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Detecting and measuring senescence in wild birds: experience with long-lived seabirds
I.C.T. Nisbet / Experimental Gerontology 36 (2001) 833±843
Experimental Gerontology 36 (2001) 833±843
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www.elsevier.nl/locate/expgero
Detecting and measuring senescence in wild birds: experience with long-lived seabirds I.C.T. Nisbet* I.C.T. Nisbet and Company, 150 Alder Lane, North Falmouth, MA 02556, USA
Abstract This paper points out and discusses several practical and methodological problems that arise in attempts to detect and measure senescent declines in survival or breeding performance of wild animals, with speci®c emphasis on long-lived seabirds. Birds have no anatomical markers of age, so studies of age-related biology require marking individuals at the time of hatching and following them throughout their lives. Seabirds live longer than the working lifespan of biologists, and longer than the turnover times of study techniques or theories of senescence. Seabirds are exposed to changing environmental and demographic conditions and cannot be assumed to be in demographic equilibrium. Sample sizes of the oldest age-classes are always small, requiring either marking very large numbers of birds at hatching or continuing studies of old birds over many years. Incomplete sampling requires the use of mark-recapture models that have only been developed in the last 20 years. Mortality selection resulting from demographic heterogeneity (selective survival of high-quality individuals) can offset or confound the effects of senescent changes within individuals. Many of these problems are amenable to solution and will be probably solved within a few years. In the meantime, this paper recommends that reviewers should be cautious about accepting published reports of senescent declines in natural populations. q 2001 Elsevier Science Inc. All rights reserved. Keywords: Common tern; Seabird; Reproduction; Senescence; Sterna hirundo; Survival
1. Introduction 1.1. Senescence Senescence is de®ned as ªage-related changes in an organism that adversely affect its vitality and functions, but most importantly, increase the mortality rate as a function of timeº (Finch, 1990). Although senescence in this sense is relatively easy to detect and has * Tel./fax: 11-508-564-4958. E-mail address: [email protected] (I.C.T. Nisbet). 0531-5565/01/$ - see front matter q 2001 Elsevier Science Inc. All rights reserved. PII: S 0531-556 5(00)00244-8
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Fig. 1. Common terns (Sterna hirundo). Photograph by F.D. Atwood.
been well documented in humans and in domestic and laboratory animals, it is more dif®cult to detect and measure in animals under natural conditions, especially longlived animals. Although individual organisms can be marked and their ªvitality and functionsº measured at intervals throughout their lives, these measurements are necessarily made under different circumstances and are not necessarily quantitatively comparable. ªMortality rateº is a property of a population and cannot be measured within an individual, so that detection of an increase in mortality rate requires population-based sampling and statistical modeling (Lebreton et al., 1992; Nichols, 1992). Although some reviews have concluded that senescent increases in mortality rates are characteristic of wild bird and mammal populations (Promislow, 1991; Holmes and Austad, 1995), others have pointed out methodological problems and have concluded that the evidence is limited and equivocal (Gaillard et al., 1994; Nichols et al., 1997). This paper discusses some of these methodological issues and assesses recent data on long-lived birds, speci®cally seabirds. It includes illustrative examples from a long-term study of common terns Sterna hirundo. 1.2. Characteristics of seabirds Birds are generally longer-lived than mammals of comparable sizes, and seabirds are especially long-lived among birds (Holmes and Austad, 1995). Most seabirds breed colonially on islands or cliffs and return to the same sites for many years or throughout their lives, often with the same mates (Wooller et al., 1992), so that it is relatively easy to locate and study marked individuals when they are breeding and to measure their reproductive performance. However, most seabirds disperse at sea after the breeding season and/or migrate to distant areas, so that it is dif®cult to locate individuals during the non-breeding season or to document deaths. Hence, estimation of survival rates is always based on statistical sampling of birds at the breeding sites in successive years.
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1.3. Case study The common tern (Fig. 1) is a small (120 g) seabird with an annual adult survival rate of about 0.90 21 year, age at ®rst breeding 2±5 year, median age of breeders 9±10 year, 95th percentile age 18 year, and maximum recorded age 26 year (Nisbet, unpublished data). It is a long-distance migrant, breeding in the North Temperate Zone and wintering in the Southern Hemisphere (Cramp, 1985); birds in this study breed at about 428 N latitude in the northeastern USA and winter mainly at 31±378 S in southern Brazil and northern Argentina (Hays et al., 1997), requiring a journey of at least 8000 km twice each year. Like other small birds, the common tern has high body temperature, high metabolic rate, rapid heart rate, and high blood glucose concentration (Ricklefs and White, 1981; Klaassen, 1994; WuÈrm and HuÈppop, 1998; Galbraith et al., 1999; Pokras, personal communication). This study was conducted mainly at Bird Island, Massachusetts, USA (41840 0 N, 70843 0 W), and more recently at a second site at Ram Island, 10 km SW of Bird Island. Numbers of common terns breeding at Bird Island increased from about 500 in 1970 to about 4500 in 1992, when they began to spread to Ram Island; the total number at the two sites is not about 8500 (Harlow, 1995; Nisbet, unpublished data). About 60,000 chicks have been banded since 1975, and about 2500 birds of known age (range, 2±25 year) are now breeding at the two sites. Studies of known-aged birds have included measurements of reproductive performance (Nisbet et al., 1984), endocrine function (Nisbet et al., 1999), ®eld metabolic rates and energy ef®ciency (Galbraith et al., 1999). Other studies in progress or recently completed include measurements of age-speci®c reproductive effort, hematology, behavior, immune function, and collagen cross-linking (Nisbet et al., unpublished data). This paper emphasizes recent studies of reproductive performance and survival (Nisbet, unpublished data).
2. Changes that occur on time-scales shorter than the lifetimes of the birds 2.1. Changes in the study populations and their environments Although the common tern has a lifespan of about 25 year, it is relatively short-lived compared to other seabirds. Albatrosses and fulmars, for example, have been recorded living up to 50±60 year, and their theoretical lifespans (99th percentile age based on average survival rate) approach or exceed 100 year (Buckland, 1982; Jouventin and Weimerskirch, 1991; Sagar et al., 2000). Within such long time-scales, many or most populations change through demographic or ecological processes. For example, my study population of common terns has increased by a factor of 15±20 during the period of study, has spread from one to two sites and has started to spread to others, and many aspects of its reproductive performance have deteriorated, perhaps as a result of density-dependent processes (see Nisbet et al., 1984; Galbraith et al., 1999). Other study populations of seabirds have changed during the decades of study (Nisbet, 1989; Harris et al., 1994), or their environment has changed in ways that have led to ¯uctuations or long-term changes in survival or reproductive performance (e.g. Aebischer, 1986; Thomas and Coulson, 1988; Jouventin and Weimerskirch, 1991; Fairweather and Coulson, 1995). In
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still other cases, ¯uctuations in the environment associated with ENSO (El NinÄo Ð Southern Oscillation) or other climatic events have led to periodic or irregular ¯uctuations in survival and/or reproductive performance of seabirds (Boekelheide and Ainley, 1989; Ainley and Boekelheide, 1990; Harris et al., 1994; Brichetti et al., 2000). These changes take place on time-scales of 3±30 year, well within the lifespans of the birds and of study programs (Nisbet, 1989). Hence, many or most seabird populations are in a dynamic or unstable relationship to their environments, so that assumptions of ecological or demographic stability are inappropriate (Nisbet, 1989). 2.2. Changes in the observers and in study programs The time-scales of 20±100 year for turnover of seabird populations are longer than the working lifespans of 3±30 year for most seabird biologists (Nisbet, 1989). Seabird biologists themselves suffer from senescence (see Frontispiece in Clutton-Brock, 1988) and cannot be relied on to produce reliable, comparable data for .30 year. Hence, most studies of long-lived seabirds require a succession of principal investigators (e.g. Sagar et al., 2000) if they are to be continued effectively. Investigators are dif®cult to replace, because long-term funding is rarely available, and individuals willing to commit their professional careers to long-term, under-funded studies are rare and idiosyncratic (Nisbet, 1989). Under these circumstances, it is dif®cult to maintain continuity of study techniques and data management (Nisbet, 1989). Techniques of study turn over even more rapidly than investigators. The case study of common terns was started in 1970, before the era of personal computers or the development of user-friendly database programs. Durable markers for terns did not become available until 1975 (Nisbet and Hatch, 1988), and internal markers (implanted transponders) were not tested on terns until 1992 (Becker and Wendeln, 1997). Statistical techniques for capture-mark-recapture modeling were not developed suf®ciently for use in studying survival of seabirds until the 1980s (Clobert et al., 1987) and did not come into wide use until the 1990s (Lebreton et al., 1992); they are still under development (Burnham and Anderson, 1998). Looking ahead 30 more years, it is likely that present-day techniques of marking and aging birds and of analyzing data will be superseded many times over. For example, a technique that would render all present-day methods for sampling obsolete would be the development of implanted transmitters (or receivers) that would record the location and physiological state of an individual bird throughout its annual cycle or its lifetime. Such techniques are already available for large seabirds (Weimerskirch et al., 1993) and it seems unlikely that it would take even 10 year to modify them for use on small seabirds. Statistical techniques for modeling survival and other demographic parameters in wild animal populations are also in a very rapid state of development (Burnham and Anderson, 1998). 2.3. Changes in scienti®c knowledge about senescence Knowledge about senescence and hypotheses about mechanisms that drive it are also developing very rapidly. Few, if any, of the ideas presented and discussed at this Symposium had been formulated when my study started in 1970. Even a relatively short-duration
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study such as the three-year cross-sectional study of survival conducted by Nisbet and Cam (unpublished data) could not be completed and published before a new set of hypotheses about mechanisms of senescence had been formulated.
3. Methodological issues in sampling open populations 3.1. Marking and recapture Birds have no anatomical markers of age, so identifying birds of known age for study requires that they were banded or otherwise individually marked in the year of hatching. This is an enormous disadvantage of birds as model organisms: it requires that studies must continue for at least the lifetimes of the oldest individuals before any information relevant to senescent declines can be collected. Although most seabirds breed colonially and chicks can be banded in large numbers (and often are for other study purposes, or by amateur banders), the proportion that survives to breed is usually low; in many species these survivors disperse among widely separated sites, so that they are dif®cult to ®nd and study. Many studies of age-related biology in seabirds bypass this problem by marking birds when they ®rst breed, and using elapsed time since ®rst breeding as a surrogate measure of chronological age (e.g. Bradley et al., 1989; Aebischer and Coulson, 1990). However, age at ®rst breeding is variable, and birds that start to breed at different ages may differ in other characteristics that in¯uence their breeding performance or survival later in life (Ainley et al., 1990). Finding birds of known age usually requires capturing them to read bands. Although many seabirds are relatively easy to catch at the nest, ®nding small numbers of known-aged birds scattered among large numbers of unknown-aged birds is often labor-intensive and disruptive to the birds. In some cases, marking birds with unique combinations of color-bands has proved to be an ef®cient way to ®nd and identify known-aged individuals without the necessity for trapping them (Cam et al., 1998; Cam and Monnat, 2000; Ratcliffe 1993). However, color-bands are less permanent than bands made of durable metal alloys, and are sometimes lost or cause injuries; we have not been able to use them on terns for these reasons (Nisbet, 1991; Spendelow et al., 1994). Whatever bands are used, there is a possibility that a few of the birds may be caught by humans and the bands removed (as demonstrated for terns wintering in Africa by Becker and Wendeln, 1996). For this reason, Becker and Wendeln (1997) switched to using implanted transponders for permanent marking of individuals, but this has the disadvantage that the transponders can only be read using an antenna within a few centimeter of the bird. This either requires catching all birds, or placing transmitters at all nests, which is only practicable in small colonies. Whatever techniques are used to mark and relocate the birds, the proportion of marked birds that is found each year is usually less than 1. Even if all birds at a site are trapped or otherwise checked every year, in most seabird species the proportion that breeds in a given year is usually less than 1, frequently much less and often variable from year to year (Cam et al., 1998; Bradley et al., 2000).
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3.2. Accounting for incomplete recaptures For measuring age-speci®c reproductive performance, it may not matter much that some individuals are not found in one or more of the years of study. In fact, several long-term studies of seabirds have yielded strong evidence of declines in reproductive performance among the oldest birds (Reilly and Cullen, 1981; Thomas and Coulson, 1988; Mills, 1989; Pugesek and Diem, 1990; Wooller et al., 1990), even though some of the same studies have not provided conclusive evidence of senescent declines in survival. Studies of age-related reproductive performance are subject to bias, however, because the individuals that skip breeding in a given year tend to be the individuals with constitutionally lower breeding performance (Cam et al., 1998). For investigating age-speci®c survival, it is essential to estimate the recapture probability and (unless it is very close to 1) to incorporate it into estimates of survival. In the ®rst step in estimating survival, N1 animals are marked in year 1 and N2 of them are recaptured in year 2. The ratio N2/N1 yields an estimate of a quantity S12 p2, the product of S12, the survival probability between years 1 and 2, and p2, the recapture probability in year 2. In earlier studies, it was often assumed that p2 was equal to 1, on the basis of a subjective evaluation of the diligence and ef®ciency of the observer (but ignoring or overlooking the possibility of temporary non-breeding or temporary emigration). This assumption always leads to a downwards-biased estimate of S12. Although a few cases have been reported in which p2 was actually close to 1 (e.g. Cam et al., 1998), this can never be known a priori, so it is always desirable to estimate this parameter. A second pitfall of assuming that p2 is equal to 1 is that survival probabilities are further underestimated in the last year of the study, because birds that are alive but skip breeding or are overlooked in the last year are then classi®ed as dead. Because the last year of the study usually includes disproportionate numbers of the oldest birds, this can lead to a spurious appearance of a decline in survival among the oldest birds. In the notation of Ricklefs (2000), assuming that p2 is equal to 1 can lead to underestimation of a and overestimation of b . A third pitfall of assuming that p2 is equal to 1 is that the precision of estimates of S12 is then overstated, because uncertainty in p2 contributes to the variance in S12. The only way in which unbiased estimates of S12 can be obtained is to repeat the sampling at a third time interval (in year 3, in most mark-recapture studies). This yields independent estimates of S12 and p2 (and their standard errors), plus another unresolvable product S23 p3 for years 2±3. A fourth year's sampling yields estimates of parameters for two years, a ®fth year's sampling for three, and so on. This general procedure of capturemark-recapture modeling has been formalized and extended for many types of application (Nichols, 1992; Lebreton et al., 1992). It is now widely used, but most estimates of survival of birds published before about 1990 did not use this method and hence are potentially biased. As an example of the importance of using formal procedures, Pugesek and Diem (1990) reported survival estimates of known-aged California gulls (Larus californicus) in relation to prior breeding activity; the estimation procedure involved the assumption that p2 was equal to 1. Data from the same study were later analyzed by Pugesek et al. (1995), who reported modeled estimates of p2 that were strongly age-dependent, ranging from 0.54 to 0.90. Although both analyses showed a decline in survival probability with age, the later,
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more rigorous analysis yielded higher estimates of survival probability at all ages, with the decline manifested only among the oldest age-classes ($15 year). 3.3. Separating effects of age and time An unavoidable problem in investigations of senescence in wild animal populations in that sample sizes in the oldest age-classes that are of primary interest are much smaller than those in earlier age-classes. Most studies of seabirds that have reported age-related declines in survival or breeding success documented these declines only among the oldest individuals Ð typically, the oldest 5±10% of the population (e.g. Bradley et al., 1989; Pugesek et al., 1995). The only ways to overcome this problem of dwindling numbers are either (a) to start with extremely large numbers of marked birds at the time of hatching or ®rst breeding, or (b) to continue the study over several years. The ®rst may be impractical (see Section 3.4); the second runs the risk of confounding effects of age and time. In several studies, variations in survival rate from year to year were as large as differences between young and old birds (e.g. Harris et al., 1994; Ratcliffe 1993). In at least two studies (Aebischer and Coulson, 1990; Weimerskirch, 1992) survival rates declined for all age-classes in the later years of the study because of changes in the environment. Because older birds were more frequent in the later years of each study, this opened the possibility of confounding between time-related and age-related declines in survival. Although modeling techniques are available for separating age and time effects (e.g. Harris et al., 1994; Ratcliffe 1993), they have not often been used. 3.4. Selecting sample sizes It is axiomatic that using larger sample sizes increases precision, other factors being equal. However, choice of sample sizes in seabird research is sometimes constrained by the characteristics of the seabird population. In large colonies, it is generally impractical to mark all individuals or to recapture all individuals that are marked. Even if a large number of individuals are recaptured, low recapture rates contribute to the variance in estimates of survival rate and may offset the gains from large sample sizes (as in my study of common terns: Nisbet, unpublished data). Some of the best studies of age-speci®c survival in seabird populations have been conducted in small colonies including only a few hundred birds (e.g. Bradley et al., 1989; Aebischer and Coulson, 1990). Although it is possible in these circumstances to check all individuals attending the colony in each year (even individuals that visit nest-sites but do not breed: Bradley et al., 2000), it is necessary to continue studies in small colonies for many years to obtain suf®cient data on old birds, because only a handful of old birds is present in any one year (see previous paragraph). More serious, small colonies may not be demographically representative of the larger populations within which they occur. It is extremely unlikely that births and deaths within a small colony will be exactly balanced over a long period, so that emigration and immigration may be disproportionately important in small colonies. For all these reasons, designing studies of age-speci®c survival involves complex trade-offs between colony sizes, sample sizes, marking techniques, study durations, and precision.
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4. Demographic heterogeneity and mortality selection A ®nal problem in all studies of senescence arises from demographic heterogeneity. If groups of individuals within the population differ constitutionally in their risks of death, and if these differences are manifested throughout life, the groups with the lowest mortality risk will be disproportionately represented among those that survive to old age, as a result of selective survival. If the heterogeneity is suf®ciently great, it may reduce or negate the effects of senescent increases in the probability of death within individuals (Vaupel and Yashin, 1985). This phenomenon is well known among human demographers (Vaupel and Yashin, 1985) and experimental gerontologists (Carey et al., 1992; Tatar et al., 1993), but has only recently attracted the attention of ®eld biologists and evolutionary biologists (McDonald et al., 1996; Nichols et al., 1997; Cam and Monnat, 2000; Service, 2000). Although it is possible to separate the effects of demographic heterogeneity and mortality selection in circumstances where complete survival histories are known for all individuals (e.g. in human demography), modeling tools are not yet available to do this in populations of wild animals where the recapture probabilities are less than 1 (Cam, personal communication). Demographic heterogeneity is not only important in investigations of age-speci®c survival. It can also offset (or augment) the effects of senescent decline in other performance parameters, including reproductive performance. If other phenotypic characteristics (e.g. those that determine breeding performance) are also heterogeneous within the population and are correlated with mortality risks, then the individuals that survive to old age may be those with constitutionally higher (or lower) breeding performance. For example, if groups of individuals with high survival probabilities also have high probabilities of successful reproduction (positive phenotypic correlation), the individuals that survive to old age will include disproportionate numbers of individuals with above-average reproductive performance. This phenomenon could offset or appear to reverse the effects of senescent decline in reproductive ef®ciency. For example, in my study of common terns, breeding performance continued to increase with age up to and probably beyond the 95th percentile age in the local population (Nisbet, unpublished data). This trend, however, was only measured in a cross-sectional study (birds of different ages compared in the same year). It is not inconsistent with the hypothesis of senescent decline in ef®ciency within individuals, if that decline were offset by selective survival of individuals with constitutionally high ef®ciency. In the ecological literature, such individuals are referred to as being of high individual `quality' (Nisbet et al., 1998; Wendeln and Becker, 1999). Many studies of seabirds have indicated that individuals of high quality (as de®ned by reproductive performance) survive better than individuals of low quality (i.e. positive phenotypic correlation: Richdale, 1949; Potts, 1969; Reilly and Cullen, 1981; Ollason and Dunnet, 1988; Thomas and Coulson, 1988; Bradley et al., 1989; Mills, 1989; Cam and Monnat, 2000). Thus, mortality selection appears to be pervasive in long-lived seabirds and may be a major in¯uence on apparent trends in reproductive performance among the older age-classes. A theoretical way to separate the effects of mortality selection and senescence in in¯uencing breeding performance is to conduct longitudinal studies within individuals. This has been attempted in several studies of seabirds (e.g. Thomas and Coulson, 1988;
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Bradley et al., 1989; Wooller et al., 1990). However, it is dif®cult or impossible to control such studies for possible effects of changes in the environment. 5. Concluding comments This paper has pointed out several practical and methodological problems that arise in ®eld studies that attempt to detect and measure senescent declines in survival or breeding performance of wild birds or other animals. This area of study is in a state of rapid change and new tools for investigating senescence are constantly being developed. Many of the problems are amendable to solution and will probably be solved within a few years. In the meantime, however, I recommend that reviewers should assess published results critically, should be cautious about accepting published reports of senescent declines in natural populations, and should be especially cautious about accepting published reports of patterns or rates of decline. References Aebischer, N.J., 1986. Retrospective investigation of an ecological disaster in the shag. Phalacrocorax aristotelis: A general method based on long-term marking. J. Anim. Ecol. 53, 613±629. Aebischer, N.J., Coulson, 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. Ainley, D.G., Boekelheide, R.J. (Eds.), 1990. Seabirds of the Farallon Islands, Ecology, Dynamics, and Structure of an Upwelling-System Community Stanford University Press, Stanford, CA. Ainley, D.G., Ribic, C.A., Wood, R.C., 1990. A demographic study of the South Polar skua (Catharacta mccormicki) at Cape Crozier. J. Anim. Ecol. 59, 1±20. Becker, P.H., Wendeln, H., 1996. Ring removal in terns caught in Africa Ð a major problem for population studies. Ring. Migr. 17, 31±32. Becker, P.H., Wendeln, H., 1997. A new application for transponders in population ecology of the common tern. Condor 99, 534±538. Boekelheide, R.J., Ainley, D.G., 1989. Age, resource availability, and breeding effort in Brandt's cormorant. Auk 106, 389±401. Bradley, J.S., Wooller, R.D., Skira, I.J., Serventy, D.L., 1989. Age-dependent survival of short-tailed shearwaters Puf®nus tenuirostris. J. Anim. Ecol. 58, 175±188. Bradley, J.S., Wooller, R.D., Skira, I.J., 2000. Intermittent breeding in the short-tailed shearwater Puf®nus tenuirostris. J. Anim. Ecol. 69, 639±650. Brichetti, P., Foschi, U.F., Boano, G., 2000. Does El NinÄo affect survival rate of Mediterranean populations of Cory's shearwater? Waterbirds 23, 147±154. Buckland, S.T., 1982. A mark-recapture survival analysis. J. Anim. Ecol. 51, 831±847. Burnham, K.P., Anderson, D.R., 1998. Model Selection and Inference. A Practical Information-Theoretic Approach. Springer, New York. Cam, E., Monnat, J.-Y., 2000. Apparent inferiority of ®rst-time breeders in the kittiwake: the role of heterogeneity among age classes. J. Anim. Ecol. 69, 380±394. Cam, E., Hines, J.E., Monnat, J.-Y., Nichols, J.D., Danchin, E., 1998. Are adult nonbreeders prudent parents? The kittiwake model. Ecology 79, 2917±2930. Carey, J.R., Liedo, P., Orozco, D., Vaupel, J.W., 1992. Slowing of mortality rates at older ages in large med¯y cohorts. Science 258, 457±461. Clobert, J., Lebreton, J.-D., Allaine, D., 1987. A general approach to survival rate estimation by recaptures or resightings of marked birds. Ardea 78, 133±142.
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I.C.T. Nisbet / Experimental Gerontology 36 (2001) 833±843
Clutton-Brock, T.H. (Ed.), 1988. Reproductive Success: Studies of Individual Variation in Contrasting Breeding Systems University of Chicago Press, Chicago, IL. Cramp, S. (Ed.), 1985. The Birds of the Western Palearctic, vol. IV. Oxford University Press, Oxford. Fairweather, J., Coulson, J.C., 1995. The in¯uence of forced site change on the dispersal and breeding of the black-legged kittiwake (Rissa tridactyla). Colon Waterbirds 18, 30±40. Finch, C.E., 1990. Longevity, Senescence, and the Genome. University of Chicago Press, Chicago, IL. Gaillard, J.-M., Allaine, D., Pontier, D., Yoccoz, N., Promislow, D.L., 1994. Senescence in natural populations of mammals: a reanalysis. Evolution 48, 509±516. Galbraith, H., Hatch, J.J., Nisbet, I.C.T., Kunz, T.H., 1999. Age-speci®c reproductive ef®ciency among breeding common terns Sterna hirundo: measurement of energy expenditure using doubly-labelled water. J. Avian. Biol. 30, 85±96. Harlow Jr., R.A., 1995. Ram island: recovery in progress. Bird Observer 23, 333±338. Harris, M.P., Buckland, S.T., Russell, S.M., Wanless, S., 1994. Year- and age-related variation in the survival of adult European shags over a 24-year period. Condor 96, 600±605. Hays, H., DiCostanzo, J., Cormons, G., Antas, P.de T.Z., Nascimento, J.do, Nascimento, I.de L.S.do, Bremer, R.E., 1997. Recoveries of roseate and common terns in South America. J. Field Ornithol. 68, 79±90. Holmes, D.J., Austad, S.N., 1995. Birds as animal models for the comparative biology of aging: a prospectus. J. Gerontol. 59A, B59±B66. Jouventin, P., Weimerskirch, H., 1991. Changes in the population size and demography of southern seabirds: management implications. In: Perrins, C.M., Lebreton, J.-D., Hirons, G.J.M. (Eds.). Bird Population Studies: Relevance to Conservation and Management. Oxford University Press, Oxford, pp. 297±316. Klaassen, M., 1994. Growth and energetics of tern chicks from temperate and polar environments. Auk 111, 525±544. Lebreton, J.-D., Burnham, K.P., Clobert, J., Anderson, D.R., 1992. Modeling survival and testing biological hypotheses using marked animals: a uni®ed approach with case studies. Ecol. Monogr. 62, 67±118. McDonald, D.B., Fitzpatrick, J.W., Woolfenden, G.E., 1996. Actuarial senescence and demographic heterogeneity in the Florida scrub jay. Ecology 77, 2373±2381. Mills, J.A., 1989. Red-billed Gull. In: Newton, I. (Ed.). Lifetime Reproductive Success. Academic Press, London, pp. 387±404. Nichols, J.D., 1992. Capture±recapture models using marked animals to study population dynamics. BioScience 42, 94±102. Nichols, J.D., Hines, J.D., Blums, P., 1997. Tests for senescent decline in annual survival probabilities of common pochards, Aythya ferina. Ecology 78, 1009±1018. Nisbet, I.C.T., 1989. Long-term ecological studies of seabirds. Colon. Waterbirds 12, 143±147. Nisbet, I.C.T., 1991. Problems with Darvic color-bands on common terns: band losses and foot injuries. N. Am. Bird Bander. 16, 61±63. Nisbet, I.C.T., Hatch, J.J., 1988. Durability of incoloy bands on common terns. Colon. Waterbirds 11, 113±114. Nisbet, I.C.T., Winchell, J.M., Heise, A.E., 1984. In¯uence of age on the breeding biology of common terns. Colon. Waterbirds 7, 117±126. Nisbet, I.C.T., Spendelow, J.A., Hat®eld, J.S., Zingo, J.M., Gough, G., 1998. Variations in growth of roseate tern chicks: II. Early growth as an index of parental quality. Condor 100, 305±315. Nisbet, I.C.T., Finch, C.E., Thompson, N., Russek-Cohen, E., Proudman, J.A., Ottinger, M.A., 1999. Endocrine patterns during aging in the common tern (Sterna hirundo). Gen. Comp. Endocrinol. 114, 279±286. Ollason, J.C., Dunnet, G.M., 1998. Variation in breeding success in fulmars. In: Clutton-Brock, T.H. (Ed.). Reproductive Success: Studies of Individual Variation in Contrasting Breeding Systems. University of Chicago Press, Chicago, IL, pp. 263±278. Potts, G.R., 1969. The in¯uence of eruptive movements, age, population size and other factors on the survival of the shag (Phalacrocorax aristotelis (L.)). J. Anim Ecol. 38, 53±102. Promislow, D.E.L., 1991. Senescence in natural populations of mammals: A comparative study. Evolution 45, 1865±1877. Pugesek, B.H., Diem, K.L., 1990. The relationship between reproduction and survival in known-aged California gulls. Ecology 71, 811±817. Pugesek, B.H., Nations, C., Diem, K.L., Pradel, R., 1995. Mark-resighting analysis of a California gull population. J. Appl. Statist. 22, 625±640.
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Ratcliffe, N., 1993. The age speci®c breeding performance of great skuas on Shetland. Unpublished Ph.D. thesis, University of Glasgow, Glasgow, UK. Reilly, P.N., Cullen, J.M., 1981. The little penguin (Eudyptula minor) in Victoria. II. Breeding. Emu 81, 1±19. Richdale, L.E., 1949. A study of a group of penguins of known age. Biol Monogr. 1, 1±88 (Otago Daily Times and Witness Newspapers, Dunedin, New Zealand). Ricklefs, R.E., 2000. Intrinsic aging-related mortality in birds. J. Avian. Biol. 31, 103±111. Ricklefs, R.E., White, S.C., 1981. Growth and energetics of the sooty tern (Sterna fuscata) and the common tern (Sterna hirundo). Auk 98, 361±378. Sagar, P.M., Molloy, J., Weimerskrich, H., Warham, J., 2000. Temporal and age-related changes in survival rates of southern Buller's albatrosses (Thalassarche bulleri bulleri) at The Snares, New Zealand. Auk 117, 699± 708. Service, P.M., 2000. Heterogeneity in individual mortality risk and its importance for evolutionary studies of senescence. Am. Nat. 156, 1±13. Spendelow, J.A., Burger, J., Nisbet, I.C.T., Nichols, J.D., Hines, J.E., Hays, H., Cormons, G.D., Gochfeld, M., 1994. Sources of variation in loss rates of color bands applied to adult roseate terns (Sterna dougallii) in the western North Atlantic. Auk 111, 879±885. Tatar, M., Carey, J.R., Vaupel, J.W., 1993. Long-term cost of reproduction with and without accelerated senescence in Callosobruchus maculatus: Analysis of age-speci®c mortality. Evolution 47, 1302±1312. Thomas, C.S., Coulson, J.C., 1988. Reproductive success of kittiwake gulls (Rissa tridactyla). In: Clutton-Brock, T.H. (Ed.). Reproductive Success: Studies of Individual Variation in Contrasting Breeding Systems. University of Chicago Press, Chicago, IL, pp. 251±262. Vaupel, J.W., Yashin, A.I., 1985. Heterogeneity's ruses: Some surprising effects of selection on population dynamics. Am. Statist. 39, 176±185. Weimerskirch, H., 1992. Reproductive effort in long-lived birds: Age-speci®c patterns of condition, reproduction, and survival in the wandering albatross. Oikos 64, 464±473. Weimerskirch, H., Salamolard, M., Sarrazin, F., Jouventin, P., 1993. Foraging strategy of wandering albatrosses through the breeding season: A study using satellite telemetry. Auk 110, 325±342. Wendeln, H., Becker, P.H., 1999. Effects of parental quality and effort on the reproduction of common terns. J. Anim. Ecol. 68, 205±214. Wooller, R.D., Bradley, J.S., Skira, J.J., Serventy, R.D., 1990. Reproductive success of short-taited shearwaters Puf®nus tenuirostris in relation to their age and breeding experience. J. Anim. Ecol. 59, 161±170. Wooller, R.D., Bradley, J.S., Croxall, J.P., 1992. Long-term population studies of seabirds. Trends Ecol. Evol. 7, 111±114. WuÈrm, S., HuÈppop, O., 1998. Reaktion der Herzschlagrate von Flussseeschwalben (Sterna hirundo) auf das Angebot akustischer Reize. SeevoÈgel, Zeitchr Ver. Jordsand 19 (Sonderheft. 1), 92±95.
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www.elsevier.nl/locate/expgero
Detecting and measuring senescence in wild birds: experience with long-lived seabirds I.C.T. Nisbet* I.C.T. Nisbet and Company, 150 Alder Lane, North Falmouth, MA 02556, USA
Abstract This paper points out and discusses several practical and methodological problems that arise in attempts to detect and measure senescent declines in survival or breeding performance of wild animals, with speci®c emphasis on long-lived seabirds. Birds have no anatomical markers of age, so studies of age-related biology require marking individuals at the time of hatching and following them throughout their lives. Seabirds live longer than the working lifespan of biologists, and longer than the turnover times of study techniques or theories of senescence. Seabirds are exposed to changing environmental and demographic conditions and cannot be assumed to be in demographic equilibrium. Sample sizes of the oldest age-classes are always small, requiring either marking very large numbers of birds at hatching or continuing studies of old birds over many years. Incomplete sampling requires the use of mark-recapture models that have only been developed in the last 20 years. Mortality selection resulting from demographic heterogeneity (selective survival of high-quality individuals) can offset or confound the effects of senescent changes within individuals. Many of these problems are amenable to solution and will be probably solved within a few years. In the meantime, this paper recommends that reviewers should be cautious about accepting published reports of senescent declines in natural populations. q 2001 Elsevier Science Inc. All rights reserved. Keywords: Common tern; Seabird; Reproduction; Senescence; Sterna hirundo; Survival
1. Introduction 1.1. Senescence Senescence is de®ned as ªage-related changes in an organism that adversely affect its vitality and functions, but most importantly, increase the mortality rate as a function of timeº (Finch, 1990). Although senescence in this sense is relatively easy to detect and has * Tel./fax: 11-508-564-4958. E-mail address: [email protected] (I.C.T. Nisbet). 0531-5565/01/$ - see front matter q 2001 Elsevier Science Inc. All rights reserved. PII: S 0531-556 5(00)00244-8
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Fig. 1. Common terns (Sterna hirundo). Photograph by F.D. Atwood.
been well documented in humans and in domestic and laboratory animals, it is more dif®cult to detect and measure in animals under natural conditions, especially longlived animals. Although individual organisms can be marked and their ªvitality and functionsº measured at intervals throughout their lives, these measurements are necessarily made under different circumstances and are not necessarily quantitatively comparable. ªMortality rateº is a property of a population and cannot be measured within an individual, so that detection of an increase in mortality rate requires population-based sampling and statistical modeling (Lebreton et al., 1992; Nichols, 1992). Although some reviews have concluded that senescent increases in mortality rates are characteristic of wild bird and mammal populations (Promislow, 1991; Holmes and Austad, 1995), others have pointed out methodological problems and have concluded that the evidence is limited and equivocal (Gaillard et al., 1994; Nichols et al., 1997). This paper discusses some of these methodological issues and assesses recent data on long-lived birds, speci®cally seabirds. It includes illustrative examples from a long-term study of common terns Sterna hirundo. 1.2. Characteristics of seabirds Birds are generally longer-lived than mammals of comparable sizes, and seabirds are especially long-lived among birds (Holmes and Austad, 1995). Most seabirds breed colonially on islands or cliffs and return to the same sites for many years or throughout their lives, often with the same mates (Wooller et al., 1992), so that it is relatively easy to locate and study marked individuals when they are breeding and to measure their reproductive performance. However, most seabirds disperse at sea after the breeding season and/or migrate to distant areas, so that it is dif®cult to locate individuals during the non-breeding season or to document deaths. Hence, estimation of survival rates is always based on statistical sampling of birds at the breeding sites in successive years.
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1.3. Case study The common tern (Fig. 1) is a small (120 g) seabird with an annual adult survival rate of about 0.90 21 year, age at ®rst breeding 2±5 year, median age of breeders 9±10 year, 95th percentile age 18 year, and maximum recorded age 26 year (Nisbet, unpublished data). It is a long-distance migrant, breeding in the North Temperate Zone and wintering in the Southern Hemisphere (Cramp, 1985); birds in this study breed at about 428 N latitude in the northeastern USA and winter mainly at 31±378 S in southern Brazil and northern Argentina (Hays et al., 1997), requiring a journey of at least 8000 km twice each year. Like other small birds, the common tern has high body temperature, high metabolic rate, rapid heart rate, and high blood glucose concentration (Ricklefs and White, 1981; Klaassen, 1994; WuÈrm and HuÈppop, 1998; Galbraith et al., 1999; Pokras, personal communication). This study was conducted mainly at Bird Island, Massachusetts, USA (41840 0 N, 70843 0 W), and more recently at a second site at Ram Island, 10 km SW of Bird Island. Numbers of common terns breeding at Bird Island increased from about 500 in 1970 to about 4500 in 1992, when they began to spread to Ram Island; the total number at the two sites is not about 8500 (Harlow, 1995; Nisbet, unpublished data). About 60,000 chicks have been banded since 1975, and about 2500 birds of known age (range, 2±25 year) are now breeding at the two sites. Studies of known-aged birds have included measurements of reproductive performance (Nisbet et al., 1984), endocrine function (Nisbet et al., 1999), ®eld metabolic rates and energy ef®ciency (Galbraith et al., 1999). Other studies in progress or recently completed include measurements of age-speci®c reproductive effort, hematology, behavior, immune function, and collagen cross-linking (Nisbet et al., unpublished data). This paper emphasizes recent studies of reproductive performance and survival (Nisbet, unpublished data).
2. Changes that occur on time-scales shorter than the lifetimes of the birds 2.1. Changes in the study populations and their environments Although the common tern has a lifespan of about 25 year, it is relatively short-lived compared to other seabirds. Albatrosses and fulmars, for example, have been recorded living up to 50±60 year, and their theoretical lifespans (99th percentile age based on average survival rate) approach or exceed 100 year (Buckland, 1982; Jouventin and Weimerskirch, 1991; Sagar et al., 2000). Within such long time-scales, many or most populations change through demographic or ecological processes. For example, my study population of common terns has increased by a factor of 15±20 during the period of study, has spread from one to two sites and has started to spread to others, and many aspects of its reproductive performance have deteriorated, perhaps as a result of density-dependent processes (see Nisbet et al., 1984; Galbraith et al., 1999). Other study populations of seabirds have changed during the decades of study (Nisbet, 1989; Harris et al., 1994), or their environment has changed in ways that have led to ¯uctuations or long-term changes in survival or reproductive performance (e.g. Aebischer, 1986; Thomas and Coulson, 1988; Jouventin and Weimerskirch, 1991; Fairweather and Coulson, 1995). In
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still other cases, ¯uctuations in the environment associated with ENSO (El NinÄo Ð Southern Oscillation) or other climatic events have led to periodic or irregular ¯uctuations in survival and/or reproductive performance of seabirds (Boekelheide and Ainley, 1989; Ainley and Boekelheide, 1990; Harris et al., 1994; Brichetti et al., 2000). These changes take place on time-scales of 3±30 year, well within the lifespans of the birds and of study programs (Nisbet, 1989). Hence, many or most seabird populations are in a dynamic or unstable relationship to their environments, so that assumptions of ecological or demographic stability are inappropriate (Nisbet, 1989). 2.2. Changes in the observers and in study programs The time-scales of 20±100 year for turnover of seabird populations are longer than the working lifespans of 3±30 year for most seabird biologists (Nisbet, 1989). Seabird biologists themselves suffer from senescence (see Frontispiece in Clutton-Brock, 1988) and cannot be relied on to produce reliable, comparable data for .30 year. Hence, most studies of long-lived seabirds require a succession of principal investigators (e.g. Sagar et al., 2000) if they are to be continued effectively. Investigators are dif®cult to replace, because long-term funding is rarely available, and individuals willing to commit their professional careers to long-term, under-funded studies are rare and idiosyncratic (Nisbet, 1989). Under these circumstances, it is dif®cult to maintain continuity of study techniques and data management (Nisbet, 1989). Techniques of study turn over even more rapidly than investigators. The case study of common terns was started in 1970, before the era of personal computers or the development of user-friendly database programs. Durable markers for terns did not become available until 1975 (Nisbet and Hatch, 1988), and internal markers (implanted transponders) were not tested on terns until 1992 (Becker and Wendeln, 1997). Statistical techniques for capture-mark-recapture modeling were not developed suf®ciently for use in studying survival of seabirds until the 1980s (Clobert et al., 1987) and did not come into wide use until the 1990s (Lebreton et al., 1992); they are still under development (Burnham and Anderson, 1998). Looking ahead 30 more years, it is likely that present-day techniques of marking and aging birds and of analyzing data will be superseded many times over. For example, a technique that would render all present-day methods for sampling obsolete would be the development of implanted transmitters (or receivers) that would record the location and physiological state of an individual bird throughout its annual cycle or its lifetime. Such techniques are already available for large seabirds (Weimerskirch et al., 1993) and it seems unlikely that it would take even 10 year to modify them for use on small seabirds. Statistical techniques for modeling survival and other demographic parameters in wild animal populations are also in a very rapid state of development (Burnham and Anderson, 1998). 2.3. Changes in scienti®c knowledge about senescence Knowledge about senescence and hypotheses about mechanisms that drive it are also developing very rapidly. Few, if any, of the ideas presented and discussed at this Symposium had been formulated when my study started in 1970. Even a relatively short-duration
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study such as the three-year cross-sectional study of survival conducted by Nisbet and Cam (unpublished data) could not be completed and published before a new set of hypotheses about mechanisms of senescence had been formulated.
3. Methodological issues in sampling open populations 3.1. Marking and recapture Birds have no anatomical markers of age, so identifying birds of known age for study requires that they were banded or otherwise individually marked in the year of hatching. This is an enormous disadvantage of birds as model organisms: it requires that studies must continue for at least the lifetimes of the oldest individuals before any information relevant to senescent declines can be collected. Although most seabirds breed colonially and chicks can be banded in large numbers (and often are for other study purposes, or by amateur banders), the proportion that survives to breed is usually low; in many species these survivors disperse among widely separated sites, so that they are dif®cult to ®nd and study. Many studies of age-related biology in seabirds bypass this problem by marking birds when they ®rst breed, and using elapsed time since ®rst breeding as a surrogate measure of chronological age (e.g. Bradley et al., 1989; Aebischer and Coulson, 1990). However, age at ®rst breeding is variable, and birds that start to breed at different ages may differ in other characteristics that in¯uence their breeding performance or survival later in life (Ainley et al., 1990). Finding birds of known age usually requires capturing them to read bands. Although many seabirds are relatively easy to catch at the nest, ®nding small numbers of known-aged birds scattered among large numbers of unknown-aged birds is often labor-intensive and disruptive to the birds. In some cases, marking birds with unique combinations of color-bands has proved to be an ef®cient way to ®nd and identify known-aged individuals without the necessity for trapping them (Cam et al., 1998; Cam and Monnat, 2000; Ratcliffe 1993). However, color-bands are less permanent than bands made of durable metal alloys, and are sometimes lost or cause injuries; we have not been able to use them on terns for these reasons (Nisbet, 1991; Spendelow et al., 1994). Whatever bands are used, there is a possibility that a few of the birds may be caught by humans and the bands removed (as demonstrated for terns wintering in Africa by Becker and Wendeln, 1996). For this reason, Becker and Wendeln (1997) switched to using implanted transponders for permanent marking of individuals, but this has the disadvantage that the transponders can only be read using an antenna within a few centimeter of the bird. This either requires catching all birds, or placing transmitters at all nests, which is only practicable in small colonies. Whatever techniques are used to mark and relocate the birds, the proportion of marked birds that is found each year is usually less than 1. Even if all birds at a site are trapped or otherwise checked every year, in most seabird species the proportion that breeds in a given year is usually less than 1, frequently much less and often variable from year to year (Cam et al., 1998; Bradley et al., 2000).
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3.2. Accounting for incomplete recaptures For measuring age-speci®c reproductive performance, it may not matter much that some individuals are not found in one or more of the years of study. In fact, several long-term studies of seabirds have yielded strong evidence of declines in reproductive performance among the oldest birds (Reilly and Cullen, 1981; Thomas and Coulson, 1988; Mills, 1989; Pugesek and Diem, 1990; Wooller et al., 1990), even though some of the same studies have not provided conclusive evidence of senescent declines in survival. Studies of age-related reproductive performance are subject to bias, however, because the individuals that skip breeding in a given year tend to be the individuals with constitutionally lower breeding performance (Cam et al., 1998). For investigating age-speci®c survival, it is essential to estimate the recapture probability and (unless it is very close to 1) to incorporate it into estimates of survival. In the ®rst step in estimating survival, N1 animals are marked in year 1 and N2 of them are recaptured in year 2. The ratio N2/N1 yields an estimate of a quantity S12 p2, the product of S12, the survival probability between years 1 and 2, and p2, the recapture probability in year 2. In earlier studies, it was often assumed that p2 was equal to 1, on the basis of a subjective evaluation of the diligence and ef®ciency of the observer (but ignoring or overlooking the possibility of temporary non-breeding or temporary emigration). This assumption always leads to a downwards-biased estimate of S12. Although a few cases have been reported in which p2 was actually close to 1 (e.g. Cam et al., 1998), this can never be known a priori, so it is always desirable to estimate this parameter. A second pitfall of assuming that p2 is equal to 1 is that survival probabilities are further underestimated in the last year of the study, because birds that are alive but skip breeding or are overlooked in the last year are then classi®ed as dead. Because the last year of the study usually includes disproportionate numbers of the oldest birds, this can lead to a spurious appearance of a decline in survival among the oldest birds. In the notation of Ricklefs (2000), assuming that p2 is equal to 1 can lead to underestimation of a and overestimation of b . A third pitfall of assuming that p2 is equal to 1 is that the precision of estimates of S12 is then overstated, because uncertainty in p2 contributes to the variance in S12. The only way in which unbiased estimates of S12 can be obtained is to repeat the sampling at a third time interval (in year 3, in most mark-recapture studies). This yields independent estimates of S12 and p2 (and their standard errors), plus another unresolvable product S23 p3 for years 2±3. A fourth year's sampling yields estimates of parameters for two years, a ®fth year's sampling for three, and so on. This general procedure of capturemark-recapture modeling has been formalized and extended for many types of application (Nichols, 1992; Lebreton et al., 1992). It is now widely used, but most estimates of survival of birds published before about 1990 did not use this method and hence are potentially biased. As an example of the importance of using formal procedures, Pugesek and Diem (1990) reported survival estimates of known-aged California gulls (Larus californicus) in relation to prior breeding activity; the estimation procedure involved the assumption that p2 was equal to 1. Data from the same study were later analyzed by Pugesek et al. (1995), who reported modeled estimates of p2 that were strongly age-dependent, ranging from 0.54 to 0.90. Although both analyses showed a decline in survival probability with age, the later,
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more rigorous analysis yielded higher estimates of survival probability at all ages, with the decline manifested only among the oldest age-classes ($15 year). 3.3. Separating effects of age and time An unavoidable problem in investigations of senescence in wild animal populations in that sample sizes in the oldest age-classes that are of primary interest are much smaller than those in earlier age-classes. Most studies of seabirds that have reported age-related declines in survival or breeding success documented these declines only among the oldest individuals Ð typically, the oldest 5±10% of the population (e.g. Bradley et al., 1989; Pugesek et al., 1995). The only ways to overcome this problem of dwindling numbers are either (a) to start with extremely large numbers of marked birds at the time of hatching or ®rst breeding, or (b) to continue the study over several years. The ®rst may be impractical (see Section 3.4); the second runs the risk of confounding effects of age and time. In several studies, variations in survival rate from year to year were as large as differences between young and old birds (e.g. Harris et al., 1994; Ratcliffe 1993). In at least two studies (Aebischer and Coulson, 1990; Weimerskirch, 1992) survival rates declined for all age-classes in the later years of the study because of changes in the environment. Because older birds were more frequent in the later years of each study, this opened the possibility of confounding between time-related and age-related declines in survival. Although modeling techniques are available for separating age and time effects (e.g. Harris et al., 1994; Ratcliffe 1993), they have not often been used. 3.4. Selecting sample sizes It is axiomatic that using larger sample sizes increases precision, other factors being equal. However, choice of sample sizes in seabird research is sometimes constrained by the characteristics of the seabird population. In large colonies, it is generally impractical to mark all individuals or to recapture all individuals that are marked. Even if a large number of individuals are recaptured, low recapture rates contribute to the variance in estimates of survival rate and may offset the gains from large sample sizes (as in my study of common terns: Nisbet, unpublished data). Some of the best studies of age-speci®c survival in seabird populations have been conducted in small colonies including only a few hundred birds (e.g. Bradley et al., 1989; Aebischer and Coulson, 1990). Although it is possible in these circumstances to check all individuals attending the colony in each year (even individuals that visit nest-sites but do not breed: Bradley et al., 2000), it is necessary to continue studies in small colonies for many years to obtain suf®cient data on old birds, because only a handful of old birds is present in any one year (see previous paragraph). More serious, small colonies may not be demographically representative of the larger populations within which they occur. It is extremely unlikely that births and deaths within a small colony will be exactly balanced over a long period, so that emigration and immigration may be disproportionately important in small colonies. For all these reasons, designing studies of age-speci®c survival involves complex trade-offs between colony sizes, sample sizes, marking techniques, study durations, and precision.
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4. Demographic heterogeneity and mortality selection A ®nal problem in all studies of senescence arises from demographic heterogeneity. If groups of individuals within the population differ constitutionally in their risks of death, and if these differences are manifested throughout life, the groups with the lowest mortality risk will be disproportionately represented among those that survive to old age, as a result of selective survival. If the heterogeneity is suf®ciently great, it may reduce or negate the effects of senescent increases in the probability of death within individuals (Vaupel and Yashin, 1985). This phenomenon is well known among human demographers (Vaupel and Yashin, 1985) and experimental gerontologists (Carey et al., 1992; Tatar et al., 1993), but has only recently attracted the attention of ®eld biologists and evolutionary biologists (McDonald et al., 1996; Nichols et al., 1997; Cam and Monnat, 2000; Service, 2000). Although it is possible to separate the effects of demographic heterogeneity and mortality selection in circumstances where complete survival histories are known for all individuals (e.g. in human demography), modeling tools are not yet available to do this in populations of wild animals where the recapture probabilities are less than 1 (Cam, personal communication). Demographic heterogeneity is not only important in investigations of age-speci®c survival. It can also offset (or augment) the effects of senescent decline in other performance parameters, including reproductive performance. If other phenotypic characteristics (e.g. those that determine breeding performance) are also heterogeneous within the population and are correlated with mortality risks, then the individuals that survive to old age may be those with constitutionally higher (or lower) breeding performance. For example, if groups of individuals with high survival probabilities also have high probabilities of successful reproduction (positive phenotypic correlation), the individuals that survive to old age will include disproportionate numbers of individuals with above-average reproductive performance. This phenomenon could offset or appear to reverse the effects of senescent decline in reproductive ef®ciency. For example, in my study of common terns, breeding performance continued to increase with age up to and probably beyond the 95th percentile age in the local population (Nisbet, unpublished data). This trend, however, was only measured in a cross-sectional study (birds of different ages compared in the same year). It is not inconsistent with the hypothesis of senescent decline in ef®ciency within individuals, if that decline were offset by selective survival of individuals with constitutionally high ef®ciency. In the ecological literature, such individuals are referred to as being of high individual `quality' (Nisbet et al., 1998; Wendeln and Becker, 1999). Many studies of seabirds have indicated that individuals of high quality (as de®ned by reproductive performance) survive better than individuals of low quality (i.e. positive phenotypic correlation: Richdale, 1949; Potts, 1969; Reilly and Cullen, 1981; Ollason and Dunnet, 1988; Thomas and Coulson, 1988; Bradley et al., 1989; Mills, 1989; Cam and Monnat, 2000). Thus, mortality selection appears to be pervasive in long-lived seabirds and may be a major in¯uence on apparent trends in reproductive performance among the older age-classes. A theoretical way to separate the effects of mortality selection and senescence in in¯uencing breeding performance is to conduct longitudinal studies within individuals. This has been attempted in several studies of seabirds (e.g. Thomas and Coulson, 1988;
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Bradley et al., 1989; Wooller et al., 1990). However, it is dif®cult or impossible to control such studies for possible effects of changes in the environment. 5. Concluding comments This paper has pointed out several practical and methodological problems that arise in ®eld studies that attempt to detect and measure senescent declines in survival or breeding performance of wild birds or other animals. This area of study is in a state of rapid change and new tools for investigating senescence are constantly being developed. Many of the problems are amendable to solution and will probably be solved within a few years. In the meantime, however, I recommend that reviewers should assess published results critically, should be cautious about accepting published reports of senescent declines in natural populations, and should be especially cautious about accepting published reports of patterns or rates of decline. References Aebischer, N.J., 1986. Retrospective investigation of an ecological disaster in the shag. Phalacrocorax aristotelis: A general method based on long-term marking. J. Anim. Ecol. 53, 613±629. Aebischer, N.J., Coulson, 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. Ainley, D.G., Boekelheide, R.J. (Eds.), 1990. Seabirds of the Farallon Islands, Ecology, Dynamics, and Structure of an Upwelling-System Community Stanford University Press, Stanford, CA. Ainley, D.G., Ribic, C.A., Wood, R.C., 1990. A demographic study of the South Polar skua (Catharacta mccormicki) at Cape Crozier. J. Anim. Ecol. 59, 1±20. Becker, P.H., Wendeln, H., 1996. Ring removal in terns caught in Africa Ð a major problem for population studies. Ring. Migr. 17, 31±32. Becker, P.H., Wendeln, H., 1997. A new application for transponders in population ecology of the common tern. Condor 99, 534±538. Boekelheide, R.J., Ainley, D.G., 1989. Age, resource availability, and breeding effort in Brandt's cormorant. Auk 106, 389±401. Bradley, J.S., Wooller, R.D., Skira, I.J., Serventy, D.L., 1989. Age-dependent survival of short-tailed shearwaters Puf®nus tenuirostris. J. Anim. Ecol. 58, 175±188. Bradley, J.S., Wooller, R.D., Skira, I.J., 2000. Intermittent breeding in the short-tailed shearwater Puf®nus tenuirostris. J. Anim. Ecol. 69, 639±650. Brichetti, P., Foschi, U.F., Boano, G., 2000. Does El NinÄo affect survival rate of Mediterranean populations of Cory's shearwater? Waterbirds 23, 147±154. Buckland, S.T., 1982. A mark-recapture survival analysis. J. Anim. Ecol. 51, 831±847. Burnham, K.P., Anderson, D.R., 1998. Model Selection and Inference. A Practical Information-Theoretic Approach. Springer, New York. Cam, E., Monnat, J.-Y., 2000. Apparent inferiority of ®rst-time breeders in the kittiwake: the role of heterogeneity among age classes. J. Anim. Ecol. 69, 380±394. Cam, E., Hines, J.E., Monnat, J.-Y., Nichols, J.D., Danchin, E., 1998. Are adult nonbreeders prudent parents? The kittiwake model. Ecology 79, 2917±2930. Carey, J.R., Liedo, P., Orozco, D., Vaupel, J.W., 1992. Slowing of mortality rates at older ages in large med¯y cohorts. Science 258, 457±461. Clobert, J., Lebreton, J.-D., Allaine, D., 1987. A general approach to survival rate estimation by recaptures or resightings of marked birds. Ardea 78, 133±142.
842
I.C.T. Nisbet / Experimental Gerontology 36 (2001) 833±843
Clutton-Brock, T.H. (Ed.), 1988. Reproductive Success: Studies of Individual Variation in Contrasting Breeding Systems University of Chicago Press, Chicago, IL. Cramp, S. (Ed.), 1985. The Birds of the Western Palearctic, vol. IV. Oxford University Press, Oxford. Fairweather, J., Coulson, J.C., 1995. The in¯uence of forced site change on the dispersal and breeding of the black-legged kittiwake (Rissa tridactyla). Colon Waterbirds 18, 30±40. Finch, C.E., 1990. Longevity, Senescence, and the Genome. University of Chicago Press, Chicago, IL. Gaillard, J.-M., Allaine, D., Pontier, D., Yoccoz, N., Promislow, D.L., 1994. Senescence in natural populations of mammals: a reanalysis. Evolution 48, 509±516. Galbraith, H., Hatch, J.J., Nisbet, I.C.T., Kunz, T.H., 1999. Age-speci®c reproductive ef®ciency among breeding common terns Sterna hirundo: measurement of energy expenditure using doubly-labelled water. J. Avian. Biol. 30, 85±96. Harlow Jr., R.A., 1995. Ram island: recovery in progress. Bird Observer 23, 333±338. Harris, M.P., Buckland, S.T., Russell, S.M., Wanless, S., 1994. Year- and age-related variation in the survival of adult European shags over a 24-year period. Condor 96, 600±605. Hays, H., DiCostanzo, J., Cormons, G., Antas, P.de T.Z., Nascimento, J.do, Nascimento, I.de L.S.do, Bremer, R.E., 1997. Recoveries of roseate and common terns in South America. J. Field Ornithol. 68, 79±90. Holmes, D.J., Austad, S.N., 1995. Birds as animal models for the comparative biology of aging: a prospectus. J. Gerontol. 59A, B59±B66. Jouventin, P., Weimerskirch, H., 1991. Changes in the population size and demography of southern seabirds: management implications. In: Perrins, C.M., Lebreton, J.-D., Hirons, G.J.M. (Eds.). Bird Population Studies: Relevance to Conservation and Management. Oxford University Press, Oxford, pp. 297±316. Klaassen, M., 1994. Growth and energetics of tern chicks from temperate and polar environments. Auk 111, 525±544. Lebreton, J.-D., Burnham, K.P., Clobert, J., Anderson, D.R., 1992. Modeling survival and testing biological hypotheses using marked animals: a uni®ed approach with case studies. Ecol. Monogr. 62, 67±118. McDonald, D.B., Fitzpatrick, J.W., Woolfenden, G.E., 1996. Actuarial senescence and demographic heterogeneity in the Florida scrub jay. Ecology 77, 2373±2381. Mills, J.A., 1989. Red-billed Gull. In: Newton, I. (Ed.). Lifetime Reproductive Success. Academic Press, London, pp. 387±404. Nichols, J.D., 1992. Capture±recapture models using marked animals to study population dynamics. BioScience 42, 94±102. Nichols, J.D., Hines, J.D., Blums, P., 1997. Tests for senescent decline in annual survival probabilities of common pochards, Aythya ferina. Ecology 78, 1009±1018. Nisbet, I.C.T., 1989. Long-term ecological studies of seabirds. Colon. Waterbirds 12, 143±147. Nisbet, I.C.T., 1991. Problems with Darvic color-bands on common terns: band losses and foot injuries. N. Am. Bird Bander. 16, 61±63. Nisbet, I.C.T., Hatch, J.J., 1988. Durability of incoloy bands on common terns. Colon. Waterbirds 11, 113±114. Nisbet, I.C.T., Winchell, J.M., Heise, A.E., 1984. In¯uence of age on the breeding biology of common terns. Colon. Waterbirds 7, 117±126. Nisbet, I.C.T., Spendelow, J.A., Hat®eld, J.S., Zingo, J.M., Gough, G., 1998. Variations in growth of roseate tern chicks: II. Early growth as an index of parental quality. Condor 100, 305±315. Nisbet, I.C.T., Finch, C.E., Thompson, N., Russek-Cohen, E., Proudman, J.A., Ottinger, M.A., 1999. Endocrine patterns during aging in the common tern (Sterna hirundo). Gen. Comp. Endocrinol. 114, 279±286. Ollason, J.C., Dunnet, G.M., 1998. Variation in breeding success in fulmars. In: Clutton-Brock, T.H. (Ed.). Reproductive Success: Studies of Individual Variation in Contrasting Breeding Systems. University of Chicago Press, Chicago, IL, pp. 263±278. Potts, G.R., 1969. The in¯uence of eruptive movements, age, population size and other factors on the survival of the shag (Phalacrocorax aristotelis (L.)). J. Anim Ecol. 38, 53±102. Promislow, D.E.L., 1991. Senescence in natural populations of mammals: A comparative study. Evolution 45, 1865±1877. Pugesek, B.H., Diem, K.L., 1990. The relationship between reproduction and survival in known-aged California gulls. Ecology 71, 811±817. Pugesek, B.H., Nations, C., Diem, K.L., Pradel, R., 1995. Mark-resighting analysis of a California gull population. J. Appl. Statist. 22, 625±640.
I.C.T. Nisbet / Experimental Gerontology 36 (2001) 833±843
843
Ratcliffe, N., 1993. The age speci®c breeding performance of great skuas on Shetland. Unpublished Ph.D. thesis, University of Glasgow, Glasgow, UK. Reilly, P.N., Cullen, J.M., 1981. The little penguin (Eudyptula minor) in Victoria. II. Breeding. Emu 81, 1±19. Richdale, L.E., 1949. A study of a group of penguins of known age. Biol Monogr. 1, 1±88 (Otago Daily Times and Witness Newspapers, Dunedin, New Zealand). Ricklefs, R.E., 2000. Intrinsic aging-related mortality in birds. J. Avian. Biol. 31, 103±111. Ricklefs, R.E., White, S.C., 1981. Growth and energetics of the sooty tern (Sterna fuscata) and the common tern (Sterna hirundo). Auk 98, 361±378. Sagar, P.M., Molloy, J., Weimerskrich, H., Warham, J., 2000. Temporal and age-related changes in survival rates of southern Buller's albatrosses (Thalassarche bulleri bulleri) at The Snares, New Zealand. Auk 117, 699± 708. Service, P.M., 2000. Heterogeneity in individual mortality risk and its importance for evolutionary studies of senescence. Am. Nat. 156, 1±13. Spendelow, J.A., Burger, J., Nisbet, I.C.T., Nichols, J.D., Hines, J.E., Hays, H., Cormons, G.D., Gochfeld, M., 1994. Sources of variation in loss rates of color bands applied to adult roseate terns (Sterna dougallii) in the western North Atlantic. Auk 111, 879±885. Tatar, M., Carey, J.R., Vaupel, J.W., 1993. Long-term cost of reproduction with and without accelerated senescence in Callosobruchus maculatus: Analysis of age-speci®c mortality. Evolution 47, 1302±1312. Thomas, C.S., Coulson, J.C., 1988. Reproductive success of kittiwake gulls (Rissa tridactyla). In: Clutton-Brock, T.H. (Ed.). Reproductive Success: Studies of Individual Variation in Contrasting Breeding Systems. University of Chicago Press, Chicago, IL, pp. 251±262. Vaupel, J.W., Yashin, A.I., 1985. Heterogeneity's ruses: Some surprising effects of selection on population dynamics. Am. Statist. 39, 176±185. Weimerskirch, H., 1992. Reproductive effort in long-lived birds: Age-speci®c patterns of condition, reproduction, and survival in the wandering albatross. Oikos 64, 464±473. Weimerskirch, H., Salamolard, M., Sarrazin, F., Jouventin, P., 1993. Foraging strategy of wandering albatrosses through the breeding season: A study using satellite telemetry. Auk 110, 325±342. Wendeln, H., Becker, P.H., 1999. Effects of parental quality and effort on the reproduction of common terns. J. Anim. Ecol. 68, 205±214. Wooller, R.D., Bradley, J.S., Skira, J.J., Serventy, R.D., 1990. Reproductive success of short-taited shearwaters Puf®nus tenuirostris in relation to their age and breeding experience. J. Anim. Ecol. 59, 161±170. Wooller, R.D., Bradley, J.S., Croxall, J.P., 1992. Long-term population studies of seabirds. Trends Ecol. Evol. 7, 111±114. WuÈrm, S., HuÈppop, O., 1998. Reaktion der Herzschlagrate von Flussseeschwalben (Sterna hirundo) auf das Angebot akustischer Reize. SeevoÈgel, Zeitchr Ver. Jordsand 19 (Sonderheft. 1), 92±95.