Oecologia (2002) 130:485Ð495 DOI 10.1007/s00442-001-0836-x

REVIEW

Gerald L. Kooyman Evolutionary and ecological aspects of some Antarctic and sub-Antarctic distributions

Received: 24 May 2001 / Accepted: 27 September 2001 / Published online: 13 November 2001 © Springer-Verlag 2001

Abstract probably originated in the core of edge. Less is known about penguins during the pelagic Gondwanaland when South America, Africa, and Ant- phase between breeding cycles. What we do know is sur- arctica were just beginning to separate. As the continents prising in regard to their dispersal, which ranges from drifted apart, the division filled with what became the hundreds to thousands of kilometers from the breeding . One of the remaining land masses colonies. moved south and was caught at the pole by the Earth’s rotation. It became incrusted with ice and is now known Keywords á Eudyptes á Platform transmitter as East . Linking it to South America was a terminal á á Time-depth recorder series of submerged mountain ranges that formed a neck- lace of islands. The northern portion of the necklace, called the Scotia Arc, is now the “fertile crescent” of the Introduction Southern Ocean. The greatest numbers and biomass of penguins are found here as well as that of , the pri- Penguins are one of the oldest, most aquatic, and argu- mary prey of most penguins, and many other ably most mystifying groups of . Their adaptation to marine predators. Today penguins are found throughout the sea was most likely a conversion from a procellariid the sub-Antarctic islands and around the entire Antarctic type of flying , such as a diving petrel (Simpson continent. Using satellite transmitters and time-depth re- 1976), to flying underwater, as modern penguins do. corders, while taking advantage of the parental dedica- There is no cladogram for penguins at the present time tion of breeding birds, numerous investigators have de- (Fordyce and Jones 1990). Most classification schemes scribed foraging habits of several species of penguins. are based on morphological characters. The exception is The information obtained is labor intensive and costly so the DNA-hybridization study used for the biochemical that studies are restricted to certain species, areas and classification of birds by Sibley and Ahlquist (1990). seasons. Here I review the patterns evident among six of Biochemical evidence indicates a much more detailed the most abundant and completely studied of the pen- classification with the addition of infraclasses, parvclass- guins. The variation in behavior is considerable from es and so on. The major difference from the classifica- those species that seldom dive deeper than 20 m in tion of other authors (Mayr and Amadon 1951; Cracraft search of prey to those that will dive to depths >500 m to 1981) is the placement of penguins in the Ciconii- catch mesopelagic and . Foraging trips from formes rather than Sphenisciformes (Sibley and Ahlquist breeding colonies vary among species and with the sea- 1990). In the Sibley/Ahlquist classification, the order son. Often the birds travel no more than 30 km and at Ciconiiformes includes 1,027 species of birds. other times the trips may exceed 600 km. Sub-Antarctic Fossil evidence places the origin of penguins at least species often reach more productive waters near or with- in the Eocene (Fordyce and Jones 1990), and Simpson in the Antarctic Polar Front zone, where the mixing of suggests the origin was likely as early as the Cretaceous Antarctic and sub-Antarctic waters provide rich resourc- (Simpson 1976). The hybridization evidence agrees with es for their prey. Antarctic species usually remain close a divergence from procellarids about 47 million years to shore, along the continental slope, or near the sea ice ago (mya) (Sibley and Ahlquist 1990). All fossil locali- ties are in the present range of penguins, but conditions G.L. Kooyman (✉) have changed considerably. Over the past 50 million Scholander Hall, 0204, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92093, USA years the continental land masses have shifted and frag- e-mail: [email protected] mented (Fig. 1). Presumably the birds evolved on the Fax: +1-858-5641305 edge of the continental land mass of Gondwanaland, but 486 tinent and adjacent waters became colder. The ultimate conclusion of this drift occurred when Antarctica reached its present position, South America and Austra- lia assumed their separation from Antarctica and the cir- cumpolar Southern Ocean formed and cooled (Eastman 1993; Knox 1994). Penguin diving ability enables some of them to forage at depths unavailable to other sea birds, but it is with some sacrifice. Their flightlessness has placed important restrictions on their distribution. Awkward on land, and relatively defenseless against even moderately sized terrestrial predators, their breeding habitat is restricted, with few exceptions, to cold temperate islands or isolated shorelines of the island continents of Australia and Ant- arctica. Only the , by breeding on sea ice, has separated itself completely from the terrestrial habitat. As the southern seas cooled, only two species evolved in ways to cope with high latitude conditions: the Emperor Penguin and Adélie Penguin. In large part, the other 15 species of penguins are associated with New Zealand, South Africa, Australia, southern South America, and islands of the sub-Antarctic region. This review will address penguin foraging behavior during the critical time when constrained by the need to provide food to rapidly growing chicks. During incuba- tion of the egg and nurturing of the chick, penguins share duties, which change from long periods at sea during in- cubation to shorter periods as the chick matures and its Fig. 1 Distribution of the continents about 100 million years ago food requirements increase. If the foraging trip of the (mya) when Gondwanaland was separating (top), and at about 60 mya (bottom), shortly before the earliest known fossil penguin partner is too long, the mate will abandon the egg or of 50 mya. The hatched area represents the central region where brooded chick. Even when the chick no longer needs its penguins probably evolved parent’s physical protection, an exceptionally long fast because of a delayed return by the adults will result in the weakening of the chick. If it does not starve, it may there is no evidence of the location of their origin be killed by nearby colony predators such as (Fordyce and Jones 1990). Most likely penguins fre- (Catharacta spp.) or giant petrels (Macronectes spp.). To quented near-shore islands which gave them protection maintain the chick’s condition it is vital that the parents’ from any continental predators that may have existed. foraging trips to sea become increasingly successful as With few exceptions they continue to enjoy (and require) the chick matures. High food intake is necessary to this isolation. Over the course of tens of millions of maintain body condition adequate to discourage preda- years penguins differentiated into many more species tors, to enhance overall growth and feather development, than exist today. There are 17 extant species, and 32 and therefore encourage the molt of the down and ulti- known extinct species (Simpson 1976). Incidentally, this mately the chick’s independent departure to sea. ratio is similar to that of the great avian diversity loss apparent in the Pleistocene. Over the course of 2 million years of great climatic changes, the number of species Tracking penguin foraging patterns declined by half to the present-day number of more than 9,600 species (Brodkorb 1971, as cited in Proctor and Perhaps the most significant technical advance in the Lynch 1993). Some of the earlier penguin species study of the behavior of marine birds and mammals at were probably substantially larger than the present-day sea has been the ability to track their movements with giant, the Emperor Penguin (Aptenodytes forsteri), which platform transmitting terminals (PTT). These transmit- is twice the mass of its congener the ters are tuned to a nominal frequency of 401.650 MHz. (A. patagonicus) and 30 times the mass of the smallest They range in mass from about 150 to 400 g. Much of present-day penguin, the ( this mass results from the thick casting necessary to minor). withstand pressures that occur when aquatic Penguins spread to many islands of the southern seas, dive to depth. The linear dimensions also vary with the as well as the southern continental coastlines of South size and number of batteries needed. A typical size is America, Africa and Australia. During this time the con- about 5 cm wide by 4 cm thick and 15 cm long. These 487 Table 1 Summary of the annual cycle and foraging range during conservative. Phase durations are the underlined values that are each phase of the cycle. Body mass is the average for the male and first in columns 3Ð7. Distances in kilometers are the bold last val- female parent during the crèche stage if reported. Unknown dis- ues of columns 3Ð8. References are cited by number in column 9, tances are indicated with a question mark. Dispersal patterns are and defined in the note below the table. The time and duration of just being determined by various means and the data presented are the cycles are from Williams (1995) Species; Breeding Incubation Guard Creche Fledging Molt Winter Referencesa mass (kg) dispersal

Macaroni, Oct/Nov 35/NovÐ 25/DecÐ 35/Jan/ 60/Feb/? 25/Mar/ AprÐSep/? (1) Eudyptes Dec/400 Jan/30 50 Colony chrysolophus; 4.6, 3.9 Royal, Sep/Oct 35/OctÐ 21/Dec/ 43/JanÐ 65/Feb/? 26/FebÐMar/ AprÐSep/? (2) E. schlegeli; Nov/650 100 Feb/300 Colony- 4.5, 4.0 Antarctica King, Nov/Dec 54/Dec/ 31/Jan/ 280/FebÐ 313/DecÐ 31/JanÐFeb/ Mar-Oct/ (3) Aptenodytes 650 689 Nov/650 Jan/? colony 2,300 patagonicus; unsexed, 13 brood Chinstrap, Oct/Nov 36/Dec/? 29/Jan/? 25/Feb/? 54/FebÐ 13/FebÐMar/ Mar-Oct/ (4) Pygoscelis Mar/? colony 2,100 antarctica; 4.4, 3.9 Adélie, Oct 33/NovÐ 22/Jan/ 29/JanÐ 51/Feb/? 20/FebÐMar/ Mar-Oct/ (5) P. adeliae; Dec/340 135 Feb/30 1200 1,500 unsexed, 4.2 Emperor, Apr/May 65/MayÐ 45/JulyÐ 105/SepÐ 150/Dec/ 35/JanÐMar/ MarÐApr/ (6) A. forsteri; July/100 Aug/100 Dec/200 3,000 1,200 1,500 unsexed, 25 a (1) Barlow and Croxall, unpublished; (2) Hull et al. 1997; (3) Moore et al. 1998; (4) Wilson et al.1998; W.Trivelpiece, personal com- munication) (5) Kerry et al. 1995; Davis et al. 1996; (6) Kirkwood and Robertson 1997; Kooyman et al. 1996; Kooyman et al. 2000 dimensions limit the species of animals to which the TDR, which must be recovered when the penguin returns units can be applied. For all species, but especially the to the colony. A drawback of the STDR is that they are small, fast swimming penguins, results must be interpret- much larger, i.e. about 250 g compared to 20Ð60 g for ed with caution because of the increased drag and extra the TDR. swimming effort induced by the transmitter (Culik et al. 1994; Bannasch et al. 1994; Hull 1997). The PTT’s transmission power is usually 0.25Ð1 W. Results of various studies This signal is received by one of the U.S. National Oce- anic and Atmospheric Administration (NOAA) satellites. Following is a review of data from six species of pen- Fortunately for high-latitude studies several locations are guins (Tables 1, 2). It is clear from the original publica- possible per day since these polar orbiting satellites tions that there is considerable variability in foraging be- make 5Ð10 passes daily within reception range for PTT havior. Rather than attempt to give details of specific transmission. The number of signals received per pass years, I have in most cases given dates the data were col- influences the accuracy of the location calculations. The lected, and the range of the results. most accurate locations are within 1 km radius of the PTT. Supplementing the geographic determination of bird Sub-Antarctic species movements are measurements from time-depth recorders (TDR), often called an archival recorder because the de- One of the most intensively studied species has been the vices now measure several other variables besides pres- (Eudyptes chrysolophus) breeding on sure and time. These recorders give a pressure profile of Bird Island of the South Georgia Island complex. Breed- the dive and hence a statistical estimate of the foraging ing commences in October/November with males return- depths, foraging time within a 24-h day, and the duration ing to colonies a week or so before females. Incubation of the dive. Other transducers incorporated into the TDR is composed of three long shifts of 10Ð20 days of which can record light intensity, water temperature and swim the male assumes the first and last shifts. In the advanced speed. Some versions (STDR) can transmit dive data to a stages of chick development the foraging trips usually satellite. The STDR overcomes the disadvantage of the range from 10 h to 48 h (Williams 1995). 488 Table 2 Variability of penguin diet, as measured in most cases during the chick phase of the breeding cycle. F Fish, K krill, S squid

Species Diet (% mass) Year Place name Location Reference

Macaroni 96Ð98 K 1977Ð1996 Bird Island, South Georgia 54.0¡S, 38.0¡W Croxall et al. 1997 Macaroni 13 K, 1994 Bird Island, South Georgia 54.0¡S, 38.0¡W Croxall et al. 1999 67 amphipod, 15 F Macaroni 87 K, 5 F 1983 Marion Is. 46.9¡S, 37.9¡E Brown and Klages 1987 Macaroni 62 K, 25 F, 13 S 1984 Marion Is. 46.9¡S, 37.9¡E Brown and Klages 1987 Royal 51 K, 45 F 1984Ð1986 Macquarie Is. 54.5¡S, 158.9¡E Hindell 1988a King >90 F 1991Ð1994 South Georgia 54.2¡S, 36.8 W Olsson and North 1997 King 87 F, 12 S, <1 K 1984, 1985 Marion Is. 46.8¡S, 37.9¡E Adams and Klages 1987 King 57 F, 32 S winter Possession Is. 46.4¡S, 51.8¡E Cherel et al. 1996 1990Ð1992 King 72 F; 28 S overall 1992 Heard Is. 53.1¡S, 73.5¡E Moore et al. 1998 41Ð100 F; 0Ð59 S seasonally King 98 F, 2 S 1984, 1985 Macquarie Is. 54.5¡S, 158.9¡E Hindell, 1988b Chinstrap 99.6 K 1977 King George Is. 62.1¡S, 58.5¡W Volkman et al. 1980 Chinstrap 68 K 1980 King George Is 62.1¡S, 58.5¡W Jablonski 1985 Chinstrap 17 K, 65 F 1981 King George Is 62.1¡S, 58.5¡W Jablonski 1985 Chinstrap 97 K, 2.9 F 1981 Signy Is. 60.7¡S, 45.6¡W Lishman 1985a Chinstrap 99.8 K 1982 Signy Is. 60.7¡S, 45.6¡W Lishman 1985a Chinstrap 99 K day; 1994 Seal Is., South Shetland Is 60.9¡S, 55.4¡W Jansen et al. 1998 74 K overnight Adélie 93 K, 1.4 F 1979 King George Is 62.1¡S, 58.5¡W Jablonski 1985 Adélie 92 K, 3.3 F 1980 King George Is 62.1¡S, 58.5¡W Jablonski 1985 Adélie 56 K, 4.4 F 1981 King George Is 62.1¡S, 58.5¡W Jablonski 1985 Adélie 60 K, 39 F 1965, 1966 Cape Crozier 77.5¡S, 169.6¡E Emison 1968 Adélie 99.6 K 1978 King George Is 62.2¡S, 58.5¡W Volkman et al. 1980 Adélie 98.3 K 1981 Signy Is. 60.7¡S, 45.6¡W Lishman 1985a Adélie 99 K 1982 Signy Is. 60.7¡S, 45.6¡W Lishman 1985a Adélie 66 K, 32 F 1983 Magnetic Is. 68.5¡S, 77.7¡E Puddicombe and Johnstone 1988 Adélie 85 K, 15 F (Jan) 1989 Hukuro Cove 69.0¡S, 39.6¡E Watanuki et al. 1993 49 K, 51 F (Feb) Adélie 86 K, 15 F (Jan) 1990 Hukuro Cove 69¡0 S, 39.6¡E Watanuki et al. 1993 2 K, 98 F (Feb) Adélie 76 K, 24 F (Jan) 1991 Hukuro Cove 69.0¡S, 39.6¡E> Watanuki et al. 1993 75 K, 25 F (Feb) Emperor 52 K, 38 F, 10 S 1986 Drescher Inlet 72.9¡S, 19.4¡W Klages 1989 Emperor 55 F, 45 S 1988 Auster 67.4¡S, 64.1¡E Robertson et al. 1994 31 F, 69 S Taylor 67.5¡S, 60.9¡E Emperor 68 K, 26 F, 5 S 1993 Auster 67.4¡S, 64.1¡E Kirkwood and Robertson (August) 10 K, 1997 20 F, 65 S (Nov) Emperor 8 K, 92 F (Nov) 1992 Cape Washington 74.7¡S, 165.4¡E Cherel and Kooyman 1998 Emperor 0.5 K, 96 F, 1993 Coulman Is. 73.3¡S, 169.6¡E Cherel and Kooyman 3 S (Nov) 1998

Preliminary results from satellite-tracking obtained in Croxall et al. 1993). The summer diet was almost exclu- 1999 indicate that during incubation both sexes traveled sively Antarctic krill (Euphausia superba) at Bird Island, 400 km or more from the colony to the north and north- south Atlantic (Table 2). Diet was much more variable at west; some tracks crossed the Antarctic Polar Front Marion Island, which is north of the APF in the Indian (APF) to reach sub-Antarctic waters (K. Barlow, unpub- Ocean. There they consumed cephalopods, , lished data) (Fig. 2). These results show a much greater and euphausiids (Table 2). foraging range than previously assessed by shipboard in- In the closely related (Eudyptes vestigators (Croxall et al. 1993; Trathan et al. 1998). Fe- schlegeli) which breeds only on (north males foraging during the guard stage (chicks attended of the APF), all trips from the Sandy Bay colony were to by at least one parent at all times) rarely traveled >30 km the southeast, mostly to the north of the APF (Fig. 2). from the colony. During the crèche stage (chicks left un- Here the surface temperature ranges from 2¡C to 6¡C guarded by parents), foraging area and range were more (Hull et al. 1997). During incubation the first foraging variable and birds frequently traveled up to 50 km from trips lasted about three weeks, and the birds ranged from the colony. 250 km to 650 km from the colony (Table 1). During the Daytime diving depths were 20Ð35 m (mean 29 m) guard stage the shortest foraging trips lasted 3 days, and and nighttime dives averaged <6 m (maximum 11 m; reached about 100 km from the colony. Later, during the 489 crèche stage, trips lengthened again to >300 km and a vation) (Table 2). While diving almost continuously week in duration (Fig. 2) (Hull et al. 1997). while at sea, the depth range of the birds tracks the daily Royal Penguins dive predominantly during daylight, light cycle closely. At night the diving depths are <50 m spending most of the time hunting at depths <60 m in (Kooyman et al. 1992; Putz and Bost 1994). Based on waters 4,000Ð5,000 m deep (Hull et al. 1997). The diet stomach temperature changes the main feeding time is consists primarily of myctophid fish, dominated by not during the shallow night dives, but during the day , and euphausiids, particularly when the fish are thought to be the deepest and most in- Euphausia vallentini (Table 2). These species commonly active (Putz and Bost 1994; Bost et al. 1997; Handrich occur at the APFZ. et al. 1997). Diet analyses completed at South Georgia, The breeding cycle of the King Penguin (A. patagon- Marion, Crozet, and Macquarie islands all showed the icus) was first described by Stonehouse (1960) at South main species consumed to be lanternfish (K. anderssoni) Georgia. The species breeds on most sub-Antarctic is- (Table 2). It is noteworthy that Royal Penguins, as stated lands; the cycle begins in early spring with the moult, above, also feed in the APFZ during the day, but dive no which takes about a month to complete. Courtship and deeper than 60 m, and frequently consume the same fish egg-laying take place normally during November and species, in addition to euphausiids. December. The single chick hatches in January/February and is fed until the beginning of the winter, by which time it can be as heavy as the parent. The chick remains Antarctic species in the colony throughout the winter. During winter peri- ods of food shortage chicks mostly fast with sporadic Chinstrap Penguins (Pygoscelis antarctica) are found feedings. Regular parental feedings are resumed in the mainly in the Scotia Arc with the highest population spring and continue until fledging in December and Jan- on the South Sandwich Islands. With the exception uary. Thereafter, the parents molt and soon after may be- of the scattered and small colonies of Gentoo Penguins gin a new breeding cycle, although this will occur con- (P. papua), the is the most northerly siderably later than in the previous year (Stonehouse occurring of the Antarctic penguins, and some of these 1960; Williams 1995). The chick of this cycle usually colonies are very large. After arrival and laying, the in- dies and its early loss enables the adults to breed at the cubation tasks are shared by the adults in shifts more propitious time of the following November. 4Ð15 days long (Table 1). Foraging trips in 1993 and In 1985, when a small or no recording device was 1994, while raising chicks ranging from 4 to 22 h from attached, foraging trips of study birds were 6.1Ð7.1 days colonies in the (Jansen et al. at Saint Andrews Bay, South Georgia (54.4¡S, 36.2¡W). 1998). During foraging trips the diving depths averaged Similarly, in a 1989 study at Possession Island (46.4¡S, 31 m and the deepest in 1988 was 121 m (Bengtson et al. 51.8¡E), Crozet Archipelago, the cycles were 6 days 1993). during the brooding stage (Kooyman et al. 1992). From Generally the diet during chick provisioning is January to mid-April in 1992 and 1993, also during 90Ð99% krill by weight, mainly E. superba (Table 2). the brooding stage, King Penguins with PTT traveled However, in some instances fish may contribute as much from Possession Island in a southerly direction for 144Ð as 39% (Table 2). At Seal Island there are two types 689 km (Table 1., Fig. 2). The trips lasted 7.9Ð32.4 days, of foragers, those that are out only during the day and averaging 16.8 days (Jouventin et al. 1994; Guinet et al. those that stay overnight. The overnight birds take a 1997). Most of these journeys were to the APFZ between substantial amount of fish that may represent about 25% 45 and 50¡S., where the water temperatures were from by mass of the stomach contents (Jansen et al. 1998) 4¡C to 5¡C (Guinet et al. 1997). Possibly the APFZ was (Table 2). closer in 1989 when the trip durations were shorter. Adélie Penguins (Pygocelis adeliae) are distributed However, as a caution about the importance of the APF, widely around the whole of the Antarctic continent, in- Ainley and Boekelheide (1983) based on ship surveys cluding the and its associated islands were unimpressed by the number of birds at the APF. north to the South Sandwich Islands (Woehler 1993) Still, birds recorded in 1994 from South Georgia swam (Fig. 2). During the November/December incubation north to 50Ð53¡S, in the region of the APFZ (Fig. 2). both adults tend the two eggs during alternating shifts The cycles lasted from 11 to 30 days. The South Georgia lasting 12 days (Table 1). Throughout the guard stage (54.15¡S, 36.8¡W) birds were experiencing a seriously foraging trips last <1 to 5 days. low food year in which there was nearly 100% loss of In the Ross Sea the birds tracked with PTT in 1988 chicks. The foraging trips were also long compared to ranged up to 272 km from the colony during the incuba- previous years when some were only 2 days (Olsson, un- tion period (Davis and Miller 1992). Birds from the published observation). Apparently, device encumbrance Béchervaise Island colony (67.6°S, 62.8°E), on the and prey abundance are important factors in trip dura- Mawson Coast, tracked with PTT in 1991Ð1993 ranged tion. from 161 to 341 km (Kerry et al. 1995). During the chick The foraging dives of King Penguins range in depth brooding period the distances ranged from 2 to 135 km from 50 m to 300 m (Kooyman et al. 1992; Putz and as the birds traveled to the shelf break (Fig. 2). It is note- Bost 1994; Bost et al. 1997; Olsson unpublished obser- worthy that the foraging cycles for these birds were as 490 491 much as double the duration for birds traveling without mostly krill in the early stages of chick development, PTT. In another study in 1989 and 1991 where VHF and shifting to fish toward the end of chick nurturing. transmitters were used for tracking birds in the guard After egg laying, the Emperor Penguin male assumes stage from a colony at Hukuro Cove (69¡S, 39.6¡E) birds all incubation duties until shortly after hatching only departed for 5Ð20 h. They fed within 1Ð2 km from (Table 1). Over the next 5 months the female and male the colony in a wide variety of conditions from tidal come and go to the colony about 10 times to feed the cracks and ice holes to the ice edge (Watanuki et al. chick. Each trip away tends to get shorter, declining from 1993) (Fig. 2). a length of about 3 weeks in August to as short as 3 days In 1990 and 1991 the foraging depths of Adelie Pen- in December (Kirkwood and Robertson 1997). Around guins ranged from about 3 to 98 m and averaged 26 m summer solstice the chicks fledge by leaving the colony, near Anvers Island, Antarctic Peninsula (Chappell et al. and the parents depart about the same time to molt 1993). Similarly shallow dives averaging from 7 to 12 m (Kooyman et al. 1990). occurred over three seasons of study at Hukuro Cove, During the early chick nurturing period of August to Enderby Land (Watanuki et al. 1993). mid-September 1993, at the Auster colony, trip durations Various studies around the continent show that the averaged 11Ð18 days. The time spent swimming in- Adélie Penguin diet usually consists of 56–93% by creased with day length from 8 h dayÐ1 in August to 12 h weight of krill, (E. crystallorophias and E. superba) dayÐ1 in September. In synchrony with the increase in (Table 2). However, fish are commonly taken, mainly time spent in the water, the dive rates increased from 92 the Antarctic silverfish (Pleuragramma antarcticum). In dives dayÐ1 in August to 149 dives dayÐ1 in September. some circumstances, fish may be 98% of the diet The most common maximum depth ranges for hunting in (Table 2). The differences in diet are seasonal with August and September were 20Ð200 m. The birds trav- elled up to about 100 km from the Auster colony (67.4¡S; 64¡E) (Kirkwood and Robertson 1997) (Fig. 2)

Fig. 2 The southern ocean region showing the sub-Antarctic is- (Table 1). lands. The colored filled areas indicate the foraging ranges deter- At a more southerly location near Coulman Island mined by recent studies. The dashed lines are hypothetical winter (73.4¡S; 169.8¡E) in the Ross Sea, birds traveled a maxi- ranges of various species based on satellite tracks and/or extrapo- lations from studies in other areas or from shipboard observations. mum distance of about 200 km from the colony while AP Adélie Penguin, CP Chinstrap Penguin, EP Emperor Penguin, foraging in November 1993. This is near the end of the KP King Penguin, MP Macaroni Penguin, RP Royal Penguin. The nurturing cycle and average length of these trips was still blue triangles are Adélie Penguin colonies exclusive of the Ant- 14.9 days. The average number of dives during these fi- arctic Peninsula and nearby islands, and the Ross Sea. In these ar- Ð1 eas the colonies are too dense to illustrate. The blue filled patches nal trips was 213 dives day (Kooyman and Kooyman are known summer foraging areas of breeding adult Adélie Pen- 1995). About 26% of foraging dives ranged from 21 to guins. The red dots are Emperor Penguin colonies. The solid red 40 m. However, 2.6% of the dives were >400 m. Dives areas are the known summer foraging zones of breeding Emperor occurred throughout the 24-h of daylight, but dives Penguins. Red dashed lines are the proposed northern winter dis- >400 m occur only between 0700 and 2000 hours local tribution of adult, breeding Emperor Penguins. The orange filled patches are the known foraging areas of breeding Chinstrap Pen- time. guins. Also, the blue areas with an orange border are known over- The primary foods of Emperor Penguins are the krill laps of summer foraging regions of Adélie and Chinstrap Pen- (E.superba), the Antarctic silverfish and some types of guins. The blue dashed line is the most likely northern winter lanternfish and squid. These vary according to colony boundary of Adélie, and juvenile and non-breeding Emperor Pen- guins. This perimeter is based on the northern limit of pack ice location and season from 20% to 96% fish by weight, (Gloersen et al. 1992). In the fall Emperor Penguin juveniles are 0.5Ð68% krill, and 3Ð65% squid (Table 2). known to travel beyond the pack ice to as far north as the PF. The orange dashed line is the observed winter distribution of adult Chinstrap Penguins from the South Shetland Islands. The solid purple areas are the summer foraging ranges of breeding King Discussion Penguins. The purple dashed line is the range of King Penguins in winter. Note that these summer areas at Kerguelen and Marion are When Gondwanaland began to breakup during the Creta- extrapolated from results of studies at Crozet, Heard and South ceous, Antarctica and Australia were already at a high Georgia. The Macquarie range is based observations while at latitude in the southern hemisphere. The oldest known sea (Ainley et al. 1984). Note also that the winter ranges at South Georgia, Marion, Kerguelen and Macquarie are extrapolated fossil penguin was deposited much later in the early from studies at Heard and Crozet. The filled green patches are Eocene, about 50Ð60 mya (Fordyce and Jones 1990). If, the known foraging areas of breeding Macaroni and Royal Pen- as suggested by Williams (1995) and Simpson (1976), guins in summer. Topography: isobath of 3,000 m in brown. 1 Pa- penguins are as old as 130 my, then their evolution is in- cific Antarctic Ridge; 2 Campbell Plateau; 3 Macquarie Ridge; 4 Kerguelen Plateau/Gaussberg Ridge; 5 Southwest Indian Ridge; timately connected with the separation and drifting apart 6 Conrad Rise; 7 Mid-Atlantic Ridge; 8 South Scotia Ridge; of the southern continents. In any case, the formation of 9 Falkland Plateau/North Scotia Ridge; 10 Antarctic Shelf. Sourc- the Scotia Arc and the associated islands, and the estab- es of the hand-sketched isobath lines were: Chase (1975); Smith lishment of the West Wind Drift that encircles Antarcti- and Sandwell (1997); and General Bathymetric Chart of the Oceans, Polar Stereographic Projection, Canadian Hydrographic ca, must have been central to the radiation of penguins Service, Ottawa, 5th edn, 1980. Antarctic Polar Front sketched (Fig. 1) as they exploited this “fertile crescent” of the from Moore et al. (1999) Southern Ocean. Presently, along the chain of islands 492 that formed the Scotia Arc, and among certain sub- On the other hand, during the glaciation, King Pen- Antarctic islands, large penguin colonies occur (Woehler guins had more ready access to polar waters of a more 1993) (Fig. 2). Curiously, there are few high latitude northerly positioned Polar Front (PF) and sea ice edge. islands between New Zealand and South America. Now, only the PF is available to the breeding animals, This is a vast area stretching across 60¡ of longitude, which while incubating eggs or nurturing chicks, are (6,000 km). As far as is known, there are few penguins limited to 1- to 3-week-long foraging trips. In fall and in this region. (One might note that in most illustrations winter with more time to travel they can reach the ice of the Antarctic and the Southern Ocean this is where the edge (Fig. 2), which in colder times may have been legend or an insert is placed to take advantage of the accessible while breeding. In a few places south of the empty space.) Even to the south of the Pacific gap, in below Marion Island, Crozet Archipela- Antarctica from 167¡ E to 75¡ W, there are few penguin go, Kerguelen Island and Heard Island, King Penguins colonies. Much of this “Antarctic Gap” is bordered may overlap in their fall and winter distribution with by the uninhabitable Ross Ice Shelf. Some of the rest Emperor Penguin juveniles dispersing from their south- may be artifact, at least for Emperor Penguins, because ern colonies (Fig. 2). It is conceivable that in times of of the lack of exploration for colonies along coastlines shortages the large number of adult King Penguins bordering the eastern Ross Sea and the Amundsen and coming from the northern colonies could with their Bellingshausen Seas. There are only two Emperor Pen- equal diving abilities and greater experience over- guin colonies, and half a dozen small Adélie Penguin whelm the Emperor Penguin juveniles from the colo- colonies known for this relatively unknown sector of nies along the Mawson coast. The ultimate result of an Antarctica. Indeed, this region has become habitable uncommon mortality among the juvenile Emperor Pen- only since the last ice age began to decline 19,000 years guins, if it persisted for a few years, would be a decline ago (Broecker and Denton 1990). As a coastline (coastal in the breeding adults at the natal colonies (Fig. 2). Marie Byrd Land and Ellsworth Land) of heavy pack ice Such a potential scenario is not likely for the juvenile and little exposed ground it has been inaccessible to and non-breeding Emperor Penguins of the Ross Sea as Adélie Penguins for breeding with the exception of a few they travel north and east to the PF in the “Antarctic isolated colonies. Although numbers of Emperor Pen- Gap” of the southern ocean. Here they may be the only guins have been seen in this area only one known colony penguin species to be found in the region, and in which exists. However, because of the heavy ice pack most sur- they only remain during the summer months before veys are conducted in the summer time after Emperor they move south to the expanding ice edge of the Penguins would have abandoned any colonies in the re- Southern Ocean. gion. In fact, the Cape Colbeck colony size and exact The overlap among Emperor Penguin colonies around location were unknown until visited by air by a group the continent is low, because of their wide separation and searching specifically for this colony in October 1993 small size of the colonies; the largest has only about (Kooyman, personal observation). 22,000 breeding pairs (Fig. 2). On the other hand, Adélie At the peak of glaciation the Ross Ice Shelf extended Penguins have considerable potential for intra- and inter- north to about 70¡S. Therefore, some of the largest species overlap. Adélie Penguins have nearly 150 colo- Adélie and Emperor colonies of the Ross Sea are a result nies around the Antarctic; 40 are along the Antarctic of recent settlement. However, there will be no fossil Peninsula, and 22 are in the western Ross sea (Woehler evidence for Emperor Penguins, because they habitually 1993). There is bound to be overlap in foraging areas breed on sea ice and all potential fossil material will sink with other colonies and, in the Peninsula, with other pyg- to the sea floor when the ice melts. On the other hand, oscelid penguins as well; even during trips as short as the oldest fossil remains of Adélie Penguins are found in 24Ð48 h (distances up to 130 km). In addition, Chinstrap the most southern colonies of the Ross Sea (Baroni and Penguins have over 100 colonies in the Antarctic Penin- Orombelli 1994). This apparent contradiction is because sula. Since both species feed to a great extent on krill, of the lack of exploration in other areas. and restrict themselves to modest depths of only about One of the profound effects of the last glacial period 20 m, they would seem to be especially susceptible to was not only the more northerly occurrence of the ice prey shortages. Lishman (1985b) suggests that the close edge and the greater areal extent in both winter and sum- proximity of breeding by pygoscelid penguins in this mer pack ice, but also that all Emperor Penguin colonies area could result in competition for food. Some inter- were along the continental edge and not at the high lati- specific overlap is relaxed by the breeding seasons tudes of some of the present colonies of the Ross and being offset, and some clear preferences in distribution Weddell Seas. A remnant of this legacy is the migration (Trivelpiece et al. 1987). Adélie Penguins breed a few of Emperor juveniles, recently fledged from their south weeks earlier, occur more in the southern range, and coastal colonies, to the APFZ (Kooyman et al. 1996). At feed around pack ice. Chinstraps, on the other hand, this time the juveniles at two-thirds the mass of the are located more to the north and feed in open water adults would probably have diving abilities, but not (Trivelpiece and Fraser 1996). Furthermore, Trivelpiece diving experience, similar to King Penguins. During et al. (1987) concluded that there is no evidence of these few months of summer and fall they may feed on competition for food or foraging area between Adélie the same prey, and at similar depths of 50Ð200 m. and Chinstrap Penguins. 493 Unlike the closeness of Adélie colonies around the Much of the food for some of the sub-Antarctic Antarctic, the vast distance between sub-Antarctic is- species occurs some distance from the colonies in the lands means that there will be no overlap in foraging vicinity of the circumpolar current, PF, or shelving areas areas except between colonies on each island. However, such as the Kerguelen Plateau (Fig. 2). In some years, these colonies can be immense. For example, the Maca- the distance to food sources may be extreme, and this roni Penguin colonies on Willis Island, just to the north liability leads to long travel times from some colonies. of South Georgia Island, harbor several million breeding For Royal and King Penguins long travel distances are pairs. What has been discovered through tracking with routinely in the range of hundreds of kilometers (Fig. 2). PTT and VHF transmitters is that the competition for the Reliance on such a distant food source can be risky for nearby food must be intense, if the food is not extremely breeding success, and this is illustrated by the failure of abundant. Added to the intraspecific competition are the King Penguins breeding at South Georgia in 1994. In variety and number of other potential competitors such that year chick mortality was nearly 100%, and trip du- as fur seals, baleen whales, volant sea birds, and other rations were 5Ð15 times longer than those of better species of penguins. The variety of predators reflects the years. So far, there are no satellite tracking data from vast abundance of food resources. This abundance is also the better years. This illustrates a problem with the de- illustrated by the short travel distances of penguins from termination of foraging areas and ranges. It is such a the colonies around the Scotia Arc. This differs especial- costly program that few studies have been accom- ly from Royal Penguins nurturing chicks at Macquarie plished, and none have been conducted over a period of Island, and likely some of the three other species of pen- several seasons. guin breeding on this island. The resources utilized by King Penguins are a good example of a species plac- these species have been reviewed in detail (Hindell et al. ing a heavy reliance on a distant food source that tends 1995), the prey ranges from inshore fish to offshore fish to be in colder waters than the breeding colony. They and krill. The offshore component of the diet is greatest may be susceptible to warming trends that push those in the King Penguin and suggests that this species forag- waters further south (except for those colonies on South ing area is as extensive as that of the Royal Penguin. Georgia). So far, this species has enjoyed a substantial, Based on shipboard observations in 12 crossings from worldwide population recovery from decimation due to New Zealand to the Antarctic, King Penguins may prefer exploitation in the previous century. If a warming trend foraging over the Campbell Plateau to the region south ensues in southern ocean waters to the degree that the PF of the PF (Ainley, personal communication). and other oceanic boundaries consistently move further It is likely that prey switching is frequent among pen- south, this may reduce reproductive success at some guins. Perhaps the most common prey among subantarc- King Penguin colonies. Ultimately recruitment would tic and Antarctic penguins is krill, but in years of low decrease and cause a population decline on all sub-Ant- abundance other prey will be taken. Most notable exam- arctic colonies where a more southerly PF and ice edge ples are the nearly exclusive consumption of krill during are untenable for successful reproduction. The pattern of chick rearing by Macaroni and Chinstrap Penguins, decline might be similar to what occurred at one of the which may change to higher proportions of fish or even more northerly of all Emperor Penguin colonies. At the amphipods (Table 2) in years of krill scarcity. Indeed, the colony near Dumont d’Urville, as a result of lower adult results of one of the longest ecosystem datasets show survival that is most closely correlated with increased that over a 20-year period from 1980 to 2000 the Maca- sea surface temperatures and reduced sea ice extent the roni Penguin population at Bird Island has declined and colony declined by 50% in the 1970s (Barbraud and the proportion of krill in the diet of this once exclusive Weimerskirsch 2001). krill feeder has shifted to a higher proportion of other In conclusion, information on foraging areas and prey (Reid and Croxall 2001). Another example of prey ranges of penguins is patchy and limited. Some of the variability is that of Emperor Penguins which show a most abundant species have received most of the atten- high degree of flexibility depending on location and sea- tion, as they should, considering their influence on the son. At the Drescher Inlet colony, which is near the shelf associated ecosystems. Studies are generally restricted to slope (Fig. 2), krill is the prevalent prey. At the Ross Sea a few specific areas, and usually for a single season. In colonies the nearest foraging areas are over the shelf. multi-season work, the annual variability is often high. Here the penguins feed almost exclusively on fish Most information on foraging is limited to the chick (Table 2). However, this can change seasonally as ob- phase of the breeding season. What is apparent is that the served at the Auster colony in 1993. Here, the squid con- birds are resourceful and have considerable ability to sumption rose from 5% of the diet in August to 65% in switch to different prey from their specialty. They are November. One of the reasons that Emperor Penguins also able to range widely if abundant prey is not near the can remain year-round at high latitudes is the range colony. The actual sea conditions that are most attractive of depths from which they find different types of prey. It for foraging are not clear. Some foraging areas are near is known that they take krill and fish from the undersur- the convergences of different oceanic conditions such as face of sea ice (Ponganis et al. 2000) and probably bent- the PF zone where temperature, salinity, currents, etc., hic prey at depths greater than 500 m (Kooyman and change abruptly. Other desirable areas are the pack ice Kooyman 1995). edge and abrupt changes in bathymetry, especially the 494 shelf slope of islands and the continents. Accordingly, Brown CR, Klages NT (1987) Seasonal and annual variation in I have incorporated some of these most prominent areas diets of macaroni (Eudyptes chrysolophus) and southern rock- hopper (E. chrysocome chrysocome) penguins at sub-Antarctic into Fig. 2, such as the 3,000 m isobath in the Southern Marion Island. J Zool 212:7Ð28 Ocean, and around the Antarctic Continent, as well as Chase TE (1975) Topography of the oceans. Scripps Institution of the APF. Oceanography, San Diego Outside the breeding season penguins are commonly Chappell MA, Shoemaker VH, Janes DN, Bucher TL, Maloney SK (1993) Diving behavior during foraging in breeding Adélie seen at sea and in the pack ice. Without knowledge of penguins. Ecology 74:1204Ð1215 the age and source of these birds this information has Cherel Y, Kooyman GL (1998) Food of emperor penguins (Apte- limited value for understanding the size of the habitat nodytes forsteri) in the western Ross Sea Antarctica. Mar Biol utilized by the birds, and the range of different age class- 130:335Ð344 es. There are only a few studies of the whereabouts of Cherel Y, Ridoux V, Rodhouse PG (1996) Fish and squid in the di- et of king penguin chicks Aptenodytes patagonicus during penguins from specific colonies after breeding (Kerry winter at sub-Antarctic . Mar Biol 126:559Ð570 et al. 1995; Kooyman et al. 1996; Kooyman et al. 2000), Cracraft J (1981) Toward a phylogenetic classification of the re- but this is changing (see Table 2). Today’s technology of cent birds of the world (class aves). Auk 98:681Ð714 remote sensing by satellites may be the most significant Croxall JP, Briggs DR, Kato A, Naito Y, Watanuki Y, Williams TD (1993) Diving pattern and performance in the Macaroni Pen- innovation in the past century for understanding the nat- guin. J Zool 230:31Ð47 ural history of marine vertebrates. The revelations from Croxall J, Prince P, Reid K (1997) Dietary segregation of krill-eat- data on the travels and habitat use by these animals have ing South Georgia seabirds. J Zool 242:531Ð556 been full of surprises, and such astonishing discoveries Croxall J, Reid K, Prince PA (1999) Diet, provisioning and pro- ductivity responses of predators to differences in availability illustrate the resilience of the different species to travel of Antarctic krill. Mar Ecol Prog Ser 177:115Ð131 great distances when the need arises, and to feed on a Culik BM, Bannasch R, Wilson RP (1994) External devices on variety of prey types. penguins: how important is shape? Mar Biol 118:353Ð357 Davis LS, Miller GD (1992) Satellite tracking of Adelie penguins. Acknowledgments Some of the ideas reflected in this study come Polar Biol 12:503Ð506 from research supported by the US National Science Foundation Davis LS, Boersma PD, Court GS (1996) Satellite telemetry of (OPP 96-15390 and OPP 98-09161 to GLK). 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