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Holocene Adélie penguin diet in Victoria Land, Antarctica

Article in Polar Biology · July 2009 DOI: 10.1007/s00300-009-0607-4

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Holocene Ade´lie penguin diet in Victoria Land, Antarctica

Sandra Lorenzini Æ Silvia Olmastroni Æ Francesco Pezzo Æ Maria Cristina Salvatore Æ Carlo Baroni

Received: 17 November 2008 / Revised: 13 February 2009 / Accepted: 25 February 2009 Ó Springer-Verlag 2009

Abstract Ornithogenic soils (N = 97) dated up to 7000 Possible explanations of the variations of the abundance of Before Present (BP) were sampled in 16 relict and modern the fish prey in the diet are discussed in the context of the breeding colonies of Ade´lie penguin along the Victoria paleoclimatic events and as possible consequences of die- Land coast (Ross Sea, Antarctica). Taxonomic identifica- tary shifts due to the temporal variation of prey availability tion of fish otoliths (N = 677) recovered in these soils in the Ross Sea ecosystem. allowed to identify the Antarctic silverfish as the most eaten prey (90.1%) throughout the investigated period. A Keywords Ade´lie penguin Ornithogenic soils morphometric analysis of the otoliths revealed that the Prey remains Paleodiet Victoria Land Ade´lie penguin primarily selected prey averaging 67.23 ± 23 mm of standard length. Temporal distribution of Pleuragramma antarcticum showed a peak between Introduction 2,000 and 4,000 years BP, a period corresponding to the maximum spread of Ade´lie penguin in the Victoria Land. First defined by Syroechkovsky (1959), ornithogenic soils (bird guano-formed) represent the biggest resource of organic matter in both maritime and continental Antarctica. Since their discovery, these soils have represented an S. Lorenzini (&) C. Baroni excellent opportunity to study pedogenetic processes (i.e. Dipartimento di Scienze della Terra, soil formation), nutrient cycling and chemistry in very Universita` di Pisa, extreme environmental conditions (Ugolini 1972; Speir Via S. Maria 53, 56126 Pisa, Italy e-mail: [email protected] and Cowling 1984; Heine and Speir 1989; Tatur and Myrcha 1989; Zhu et al. 2005; Barrett et al. 2006; Michel C. Baroni e-mail: [email protected] et al. 2006; Liu et al. 2006; Simas et al. 2007). In conti- nental Antarctica, ornithogenic soils are provided by a S. Olmastroni F. Pezzo single animal source: the Ade´lie Penguin (Pygoscelis Dipartimento di Scienze Ambientali ‘‘G. Sarfatti’’, adeliae Hombron and Jacquinot 1841). In a long-term Universita` degli Studi di Siena, Via P. A. Mattioli 4, 53100 Siena, Italy occupied colony, penguin guano seeps through the per- meable pebbly nests and accumulates at their base to form S. Olmastroni e-mail: [email protected] ornithogenic soils. Thanks to the dry and cold Antarctic conditions, ornithogenic soils also preserve a long-dated F. Pezzo e-mail: [email protected] heritage of the Ade´lie penguin community (Spellerberg 1970; Stonehouse 1970; Bochenski 1985; Baroni 1994; M. C. Salvatore Baroni and Orombelli 1994a; Emslie 1995; Emslie et al. Dipartimento di Scienze della Terra, 1998). The extension of the organic layers is a function of Universita` di Roma ‘‘La Sapienza’’, P.le A. Moro 5, 00185 Rome, Italy the size, the age of establishment, and the persistence of the e-mail: [email protected] colony (Baroni 1994). Accurate stratigraphic sections of 123 Polar Biol ornithogenic soils have revealed different guano layers (up conditions inhibited the presence and settling of Ade´lie to five) that record multi-occupational phases of the colo- penguin colonies (Hall et al. 2006). nies (Baroni and Orombelli 1991, 1994a; Baroni and Hall Ornithogenic soils also well preserve hard parts of die- 2004). Radiocarbon-dated penguin remains, such as bones, tary remains, such as fish otoliths, bones, teeth, and squid guano, and eggshell fragments collected from these organic beaks. Calcareous fish otoliths and chitinous squid beaks in soils, provide a multi-millenary record of Ade´lie Penguin particular have demonstrated a strong preservation power. colonization that has been revealed to be particularly Taxonomic identification of such remains allows us to interesting for paleoenvironmental studies (Baroni and define a long-term Ade´lie penguin paleodietary record Orombelli 1991, 1994a;Baroni1994;Emslie2001; Lambert (Emslie et al. 1998; McDaniel and Emslie 2002; Emslie et al. 2002; Emslie et al. 2003; Shepherd et al. 2005; and McDaniel 2002; Polito et al. 2002; Emslie and Hall et al. 2006; Emslie and Patterson 2007; Emslie et al. Woehler 2005). 2007). Ade´lie penguins are sensitive indicators of the Previous paleoecological studies have yielded consi- Antarctic climate and of environmental parameters that derable dietary information on non-krill prey thanks to the regulate their presence and distribution (Ainley 2002). excellent preservation of remains found within ornithogenic Where ornithogenic soils are common features, Ade´lie soils. Concentrated in the area of the Antarctica Peninsula penguins have found encouraging ecological conditions for and in the East Antarctica, these studies have confirmed that their colonization. At these sites, the endurance of these from the mid-Holocene to the present day the Antarctic favorable setting environments is related to the thickness of silverfish (Pleuragramma antarcticum Boulenger 1902) these soils: an enduring occupation of a colony drops a and glacial squid (Psychroteuthis glacialis Thiele 1920) thick layer made from nest pebbles, penguin remains and have been important components in the Ade´lie penguin guano, and the older the colony, the thicker the accumu- diet, being the most common species represented in the lation of guano (Ugolini 1972). In particular, well- sediments (Emslie et al. 1998; Emslie 2001; Emslie and developed sequences of ornithogenic soils testify the McDaniel 2002; McDaniel and Emslie 2002, Emslie and ancient availability of ice-free coastal terrains suitable to Woehler 2005). Furthermore, the proportion of these prey nest and breed. In Victoria Land (Ross Sea), radiocarbon items in the past Ade´lie penguin diet varied in accordance dating of penguin guano, bones, and eggshells collected with climatic cooling and warming trends (cfr. Emslie et al. from these soils together with other datable organic mate- 1998; Emslie and McDaniel 2002). In the Ross Sea Region, rials provides data for reconstructing the retreat of glaciers detailed information on long-term Ade´lie penguin paleodiet in coastal areas after the last Glacial Maximum (&18– composition, prey fluctuations and possible environmental 20,000 years Before Present, BP) and the following emer- implications is lacking, with the exception of the southern sion of coastline during the Holocene period (starting about area. At Ross Island, a 1,000-year record of Ade´lie penguin 8000 BP) (Baroni and Orombelli 1991, 1994b; Baroni and diet indicates P. antarcticum as the most abundant non-krill Hall 2004; Hall et al. 2004). Radiocarbon dates from prey species, although it has been decreasing in importance abandoned penguin colonies scattered on the VL coast over the past 600 years, perhaps in response to the Little Ice (from the northernmost site at Cape Adare to the south- Age cooling period (Polito et al. 2002). The present study ernmost sites at Ross Island) indicate that Ade´lie penguins investigates for the first time an up-to-7000 BP Ade´lie occupied colonies in the Terra Nova Bay region since 7200 penguin non-krill paleodiet record, distributed in an about BP (Baroni and Orombelli 1994a). The occurrence of 600-km-long spatial dataset spanning from Cape Adare ornithogenic soils both in the vicinity of currently occupied (71°180S) to Dunlop Island (77°140S) along the Victoria colonies and in areas no longer colonized by penguins Land Coast, Ross Sea. The extent of the investigated spatial attests that, during the Holocene, the penguin population and temporal context allows us to reconstruct the as yet varied according to changing environmental conditions longest and widest Ade´lie penguin paleodietary record of (Baroni and Orombelli 1994a; Lambert et al. 2002; Polito Victoria Land. et al. 2002). Especially after the period between 4500 and 97 previously 14C-dated penguin guano samples, col- 2500 BP, indicated as a ‘‘penguin optimum’’ by Baroni and lected from several locations, have been analyzed through Orombelli (1994a), abrupt environmental changes caused a taxonomic identification and quantification of recovered drastic abandonment of several colonies and a dramatic fish otoliths. Compared to previous studies, the accurate decrease in the penguin population on the southern Scott stratigraphic sampling of ornithogenic soils has provided a Coast and in Terra Nova Bay (Baroni and Orombelli more detailed and precise paleodiet reconstruction. This 1994a). Between 2300 and 1100 BP, as documented by the archeological approach allows us to collect soil samples contemporary great spreading of elephant seals (Mirounga weighing only some 100 grams, preventing the complete leonina) in the Ross Sea Embayment, the establishment destruction of the relict colonies, which must be considered and persistence of sub-Antarctic climatic/environmental a unique record of the heritage of penguin settling. 123 Polar Biol

penguin nesting sites and tens of relict colonies have been discovered from Cape Adare to Ross Island. Well-sorted and rounded nesting pebbly patches clearly mark and characterize abandoned sites, allowing their still easy identification both at the margin of present-day penguin colonies and where present Ade´lie penguins do not nest.

Conservative excavation technique and sample collection

After identifying abandoned penguin settlements, we established test pits generally 1–6 m2 in area. The sampling was conducted in the late summer to reduce disturbance to birds during excavation near existing nesting areas. Cleaning the entire surface from the top and using stratigraphic excavation techniques commonly used in archeological research, we excavated layer-by-layer the organic soils and reached the underlying bedrock or undisturbed marine or glacial sediments. In this way, we could collect constrained-age guano samples and also identify and already separate during field work different penguin organic remains (bones, eggshells and guano), even within the same layer. The number of samples collected per locality depended on the discovery of nesting sites and on the number of organic layers rec- ognizable in each stratigraphic excavation. For this reason, each investigated locality can show a different Fig. 1 Map of the Victoria Land coast showing the geographic sampling setting with regard to the number of retrievable distribution of study sites. Ornithogenic soils were sampled at the guano samples. margin of presently occupied Ade´lie penguin colonies (solid circles), as well as in areas no longer occupied by penguins (relict colonies) Laboratory analyses (stars) Ninety-seven 14C previously dated penguin guano samples Materials and methods were processed in the laboratory to recover penguin dietary remains. Previously published papers (cfr. Baroni 1994; Study area and geomorphological setting Baroni and Orombelli 1991, 1994a; Lambert et al. 2002; Baroni and Hall 2004; Hall et al. 2004) provided samples 0 Extending southward from about 71°18 S (Cape Adare) to used in this study spanning up to 7200 BP corrected ages. 0 14 78°00 S (McMurdo Sound), the Victoria Land (hereafter All conventional dates (in C BP) were in fact corrected for reported as VL) coast borders the western side of the Ross the upwelling of old water in the Southern Ocean by sub- Sea (Fig. 1). tracting a marine-carbon reservoir effect of 1,300 years Aerial photograph analysis, several field surveys, (Berkman and Forman 1996), and thereafter all the values detailed geomorphologic analyses of key sites, and reported in the present study were marine effect removed. ornithogenic soil sampling were conducted in previous At the moment, this value represents the best estimate and studies in ice-free areas along the VL coast (Baroni and conventional value used for the Ross Sea region, based on Orombelli 1991, 1994a; Baroni and Hall 2004; Hall et al. dates of ‘‘pre-bomb’’ organisms (i.e. before 1950) of 2004) (Fig. 1). Ade´lie penguin-abandoned nesting sites known ages (Berkman and Forman 1996). Although cali- represent a common landscape feature of the ice-free VL brating the dates would be preferable, this approach coast. They occur both at the outskirts of present-day allowed us to compare the dates from the penguin remains colonies and in areas no longer occupied by penguins with sets of dates supplied by other organisms (i.e., ele- (Fig. 1). Resting on Holocene raised beaches, marine ter- phant seals; Hall et al. 2006) and with other proxy data, races, debris cones and slopes, piedmont rock-glaciers, and such as ice-core datasets (Lorius et al. 1985; Petit et al. ice-cored and depositional moraines, abandoned Ade´lie 1997). 123 Polar Biol

Sediments were washed (distilled water) and sieved suitable for the morphometric analysis because some were through seven nested screens with square mesh sizes strongly eroded or broken. Especially for the smallest ranging from 2 mm to 63 lm. The matrix from each screen otoliths (B250 lm), the smoothed borders made it impos- was dried and subsequently sorted under a low-power sible to orient the otolith correctly and to distinguish the (5–10x) stereomicroscope to separate eggshell fragments, dorsal and ventral margins from the anterior and posterior feathers, and dietary remains (otoliths, fish vertebrae and ones. To avoid any estimation bias, we selected and mea- teeth) (Fig. 2). sured only those otoliths with well recognizable Samples were classified according to the presence/ morphometric parameters. To avoid bias due to variable absence of dietary remains and are hereafter reported as amounts of sorted sediments, we express the relative den- sample with ‘‘dietary remains’’ (DR) or samples with ‘‘no sity as the ratio of MNI/dry mass by dividing the MNI dietary remains’’ (NDR), respectively. Otoliths were sep- value by the total mass (in gram) for each guano sample. arated from fish bones in order to carry out taxonomic identification. They were identified using anatomic-com- Statistical analysis parative tables proposed by Williams and McEldowney (1990) for Antarctic fish taxa. These prey remains are In order to evaluate the possible factors affecting the quantified by the minimum number of individuals (MNI) presence of fish remains in the ornithogenic samples, we represented for each identified fish taxon. According to built three logistic models (Tabachnick and Fidell 1996) Emslie et al. (1998), the MNI is determined by counting the using as binary-dependent variable the presence/absence number of whole otoliths of known side (right or left) and of: (a) dietary remains, (b) P. antarcticum, (c) other iden- using the greater value of the two sides. In addition, oto- tified species and as independent variables the latitude and liths of unknown side were counted and their number was the age of the samples. In model (b) and (c) samples halved to give a conservative estimate of the total number containing only unidentified fish bones (n = 18) were of right and left sides represented, which was then added to excluded from these analyses. Fish taxa different from the MNI obtained from known-side otoliths to yield a total silverfish were very low in number and thus were grouped MNI for each species. into a unique category named ‘‘other fish’’. Otoliths were measured using a stereomicroscope with a Differences in the standard length of silverfish with micrometric eye piece (10x) to an accuracy of 0.1 mm. The respect to latitude were analyzed with the Mann–Whitney maximum distances between the rostrum and the posterior non-parametric test. All tests were two-tailed and the sta- margin (otolith length, OL) and between the dorsal and tistical significance was set to a = 0.05. For this analysis ventral margins (otolith width, OW) were measured. By samples were grouped by dividing the Ross Sea into two using given regression formulae, morphometric analysis of main regions, the north and the south, with respect to the the otoliths provides a mean estimate of prey item size Drygalski ice tongue, which extend from Cape Adare to (Williams and McEldowney 1990). Since very few other Inexpressible Is. (North, N) and from Cape Irizar to Dunlop fish taxa remains were found, only P. antarcticum otoliths Is. (South, S). All the analyses were performed using the were considered. The corresponding standard length (SL) software SPSS 12.0. All mean are given as ±1 SD. in millimeters was determined according to the regression equations calculated by Williams and McEldowney (1990). Fish otoliths show clear erosion signals, ranging from 2 Results to 4 according to Leopold et al. (1998), but most of them still preserve the morphological parameters required for Matrix screening and sorting allowed us to recover a large taxon identification. Not all recovered fish otoliths were amount of well-preserved organic material, including

Fig. 2 Organic remains recovered in ornithogenic soils from the Victoria Land coast. Specimens were photographed using SEM and used as reference material: a left side Pleuragramma antarcticum otolith; b fish vertebra; c fish tooth; d penguin eggshell fragment

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Table 1 Number of dietary remains recovered in ornithogenic soil samples discovered in Victoria Land Collection site Latitude No. of guano Radiocarbon Total mass No. of recovered No. of recovered samples (NDR) date range (BP) (g) fish otolith fish bones

Cape Adare 71°180S 1 1,180 38 1 1 Duke of York 71°370S 1 920 121 – 11 Cape Hallett 72°190S 4(1) 320–400 315.5 11 4 Edmonson point 74°200S 5(1) 770–990 801 12 13 Gondwana station 74°380S 2 3,330–3,370 280 – 112 Terra Nova station 74°420S 9(1) 3,580–5,180 1,716 50 178 Icarus Camp 74°430S 21(9) 2,780–6,060 4,389 47 29 N Ade´lie Cove 74°460S 7(2) 4,525–7,190 1,490 8 17 Inexpressible Island 74°530S 9(5) 1,220–5,058 2,078 9 6 Cape Irizar 75°340S 7 860–4,010 1,830 299 1 Prior Island 75°410S 6(1) 2,980–4,525 834 118 3 Cape Hickey 76°050S 10(7) 1,985–6,240 1,627.4 29 2 N Cape Day 76°150S 1 3,060 226 41 – Depot Island 76°420S 5(4) 2,020–5,840 766 10 1 Cape Ross 76°440S 5(1) 2,835–3,015 753.5 36 27 Dunlop Island 77°140S 4 2,230–4,330 703 6 29

Analyzed guano samples are grouped by collection site with the age range (BP) and total dry mass (g) of sorted sediments. The numbers of samples without dietary remains are reported in parentheses

penguin bones, feathers, eggshell fragments and hard parts Table 2 Fish taxa identified from otoliths recovered from ornitho- of dietary remains such as fish bones (vertebrae), scales, genic soils sampled at Ade´lie penguin colonies along the Victoria and otoliths. Since krill and their fragile carapaces are not Land coast, Ross Sea, Antarctica preserved in sediments, the ornithogenic soils investigation Taxon Number of otoliths (%) MNI (%) provided data only about the non-euphausiid (i.e. fish) Pleuragramma antarcticum 610 (90.10) 355 (91.26) paleodietary components. The thickness of ornithogenic Trematomus sp. 10 (1.48) 10 (2.57) soils ranged from centimeters to decimeters and the mean Pagothenia sp. 23 (3.40) 17 (4.37) mass of the samples was 186 g (range 6–885 g). Among a total of 97 samples, 32 did not contain dietary remains Unidentified Nototheniidae 34 (5.02) 27 (6.94) (NDR) and 18 contained only fish vertebrae (Table 1). In Total 677 409 NDR samples, neither fish bones nor otoliths were recov- The total numbers of identifiable otoliths and MNI are provided for ered, but eggshell fragments and feathers testified to the each taxon; percentages are reported in parentheses ornithogenic nature of those samples and confirmed the presence of nesting sites. (1.48% of MNI). Among the individuals of the genus Among the 16 visited localities, Cape Irizar, Prior Trematomus, six were recognized as Trematomus ber- Island, Cape Ross, and Cape Day were the most productive nacchii. The rest of the recovered otoliths (5.02%), too in terms of the number of fish otoliths. Samples from eroded to estimate side and size, are taxonomically Gondwana station samples were the richest in fish bones, uncertain but among the family Nototheniidae. but no otoliths were found. At Inexpressible Island, Cape Hickey, and Depot Island, there was a clear prevalence of Comparison among dietary items, latitude and age NDR compared to the DR samples (Table 1). Otoliths were found in 47 samples and were analyzed Results from model (a) showed that neither latitude nor age to identify prey taxa. A total of 677 otoliths correspond- had an effect on the presence/absence of fish remains in all ing to 409 individuals (8.7 ± 12.58 preys per sample) the ornithogenic samples (n = 97) (Table 3). On the con- belonging to four taxa were identified (Table 2). Taxo- trary the model (b) revealed that the age of the samples nomic identification indicated that all penguins fish prey significantly explained the presence of P. antarcticum, belonged to the family Nototheniidae and consisted while the latitude did not appear to have any explanatory mainly of P. antarcticum (90.10% of MNI) followed effect (Table 3). The model (b) correctly reclassified by Pagothenia sp. (3.40% of MNI) and Trematomus sp. 80.4% of the samples with P. antarcticum and 62% of the 123 Polar Biol

Table 3 Logistic models testing the effect of latitude and age on the 30 Pleuragramma antarcticum presence/absence, in the ornithogenic samples, of models a, b, c 25 Variable B Wald statistic df P 20 Model a) Latitude -0.840 0.140 1 0.709 15 Age of samples 0.000 2.701 1 0.100 10 Constant 7.914 0.223 1 0.637 Model b) Latitude 0.032 0.017 1 0.896 5

Age of samples 0.000 5.463 1 0.019* Frequency of occurrence (%) 0 Constant -0.651 0.001 1 0.972 0 10 20 30 40 50 60 70 80 90 100 110 120 130 140 150 160 170 180 SL classes (mm) Model c) Latitude 0.653 3.757 1 0.050* Age of samples 0.000 0.010 1 0.921 Fig. 4 Antarctic silverfish size class distribution in ornithogenic Constant -50.665 3.955 1 0.047 samples. For each class, the lower limit (mm) is reported Model a, fish remains (n = 97; 65 with fish remains and 32 without); Model b, Antarctic silverfish (n = 79; 46 with silverfish and 33 without); Model c, other species (Nototheniods different from Ple- Prey size classes in ornithogenic soils uragramma antarcticum)(n = 79; 16 with other species and 63 without) A morphometric analysis of 380 Antarctic silverfish * Significant effects are indicated otoliths showed that the mean silverfish SL was 67.23 ± 23.47 mm (range 40.18–182.67). Furthermore, our data indicate that 82.89% of the silverfish eaten by all samples. In fact the age distribution of the samples Ade´lie penguins belonged to the 40–80 mm length class confirms that fish remains increased in samples dated (Fig. 4). between 2000 and 4000 BP, a period that includes the time There was no significant difference in the distribution of lag defined as the ‘‘penguin optimum’’ by Hall et al. (2006) the size classes of P. antarcticum according to age of the (Fig. 3). samples. Grouping colonies according to a north to south Fish species different from P. antarcticum composed a gradient, samples from the northern colonies (n = 70 mean very small percentage of the organic material sorted in the 71.39 ± 23.007 mm) contained longer Antarctic silverfish ornithogenic sediment. Species other than silverfish compared to the southern colonies (n = 310, mean occurred only at southern latitudes between 74°420 and 66.285 ± 23.508 mm); this difference appears to be sig- 77°140S. When included in the logistical model (c) the nificant (U Mann–Whitney = 7,828.50, Z =-3.521, presence/absence of other fishes was significantly P = 0.000). explained by the latitude alone (Table 3) and the model correctly reclassified 79.7% of the samples. Discussion and conclusion

Guano samples collected from ornithogenic soils have proved to be a valid source of penguin dietary remains (Emslie et al. 1998; Emslie 2001; Emslie and McDaniel 2002; McDaniel and Emslie 2002; Emslie and Woehler 2005). In this study, we sampled ornithogenic soil in the area from Cape Adare to Dunlop Island, spanning over 600 km. Radiocarbon dating for the Ross Sea ranged from ca. 7200 to 320 BP (Baroni 1994; Baroni and Orombelli 1991, 1994a; Lambert et al. 2002; Baroni and Hall 2004; Hall et al. 2004). Most of the samples (57%) occurred between 2000 and 4000 BP (Fig. 3) and between 74°420 and 77°140S (86.6%). The abundance in guano sample’s Fig. 3 Samples with fish remains (DR) (n = 65; black bars) and availability during this period may be a consequence of the samples with P. antarcticum (n = 46; light bars) grouped for each great spread of Ade´lie penguin colonies recorded for the 1,000 years (from 320 to 7,200 BP). NDR samples of the period are VL between 2300 and 4000 BP and indicated as the ‘‘pen- reported in parentheses. The time periods of occupational history for Victoria Land as described by Hall et al. (2006) are reported in the guin optimum’’ (cfr. Baroni and Orombelli 1994a; Hall background et al. 2006).

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Except for fish otoliths and bones, no other dietary supported by the dry and cold condition of Antarctic remains were recovered in this study, although Polito et al. environment, where the arid climate and low temperatures (2002) identified several squid beaks in organic sediments slow the damage action of soil processes on organic at Ross Island. One possible explanation for the lack of remains. squid remains in our sample could be the lower preserva- Latitude did not significantly affect the mean relative tion of the cephalopod beak compared to fish otoliths abundance of Antarctic silverfish, indicating that in the past (Emslie and McDaniel 2002), or it is possible that squid did this species represented an important food source for not contribute to the diet of Ade´lie penguins in the inves- penguin breeding throughout the VL coast. This prey tigated period and locations. Assuming that Ade´lie species has fluctuated in importance over the past penguins are still feeding upon the same preys since the 6,000 years (Fig. 3). This pattern seems to agree with Hall Holocene, recent literature reports that squid are preyed et al. (2006), who delineated the Ade´lie penguin and ele- during the summer in East Antarctica and the Weddell Sea, phant seal occupation history for the VL coast. Decreasing but have not been reported for the Ross Sea (cfr. Ainley periods of silverfish remains in the present study (Fig. 3; 2002). In this region, two krill species (Euphausia superba 1000–2000 and 5000–6000 BP) correspond approximately and E. crystallorophias) and fish compose the Ade´lie to the seal optimum (1100–2300 BP) and to the coeval penguin diet, mixed together in different proportions occupation (i.e. contemporary occupation by both species) (Ainley 2002; Olmastroni et al. 2000). (4000–6000 BP) reported by Hall et al. (2006). Both of these periods were characterized by a sea ice decrease in Temporal and spatial variation of prey the Ross Sea, particularly severe during the most recent period. On the other hand, our data show an increase in the Taxonomic identification of fish otoliths indicated P. ant- silverfish remains abundance in the past 1,000 years and arcticum as the most eaten prey throughout the investigated during the ‘‘penguin optimum,’’ this latter being the highest period. The abundance of Antarctic silverfish remains value among all the investigated periods. The ‘‘penguin identified in this study agrees with previous paleodietary optimum’’ and the most recent ages were characterized by investigations in the Antarctica Peninsula, East Antarctica, higher sea ice in the Ross Sea region, producing a more and in the southern Ross Sea region (Emslie and McDaniel fitting habitat for the sea ice obligate Ade´lie penguin (Hall 2002; McDaniel and Emslie 2002; Polito et al. 2002; et al. 2006). The shifts in the presence of fish remains and Emslie and Woehler 2005), as well as with present-day in particular of P. antarcticum might also represent chan- data, since this species today accounts for more than 90% ges in Antarctic silverfish population according to the sea of the local fish community in the Ross Sea (Vacchi et al. ice advance and retreat (Eastman 1993). Zane et al. (2006) 2004) and represents a key species in the diet of Antarctic used mitochondrial DNA sequencing to hypothesize that a apex predators (La Mesa et al. 2004). In particular, during demographic expansion that occurred for P. antarcticum the chick rearing period, P. antarcticum can contribute up during a cooling period (last glaciation peak, 111000– to 50–75% by mass to the Ade´lie penguin diet, even 126000 BP), suggesting a strong link between this species exceeding crystal krill (E. crystallorophias) consumption (and its prey, cfr. Smetacek and Nicol 2005) and paleo- in the southern Ross Sea (Ainley 2002; Ainley et al. 2003). climatic regime shifts. Only a very low percentage of remains belongs to other Nevertheless, Antarctic silverfish is characterized by a fish genera. The interspecific variation in samples found strong trophic flexibility and adaptability (Eastman 1993; exclusively at southern latitudes was probably a conse- Zane et al. 2006) and at present compose the main part of quence of the fact that those samples composed 86.6% of the diet of marine predators, which are also ice-avoiding the total and contained 96% of the recovered otoliths. The species that prefer open water such as elephant seals low percentage of occurrence of ‘‘other species’’ in our (Daneri and Carlini 2002). For this reason we hypothesize samples is not surprising; Ade´lie penguins primarily forage that, rather than indicating a decrease in silverfish avail- in the continental shelf waters surrounding Antarctica, ability, the shifts in abundance of P. antarcticum in the which are characterized by a very low ichthyic biodiversity present study could reflect a higher number of fish remains (cfr. Ainley 2002). Most unidentifiable fish otoliths in samples as a consequence of a higher number of birds retrieved in the older guano samples maybe related to attending the colonies during periods with more sea ice. sediment transformation processes (such as pedogenesis and diagenesis). However, since many of the best-pre- Prey size selection served P. antarcticum otoliths come from the older guano samples, preservation factors appear here to be related Despite their dense structures, fish otoliths are exposed to more to acidic digestion processes rather than to the sample variable mechanical and chemical abrasions on calcium age or to erosion action through time. This is also carbonate in the digestive tracts of predators. The 123 Polar Biol susceptibility of fish otoliths (and bones) to digestive ero- in colonies located north of the Drygalski ice tongue were sion appears to change widely taxon by taxon (Ha¨rko¨nen feeding on slightly larger Antarctic silverfish. 1986; Pierce et al. 1993; Tollit et al. 1997). Furthermore, in the ornithogenic soils, continuous freeze/thaw action Sample without fish remains: are they evidence through time and sediment transformation processes can of a dietary shift? contribute to the consumption and damage of otoliths. These erosive processes act on otolith morphological fea- Although fish otoliths and bones regularly occur in the tures and size, and can lead to non-detection of some prey analyzed ornithogenic sediments, some guano samples did categories or of some individuals in a prey category and to not provide any kind of dietary remains. Polito et al. (2002) underestimation of prey body size. Nevertheless, the rela- reported the occurrence of feathers in Cape Bird organic tive frequency and size of prey estimated from the hard levels without dietary remains, which may reflect their remains found in guano samples are valuable, and are very deposition at the time when the area was used by penguin likely the only available information on the kind of prey only to molt and not to nest. Stratigraphic and geomor- consumed. phologic features of our samples indicate their nesting site Juvenile P. antarcticum with a 40–80 mm standard origin, confirmed by the presence of eggshell fragments length range (conforming to juvenile age classes 1? and collected at the same level, suggesting that penguins were 2?; Hubold and Tomo 1989) are the most-represented nesting. A small number of breeding penguins could be individuals in the VL sediments. McDaniel and Emslie responsible for the paucity of remains, or erosion processes (2002) recognized this prevalence in Northern Marguerite may have accounted for otolith loss. We can also hypoth- Bay (Antarctic Peninsula), although with a wider value esize that the lack of prey remains could be a shift to a range (15.82–187.4 mm) and higher mean SL (108.19 ± prevalent non-fish diet. Considering in fact that krill is not 25.53 mm). Juvenile P. antarcticum occur primarily at maintained in the soils, guano samples without fish remains depths of 50–400 m and are well accessible to penguin could reflect a tendency towards a prevalent krill-based capture since their normal foraging depths range between 3 paleodiet. At present time Ade´lie penguin diet switching and 98 m (Chappell et al. 1993). When analyzing the between fish and krill may reflect changes in the foraging temporal distribution of P. antarcticum SL, significant setting in relation to environmental and ecological features. differences were not found throughout the investigated Several authors indicated particular climate and marine period. In Northern Marguerite Bay (Antarctic Peninsula) conditions (i.e. sea-ice extension and persistence) as cause (McDaniel and Emslie 2002), some variations within mean of penguin dietary fluctuation between fish and krill silverfish SL have been recognized among different time (Ainley et al. 1998; Olmastroni et al. 2000; cfr. Ainley periods, but these did not result in a predictable temporal 2002; Ainley et al. 2003). But Ainley et al. (2006)ina pattern in accord with past climate change, although more recent study suggested also that feeding competition Holocene climatic environmental changes are well docu- among penguins and cetaceans rather than change in mented in both the Antarctic Peninsula and the Ross Sea sea-ice cover can better explain the annual switch in the region (Bjorck et al. 1996; Ingolfsson et al. 1998; Baroni penguins’ prey items. and Orombelli 1991, 1994b; Baroni and Hall 2004; Hall If the temporal distribution of DR samples versus NDR et al. 2004, 2006). The absence of temporal variations of ones revealed no significant differences, some consider- the silverfish size over the past 7,000 years reflects a cer- ations on their spatial distribution could be made. In certain tain stability in penguin foraging habits, which is also locations, including Inexpressible Island, Cape Hickey and confirmed by modern diet data on the species predated (crf. Depot Island, NDR guano samples prevail over those Ainley 2002) and on the prey size (Olmastroni et al. 2004a, containing fish remains (Table 1). In these cases, particular b). No significant temporal variation in prey size was local marine conditions or other ecological factors, as well found. The significant difference in silverfish mean size as foraging competition with other predators, could have between the northern and southern colonies was not due to resulted in different krill availability and/or consumption the amount of older, thus more eroded, otoliths in the (cfr. Ainley et al. 2006). Occurring in earlier periods at southern samples. In fact, the percentage of recent otoliths Inexpressible Island (5058–3900 BP) and later at Cape for the north and south colonies remains very similar for Hickey (4075–1985 BP), and at Dunlop Island (3100–2020 the 0–1,000 period (20 and 19.67%), and furthermore BP), it is not possible to define a common paleoenviron- northern samples contain higher percentages of older mental factor that explains this pattern at the regional scale. (period 4,000–6,000) otoliths with respect to the south area At Inexpressible Island, for example, between 6000 and (67.13 and 48.06%, respectively). Therefore, although the 4000 BP, Ade´lie penguins shared ice-free coastal terrain difference accounts only for a mean value of 5.11 mm, we with elephant seals (Hall et al. 2006). Thus, it is possible can hypothesize that at least in the past, penguins breeding that in this area feeding competition due to this coeval 123 Polar Biol occupation led penguins to change their diet by targeting Baroni C, Hall BL (2004) A new Holocene relative sea-level curve for primarily krill, which may be eaten only occasionally by Terra Nova Bay, Victoria Land, Antarctica. J Quat Sci 19:377– 396. doi:10.1002/jqs.825 elephant seals (Daneri and Carlini 2002; van den Hoff et al. Baroni C, Orombelli G (1991) Holocene raised beaches at Terra 2003). Even if not revealed by the spatial and temporal Nova Bay, Victoria Land, Antartica. Quat Res 36:157–177. distribution of our samples, different sea ice regimes doi:10.1016/0033-5894(91)90023-X (Olmastroni et al. 2004a, b) and/or mega icebergs calving Baroni C, Orombelli G (1994a) Abandoned penguin rookeries as Holocene paleoclimatic indicators in Antarctica. Geology (Arrigo et al. 2002), might have had an effect at local scale. 22:23–26. doi:10.1130/0091-7613(1994)022\0023:APRAHP[ These events in fact are known to play an important role on 2.3.CO;2 penguin life cycle, and they have been reported to occur in Baroni C, Orombelli G (1994b) Holocene glacier variations in Terra the past (cfr. Shepherd et al. 2005). Nova bay area (Victoria Land, Antartica). Antarct Sci 6:497– 505. doi:10.1017/S0954102094000751 Although Holocene climatic and environmental changes Barrett JE, Virginia RA, Hopkins DW, Aislabie J, Bargagli R, have clearly affected the VL coast as indicated by Ade´lie Bockheim JG, Campbell IB, Lyons WB, Moorhead DL, Nkem penguin colonization history (Baroni and Orombelli JN, Sletten RS, Steltzer H, Wall DH, Wallenstein MD (2006) 1994a; Lambert et al. 2002; Emslie et al. 2003; Hall et al. Terrestrial ecosystem processes of Victoria Land, Antarctica. 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