Comparative biology of aging in birds: an update

D.J. Holmes et al. / Experimental Gerontology 36 (2001) 869±883

Experimental Gerontology 36 (2001) 869±883

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Comparative biology of aging in birds: an update D.J. Holmes a,*, R. FluÈckiger a, S.N. Austad b a

Department of Biological Sciences, University of Idaho, Moscow, ID 83844-3051, USA b Novacule, LLC, 24 Beacons®eld Rd., Brookline, MA 02445, USA

Abstract The long life spans and slow aging rates of birds relative to mammals are paradoxical in view of birds' high metabolic rates, body temperatures and blood glucose levels, all of which are predicted to be liabilities by current biochemical theories of aging. Available avian life-table data show that most birds undergo rapid to slow ªgradualº senescence. Some seabird species exhibit extremely slow agerelated declines in both survival and reproductive output, and even increase reproductive success as they get older. Slow avian senescence is thought to be coupled evolutionarily with delayed maturity and low annual fecundity. Recent research in our lab and others supports the hypothesis that birds have special adaptations for preventing age-related tissue damage caused by reactive oxygen species (ROS) and advanced glycosylation endproducts, or AGEs, as well as an unusual capacity for neurogeneration in brain. Much of this work is in its early stages, however, and reliable biomarkers for comparing avian and mammalian aging need more thorough development. q 2001 Elsevier Science Inc. All rights reserved. Keywords: Aging; Senescence; Birds; Neurogeneration; Reactive oxygen species; Oxidative defenses; Advanced glycosylation endoproducts; Glycosylation

1. The paradox of avian longevity With few exceptions, bird species are strikingly long-lived compared to their mammalian counterparts (Finch, 1990; Holmes and Austad, 1995a,b); many birds live up to three times longer than mammals of equivalent body mass. The slow aging rates typical of the class Aves are paradoxical, given their high metabolic rates (2±2.5 times higher, with lifetime energy expenditures up to 15 times higher), body temperatures (approximately 38C higher), and blood glucose levels (two- to four-fold higher). According to current biochemical theories of aging, elevation of these parameters in birds should contribute to accelerated tissue damage from the accumulation of deleterious by-products of oxidative * Corresponding author. Tel.: 1 1-208-885-2665; fax: 11-208-885-7905. E-mail address: [email protected] (D.J. Holmes). 0531-5565/01/$ - see front matter q 2001 Elsevier Science Inc. All rights reserved. PII: S 0531-556 5(00)00247-3

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metabolism and the Malliard reaction (Harman, 1956; Del Maestro, 1980; Cerami, 1985; Monnier, 1990; Monnier et al., 1991; Kristal and Yu, 1992). Five years ago we offered a prospectus for the use of selected avian models for aging, including a detailed comparative rationale (Holmes and Austad, 1995a,b). We reviewed general features of avian aging, including pathophysiological phenomena of special interest to biogerontologists, discussed natural variation in avian life span and lifetime reproductive patterns as documented up to then, and expanded on the prediction by Monnier et al. (1991) that birds may employ special molecular adaptations to prevent or protect against production of advanced glycosylation endproducts (AGEs) and pro-oxidants. In this paper we will report recent progress in the study of avian aging since then, with an emphasis on ®ndings of particular interest to comparative biogerontologists. 2. How do birds age? Population-level-phenomena Finch (1990) organized aging patterns around three general models: (1) rapid senescence with sudden death; (2) gradual senescence with de®nite (®nite) life span; and (3) negligible senescence. Sexually reproducing ªunitaryº animals (as de®ned by Begon et al., 1990) generally exhibit either the ®rst or second pattern, while negligible senescence tends to be limited to clonally reproducing, ªmodularº organisms. The ®rst theme is characteristic of semelparous animals (vertebrate examples include anadromous salmon and short-lived marsupial ªmiceº (Antechinus sp.)). Birds (class Aves) and other homiothermic vertebrates (including humans and primates) exhibit the second pattern, that of gradual senescence with de®nite life span. Relative to their mammalian counterparts, birds age much more slowly. Among various avian orders, however, there is tremendous variation in aging rates and patterns. Poultry species (order Galliformes), including the most common laboratory bird models, domestic chickens and coturnix quail, are the shortest-lived and most quickly aging birds. On the other end of the spectrum, parrots (order Psittaciformes), seabirds (Charadriiformes), songbirds (Passeriformes), hummingbirds (Apodiformes) and raptors (Falconiformes) all include representatives with exceptionally long life spans and slow aging rates for their body size (Holmes and Austad, 1995a; Table 1). The comparative longevity and slow aging of birds vs. mammals is solidly documented with data from captive zoo and pet birds as well as maximum life-span data from mark± recapture studies of wild birds in nature (Lindstedt and Calder, 1976; Finch, 1990; Holmes and Austad, 1995a,b; Ricklefs and Finch, 1995; Ricklefs, 1998). Over the past decade we have seen a remarkable increase in the number of published reports of demographic data consistent with aging in wild bird populations (see Appendix A for a list of 30 species in nine orders). While only a subset of these reports meets the most stringent standards of actuarial analysis of life-table data (see, for example, Tatar et al., 1993; Vaupel, 1997; Ricklefs, 1998; Carey, 1999; Nisbet, 2001), and we recommend due caution in their interpretation, it seems reasonable now to suppose that measurable senescence (as evidenced by consistently increasing mortality or decreasing fecundity with chronological age) does indeed take place in a number of wild bird populations, as it appears to in mammals (Promislow, 1991). Birds maintained in captivity, moreover, exhibit

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Table 1 Comparison of longevities and lifetime energy expenditures in birds and mammals (c, captive) (revised from Holmes and Austad (1995a)). Data from Welty (1982) unless otherwise noted Species

Body mass (g)

Maximum recorded longevity (years)

Lifetime energy expenditure (kcal/g)

House mouse (Mus domesticus) Human (Homo sapiens) Broad-billed hummingbird (Selasphorus platycercus) Barn swallow (Hirundo rustica) Eurasian gold®nch (Carduelis carduelis) Canary (Serinus canaria) a,b Budgerigar (Melopsittacus undulatus) Scarlet tanager (Piranga olivacea) American robin (Turdus migratorius) Raven (Corvus corax)

20 50 000 5

4(c) 122(c) 14

250 800

16 16

16 27(c)

1440 4000

22 35

24(c) 20(c)

3200

40

9

1030

77

11

1050

1200

69(c)

14 000

a

From Altman and Dittmer, 1972. The apparently longer life spans of commercially bred relative to wild species may be attributed to a larger pool of available data rather than an actual difference. b

aging-related changes that are not qualitatively different from those in mammals Ð they simply occur later or more gradually. Some birds, including captive galliforms like chickens and quail, show comparatively rapid aging quite similar to that in laboratory rodents, in which increases in mortality are preceded or accompanied by obvious reproductive decline (Table 2). This pattern is by no means typical of all avian species, however: representatives of most other orders age more slowly, and some seabirds exhibit exceptionally slow age-related declines in survival (Appendix A). Reliable demographic analyses show very gradual to almost negligible reproductive senescence in certain seabirds, even in those species which show mortality increases with age. In the California Gull, for example, average reproductive success increases for older breeding pairs until they disappear from the breeding population (Pugesek, 1981; Pugesek and Diem, 1990; Pugesek et al., 1995). Recent studies by Nisbet et al. (1999) and Nisbet (2001), moreover, show a distinct lack of endocrine correlates of aging in common terns. Such extremely slow avian aging rates, coupled with nearly negligible reproductive declines, are limited to avian species with life histories characterized by delayed sexual maturation, increasing breeding success with repeated efforts, and very small clutch sizes (e.g. two eggs) throughout the entire breeding life span (Table 2). When protected from natural causes of mortality such as disease, predation and accident, some captive female birds exhibit a postreproductive life span of up 30% of

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Table 2 Age-related parameters from some extreme avian life histories (references: Vom Saal and Finch, 1988; Nisbet et al., 1999; Pugesek, 1981; Pugesek and Diem, 1990; Pugesek et al., 1995; Ottinger, pers. commun.) Species

Age at maturity

Fertility changes/reproductive aging

Life span

Domestic galliforms Chicken Leghorn (egg-layer)

20±22 weeks

300 1 eggs/year; declines rapidly Higher fertility; but declines at 50 1 weeks both sexes Declines . 56 weeks in females; more gradual in males

20 1 years max

Fertility sustained 20 1 years with no measurable decline Increased reproductive success with age; no measurable decline

. 20 years max

Broiler Coturnix quail

Slower maturation (26± 28 weeks); heavier bodies 10±12 weeks

Wild seabirds Common tern

Delayed 3±5 years

California gull

Delayed 3±4 years

6±7 years max

. 25 years max

their maximum life span (vom Saal and Finch, 1988; vom Saal et al., 1994). This female-speci®c decline in fertility seems to be typical of homiothermic vertebrates, whose primary oocytes are formed in embryonic development and undergo gradual deterioration after birth, including most mammals, birds, and some ®shes.

3. Biochemical and physiological aspects of avian aging In the following sections, we brie¯y review recent advances in research on aging in birds. We include studies of avian neuroregeneration, oxidative metabolism and the prevention of its harmful by-products and nonenzymatic glycosylation (see also Austad, 2001; Nisbet, 2001; Ottinger, 2001). 3.1. Neural regeneration Neurobiologists have long used laboratory bird models, especially canaries and zebra ®nches, for studies of social learning and brain development, including age-related deterioration in behavior (for a review, see Konishi et al., 1989). Recent work by Constance Scharff and Fernando Nottebohm at Rockefeller University, in collaboration with Jefferey Macklis in Harvard Medical School, has shown a remarkable capacity for regeneration of neurons related to song production in adult male zebra ®nches (Scharff et al., 2000). Apoptosis (programmed cell death) induced in ®nches' brains resulted in renewed neurogenesis. This ®nding has implications for the restoration of nerve-cell function in humans with Alzheimer's disease and other aging-related brain dysfunction.

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3.2. Oxidative processes 3.2.1. Avian defenses against oxidative damage and aging Most birds process many times more oxygen per gram of tissue in a lifetime than most mammals (Table 1). A large body of evidence indicates that damaging reactive oxygen species (ROS), produced as an inescapable by-product of normal metabolism, contribute signi®cantly to the accumulated cellular damage associated with aging. How do birds avoid or minimize this damage? In principle, two mechanisms could explain the longevity difference between birds and mammals, assuming that oxidative damage is a major challenge to longevity. First, birds might produce fewer ROS per mole of oxygen consumed, as a result of more effective mitochondrial electron transfer. In fact, this seems to be the case. Two laboratories independently found substantially (up to 10-fold) lower production of H2O2 in tissues of pigeons (Columbia livia) compared with tissues from similar-sized Norway rats (Rattus norvegicus) (Ku and Sohal, 1993; Barja et al., 1994). Additionally, birds might possess superior defenses against damage by free radicals. The above-mentioned pigeon±rat comparisons, however, reached opposite conclusions regarding relative activity of antioxidant enzymes. Ku and Sohal (1993) found a general increase in antioxidant enzyme activity, whereas Barja et al., 1994, as well as Herrero and Barja (1988), found a general decrease in these enzymes in pigeons and other long-lived bird species compared with similar-sized mammals. We have determined that avian cells have better resistance to oxidative challenge by directly exposing cultured kidney epithelial cells to various pro-oxidants (95% oxygen, H2O2, and paraquat) and observing that cells from three small long-lived bird species survived better and suffered less DNA damage than did mouse cells (Ogburn et al., 1988). In principle, the defenses we have seen could be structural and constitutive, inducible (as with stress response genes) or both. In support of the notion that structural elements of the cell are important, Pamplona et al. (1996) found that liver mitochondrial membranes were more resistant to lipid peroxidation in pigeons as compared with rats, due to the lower fatty acid unsaturation in those membranes. Furthermore, long-lived parakeets and canaries exhibited similar peroxidation-resistant membranes in heart tissue (Pamplona et al., 1999). However, such ®ndings do not preclude the existence of inducible oxidative defenses. More recently, we have found evidence that embryonic ®broblasts from budgerigars require active gene transcription and translation in order to survive better under oxidative challenge than do ®broblasts of mammals or short-lived birds (Ogburn et al., in prep.). 3.2.2. Antioxidants and avian social evolution Almost 20 years ago, Hamilton and Zuk (1982) suggested that dietary antioxidants like carotenoids might be a reliable correlate of ®tness for birds selecting among potential mates. Specially, they hypothesized that bright plumage in male birds should be attractive to females assessing the genetic quality of perspective mates. This was based on the idea that colorful feather pigments are expensive energetically, and that the ability to produce and maintain bright feathers should be associated with more direct determinants of ®tness, such as diet quality and levels of parasite infestation. The Hamilton±Zuk hypothesis on brightly colored birds and parasitism has generated a tremendous amount of research (for

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reviews, see Hamilton, 1990; Olsen and Owens, 1998; von Schantz et al., 1999), most of which con®rms the original hypothesis. Only recently, however, has the possibility been addressed of a general role of avian antioxidant systems in determining ®tness and longevity in bird populations in nature (see, for example, Surai et al., 1996; Surai and Speake, 1988; Speake, 1999; von Schantz et al., 1999; Blount et al., 2000). Carotenoids, vitamin E and other antioxidant pigments in the yolk of birds' eggs clearly provide protection against lipid peroxidation in young birds, contributing to healthy embryonic development and the maturation of the immune system. Blount et al. (2000) suggested that carotenoid availability may be one of the key energetic bases underlying complex reproductive and life-history trade-offs, and thus an important factor in sexual selection and the evolution of mating and parental care systems. These ecological trade-offs should also be key determinants of variability between species and populations with respect to timing of reproduction, longevity and aging. 3.3. Advanced glycosylation end-products Products of the Maillard reaction (Cerami, 1985; Monnier, 1990; Monnier et al., 1991; Monnier et al., 1999), (glycation or nonenzymatic glycosylation) continue to be used as biomarkers of aging in key tissues in humans and laboratory animals. Following nonenzymatically mediated attachment of glucose to reactive amino groups on proteins in blood and other tissues, glycated sugar±protein residues can react further to form advanced glycosylation end products or ªAGEsº or ªAGEsº (for speci®c structures, see Wells-Knecht et al., 1996), which are thought to cause the age-dependent yellowing and crosslinking of long-lived proteins such as collagen and lens crystallins. AGEs are recognized by cellular receptors, and the AGE-receptor interaction can initiate cellular events that induce the tissue damage characteristic of aging. Since it often involves oxidative steps, and may be synergistic with free-radical damage (Kristal and Yu, 1992) the formation of AGEs is also sometimes referred to as `glycoxidation'. AGEs have now been measured in a few laboratories and in a number of different bird species, including members of very long-lived avian orders (hummingbirds [Apodiformes]: Beuchat and Chong, 1998; budgerigars [Psittaciformes]: R. FluÈckiger, unpublished data), as well as chickens and turkeys, in the relatively short-lived order Galliformes (see, for example, Rendell et al., 1985; Iqbal et al., 1999; Klandorf and Iqbal, 1999). Glycation products assayed to date include pentosidine in skin collagen and glycated hemoglobin. Although the available evidence thus far broadly supports the prediction that birds accumulate AGEs more slowly than mammals, the measurement of these compounds may vary in sensitivity and reliability among laboratories and compounds, and certain AGEs may lend themselves better than others to the comparison of avian and mammalian aging rates. We outline this recent work below, identifying some pitfalls and potential sources of confusion. 3.3.1. AGEs in collagen Pentosidine is an AGE with measurable ¯uorescent properties that forms as a consequence of an interaction of the guanidino group of arginine with fructosyllysine via a mechanism involving an oxidative step (Grandhee and Monnier, 1991). Iqbal, Klandorf

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and coworkers at University of West Virgina Veterinary School have determined that the pentosidine content in collagen of skin in chickens is 1000 times lower than that in mammals (Klandorf and Iqbal, 1999), and they have described a linear trend in accumulation of this crosslink with age (Iqbal et al., 1999; Fig. 1a). In addition, they report experimental reductions in skin pentosidine in chickens which either have been calorically restricted or given aminoguanidine, an AGE inhibitor (Fig. 1b). It should be noted that pentosidine levels will re¯ect oxidative AGE formation only in proteins containing an appropriately located arginine side chain. Moreover, while pentosidine accounts for much of the characteristic yellowing of proteins with age, measurable tissue pentosidine levels account for only a small proportion of glucosederived cross-links in biological samples (Dyer et al., 1991). An AGE crosslink

Fig. 1. (a) Increasing accumulation of pentosidine (Ps) in skin with age in broiler hens fed ad libitum. (b) Effects of 40% diet restriction (DR) and aminoguanidine (AG) on age-associated accumulation of pentosidine in skin of broiler hens. Values represent means ^ standard errors for each experimental group …n ˆ 5†: pp denotes signi®cant differences at that age (2 £ 2 factorial analysis). Aminoguanidine is an inhibitor of pentosidine formation. Reprinted from Iqbal et al., 1999; permission from Copyright Clearance Center, Inc.

876

D.J. Holmes et al. / Experimental Gerontology 36 (2001) 869±883 COOH H CH NH (CH2)4 O2, Men+

H H C OH H C OH

---Lys---

C

C

H C OH

O2,

Men+

C

+

N

HO C

NH

N

C

H2N

H N

N N

(CH2)4

C O HC H

C

CML

---Arg--Pentosidine

---Lys---

NH2 NH

(CH2)4 -3H20 ---Lys---

OH HO C

C

Fructosyllysine

C C

C

C

NH (CH2)4 ---Lys---

N

ALI

N NH (CH2)3 ---Arg---

Fig. 2. Structure and pathways for formation of three advanced glycosylation endproducts (AGEs). Formation of carboxymethyllysine (CML) and pentosidine involves oxidative steps, while marginine±lysine imidazole (ALI) forms non-oxidatively. Aminoguanidine is an inhibitor of pentosidine formation.

identi®ed only recently, arginine±lysine imidazole (ALI), may represent the critical non-¯uorescent, glycation-derived crosslinking compound responsible for the balance of protein yellowing not explained by pentosidine. ALI arises from the interaction of the guanidino group of arginine with fructosyllsine and subsequent dehydrations without an oxidative step (Fig. 2) (Al-Abed and Bucala, 2000). The exact reason for the low pentosidine content of chicken skin collagen, therefore, remains unclear. Collagen protein sequence or structure may differ in birds and mammals, constraining glycosylation reactions involving an arginine side chain and limiting pentosidine formation to a very low level. Alternatively, birds may be protected from glycoxidation by high levels of circulating uric acid, as suggested by Klandorf and Iqbal (1999), since uric acid is a potent hydroxyl radical scavenger and could prevent the oxidative step required for pentosidine to form. To conclusively establish that an adaptive avian strategy exists to combat the deleterious effects of hyperglycemia, it must be shown

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®rst that collagen in skin is capable of being glycated to the same extent as mammalian collagen in the absence of uric acid, and, second, that uric acid can indeed prevent pentosidine formation in vitro. To our knowledge, there has been no completed long-term study (using the standard biogerontological paradigm allowing natural longevity and mortality in the laboratory) on the effects of caloric restriction on longevity, patterns of onset of aging-related diseases, or glycoxidative processes in any bird species.

3.3.2. AGEs and blood proteins Levels of glycated hemoglobin have been determined in a few bird species using either ion exchange or boronate af®nity chromatography (Rendell et al., 1985; Beuchat and Chong, 1998). Data obtained with the latter methodology, which re¯ect more reliably the extent of hemoglobin glycation, show levels of glycohemoglobin to be substantially lower than in mammals. Glycated hemoglobin levels in duck, chicken, and turkey fell in the 0.5±1.0% range, while values for mammals ranged from 1.7 to 5.8%. The only mammal with glycated hemoglobin in the range seen in birds was the pig; this is consistent with the fact that glucose concentrations within pig erythrocytes are lower than in plasma, due to a limited permeability for glucose in this species. Bird erythrocytes (which are nucleated, unlike those of mammals) are not only less permeable to glucose than most mammalian red blood cells, but also have half-lives of 50±70% of mammalian red cells. Comparatively low glucose permeability and short life span of avian erythrocytes should limit the formation and accumulation of glycated hemoglobin in birds. Interpretation of apparent differences in levels of glycated hemoglobin in birds and mammals must be made with these hematological differences in mind. Serum albumin, in contrast, is directly exposed to the prevailing blood glucose, and hence appears to be glycated at comparable rates in chicken and mammals (Rendell et al., 1985). Glycated albumin levels reported for birds were much higher than those in mammals Ð comparable, in fact, to those seen in human diabetic patients with poor therapeutic control of glycemia. But boronate af®nity chromatography can yield erroneously high values when protein is adsorbed nonspeci®cally to the af®nity resin and not eluted with excess competing ligand. This source of error cannot be ruled out in the protocol described by Rendell et al. (1985), in which glycated protein is eluted by lowering the pH. We probed the extent of plasma protein glycation in budgerigars using immunoblast analysis with a polyclonal antibody speci®c to reduced glycated lysine residues (Myint et al., 1995). As expected under the prediction that birds should accumulate much lower levels of AGEs than mammals, this analysis revealed strong immunoreactivity in a sample of human plasma, but only a faint signal for samples from three budgerigars (FluÈckiger, Holmes, and Austad, unpublished). The reason for this apparently low glycation of bird plasma proteins overall is not clear, however Ð particularly in view of the extensive glycation of albumin, the main protein constituent of plasma. Clearly there is a need to reliably and unambiguously determine the

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glycation status of plasma proteins in bird species with varying life spans and aging rates. 3.3.3. Receptor-mediated effects of AGEs: special applicability for bird±mammal comparisons? Interaction of AGEs with their speci®c cellular receptors can cause oxidative stress resulting in changes in gene expression and other cellular attributes that may contribute to the development of age-related vascular lesions. This view was documented elegantly by Yan et al. (1994), who showed that AGE-albumin or other AGEs immunoisolated from diabetic plasma can induce endothelial oxidant stress, activate the nuclear transcription factor, NF-kB, and in turn induce heme oxygenase mRNA. The principal antigenic determinant in AGE-modi®ed proteins is the non-¯uorescent, noncrosslinking carboxymethyllysine, or CML (Ahmed et al., 1986; Reddy et al., 1995) (Fig. 2). CML also activates cell-signaling pathways and modulates gene expression (Kislinger et al., 1999). With their apparently stronger antioxdant defenses, birds may be better able than mammals to limit the consequences of AGE-induced oxidative stress. Not all birds, however, are protected from age-related vascular complications: pigeons and some carnivorous birds develop atherosclerosis (Holmes and Austad, 1995a). It would be interesting to establish whether birds can limit the formation of CML, reducing adverse receptor-mediated cellular effects and, in turn, preventing further oxidative damage that can result in changes in gene expression. 3.3.4. Potential for AGEs as biomarkers in wild bird populations Results of a preliminary study (R. Chaney, M. Iqbal, and H. Klandorf, unpublished data) suggest an association between accumulated skin pentosidine levels and chronological age in captive wild birds when data from 24 individuals from different species are combined in the analysis with no phylogenetic controls. Since skin biopsies can be performed relatively innocuously on live birds, pentosidine measurement Ð if demonstrated to covary reliably with chronological age within a species Ð could prove useful for monitoring aging processes in wild bird populations. Hopefully, selected AGE assays will become standardized for particular applications as their utility for comparative analysis is recognized more widely and more data become available. Appendix A. Reports consistent with avian senescence in wild bird populations Notes: key to abbreviations: AS ˆ actuarial senescence (age-speci®c increases in mortality or decreases in survivorship); RS ˆ reproductive senescence (fecundity declines with age); RE ˆ reproductive effort increases or remains constant with age: PS ˆ other age-speci®c physiological declines. p, a captive study. pp, decrease in male secondary sexual character with age. All data from wild populations unless otherwise noted. c ˆ captive population.

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Order/species Sphenisciformes Little blue penguin Eudyptyla minor Procellariiformes Northern fulmar Fulmaris glacialis Short-tailed shearwater Puf®nus tenuirostris Falconiformes European sparrowhawk Accipiter nisus Peregrine falcon p Falco peregrinus Galliformes Brush Turkey Alectura lathami White-tailed ptarmigan; Willow ptarmigan Lagopus leucurus; L. lagopus Peafowl Pavo cristatus Reeves pheasant Syrmaticus reevesi Charadriformes Temminck's stint Calidris temminekii Common gull Largentus argentatus California gull Larus californicus Kittiwake Rissa tridactyla Common tern Sterna hirundo Arctic tern Sterna paradisaea

879

Age-related References trend AS

Dann and Cullen (1990)

AS;RE

Ollasen and Dunnet (1988) and Finch (1990)

AS: RE

Newton (1989)

AS;RS RS

Newton (1989) and Newton and Rothery (1997) Clum (1995)

AS

Finch (1990) and Ricklefs and Finch (1995)

AS;RS

Weibe and Martin (1998)

AS

Finch (1990)

AS

Finch (1990)

AS

Newton (1989)

AS

Newton (1989)

AS, RE

Pugesek (1981), Pugesek and Diem (1990) and Pugesek et al. (1995)

AS Lack of endocrine aging RS

Aebischer and Colson (1990) Nisbet et al. (1999) and Nisbet (2001) Newton (1989)

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(continued) Order/species

Age-related References trend

Strigiformes Tengmalm's owl Aegiolius funereus

RS

Newton (1989)

Apodiformes Broad-tailed hummingbird Selasphorus platycerus

AS;PS

Newton (1989) and Calder (1990)

Piciformes Acorn woodpecker Melanerpes formicivorous

RS

Koenig and Mumme (1987)

AS

Davies (1992)

AS

Newton (1989)

AS

Gustafsson and PaÈrt (1991)

PS

A. Coburn, pers. commun.

Passeriformes Dunnock Prunella modularis Pied ¯ycatcher Ficedula hypoleuca Collared ¯ycatcher Ficedula albicollis Splendid fairy wren Malurus sp. Florida scrub jay Aphelocoma caerulescens Pinyon jay Gymnorhinus cyanocephalis Black-capped chickadee Parus airicapillus Great tit Parus major Barn swallow Hirundo rusticus Junco Junco hyemalis Bengalese ®nch (c) Loncura striata

AS;RS;PS Woolfenden and Fitzpatrick (1990) and MacDonald, unpublished AS Marzluff and Balda (1990) AS

Loery et al. (1987)

AS;RS AS;RS pp

McCleery and Perrins (1988), Newton (1989) and Holmes and Austad (1995b) Mùller and DeLope (1999)

PS

E. Ketterson, pers. commun.

AS;RS

Eisner and Etoh (1967) cited in Finch (1990)

References Aebischer, N.J., Colson, J.C., 1990. Survival of the kittiwake in relation to sex, year, breeding experience and position in the colony. J. Anim. Ecol. 59, 1063±1071.

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