at least avian species Clark and the are in chemosensory of birds or to avian compounds are also even though the of chemical in other vertebrates can involve and behavioral (e.g., et al. et al. investigations have and in birds and birds a functional system and Wenzel which is considered important for in mammals and other vertebrates (e.g., et al. birds and the which has been to to of the that (e.g., 2007). the function in birds provide for the avian of the has also that birds exhibit a of olfactory some of which are to those in humans (e.g., 2004, et al. out that which are to and occur in both humans and is in fatty and in birds it may of in and avian odor or other secretions et al. 2007). Birds and on and chemosignals and the that them are clearly as an overlooked aspect of our of chemical defense and intraspecific chemosignals in birds have the potential to our of avian biology as as the toxins and et al. the of avian chemosignals is to birds to plumage that humans see et al. 1997). The we have the secretions, and other chemical substances are in birds and derived from a of sources. for avian chemical defense is for our of these and other species will from studies that consider interspecific as as intraspecific for how chemical substances Avian body odors and have been linked to social involving conspecific mate to nest odor and of which involve adaptive behavioral of are inherently interdisciplinary, and the is for investigations that focus on odors or chemical substances at every of avian those that of chemosensory for other animal groups. This is to the of and chemical our to studies of Crested J. C. also for and Wenzel for J. Dumbacher and two important on a of the

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