WHY PENGUIN EGGSHELLS ARE THICK

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1 The Auk 121(1): , 2004 WHY PENGUIN EGGSHELLS ARE THICK P. D B, 1,3 G A. R, 1 D L. S 2 1 Department of Biology, Box , University of Washington, Sea le, Washington 98195, USA; and 2 Department of Environmental Studies and Planning, Sonoma State University, Rohnert Park, California 94928, USA A. Like most other penguin species, Magellanic Penguins (Spheniscus magellanicus) are large-bodied birds that incubate their eggs for a prolonged period on hard substrates with li le nesting material all circumstances that could lead to high rates of egg breakage. However, Magellanic Penguin eggs at Punta Tombo, Argentina are seldom broken. From 1984 to 2001, only 2.6% of 10,023 eggs in our study areas broke or cracked. Most of those were broken in unusual or catastrophic events, mainly penguin fights and rainstorms. Low breakage rates appear to be a ributable to thick eggshells. Shells of Magellanic Penguin eggs averaged 0.81 mm without the egg membranes at least 56% thicker than expected for bird eggs of similar mass. The calcium required for those thick eggshells cannot be supplied by normal food intake because females lay eggs during a fasting period. It is also unlikely that sufficient skeletal calcium can be mobilized. An alternative potential calcium source is mollusk shells. To determine whether female penguins were selectively ingesting calcium to form thick eggshells, we examined stomach contents of birds during the egg period (se lement, egg laying, and early incubation) and the post-egg period (late incubation and chick rearing). Both females and males were more likely to have mollusk shells in their stomachs during the egg period than during the post-egg period. However, females were much more likely than males to have shells in their stomachs during the egg period, whereas the proportions of males and females with mollusk shells did not differ in the post-egg period. Selective ingestion of mollusk shells by Magellanic Penguins, resulting in thick eggshells, appears to be an adaptive response that reduces egg breakage. Received 16 January 2003, accepted 5 October R. Como la mayoría de las demás especies de pingüinos, Spheniscus magellanicus es un ave de tamaño corporal grande que incuba sus huevos por un período prolongado sobre sustratos duros y utiliza poco material de nido. Todas estas circunstancias podrían conducir a altas tasas de ruptura de huevos. Sin embargo, es raro que los huevos de S. magellanicus en Punta Tombo (Argentina) se rompan: entre 1984 y 2001, sólo el 2.6% de 10,023 huevos en nuestras áreas de estudio se rompieron o se rajaron. La mayoría de los huevos se rompieron en eventos poco usuales o catastróficos, principalmente peleas entre los pingüinos y tormentas de lluvia. Las bajas tasas de ruptura parecen ser debidas a los cascarones gruesos de los huevos. El grosor promedio del cascarón en S. magellanicus, sin incluir las membranas del huevo, fue de 0.81 mm, lo que es al menos un 56% más grueso de lo que se esperaría para huevos de aves de masa similar. El calcio necesario para formar estos cascarones gruesos no puede ser provisto por la tasa normal de ingestión de alimento porque las hembras ponen los huevos durante un período de ayuno. También es poco probable que sea posible movilizar suficiente calcio esquelético. Una fuente alternativa de calcio potencial son las conchas de moluscos. Para determinar si las hembras estaban ingiriendo calcio selectivamente para formar cascarones gruesos, examinamos los contenidos estomacales de aves durante el período de postura de huevos (establecimiento, postura e incubación temprana) y el período posterior a la postura (incubación tardía y crianza de los pichones). Fue más probable que los machos y las hembras tuvieran conchas de moluscos en el estómago en el período de postura que en el período posterior. Sin embargo, la probabilidad de tener conchas en el estómago fue mucho mayor en las hembras que en los machos durante el período de postura, mientras que las proporciones de hembras y machos con conchas en el estómago fueron similares en el período posterior a la postura. El cascarón grueso de los huevos de S. magellanicus, junto con la ingestión selectiva de conchas de moluscos, parece ser una respuesta adaptativa que reduce la ruptura de huevos. B composed mainly of calcium carbonate (Romanoff and Romanoff 1949). Consequently, dietary calcium is important to 3 boersma@u.washington.edu female birds at the time of egg production (see Simkiss 1961). Females of many species ingest calcium-rich items such as mollusk shells, calcareous grit, calcareous ash, and bones before egg laying (e.g. Johnson and Barclay 1996). Lack 148

2 January 2004] Why Penguin Eggshells Are Thick 149 of calcium can reduce reproductive success in passerines, and birds breeding in areas with calcium-poor soils may not be able to obtain sufficient calcium for eggshells from their diet (Graveland and Drent 1997). Compared to eggs of most other birds, the eggshells of some seabird species constitute a larger proportion of total egg mass. (Schönwe er 1960, Williams 1981, Williams et al. 1982). Despite the large mass of their eggshells, seabirds are nearly absent from the list of species known to selectively ingest calcium-rich items before egg laying (but see Brenninkmeij er et al. 1997), probably because their diet of fish and shellfish is high in calcium. The eggs of penguins (Spheniscidae), cormorants (Phalacrocoracidae), and some alcids (Alcidae), such as murres (Uria) and guillemots (Cepphus), have the highest proportions of shell mass among the seabirds (Schönwe er 1960, Williams et al. 1982). A thick eggshell was at one time thought to correlate positively with the developmental level (precocity) of the chick, but Ar and Yom-Tov (1978) found no correlation when they controlled for egg size. Williams et al. (1982) likewise found no correlation across seabird species between eggshell mass and chick development at hatching, nor is total egg mass correlated with the proportion of total mass formed by the eggshell. High eggshell mass may be an adaptation to hard nesting substrates. In seabirds with a calcium-rich diet, thick eggshells may be an inexpensive way to reduce egg breakage. Penguins are large birds that nest on hard substrates, o en using li le or no so nesting material, and incubate for a prolonged period (30 64 days; Williams 1995). Although female penguins o en fast for several days to weeks before egg laying, they may be able to obtain calcium through ingestion of mollusk shells prior to fasting. Those shells digest slowly and may release calcium that can be used for eggshell formation. Females may also ingest shells shortly a er egg laying to replenish depleted calcium levels. To test the hypothesis that eggshell thickness is an adaptive feature of penguin nesting ecology, we investigated eggshell mass, rates of egg breakage, and ingestion of mollusk shells in Magellanic Penguins (Spheniscus magellanicus) nesting at the species largest breeding colony, at Punta Tombo, Argentina. Magellanic Penguins typically lay a clutch of two eggs on hard surfaces with li le or no nesting material and incubate the eggs for ~42 days (Boersma et al. 1990). At Punta Tombo, their diet is dominated by schooling fish, primarily anchovy (Engraulis anchoita; Scolaro et al. 1999, P. D. Boersma pers. obs.). We hypothesized that (1) eggshells of Magellanic Penguins should be thick relative to those of other types of birds; (2) egg breakage rates should be low and comparable to those of birds that do not nest on hard surfaces; (3) female penguins should ingest more mollusk shells than do males around the time of egg laying; (4) a er egg laying, males and females should ingest similar, small amounts of shell; (5) females should ingest more shells during the egg-laying period than later in the breeding season; and (6) ingestion of shells by males should be independent of stage of breeding season. M We have studied the Magellanic Penguin colony at Punta Tombo, Argentina (44 02 S, W) since 1982 (Boersma et al. 1990, Boersma and Stokes 1995, Stokes and Boersma 1999). Each year, active nests in study areas within the colony are checked every 1 to 10 days to determine the fate of nest contents. At each check, presence and status of eggs are recorded. For each year, , the percentage of eggs that were cracked or broken, without signs of predation or human disturbance, within the normal incubation period (<45 days of laying of first egg) was recorded. Excluded were eggs broken outside the nest that clearly had been preyed upon as evidenced by discrete holes in the shells (bird predation), eggs broken in half and eaten (fox or skunk predation), or shells reduced to very small pieces (armadillo predation). The interval between laying of the two eggs was also calculated for 1,170 nests checked daily between 1984 and In October 1989, 30 eggs from 30 different nests were collected to determine eggshell thickness and mass of egg components. All eggs were the first laid in their respective nests and were collected within 24 h of laying. One egg was broken during transport and could be used only to measure shell thickness. Albumen, yolk, and shell were separated and weighed fresh (to the nearest g on a Me ler balance) and reweighed a er drying in an oven. Thickness of shells, excluding membranes, was measured with vernier calipers to the nearest 0.05 mm. A single location on the fla est part of the egg was chosen to reduce bias from measuring a strongly curved surface, and surface irregularities that would produce unrepresentative measurements were avoided.

3 150 B, R, S [Auk, Vol. 121 To estimate amount of skeletal calcium available for eggshell formation, skeletons of Magellanic Penguins (10 females, 8 males) were weighed. Those specimens were found dead at Punta Tombo and curated by the Burke Museum of Natural History and Culture, Sea le, Washington. Cleaned skeletons were weighed on a triple-beam balance to the nearest 0.1 g. To determine rate of ingestion of mollusk shells, stomach samples were collected from dead and live birds. Necropsies were performed on adult penguins found recently dead (within hours to two weeks, depending on temperature and exposure to sunlight) in the colony in 1984 and from 1987 through 1997 (n = 57). Some of those birds died when their burrows collapsed a er heavy rainstorms. Others were killed by predators, in fights, or by heat stress. For all stomach samples, sex of the individual, stomach contents including presence of shells or rocks, and date found were recorded. Stomach contents were also sampled from live penguins that were returning to the colony from foraging trips during two seasons, (n = 85) and (n = 48). Penguins walking inland were captured and their stomachs flushed using a minimally invasive water-offloading technique (Wilson 1984). Stomach contents were immediately identified or collected for later identification. Reported here are presence or absence of mollusk shell fragments by sex of penguin (determined by bill measurements and cloaca size; Scolaro et al. 1983, Boersma and Davies 1987) and time of season. Stomach samples from both dead and live birds were categorized according to whether they occurred at a time of possible high calcium demand caused by egg production. Most eggs are laid in early to mid-october (Boersma et al. 1990). Samples taken in September October were assigned to the egg period (se lement, egg laying, and early incubation), and those taken in November March were assigned to the post-egg period (late incubation, chick rearing, and premolt). Frequency of mollusk shells in stomach samples from live penguins was compared with frequency in samples from penguins we necropsied, to determine whether the two groups could be pooled for statistical testing. There were no significant differences for either sex or either period (G = , P > 0.1 for all comparisons). Therefore, necropsy and stomachflush data were combined for comparisons of stomach contents between sexes and between egg and post-egg periods. Log-likelihood (G) ratios were used to compare shell ingestion between sexes and stages of breeding season to avoid bias resulting from small expected frequencies, with Yates correction for continuity for 2 2 tables (Zar 1984). We arcsine-transformed proportions for statistical testing (Zar 1984). R Magellanic Penguin females at Punta Tombo lay their two eggs 3.7 days apart, on average (SE = 0.02, range 0 13 days, n = 1170; note that because nests were checked at ~24-h intervals, 0 days means <24 h). The mean thickness of Magellanic Penguin eggshells was 0.81 mm (SE = 0.24, n = 30) without egg membranes. The mean weight of 29 fresh Magellanic Penguin eggs was 128 g (SE = 1.63, range g). That is very close to the average mass of first eggs at Punta Tombo measured from 1983 to 1988 (mean = 125 g; Boersma et al. 1990). Eggshell accounted for 11.4% or g (SE = 0.1, range %) of total wet mass of the eggs. Albumen accounted for 63.8% (SE = 0.3) and yolk for 24.8% (SE = 0.3) of egg mass. The dried mass of the eggshell was 35.8% of the dry mass of the egg. Skeletons of females averaged g (SE = 6.6, n = 10), whereas skeletons of males averaged g (SE = 10.9, n = 8; Mann- Whitney U = 7.0, P = 0.004). The percentage of Magellanic Penguin eggs cracked or broken, excluding predation, over 18 years of study was consistently low, ranging from 0.2% to 5.5% per year. Out of 10,023 eggs laid, 257 were broken (2.6%). Among nests where only one of the two eggs was broken, first and second eggs were equally likely to be broken (paired t-test, t = 1.47, df = 17, P = 0.16). For most of the 257 broken eggs, we inferred cause of breakage from various forms of indirect evidence. In 25 cases, fights were observed or were indicated by fresh blood and cuts on the adult at the nest, by the presence of an adult other than the parents, or by an unusually vigorous nest relief display. Eggs are frequently broken when penguins fight in the nest or rush into the nest a er a fight. Eighty-six eggs were crushed, with the egg contents still in the nest and an adult present, indicating that those eggs were most likely broken by penguins and not by predators. Forty-three percent of egg breakage likely resulted from fights. We found 38 eggs broken a er observing them una ended for one or more days. Almost all abandoned eggs are eventually taken by predators, which may have been the fate of those eggs the evidence was inconclusive. Rain caused burrows to collapse, breaking 12 eggs. Eggs were sometimes buried in flooded burrows that did not collapse, then dug out by

4 January 2004] Why Penguin Eggshells Are Thick 151 adults, a process that may break eggs. The latter events were not recorded as weather-related breakages and therefore the importance of weather in egg breakage may be understated. Of 18 eggs that were cracked, probably by jostling in the nest, four hatched successfully. Minor causes of egg breakage included adults pecking the egg when researchers handled it (3); infertile, decomposed eggs bursting (2); and eggs laid without eggshells (1). In 72 cases, we were unable to infer cause of breakage. Breakage was significantly correlated with rainfall during the incubation period (Fig. 1; r 2 = 0.27, F = 5.76, P = 0.03), confirming the role of storms in egg breakage. There was high rainfall but low egg breakage in the years 1999 and 2000 (Fig. 1). In both those years, many eggs were deserted when adults reached critically low weights and le the colony to forage at sea. Deserted eggs are usually taken by predators; hence we found few broken eggs in those years. We compared frequency of mollusk-shell presence in stomachs of males and females during egg and post-egg periods (Table 1). Anchovy (Engraulis anchoita) was the main food item in all stomachs. During the egg period, females were significantly more likely to have shells in their stomachs than males (G = 5.7, P = 0.017). During the post-egg period, we found shells in few penguin stomachs, and there was no difference in the frequency of shells in the stomachs of males and females (G = 1.2, P = 0.28). F. 1. Percentage of eggs cracked or broken in study-area nests by amount of rainfall during incubation (October 10 November 30), at Punta Tombo, Each point represents a separate breeding season. Years of high nest-desertion rates are labeled (1999 and 2000). We also compared frequency of shell presence between the egg and post-egg periods for each sex (Table 1). Both females and males were much more likely to have shells in their stomachs during the egg period than during the post-egg period (females: G = 42.5, P << ; males: G = 16.8, P < ). Most shells were bivalves, especially clams and some mussels. In some cases the stomach had several dozen shells or shell pieces. Many of those shells did not appear to be remains of food items because the shells were fragmented; only one half of the shell of many bivalves was present; and some clam shells had a drill hole caused by invertebrate predators, which suggests that the bivalve s tissues were gone before the penguin ingested the shell. Rocks were rarely found in the stomachs of adults in either the egg or postegg period. For example, in 1993 and 1995, we performed necropsies on 15 males and 18 females and found no rocks in any of the stomachs. D Eggshell thickness. Magellanic Penguin eggshells are thick. Our results show that they are 56% thicker than expected for their size, based on a regression of shell thickness by egg mass in 47 species from 11 orders of birds (Ar et al. 1979). The expected eggshell thickness (including egg membranes) for an average Magellanic Penguin egg (128 g) is 0.52 mm (95% confidence intervals for predicted value: mm), far thinner than our mean of 0.81 mm. Furthermore, because our measurements did not include shell membranes, we may be understating the relative thickness of Magellanic Penguin eggs. Earlier estimates of eggshell thickness in the species are inconsistent with our results but are not based on actual measurements of large samples of fresh eggs. Tyler (1965) measured two Magellanic Penguin eggs and found a mean eggshell thickness of mm. He stated that

5 152 B, R, S [Auk, Vol. 121 the shells were shiny and appeared to have no cover. Fresh Magellanic Penguin eggs are rough and dull, not shiny, indicating that Tyler s eggshells had been altered in some way and were probably not intact. Based on a formula and not measurements, Schönwe er (1960) gave a mean thickness of 0.53 mm for 30 Magellanic Penguin eggshells. However, our measurements show that Magellanic Penguin eggshells do not conform to regression formulas such as that of Ar et al. (1979). Our measurement of eggshell weight as a percentage of whole fresh-egg weight (11.4%) is consistent with values from other studies of penguins, which range from 9% to 15.8% (Schönwe er 1960, Siegfried et al. 1978, Williams et al. 1982). Rates of egg breakage. Thick eggshells appear to protect eggs from breakage. Magellanic Penguin eggs are seldom broken by adults during normal activities. However, fights are a major cause of egg loss and lower reproductive success (Stokes and Boersma 2000, Renison et al. 2002). Incubating Common Murres (Uria aalge; Birkhead 1978) and Thick-billed Murres (U. lomvia; Gaston and Hipfner 2000) show reduced aggressive behaviors compared to nonincubating birds, an adaptation that reduces loss of eggs. Unusually heavy rainstorms may also cause substantial losses, as indicated by the correlation between egg breakage and seasonal rainfall. Our average egg-breakage rate of 2.6% for Magellanic Penguins is similar to that of 2.3% for Adélie Penguins (Pygoscelis adeliae; Davis and McCafrey 1986) and 1 5% for Common Murres (Harris and Wanless 1988). It is also comparable to breakage rates in species that are smaller than penguins, do not nest on hard substrates, have shorter incubation periods, or do not fight at the nest with conspecifics. Those include Peregrine Falcons (Falco peregrinus, 3%; Ratcliffe 1970); Hooded Mergansers (Lophodytes cucullatus, 1%), Wood Ducks (Aix sponsa, 1%), and Common Goldeneye (Bucephala clangula, 8.5%) (Zicus et al. 1988); and domestic turkeys (Meleagris gallopavo; 3.7% for small-bodied turkeys, 8.2% for large-bodied turkeys; Anthony et al. 1992). Thus, egg-breakage rates in Magellanic Penguins are no higher than rates in a wide variety of birds, even though penguins lay eggs on hard surfaces and use li le nesting material. Calcium acquisition. How do female penguins get enough calcium to form such thick eggshells? Calcium is mobilized under hormonal control prior to egg laying in female birds (Ghebremeskel et al. 1991, Zaias et al. 2000). Several studies have found plasma calcium levels to be higher in females than in males of various seabird species (Newman et al. 1997, Zaias et al. 2000). In Macaroni Penguins (Eudyptes chrysolophus), plasma calcium levels were higher in females than in males prior to breeding but not prior to molting (Ghebremeskel et al. 1991). Calcium levels were also higher in prebreeding females than in premolting females. Female Magellanic Penguins need ~10.5 g calcium to produce two eggs. Each eggshell weighs 14.6 g on average and penguin eggshells contain ~36% calcium (Siegfried et al. 1978). Animal skeletons contain 25 30% calcium (Brenninkmeij er et al. 1997, Crampton and Harris 1969). Female birds can mobilize 15% of their skeletal calcium for egg production (Brenninkmeij er et al. 1997). Hence, female Magellanic Penguins may be able to mobilize g of calcium (178.8 g 25 30% 15%) of the needed 10.5 g for two eggs. Because female Magellanic Penguins fast for a week or more prior to egg laying, diet cannot directly supply the calcium required for eggshells. Skeletal calcium may be adequate for the first egg, but not for the second; and in any event, depleted skeletal calcium must be replenished. Nonetheless, the similar rates of breakage of first and second eggs indicate that formation of second eggs is not calciumlimited, which suggests that an additional source of calcium is used. Mollusk shells contain ~36% calcium (Crampton and Harris 1969), 50 70% of which is assimilated during digestion (Brenninkmeij er et al. 1997). Thus, g of mollusk shells, or approximately 1 2% of the mass of a female Magellanic Penguin, would be sufficient to supply all the calcium needed for two eggshells. Both male and female Magellanic Penguins ingest mollusk shells, and both had more shells in their stomachs during the egg period than during the post-egg period. Penguins of both sexes may ingest shells to alleviate sensations of hunger during fasts that can last three to five weeks. In addition, shells may be retained in the stomach longer during the egg period than during the post-egg period because adults feeding chicks regurgitate shells with the rest of the stomach contents (P. D. Boersma pers. obs.).

6 January 2004] Why Penguin Eggshells Are Thick 153 Furthermore, fasting periods are shorter in the post-egg period; and even when not feeding chicks, nonfasting penguins sometimes regurgitate pellets of indigestible material (P. D. Boersma pers. obs.). Thus, the residence time of shells in the stomach is expected to be longer in the egg period and may account for the greater frequency of shells in the stomachs of males during the egglaying period than in the post-egg period. Taylor (1993) suggested that gastroliths might be important in buoyancy control. However, mollusk shells are dissolved by stomach acid, undermining their importance for buoyancy (Taylor 1993). Penguins have several adaptations to control buoyancy, such as dense bodies, feathers that hold li le air, and control of inhaled air volume (Wilson et al. 1992, Sato et al. 2002). Differences in mollusk-shell ingestion between sexes and between stages of the breeding season, along with the absence of rocks in penguin stomachs, suggest that shells are not ingested for buoyancy control. Female Magellanic Penguins ingested shells much more frequently than did males during the egg period, but not during the post-egg period. Because shells showed evidence of prior predation, they probably were not remains of food items. Magellanic Penguin females ingesting calcium-rich mollusk shells around the time of egg laying may gain the calcium they need for eggshell formation or replace calcium that was mobilized from bone. We predict that many seabirds that lay thick-shelled eggs, such as murres and other penguin species, ingest shells before egg laying. Thick eggshells: An adaptive trait. Thick eggshells, and the mollusk-shell ingestion behavior that makes thick eggshells possible, may have evolved for several reasons. The force required to break an egg is proportional to the square of eggshell thickness (Ar et al. 1979). Williams et al. (1982) proposed that seabirds that nest on hard substrates should lay thick eggshells to prevent breakage of eggs. Penguins, cormorants, murres, and guillemots all pursuit divers have, among seabirds, the heaviest eggshells as a percentage of whole-egg weight (Schönwe er 1960, Williams et al. 1982). Pursuit-diving seabirds have legs set far back on the body, making them clumsy on land and possibly more likely than other birds to break their eggs (Williams et al. 1982). Mallory and Weatherhead (1990) suggested that thick eggshells may have evolved in cavity-nesting waterfowl to reduce breakage when eggs are jostled in the nest. Penguins generally nest on rock, ice, or hard dirt, using li le or no so nest material, have an extended incubation period, and o en fight. Magellanic Penguins o en nest in burrows with limited space and may jostle eggs when moving within the burrow. Thus, because of how and where they nest and their proclivity for fighting in and near their nests, penguins would be among the most vulnerable to egg breakage without their unusually thick eggshells. Although thick eggshells may confer substantial benefits to penguins, added shell thickness presumably imposes costs as well. Williams (1981) argued that the long laying interval in penguins ( days on average) may result from the high amount of mineral elements that females mobilize for egg laying. In Magellanic Penguins at Punta Tombo, the interval between eggs averages 3.7 days, compared to 1 or 2 days in most nonpenguin bird species (Lack 1968). That long laying interval has at least two potential costs. First, it extends the fasting period of females by a few days. This may increase the likelihood of egg loss resulting from desertion, because a female in poor body condition will sometimes abandon the nest before being relieved by her mate (Yorio and Boersma 1994). Second, eggs that are laid four days apart hatch two days apart, on average (Boersma and Stokes 1995), meaning that the first egg is not incubated immediately, which increases risk of predation on the egg, especially in relatively exposed nests. Other potential costs of thick eggshells include time and energy that females must expend to collect and carry mollusk shells in their stomachs for extended periods. Those costs may be minimal, however. Mollusk shells are abundant both on the beach at Punta Tombo and on the shallow seafloor nearby, and added weight is not as important to the energetic balance of penguins as to that of flying birds. Many flying birds protect eggs from breakage by building so nests. At least some populations in most species of penguins breed in areas with li le or no terrestrial material that could be used to create so nests. Stones, pebbles, and bones are common nesting materials in Pygoscelis and Eudyptes species (Williams 1995). Some species line nests with vegetation where it is available, but sometimes make nests in rocky areas with li le vegetation. Magellanic Penguins gather

7 154 B, R, S [Auk, Vol. 121 nesting materials, but most individuals find no so material for their nests in the barren steppe environment where they breed (P. D. Boersma pers. obs.). Spheniscus species generally use unlined nests in burrows, crevices, caves, or surface scrapes. To build so nests, those penguins would have to find and carry material in their bills long distances overland, a much more energy-demanding proposition for a penguin than for a flying bird. Costs of collecting and transporting mollusk shells being minor, it may be more efficient for penguins to carry that dense material in their stomachs and lay thickshelled eggs than to find and carry so nest material in their bills to protect thin-shelled eggs. A This work was supported by the Wildlife Conservation Society, Exxon/Mobil Foundation, MKCG Foundation, Kellogg Foundation, and Friends of the Penguins, and made possible by a joint agreement between the Wildlife Conservation Society and the Office of Tourism, Province of Chubut, Argentina. We thank the many U.S. and Argentine students and volunteers who helped collect these data over the past 18 years, L. Astheimer for help in measuring egg components, D. Thayer for help in researching causes of egg breakage, G. Harris and the province of Chubut for assistance with local arrangements, and two reviewers who made helpful comments on the manuscript. L C A, N. B., P. A. R, D. A. E, D. O. N, K. E. N Research note: A comparison of the influence of nesting materials on breakage and shell cleanliness of eggs from large- and small-bodied lines of turkeys. Poultry Science 71: A, A., H. R, C. V. P The avian egg: Mass and strength. Condor 81: A, A., Y. Y -T The evolution of paternal care in birds. Evolution 32: B, T. R Behavioural adaptations to high density nesting in the common guillemot Uria aalge. Animal Behaviour 26: B, P. D., E. M. D Sexing monomorphic birds by vent measurements. Auk 104: B, P. D., D. L. S Mortality pa erns, hatching asynchrony, and size asymmetry in Magellanic Penguin (Spheniscus magellanicus) chicks. Pages 3 25 in The Penguins: Ecology and Management (P. Dann, I. Norman, and P. Reilly, Eds.). Surrey Bea y and Sons, Chipping Norton, New South Wales, Australia. B, P. D., D. L. S, P. M. Y Reproductive variability and historical change of Magellanic Penguins (Spheniscus magellanicus) at Punta Tombo, Argentina. Pages in Penguin Biology (L. Davis and J. Darby Eds.). Academic Press, San Diego, California. B, A., M. K, E. W. M. S Sandwich Terns Sterna sandvicensis feeding on shell fractions. Ibis 139: C, E. W., L. E. H Applied Animal Nutrition, 2nd ed. W. H. Freeman and Company, San Francisco, California. D, L. S., F. T. M C Survival analysis of eggs and chicks of Adélie Penguins (Pygoscelis adeliae). Auk 103: G, A. J., J. M. H Thick-billed Murre (Uria lomvia). In The Birds of North America, no. 497 (A. Poole and F. Gill, Eds.). Birds of North America, Inc., Philadelphia. G, K., T. D. W, G. W, D. A. G, M. A. C Plasma metabolites in Macaroni Penguins (Eudyptes chrysolophus) arriving on land for breeding and moulting. Comparative Biochemistry and Physiology 99A: G, J., R. H. D Calcium availability limits breeding success of passerines on poor soils. Journal of Animal Ecology 66: H, M. P., S. W The breeding biology of Guillemots Uria aalge on the Isle of May over a six year period. Ibis 130: J, L. S., R. M. R. B Effects of supplemental calcium on the reproductive output of a small passerine bird, the House Wren (Troglodytes aedon). Canadian Journal of Zoology 74: L, D Ecological Adaptations for Breeding in Birds. Methuen, London, United Kingdom. M, M. L., P. J. W Effects of nest parasitism and nest location on eggshell strength in waterfowl. Condor 92: N, S. H., J. F. P, J. W Hematological and plasma biochemical reference ranges of Alaskan seabirds: Their ecological significance and clinical importance. Colonial Waterbirds 20: R, D. A Changes a ributable to pesticides in egg breakage frequency and eggshell thickness in some British birds. Journal of Applied Ecology 7: R, D., P. D. B, M. B. M Winning and losing: Causes for vari-

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