Adélie penguin dietary remains reveal Holocene environmental changes in the western Ross Sea (Antarctica)

Palaeogeography, Palaeoclimatology, Palaeoecology 395 (2014) 21–28

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Palaeogeography, Palaeoclimatology, Palaeoecology journal homepage: www.elsevier.com/locate/palaeo

Adélie penguin dietary remains reveal Holocene environmental changes in the western Ross Sea (Antarctica) Sandra Lorenzini a,⁎, Carlo Baroni a,b, Ilaria Baneschi b, Maria Cristina Salvatore a, Anthony E. Fallick c, Brenda L. Hall d a

Dipartimento di Scienze della Terra, Università degli Studi di Pisa, Via S. Maria 53, 56126 Pisa, Italy Istituto di Geoscienze e Georisorse, Consiglio Nazionale delle Ricerche, Via G. Moruzzi 1, 56124 Pisa, Italy Scottish Universities Environmental Research Centre, East Kilbride G75 0QF, Scotland, UK d School of Earth and Climate Sciences and the Climate Change Institute, University of Maine, Orono, ME 04469 USA b c

a r t i c l e

i n f o

Article history: Received 8 June 2013 Received in revised form 28 November 2013 Accepted 8 December 2013 Available online 18 December 2013 Keywords: Adélie penguin Ornithogenic soil Stable isotope Paleoenvironment Paleoceanography

a b s t r a c t Carbon and nitrogen stable isotope analyses were performed on modern and Holocene Adélie penguin guano samples collected from ornithogenic soils along the Scott Coast (Southern Victoria Land, Antarctica), from Cape Irizar to Dunlop Island, and at Cape Bird (Ross Island). Guano samples also were sieved and sorted under stereomicroscope in order to select penguin dietary remains, such as fish bones and otoliths. Carbon and nitrogen stable isotope composition, coupled with the taxonomic identification of fish otoliths from Scott Coast Holocene samples, indicated a mainly fish-based diet for this area, with Pleuragramma antarcticum as the most eaten prey throughout the investigated period (from 390 cal BP to ca 7300 cal BP). The isotopic values of Ross Island samples (from modern to 3850 cal BP) showed a krill consumption increase in the samples younger than 2000 cal BP, with the maximum in modern samples. Scott Coast and Ross Island Holocene samples showed δ13C and δ15N trends similar to those previously published from Terra Nova Bay (northern Victoria Land), whereas modern samples from Ross Island have similar δ15N composition but different δ13C values. This δ13C divergence started at ca 2000 BP and follows the abandonment of the Scott Coast colonies. The δ13C trend observed in Ross Island and Terra Nova Bay samples and the abandonment of the Scott Coast colonies could suggest the stability and the persistence of the previous oceanographic conditions (i.e. polynya) for the Terra Nova Bay area and the establishment of new conditions for water circulation in the Southern Ross Sea since ~2000 BP when persistent sea-ice sealed the Scott Coast. © 2013 Elsevier B.V. All rights reserved.

1. Introduction A fundamental idea in biology is that climatic and environmental changes are the driving force behind biodiversity adaptation through ecological and evolutionary responses (Walther et al., 2002; Parmesan, 2006; Lambert et al., 2010). This assumption is especially true for Adélie penguins (Pygoscelis adeliae) which, because of their extraordinary environmental sensitivity, have become well known as a ‘bellwether’ of Antarctic climate change (Ainley, 2002). Given the significant role that this species plays in the understanding of how the Antarctic environment is changing, Adélie penguins represent one of the best-studied animal species in the world. Moreover, since the description of ornithogenic soils in the Ross Sea area (multi-millennia penguin-guano deposits, Ugolini, 1972), Adélie penguins have also provided valuable new insights into the late Pleistocene and Holocene glaciological history of Antarctica. In fact, the pristine cold and dry Antarctic environment have led to a high concentration of well-preserved penguin remains (bones, eggshells, guano and dietary remains) in the ornithogenic soils dated back to the ⁎ Corresponding author. Tel.: +39 0502215738, fax: +39 0502215800. E-mail address: [email protected] (S. Lorenzini). 0031-0182/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.palaeo.2013.12.014

late Pleistocene and underlying both existing and abandoned colonies (Ugolini, 1972; Baroni and Orombelli, 1994). These remains represent a unique paleoecological heritage in the context of Antarctic paleoclimatic and paleoenvironmental research. Therefore, since the 1990s, multidisciplinary studies have intensively investigated Adélie penguin paleoecology and their colonization history, contributing important information for understanding the Holocene history of key areas of Antarctica (Baroni and Orombelli, 1994; Lambert et al., 2002; Baroni and Hall, 2004; Hall et al., 2004, 2006; Emslie and Woehler, 2005; De Bruyn et al., 2009; Hall, 2009). Moreover, investigation has demonstrated that over at least the last 55,000 yr, local and regional environmental conditions frequently changed and Adélie penguins have survived by adapting both their ecological behavior (i.e. foraging and feeding behavior) and the geographic distribution of their colonies (Baroni and Orombelli, 1994; Lambert et al., 2002; Baroni and Hall, 2004; Hall et al., 2004, 2006; Emslie and Woehler, 2005; De Bruyn et al., 2009; Hall, 2009; Lorenzini et al., 2010). The Adélie penguin colonization history of the Southern Victoria Land Coast indicates that abrupt environmental changes occurred during the Late Holocene when the persistence of year-round fast ice caused abandonment of the Scott Coast's colonies, which have not been reoccupied since. This abandonment occurred almost

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concurrently with evidence for the first occupation by breeding penguins on Ross Island where suitable conditions for Adélie's settlement have persisted to the present (Baroni and Orombelli, 1994; Emslie et al., 2003; Hall et al., 2006; De Bruyn et al., 2009). The guano deposit serves as a unique natural archive of ecologically relevant indicators of diet composition by preserving fish vertebrae and otoliths, and stable isotopes of carbon (δ13C) and nitrogen (δ15N) that provide insight into possible food web shifts. In particular, this buildup of material at bird nesting sites represents thousands of years of occupancy, with stable-isotope analysis revealing colonization patterns and changes in prey selection and foraging habitat over long periods of time (e.g. snow petrels Pagodroma nivea—Ainley et al., 2006; Adélie penguins Pygoscelis adeliae—Emslie and Patterson, 2007; gyrfalcons Falco rusticolus—Burnham et al., 2009). Stable isotopes in feces, which are composed of undigested food matter, gut microbes, digestive secretions, uric acid, and sloughed epithelial tissues, have been demonstrated in experimental and wild settings to reflect ingested diet in mammalian herbivores and primates (Van der Merwe, 1986; Codron et al., 2005; Sponheimer et al., 2009). Stablecarbon isotope composition (δ13C) provide information on the fundamental carbon source of the food web and regional origin of the primary producers at the base of the food chain (Post, 2002; McCutchan et al., 2003). Hence, δ13C values are used to characterize the foraging habitats of predators, including penguin (Cherel and Hobson, 2007; Cherel et al., 2011). Stable-nitrogen isotope composition (δ15N) is used mainly to establish trophic relationships (Rau et al., 1982; Hobson and Montevecchi, 1991; Hobson and Welch, 1992). To date, several studies have shown δ13C and δ15N values of animal feces to be a faithful tracer of dietary sources, in particular of bats (Mizutani et al., 1992a,b; Wurster et al., 2010 and references therein), birds and also modern penguins (Mizutani and Wada, 1988). Stable isotope studies applied to Adélie penguin remains collected on the Antarctica Peninsula and along the Victoria Land coast have recently added considerable information about the paleoecology of this species and are a valuable tool for examining biodiversity history and its development through time (Emslie and Patterson, 2007; Lorenzini et al., 2009, 2012). Particularly, stable carbon (δ13C) and nitrogen (δ15N) isotope analyses of Adélie penguin eggshell and guano samples have demonstrated to give remarkable temporally different paleoenvironmental information (Emslie and Patterson, 2007; Lorenzini et al., 2010). In fact, the comparison between eggshell and guano isotopic composition has highlighted that the isotopic ratios of eggshell and guano samples provide different kinds of information on Adélie penguin diet, corresponding to short and long periods, respectively: the egg-laying event for eggshell and the summer season for the second (Emslie and Patterson, 2007; Lorenzini et al., 2010). In this paper, we present the results of stable carbon (δ13C) and nitrogen (δ15N) isotope analyses performed on Adélie penguin guano samples collected from abandoned penguin colonies distributed along the Scott Coast from Cape Irizar (75°34′S) to Dunlop Island (77°14′S), and on Ross Island, at the extant Cape Bird colony and its outskirts at McDonald Beach (77°13′E). Dietary data obtained from microscopic analyses and the isotopic signature of penguin guano are also discussed. Furthermore, comparison with published carbon and nitrogen isotope composition of guano collected from the Terra Nova Bay area (Lorenzini et al., 2010) enable the interpretation of Holocene environmental and oceanographic conditions of different sectors of the Ross Sea Embayment, especially through the use of carbon isotopes. 2. Study area 2.1. The Scott Coast The Scott Coast lies to the south of the Drygalski Ice Tongue (75°30′S) extending south to Minna Bluff (78°31′S) (Fig. 1). Characterized by yearround fast ice, the Scott Coast is a key area for determining both the

extent and the chronology of grounded ice in the Ross Sea Embayment at the Last Glacial Maximum (LGM), because it displays raised beaches critical for developing relative sea-level (RSL) curves (Hall and Denton, 1999; Hall et al., 2004). Several ice-free promontories and islands, with well-developed raised beaches, occur between Explorers Cove and Depot Island (Fig. 1). North of Depot Island to the Drygalski Ice Tongue, the icebound coast is heavily glaciated, with rare ice-free areas and very reduced Holocene raised beaches. Abandoned colonies have been identified, described and sampled on beach deposits, abrasion platforms, glacial deposits, regolith, and bedrock at Cape Irizar, Prior Island, Cape Hickey, Cape Day, Depot Island, Depot Island Peninsula, Cape Ross, Cape Roberts, Dunlop Island, Spike Cape, and Marble Point (Baroni and Orombelli, 1994; Hall and Denton, 1999; Lambert et al., 2002; Hall et al., 2004). 2.2. Ross Island Ross Island is separated by McMurdo Sound from the Scott Coast mainland (Fig. 1). The northern margin of Ross Ice Shelf abuts the southern coast of the island. Ross Island is almost entirely ice-covered with only a few ice-free coastal areas available to penguins. Despite this fact, more than 20% of all nesting pairs breeding in the Ross Sea Embayment occur on Ross Island, distributed in just three colonies: Cape Bird, Cape Crozier and Cape Royds, the latter being the smallest colony on Ross Island and the southernmost penguin colony in the world (77°34′S. 166°11′E) (Ainley, 2002; Ballard et al., 2010). 3. Materials and methods 3.1. Field survey and sample collection Aerial photograph analysis, several field surveys, and detailed geomorphologic analysis of key sites have been conducted along the VL coast and on Ross Island. The accurate field survey of ice-free areas allowed the discovery of tens of abandoned Adélie penguin colonies from Cape Adare to Ross Island (Baroni and Orombelli, 1991, 1994; Baroni and Hall, 2004; Hall et al., 2004). Well-sorted pebbles selected by penguins for building their nests characterize abandoned nesting sites: after the abandonment of nests, pebbles are concentrated at the surface by wind deflation and prevent the erosion of the lower guano. Pebbly patches hide and protect the lower organic soil formed by bird ejecta and remains. After identifying abandoned colonies, test pits (generally 1–2 m2) were established. Cleaning the entire surface from the top, ornithogenic soils were excavated layer-by-layer using techniques commonly used in archeological research until the underlying bedrock or undisturbed marine/glacial sediments were reached (Baroni and Orombelli, 1994; Lambert et al., 2002). The thickness of ornithogenic soils ranges from some centimeters to some decimeters. Through the accurate stratigraphic excavation of penguin settlements, multi-occupational phases of the colonies (eventually separated by mineral layers such as sand and gravel of colluvial or periglacial origin, aeolian deposits, etc.) have been identified (Lambert et al., 2002; Baroni and Hall, 2004; Hall et al., 2004). This careful fieldwork allowed collection at distinct organic layers of several well-preserved and age-constrained Holocene penguin remains and leavings, including penguin bones, feathers, eggshell fragments. The good correspondence among multiple radiocarbon dates obtained from different remains collected from the same layer and the accurate stratigraphic control of sampling, show that no significant contamination or mixing occurred since the ornithogenic soils formed (Lambert et al., 2002; Baroni and Hall, 2004; Hall et al., 2004). To prevent the complete destruction of the abandoned colonies, which must be regarded as a unique record of the heritage of penguin settling, we collected soil samples weighing (as a mean) only some hundreds of grams.

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Fig. 1. Map of Victoria Land showing the location of the modern (asterisk) and abandoned (circles) Adélie penguin colonies sampled in this work. Triangles indicate other colonies occupied at present in the Ross Sea.

For this study, we analyzed penguin guano samples collected over several field surveys between 1994 and 2007. Samples from eight abandoned penguin colonies along the Scott Coast (Cape Irizar, Prior Island, Cape Hickey, Cape Day, Depot Island Peninsula, Cape Ross, Cape Roberts, and Dunlop Island) and from the modern colony of Cape Bird and its outskirts at McDonald Beach (Ross Island) were investigated. Fresh guano samples were collected at the outskirts of the occupied nests; Holocene guano was sampled from each excavated ornithogenic level.

deionized water to neutral pH and dried. Isotope ratios of organic carbon and nitrogen were analyzed using the same sample aliquot. Subsamples of 2–20 mg, depending on nitrogen and carbon content, were weighed into tin capsules and analyzed using a Thermo Finnigan Elemental Analyzer EA-1108 interfaced with an isotope ratio mass spectrometer (Finnigan DeltaPlus) via the Conflo II interface (Finnigan MAT, Bremen, Germany). Isotope ratios were normalized to VPDB for δ13C and AIR for δ15N using International Atomic Energy Agency (IAEA) NO-3, IAEA CH-6, and internal standards. Precision was better than 0.2‰ at one sigma for both carbon and nitrogen isotope values.

3.2. Stable isotope analyses 3.3. Microscopic analyses We performed organic carbon and nitrogen stable isotope analyses on 81 Holocene and 5 modern penguin guano samples at the IGG-CNR laboratories (Pisa, Italy). For each sample we selected the b63 μm grain size fraction that quantitative analyses carried out in the laboratory for previous studies have indicated to be the richest in organic carbon content (Lorenzini et al., 2010, 2012). Samples were treated with 10% HCl to remove inorganic carbon and then washed several times with

We washed and sieved 47 Holocene and 5 modern guano samples through seven nested screens with square mesh sizes ranging from 2 mm to 63 μm. To avoid bias due to variable amounts of sorted sediments, we selected and processed 150 g of dry mass for each sample (when available). We report results as weight percent that is the number of dietary remains normalized for 100 g of soil. The matrix from

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each screen was dried at low temperature and subsequently sorted under a low power (5–10 ×) stereomicroscope to separate eggshell fragments, feathers, and dietary remains (fish vertebrae and otoliths). We classified samples according to the presence/absence of dietary remains. We separated otoliths from fish bones in order to carry out taxonomic identification. Otoliths were identified using anatomic-comparative tables proposed by Williams and McEldowney (1990) for Antarctic fish taxa and the Anfibo Base software (Busekist et al., 2007). Fish otoliths were well-preserved and showed erosion signals ranging from 1 to 2 according to Leopold et al. (1998), with most of them still preserving the morphological parameters that are required for taxon identification. 3.4. Radiocarbon dating and statistical analysis Accelerator mass spectrometry (AMS) dating of penguin guano was performed by the NOSAMS laboratory of Woods Hole, USA. All AMS radiocarbon dates were corrected and calibrated for the marine-carbon reservoir effect and upwelling of old water in the Southern Ocean by using a ΔR = 791 ± 121 yr based on 14C of the solitary coral, Gardineria antarctica collected from debris bands on the McMurdo and Hell's Gate Ice Shelves (Hall et al., 2010). The uncorrected conventional dates ±SD are given with the 2σ calibrated range in calendar years before present (BP) determined from the Calib 6.0.1 software program and INTCAL 09 marine calibration curve (Reimer et al., 2009). This range provides 95% confidence that the true age of the specimen falls within the specified time period. A few samples also were dated by association with other penguin remains of known age (i.e. penguin bones and eggshells) collected from the same stratigraphic level. Samples younger than 560 cal BP all were collected from Ross Island, with the exception of one sample from the Scott Coast. By contrast, almost all samples older than 560 cal BP were from Scott Coast. All statistical analyses were performed using the software Statistica, version 7.1 for Windows (StatSoft, Inc., 2005).

4.2. Microscopic analyses Guano screening and sorting allowed us to recover wellpreserved biological material, including penguin bones, eggshell fragments and hard parts of dietary remains, such as fish bones (vertebrae) and fish otoliths. Of 52 samples, 20 did not contain dietary remains and 18 contained only unidentifiable fish vertebrae and fish teeth. Squid beaks were recovered only in one sample at Cape Roberts. The presence of eggshell fragments in those samples where neither fish bones nor otoliths were recovered still testified to their ornithogenic nature. We found 26 otoliths in 14 samples (9 from Ross Island and 5 from the Scott Coast) and analyzed them to identify prey taxa. Taxonomic identification indicated that all fish prey belonged to the family Nototheniidae and consisted mostly (81%) of Pleuragramma antarcticum. Only a very small percentage of the recovered otoliths (5.2%) belonged to fish individuals different from P. antarcticum (identified as Trematomus sp. and, in one case at Dunlop Island, as Trematomus bernacchii) or were remains that could be identified only to the Nototheniidae family (13.8%). Based on our new data and those previously published for the Scott Coast (Lorenzini et al., 2009), the Scott Coast samples showed a higher interspecific richness than the Ross Island samples that, on the contrary, exhibited a paucity both of otoliths and fish bones that persists until the present time (Table 1).

5. Discussion The data obtained from this study will be discussed in conjunction with previously published results (Lorenzini et al., 2009, 2012) in order to describe in detail the paleodietary record of Adélie penguins along the Scott Coast to Terra Nova Bay, as well as to provide new late Holocene dietary information about this species at Ross Island.

4. Results

5.1. Paleodietary reconstruction from microscopic analyses

4.1. Stable isotope data

Adélie penguins primarily feed on krill (Euphausia superba, Euphausia cristallorophias) and fish (mainly the silverfish, Pleuragramma antarcticum) (Ainley, 2002; Ainley et al., 2003). Krill plays a key role in the present-day penguin diet but unlike fish, krill exploitation leaves no visible record in Holocene sediments. Taxonomic identification of fish otoliths indicated Pleuragramma antarcticum as the most eaten fish prey throughout the investigated period both along the Scott Coast and at Ross Island. Very few otoliths were recognized as Trematomus sp. genus or remained unidentified. The abundance of remains of Antarctic silverfish observed in this study agrees with previous paleodietary investigations in the Antarctica Peninsula, East Antarctica, and in the Ross Sea region (Polito et al., 2002; Emslie and Woehler, 2005; Lorenzini et al., 2009), as well as with present-day data, since this species today accounts for more than 90% of the local fish community in the Ross Sea (Vacchi et al., 2004) and represents a key species in the diet of Antarctic apex predators (La Mesa et al., 2004). In particular, during the chick-rearing period, P. antarcticum can contribute up to 50–75% by mass to the Adélie penguin diet, even exceeding crystal krill (Euphausia cristallorophias) consumption in the southern Ross Sea (Ainley, 2002; Ainley et al., 2003). Samples younger than 3000 cal BP collected along the Scott Coast show a general decrease in the number of dietary remains. In addition, even though P. antarticum is the most represented fish taxon, Scott Coast samples also showed variety in the prey fish taxa, with a contribution from Pagothenia sp. and Trematomus sp. similar to that at Terra Nova Bay (Lorenzini et al., 2009) (Table 1). In contrast, with the exception of two samples, noneuphausiid paleodiet at Ross Island appears to be almost monospecific and entirely based on silverfish consumption.

The δ13C and δ15N data obtained from modern and fossil penguin guano are given in Appendix 1. The δ 13C values of guano samples range from − 28.9‰ to − 24.0‰. Modern samples have a mean value of − 27.3 ± 0.4‰, whereas Holocene samples show a gradual tendency toward more positive values. In particular, the samples older than 560 BP show an average δ13C of − 25.5 ± 0.9‰, whereas the mean value for the younger samples, excluding the modern ones, is − 27.0 ± 0.7‰. Samples younger than 560 BP are not statistically different from each other (t-test, t = 1.14, P = 0.265). This supports the contention that no diagenetic post-depositional effects have influenced the sample isotopic composition. The samples older than 560 BP show an interquartile range of 1.0‰, whereas that for younger samples is 0.3‰, suggesting more variable feeding in older than in more recent times. Comparison of samples older and younger than 560 BP, including modern ones, using an F-test, shows that the standard deviations of the two groups are not different (F = 2.28, P = 0.04). Hence, a t-test can be used to compare the mean values of the two groups and this reveals that δ13C mean values of younger samples are statistically more negative than those for older ones (t = 10.22, P b b0.05). The δ15N values of guano samples range from + 7.7‰ to +27.5‰. Fresh excreta have a mean value of + 16.0 ± 2.2‰, not statistically different from the mean value of Holocene samples younger than 560 cal BP (+16.1 ± 1.4‰). Samples older than 560 BP have an average of +19.3 ± 2.2‰ and are all higher than +16.4‰, except for two samples at around 2900 and 3500 cal BP.

2.44

12.50

9.48 11.11 7.14 7.32 1.44

5.88

12.50

10.53

0.29 0.29

1 35 2 49 120

Radiocarbon data range (cal yrs BP)

839–4702 391–5374 2,151–7288 3470 2192–6823 2983–3708 2902 0–3852 1248–5126 75°34′S 75°41′S 76°05′S 76°15′S 76°42′S 76°44′S 77°00′S 77°13′S 77°14′S

2111 1127.6 1762.4 226 766 1148 290 5372.3 1548.6

348 63 28 41 9 34 0 19 8

3 8 2

2

89.47 75.00

86.49 88.89 92.86 90.24 100.00 94.12

n.d. (%) Pagothenia sp. (%) Trematomus sp. (%) Trematomus bernacchii (%) Pleuragramma antarcticum (%) No. of recovered squid beaks No. of recovered fish bones No. of recovered fish otoliths

5.2. Paleodietary reconstruction from C and N stable isotope analyses

Latitude

Total mass (g)

25

Although direct information about past krill consumption cannot be obtained by guano screening, because krill and their fragile carapaces are not preserved in the soils, the isotopic approach enables us to identify the dietary contribution of krill and to reconstruct a more detailed paleodietary record as krill is metabolized and contributes to carbon and nitrogen isotopic composition of tissues, including guano. We reported the δ13C values for guano samples from the three different sites (Southern Victoria Land — SVL, Ross Island —RI and Terra Nova Bay — TNB) (Fig. 2). Samples from TNB and SVL show similar values and insignificant variation through the Holocene period. However, δ13C values of samples from RI and TNB younger than 560 BP are significantly different (t-test, t = −8.06, P b b0.05). This implies a different balance of sources of carbon. Fish and krill belong to two different trophic levels and are characterized by different isotopic composition (δ13C = −24.7‰, δ15N = 10.6‰, and δ13C = −31.4‰, δ15N = 5.2‰, respectively; Emslie and Patterson, 2007). Thus, major krill consumption implies lower isotopic values in penguin tissues. Furthermore, δ13C may provide valuable information on the carbon source of food web and the regional origin of the primary producers. The δ13C signature of particulate organic matter decreases from inshore to offshore waters (Hill et al., 2006), including Antarctic waters (Trull and Armand, 2001), and from surface waters to sea ice (Henley et al., 2011). Moreover, phytoplankton blooms, characteristic of high productivity water, lead to more positive δ13C values of particulate organic carbon of waters. Various authors also have reported that δ13C values of fish should be higher in benthic than in pelagic species, because benthic organisms have higher 13C values when compared to pelagic organisms (France, 1995; Kaehler et al., 2000; Dunton, 2001; Pruell et al., 2003; Cherel et al., 2011). Furthermore, the δ13C values of fish caught in northern waters should be higher than that of southern species, because marine plankton δ13C, and thus consumer δ13C, varies with latitude in oceanic waters (Rau et al., 1982), including the Southern Ocean (Trull and Armand, 2001; Cherel and Hobson, 2007; Jaeger et al., 2010; Quillfeldt et al., 2010). In our case, these oceanographic features, and in particular the δ13C latitudinal gradient and the higher δ13C composition of benthic taxa, such as Trematomus bernacchii, could then reasonably explain the higher δ13C values recorded at Terra Nova Bay and along the Scott Coast, compared to those found on Ross Island. δ15N values combined with dietary remains afford further information about penguin diet. Screening of modern samples resulted in very few dietary remains (less than 10 in 150 g of matrix sorted). Most dietary remains (up to 67 in 150 g) were found in Holocene samples that also showed higher δ15N values. The number of dietary remains represents a discriminating factor between the Scott Coast and Ross Island. Samples from Ross Island that are dated older than 560 BP contain less than 15 prey items (fish bones and/or otoliths) in 150 g of matrix, whereas dietary remains found in the Scott Coast samples can vary from 2 to 85 per 150 g. Moreover, the Scott Coast stable isotope data showed higher δ15N values typical of a predominantly fish-based diet. Previous studies carried out in different areas of the Victoria Land coast documented the same correlation between δ15N values and the number of dietary remains. At Terra Nova Bay, for example, δ15N b+ 12‰ was measured in samples without dietary remains, whereas samples with a higher δ15N also provided a great number of dietary remains (N20 in 150 g) (Lorenzini et al., 2009, 2010).

Cape Irizar Prior Is. Cape Hickey N Cape Day Depot Is. Peninsula Cape Ross Cape Roberts Cape Bird Dunlop Is.

5.3. C and N isotopes Collection site

Table 1 Number and taxonomic identification of dietary remains recovered in ornithogenic soil samples from the Scott Coast and Ross Island based on new data reported here and those previously published (Lorenzini et al., 2009). Analyzed guano samples are grouped by collection site with the age range (cal yr BP, using a ΔR = 791 ± 121 yr; Hall et al., 2010) and total dry mass (g) of sorted sediments.

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Between ca. 8000 and ca. 1500 cal BP, Scott Coast samples show a generally constant carbon isotope signature of − 25.3 ± 0.7‰. Although some older Ross Island samples lie in that range, those younger than 1500 cal BP tend towards more negative δ13C values. As illustrated in Fig. 2, modern samples from Ross Island and Terra Nova Bay show a

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penguin guano have to be considered as a touchier issue. As reported in previous studies (Lorenzini et al., 2010), the gap between old and modern nitrogen isotope ratios is too high (_δ15Nold-new ≅ + 20‰) to be interpreted simply as a result of nutrient uptake. In fact, a change in the diet could explain an isotopic increase of about 3.4‰ with each trophic level (Minagawa and Wada, 1984; Vander Zanden and Rasmussen, 2001). Mizutani and Wada (1988) reported an increase in δ15N of residual nitrogen, up to 10‰ caused by a nitrogen isotope fractionation associated with the volatilization of ammonia after excreta deposition. Thus, the very high δ15N values of ornithogenic samples compared to modern guano and the shift observed between fossil and modern guano samples could be reasonably explained by adducing an ammonia volatilization effect. On the other hand, it is important to consider that the ammonia volatilization effect happens shortly after excreta deposition (Mizutani and Wada, 1985) but in our case not only modern but also older samples show low δ15N values: the shift toward lower δ15N started at least by about 2000 cal BP. 6. Conclusion

Fig. 2. δ13C values from guano samples during the investigated period. Squares and circles indicate samples from Ross Island and Scott Coast, respectively. Diamonds indicate previously published data from Terra Nova Bay (Lorenzini et al., 2010). Dashed lines indicate δ13C mean values of potential dietary sources (Emslie and Patterson, 2007).

divergence in δ13C with the latter values in general more positive than −26‰, with the exception of only two samples that show more negative values, while no value more positive than −27‰ has been recorded in Ross Island samples. This divergence seems to have started at least by 2000 cal BP and progressively increased towards the modern samples. This could be explained by the different δ13C composition of POC at lower latitude due to the latitudinal gradient (Norkko et al., 2007) and/or to waters consequently more productive at Terra Nova Bay because of the presence of the polynya off Inexpressible Island. In fact, a latitudinal δ13C gradient in Southern Ocean has been reported due to water masses and fronts with different physical and biological characteristics encircling the Antarctic continent (Orsi et al., 1995; Cherel et al., 2011). Consequently, bulk δ13C POC values in Southern Ocean surface waters are more negative (−33 compared to − 21‰) relative to POC from lower-latitude surface waters (Rau et al., 1991a,b; Dehairs et al., 1997; Villinski et al., 2000). Significant enrichment in δ13C of POC from the Southern Ocean has been documented in the water column and in habitats associated with sea ice and seasonally during summer (Fischer, 1991; Rau et al., 1991b; Dunbar and Leventer, 1992; McMinn et al., 1999; Villinski et al., 2000; Kennedy et al., 2002; Arrigo et al., 2003). Other factors that may be responsible for isotopic enrichment include high growth rates of primary producers during periods of high productivity, species-specific isotope fractionation, increased heterotrophic recycling in the upper water column, and bloom-related drawdown of [CO2(aq)] in stratified surface waters (Villinski et al., 2000, 2008). Radiocarbon dating indicates a narrow temporal window between 1000 and 2000 cal BP when Ross Island and Scott Coast guano samples coexisted. During this period, Ross Island generally records δ15N values relatively lower than those measured in the Scott Coast samples, even though the difference is not large. These low values persist in Ross Island samples up to the present time (Fig. 3). Furthermore, as is the case for Ross Island, Terra Nova Bay guano samples record a shift toward lower δ15N values in the modern samples (Lorenzini et al., 2010). On Ross Island the low percentage of dietary remains and the lower δ15N values, especially in modern samples, probably indicate a mixed diet, but one predominantly based on krill exploitation. However, compared to δ13C values, dietary inferences obtained by analyzing δ15N values of

This study provides new insights into the Holocene paleoecological and paleoenvironmental evolution of the Scott Coast and McMurdo Sound area. Together with the screening of guano samples, C and N isotope analyses of penguin guano allowed us to reconstruct a detailed and comprehensive paleodietary record. Taxonomic identification of fish otoliths indicated Pleuragramma antarcticum as the most eaten noneuphausiid prey throughout the investigated period (ca 7300 cal BP to present). Only a very low percentage of remains belongs to Trematomus sp. genus. Compared to guano samples collected along the Scott Coast, samples collected at Cape Bird on Ross Island (3850 cal BP to present) generally show fewer fish bones and otoliths and a lower diversity of preyed fish taxa, with a non-euphausiid diet almost entirely based on silverfish consumption. Holocene samples from Terra Nova Bay and Scott Coast showed an almost perfect overlap for both carbon and nitrogen isotopic ratios. Ross Island Holocene samples generally showed lower δ13C values but δ15N values similar to those of Terra Nova Bay and Scott Coast. Compared to Terra Nova Bay, modern samples from Ross Island show the

Fig. 3. δ15N values from guano samples during the investigated period. Squares and circles indicate samples from Ross Island and Scott Coast, respectively. Diamonds indicate previously published data from Terra Nova Bay (Lorenzini et al., 2010). Dashed lines indicate δ15N mean values of potential dietary sources (Emslie and Patterson, 2007).

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same gradual shift toward lower δ15N but a divergence in δ13C values, which started at least by about 2000 cal BP. Terra Nova Bay samples display values higher than −26‰ (only two samples show more negative values), while no value N−27‰ has been recorded at Terra Nova Bay. The δ15N trend of Ross Island samples agrees with the dietary change in modern samples also recorded in Terra Nova Bay and indicates an increase in the krill consumption in the modern samples. The strong divergence apparent in the δ13C values between the two areas could be explained by (paleo)oceanographic features and physical and biological characteristics of the Ross Sea water masses. In particular, the presence of more productive water and of krill specimens with consequently higher δ13C values at Terra Nova Bay could reasonably explain the higher δ13C values recorded in this area. Also the higher contribution of fish remains belonging to benthic fish taxa, such as Trematomus bernacchii, could contribute to an increase in the δ13C values (France, 1995; Kaehler et al., 2000; Dunton, 2001; Pruell et al., 2003; Cherel et al., 2011). Less certain and more complex is the issue regarding the paleoenvironmental and paleoecological evolution along the Scott Coast. The Adélie penguin colonization history of this region documents a rapid abandonment of the Scott Coast colonies during the Late Holocene (Baroni and Orombelli, 1994; Hall et al., 2006). However, before this abandonment, the C and N isotopic composition of guano samples indicate the persistence along the Scott Coast of paleoecological conditions similar to those recorded at Terra Nova Bay. Interestingly, we note that the δ13C divergence between Terra Nova Bay and Ross Island that occurred at least by 2000 cal BP postdates the abandonment of the Scott Coast colonies (Hall et al., 2006). The (paleo)oceanographic features of the Ross Sea circulation could explain the different evolutions during the Late Holocene of these two regions of Victoria Land Coast. Norkko et al. (2007) indicated that the Scott Coast is influenced by less-productive water due to a plankton-depleted current from underneath the Ross Ice Shelf. The persistence of cold stenothermal conditions caused the progressive cooling that induced expansion and persistence of sea ice coverage. So, the divergence in δ13C observed in Ross Island and Terra Nova Bay samples and the concurrent abandonment of the Scott Coast might suggest the stability and the persistence of the polynya for the Terra Nova Bay area, but the establishment of new water circulation in western McMurdo Sound. In contrast to Terra Nova Bay, which experienced a longer period with persistent open water and a large productive polynya (Faranda et al., 2000) the water offshore the Scott Coast today is oligotrophic (Dayton and Oliver, 1977), which is extremely disadvantageous for penguin survival. We suggest that onset of these conditions probably started earlier than 2000 cal BP could explain the abandonment of the Scott Coast in the Late Holocene. This study highlights the usefulness of developing long-term guano sampling and data bases on isotopic composition of key marine organisms to track potential changes in their isotopic niches and in the carrying capacity of the environment. Acknowledgment This work was funded by the financial support of the Italian National Program on Antarctic Research (PNRA) and executed in the framework of the PNRA and the US National Science Foundation (NSF). Isotopic analyses were performed at the IGG-CNR of Pisa (Italy). New radiocarbon dates on penguin remains used in this work were performed at the National Ocean Sciences Accelerator Mass Spectrometry Facility (NOSAMS) at the Woods Hole Oceanographic Institution (USA). Appendix A. Supplementary data Supplementary data to this article can be found online at http:// dx.doi.org/10.1016/j.palaeo.2013.12.014.

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