Studies in Avian Biology No. 22:281-290, 2001.

THE EVOLUTION OF LIFE HISTORIES ON OCEANIC ISLANDS, AND ITS IMPLICATIONS FOR THE DYNAMICS OF POPULATION DECLINE AND RECOVERY

BERTRAM G. MURRAY, JR.

Abstract. The Archipelago in the Indian Ocean lies a few degrees south of the equator, about 1,600 km east of Kenya. The Galapagos Archipelago in the Pacific Ocean lies on the equator about 1,000 km west of Ecuador. The Hawaiian Islands straddle the Tropic of Cancer and are about 3,500 km southwest of California. The Seychelles Warbler ( sechellensis) has a long life, usually begins breeding at age four, lays a one-egg clutch, and is single brooded (a combination that is extraordinary for a small passerine). In contrast, the Large Cactus Finch (Geospiza conirostris)of the Galapagos has a short life (some cohorts live no more than seven years), usually begins breeding at age one (but some may begin at age two or three), lays a large clutch (about four eggs), and successfully rears as many as six broods per year (occasionally, it rears none). The life history of Hawaiian appears to be intermediate between these extremes. These differences are attrib- utable to environmental differences affecting the length of the breeding season, survivorship, and reproductive success. Many island populations are threatened with because of introduced disease, such as avian malaria, and predators, such as rats, cats, and humans, as well as destruction of their habitats by introduced , such as goats, and by humans. Island populations are at greater risk of serious population decline than mainland populations because of the limited amount of habitat and because they have evolved a small biotic potential (rim). The small biotic potential results from the evolution of long life expectancy and small clutch size in environments that were virtually predator- and disease- free prior to their discovery by the human species. Conservation of endemic island populationswill require, at least, the preservationof suitable habitat and control of predator and diseaseorganisms. Key Words: age of first breeding; biotic potential, breeding season;clutch size; demography;Gal& pagos; Hawai‘i; life history; population dynamics; r,,,,; Seychelles; survival.

Clutch-size variations in are well-known, ern Indian Ocean. In 1959 the global population the most prominent of which is the increase in of Seychelles Warbler numbered 26 individuals, clutch size with increasing latitude (Lack 1947, and in 1968 the International Council for 1948; Cody 1966, 1971; Klomp 1970). Clutch Preservation undertook management of the is- size also tends to be smaller on oceanic islands land for the preservation of the species. Because than on the nearest mainland in the temperate the coconut palms (Cocos nucifera) were pre- zone, but not in the tropics, where clutch size is vented from regenerating and the indigenous about the same on islands and on the adjacent vegetation was allowed to flourish, the warbler mainland (Lack 1968, Cody 1971). On oceanic population grew to over 300 birds by 1982 islands within the tropics, however, clutch size (Komdeur 1994a). In 1988, 29 birds were trans- in passerines varies from one egg in the long- ferred to Aride Island, and in 1990 another 29 lived, single-brooded Seychelles Warbler (Ac- were transferred to Cousine Island. Both intro- rocephalus sechellensis) to four eggs in the ductions have been successful (Komdeur short-lived, multibrooded Large Cactus Finch 1994a). (Geospiza conirostris). In this paper I explore On , the Seychelles Warbler is the evolution of life-history variations of pas- long-lived with an annual adult survival rate of serines on tropical oceanic archipelagos. 0.82 (Table 1). One bird survived to its 28th year The theory on the evolution of clutch size, (S. Dykstra, pers. comm.). Females begin breed- proposed to explain this variation in life histories ing at age four and rarely lay more than one one- among passerines on oceanic archipelagos, will egg clutch per year (Komdeur et al. 1995, 1997). be used to explore the evolution of a species’ On Aride and Cousine islands, where the pop- biotic potential (i.e., Y,,), that is, its maximum ulations are still growing, females begin breed- rate of increase in natural habitat in uncrowded ing at age one, lay a larger clutch, and often rear conditions. A species’ biotic potential is a mea- more than one brood per year (Komdeur 1994a, sure of the rate of recovery of a population when 1996). the environment is managed for that population. The life history of the Large Cactus Finch on THE BIRDS Isla Genovesa in the Galapagos Archipelago The Seychelles Warbler is endemic to Cousin (Grant and Grant 1989) is strikingly different Island in the Seychelles Archipelago in the west- from that of the Seychelles Warbler (Table 1).

281 282 STUDIES IN AVIAN BIOLOGY NO. 22

TABLE 1. LIFE-HISTORY CHARACTERISTICS OF FIVE PASSERINE SPECIES FROM THREE OCEANIC ARCHIPELAGOS

Seychelles Large cac- Warbler" Pali@ Hawai‘i ‘.%kepa' 'Oma‘od Elepaio‘ ’ tus Finch ’

Age of first breeding 4 3 (males) 2 (males) 1 l-3 1-2 (females) 1 (females) Mean clutch size 1 1.9 2-3 1-2 2 3.5 Maximum broods per 1 3 1 2 O-6 year Breeding season length 12 6-7 4 12 (peak 3 O-6 (mo) May-July) Survival of fledglings 0.44 0.36 0.43 0.40 0.10 Adult survival 0.81 0.65 (males) 0.83 (males) 0.66 0.88 (males) 0.62s 0.62 (females) 0.80 (females) 0.80 (females) dKomdeur (1992._ 1994aXKomdeuret, al. 11997).i , "wm Riper (1980a),Lindsey et al. (1995),T K.Pratt (pers. comm.). 'Lrpsonand Freed 1995, LI A. Freed (pus. comm.). "Bwzer (1981). Raloh and Fancv (1994~). rvan Riper (1995), Vander Werf(unpubl. abstract). Grant‘ and Grant(l989). E See text.

Females usually begin breeding at age one or 13. However, there was no cohort of G. fortis two, but some females do not breed until age produced in 1977, and the 1976 cohort had only three, and lay a modal clutch size of four eggs. one bird survive two years. One cohort (1977) Annual variation in number of clutches laid var- of G. scandens did not survive three months, ies greatly, from zero in severe drought years to and another (1976) had one bird survive two as many as seven in wet years (see Fig. 4.6 in years. Although adult survivorship appears to be Grant and Grant 1989). Consistent with high re- high (about 80%) in some cohorts, the mean life production is the short life of Large Cactus expectancy of the average bird from the time of Finches, four of five reported cohorts of females its being laid as an egg is short. Females of both surviving no more than seven years (males tend species lay a modal clutch of four eggs (Grant to survive longer, one cohort of males surviving and Grant 1989). beyond ten years). About 10% of fledglings sur- The Seychelles Warbler and the Geospiza vive their first year (see Tables 3.1 and 3.2 in finches seem to represent extremes in the evo- Grant and Grant 1989). Although Grant and lution of life histories on tropical oceanic is- Grant (1989, Table 3.2) use subsamples to give lands. The Seychelles Warbler has a long life estimates of annual adult survival for males of and low reproductive rate, whereas the Geospiza 0.81 and for females of 0.78, the largest sample finches have short life expectancies and high re- (1,244 banded birds known to have fledged in productive rates. the years 1978 to 1983) gives an annual adult Intermediate are the indigenous Hawaiian survival of 0.50. This is probably an underesti- passerines (Table 1). For example, the Palila mate (with annual adult survival of 0.50, we (Loxioides bailleui) has a clutch size of 1.9 (van should expect to see 1 in 1,000 reach age eight). Riper 1980a). Females begin breeding at age one Annual adult female survival may be closer to or two and rear at most three broods in a season 0.62 (Table 3.2 in Grant and Grant 1989). With (T. K. Pratt, pers. comm.). Survivorship of fledg- this survival rate, we should expect 1 in 1,000 lings is 0.36, and annual adult survivorship is females to reach age ten). This may also be an 0.63 (Lindsey et al. 1995a). T K. Pratt et al. underestimate (I? R. Grant, pers. comm.). An- (unpubl. data) found a small difference in sur- nual adult female survival of 0.78, however, is vivorship between males and females, 0.65 and too great (1 in 1,000 expected to reach age 19). 0.62, respectively. The life histories of the Medium Ground In other Hawaiian passerines, clutch size var- Finch (Geospiza fortis) and Common Cactus ies between two in the Poouli‘ (Melamprosops Finch (Geospiza scandens) on Isla Daphne Ma- phaeosoma; Pratt et al. 1997b) and Elepaio‘ jor are similar to that of the Large Cactus Finch (Chasiempis sandwichensis; van Riper 1995, (Grant and Grant 1992). Most females begin VanderWerf 1998a) and 3.2 in the Laysan Finch breeding between ages one and three. One of (Telespiza cantans; Morin 1992a). Adult survi- four cohorts (1975, sexes combined) of each vorship varies between 0.55 in the I‘ iwi‘ (Ves- speciessurvived to age 15 (G. fortis) and 16 (G. tiaria coccinea; Ralph and Fancy 1995), 0.80 for scandens), and the 1978 cohorts had three (G. female and 0.83 for male Hawaii‘ Akepa‘ (Lox- scandens) and five (G. fortis) survivors at age ops coccineus; Lepson and Freed 1995), and LIFE HISTORY EVOLUTION-Murmuy 283

0.78 for female and 0.87 for male ‘Elepaio in July 1983; Grant and Grant 1989). Neverthe- (VanderWerf 1998a). Most females produce at less, the average monthly rainfall during the wet most a single brood a year. Unfortunately, sur- season in the Galgpagos (55 mm from 1978 vivorship from the laying of the egg through the through 1988; Grant and Grant 1989) is consid- first year is poorly known in all these species. erably less than the mean monthly low during the five drier months of the southeast monsoon THE ENVIRONMENTS at the Seychelles (91 mm from May through The granitic central islands of the Seychelles September; Court 1992). Archipelago are the remains of the breakup of The food supply for the finches varies with Gondwanaland. The climate is relatively benign the amount of rainfall (Grant and Grant 1989), (Court 1992). The drier southeast monsoon oc- and thus breeding activity of the birds is extraor- curs from May through October, and the wetter dinarily variable. During drought years, breed- northwest monsoon occurs between December ing may not occur at all, and during wet years and March. The mean annual precipitation of breeding may continue for seven to eight 1,500 to 2,200 mm is distributed throughout the months, during which females may lay as many year, varying from 61 and 64 mm in June and as seven clutches and rear as many as six broods July to 296 and 387 mm in December and Jan- (Grant and Grant 1989). uary (at Point La Rue international airport; Lying about 20” north of the equator, the “Ha- Court 1992). Temperature varies slightly, from a waiian Islands are justly famous for mild, uni- mean low of 23.9” C in December to a mean form, subtropical weather . ” (Carlquist 1970: high of 31.3” C in April (Court 1992). 63). The northeast trade winds blow throughout Although the availability of food and the most of the year (averaging about 300 days), and probability of success in rearing young from a the difference between the mean summer (May breeding attempt varied considerably, some to October) and mean winter (November to breeding activity (nest building, incubation, and April) temperature is only 4” C. During the win- feeding of young) on Cousin and Cousine is- ter the wind sometimes shifts to the south (Kona lands occurred throughout the year (Komdeur winds), bringing hotter, stickier weather. Rain 1994a, 1996; Komdeur et al. 1995). On Aride falls throughout the year but varies considerably Island, where the Seychelles Warbler has re- between leeward and windward sides and with cently been introduced, some breeding activity elevation. Hilo, on the island of Hawai‘i, is the occurred in almost 100% of territories in every wettest city in the United States (3,300 mm per month of the year. year), whereas on the leeward side of the islands In contrast, the climate of the volcanic Gal& rainfall may be as little as 250 mm. pagos Archipelago is more variable, severe, and Despite the year around near uniformity of the unpredictable, especially with regard to rainfall climate, the length of the breeding season of the (Grant and Boag 1980, Grant 1986, Grant and endemic passerines varies from as short as two Grant 1989). Normally, a warm wet period from months (Po‘ouli; Pratt et al. 199713) to year- about January to May is followed by a cool dry round (‘Oma‘o [My&es&s obscurus]; Ralph period from about June to December, in re- and Fancy 1994~). sponse to the annual north-south movements of the southern, cooler Humboldt Current and the DlSCUSSION warmer, tropical current flowing from the Gulf THE EVOLUTION OF CLUTCH SIZE of Panama. Temperature varies between a mean high of about 30” C in March to a mean low of The clutch size of birds on oceanic islands about 19” C in September at the Charles Darwin tends to be smaller than on the nearest mainland Research Station. According to Grant (1986:25), in the temperate zone and about the same size “The most striking feature of the Galripagos cli- in the tropics (Cody 1966, Lack 1968). The mate is the extraordinary year-to-year variation clutch sizes of Galapagos finches are exceptional in rainfall.” During the wet season, rainfall var- in being larger than those of passerine species ies from completely absent (in 1985) to quite on the Santa Elena Peninsula of Ecuador (Mar- heavy (116 mm in February 1980, compared chant 1960), which in turn are larger than typical with a mean precipitation of about 18 mm per for tropical species (Marchant 1960, Cody 1966, month from January to May in years without El Lack 1968, Skutch 1985). The clutch size of the Nifio rainfall: Grant and Grant 1989). Superim- Seychelles Warbler is exceptional in being the posed on these variations are El Nifio-Southern smallest for a passerine species. Oscillation (ENSO) events, which occur every 2 If we are to understand the evolution of life- to 11 years (averaging 7 years). At these times history variations, we must keep three facts in precipitation can be very heavy, even during the mind. First, the relationship between clutch size “dry” season (e.g., 505 mm on Isla Genovesa and other demographic parameters is given by 284 STUDIES IN AVIAN BIOLOGY NO. 22 the clutch-size equation (Murray and Nolan July, or a five-egg clutch laid by a female of one 1989), species with a four-egg clutch laid by a female of another species. If we are observing a female a+1 that has just laid a fourth egg in a clutch, we c= (1) may ask, would she increase her probability of i: A;$ P, ’ u rearing any young from that clutch by laying an additional egg? The answer is, no. The only ap- where a is the primary sex ratio (assumed to be parent exception: a female that lays two eggs one in birds), A, is the probability of surviving and begins incubation with the first egg can do from birth (in birds, from the laying of the egg) better than if she had laid one egg (Murray to age class x of those individuals from success- 1994a). If she began incubation with the second ful clutches or litters, (Y is the mean age class of egg, however, s, would be less than if she had first breeding, o is the age class of last breeding, laid one egg. and %P, is the mean number of broods success- Third, it is important to understand that we fully reared during a breeding season. %P, = P, cannot compare one or two components of a life + P, + . . + P,L, where P,, P,, and P, are the history within, between, or among species and probabilities of the females of a genotype suc- draw a conclusion about fitness (Murray 1992b, cessfully rearing at least one, two, and n broods 1997a), much less make a prediction of what we during a breeding season. Furthermore, P, + P, should find in nature. We must consider the + . . + P, = c,s, + c2s2 + . . + c,s,, where combination of factors explicit in Equation 1. cl, c2, and c,, are the mean number of clutches For example, if annual adult survival is greater laid in producing a first, second, and nth brood, in one species than in another, we should not and s,, s2, and s, are the probabilities that first, expect that it should necessarily have the smaller second, and nth brood clutches produce at least clutch. If juvenile survival of the first species one young to independence (Murray 1991a,b). were poorer than in the second, each species Equation I must hold, regardless of ones’ expla- could have the same clutch size, or the first nation for the evolution of clutch size (Wootton could have a larger clutch size. If age of first et al. 1991, Murray 1992a). breeding were later in the first species than in With high quality data (large samples for al- the second, then each species could have the most 20 years), such as are available for the same clutch size, or the first could have a larger Florida Scrub-Jay (Aphelocoma coerulescens; clutch size. In comparing species, we must be Woolfenden and Fitzpatrick 1984), the equation careful to control for or at least consider the pos- works exceptionally well (Murray et al. 1989). sibility of multiple demographic differences be- The equation has been applied to data on only tween them. two other species, each producing a very good With these constraints in mind, I have pro- estimate of clutch size (Prairie Warbler [Den- posed that selection favors those females that lay droica discolor], Murray and Nolan 1989; as few eggs or bear as few young as are consis- House Wren [Troglodytes aedon], Kennedy tent with replacement because they have the 1991). highest probability of surviving to breed again, Second, if the probability of nest contents their young have the highest probability of sur- (eggs or nestlings) surviving from one day to the viving to breed, or both (Murray 1979, 199 la, next is less than one, then smaller clutches al- 1999). What this means is that the genotype that ways have a higher probability of having young has a clutch size that can replace itself has the leave the nest (s,) than larger clutch sizes (Mur- greatest Malthusian parameter, the best measure ray 1999). For example, a two-egg clutch always of fitness (Murray 1992b, 1997a). Genotypes has a greater s, than a three-egg clutch, and a with clutch sizes smaller than replacement have four-egg clutch always has a higher si than a negative Malthusian parameters because they five-egg clutch because, in each case, the larger are not producing enough young to replace clutch always requires at least one more day to themselves. Genotypes with larger clutch sizes rear young to nest-leaving. The difference is have smaller Malthusian parameters than the re- small, but inasmuch as small differences may placement genotype because of the reduced re- have big evolutionary effects (Fisher 1930), we productive success or survivorship imposed by should probably ask whether this small differ- the extra egg(s). This is a hypothesis that should ence in survival of clutches of different size has be tested against empirical fact. So far, this hy- evolutionary significance. pothesis has led to several predictions that seem By “always” I am referring to a particular confirmed by the empirical evidence (Murray clutch laid by a particular female. I am not re- 1979, 1985, 1991a, 1999). ferring to a comparison between a five-egg According to this hypothesis, selection favors clutch laid in May with a four-egg clutch laid in the mean clutch size that just balances the im- LIFE HISTORY EVOLUTION-Murray 285

year, and, initially, young disperse to breeding territories rather than postpone breeding and act as helpers (Komdeur et al. 1995, Komdeur 1996). In contrast, climatic variation on the Galapa- gos is so severe that life expectancy of the Large Cactus Finch at hatching is short (only about 10% survive the first year, whereas 10% of Pa- lila survive to beyond age three and 10% of Sey- chelles Warbler to age eight [Fig. l]), some fe- males are forced to postpone breeding until suit- able conditions occur, and in some years no breeding occurs at all. Under such conditions, the Galapagos finches must evolve a large clutch Age size and rear multiple broods when conditions FIGURE 1. Survivorship curves for three species of favor breeding or become extinct. passerines (data in Table 1). A = SeychellesWarbler, The climate of the Hawaiian Islands is benign. B = Palila, C = Large CactusFinch. Breeding may be year-round in some species (e.g., Gma‘ o;‘ Ralph and Fancy 1994~) but short in others, three to seven months in the Elepaio‘ pact of environmental factors affecting longevity (van Riper 1995) and only two months in the (i.e., CA,) and the age of first breeding (i.e., (Y), Poouli‘ (Pratt et al. 1997b). Nevertheless, breed- both of which affect x;h,, and the probability of ing occurs each year, during which as many as rearing young successfully from brood i (i.e., si, two or three broods may be reared. Juvenile sur- which affects %P,). Such factors include the in- vivorship (0.36 in Palila and 0.40 in Gma‘ o‘ tensity of predation, disease, competition, and [Table 11) is greater than in the Large Cactus inclement weather, and the length of the breed- Finch, but adult survivorship may be more typ- ing season. The latter especially affects %P,. A ical of temperate zone birds (e.g., 0.62 in Palila long breeding season increases the number of and 0.66 in Gma‘ o)‘ or as great as in the Sey- opportunities (c,) to rear a successful first brood chelles Warbler (e.g., 0.8 in female Elepaio‘ and (i.e., increasing P,) and increases the probability Hawaii‘ Amakihi).‘ An intermediate clutch size of rearing several broods during a breeding sea- between those of the Seychelles Warbler and son, increasing Z?P,. Large Cactus Finch is not surprising in these Unfortunately, the reported demographic data species. on the Seychelles Warbler, the Hawaiian passer- The life histories of the passerines in the Sey- ines, and the Galapagos finches are not suitable chelles, Galapagos, and Hawaiian islands seem for a rigorous comparative analysis. Data on one consistent with the notion that the clutch size is or more important parameters are usually lack- adjusted to the populations’ life expectancy, age ing, based on small samples, or incorrectly cal- of first breeding, and probability of rearing one culated. Nevertheless, there are enough data (Ta- or more broods during a breeding season, which ble 1; Fig. 1) to support a preliminary analysis are constrained by environmental variables such that may spur further investigation. Further in- as the intensity of predation, disease, competi- vestigation may change the numbers, but it prob- tion, and inclement weather, and by the length ably would not change the interpretation. of the breeding season. Environmental conditions on the Seychelles Alternative hypotheses on the evolution of certainly allow for a long life in the Seychelles clutch size, such as Lacks’ hypothesis that the Warbler. According to this hypothesis, selection clutch size reflects the amount of food available should favor a small clutch size and few breed- for laying eggs and rearing young (Lack 1947, ing attempts. Although the climate is suitable for 1948, 1954, 1968) or the nest-predation hypoth- breeding year-round on Cousin Island, where the esis of Skutch (1949) and Martin (1992b), imply population is limited by suitable breeding habi- that the rest of a populations’ demographic char- tat, females normally lay only one egg per year. acteristics are adjustments to the evolved clutch Furthermore, Seychelles Warblers live so long size. Thus, according to these hypotheses, pop- that initial breeding can be postponed, which in ulations with small clutch sizes, which have turn allows for the evolution of helpers at the evolved in response to a limited food supply or nest (Komdeur 1992). On Aride and Cousine is- to a high incidence of predation on nest con- lands, however, where the species has recently tents, have evolved longer life (i.e., greater adult been introduced, breeding often begins at age survivorship) or longer breeding seasons and one, females often lay more than one egg per multibroodedness. It is difficult to imagine how 286 STUDIES IN AVIAN BIOLOGY NO. 22 a population could evolve a longer life when nual survival rates (from which we calculate A,). lacking sufficient food for rearing a larger family In order to understand the evolution of clutch or how a longer breeding season and multi- size, we will need to know further the influence broodedness could evolve in response to heavy of the factors affecting these parameters, such as predation on nest contents. the intensity of predation, disease, and compe- On the other hand, if reduced predation, dis- tition, and the length of the breeding season (i.e., ease, competition, and other sources of mortality egg-laying season). result in increased longevity, and if s, (the prob- ability of rearing any young from a clutch) is IMPLICATIONSFOR THE DYNAMICS OF POPULATION greater for smaller clutches, then longer life DECLINE AND RECOVERY should easily lead to the evolution of smaller This analysis of clutch-size variations of is- clutches. If a population lives in a region that land passerines is based on a conception of pop- provides suitable conditions for breeding for ulation dynamics different from that prevailing much of the year (say, the tropics), it could during the fifty years since Lack (1947, 1948, evolve small clutches because s, is greater for 1954, 1966) proposed that the clutch size reflect- smaller clutches and females could lay more re- ed the maximum number of young the parents placement clutches after failure (increasing c,) could rear on average and that the excess pro- and produce second, third, or more broods (in- duction was eliminated by density-dependent creasing l$P,), whereas a population in a region mortality, especially prior to the age of first with short breeding seasons (say, at higher lati- breeding. This view was consistent with the old- tudes), where few replacement clutches could be er view of a populations’ “biotic potential” be- laid and no more than a single brood could be ing kept in check by “environmental resistance” reared, should have a large clutch size. (Chapman 1928). Modifications to Lacks’ It seems more likely that humans, whales, al- clutch-size hypothesis do not change the dynam- batrosses, and the Seychelles Warbler have small ics. Cody (1966) suggested that the clutch size litter and clutch sizes because they have evolved was a function of the amount of energy available a long life, rather than because they have limited to the parents for reproduction, and Williams amounts of food available for rearing young or (1966) and Charnov and Krebs (1974) suggested suffer high predation rates. It seems more likely that the clutch size was an “optimum,” balanc- that pigs, mice, phasianids, and the Large Cactus ing the benefit of current reproduction against Finch have large litter and clutch sizes because the costs of decreased future reproduction. The they have a short life expectancy, rather than implication of these hypotheses seems to be that because they have access to a more abundant natural selection favors maximizing reproduc- food supply or have fewer predators than longer tion to the extent allowable by environmental lived species. conditions. Equation 1 provides another clue. The only In contrast, 1 proposed that natural selection life history parameter that can be predicted from for longer life (by reducing age-specific mortal- knowledge of the others is a populations’ mean ity) is the driving force in the evolution of life clutch size. The other parameters of Equation 1, histories, with clutch size being minimized to I%;h, and QP,, are composites of two or more the extent allowable by mortality, and that pop- life history parameters, age-specific survivorship ulation size was limited, not regulated, by the and age of first breeding in the former, and prob- availability of resources, predation, disease, or ability of rearing young from a clutch and num- other sources of mortality or reduced reproduc- ber of clutches laid in rearing a brood in the tive success (Murray 1979, 1982, 1986, 1991a). latter. All kinds of life history combinations (of These fundamentally different perspectives of juvenile survival, adult survival, age of first population dynamics may have implications for breeding, single- or multibroodedness) may have conservation biology, especially with regard to the same clutch size. Philosophically, it seems our understanding of the rates of decline and re- more likely that the clutch size is a consequence covery. Consider a simple model of population of the evolution of the other life-history traits. growth (Murray 1979). In Figure 2 the birth and This study points out the need for high quality death rates in pristine natural conditions (i.e., be- demographic data in evaluating evolutionary hy- fore human interventions) are shown by the sol- potheses. In order to predict clutch size from id lines. Between the lower critical density other demographic parameters, we need to know (LCD) and the upper critical density (UCD) re- the number of clutches laid per female in rearing sources are sufficiently abundant that individuals a first, second, or later brood (i.e., c,, c2, . . , have equal access to the resources that permit c,); the probability of rearing a first, second, or the expression of the maximum birth rate (given later brood from a clutch (i.e., sI, s*, . . , s,); their evolved fecundity) and minimum death the mean age of first breeding (i.e., 01); and an- rate. Above the UCD the birth rate decreases LIFE HISTORY EVOLUTION--Murray 281

LCD UCD Birth Rate A I

Birth Rate B ------__----_

Death Rate C -----______----______-----

______------Birth Rate C

Death Rate B ------_------0 Death Rate A

FIGURE 2. Relationship between a population’s birth (h), death (4, and growth (r) rates, r = ln( 1 + b--d), and its density. Birth and death rates A are natural rates unaffected by human intrusion. Birth and death rates B are those resulting from a moderate amount of anthropogenic increases in mortality. Birth and death rates C are those resulting from further anthropogenic increases in mortality, leading to eventual extinction. LCD = lower critical density, UCD = upper critical density, N, = mean steady state size of population in natural conditions, and N, = mean steady state size of population subjected to anthropogenic mortality rate B.

and death rate increases because of decreasing genie mortality, the death rate increases and the per capita availability of resources (e.g., food, birth rate decreases further. If the death rate ex- space) or increasing levels of predation, disease, ceeds the birth rate (Y < 0), as shown by the or other source of mortality. The population nor- short dashed lines in Figure 2, the population mally fluctuates in size around the mean steady- declines toward extinction (i.e., size and density state size, IV,. Below the LCD the birth rate may decrease). decrease and the death rate may increase be- The rate at which a population recovers from cause the population is so small that individuals decline (that is, increases in numbers, r) is a have difficulty in finding one another or in de- function of how well humans have managed to fending themselves from predators or other clean up the environment and to reduce preda- sources of mortality (e.g., Allee effects). tion, disease, and other sources of anthropogenic Second, consider that the exponential rate of mortality. The maximum rate of increase is r,n,x, change in numbers of a population (Y) is a func- that is the populations’ theoretical biotic poten- tion of the difference between the birth (h) and tial, unless management has also reduced the death (cl) rates (Murray 1997b), natural causes of mortality. Indeed, anthropogenic activity may affect all e=h=l+b-d,’ r = ln(1 + b - d), species, reducing predator populations as well as where e is the base of the natural logarithms and prey. A decline in predators could result in in- A is the finite rate of change in population size. creasing r,,, of the prey and greater N, but the Between the LCD and UCD in Figure 2, v,~, = latter only if predation limited population size. I ln(1 + b,, - d,,,,), which corresponds to the suspect that populations of most passerine spe- populations’ natural biotic potential. cies, if not most species of birds, are limited by In Figure 2 the long dashed lines show the territorial behavior (Murray 1979, 1982). The effects on birth and death rates of a moderate elimination of predators in territorial species increase in mortality (the birth rate decreases could result in a greater r,,,, but not in a greater with increasing mortality because of a changing population size, N,. The beauty of the model in age structure; Murray 1979). With moderate Figure 2 is that one can plot the consequences mortality, the mean steady-state population size, of multiple causes of mortality, as shown in N, is smaller than N,. With greater anthropo- greater detail in Murray (1986). 288 STUDIES IN AVIAN BIOLOGY NO. 22

TABLE 2. LIFE HISTORY PARAMETERS OF GROWING fecundity population exposed to the same inten- (I;nax = 0.05) LONG-LIVED (A) AND SHORT-LIVED (B) sity of anthropogenic mortality as the long-lived, POPULATIONS low-fecundity population. This result seems counterintuitive. Popuhon Indeed, Freed ( 1999) has pointed out that spe- PaIallleteI A B cies of endangered Hawaiian honeycreepers Survival during first year (sX = ,)a 0.40 0.15 (Kauai‘ Creeper [Oreomystis bairdi] and Kauai‘ Survival after first year (s, 9 1)8 0.80 0.50 Akepa‘ [Loxops caeruleirostris]) have small Age classa of first breeding (o) 4 2 clutch sizes and tend to be single brooded, com- Maximum age classa (0) 27 10 pared with the more abundant species (Kauai‘ Mean fecundity of breeders 1.1420 3.8685 Amakihi‘ [Hemignathus kauaiensis], Apapane‘ (Q)” [Himatione sanguinea], and Iiw‘ i)‘ living in Generation time (?“) 7.8861 2.9824 ohi‘ a-koa‘ forest on Kauai.’ These data and the Birth rate (b) 0.4058 0.8266 Death rate (d) 0.3545 0.7754 result shown in Figure 3 indicate to me that, for rm, 0.05 0.05 some reason, low-fecundity species must have a smaller r,, than high-fecundity species. Low- *x = age&as = age+ 1 (Murray1997b). fecundity species are at greater risk because of a naturally low r,, rather than a low fecundity We can examine the dynamics of population per se. We should consider how differences in change further by comparing, quantitatively, the r_, could evolve. effects on a populations’ growth rate (r) of in- First, if age-specific survival and longevity creasing amounts of pollution, predation, or dis- (i.e., s, and 1, respectively) reflect density-de- ease in populations with different life histories. pendent responses to the evolution of clutch size For illustration (Table 2), I have created for and, therefore, fecundity (i.e., m, = (mean clutch comparison a long-lived, low-fecundity popula- size X mean number of clutches)/%), as implied tion, A, and a short-lived, high-fecundity popu- by Lack (1947, 1948, 1954, 1966) and Cody lation, B. I have assumed for each an r,,,, of 0.05 (1966) or if clutch size, survival, and longevity in pristine environments. With increasing inten- are optimized, as suggested by Williams (1966) sity of mortality, the death rate increases, the and Charnov and Krebs (1974), the situation de- birth rate decreases, and, thus, r decreases (Fig. scribed in Table 2 and Figure 3 is possible. We 3). What is striking in this example is the much should expect to find some long-lived, low-fe- greater risk of extinction of the short-lived, high- cundity species with an u,,,, that is equal to or

Increase in Annual Death Rate

FIGURE 3. A comparison of the effect of r,, (i.e., between the LCD and UCD in Figure 2) of increases in the death rate from increasing anthropogenic causes of mortality in a long-lived, low-fecundity population A (circles) and short-lived, high-fecundity population B (squares). The data for each population when r,,, = 0.05 are given in Table 2. LIFE HISTORY EVOLUTION--Murray 289

TABLE 3. LIFE HISTORY PARAMETERS OF LONG-LIVED (C)AND SHORT-LIVED (D) STEADY-STATE (Y = o)POPU- LATIONS

Population 4 0.70 Parameter C D II ,m 0.65 Survival during first year (s, = t)8 0.310 0.126 '5 Survival after first year (sX , t)” 0.710 0.476 Age classaof first breeding ((w) 4 2 z 0.55 Maximum age class” (w) 27 10 9a 0.60 / Mean fecundity of breeders 1.4621 4.164 (m,Y Generation time (7) 6.4418 2.8971 Birth rate (b) 0.4834 0.8063 0.000 0.005 0.010 0.015 0.020 Death rate (d) 0.4834 0.8063 Increasein Age-specific Survival Rate r,ax 0.0000 0.0000 Decreasing Density .-b il~ = ngeclas\ = age+ I (Murray 1997b) FIGURE 4. A comparisonof the birth (squares)and death (circles) rates of long-lived populationC (lower) even greater than the r,,, of some short-lived, and short-lived population D (upper) when their age- high-fecundity species. In the long-lived popu- specific survival is increased above what is at N,. Data lation in our example, the mean annual m, is for populations at N, are in Table 3. 1.1420 of breeders (some females should be lay- ing three or more eggs [i.e., mean = 2 X 1.14201 per year) and is sufficient to maintain r,,,, at 0.05 posed (Murray 1979, 1991a, 1999), then we with its survivorship schedule. In the short-lived should expect r_, to be smaller in long-lived population, the mean annual m, is 3.8695 of species than in short-lived species, according to breeders (some females should be laying eight the following argument. or more [i.e., mean = 2 X 3.86951 eggs per We can examine the demography of popula- year) and is sufficient to maintain r,, at 0.05 tions of different life histories by creating two with its survivorship schedule. new populations, a long-lived (C) and a short- According to the theories of Lack, Cody, Wil- lived (D) steady-state population (Table 3). Ac- liams, and Chamov and Krebs, there is no ap- cording to the population dynamics model (Fig. parent reason for r,,, to be smaller in a low- 2), we should expect that the birth rate would be fecundity, long-lived population. For example, greater and the death rate smaller at population suppose a mutation occurs that allows the long- sizes less than N,, compared with the birth and lived females in population A (Table 1) to lay death rates at N,. Assuming that age-specific fe- on average an additional egg per year (m, = cundity within each population is the same at all (2.284 + 1)/2 = 1.642). Suppose further that the densities, we can calculate the birth, death, and larger fecundity reduces survival during the first growth rates when age-specific survival is in- year from 0.40 to 0.35 and survival of females creased, simulating the effect of densities below of breeding age from 0.80 to 0.75. Under these N,. For the same change in age-specific survival, conditions, r,,, = 0.0576. Thus, the benefit of the relative and absolute changes in birth and an increase in fecundity exceeds the cost of de- death rates are greater in the high-fecundity pop- creasing survival, resulting in an increase in r,,,. ulation than in the low-fecundity population, re- If the new, larger fecundity should evolve be- sulting in greater r (i.e., ln(1 + b - d)) in the cause it is “optimal,” we should expect to find high-fecundity population (Fig. 4). at least some low-fecundity species with a high As far as I am aware, the notion that the r,,,, and, therefore, with a lower risk of extinc- clutch size reflects the fewest eggs that a female tion than some high-fecundity species. can lay, consistent with replacement, is the only On the other hand, according to my theory, explanation for the evolution of a smaller r,, in selection acts on clutch size when the population long-lived populations than in shot--lived pop- is fluctuating around the populations’ mean size, ulations. Long-lived populations are not at great- N,, that is, when r = 0 over evolutionary time er risk of extinction than short-lived populations (Murray 1999). If natural selection favors the because of their lower fecundity per se but be- genotype whose females lay as few eggs as are cause of their smaller r,,,. However intuitive it consistent with replacement because they have is that low-fecundity species should be at greater the highest probability of surviving to breed risk for extinction and have slower rates of re- again, their young have the highest probability covery than high-fecundity species, current life- of surviving to breed, or both, as I have pro- history theory does not explain it. On the other 290 STUDIES IN AVIAN BIOLOGY NO. 22 hand, the comparison of the demography of spe- rally subjected to higher mortality than island cies at risk and not at risk comprises a small populations, have evolved larger clutch sizes sample. Further comparisons would be desir- and, thus, greater r,, The mortality effects of a able. newly introduced predator should probably not If selection results in a mean clutch size that be additive because the new predator would be just balances average mortality, as my theory as- expected to be competing with the already pres- serts (Murray 1979, 1991a, 1999), then we ent predators, reducing the old predators ’ pop- should expect that island species, which usually ulations and their effect on the prey. have evolved in environments with little preda- The conservation of endemic island popula- tion, disease, and other causes of mortality, tions will require preservation or restoration of should have greater mean life expectancy and suitable habitat and protection from predation lower fecundity than species exposed to greater and disease. natural mortality. Populations on islands, which have been assaulted by the introduction of dis- ACKNOWLEDGMENTS ease (e.g., avian malaria), brood parasites (e.g., I thank J. Burger, L. A. Freed, M. Gochfeld, l? R. Glossy Cowbird [Molothrus bonariensis]), pred- Grant, J. R. Jehl, Jr., and J. M. Scott for reading and ators (e.g., rats, cats, and humans), as well as commenting on the manuscript. I thank L. A. Freed, loss of habitat (e.g., to goats and humans), suffer T K. Pratt, and C. J. Ralph for drawing my attention disproportionately. Mainland populations, natu- to papers on the Hawaiian avifauna.