ORIGINAL PAPER

Holocene Adelie penguin diet in Victoria Land Antarctica

Sandra Lorenzini AElig Silvia Olmastroni AEligFrancesco Pezzo AElig Maria Cristina Salvatore AEligCarlo Baroni

Received 17 November 2008 Revised 13 February 2009 Accepted 25 February 2009

Springer-Verlag 2009

Abstract Ornithogenic soils (N = 97) dated up to 7000

Before Present (BP) were sampled in 16 relict and modern

breeding colonies of Adelie penguin along the Victoria

Land coast (Ross Sea Antarctica) Taxonomic identifica-

tion of fish otoliths (N = 677) recovered in these soils

allowed to identify the Antarctic silverfish as the most

eaten prey (901) throughout the investigated period A

morphometric analysis of the otoliths revealed that the

Adelie penguin primarily selected prey averaging

6723 plusmn 23 mm of standard length Temporal distribution

of Pleuragramma antarcticum showed a peak between

2000 and 4000 years BP a period corresponding to the

maximum spread of Adelie penguin in the Victoria Land

Possible explanations of the variations of the abundance of

the fish prey in the diet are discussed in the context of the

paleoclimatic events and as possible consequences of die-

tary shifts due to the temporal variation of prey availability

in the Ross Sea ecosystem

Keywords Adelie penguin Ornithogenic soils Prey remains Paleodiet Victoria Land

Introduction

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

excellent opportunity to study pedogenetic processes (ie

soil formation) nutrient cycling and chemistry in very

extreme environmental conditions (Ugolini 1972 Speir

and Cowling 1984 Heine and Speir 1989 Tatur and

Myrcha 1989 Zhu et al 2005 Barrett et al 2006 Michel

et al 2006 Liu et al 2006 Simas et al 2007) In conti-

nental Antarctica ornithogenic soils are provided by a

single animal source the Adelie Penguin (Pygoscelis

adeliae Hombron and Jacquinot 1841) In a long-term

occupied colony penguin guano seeps through the per-

meable pebbly nests and accumulates at their base to form

ornithogenic soils Thanks to the dry and cold Antarctic

conditions ornithogenic soils also preserve a long-dated

heritage of the Adelie penguin community (Spellerberg

1970 Stonehouse 1970 Bochenski 1985 Baroni 1994

Baroni and Orombelli 1994a Emslie 1995 Emslie et al

1998) The extension of the organic layers is a function of

the size the age of establishment and the persistence of the

colony (Baroni 1994) Accurate stratigraphic sections of

S Lorenzini (amp) C Baroni

Dipartimento di Scienze della Terra

Universita di Pisa

Via S Maria 53 56126 Pisa Italy

e-mail lorenzinidstunipiit

C Baroni

e-mail baronidstunipiit

S Olmastroni F Pezzo

Dipartimento di Scienze Ambientali lsquolsquoG Sarfattirsquorsquo

Universita degli Studi di Siena Via P A Mattioli 4

53100 Siena Italy

S Olmastroni

e-mail olmastroniunisiit

F Pezzo

e-mail pezzounisiit

M C Salvatore

Dipartimento di Scienze della Terra

Universita di Roma lsquolsquoLa Sapienzarsquorsquo

Ple A Moro 5 00185 Rome Italy

e-mail mariacristinasalvatoreuniroma1it

123

Polar Biol

DOI 101007s00300-009-0607-4

ornithogenic soils have revealed different guano layers (up

to five) that record multi-occupational phases of the colo-

nies (Baroni and Orombelli 1991 1994a Baroni and Hall

2004) Radiocarbon-dated penguin remains such as bones

guano and eggshell fragments collected from these organic

soils provide a multi-millenary record of Adelie Penguin

colonization that has been revealed to be particularly

interesting for paleoenvironmental studies (Baroni and

Orombelli 1991 1994a Baroni 1994 Emslie 2001 Lambert

et al 2002 Emslie et al 2003 Shepherd et al 2005

Hall et al 2006 Emslie and Patterson 2007 Emslie et al

2007) Adelie penguins are sensitive indicators of the

Antarctic climate and of environmental parameters that

regulate their presence and distribution (Ainley 2002)

Where ornithogenic soils are common features Adelie

penguins have found encouraging ecological conditions for

their colonization At these sites the endurance of these

favorable setting environments is related to the thickness of

these soils an enduring occupation of a colony drops a

thick layer made from nest pebbles penguin remains and

guano and the older the colony the thicker the accumu-

lation of guano (Ugolini 1972) In particular well-

developed sequences of ornithogenic soils testify the

ancient availability of ice-free coastal terrains suitable to

nest and breed In Victoria Land (Ross Sea) radiocarbon

dating of penguin guano bones and eggshells collected

from these soils together with other datable organic mate-

rials provides data for reconstructing the retreat of glaciers

in coastal areas after the last Glacial Maximum (amp18ndash

20000 years Before Present BP) and the following emer-

sion of coastline during the Holocene period (starting about

8000 BP) (Baroni and Orombelli 1991 1994b Baroni and

Hall 2004 Hall et al 2004) Radiocarbon dates from

abandoned penguin colonies scattered on the VL coast

(from the northernmost site at Cape Adare to the south-

ernmost sites at Ross Island) indicate that Adelie penguins

occupied colonies in the Terra Nova Bay region since 7200

BP (Baroni and Orombelli 1994a) The occurrence of

ornithogenic soils both in the vicinity of currently occupied

colonies and in areas no longer colonized by penguins

attests that during the Holocene the penguin population

varied according to changing environmental conditions

(Baroni and Orombelli 1994a Lambert et al 2002 Polito

et al 2002) Especially after the period between 4500 and

2500 BP indicated as a lsquolsquopenguin optimumrsquorsquo by Baroni and

Orombelli (1994a) abrupt environmental changes caused a

drastic abandonment of several colonies and a dramatic

decrease in the penguin population on the southern Scott

Coast and in Terra Nova Bay (Baroni and Orombelli

1994a) Between 2300 and 1100 BP as documented by the

contemporary great spreading of elephant seals (Mirounga

leonina) in the Ross Sea Embayment the establishment

and persistence of sub-Antarctic climaticenvironmental

conditions inhibited the presence and settling of Adelie

penguin colonies (Hall et al 2006)

Ornithogenic soils also well preserve hard parts of die-

tary remains such as fish otoliths bones teeth and squid

beaks Calcareous fish otoliths and chitinous squid beaks in

particular have demonstrated a strong preservation power

Taxonomic identification of such remains allows us to

define a long-term Adelie penguin paleodietary record

(Emslie et al 1998 McDaniel and Emslie 2002 Emslie

and McDaniel 2002 Polito et al 2002 Emslie and

Woehler 2005)

Previous paleoecological studies have yielded consi-

derable dietary information on non-krill prey thanks to the

excellent preservation of remains found within ornithogenic

soils Concentrated in the area of the Antarctica Peninsula

and in the East Antarctica these studies have confirmed that

from the mid-Holocene to the present day the Antarctic

silverfish (Pleuragramma antarcticum Boulenger 1902)

and glacial squid (Psychroteuthis glacialis Thiele 1920)

have been important components in the Adelie penguin

diet being the most common species represented in the

sediments (Emslie et al 1998 Emslie 2001 Emslie and

McDaniel 2002 McDaniel and Emslie 2002 Emslie and

Woehler 2005) Furthermore the proportion of these prey

items in the past Adelie penguin diet varied in accordance

with climatic cooling and warming trends (cfr Emslie et al

1998 Emslie and McDaniel 2002) In the Ross Sea Region

detailed information on long-term Adelie penguin paleodiet

composition prey fluctuations and possible environmental

implications is lacking with the exception of the southern

area At Ross Island a 1000-year record of Adelie penguin

diet indicates P antarcticum as the most abundant non-krill

prey species although it has been decreasing in importance

over the past 600 years perhaps in response to the Little Ice

Age cooling period (Polito et al 2002) The present study

investigates for the first time an up-to-7000 BP Adelie

penguin non-krill paleodiet record distributed in an about

600-km-long spatial dataset spanning from Cape Adare

(71180S) to Dunlop Island (77140S) along the Victoria

Land Coast Ross Sea The extent of the investigated spatial

and temporal context allows us to reconstruct the as yet

longest and widest Adelie penguin paleodietary record of

Victoria Land

97 previously 14C-dated penguin guano samples col-

lected from several locations have been analyzed through

taxonomic identification and quantification of recovered

fish otoliths Compared to previous studies the accurate

stratigraphic sampling of ornithogenic soils has provided a

more detailed and precise paleodiet reconstruction This

archeological approach allows us to collect soil samples

weighing only some 100 grams preventing the complete

destruction of the relict colonies which must be considered

a unique record of the heritage of penguin settling

Polar Biol

123

Materials and methods

Study area and geomorphological setting

Extending southward from about 71180S (Cape Adare) to

78000S (McMurdo Sound) the Victoria Land (hereafter

reported as VL) coast borders the western side of the Ross

Sea (Fig 1)

Aerial photograph analysis several field surveys

detailed geomorphologic analyses of key sites and

ornithogenic soil sampling were conducted in previous

studies in ice-free areas along the VL coast (Baroni and

Orombelli 1991 1994a Baroni and Hall 2004 Hall et al

2004) (Fig 1) Adelie penguin-abandoned nesting sites

represent a common landscape feature of the ice-free VL

coast They occur both at the outskirts of present-day

colonies and in areas no longer occupied by penguins

(Fig 1) Resting on Holocene raised beaches marine ter-

races debris cones and slopes piedmont rock-glaciers and

ice-cored and depositional moraines abandoned Adelie

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 Adelie penguins do not nest

Conservative excavation technique and sample

collection

After identifying abandoned penguin settlements we

established test pits generally 1ndash6 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

sampling setting with regard to the number of retrievable

guano samples

Laboratory analyses

Ninety-seven 14C previously dated penguin guano samples

were processed in the laboratory to recover penguin dietary

remains Previously published papers (cfr Baroni 1994

Baroni and Orombelli 1991 1994a Lambert et al 2002

Baroni and Hall 2004 Hall et al 2004) provided samples

used in this study spanning up to 7200 BP corrected ages

All conventional dates (in 14C BP) were in fact corrected for

the upwelling of old water in the Southern Ocean by sub-

tracting a marine-carbon reservoir effect of 1300 years

(Berkman and Forman 1996) and thereafter all the values

reported in the present study were marine effect removed

At the moment this value represents the best estimate and

conventional value used for the Ross Sea region based on

dates of lsquolsquopre-bombrsquorsquo organisms (ie before 1950) of

known ages (Berkman and Forman 1996) Although cali-

brating the dates would be preferable this approach

allowed us to compare the dates from the penguin remains

with sets of dates supplied by other organisms (ie ele-

phant seals Hall et al 2006) and with other proxy data

such as ice-core datasets (Lorius et al 1985 Petit et al

1997)

Fig 1 Map of the Victoria Land coast showing the geographic

distribution of study sites Ornithogenic soils were sampled at the

margin of presently occupied Adelie penguin colonies (solid circles)

as well as in areas no longer occupied by penguins (relict colonies)

(stars)

Polar Biol

123

Sediments were washed (distilled water) and sieved

through seven nested screens with square mesh sizes

ranging from 2 mm to 63 lm The matrix from each screen

was dried and subsequently sorted under a low-power

(5ndash10x) stereomicroscope to separate eggshell fragments

feathers and dietary remains (otoliths fish vertebrae and

teeth) (Fig 2)

Samples were classified according to the presence

absence of dietary remains and are hereafter reported as

sample with lsquolsquodietary remainsrsquorsquo (DR) or samples with lsquolsquono

dietary remainsrsquorsquo (NDR) respectively Otoliths were sep-

arated from fish bones in order to carry out taxonomic

identification They were identified using anatomic-com-

parative tables proposed by Williams and McEldowney

(1990) for Antarctic fish taxa These prey remains are

quantified by the minimum number of individuals (MNI)

represented for each identified fish taxon According to

Emslie et al (1998) the MNI is determined by counting the

number of whole otoliths of known side (right or left) and

using the greater value of the two sides In addition oto-

liths of unknown side were counted and their number was

halved to give a conservative estimate of the total number

of right and left sides represented which was then added to

the MNI obtained from known-side otoliths to yield a total

MNI for each species

Otoliths were measured using a stereomicroscope with a

micrometric eye piece (10x) to an accuracy of 01 mm The

maximum distances between the rostrum and the posterior

margin (otolith length OL) and between the dorsal and

ventral margins (otolith width OW) were measured By

using given regression formulae morphometric analysis of

the otoliths provides a mean estimate of prey item size

(Williams and McEldowney 1990) Since very few other

fish taxa remains were found only P antarcticum otoliths

were considered The corresponding standard length (SL)

in millimeters was determined according to the regression

equations calculated by Williams and McEldowney (1990)

Fish otoliths show clear erosion signals ranging from 2

to 4 according to Leopold et al (1998) but most of them

still preserve the morphological parameters required for

taxon identification Not all recovered fish otoliths were

suitable for the morphometric analysis because some were

strongly eroded or broken Especially for the smallest

otoliths (B250 lm) the smoothed borders made it impos-

sible to orient the otolith correctly and to distinguish the

dorsal and ventral margins from the anterior and posterior

ones To avoid any estimation bias we selected and mea-

sured only those otoliths with well recognizable

morphometric parameters To avoid bias due to variable

amounts of sorted sediments we express the relative den-

sity as the ratio of MNIdry mass by dividing the MNI

value by the total mass (in gram) for each guano sample

Statistical analysis

In order to evaluate the possible factors affecting the

presence of fish remains in the ornithogenic samples we

built three logistic models (Tabachnick and Fidell 1996)

using as binary-dependent variable the presenceabsence

of (a) dietary remains (b) P antarcticum (c) other iden-

tified species and as independent variables the latitude and

the age of the samples In model (b) and (c) samples

containing only unidentified fish bones (n = 18) were

excluded from these analyses Fish taxa different from

silverfish were very low in number and thus were grouped

into a unique category named lsquolsquoother fishrsquorsquo

Differences in the standard length of silverfish with

respect to latitude were analyzed with the MannndashWhitney

non-parametric test All tests were two-tailed and the sta-

tistical significance was set to a = 005 For this analysis

samples were grouped by dividing the Ross Sea into two

main regions the north and the south with respect to the

Drygalski ice tongue which extend from Cape Adare to

Inexpressible Is (North N) and from Cape Irizar to Dunlop

Is (South S) All the analyses were performed using the

software SPSS 120 All mean are given as plusmn1 SD

Results

Matrix screening and sorting allowed us to recover a large

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 sidePleuragramma antarcticumotolith b fish vertebra c fish

tooth d penguin eggshell

fragment

Polar Biol

123

penguin bones feathers eggshell fragments and hard parts

of dietary remains such as fish bones (vertebrae) scales

and otoliths Since krill and their fragile carapaces are not

preserved in sediments the ornithogenic soils investigation

provided data only about the non-euphausiid (ie fish)

paleodietary components The thickness of ornithogenic

soils ranged from centimeters to decimeters and the mean

mass of the samples was 186 g (range 6ndash885 g) Among a

total of 97 samples 32 did not contain dietary remains

(NDR) and 18 contained only fish vertebrae (Table 1) In

NDR samples neither fish bones nor otoliths were recov-

ered but eggshell fragments and feathers testified to the

ornithogenic nature of those samples and confirmed the

presence of nesting sites

Among the 16 visited localities Cape Irizar Prior

Island Cape Ross and Cape Day were the most productive

in terms of the number of fish otoliths Samples from

Gondwana station samples were the richest in fish bones

but no otoliths were found At Inexpressible Island Cape

Hickey and Depot Island there was a clear prevalence of

NDR compared to the DR samples (Table 1)

Otoliths were found in 47 samples and were analyzed

to identify prey taxa A total of 677 otoliths correspond-

ing to 409 individuals (87 plusmn 1258 preys per sample)

belonging to four taxa were identified (Table 2) Taxo-

nomic identification indicated that all penguins fish prey

belonged to the family Nototheniidae and consisted

mainly of P antarcticum (9010 of MNI) followed

by Pagothenia sp (340 of MNI) and Trematomus sp

(148 of MNI) Among the individuals of the genus

Trematomus six were recognized as Trematomus ber-

nacchii The rest of the recovered otoliths (502) too

eroded to estimate side and size are taxonomically

uncertain but among the family Nototheniidae

Comparison among dietary items latitude and age

Results from model (a) showed that neither latitude nor age

had an effect on the presenceabsence of fish remains in all

the ornithogenic samples (n = 97) (Table 3) On the con-

trary the model (b) revealed that the age of the samples

significantly explained the presence of P antarcticum

while the latitude did not appear to have any explanatory

effect (Table 3) The model (b) correctly reclassified

804 of the samples with P antarcticum and 62 of the

Table 1 Number of dietary remains recovered in ornithogenic soil samples discovered in Victoria Land

Collection site Latitude No of guano

samples (NDR)

Radiocarbon

date range (BP)

Total mass

(g)

No of recovered

fish otolith

No of recovered

fish bones

Cape Adare 71180S 1 1180 38 1 1

Duke of York 71370S 1 920 121 ndash 11

Cape Hallett 72190S 4(1) 320ndash400 3155 11 4

Edmonson point 74200S 5(1) 770ndash990 801 12 13

Gondwana station 74380S 2 3330ndash3370 280 ndash 112

Terra Nova station 74420S 9(1) 3580ndash5180 1716 50 178

Icarus Camp 74430S 21(9) 2780ndash6060 4389 47 29

N Adelie Cove 74460S 7(2) 4525ndash7190 1490 8 17

Inexpressible Island 74530S 9(5) 1220ndash5058 2078 9 6

Cape Irizar 75340S 7 860ndash4010 1830 299 1

Prior Island 75410S 6(1) 2980ndash4525 834 118 3

Cape Hickey 76050S 10(7) 1985ndash6240 16274 29 2

N Cape Day 76150S 1 3060 226 41 ndash

Depot Island 76420S 5(4) 2020ndash5840 766 10 1

Cape Ross 76440S 5(1) 2835ndash3015 7535 36 27

Dunlop Island 77140S 4 2230ndash4330 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

Table 2 Fish taxa identified from otoliths recovered from ornitho-

genic soils sampled at Adelie penguin colonies along the Victoria

Land coast Ross Sea Antarctica

Taxon Number of otoliths () MNI ()

Pleuragramma antarcticum 610 (9010) 355 (9126)

Trematomus sp 10 (148) 10 (257)

Pagothenia sp 23 (340) 17 (437)

Unidentified Nototheniidae 34 (502) 27 (694)

Total 677 409

The total numbers of identifiable otoliths and MNI are provided for

each taxon percentages are reported in parentheses

Polar Biol

123

all samples In fact the age distribution of the samples

confirms that fish remains increased in samples dated

between 2000 and 4000 BP a period that includes the time

lag defined as the lsquolsquopenguin optimumrsquorsquo by Hall et al (2006)

(Fig 3)

Fish species different from P antarcticum composed a

very small percentage of the organic material sorted in the

ornithogenic sediment Species other than silverfish

occurred only at southern latitudes between 74420 and

77140S When included in the logistical model (c) the

presenceabsence of other fishes was significantly

explained by the latitude alone (Table 3) and the model

correctly reclassified 797 of the samples

Prey size classes in ornithogenic soils

A morphometric analysis of 380 Antarctic silverfish

otoliths showed that the mean silverfish SL was

6723 plusmn 2347 mm (range 4018ndash18267) Furthermore

our data indicate that 8289 of the silverfish eaten by

Adelie penguins belonged to the 40ndash80 mm length class

(Fig 4)

There was no significant difference in the distribution of

the size classes of P antarcticum according to age of the

samples Grouping colonies according to a north to south

gradient samples from the northern colonies (n = 70 mean

7139 plusmn 23007 mm) contained longer Antarctic silverfish

compared to the southern colonies (n = 310 mean

66285 plusmn 23508 mm) this difference appears to be sig-

nificant (U MannndashWhitney = 782850 Z = -3521

P = 0000)

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 74420 and

77140S (866) The abundance in guano samplersquos

availability during this period may be a consequence of the

great spread of Adelie penguin colonies recorded for the

VL between 2300 and 4000 BP and indicated as the lsquolsquopen-

guin optimumrsquorsquo (cfr Baroni and Orombelli 1994a Hall

et al 2006)

Table 3 Logistic models testing the effect of latitude and age on the

presenceabsence in the ornithogenic samples of models a b c

Variable B Wald statistic df P

Model a) Latitude -0840 0140 1 0709

Age of samples 0000 2701 1 0100

Constant 7914 0223 1 0637

Model b) Latitude 0032 0017 1 0896

Age of samples 0000 5463 1 0019

Constant -0651 0001 1 0972

Model c) Latitude 0653 3757 1 0050

Age of samples 0000 0010 1 0921

Constant -50665 3955 1 0047

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-uragramma antarcticum) (n = 79 16 with other species and 63

without)

Significant effects are indicated

Fig 3 Samples with fish remains (DR) (n = 65 black bars) and

samples with P antarcticum (n = 46 light bars) grouped for each

1000 years (from 320 to 7200 BP) NDR samples of the period are

reported in parentheses The time periods of occupational history for

Victoria Land as described by Hall et al (2006) are reported in the

background

Pleuragramma antarcticum

0

5

10

15

20

25

30

0 10 20 30 40 50 60 70 80 90 100 110 120 130 140 150 160 170 180

SL classes (mm)

Fre

qu

ency

of

occ

urr

ence

(

)

Fig 4 Antarctic silverfish size class distribution in ornithogenic

samples For each class the lower limit (mm) is reported

Polar Biol

123

Except for fish otoliths and bones no other dietary

remains were recovered in this study although Polito et al

(2002) identified several squid beaks in organic sediments

at Ross Island One possible explanation for the lack of

squid remains in our sample could be the lower preserva-

tion of the cephalopod beak compared to fish otoliths

(Emslie and McDaniel 2002) or it is possible that squid did

not contribute to the diet of Adelie penguins in the inves-

tigated period and locations Assuming that Adelie

penguins are still feeding upon the same preys since the

Holocene recent literature reports that squid are preyed

during the summer in East Antarctica and the Weddell Sea

but have not been reported for the Ross Sea (cfr Ainley

2002) In this region two krill species (Euphausia superba

and E crystallorophias) and fish compose the Adelie

penguin diet mixed together in different proportions

(Ainley 2002 Olmastroni et al 2000)

Temporal and spatial variation of prey

Taxonomic identification of fish otoliths indicated P ant-

arcticum as the most eaten prey throughout the investigated

period The abundance of Antarctic silverfish remains

identified in this study agrees with previous paleodietary

investigations in the Antarctica Peninsula East Antarctica

and in the southern Ross Sea region (Emslie and McDaniel

2002 McDaniel and Emslie 2002 Polito et al 2002

Emslie and Woehler 2005) 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 50ndash75 by mass to the Adelie penguin diet even

exceeding crystal krill (E crystallorophias) consumption

in the southern Ross Sea (Ainley 2002 Ainley et al 2003)

Only a very low percentage of remains belongs to other

fish genera The interspecific variation in samples found

exclusively at southern latitudes was probably a conse-

quence of the fact that those samples composed 866 of

the total and contained 96 of the recovered otoliths The

low percentage of occurrence of lsquolsquoother speciesrsquorsquo in our

samples is not surprising Adelie penguins primarily forage

in the continental shelf waters surrounding Antarctica

which are characterized by a very low ichthyic biodiversity

(cfr Ainley 2002) Most unidentifiable fish otoliths

retrieved in the older guano samples maybe related to

sediment transformation processes (such as pedogenesis

and diagenesis) However since many of the best-pre-

served P antarcticum otoliths come from the older guano

samples preservation factors appear here to be related

more to acidic digestion processes rather than to the sample

age or to erosion action through time This is also

supported by the dry and cold condition of Antarctic

environment where the arid climate and low temperatures

slow the damage action of soil processes on organic

remains

Latitude did not significantly affect the mean relative

abundance of Antarctic silverfish indicating that in the past

this species represented an important food source for

penguin breeding throughout the VL coast This prey

species has fluctuated in importance over the past

6000 years (Fig 3) This pattern seems to agree with Hall

et al (2006) who delineated the Adelie penguin and ele-

phant seal occupation history for the VL coast Decreasing

periods of silverfish remains in the present study (Fig 3

1000ndash2000 and 5000ndash6000 BP) correspond approximately

to the seal optimum (1100ndash2300 BP) and to the coeval

occupation (ie contemporary occupation by both species)

(4000ndash6000 BP) reported by Hall et al (2006) Both of

these periods were characterized by a sea ice decrease in

the Ross Sea particularly severe during the most recent

period On the other hand our data show an increase in the

silverfish remains abundance in the past 1000 years and

during the lsquolsquopenguin optimumrsquorsquo this latter being the highest

value among all the investigated periods The lsquolsquopenguin

optimumrsquorsquo and the most recent ages were characterized by

higher sea ice in the Ross Sea region producing a more

fitting habitat for the sea ice obligate Adelie penguin (Hall

et al 2006) The shifts in the presence of fish remains and

in particular of P antarcticum might also represent chan-

ges in Antarctic silverfish population according to the sea

ice advance and retreat (Eastman 1993) Zane et al (2006)

used mitochondrial DNA sequencing to hypothesize that a

demographic expansion that occurred for P antarcticum

during a cooling period (last glaciation peak 111000ndash

126000 BP) suggesting a strong link between this species

(and its prey cfr Smetacek and Nicol 2005) and paleo-

climatic regime shifts

Nevertheless Antarctic silverfish is characterized by a

strong trophic flexibility and adaptability (Eastman 1993

Zane et al 2006) and at present compose the main part of

the diet of marine predators which are also ice-avoiding

species that prefer open water such as elephant seals

(Daneri and Carlini 2002) For this reason we hypothesize

that rather than indicating a decrease in silverfish avail-

ability the shifts in abundance of P antarcticum in the

present study could reflect a higher number of fish remains

in samples as a consequence of a higher number of birds

attending the colonies during periods with more sea ice

Prey size selection

Despite their dense structures fish otoliths are exposed to

variable mechanical and chemical abrasions on calcium

carbonate in the digestive tracts of predators The

Polar Biol

123

susceptibility of fish otoliths (and bones) to digestive ero-

sion appears to change widely taxon by taxon (Harkonen

1986 Pierce et al 1993 Tollit et al 1997) Furthermore in

the ornithogenic soils continuous freezethaw action

through time and sediment transformation processes can

contribute to the consumption and damage of otoliths

These erosive processes act on otolith morphological fea-

tures and size and can lead to non-detection of some prey

categories or of some individuals in a prey category and to

underestimation of prey body size Nevertheless the rela-

tive frequency and size of prey estimated from the hard

remains found in guano samples are valuable and are very

likely the only available information on the kind of prey

consumed

Juvenile P antarcticum with a 40ndash80 mm standard

length range (conforming to juvenile age classes 1 and

2 Hubold and Tomo 1989) are the most-represented

individuals in the VL sediments McDaniel and Emslie

(2002) recognized this prevalence in Northern Marguerite

Bay (Antarctic Peninsula) although with a wider value

range (1582ndash1874 mm) and higher mean SL (10819 plusmn

2553 mm) Juvenile P antarcticum occur primarily at

depths of 50ndash400 m and are well accessible to penguin

capture since their normal foraging depths range between 3

and 98 m (Chappell et al 1993) When analyzing the

temporal distribution of P antarcticum SL significant

differences were not found throughout the investigated

period In Northern Marguerite Bay (Antarctic Peninsula)

(McDaniel and Emslie 2002) some variations within mean

silverfish SL have been recognized among different time

periods but these did not result in a predictable temporal

pattern in accord with past climate change although

Holocene climatic environmental changes are well docu-

mented in both the Antarctic Peninsula and the Ross Sea

region (Bjorck et al 1996 Ingolfsson et al 1998 Baroni

and Orombelli 1991 1994b Baroni and Hall 2004 Hall

et al 2004 2006) The absence of temporal variations of

the silverfish size over the past 7000 years reflects a cer-

tain stability in penguin foraging habits which is also

confirmed by modern diet data on the species predated (crf

Ainley 2002) and on the prey size (Olmastroni et al 2004a

b) No significant temporal variation in prey size was

found The significant difference in silverfish mean size

between the northern and southern colonies was not due to

the amount of older thus more eroded otoliths in the

southern samples In fact the percentage of recent otoliths

for the north and south colonies remains very similar for

the 0ndash1000 period (20 and 1967) and furthermore

northern samples contain higher percentages of older

(period 4000ndash6000) otoliths with respect to the south area

(6713 and 4806 respectively) Therefore although the

difference accounts only for a mean value of 511 mm we

can hypothesize that at least in the past penguins breeding

in colonies located north of the Drygalski ice tongue were

feeding on slightly larger Antarctic silverfish

Sample without fish remains are they evidence

of a dietary shift

Although fish otoliths and bones regularly occur in the

analyzed ornithogenic sediments some guano samples did

not provide any kind of dietary remains Polito et al (2002)

reported the occurrence of feathers in Cape Bird organic

levels without dietary remains which may reflect their

deposition at the time when the area was used by penguin

only to molt and not to nest Stratigraphic and geomor-

phologic features of our samples indicate their nesting site

origin confirmed by the presence of eggshell fragments

collected at the same level suggesting that penguins were

nesting A small number of breeding penguins could be

responsible for the paucity of remains or erosion processes

may have accounted for otolith loss We can also hypoth-

esize that the lack of prey remains could be a shift to a

prevalent non-fish diet Considering in fact that krill is not

maintained in the soils guano samples without fish remains

could reflect a tendency towards a prevalent krill-based

paleodiet At present time Adelie penguin diet switching

between fish and krill may reflect changes in the foraging

setting in relation to environmental and ecological features

Several authors indicated particular climate and marine

conditions (ie sea-ice extension and persistence) as cause

of penguin dietary fluctuation between fish and krill

(Ainley et al 1998 Olmastroni et al 2000 cfr Ainley

2002 Ainley et al 2003) But Ainley et al (2006) in a

more recent study suggested also that feeding competition

among penguins and cetaceans rather than change in

sea-ice cover can better explain the annual switch in the

penguinsrsquo prey items

If the temporal distribution of DR samples versus NDR

ones revealed no significant differences some consider-

ations on their spatial distribution could be made In certain

locations including Inexpressible Island Cape Hickey and

Depot Island NDR guano samples prevail over those

containing fish remains (Table 1) In these cases particular

local marine conditions or other ecological factors as well

as foraging competition with other predators could have

resulted in different krill availability andor consumption

(cfr Ainley et al 2006) Occurring in earlier periods at

Inexpressible Island (5058ndash3900 BP) and later at Cape

Hickey (4075ndash1985 BP) and at Dunlop Island (3100ndash2020

BP) it is not possible to define a common paleoenviron-

mental factor that explains this pattern at the regional scale

At Inexpressible Island for example between 6000 and

4000 BP Adelie penguins shared ice-free coastal terrain

with elephant seals (Hall et al 2006) Thus it is possible

that in this area feeding competition due to this coeval

Polar Biol

123

occupation led penguins to change their diet by targeting

primarily krill which may be eaten only occasionally by

elephant seals (Daneri and Carlini 2002 van den Hoff et al

2003) Even if not revealed by the spatial and temporal

distribution of our samples different sea ice regimes

(Olmastroni et al 2004a b) andor mega icebergs calving

(Arrigo et al 2002) might have had an effect at local scale

These events in fact are known to play an important role on

penguin life cycle and they have been reported to occur in

the past (cfr Shepherd et al 2005)

Although Holocene climatic and environmental changes

have clearly affected the VL coast as indicated by Adelie

penguin colonization history (Baroni and Orombelli

1994a Lambert et al 2002 Emslie et al 2003 Hall et al

2006) over the past 7000 years the Ross Sea ecosystem

seemed to be a relatively stable ecosystem with P ant-

arcticum being the most important fish component in the

Adelie penguin diet for several thousand years The

present study provides the most detailed Adelie penguin

paleodiet records for this area These records may supply

new insights into the past feeding penguin behavior in

the VL coastal area and on a larger scale about the

ecological conditions of the Ross Sea ecosystem during

the Holocene

Acknowledgments This work was executed within the framework

of the Italian National Program on Antarctic Research (PNRA) and

was financially supported by joint research programs in geology at

the University of Pisa The authors thank Fabrizio Ciampolini

(University of Siena) for scanning electron micrographs Silvano

Focardi head of the laboratories at the Department of Environ-

mental Science (University of Siena) where the morphometric

analyses were performed David Lambert Grant Ballard and one

anonymous referee greatly improved an earlier version of the

manuscript

References

Ainley DG (2002) The Adelie penguin bellwether of climate change

Columbia University Press New York

Ainley DG Wilson PR Barton KJ Ballard G Nur N Karl B (1998)

Diet and foraging effort of Adelie penguins in relation to pack-

ice conditions in the southern Ross Sea Polar Biol 20311ndash319

doi101007s003000050308

Ainley DG Ballard G Barton KJ Karl BJ Rau GH Ribic CA

Wilson PR (2003) Spatial and temporal variation of diet within a

presumed metapopulation of Adelie penguins Condor 10595ndash

106 doi1016500010-5422(2003)105[95SATVOD]20CO2

Ainley DG Ballard G Dugger KM (2006) Competition among

penguins and cetaceans reveals trophic cascade in the Western

Ross Sea Antarctica Ecology 872080ndash2093 doi1018900012-

9658(2006)87[2080CAPACR]20CO2

Arrigo KR van Dijken GL Ainley DG Fahnestock MA Markus T

(2002) Ecological impact of a large Antarctic iceberg Geophys

Res Lett 291104 doi1010292001GL014160

Baroni C (1994) Notes on late-glacial retreat of the Antarctic ice sheet

and Holocene environmental changes along the Victoria Land

Coast Mem Natl Inst Polar Res (Jpn) C 5085ndash107

Baroni C Hall BL (2004) A new Holocene relative sea-level curve for

Terra Nova Bay Victoria Land Antarctica J Quat Sci 19377ndash

396 doi101002jqs825

Baroni C Orombelli G (1991) Holocene raised beaches at Terra

Nova Bay Victoria Land Antartica Quat Res 36157ndash177

doi1010160033-5894(91)90023-X

Baroni C Orombelli G (1994a) Abandoned penguin rookeries

as Holocene paleoclimatic indicators in Antarctica Geology

2223ndash26 doi1011300091-7613(1994)0220023APRAHP[23CO2

Baroni C Orombelli G (1994b) Holocene glacier variations in Terra

Nova bay area (Victoria Land Antartica) Antarct Sci 6497ndash

505 doi101017S0954102094000751

Barrett JE Virginia RA Hopkins DW Aislabie J Bargagli R

Bockheim JG Campbell IB Lyons WB Moorhead DL Nkem

JN Sletten RS Steltzer H Wall DH Wallenstein MD (2006)

Terrestrial ecosystem processes of Victoria Land Antarctica

Soil Biol Biochem 383019ndash3034 doi101016jsoilbio2006

04041

Berkman PA Forman SL (1996) Pre-bomb radiocarbon and the

reservoir correction for calcareous marine species in the

Southern Ocean Geophys Res Lett 23363ndash366 doi101029

96GL00151

Bjorck S Hakansson H Olsson S Ellis-Evans C Humlum O Lirio

JM (1996) Late Holocene palaeoclimatic records from lakes

sediments on James Ross Island Antarctica Palaeogeogr

Palaeoclimatol Palaeoecol 113195ndash220 doi1010160031-

0182(95)00086-0

Bochenski Z (1985) Remains of subfossil birds from King George

Island (South Shetland Islands) Acta Zool Cracov 29109ndash116

Chappell MA Shoemaker VH Janes DN Bucher TL Maloney SK

(1993) Diving behavior during foraging in breeding Adelie

penguins Ecol USA 741204ndash1215

Daneri GA Carlini AR (2002) Fish prey of southern elephant seals

Mirounga leonine at King George Island Polar Biol 25739ndash743

Eastman JT (1993) Antarctic fish biology evolution in a unique

environment Academic Press San Diego

Emslie SD (1995) Age and taphonomy of abandoned penguin

rookeries in the Antarctic Peninsula region Polar Rec (Gr Brit)

31409ndash418

Emslie SD (2001) Radiocarbon dates from abandoned penguin

colonies in the Antarctica peninsula region Antarct Sci

13289ndash295 doi101017S0954102001000414

Emslie SD McDaniel JD (2002) Adelie penguin diet and climate

change during the middle to late Holocene in northern Margue-

rite Bay Antarctic Peninsula Polar Biol 25222ndash229

Emslie SD Patterson WP (2007) Abrupt shift in d13C and d15N

values in Adelie penguin eggshell in Antarctica Proc Natl Acad

Sci USA 10411666ndash11669 doi101073pnas0608477104

Emslie SD Woehler EJ (2005) A 9000-year record of Adelie penguin

occupation and diet in the Windmill Islands East Antarctica

Antarct Sci 1757ndash66 doi101017S0954102005002427

Emslie SD Fraser W Smith RC Walker W (1998) Abandoned

penguin colonies and environmental change in the Palmer

Station area Anvers Island Antarctic Peninsula Antarct Sci

10257ndash268 doi101017S0954102098000352

Emslie SD Berkman PA Ainley DG Coats L Polito M (2003) Late-

Holocene initiation of ice-free ecosystems in the southern Ross

Sea Antarctica Mar Ecol Prog Ser 26219ndash25 doi103354

meps262019

Emslie SD Coats L Licht K (2007) A 45000 year record of Adelie

penguins and climate change in the Ross Sea Antarctica

Geology 3561ndash64 doi101130G23011A1

Hall BL Baroni C Denton GH (2004) Holocene relative sea-level

history of the Southern Victoria Land Coast Antarctica Glob

Planet Chang 42241ndash263 doi101016jgloplacha200309004

Polar Biol

123

ornithogenic soils have revealed different guano layers (up

to five) that record multi-occupational phases of the colo-

nies (Baroni and Orombelli 1991 1994a Baroni and Hall

2004) Radiocarbon-dated penguin remains such as bones

guano and eggshell fragments collected from these organic

soils provide a multi-millenary record of Adelie Penguin

colonization that has been revealed to be particularly

interesting for paleoenvironmental studies (Baroni and

Orombelli 1991 1994a Baroni 1994 Emslie 2001 Lambert

et al 2002 Emslie et al 2003 Shepherd et al 2005

Hall et al 2006 Emslie and Patterson 2007 Emslie et al

2007) Adelie penguins are sensitive indicators of the

Antarctic climate and of environmental parameters that

regulate their presence and distribution (Ainley 2002)

Where ornithogenic soils are common features Adelie

penguins have found encouraging ecological conditions for

their colonization At these sites the endurance of these

favorable setting environments is related to the thickness of

these soils an enduring occupation of a colony drops a

thick layer made from nest pebbles penguin remains and

guano and the older the colony the thicker the accumu-

lation of guano (Ugolini 1972) In particular well-

developed sequences of ornithogenic soils testify the

ancient availability of ice-free coastal terrains suitable to

nest and breed In Victoria Land (Ross Sea) radiocarbon

dating of penguin guano bones and eggshells collected

from these soils together with other datable organic mate-

rials provides data for reconstructing the retreat of glaciers

in coastal areas after the last Glacial Maximum (amp18ndash

20000 years Before Present BP) and the following emer-

sion of coastline during the Holocene period (starting about

8000 BP) (Baroni and Orombelli 1991 1994b Baroni and

Hall 2004 Hall et al 2004) Radiocarbon dates from

abandoned penguin colonies scattered on the VL coast

(from the northernmost site at Cape Adare to the south-

ernmost sites at Ross Island) indicate that Adelie penguins

occupied colonies in the Terra Nova Bay region since 7200

BP (Baroni and Orombelli 1994a) The occurrence of

ornithogenic soils both in the vicinity of currently occupied

colonies and in areas no longer colonized by penguins

attests that during the Holocene the penguin population

varied according to changing environmental conditions

(Baroni and Orombelli 1994a Lambert et al 2002 Polito

et al 2002) Especially after the period between 4500 and

2500 BP indicated as a lsquolsquopenguin optimumrsquorsquo by Baroni and

Orombelli (1994a) abrupt environmental changes caused a

drastic abandonment of several colonies and a dramatic

decrease in the penguin population on the southern Scott

Coast and in Terra Nova Bay (Baroni and Orombelli

1994a) Between 2300 and 1100 BP as documented by the

contemporary great spreading of elephant seals (Mirounga

leonina) in the Ross Sea Embayment the establishment

and persistence of sub-Antarctic climaticenvironmental

conditions inhibited the presence and settling of Adelie

penguin colonies (Hall et al 2006)

Ornithogenic soils also well preserve hard parts of die-

tary remains such as fish otoliths bones teeth and squid

beaks Calcareous fish otoliths and chitinous squid beaks in

particular have demonstrated a strong preservation power

Taxonomic identification of such remains allows us to

define a long-term Adelie penguin paleodietary record

(Emslie et al 1998 McDaniel and Emslie 2002 Emslie

and McDaniel 2002 Polito et al 2002 Emslie and

Woehler 2005)

Previous paleoecological studies have yielded consi-

derable dietary information on non-krill prey thanks to the

excellent preservation of remains found within ornithogenic

soils Concentrated in the area of the Antarctica Peninsula

and in the East Antarctica these studies have confirmed that

from the mid-Holocene to the present day the Antarctic

silverfish (Pleuragramma antarcticum Boulenger 1902)

and glacial squid (Psychroteuthis glacialis Thiele 1920)

have been important components in the Adelie penguin

diet being the most common species represented in the

sediments (Emslie et al 1998 Emslie 2001 Emslie and

McDaniel 2002 McDaniel and Emslie 2002 Emslie and

Woehler 2005) Furthermore the proportion of these prey

items in the past Adelie penguin diet varied in accordance

with climatic cooling and warming trends (cfr Emslie et al

1998 Emslie and McDaniel 2002) In the Ross Sea Region

detailed information on long-term Adelie penguin paleodiet

composition prey fluctuations and possible environmental

implications is lacking with the exception of the southern

area At Ross Island a 1000-year record of Adelie penguin

diet indicates P antarcticum as the most abundant non-krill

prey species although it has been decreasing in importance

over the past 600 years perhaps in response to the Little Ice

Age cooling period (Polito et al 2002) The present study

investigates for the first time an up-to-7000 BP Adelie

penguin non-krill paleodiet record distributed in an about

600-km-long spatial dataset spanning from Cape Adare

(71180S) to Dunlop Island (77140S) along the Victoria

Land Coast Ross Sea The extent of the investigated spatial

and temporal context allows us to reconstruct the as yet

longest and widest Adelie penguin paleodietary record of

Victoria Land

97 previously 14C-dated penguin guano samples col-

lected from several locations have been analyzed through

taxonomic identification and quantification of recovered

fish otoliths Compared to previous studies the accurate

stratigraphic sampling of ornithogenic soils has provided a

more detailed and precise paleodiet reconstruction This

archeological approach allows us to collect soil samples

weighing only some 100 grams preventing the complete

destruction of the relict colonies which must be considered

a unique record of the heritage of penguin settling

Polar Biol

123

Materials and methods

Study area and geomorphological setting

Extending southward from about 71180S (Cape Adare) to

78000S (McMurdo Sound) the Victoria Land (hereafter

reported as VL) coast borders the western side of the Ross

Sea (Fig 1)

Aerial photograph analysis several field surveys

detailed geomorphologic analyses of key sites and

ornithogenic soil sampling were conducted in previous

studies in ice-free areas along the VL coast (Baroni and

Orombelli 1991 1994a Baroni and Hall 2004 Hall et al

2004) (Fig 1) Adelie penguin-abandoned nesting sites

represent a common landscape feature of the ice-free VL

coast They occur both at the outskirts of present-day

colonies and in areas no longer occupied by penguins

(Fig 1) Resting on Holocene raised beaches marine ter-

races debris cones and slopes piedmont rock-glaciers and

ice-cored and depositional moraines abandoned Adelie

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 Adelie penguins do not nest

Conservative excavation technique and sample

collection

After identifying abandoned penguin settlements we

established test pits generally 1ndash6 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

sampling setting with regard to the number of retrievable

guano samples

Laboratory analyses

Ninety-seven 14C previously dated penguin guano samples

were processed in the laboratory to recover penguin dietary

remains Previously published papers (cfr Baroni 1994

Baroni and Orombelli 1991 1994a Lambert et al 2002

Baroni and Hall 2004 Hall et al 2004) provided samples

used in this study spanning up to 7200 BP corrected ages

All conventional dates (in 14C BP) were in fact corrected for

the upwelling of old water in the Southern Ocean by sub-

tracting a marine-carbon reservoir effect of 1300 years

(Berkman and Forman 1996) and thereafter all the values

reported in the present study were marine effect removed

At the moment this value represents the best estimate and

conventional value used for the Ross Sea region based on

dates of lsquolsquopre-bombrsquorsquo organisms (ie before 1950) of

known ages (Berkman and Forman 1996) Although cali-

brating the dates would be preferable this approach

allowed us to compare the dates from the penguin remains

with sets of dates supplied by other organisms (ie ele-

phant seals Hall et al 2006) and with other proxy data

such as ice-core datasets (Lorius et al 1985 Petit et al

1997)

Fig 1 Map of the Victoria Land coast showing the geographic

distribution of study sites Ornithogenic soils were sampled at the

margin of presently occupied Adelie penguin colonies (solid circles)

as well as in areas no longer occupied by penguins (relict colonies)

(stars)

Polar Biol

123

Sediments were washed (distilled water) and sieved

through seven nested screens with square mesh sizes

ranging from 2 mm to 63 lm The matrix from each screen

was dried and subsequently sorted under a low-power

(5ndash10x) stereomicroscope to separate eggshell fragments

feathers and dietary remains (otoliths fish vertebrae and

teeth) (Fig 2)

Samples were classified according to the presence

absence of dietary remains and are hereafter reported as

sample with lsquolsquodietary remainsrsquorsquo (DR) or samples with lsquolsquono

dietary remainsrsquorsquo (NDR) respectively Otoliths were sep-

arated from fish bones in order to carry out taxonomic

identification They were identified using anatomic-com-

parative tables proposed by Williams and McEldowney

(1990) for Antarctic fish taxa These prey remains are

quantified by the minimum number of individuals (MNI)

represented for each identified fish taxon According to

Emslie et al (1998) the MNI is determined by counting the

number of whole otoliths of known side (right or left) and

using the greater value of the two sides In addition oto-

liths of unknown side were counted and their number was

halved to give a conservative estimate of the total number

of right and left sides represented which was then added to

the MNI obtained from known-side otoliths to yield a total

MNI for each species

Otoliths were measured using a stereomicroscope with a

micrometric eye piece (10x) to an accuracy of 01 mm The

maximum distances between the rostrum and the posterior

margin (otolith length OL) and between the dorsal and

ventral margins (otolith width OW) were measured By

using given regression formulae morphometric analysis of

the otoliths provides a mean estimate of prey item size

(Williams and McEldowney 1990) Since very few other

fish taxa remains were found only P antarcticum otoliths

were considered The corresponding standard length (SL)

in millimeters was determined according to the regression

equations calculated by Williams and McEldowney (1990)

Fish otoliths show clear erosion signals ranging from 2

to 4 according to Leopold et al (1998) but most of them

still preserve the morphological parameters required for

taxon identification Not all recovered fish otoliths were

suitable for the morphometric analysis because some were

strongly eroded or broken Especially for the smallest

otoliths (B250 lm) the smoothed borders made it impos-

sible to orient the otolith correctly and to distinguish the

dorsal and ventral margins from the anterior and posterior

ones To avoid any estimation bias we selected and mea-

sured only those otoliths with well recognizable

morphometric parameters To avoid bias due to variable

amounts of sorted sediments we express the relative den-

sity as the ratio of MNIdry mass by dividing the MNI

value by the total mass (in gram) for each guano sample

Statistical analysis

In order to evaluate the possible factors affecting the

presence of fish remains in the ornithogenic samples we

built three logistic models (Tabachnick and Fidell 1996)

using as binary-dependent variable the presenceabsence

of (a) dietary remains (b) P antarcticum (c) other iden-

tified species and as independent variables the latitude and

the age of the samples In model (b) and (c) samples

containing only unidentified fish bones (n = 18) were

excluded from these analyses Fish taxa different from

silverfish were very low in number and thus were grouped

into a unique category named lsquolsquoother fishrsquorsquo

Differences in the standard length of silverfish with

respect to latitude were analyzed with the MannndashWhitney

non-parametric test All tests were two-tailed and the sta-

tistical significance was set to a = 005 For this analysis

samples were grouped by dividing the Ross Sea into two

main regions the north and the south with respect to the

Drygalski ice tongue which extend from Cape Adare to

Inexpressible Is (North N) and from Cape Irizar to Dunlop

Is (South S) All the analyses were performed using the

software SPSS 120 All mean are given as plusmn1 SD

Results

Matrix screening and sorting allowed us to recover a large

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 sidePleuragramma antarcticumotolith b fish vertebra c fish

tooth d penguin eggshell

fragment

Polar Biol

123

penguin bones feathers eggshell fragments and hard parts

of dietary remains such as fish bones (vertebrae) scales

and otoliths Since krill and their fragile carapaces are not

preserved in sediments the ornithogenic soils investigation

provided data only about the non-euphausiid (ie fish)

paleodietary components The thickness of ornithogenic

soils ranged from centimeters to decimeters and the mean

mass of the samples was 186 g (range 6ndash885 g) Among a

total of 97 samples 32 did not contain dietary remains

(NDR) and 18 contained only fish vertebrae (Table 1) In

NDR samples neither fish bones nor otoliths were recov-

ered but eggshell fragments and feathers testified to the

ornithogenic nature of those samples and confirmed the

presence of nesting sites

Among the 16 visited localities Cape Irizar Prior

Island Cape Ross and Cape Day were the most productive

in terms of the number of fish otoliths Samples from

Gondwana station samples were the richest in fish bones

but no otoliths were found At Inexpressible Island Cape

Hickey and Depot Island there was a clear prevalence of

NDR compared to the DR samples (Table 1)

Otoliths were found in 47 samples and were analyzed

to identify prey taxa A total of 677 otoliths correspond-

ing to 409 individuals (87 plusmn 1258 preys per sample)

belonging to four taxa were identified (Table 2) Taxo-

nomic identification indicated that all penguins fish prey

belonged to the family Nototheniidae and consisted

mainly of P antarcticum (9010 of MNI) followed

by Pagothenia sp (340 of MNI) and Trematomus sp

(148 of MNI) Among the individuals of the genus

Trematomus six were recognized as Trematomus ber-

nacchii The rest of the recovered otoliths (502) too

eroded to estimate side and size are taxonomically

uncertain but among the family Nototheniidae

Comparison among dietary items latitude and age

Results from model (a) showed that neither latitude nor age

had an effect on the presenceabsence of fish remains in all

the ornithogenic samples (n = 97) (Table 3) On the con-

trary the model (b) revealed that the age of the samples

significantly explained the presence of P antarcticum

while the latitude did not appear to have any explanatory

effect (Table 3) The model (b) correctly reclassified

804 of the samples with P antarcticum and 62 of the

Table 1 Number of dietary remains recovered in ornithogenic soil samples discovered in Victoria Land

Collection site Latitude No of guano

samples (NDR)

Radiocarbon

date range (BP)

Total mass

(g)

No of recovered

fish otolith

No of recovered

fish bones

Cape Adare 71180S 1 1180 38 1 1

Duke of York 71370S 1 920 121 ndash 11

Cape Hallett 72190S 4(1) 320ndash400 3155 11 4

Edmonson point 74200S 5(1) 770ndash990 801 12 13

Gondwana station 74380S 2 3330ndash3370 280 ndash 112

Terra Nova station 74420S 9(1) 3580ndash5180 1716 50 178

Icarus Camp 74430S 21(9) 2780ndash6060 4389 47 29

N Adelie Cove 74460S 7(2) 4525ndash7190 1490 8 17

Inexpressible Island 74530S 9(5) 1220ndash5058 2078 9 6

Cape Irizar 75340S 7 860ndash4010 1830 299 1

Prior Island 75410S 6(1) 2980ndash4525 834 118 3

Cape Hickey 76050S 10(7) 1985ndash6240 16274 29 2

N Cape Day 76150S 1 3060 226 41 ndash

Depot Island 76420S 5(4) 2020ndash5840 766 10 1

Cape Ross 76440S 5(1) 2835ndash3015 7535 36 27

Dunlop Island 77140S 4 2230ndash4330 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

Table 2 Fish taxa identified from otoliths recovered from ornitho-

genic soils sampled at Adelie penguin colonies along the Victoria

Land coast Ross Sea Antarctica

Taxon Number of otoliths () MNI ()

Pleuragramma antarcticum 610 (9010) 355 (9126)

Trematomus sp 10 (148) 10 (257)

Pagothenia sp 23 (340) 17 (437)

Unidentified Nototheniidae 34 (502) 27 (694)

Total 677 409

The total numbers of identifiable otoliths and MNI are provided for

each taxon percentages are reported in parentheses

Polar Biol

123

all samples In fact the age distribution of the samples

confirms that fish remains increased in samples dated

between 2000 and 4000 BP a period that includes the time

lag defined as the lsquolsquopenguin optimumrsquorsquo by Hall et al (2006)

(Fig 3)

Fish species different from P antarcticum composed a

very small percentage of the organic material sorted in the

ornithogenic sediment Species other than silverfish

occurred only at southern latitudes between 74420 and

77140S When included in the logistical model (c) the

presenceabsence of other fishes was significantly

explained by the latitude alone (Table 3) and the model

correctly reclassified 797 of the samples

Prey size classes in ornithogenic soils

A morphometric analysis of 380 Antarctic silverfish

otoliths showed that the mean silverfish SL was

6723 plusmn 2347 mm (range 4018ndash18267) Furthermore

our data indicate that 8289 of the silverfish eaten by

Adelie penguins belonged to the 40ndash80 mm length class

(Fig 4)

There was no significant difference in the distribution of

the size classes of P antarcticum according to age of the

samples Grouping colonies according to a north to south

gradient samples from the northern colonies (n = 70 mean

7139 plusmn 23007 mm) contained longer Antarctic silverfish

compared to the southern colonies (n = 310 mean

66285 plusmn 23508 mm) this difference appears to be sig-

nificant (U MannndashWhitney = 782850 Z = -3521

P = 0000)

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 74420 and

77140S (866) The abundance in guano samplersquos

availability during this period may be a consequence of the

great spread of Adelie penguin colonies recorded for the

VL between 2300 and 4000 BP and indicated as the lsquolsquopen-

guin optimumrsquorsquo (cfr Baroni and Orombelli 1994a Hall

et al 2006)

Table 3 Logistic models testing the effect of latitude and age on the

presenceabsence in the ornithogenic samples of models a b c

Variable B Wald statistic df P

Model a) Latitude -0840 0140 1 0709

Age of samples 0000 2701 1 0100

Constant 7914 0223 1 0637

Model b) Latitude 0032 0017 1 0896

Age of samples 0000 5463 1 0019

Constant -0651 0001 1 0972

Model c) Latitude 0653 3757 1 0050

Age of samples 0000 0010 1 0921

Constant -50665 3955 1 0047

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-uragramma antarcticum) (n = 79 16 with other species and 63

without)

Significant effects are indicated

Fig 3 Samples with fish remains (DR) (n = 65 black bars) and

samples with P antarcticum (n = 46 light bars) grouped for each

1000 years (from 320 to 7200 BP) NDR samples of the period are

reported in parentheses The time periods of occupational history for

Victoria Land as described by Hall et al (2006) are reported in the

background

Pleuragramma antarcticum

0

5

10

15

20

25

30

0 10 20 30 40 50 60 70 80 90 100 110 120 130 140 150 160 170 180

SL classes (mm)

Fre

qu

ency

of

occ

urr

ence

(

)

Fig 4 Antarctic silverfish size class distribution in ornithogenic

samples For each class the lower limit (mm) is reported

Polar Biol

123

Except for fish otoliths and bones no other dietary

remains were recovered in this study although Polito et al

(2002) identified several squid beaks in organic sediments

at Ross Island One possible explanation for the lack of

squid remains in our sample could be the lower preserva-

tion of the cephalopod beak compared to fish otoliths

(Emslie and McDaniel 2002) or it is possible that squid did

not contribute to the diet of Adelie penguins in the inves-

tigated period and locations Assuming that Adelie

penguins are still feeding upon the same preys since the

Holocene recent literature reports that squid are preyed

during the summer in East Antarctica and the Weddell Sea

but have not been reported for the Ross Sea (cfr Ainley

2002) In this region two krill species (Euphausia superba

and E crystallorophias) and fish compose the Adelie

penguin diet mixed together in different proportions

(Ainley 2002 Olmastroni et al 2000)

Temporal and spatial variation of prey

Taxonomic identification of fish otoliths indicated P ant-

arcticum as the most eaten prey throughout the investigated

period The abundance of Antarctic silverfish remains

identified in this study agrees with previous paleodietary

investigations in the Antarctica Peninsula East Antarctica

and in the southern Ross Sea region (Emslie and McDaniel

2002 McDaniel and Emslie 2002 Polito et al 2002

Emslie and Woehler 2005) 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 50ndash75 by mass to the Adelie penguin diet even

exceeding crystal krill (E crystallorophias) consumption

in the southern Ross Sea (Ainley 2002 Ainley et al 2003)

Only a very low percentage of remains belongs to other

fish genera The interspecific variation in samples found

exclusively at southern latitudes was probably a conse-

quence of the fact that those samples composed 866 of

the total and contained 96 of the recovered otoliths The

low percentage of occurrence of lsquolsquoother speciesrsquorsquo in our

samples is not surprising Adelie penguins primarily forage

in the continental shelf waters surrounding Antarctica

which are characterized by a very low ichthyic biodiversity

(cfr Ainley 2002) Most unidentifiable fish otoliths

retrieved in the older guano samples maybe related to

sediment transformation processes (such as pedogenesis

and diagenesis) However since many of the best-pre-

served P antarcticum otoliths come from the older guano

samples preservation factors appear here to be related

more to acidic digestion processes rather than to the sample

age or to erosion action through time This is also

supported by the dry and cold condition of Antarctic

environment where the arid climate and low temperatures

slow the damage action of soil processes on organic

remains

Latitude did not significantly affect the mean relative

abundance of Antarctic silverfish indicating that in the past

this species represented an important food source for

penguin breeding throughout the VL coast This prey

species has fluctuated in importance over the past

6000 years (Fig 3) This pattern seems to agree with Hall

et al (2006) who delineated the Adelie penguin and ele-

phant seal occupation history for the VL coast Decreasing

periods of silverfish remains in the present study (Fig 3

1000ndash2000 and 5000ndash6000 BP) correspond approximately

to the seal optimum (1100ndash2300 BP) and to the coeval

occupation (ie contemporary occupation by both species)

(4000ndash6000 BP) reported by Hall et al (2006) Both of

these periods were characterized by a sea ice decrease in

the Ross Sea particularly severe during the most recent

period On the other hand our data show an increase in the

silverfish remains abundance in the past 1000 years and

during the lsquolsquopenguin optimumrsquorsquo this latter being the highest

value among all the investigated periods The lsquolsquopenguin

optimumrsquorsquo and the most recent ages were characterized by

higher sea ice in the Ross Sea region producing a more

fitting habitat for the sea ice obligate Adelie penguin (Hall

et al 2006) The shifts in the presence of fish remains and

in particular of P antarcticum might also represent chan-

ges in Antarctic silverfish population according to the sea

ice advance and retreat (Eastman 1993) Zane et al (2006)

used mitochondrial DNA sequencing to hypothesize that a

demographic expansion that occurred for P antarcticum

during a cooling period (last glaciation peak 111000ndash

126000 BP) suggesting a strong link between this species

(and its prey cfr Smetacek and Nicol 2005) and paleo-

climatic regime shifts

Nevertheless Antarctic silverfish is characterized by a

strong trophic flexibility and adaptability (Eastman 1993

Zane et al 2006) and at present compose the main part of

the diet of marine predators which are also ice-avoiding

species that prefer open water such as elephant seals

(Daneri and Carlini 2002) For this reason we hypothesize

that rather than indicating a decrease in silverfish avail-

ability the shifts in abundance of P antarcticum in the

present study could reflect a higher number of fish remains

in samples as a consequence of a higher number of birds

attending the colonies during periods with more sea ice

Prey size selection

Despite their dense structures fish otoliths are exposed to

variable mechanical and chemical abrasions on calcium

carbonate in the digestive tracts of predators The

Polar Biol

123

susceptibility of fish otoliths (and bones) to digestive ero-

sion appears to change widely taxon by taxon (Harkonen

1986 Pierce et al 1993 Tollit et al 1997) Furthermore in

the ornithogenic soils continuous freezethaw action

through time and sediment transformation processes can

contribute to the consumption and damage of otoliths

These erosive processes act on otolith morphological fea-

tures and size and can lead to non-detection of some prey

categories or of some individuals in a prey category and to

underestimation of prey body size Nevertheless the rela-

tive frequency and size of prey estimated from the hard

remains found in guano samples are valuable and are very

likely the only available information on the kind of prey

consumed

Juvenile P antarcticum with a 40ndash80 mm standard

length range (conforming to juvenile age classes 1 and

2 Hubold and Tomo 1989) are the most-represented

individuals in the VL sediments McDaniel and Emslie

(2002) recognized this prevalence in Northern Marguerite

Bay (Antarctic Peninsula) although with a wider value

range (1582ndash1874 mm) and higher mean SL (10819 plusmn

2553 mm) Juvenile P antarcticum occur primarily at

depths of 50ndash400 m and are well accessible to penguin

capture since their normal foraging depths range between 3

and 98 m (Chappell et al 1993) When analyzing the

temporal distribution of P antarcticum SL significant

differences were not found throughout the investigated

period In Northern Marguerite Bay (Antarctic Peninsula)

(McDaniel and Emslie 2002) some variations within mean

silverfish SL have been recognized among different time

periods but these did not result in a predictable temporal

pattern in accord with past climate change although

Holocene climatic environmental changes are well docu-

mented in both the Antarctic Peninsula and the Ross Sea

region (Bjorck et al 1996 Ingolfsson et al 1998 Baroni

and Orombelli 1991 1994b Baroni and Hall 2004 Hall

et al 2004 2006) The absence of temporal variations of

the silverfish size over the past 7000 years reflects a cer-

tain stability in penguin foraging habits which is also

confirmed by modern diet data on the species predated (crf

Ainley 2002) and on the prey size (Olmastroni et al 2004a

b) No significant temporal variation in prey size was

found The significant difference in silverfish mean size

between the northern and southern colonies was not due to

the amount of older thus more eroded otoliths in the

southern samples In fact the percentage of recent otoliths

for the north and south colonies remains very similar for

the 0ndash1000 period (20 and 1967) and furthermore

northern samples contain higher percentages of older

(period 4000ndash6000) otoliths with respect to the south area

(6713 and 4806 respectively) Therefore although the

difference accounts only for a mean value of 511 mm we

can hypothesize that at least in the past penguins breeding

in colonies located north of the Drygalski ice tongue were

feeding on slightly larger Antarctic silverfish

Sample without fish remains are they evidence

of a dietary shift

Although fish otoliths and bones regularly occur in the

analyzed ornithogenic sediments some guano samples did

not provide any kind of dietary remains Polito et al (2002)

reported the occurrence of feathers in Cape Bird organic

levels without dietary remains which may reflect their

deposition at the time when the area was used by penguin

only to molt and not to nest Stratigraphic and geomor-

phologic features of our samples indicate their nesting site

origin confirmed by the presence of eggshell fragments

collected at the same level suggesting that penguins were

nesting A small number of breeding penguins could be

responsible for the paucity of remains or erosion processes

may have accounted for otolith loss We can also hypoth-

esize that the lack of prey remains could be a shift to a

prevalent non-fish diet Considering in fact that krill is not

maintained in the soils guano samples without fish remains

could reflect a tendency towards a prevalent krill-based

paleodiet At present time Adelie penguin diet switching

between fish and krill may reflect changes in the foraging

setting in relation to environmental and ecological features

Several authors indicated particular climate and marine

conditions (ie sea-ice extension and persistence) as cause

of penguin dietary fluctuation between fish and krill

(Ainley et al 1998 Olmastroni et al 2000 cfr Ainley

2002 Ainley et al 2003) But Ainley et al (2006) in a

more recent study suggested also that feeding competition

among penguins and cetaceans rather than change in

sea-ice cover can better explain the annual switch in the

penguinsrsquo prey items

If the temporal distribution of DR samples versus NDR

ones revealed no significant differences some consider-

ations on their spatial distribution could be made In certain

locations including Inexpressible Island Cape Hickey and

Depot Island NDR guano samples prevail over those

containing fish remains (Table 1) In these cases particular

local marine conditions or other ecological factors as well

as foraging competition with other predators could have

resulted in different krill availability andor consumption

(cfr Ainley et al 2006) Occurring in earlier periods at

Inexpressible Island (5058ndash3900 BP) and later at Cape

Hickey (4075ndash1985 BP) and at Dunlop Island (3100ndash2020

BP) it is not possible to define a common paleoenviron-

mental factor that explains this pattern at the regional scale

At Inexpressible Island for example between 6000 and

4000 BP Adelie penguins shared ice-free coastal terrain

with elephant seals (Hall et al 2006) Thus it is possible

that in this area feeding competition due to this coeval

Polar Biol

123

occupation led penguins to change their diet by targeting

primarily krill which may be eaten only occasionally by

elephant seals (Daneri and Carlini 2002 van den Hoff et al

2003) Even if not revealed by the spatial and temporal

distribution of our samples different sea ice regimes

(Olmastroni et al 2004a b) andor mega icebergs calving

(Arrigo et al 2002) might have had an effect at local scale

These events in fact are known to play an important role on

penguin life cycle and they have been reported to occur in

the past (cfr Shepherd et al 2005)

Although Holocene climatic and environmental changes

have clearly affected the VL coast as indicated by Adelie

penguin colonization history (Baroni and Orombelli

1994a Lambert et al 2002 Emslie et al 2003 Hall et al

2006) over the past 7000 years the Ross Sea ecosystem

seemed to be a relatively stable ecosystem with P ant-

arcticum being the most important fish component in the

Adelie penguin diet for several thousand years The

present study provides the most detailed Adelie penguin

paleodiet records for this area These records may supply

new insights into the past feeding penguin behavior in

the VL coastal area and on a larger scale about the

ecological conditions of the Ross Sea ecosystem during

the Holocene

Acknowledgments This work was executed within the framework

of the Italian National Program on Antarctic Research (PNRA) and

was financially supported by joint research programs in geology at

the University of Pisa The authors thank Fabrizio Ciampolini

(University of Siena) for scanning electron micrographs Silvano

Focardi head of the laboratories at the Department of Environ-

mental Science (University of Siena) where the morphometric

analyses were performed David Lambert Grant Ballard and one

anonymous referee greatly improved an earlier version of the

manuscript

References

Ainley DG (2002) The Adelie penguin bellwether of climate change

Columbia University Press New York

Ainley DG Wilson PR Barton KJ Ballard G Nur N Karl B (1998)

Diet and foraging effort of Adelie penguins in relation to pack-

ice conditions in the southern Ross Sea Polar Biol 20311ndash319

doi101007s003000050308

Ainley DG Ballard G Barton KJ Karl BJ Rau GH Ribic CA

Wilson PR (2003) Spatial and temporal variation of diet within a

presumed metapopulation of Adelie penguins Condor 10595ndash

106 doi1016500010-5422(2003)105[95SATVOD]20CO2

Ainley DG Ballard G Dugger KM (2006) Competition among

penguins and cetaceans reveals trophic cascade in the Western

Ross Sea Antarctica Ecology 872080ndash2093 doi1018900012-

9658(2006)87[2080CAPACR]20CO2

Arrigo KR van Dijken GL Ainley DG Fahnestock MA Markus T

(2002) Ecological impact of a large Antarctic iceberg Geophys

Res Lett 291104 doi1010292001GL014160

Baroni C (1994) Notes on late-glacial retreat of the Antarctic ice sheet

and Holocene environmental changes along the Victoria Land

Coast Mem Natl Inst Polar Res (Jpn) C 5085ndash107

Baroni C Hall BL (2004) A new Holocene relative sea-level curve for

Terra Nova Bay Victoria Land Antarctica J Quat Sci 19377ndash

396 doi101002jqs825

Baroni C Orombelli G (1991) Holocene raised beaches at Terra

Nova Bay Victoria Land Antartica Quat Res 36157ndash177

doi1010160033-5894(91)90023-X

Baroni C Orombelli G (1994a) Abandoned penguin rookeries

as Holocene paleoclimatic indicators in Antarctica Geology

2223ndash26 doi1011300091-7613(1994)0220023APRAHP[23CO2

Baroni C Orombelli G (1994b) Holocene glacier variations in Terra

Nova bay area (Victoria Land Antartica) Antarct Sci 6497ndash

505 doi101017S0954102094000751

Barrett JE Virginia RA Hopkins DW Aislabie J Bargagli R

Bockheim JG Campbell IB Lyons WB Moorhead DL Nkem

JN Sletten RS Steltzer H Wall DH Wallenstein MD (2006)

Terrestrial ecosystem processes of Victoria Land Antarctica

Soil Biol Biochem 383019ndash3034 doi101016jsoilbio2006

04041

Berkman PA Forman SL (1996) Pre-bomb radiocarbon and the

reservoir correction for calcareous marine species in the

Southern Ocean Geophys Res Lett 23363ndash366 doi101029

96GL00151

Bjorck S Hakansson H Olsson S Ellis-Evans C Humlum O Lirio

JM (1996) Late Holocene palaeoclimatic records from lakes

sediments on James Ross Island Antarctica Palaeogeogr

Palaeoclimatol Palaeoecol 113195ndash220 doi1010160031-

0182(95)00086-0

Bochenski Z (1985) Remains of subfossil birds from King George

Island (South Shetland Islands) Acta Zool Cracov 29109ndash116

Chappell MA Shoemaker VH Janes DN Bucher TL Maloney SK

(1993) Diving behavior during foraging in breeding Adelie

penguins Ecol USA 741204ndash1215

Daneri GA Carlini AR (2002) Fish prey of southern elephant seals

Mirounga leonine at King George Island Polar Biol 25739ndash743

Eastman JT (1993) Antarctic fish biology evolution in a unique

environment Academic Press San Diego

Emslie SD (1995) Age and taphonomy of abandoned penguin

rookeries in the Antarctic Peninsula region Polar Rec (Gr Brit)

31409ndash418

Emslie SD (2001) Radiocarbon dates from abandoned penguin

colonies in the Antarctica peninsula region Antarct Sci

13289ndash295 doi101017S0954102001000414

Emslie SD McDaniel JD (2002) Adelie penguin diet and climate

change during the middle to late Holocene in northern Margue-

rite Bay Antarctic Peninsula Polar Biol 25222ndash229

Emslie SD Patterson WP (2007) Abrupt shift in d13C and d15N

values in Adelie penguin eggshell in Antarctica Proc Natl Acad

Sci USA 10411666ndash11669 doi101073pnas0608477104

Emslie SD Woehler EJ (2005) A 9000-year record of Adelie penguin

occupation and diet in the Windmill Islands East Antarctica

Antarct Sci 1757ndash66 doi101017S0954102005002427

Emslie SD Fraser W Smith RC Walker W (1998) Abandoned

penguin colonies and environmental change in the Palmer

Station area Anvers Island Antarctic Peninsula Antarct Sci

10257ndash268 doi101017S0954102098000352

Emslie SD Berkman PA Ainley DG Coats L Polito M (2003) Late-

Holocene initiation of ice-free ecosystems in the southern Ross

Sea Antarctica Mar Ecol Prog Ser 26219ndash25 doi103354

meps262019

Emslie SD Coats L Licht K (2007) A 45000 year record of Adelie

penguins and climate change in the Ross Sea Antarctica

Geology 3561ndash64 doi101130G23011A1

Hall BL Baroni C Denton GH (2004) Holocene relative sea-level

history of the Southern Victoria Land Coast Antarctica Glob

Planet Chang 42241ndash263 doi101016jgloplacha200309004

Polar Biol

123

Materials and methods

Study area and geomorphological setting

Extending southward from about 71180S (Cape Adare) to

78000S (McMurdo Sound) the Victoria Land (hereafter

reported as VL) coast borders the western side of the Ross

Sea (Fig 1)

Aerial photograph analysis several field surveys

detailed geomorphologic analyses of key sites and

ornithogenic soil sampling were conducted in previous

studies in ice-free areas along the VL coast (Baroni and

Orombelli 1991 1994a Baroni and Hall 2004 Hall et al

2004) (Fig 1) Adelie penguin-abandoned nesting sites

represent a common landscape feature of the ice-free VL

coast They occur both at the outskirts of present-day

colonies and in areas no longer occupied by penguins

(Fig 1) Resting on Holocene raised beaches marine ter-

races debris cones and slopes piedmont rock-glaciers and

ice-cored and depositional moraines abandoned Adelie

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 Adelie penguins do not nest

Conservative excavation technique and sample

collection

After identifying abandoned penguin settlements we

established test pits generally 1ndash6 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

sampling setting with regard to the number of retrievable

guano samples

Laboratory analyses

Ninety-seven 14C previously dated penguin guano samples

were processed in the laboratory to recover penguin dietary

remains Previously published papers (cfr Baroni 1994

Baroni and Orombelli 1991 1994a Lambert et al 2002

Baroni and Hall 2004 Hall et al 2004) provided samples

used in this study spanning up to 7200 BP corrected ages

All conventional dates (in 14C BP) were in fact corrected for

the upwelling of old water in the Southern Ocean by sub-

tracting a marine-carbon reservoir effect of 1300 years

(Berkman and Forman 1996) and thereafter all the values

reported in the present study were marine effect removed

At the moment this value represents the best estimate and

conventional value used for the Ross Sea region based on

dates of lsquolsquopre-bombrsquorsquo organisms (ie before 1950) of

known ages (Berkman and Forman 1996) Although cali-

brating the dates would be preferable this approach

allowed us to compare the dates from the penguin remains

with sets of dates supplied by other organisms (ie ele-

phant seals Hall et al 2006) and with other proxy data

such as ice-core datasets (Lorius et al 1985 Petit et al

1997)

Fig 1 Map of the Victoria Land coast showing the geographic

distribution of study sites Ornithogenic soils were sampled at the

margin of presently occupied Adelie penguin colonies (solid circles)

as well as in areas no longer occupied by penguins (relict colonies)

(stars)

Polar Biol

123

Sediments were washed (distilled water) and sieved

through seven nested screens with square mesh sizes

ranging from 2 mm to 63 lm The matrix from each screen

was dried and subsequently sorted under a low-power

(5ndash10x) stereomicroscope to separate eggshell fragments

feathers and dietary remains (otoliths fish vertebrae and

teeth) (Fig 2)

Samples were classified according to the presence

absence of dietary remains and are hereafter reported as

sample with lsquolsquodietary remainsrsquorsquo (DR) or samples with lsquolsquono

dietary remainsrsquorsquo (NDR) respectively Otoliths were sep-

arated from fish bones in order to carry out taxonomic

identification They were identified using anatomic-com-

parative tables proposed by Williams and McEldowney

(1990) for Antarctic fish taxa These prey remains are

quantified by the minimum number of individuals (MNI)

represented for each identified fish taxon According to

Emslie et al (1998) the MNI is determined by counting the

number of whole otoliths of known side (right or left) and

using the greater value of the two sides In addition oto-

liths of unknown side were counted and their number was

halved to give a conservative estimate of the total number

of right and left sides represented which was then added to

the MNI obtained from known-side otoliths to yield a total

MNI for each species

Otoliths were measured using a stereomicroscope with a

micrometric eye piece (10x) to an accuracy of 01 mm The

maximum distances between the rostrum and the posterior

margin (otolith length OL) and between the dorsal and

ventral margins (otolith width OW) were measured By

using given regression formulae morphometric analysis of

the otoliths provides a mean estimate of prey item size

(Williams and McEldowney 1990) Since very few other

fish taxa remains were found only P antarcticum otoliths

were considered The corresponding standard length (SL)

in millimeters was determined according to the regression

equations calculated by Williams and McEldowney (1990)

Fish otoliths show clear erosion signals ranging from 2

to 4 according to Leopold et al (1998) but most of them

still preserve the morphological parameters required for

taxon identification Not all recovered fish otoliths were

suitable for the morphometric analysis because some were

strongly eroded or broken Especially for the smallest

otoliths (B250 lm) the smoothed borders made it impos-

sible to orient the otolith correctly and to distinguish the

dorsal and ventral margins from the anterior and posterior

ones To avoid any estimation bias we selected and mea-

sured only those otoliths with well recognizable

morphometric parameters To avoid bias due to variable

amounts of sorted sediments we express the relative den-

sity as the ratio of MNIdry mass by dividing the MNI

value by the total mass (in gram) for each guano sample

Statistical analysis

In order to evaluate the possible factors affecting the

presence of fish remains in the ornithogenic samples we

built three logistic models (Tabachnick and Fidell 1996)

using as binary-dependent variable the presenceabsence

of (a) dietary remains (b) P antarcticum (c) other iden-

tified species and as independent variables the latitude and

the age of the samples In model (b) and (c) samples

containing only unidentified fish bones (n = 18) were

excluded from these analyses Fish taxa different from

silverfish were very low in number and thus were grouped

into a unique category named lsquolsquoother fishrsquorsquo

Differences in the standard length of silverfish with

respect to latitude were analyzed with the MannndashWhitney

non-parametric test All tests were two-tailed and the sta-

tistical significance was set to a = 005 For this analysis

samples were grouped by dividing the Ross Sea into two

main regions the north and the south with respect to the

Drygalski ice tongue which extend from Cape Adare to

Inexpressible Is (North N) and from Cape Irizar to Dunlop

Is (South S) All the analyses were performed using the

software SPSS 120 All mean are given as plusmn1 SD

Results

Matrix screening and sorting allowed us to recover a large

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 sidePleuragramma antarcticumotolith b fish vertebra c fish

tooth d penguin eggshell

fragment

Polar Biol

123

penguin bones feathers eggshell fragments and hard parts

of dietary remains such as fish bones (vertebrae) scales

and otoliths Since krill and their fragile carapaces are not

preserved in sediments the ornithogenic soils investigation

provided data only about the non-euphausiid (ie fish)

paleodietary components The thickness of ornithogenic

soils ranged from centimeters to decimeters and the mean

mass of the samples was 186 g (range 6ndash885 g) Among a

total of 97 samples 32 did not contain dietary remains

(NDR) and 18 contained only fish vertebrae (Table 1) In

NDR samples neither fish bones nor otoliths were recov-

ered but eggshell fragments and feathers testified to the

ornithogenic nature of those samples and confirmed the

presence of nesting sites

Among the 16 visited localities Cape Irizar Prior

Island Cape Ross and Cape Day were the most productive

in terms of the number of fish otoliths Samples from

Gondwana station samples were the richest in fish bones

but no otoliths were found At Inexpressible Island Cape

Hickey and Depot Island there was a clear prevalence of

NDR compared to the DR samples (Table 1)

Otoliths were found in 47 samples and were analyzed

to identify prey taxa A total of 677 otoliths correspond-

ing to 409 individuals (87 plusmn 1258 preys per sample)

belonging to four taxa were identified (Table 2) Taxo-

nomic identification indicated that all penguins fish prey

belonged to the family Nototheniidae and consisted

mainly of P antarcticum (9010 of MNI) followed

by Pagothenia sp (340 of MNI) and Trematomus sp

(148 of MNI) Among the individuals of the genus

Trematomus six were recognized as Trematomus ber-

nacchii The rest of the recovered otoliths (502) too

eroded to estimate side and size are taxonomically

uncertain but among the family Nototheniidae

Comparison among dietary items latitude and age

Results from model (a) showed that neither latitude nor age

had an effect on the presenceabsence of fish remains in all

the ornithogenic samples (n = 97) (Table 3) On the con-

trary the model (b) revealed that the age of the samples

significantly explained the presence of P antarcticum

while the latitude did not appear to have any explanatory

effect (Table 3) The model (b) correctly reclassified

804 of the samples with P antarcticum and 62 of the

Table 1 Number of dietary remains recovered in ornithogenic soil samples discovered in Victoria Land

Collection site Latitude No of guano

samples (NDR)

Radiocarbon

date range (BP)

Total mass

(g)

No of recovered

fish otolith

No of recovered

fish bones

Cape Adare 71180S 1 1180 38 1 1

Duke of York 71370S 1 920 121 ndash 11

Cape Hallett 72190S 4(1) 320ndash400 3155 11 4

Edmonson point 74200S 5(1) 770ndash990 801 12 13

Gondwana station 74380S 2 3330ndash3370 280 ndash 112

Terra Nova station 74420S 9(1) 3580ndash5180 1716 50 178

Icarus Camp 74430S 21(9) 2780ndash6060 4389 47 29

N Adelie Cove 74460S 7(2) 4525ndash7190 1490 8 17

Inexpressible Island 74530S 9(5) 1220ndash5058 2078 9 6

Cape Irizar 75340S 7 860ndash4010 1830 299 1

Prior Island 75410S 6(1) 2980ndash4525 834 118 3

Cape Hickey 76050S 10(7) 1985ndash6240 16274 29 2

N Cape Day 76150S 1 3060 226 41 ndash

Depot Island 76420S 5(4) 2020ndash5840 766 10 1

Cape Ross 76440S 5(1) 2835ndash3015 7535 36 27

Dunlop Island 77140S 4 2230ndash4330 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

Table 2 Fish taxa identified from otoliths recovered from ornitho-

genic soils sampled at Adelie penguin colonies along the Victoria

Land coast Ross Sea Antarctica

Taxon Number of otoliths () MNI ()

Pleuragramma antarcticum 610 (9010) 355 (9126)

Trematomus sp 10 (148) 10 (257)

Pagothenia sp 23 (340) 17 (437)

Unidentified Nototheniidae 34 (502) 27 (694)

Total 677 409

The total numbers of identifiable otoliths and MNI are provided for

each taxon percentages are reported in parentheses

Polar Biol

123

all samples In fact the age distribution of the samples

confirms that fish remains increased in samples dated

between 2000 and 4000 BP a period that includes the time

lag defined as the lsquolsquopenguin optimumrsquorsquo by Hall et al (2006)

(Fig 3)

Fish species different from P antarcticum composed a

very small percentage of the organic material sorted in the

ornithogenic sediment Species other than silverfish

occurred only at southern latitudes between 74420 and

77140S When included in the logistical model (c) the

presenceabsence of other fishes was significantly

explained by the latitude alone (Table 3) and the model

correctly reclassified 797 of the samples

Prey size classes in ornithogenic soils

A morphometric analysis of 380 Antarctic silverfish

otoliths showed that the mean silverfish SL was

6723 plusmn 2347 mm (range 4018ndash18267) Furthermore

our data indicate that 8289 of the silverfish eaten by

Adelie penguins belonged to the 40ndash80 mm length class

(Fig 4)

There was no significant difference in the distribution of

the size classes of P antarcticum according to age of the

samples Grouping colonies according to a north to south

gradient samples from the northern colonies (n = 70 mean

7139 plusmn 23007 mm) contained longer Antarctic silverfish

compared to the southern colonies (n = 310 mean

66285 plusmn 23508 mm) this difference appears to be sig-

nificant (U MannndashWhitney = 782850 Z = -3521

P = 0000)

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 74420 and

77140S (866) The abundance in guano samplersquos

availability during this period may be a consequence of the

great spread of Adelie penguin colonies recorded for the

VL between 2300 and 4000 BP and indicated as the lsquolsquopen-

guin optimumrsquorsquo (cfr Baroni and Orombelli 1994a Hall

et al 2006)

Table 3 Logistic models testing the effect of latitude and age on the

presenceabsence in the ornithogenic samples of models a b c

Variable B Wald statistic df P

Model a) Latitude -0840 0140 1 0709

Age of samples 0000 2701 1 0100

Constant 7914 0223 1 0637

Model b) Latitude 0032 0017 1 0896

Age of samples 0000 5463 1 0019

Constant -0651 0001 1 0972

Model c) Latitude 0653 3757 1 0050

Age of samples 0000 0010 1 0921

Constant -50665 3955 1 0047

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-uragramma antarcticum) (n = 79 16 with other species and 63

without)

Significant effects are indicated

Fig 3 Samples with fish remains (DR) (n = 65 black bars) and

samples with P antarcticum (n = 46 light bars) grouped for each

1000 years (from 320 to 7200 BP) NDR samples of the period are

reported in parentheses The time periods of occupational history for

Victoria Land as described by Hall et al (2006) are reported in the

background

Pleuragramma antarcticum

0

5

10

15

20

25

30

0 10 20 30 40 50 60 70 80 90 100 110 120 130 140 150 160 170 180

SL classes (mm)

Fre

qu

ency

of

occ

urr

ence

(

)

Fig 4 Antarctic silverfish size class distribution in ornithogenic

samples For each class the lower limit (mm) is reported

Polar Biol

123

Except for fish otoliths and bones no other dietary

remains were recovered in this study although Polito et al

(2002) identified several squid beaks in organic sediments

at Ross Island One possible explanation for the lack of

squid remains in our sample could be the lower preserva-

tion of the cephalopod beak compared to fish otoliths

(Emslie and McDaniel 2002) or it is possible that squid did

not contribute to the diet of Adelie penguins in the inves-

tigated period and locations Assuming that Adelie

penguins are still feeding upon the same preys since the

Holocene recent literature reports that squid are preyed

during the summer in East Antarctica and the Weddell Sea

but have not been reported for the Ross Sea (cfr Ainley

2002) In this region two krill species (Euphausia superba

and E crystallorophias) and fish compose the Adelie

penguin diet mixed together in different proportions

(Ainley 2002 Olmastroni et al 2000)

Temporal and spatial variation of prey

Taxonomic identification of fish otoliths indicated P ant-

arcticum as the most eaten prey throughout the investigated

period The abundance of Antarctic silverfish remains

identified in this study agrees with previous paleodietary

investigations in the Antarctica Peninsula East Antarctica

and in the southern Ross Sea region (Emslie and McDaniel

2002 McDaniel and Emslie 2002 Polito et al 2002

Emslie and Woehler 2005) 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 50ndash75 by mass to the Adelie penguin diet even

exceeding crystal krill (E crystallorophias) consumption

in the southern Ross Sea (Ainley 2002 Ainley et al 2003)

Only a very low percentage of remains belongs to other

fish genera The interspecific variation in samples found

exclusively at southern latitudes was probably a conse-

quence of the fact that those samples composed 866 of

the total and contained 96 of the recovered otoliths The

low percentage of occurrence of lsquolsquoother speciesrsquorsquo in our

samples is not surprising Adelie penguins primarily forage

in the continental shelf waters surrounding Antarctica

which are characterized by a very low ichthyic biodiversity

(cfr Ainley 2002) Most unidentifiable fish otoliths

retrieved in the older guano samples maybe related to

sediment transformation processes (such as pedogenesis

and diagenesis) However since many of the best-pre-

served P antarcticum otoliths come from the older guano

samples preservation factors appear here to be related

more to acidic digestion processes rather than to the sample

age or to erosion action through time This is also

supported by the dry and cold condition of Antarctic

environment where the arid climate and low temperatures

slow the damage action of soil processes on organic

remains

Latitude did not significantly affect the mean relative

abundance of Antarctic silverfish indicating that in the past

this species represented an important food source for

penguin breeding throughout the VL coast This prey

species has fluctuated in importance over the past

6000 years (Fig 3) This pattern seems to agree with Hall

et al (2006) who delineated the Adelie penguin and ele-

phant seal occupation history for the VL coast Decreasing

periods of silverfish remains in the present study (Fig 3

1000ndash2000 and 5000ndash6000 BP) correspond approximately

to the seal optimum (1100ndash2300 BP) and to the coeval

occupation (ie contemporary occupation by both species)

(4000ndash6000 BP) reported by Hall et al (2006) Both of

these periods were characterized by a sea ice decrease in

the Ross Sea particularly severe during the most recent

period On the other hand our data show an increase in the

silverfish remains abundance in the past 1000 years and

during the lsquolsquopenguin optimumrsquorsquo this latter being the highest

value among all the investigated periods The lsquolsquopenguin

optimumrsquorsquo and the most recent ages were characterized by

higher sea ice in the Ross Sea region producing a more

fitting habitat for the sea ice obligate Adelie penguin (Hall

et al 2006) The shifts in the presence of fish remains and

in particular of P antarcticum might also represent chan-

ges in Antarctic silverfish population according to the sea

ice advance and retreat (Eastman 1993) Zane et al (2006)

used mitochondrial DNA sequencing to hypothesize that a

demographic expansion that occurred for P antarcticum

during a cooling period (last glaciation peak 111000ndash

126000 BP) suggesting a strong link between this species

(and its prey cfr Smetacek and Nicol 2005) and paleo-

climatic regime shifts

Nevertheless Antarctic silverfish is characterized by a

strong trophic flexibility and adaptability (Eastman 1993

Zane et al 2006) and at present compose the main part of

the diet of marine predators which are also ice-avoiding

species that prefer open water such as elephant seals

(Daneri and Carlini 2002) For this reason we hypothesize

that rather than indicating a decrease in silverfish avail-

ability the shifts in abundance of P antarcticum in the

present study could reflect a higher number of fish remains

in samples as a consequence of a higher number of birds

attending the colonies during periods with more sea ice

Prey size selection

Despite their dense structures fish otoliths are exposed to

variable mechanical and chemical abrasions on calcium

carbonate in the digestive tracts of predators The

Polar Biol

123

susceptibility of fish otoliths (and bones) to digestive ero-

sion appears to change widely taxon by taxon (Harkonen

1986 Pierce et al 1993 Tollit et al 1997) Furthermore in

the ornithogenic soils continuous freezethaw action

through time and sediment transformation processes can

contribute to the consumption and damage of otoliths

These erosive processes act on otolith morphological fea-

tures and size and can lead to non-detection of some prey

categories or of some individuals in a prey category and to

underestimation of prey body size Nevertheless the rela-

tive frequency and size of prey estimated from the hard

remains found in guano samples are valuable and are very

likely the only available information on the kind of prey

consumed

Juvenile P antarcticum with a 40ndash80 mm standard

length range (conforming to juvenile age classes 1 and

2 Hubold and Tomo 1989) are the most-represented

individuals in the VL sediments McDaniel and Emslie

(2002) recognized this prevalence in Northern Marguerite

Bay (Antarctic Peninsula) although with a wider value

range (1582ndash1874 mm) and higher mean SL (10819 plusmn

2553 mm) Juvenile P antarcticum occur primarily at

depths of 50ndash400 m and are well accessible to penguin

capture since their normal foraging depths range between 3

and 98 m (Chappell et al 1993) When analyzing the

temporal distribution of P antarcticum SL significant

differences were not found throughout the investigated

period In Northern Marguerite Bay (Antarctic Peninsula)

(McDaniel and Emslie 2002) some variations within mean

silverfish SL have been recognized among different time

periods but these did not result in a predictable temporal

pattern in accord with past climate change although

Holocene climatic environmental changes are well docu-

mented in both the Antarctic Peninsula and the Ross Sea

region (Bjorck et al 1996 Ingolfsson et al 1998 Baroni

and Orombelli 1991 1994b Baroni and Hall 2004 Hall

et al 2004 2006) The absence of temporal variations of

the silverfish size over the past 7000 years reflects a cer-

tain stability in penguin foraging habits which is also

confirmed by modern diet data on the species predated (crf

Ainley 2002) and on the prey size (Olmastroni et al 2004a

b) No significant temporal variation in prey size was

found The significant difference in silverfish mean size

between the northern and southern colonies was not due to

the amount of older thus more eroded otoliths in the

southern samples In fact the percentage of recent otoliths

for the north and south colonies remains very similar for

the 0ndash1000 period (20 and 1967) and furthermore

northern samples contain higher percentages of older

(period 4000ndash6000) otoliths with respect to the south area

(6713 and 4806 respectively) Therefore although the

difference accounts only for a mean value of 511 mm we

can hypothesize that at least in the past penguins breeding

in colonies located north of the Drygalski ice tongue were

feeding on slightly larger Antarctic silverfish

Sample without fish remains are they evidence

of a dietary shift

Although fish otoliths and bones regularly occur in the

analyzed ornithogenic sediments some guano samples did

not provide any kind of dietary remains Polito et al (2002)

reported the occurrence of feathers in Cape Bird organic

levels without dietary remains which may reflect their

deposition at the time when the area was used by penguin

only to molt and not to nest Stratigraphic and geomor-

phologic features of our samples indicate their nesting site

origin confirmed by the presence of eggshell fragments

collected at the same level suggesting that penguins were

nesting A small number of breeding penguins could be

responsible for the paucity of remains or erosion processes

may have accounted for otolith loss We can also hypoth-

esize that the lack of prey remains could be a shift to a

prevalent non-fish diet Considering in fact that krill is not

maintained in the soils guano samples without fish remains

could reflect a tendency towards a prevalent krill-based

paleodiet At present time Adelie penguin diet switching

between fish and krill may reflect changes in the foraging

setting in relation to environmental and ecological features

Several authors indicated particular climate and marine

conditions (ie sea-ice extension and persistence) as cause

of penguin dietary fluctuation between fish and krill

(Ainley et al 1998 Olmastroni et al 2000 cfr Ainley

2002 Ainley et al 2003) But Ainley et al (2006) in a

more recent study suggested also that feeding competition

among penguins and cetaceans rather than change in

sea-ice cover can better explain the annual switch in the

penguinsrsquo prey items

If the temporal distribution of DR samples versus NDR

ones revealed no significant differences some consider-

ations on their spatial distribution could be made In certain

locations including Inexpressible Island Cape Hickey and

Depot Island NDR guano samples prevail over those

containing fish remains (Table 1) In these cases particular

local marine conditions or other ecological factors as well

as foraging competition with other predators could have

resulted in different krill availability andor consumption

(cfr Ainley et al 2006) Occurring in earlier periods at

Inexpressible Island (5058ndash3900 BP) and later at Cape

Hickey (4075ndash1985 BP) and at Dunlop Island (3100ndash2020

BP) it is not possible to define a common paleoenviron-

mental factor that explains this pattern at the regional scale

At Inexpressible Island for example between 6000 and

4000 BP Adelie penguins shared ice-free coastal terrain

with elephant seals (Hall et al 2006) Thus it is possible

that in this area feeding competition due to this coeval

Polar Biol

123

occupation led penguins to change their diet by targeting

primarily krill which may be eaten only occasionally by

elephant seals (Daneri and Carlini 2002 van den Hoff et al

2003) Even if not revealed by the spatial and temporal

distribution of our samples different sea ice regimes

(Olmastroni et al 2004a b) andor mega icebergs calving

(Arrigo et al 2002) might have had an effect at local scale

These events in fact are known to play an important role on

penguin life cycle and they have been reported to occur in

the past (cfr Shepherd et al 2005)

Although Holocene climatic and environmental changes

have clearly affected the VL coast as indicated by Adelie

penguin colonization history (Baroni and Orombelli

1994a Lambert et al 2002 Emslie et al 2003 Hall et al

2006) over the past 7000 years the Ross Sea ecosystem

seemed to be a relatively stable ecosystem with P ant-

arcticum being the most important fish component in the

Adelie penguin diet for several thousand years The

present study provides the most detailed Adelie penguin

paleodiet records for this area These records may supply

new insights into the past feeding penguin behavior in

the VL coastal area and on a larger scale about the

ecological conditions of the Ross Sea ecosystem during

the Holocene

Acknowledgments This work was executed within the framework

of the Italian National Program on Antarctic Research (PNRA) and

was financially supported by joint research programs in geology at

the University of Pisa The authors thank Fabrizio Ciampolini

(University of Siena) for scanning electron micrographs Silvano

Focardi head of the laboratories at the Department of Environ-

mental Science (University of Siena) where the morphometric

analyses were performed David Lambert Grant Ballard and one

anonymous referee greatly improved an earlier version of the

manuscript

References

Ainley DG (2002) The Adelie penguin bellwether of climate change

Columbia University Press New York

Ainley DG Wilson PR Barton KJ Ballard G Nur N Karl B (1998)

Diet and foraging effort of Adelie penguins in relation to pack-

ice conditions in the southern Ross Sea Polar Biol 20311ndash319

doi101007s003000050308

Ainley DG Ballard G Barton KJ Karl BJ Rau GH Ribic CA

Wilson PR (2003) Spatial and temporal variation of diet within a

presumed metapopulation of Adelie penguins Condor 10595ndash

106 doi1016500010-5422(2003)105[95SATVOD]20CO2

Ainley DG Ballard G Dugger KM (2006) Competition among

penguins and cetaceans reveals trophic cascade in the Western

Ross Sea Antarctica Ecology 872080ndash2093 doi1018900012-

9658(2006)87[2080CAPACR]20CO2

Arrigo KR van Dijken GL Ainley DG Fahnestock MA Markus T

(2002) Ecological impact of a large Antarctic iceberg Geophys

Res Lett 291104 doi1010292001GL014160

Baroni C (1994) Notes on late-glacial retreat of the Antarctic ice sheet

and Holocene environmental changes along the Victoria Land

Coast Mem Natl Inst Polar Res (Jpn) C 5085ndash107

Baroni C Hall BL (2004) A new Holocene relative sea-level curve for

Terra Nova Bay Victoria Land Antarctica J Quat Sci 19377ndash

396 doi101002jqs825

Baroni C Orombelli G (1991) Holocene raised beaches at Terra

Nova Bay Victoria Land Antartica Quat Res 36157ndash177

doi1010160033-5894(91)90023-X

Baroni C Orombelli G (1994a) Abandoned penguin rookeries

as Holocene paleoclimatic indicators in Antarctica Geology

2223ndash26 doi1011300091-7613(1994)0220023APRAHP[23CO2

Baroni C Orombelli G (1994b) Holocene glacier variations in Terra

Nova bay area (Victoria Land Antartica) Antarct Sci 6497ndash

505 doi101017S0954102094000751

Barrett JE Virginia RA Hopkins DW Aislabie J Bargagli R

Bockheim JG Campbell IB Lyons WB Moorhead DL Nkem

JN Sletten RS Steltzer H Wall DH Wallenstein MD (2006)

Terrestrial ecosystem processes of Victoria Land Antarctica

Soil Biol Biochem 383019ndash3034 doi101016jsoilbio2006

04041

Berkman PA Forman SL (1996) Pre-bomb radiocarbon and the

reservoir correction for calcareous marine species in the

Southern Ocean Geophys Res Lett 23363ndash366 doi101029

96GL00151

Bjorck S Hakansson H Olsson S Ellis-Evans C Humlum O Lirio

JM (1996) Late Holocene palaeoclimatic records from lakes

sediments on James Ross Island Antarctica Palaeogeogr

Palaeoclimatol Palaeoecol 113195ndash220 doi1010160031-

0182(95)00086-0

Bochenski Z (1985) Remains of subfossil birds from King George

Island (South Shetland Islands) Acta Zool Cracov 29109ndash116

Chappell MA Shoemaker VH Janes DN Bucher TL Maloney SK

(1993) Diving behavior during foraging in breeding Adelie

penguins Ecol USA 741204ndash1215

Daneri GA Carlini AR (2002) Fish prey of southern elephant seals

Mirounga leonine at King George Island Polar Biol 25739ndash743

Eastman JT (1993) Antarctic fish biology evolution in a unique

environment Academic Press San Diego

Emslie SD (1995) Age and taphonomy of abandoned penguin

rookeries in the Antarctic Peninsula region Polar Rec (Gr Brit)

31409ndash418

Emslie SD (2001) Radiocarbon dates from abandoned penguin

colonies in the Antarctica peninsula region Antarct Sci

13289ndash295 doi101017S0954102001000414

Emslie SD McDaniel JD (2002) Adelie penguin diet and climate

change during the middle to late Holocene in northern Margue-

rite Bay Antarctic Peninsula Polar Biol 25222ndash229

Emslie SD Patterson WP (2007) Abrupt shift in d13C and d15N

values in Adelie penguin eggshell in Antarctica Proc Natl Acad

Sci USA 10411666ndash11669 doi101073pnas0608477104

Emslie SD Woehler EJ (2005) A 9000-year record of Adelie penguin

occupation and diet in the Windmill Islands East Antarctica

Antarct Sci 1757ndash66 doi101017S0954102005002427

Emslie SD Fraser W Smith RC Walker W (1998) Abandoned

penguin colonies and environmental change in the Palmer

Station area Anvers Island Antarctic Peninsula Antarct Sci

10257ndash268 doi101017S0954102098000352

Emslie SD Berkman PA Ainley DG Coats L Polito M (2003) Late-

Holocene initiation of ice-free ecosystems in the southern Ross

Sea Antarctica Mar Ecol Prog Ser 26219ndash25 doi103354

meps262019

Emslie SD Coats L Licht K (2007) A 45000 year record of Adelie

penguins and climate change in the Ross Sea Antarctica

Geology 3561ndash64 doi101130G23011A1

Hall BL Baroni C Denton GH (2004) Holocene relative sea-level

history of the Southern Victoria Land Coast Antarctica Glob

Planet Chang 42241ndash263 doi101016jgloplacha200309004

Polar Biol

123

Sediments were washed (distilled water) and sieved

through seven nested screens with square mesh sizes

ranging from 2 mm to 63 lm The matrix from each screen

was dried and subsequently sorted under a low-power

(5ndash10x) stereomicroscope to separate eggshell fragments

feathers and dietary remains (otoliths fish vertebrae and

teeth) (Fig 2)

Samples were classified according to the presence

absence of dietary remains and are hereafter reported as

sample with lsquolsquodietary remainsrsquorsquo (DR) or samples with lsquolsquono

dietary remainsrsquorsquo (NDR) respectively Otoliths were sep-

arated from fish bones in order to carry out taxonomic

identification They were identified using anatomic-com-

parative tables proposed by Williams and McEldowney

(1990) for Antarctic fish taxa These prey remains are

quantified by the minimum number of individuals (MNI)

represented for each identified fish taxon According to

Emslie et al (1998) the MNI is determined by counting the

number of whole otoliths of known side (right or left) and

using the greater value of the two sides In addition oto-

liths of unknown side were counted and their number was

halved to give a conservative estimate of the total number

of right and left sides represented which was then added to

the MNI obtained from known-side otoliths to yield a total

MNI for each species

Otoliths were measured using a stereomicroscope with a

micrometric eye piece (10x) to an accuracy of 01 mm The

maximum distances between the rostrum and the posterior

margin (otolith length OL) and between the dorsal and

ventral margins (otolith width OW) were measured By

using given regression formulae morphometric analysis of

the otoliths provides a mean estimate of prey item size

(Williams and McEldowney 1990) Since very few other

fish taxa remains were found only P antarcticum otoliths

were considered The corresponding standard length (SL)

in millimeters was determined according to the regression

equations calculated by Williams and McEldowney (1990)

Fish otoliths show clear erosion signals ranging from 2

to 4 according to Leopold et al (1998) but most of them

still preserve the morphological parameters required for

taxon identification Not all recovered fish otoliths were

suitable for the morphometric analysis because some were

strongly eroded or broken Especially for the smallest

otoliths (B250 lm) the smoothed borders made it impos-

sible to orient the otolith correctly and to distinguish the

dorsal and ventral margins from the anterior and posterior

ones To avoid any estimation bias we selected and mea-

sured only those otoliths with well recognizable

morphometric parameters To avoid bias due to variable

amounts of sorted sediments we express the relative den-

sity as the ratio of MNIdry mass by dividing the MNI

value by the total mass (in gram) for each guano sample

Statistical analysis

In order to evaluate the possible factors affecting the

presence of fish remains in the ornithogenic samples we

built three logistic models (Tabachnick and Fidell 1996)

using as binary-dependent variable the presenceabsence

of (a) dietary remains (b) P antarcticum (c) other iden-

tified species and as independent variables the latitude and

the age of the samples In model (b) and (c) samples

containing only unidentified fish bones (n = 18) were

excluded from these analyses Fish taxa different from

silverfish were very low in number and thus were grouped

into a unique category named lsquolsquoother fishrsquorsquo

Differences in the standard length of silverfish with

respect to latitude were analyzed with the MannndashWhitney

non-parametric test All tests were two-tailed and the sta-

tistical significance was set to a = 005 For this analysis

samples were grouped by dividing the Ross Sea into two

main regions the north and the south with respect to the

Drygalski ice tongue which extend from Cape Adare to

Inexpressible Is (North N) and from Cape Irizar to Dunlop

Is (South S) All the analyses were performed using the

software SPSS 120 All mean are given as plusmn1 SD

Results

Matrix screening and sorting allowed us to recover a large

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 sidePleuragramma antarcticumotolith b fish vertebra c fish

tooth d penguin eggshell

fragment

Polar Biol

123

penguin bones feathers eggshell fragments and hard parts

of dietary remains such as fish bones (vertebrae) scales

and otoliths Since krill and their fragile carapaces are not

preserved in sediments the ornithogenic soils investigation

provided data only about the non-euphausiid (ie fish)

paleodietary components The thickness of ornithogenic

soils ranged from centimeters to decimeters and the mean

mass of the samples was 186 g (range 6ndash885 g) Among a

total of 97 samples 32 did not contain dietary remains

(NDR) and 18 contained only fish vertebrae (Table 1) In

NDR samples neither fish bones nor otoliths were recov-

ered but eggshell fragments and feathers testified to the

ornithogenic nature of those samples and confirmed the

presence of nesting sites

Among the 16 visited localities Cape Irizar Prior

Island Cape Ross and Cape Day were the most productive

in terms of the number of fish otoliths Samples from

Gondwana station samples were the richest in fish bones

but no otoliths were found At Inexpressible Island Cape

Hickey and Depot Island there was a clear prevalence of

NDR compared to the DR samples (Table 1)

Otoliths were found in 47 samples and were analyzed

to identify prey taxa A total of 677 otoliths correspond-

ing to 409 individuals (87 plusmn 1258 preys per sample)

belonging to four taxa were identified (Table 2) Taxo-

nomic identification indicated that all penguins fish prey

belonged to the family Nototheniidae and consisted

mainly of P antarcticum (9010 of MNI) followed

by Pagothenia sp (340 of MNI) and Trematomus sp

(148 of MNI) Among the individuals of the genus

Trematomus six were recognized as Trematomus ber-

nacchii The rest of the recovered otoliths (502) too

eroded to estimate side and size are taxonomically

uncertain but among the family Nototheniidae

Comparison among dietary items latitude and age

Results from model (a) showed that neither latitude nor age

had an effect on the presenceabsence of fish remains in all

the ornithogenic samples (n = 97) (Table 3) On the con-

trary the model (b) revealed that the age of the samples

significantly explained the presence of P antarcticum

while the latitude did not appear to have any explanatory

effect (Table 3) The model (b) correctly reclassified

804 of the samples with P antarcticum and 62 of the

Table 1 Number of dietary remains recovered in ornithogenic soil samples discovered in Victoria Land

Collection site Latitude No of guano

samples (NDR)

Radiocarbon

date range (BP)

Total mass

(g)

No of recovered

fish otolith

No of recovered

fish bones

Cape Adare 71180S 1 1180 38 1 1

Duke of York 71370S 1 920 121 ndash 11

Cape Hallett 72190S 4(1) 320ndash400 3155 11 4

Edmonson point 74200S 5(1) 770ndash990 801 12 13

Gondwana station 74380S 2 3330ndash3370 280 ndash 112

Terra Nova station 74420S 9(1) 3580ndash5180 1716 50 178

Icarus Camp 74430S 21(9) 2780ndash6060 4389 47 29

N Adelie Cove 74460S 7(2) 4525ndash7190 1490 8 17

Inexpressible Island 74530S 9(5) 1220ndash5058 2078 9 6

Cape Irizar 75340S 7 860ndash4010 1830 299 1

Prior Island 75410S 6(1) 2980ndash4525 834 118 3

Cape Hickey 76050S 10(7) 1985ndash6240 16274 29 2

N Cape Day 76150S 1 3060 226 41 ndash

Depot Island 76420S 5(4) 2020ndash5840 766 10 1

Cape Ross 76440S 5(1) 2835ndash3015 7535 36 27

Dunlop Island 77140S 4 2230ndash4330 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

Table 2 Fish taxa identified from otoliths recovered from ornitho-

genic soils sampled at Adelie penguin colonies along the Victoria

Land coast Ross Sea Antarctica

Taxon Number of otoliths () MNI ()

Pleuragramma antarcticum 610 (9010) 355 (9126)

Trematomus sp 10 (148) 10 (257)

Pagothenia sp 23 (340) 17 (437)

Unidentified Nototheniidae 34 (502) 27 (694)

Total 677 409

The total numbers of identifiable otoliths and MNI are provided for

each taxon percentages are reported in parentheses

Polar Biol

123

all samples In fact the age distribution of the samples

confirms that fish remains increased in samples dated

between 2000 and 4000 BP a period that includes the time

lag defined as the lsquolsquopenguin optimumrsquorsquo by Hall et al (2006)

(Fig 3)

Fish species different from P antarcticum composed a

very small percentage of the organic material sorted in the

ornithogenic sediment Species other than silverfish

occurred only at southern latitudes between 74420 and

77140S When included in the logistical model (c) the

presenceabsence of other fishes was significantly

explained by the latitude alone (Table 3) and the model

correctly reclassified 797 of the samples

Prey size classes in ornithogenic soils

A morphometric analysis of 380 Antarctic silverfish

otoliths showed that the mean silverfish SL was

6723 plusmn 2347 mm (range 4018ndash18267) Furthermore

our data indicate that 8289 of the silverfish eaten by

Adelie penguins belonged to the 40ndash80 mm length class

(Fig 4)

There was no significant difference in the distribution of

the size classes of P antarcticum according to age of the

samples Grouping colonies according to a north to south

gradient samples from the northern colonies (n = 70 mean

7139 plusmn 23007 mm) contained longer Antarctic silverfish

compared to the southern colonies (n = 310 mean

66285 plusmn 23508 mm) this difference appears to be sig-

nificant (U MannndashWhitney = 782850 Z = -3521

P = 0000)

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 74420 and

77140S (866) The abundance in guano samplersquos

availability during this period may be a consequence of the

great spread of Adelie penguin colonies recorded for the

VL between 2300 and 4000 BP and indicated as the lsquolsquopen-

guin optimumrsquorsquo (cfr Baroni and Orombelli 1994a Hall

et al 2006)

Table 3 Logistic models testing the effect of latitude and age on the

presenceabsence in the ornithogenic samples of models a b c

Variable B Wald statistic df P

Model a) Latitude -0840 0140 1 0709

Age of samples 0000 2701 1 0100

Constant 7914 0223 1 0637

Model b) Latitude 0032 0017 1 0896

Age of samples 0000 5463 1 0019

Constant -0651 0001 1 0972

Model c) Latitude 0653 3757 1 0050

Age of samples 0000 0010 1 0921

Constant -50665 3955 1 0047

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-uragramma antarcticum) (n = 79 16 with other species and 63

without)

Significant effects are indicated

Fig 3 Samples with fish remains (DR) (n = 65 black bars) and

samples with P antarcticum (n = 46 light bars) grouped for each

1000 years (from 320 to 7200 BP) NDR samples of the period are

reported in parentheses The time periods of occupational history for

Victoria Land as described by Hall et al (2006) are reported in the

background

Pleuragramma antarcticum

0

5

10

15

20

25

30

0 10 20 30 40 50 60 70 80 90 100 110 120 130 140 150 160 170 180

SL classes (mm)

Fre

qu

ency

of

occ

urr

ence

(

)

Fig 4 Antarctic silverfish size class distribution in ornithogenic

samples For each class the lower limit (mm) is reported

Polar Biol

123

Except for fish otoliths and bones no other dietary

remains were recovered in this study although Polito et al

(2002) identified several squid beaks in organic sediments

at Ross Island One possible explanation for the lack of

squid remains in our sample could be the lower preserva-

tion of the cephalopod beak compared to fish otoliths

(Emslie and McDaniel 2002) or it is possible that squid did

not contribute to the diet of Adelie penguins in the inves-

tigated period and locations Assuming that Adelie

penguins are still feeding upon the same preys since the

Holocene recent literature reports that squid are preyed

during the summer in East Antarctica and the Weddell Sea

but have not been reported for the Ross Sea (cfr Ainley

2002) In this region two krill species (Euphausia superba

and E crystallorophias) and fish compose the Adelie

penguin diet mixed together in different proportions

(Ainley 2002 Olmastroni et al 2000)

Temporal and spatial variation of prey

Taxonomic identification of fish otoliths indicated P ant-

arcticum as the most eaten prey throughout the investigated

period The abundance of Antarctic silverfish remains

identified in this study agrees with previous paleodietary

investigations in the Antarctica Peninsula East Antarctica

and in the southern Ross Sea region (Emslie and McDaniel

2002 McDaniel and Emslie 2002 Polito et al 2002

Emslie and Woehler 2005) 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 50ndash75 by mass to the Adelie penguin diet even

exceeding crystal krill (E crystallorophias) consumption

in the southern Ross Sea (Ainley 2002 Ainley et al 2003)

Only a very low percentage of remains belongs to other

fish genera The interspecific variation in samples found

exclusively at southern latitudes was probably a conse-

quence of the fact that those samples composed 866 of

the total and contained 96 of the recovered otoliths The

low percentage of occurrence of lsquolsquoother speciesrsquorsquo in our

samples is not surprising Adelie penguins primarily forage

in the continental shelf waters surrounding Antarctica

which are characterized by a very low ichthyic biodiversity

(cfr Ainley 2002) Most unidentifiable fish otoliths

retrieved in the older guano samples maybe related to

sediment transformation processes (such as pedogenesis

and diagenesis) However since many of the best-pre-

served P antarcticum otoliths come from the older guano

samples preservation factors appear here to be related

more to acidic digestion processes rather than to the sample

age or to erosion action through time This is also

supported by the dry and cold condition of Antarctic

environment where the arid climate and low temperatures

slow the damage action of soil processes on organic

remains

Latitude did not significantly affect the mean relative

abundance of Antarctic silverfish indicating that in the past

this species represented an important food source for

penguin breeding throughout the VL coast This prey

species has fluctuated in importance over the past

6000 years (Fig 3) This pattern seems to agree with Hall

et al (2006) who delineated the Adelie penguin and ele-

phant seal occupation history for the VL coast Decreasing

periods of silverfish remains in the present study (Fig 3

1000ndash2000 and 5000ndash6000 BP) correspond approximately

to the seal optimum (1100ndash2300 BP) and to the coeval

occupation (ie contemporary occupation by both species)

(4000ndash6000 BP) reported by Hall et al (2006) Both of

these periods were characterized by a sea ice decrease in

the Ross Sea particularly severe during the most recent

period On the other hand our data show an increase in the

silverfish remains abundance in the past 1000 years and

during the lsquolsquopenguin optimumrsquorsquo this latter being the highest

value among all the investigated periods The lsquolsquopenguin

optimumrsquorsquo and the most recent ages were characterized by

higher sea ice in the Ross Sea region producing a more

fitting habitat for the sea ice obligate Adelie penguin (Hall

et al 2006) The shifts in the presence of fish remains and

in particular of P antarcticum might also represent chan-

ges in Antarctic silverfish population according to the sea

ice advance and retreat (Eastman 1993) Zane et al (2006)

used mitochondrial DNA sequencing to hypothesize that a

demographic expansion that occurred for P antarcticum

during a cooling period (last glaciation peak 111000ndash

126000 BP) suggesting a strong link between this species

(and its prey cfr Smetacek and Nicol 2005) and paleo-

climatic regime shifts

Nevertheless Antarctic silverfish is characterized by a

strong trophic flexibility and adaptability (Eastman 1993

Zane et al 2006) and at present compose the main part of

the diet of marine predators which are also ice-avoiding

species that prefer open water such as elephant seals

(Daneri and Carlini 2002) For this reason we hypothesize

that rather than indicating a decrease in silverfish avail-

ability the shifts in abundance of P antarcticum in the

present study could reflect a higher number of fish remains

in samples as a consequence of a higher number of birds

attending the colonies during periods with more sea ice

Prey size selection

Despite their dense structures fish otoliths are exposed to

variable mechanical and chemical abrasions on calcium

carbonate in the digestive tracts of predators The

Polar Biol

123

susceptibility of fish otoliths (and bones) to digestive ero-

sion appears to change widely taxon by taxon (Harkonen

1986 Pierce et al 1993 Tollit et al 1997) Furthermore in

the ornithogenic soils continuous freezethaw action

through time and sediment transformation processes can

contribute to the consumption and damage of otoliths

These erosive processes act on otolith morphological fea-

tures and size and can lead to non-detection of some prey

categories or of some individuals in a prey category and to

underestimation of prey body size Nevertheless the rela-

tive frequency and size of prey estimated from the hard

remains found in guano samples are valuable and are very

likely the only available information on the kind of prey

consumed

Juvenile P antarcticum with a 40ndash80 mm standard

length range (conforming to juvenile age classes 1 and

2 Hubold and Tomo 1989) are the most-represented

individuals in the VL sediments McDaniel and Emslie

(2002) recognized this prevalence in Northern Marguerite

Bay (Antarctic Peninsula) although with a wider value

range (1582ndash1874 mm) and higher mean SL (10819 plusmn

2553 mm) Juvenile P antarcticum occur primarily at

depths of 50ndash400 m and are well accessible to penguin

capture since their normal foraging depths range between 3

and 98 m (Chappell et al 1993) When analyzing the

temporal distribution of P antarcticum SL significant

differences were not found throughout the investigated

period In Northern Marguerite Bay (Antarctic Peninsula)

(McDaniel and Emslie 2002) some variations within mean

silverfish SL have been recognized among different time

periods but these did not result in a predictable temporal

pattern in accord with past climate change although

Holocene climatic environmental changes are well docu-

mented in both the Antarctic Peninsula and the Ross Sea

region (Bjorck et al 1996 Ingolfsson et al 1998 Baroni

and Orombelli 1991 1994b Baroni and Hall 2004 Hall

et al 2004 2006) The absence of temporal variations of

the silverfish size over the past 7000 years reflects a cer-

tain stability in penguin foraging habits which is also

confirmed by modern diet data on the species predated (crf

Ainley 2002) and on the prey size (Olmastroni et al 2004a

b) No significant temporal variation in prey size was

found The significant difference in silverfish mean size

between the northern and southern colonies was not due to

the amount of older thus more eroded otoliths in the

southern samples In fact the percentage of recent otoliths

for the north and south colonies remains very similar for

the 0ndash1000 period (20 and 1967) and furthermore

northern samples contain higher percentages of older

(period 4000ndash6000) otoliths with respect to the south area

(6713 and 4806 respectively) Therefore although the

difference accounts only for a mean value of 511 mm we

can hypothesize that at least in the past penguins breeding

in colonies located north of the Drygalski ice tongue were

feeding on slightly larger Antarctic silverfish

Sample without fish remains are they evidence

of a dietary shift

Although fish otoliths and bones regularly occur in the

analyzed ornithogenic sediments some guano samples did

not provide any kind of dietary remains Polito et al (2002)

reported the occurrence of feathers in Cape Bird organic

levels without dietary remains which may reflect their

deposition at the time when the area was used by penguin

only to molt and not to nest Stratigraphic and geomor-

phologic features of our samples indicate their nesting site

origin confirmed by the presence of eggshell fragments

collected at the same level suggesting that penguins were

nesting A small number of breeding penguins could be

responsible for the paucity of remains or erosion processes

may have accounted for otolith loss We can also hypoth-

esize that the lack of prey remains could be a shift to a

prevalent non-fish diet Considering in fact that krill is not

maintained in the soils guano samples without fish remains

could reflect a tendency towards a prevalent krill-based

paleodiet At present time Adelie penguin diet switching

between fish and krill may reflect changes in the foraging

setting in relation to environmental and ecological features

Several authors indicated particular climate and marine

conditions (ie sea-ice extension and persistence) as cause

of penguin dietary fluctuation between fish and krill

(Ainley et al 1998 Olmastroni et al 2000 cfr Ainley

2002 Ainley et al 2003) But Ainley et al (2006) in a

more recent study suggested also that feeding competition

among penguins and cetaceans rather than change in

sea-ice cover can better explain the annual switch in the

penguinsrsquo prey items

If the temporal distribution of DR samples versus NDR

ones revealed no significant differences some consider-

ations on their spatial distribution could be made In certain

locations including Inexpressible Island Cape Hickey and

Depot Island NDR guano samples prevail over those

containing fish remains (Table 1) In these cases particular

local marine conditions or other ecological factors as well

as foraging competition with other predators could have

resulted in different krill availability andor consumption

(cfr Ainley et al 2006) Occurring in earlier periods at

Inexpressible Island (5058ndash3900 BP) and later at Cape

Hickey (4075ndash1985 BP) and at Dunlop Island (3100ndash2020

BP) it is not possible to define a common paleoenviron-

mental factor that explains this pattern at the regional scale

At Inexpressible Island for example between 6000 and

4000 BP Adelie penguins shared ice-free coastal terrain

with elephant seals (Hall et al 2006) Thus it is possible

that in this area feeding competition due to this coeval

Polar Biol

123

occupation led penguins to change their diet by targeting

primarily krill which may be eaten only occasionally by

elephant seals (Daneri and Carlini 2002 van den Hoff et al

2003) Even if not revealed by the spatial and temporal

distribution of our samples different sea ice regimes

(Olmastroni et al 2004a b) andor mega icebergs calving

(Arrigo et al 2002) might have had an effect at local scale

These events in fact are known to play an important role on

penguin life cycle and they have been reported to occur in

the past (cfr Shepherd et al 2005)

Although Holocene climatic and environmental changes

have clearly affected the VL coast as indicated by Adelie

penguin colonization history (Baroni and Orombelli

1994a Lambert et al 2002 Emslie et al 2003 Hall et al

2006) over the past 7000 years the Ross Sea ecosystem

seemed to be a relatively stable ecosystem with P ant-

arcticum being the most important fish component in the

Adelie penguin diet for several thousand years The

present study provides the most detailed Adelie penguin

paleodiet records for this area These records may supply

new insights into the past feeding penguin behavior in

the VL coastal area and on a larger scale about the

ecological conditions of the Ross Sea ecosystem during

the Holocene

Acknowledgments This work was executed within the framework

of the Italian National Program on Antarctic Research (PNRA) and

was financially supported by joint research programs in geology at

the University of Pisa The authors thank Fabrizio Ciampolini

(University of Siena) for scanning electron micrographs Silvano

Focardi head of the laboratories at the Department of Environ-

mental Science (University of Siena) where the morphometric

analyses were performed David Lambert Grant Ballard and one

anonymous referee greatly improved an earlier version of the

manuscript

References

Ainley DG (2002) The Adelie penguin bellwether of climate change

Columbia University Press New York

Ainley DG Wilson PR Barton KJ Ballard G Nur N Karl B (1998)

Diet and foraging effort of Adelie penguins in relation to pack-

ice conditions in the southern Ross Sea Polar Biol 20311ndash319

doi101007s003000050308

Ainley DG Ballard G Barton KJ Karl BJ Rau GH Ribic CA

Wilson PR (2003) Spatial and temporal variation of diet within a

presumed metapopulation of Adelie penguins Condor 10595ndash

106 doi1016500010-5422(2003)105[95SATVOD]20CO2

Ainley DG Ballard G Dugger KM (2006) Competition among

penguins and cetaceans reveals trophic cascade in the Western

Ross Sea Antarctica Ecology 872080ndash2093 doi1018900012-

9658(2006)87[2080CAPACR]20CO2

Arrigo KR van Dijken GL Ainley DG Fahnestock MA Markus T

(2002) Ecological impact of a large Antarctic iceberg Geophys

Res Lett 291104 doi1010292001GL014160

Baroni C (1994) Notes on late-glacial retreat of the Antarctic ice sheet

and Holocene environmental changes along the Victoria Land

Coast Mem Natl Inst Polar Res (Jpn) C 5085ndash107

Baroni C Hall BL (2004) A new Holocene relative sea-level curve for

Terra Nova Bay Victoria Land Antarctica J Quat Sci 19377ndash

396 doi101002jqs825

Baroni C Orombelli G (1991) Holocene raised beaches at Terra

Nova Bay Victoria Land Antartica Quat Res 36157ndash177

doi1010160033-5894(91)90023-X

Baroni C Orombelli G (1994a) Abandoned penguin rookeries

as Holocene paleoclimatic indicators in Antarctica Geology

2223ndash26 doi1011300091-7613(1994)0220023APRAHP[23CO2

Baroni C Orombelli G (1994b) Holocene glacier variations in Terra

Nova bay area (Victoria Land Antartica) Antarct Sci 6497ndash

505 doi101017S0954102094000751

Barrett JE Virginia RA Hopkins DW Aislabie J Bargagli R

Bockheim JG Campbell IB Lyons WB Moorhead DL Nkem

JN Sletten RS Steltzer H Wall DH Wallenstein MD (2006)

Terrestrial ecosystem processes of Victoria Land Antarctica

Soil Biol Biochem 383019ndash3034 doi101016jsoilbio2006

04041

Berkman PA Forman SL (1996) Pre-bomb radiocarbon and the

reservoir correction for calcareous marine species in the

Southern Ocean Geophys Res Lett 23363ndash366 doi101029

96GL00151

Bjorck S Hakansson H Olsson S Ellis-Evans C Humlum O Lirio

JM (1996) Late Holocene palaeoclimatic records from lakes

sediments on James Ross Island Antarctica Palaeogeogr

Palaeoclimatol Palaeoecol 113195ndash220 doi1010160031-

0182(95)00086-0

Bochenski Z (1985) Remains of subfossil birds from King George

Island (South Shetland Islands) Acta Zool Cracov 29109ndash116

Chappell MA Shoemaker VH Janes DN Bucher TL Maloney SK

(1993) Diving behavior during foraging in breeding Adelie

penguins Ecol USA 741204ndash1215

Daneri GA Carlini AR (2002) Fish prey of southern elephant seals

Mirounga leonine at King George Island Polar Biol 25739ndash743

Eastman JT (1993) Antarctic fish biology evolution in a unique

environment Academic Press San Diego

Emslie SD (1995) Age and taphonomy of abandoned penguin

rookeries in the Antarctic Peninsula region Polar Rec (Gr Brit)

31409ndash418

Emslie SD (2001) Radiocarbon dates from abandoned penguin

colonies in the Antarctica peninsula region Antarct Sci

13289ndash295 doi101017S0954102001000414

Emslie SD McDaniel JD (2002) Adelie penguin diet and climate

change during the middle to late Holocene in northern Margue-

rite Bay Antarctic Peninsula Polar Biol 25222ndash229

Emslie SD Patterson WP (2007) Abrupt shift in d13C and d15N

values in Adelie penguin eggshell in Antarctica Proc Natl Acad

Sci USA 10411666ndash11669 doi101073pnas0608477104

Emslie SD Woehler EJ (2005) A 9000-year record of Adelie penguin

occupation and diet in the Windmill Islands East Antarctica

Antarct Sci 1757ndash66 doi101017S0954102005002427

Emslie SD Fraser W Smith RC Walker W (1998) Abandoned

penguin colonies and environmental change in the Palmer

Station area Anvers Island Antarctic Peninsula Antarct Sci

10257ndash268 doi101017S0954102098000352

Emslie SD Berkman PA Ainley DG Coats L Polito M (2003) Late-

Holocene initiation of ice-free ecosystems in the southern Ross

Sea Antarctica Mar Ecol Prog Ser 26219ndash25 doi103354

meps262019

Emslie SD Coats L Licht K (2007) A 45000 year record of Adelie

penguins and climate change in the Ross Sea Antarctica

Geology 3561ndash64 doi101130G23011A1

Hall BL Baroni C Denton GH (2004) Holocene relative sea-level

history of the Southern Victoria Land Coast Antarctica Glob

Planet Chang 42241ndash263 doi101016jgloplacha200309004

Polar Biol

123

penguin bones feathers eggshell fragments and hard parts

of dietary remains such as fish bones (vertebrae) scales

and otoliths Since krill and their fragile carapaces are not

preserved in sediments the ornithogenic soils investigation

provided data only about the non-euphausiid (ie fish)

paleodietary components The thickness of ornithogenic

soils ranged from centimeters to decimeters and the mean

mass of the samples was 186 g (range 6ndash885 g) Among a

total of 97 samples 32 did not contain dietary remains

(NDR) and 18 contained only fish vertebrae (Table 1) In

NDR samples neither fish bones nor otoliths were recov-

ered but eggshell fragments and feathers testified to the

ornithogenic nature of those samples and confirmed the

presence of nesting sites

Among the 16 visited localities Cape Irizar Prior

Island Cape Ross and Cape Day were the most productive

in terms of the number of fish otoliths Samples from

Gondwana station samples were the richest in fish bones

but no otoliths were found At Inexpressible Island Cape

Hickey and Depot Island there was a clear prevalence of

NDR compared to the DR samples (Table 1)

Otoliths were found in 47 samples and were analyzed

to identify prey taxa A total of 677 otoliths correspond-

ing to 409 individuals (87 plusmn 1258 preys per sample)

belonging to four taxa were identified (Table 2) Taxo-

nomic identification indicated that all penguins fish prey

belonged to the family Nototheniidae and consisted

mainly of P antarcticum (9010 of MNI) followed

by Pagothenia sp (340 of MNI) and Trematomus sp

(148 of MNI) Among the individuals of the genus

Trematomus six were recognized as Trematomus ber-

nacchii The rest of the recovered otoliths (502) too

eroded to estimate side and size are taxonomically

uncertain but among the family Nototheniidae

Comparison among dietary items latitude and age

Results from model (a) showed that neither latitude nor age

had an effect on the presenceabsence of fish remains in all

the ornithogenic samples (n = 97) (Table 3) On the con-

trary the model (b) revealed that the age of the samples

significantly explained the presence of P antarcticum

while the latitude did not appear to have any explanatory

effect (Table 3) The model (b) correctly reclassified

804 of the samples with P antarcticum and 62 of the

Table 1 Number of dietary remains recovered in ornithogenic soil samples discovered in Victoria Land

Collection site Latitude No of guano

samples (NDR)

Radiocarbon

date range (BP)

Total mass

(g)

No of recovered

fish otolith

No of recovered

fish bones

Cape Adare 71180S 1 1180 38 1 1

Duke of York 71370S 1 920 121 ndash 11

Cape Hallett 72190S 4(1) 320ndash400 3155 11 4

Edmonson point 74200S 5(1) 770ndash990 801 12 13

Gondwana station 74380S 2 3330ndash3370 280 ndash 112

Terra Nova station 74420S 9(1) 3580ndash5180 1716 50 178

Icarus Camp 74430S 21(9) 2780ndash6060 4389 47 29

N Adelie Cove 74460S 7(2) 4525ndash7190 1490 8 17

Inexpressible Island 74530S 9(5) 1220ndash5058 2078 9 6

Cape Irizar 75340S 7 860ndash4010 1830 299 1

Prior Island 75410S 6(1) 2980ndash4525 834 118 3

Cape Hickey 76050S 10(7) 1985ndash6240 16274 29 2

N Cape Day 76150S 1 3060 226 41 ndash

Depot Island 76420S 5(4) 2020ndash5840 766 10 1

Cape Ross 76440S 5(1) 2835ndash3015 7535 36 27

Dunlop Island 77140S 4 2230ndash4330 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

Table 2 Fish taxa identified from otoliths recovered from ornitho-

genic soils sampled at Adelie penguin colonies along the Victoria

Land coast Ross Sea Antarctica

Taxon Number of otoliths () MNI ()

Pleuragramma antarcticum 610 (9010) 355 (9126)

Trematomus sp 10 (148) 10 (257)

Pagothenia sp 23 (340) 17 (437)

Unidentified Nototheniidae 34 (502) 27 (694)

Total 677 409

The total numbers of identifiable otoliths and MNI are provided for

each taxon percentages are reported in parentheses

Polar Biol

123

all samples In fact the age distribution of the samples

confirms that fish remains increased in samples dated

between 2000 and 4000 BP a period that includes the time

lag defined as the lsquolsquopenguin optimumrsquorsquo by Hall et al (2006)

(Fig 3)

Fish species different from P antarcticum composed a

very small percentage of the organic material sorted in the

ornithogenic sediment Species other than silverfish

occurred only at southern latitudes between 74420 and

77140S When included in the logistical model (c) the

presenceabsence of other fishes was significantly

explained by the latitude alone (Table 3) and the model

correctly reclassified 797 of the samples

Prey size classes in ornithogenic soils

A morphometric analysis of 380 Antarctic silverfish

otoliths showed that the mean silverfish SL was

6723 plusmn 2347 mm (range 4018ndash18267) Furthermore

our data indicate that 8289 of the silverfish eaten by

Adelie penguins belonged to the 40ndash80 mm length class

(Fig 4)

There was no significant difference in the distribution of

the size classes of P antarcticum according to age of the

samples Grouping colonies according to a north to south

gradient samples from the northern colonies (n = 70 mean

7139 plusmn 23007 mm) contained longer Antarctic silverfish

compared to the southern colonies (n = 310 mean

66285 plusmn 23508 mm) this difference appears to be sig-

nificant (U MannndashWhitney = 782850 Z = -3521

P = 0000)

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 74420 and

77140S (866) The abundance in guano samplersquos

availability during this period may be a consequence of the

great spread of Adelie penguin colonies recorded for the

VL between 2300 and 4000 BP and indicated as the lsquolsquopen-

guin optimumrsquorsquo (cfr Baroni and Orombelli 1994a Hall

et al 2006)

Table 3 Logistic models testing the effect of latitude and age on the

presenceabsence in the ornithogenic samples of models a b c

Variable B Wald statistic df P

Model a) Latitude -0840 0140 1 0709

Age of samples 0000 2701 1 0100

Constant 7914 0223 1 0637

Model b) Latitude 0032 0017 1 0896

Age of samples 0000 5463 1 0019

Constant -0651 0001 1 0972

Model c) Latitude 0653 3757 1 0050

Age of samples 0000 0010 1 0921

Constant -50665 3955 1 0047

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-uragramma antarcticum) (n = 79 16 with other species and 63

without)

Significant effects are indicated

Fig 3 Samples with fish remains (DR) (n = 65 black bars) and

samples with P antarcticum (n = 46 light bars) grouped for each

1000 years (from 320 to 7200 BP) NDR samples of the period are

reported in parentheses The time periods of occupational history for

Victoria Land as described by Hall et al (2006) are reported in the

background

Pleuragramma antarcticum

0

5

10

15

20

25

30

0 10 20 30 40 50 60 70 80 90 100 110 120 130 140 150 160 170 180

SL classes (mm)

Fre

qu

ency

of

occ

urr

ence

(

)

Fig 4 Antarctic silverfish size class distribution in ornithogenic

samples For each class the lower limit (mm) is reported

Polar Biol

123

Except for fish otoliths and bones no other dietary

remains were recovered in this study although Polito et al

(2002) identified several squid beaks in organic sediments

at Ross Island One possible explanation for the lack of

squid remains in our sample could be the lower preserva-

tion of the cephalopod beak compared to fish otoliths

(Emslie and McDaniel 2002) or it is possible that squid did

not contribute to the diet of Adelie penguins in the inves-

tigated period and locations Assuming that Adelie

penguins are still feeding upon the same preys since the

Holocene recent literature reports that squid are preyed

during the summer in East Antarctica and the Weddell Sea

but have not been reported for the Ross Sea (cfr Ainley

2002) In this region two krill species (Euphausia superba

and E crystallorophias) and fish compose the Adelie

penguin diet mixed together in different proportions

(Ainley 2002 Olmastroni et al 2000)

Temporal and spatial variation of prey

Taxonomic identification of fish otoliths indicated P ant-

arcticum as the most eaten prey throughout the investigated

period The abundance of Antarctic silverfish remains

identified in this study agrees with previous paleodietary

investigations in the Antarctica Peninsula East Antarctica

and in the southern Ross Sea region (Emslie and McDaniel

2002 McDaniel and Emslie 2002 Polito et al 2002

Emslie and Woehler 2005) 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 50ndash75 by mass to the Adelie penguin diet even

exceeding crystal krill (E crystallorophias) consumption

in the southern Ross Sea (Ainley 2002 Ainley et al 2003)

Only a very low percentage of remains belongs to other

fish genera The interspecific variation in samples found

exclusively at southern latitudes was probably a conse-

quence of the fact that those samples composed 866 of

the total and contained 96 of the recovered otoliths The

low percentage of occurrence of lsquolsquoother speciesrsquorsquo in our

samples is not surprising Adelie penguins primarily forage

in the continental shelf waters surrounding Antarctica

which are characterized by a very low ichthyic biodiversity

(cfr Ainley 2002) Most unidentifiable fish otoliths

retrieved in the older guano samples maybe related to

sediment transformation processes (such as pedogenesis

and diagenesis) However since many of the best-pre-

served P antarcticum otoliths come from the older guano

samples preservation factors appear here to be related

more to acidic digestion processes rather than to the sample

age or to erosion action through time This is also

supported by the dry and cold condition of Antarctic

environment where the arid climate and low temperatures

slow the damage action of soil processes on organic

remains

Latitude did not significantly affect the mean relative

abundance of Antarctic silverfish indicating that in the past

this species represented an important food source for

penguin breeding throughout the VL coast This prey

species has fluctuated in importance over the past

6000 years (Fig 3) This pattern seems to agree with Hall

et al (2006) who delineated the Adelie penguin and ele-

phant seal occupation history for the VL coast Decreasing

periods of silverfish remains in the present study (Fig 3

1000ndash2000 and 5000ndash6000 BP) correspond approximately

to the seal optimum (1100ndash2300 BP) and to the coeval

occupation (ie contemporary occupation by both species)

(4000ndash6000 BP) reported by Hall et al (2006) Both of

these periods were characterized by a sea ice decrease in

the Ross Sea particularly severe during the most recent

period On the other hand our data show an increase in the

silverfish remains abundance in the past 1000 years and

during the lsquolsquopenguin optimumrsquorsquo this latter being the highest

value among all the investigated periods The lsquolsquopenguin

optimumrsquorsquo and the most recent ages were characterized by

higher sea ice in the Ross Sea region producing a more

fitting habitat for the sea ice obligate Adelie penguin (Hall

et al 2006) The shifts in the presence of fish remains and

in particular of P antarcticum might also represent chan-

ges in Antarctic silverfish population according to the sea

ice advance and retreat (Eastman 1993) Zane et al (2006)

used mitochondrial DNA sequencing to hypothesize that a

demographic expansion that occurred for P antarcticum

during a cooling period (last glaciation peak 111000ndash

126000 BP) suggesting a strong link between this species

(and its prey cfr Smetacek and Nicol 2005) and paleo-

climatic regime shifts

Nevertheless Antarctic silverfish is characterized by a

strong trophic flexibility and adaptability (Eastman 1993

Zane et al 2006) and at present compose the main part of

the diet of marine predators which are also ice-avoiding

species that prefer open water such as elephant seals

(Daneri and Carlini 2002) For this reason we hypothesize

that rather than indicating a decrease in silverfish avail-

ability the shifts in abundance of P antarcticum in the

present study could reflect a higher number of fish remains

in samples as a consequence of a higher number of birds

attending the colonies during periods with more sea ice

Prey size selection

Despite their dense structures fish otoliths are exposed to

variable mechanical and chemical abrasions on calcium

carbonate in the digestive tracts of predators The

Polar Biol

123

susceptibility of fish otoliths (and bones) to digestive ero-

sion appears to change widely taxon by taxon (Harkonen

1986 Pierce et al 1993 Tollit et al 1997) Furthermore in

the ornithogenic soils continuous freezethaw action

through time and sediment transformation processes can

contribute to the consumption and damage of otoliths

These erosive processes act on otolith morphological fea-

tures and size and can lead to non-detection of some prey

categories or of some individuals in a prey category and to

underestimation of prey body size Nevertheless the rela-

tive frequency and size of prey estimated from the hard

remains found in guano samples are valuable and are very

likely the only available information on the kind of prey

consumed

Juvenile P antarcticum with a 40ndash80 mm standard

length range (conforming to juvenile age classes 1 and

2 Hubold and Tomo 1989) are the most-represented

individuals in the VL sediments McDaniel and Emslie

(2002) recognized this prevalence in Northern Marguerite

Bay (Antarctic Peninsula) although with a wider value

range (1582ndash1874 mm) and higher mean SL (10819 plusmn

2553 mm) Juvenile P antarcticum occur primarily at

depths of 50ndash400 m and are well accessible to penguin

capture since their normal foraging depths range between 3

and 98 m (Chappell et al 1993) When analyzing the

temporal distribution of P antarcticum SL significant

differences were not found throughout the investigated

period In Northern Marguerite Bay (Antarctic Peninsula)

(McDaniel and Emslie 2002) some variations within mean

silverfish SL have been recognized among different time

periods but these did not result in a predictable temporal

pattern in accord with past climate change although

Holocene climatic environmental changes are well docu-

mented in both the Antarctic Peninsula and the Ross Sea

region (Bjorck et al 1996 Ingolfsson et al 1998 Baroni

and Orombelli 1991 1994b Baroni and Hall 2004 Hall

et al 2004 2006) The absence of temporal variations of

the silverfish size over the past 7000 years reflects a cer-

tain stability in penguin foraging habits which is also

confirmed by modern diet data on the species predated (crf

Ainley 2002) and on the prey size (Olmastroni et al 2004a

b) No significant temporal variation in prey size was

found The significant difference in silverfish mean size

between the northern and southern colonies was not due to

the amount of older thus more eroded otoliths in the

southern samples In fact the percentage of recent otoliths

for the north and south colonies remains very similar for

the 0ndash1000 period (20 and 1967) and furthermore

northern samples contain higher percentages of older

(period 4000ndash6000) otoliths with respect to the south area

(6713 and 4806 respectively) Therefore although the

difference accounts only for a mean value of 511 mm we

can hypothesize that at least in the past penguins breeding

in colonies located north of the Drygalski ice tongue were

feeding on slightly larger Antarctic silverfish

Sample without fish remains are they evidence

of a dietary shift

Although fish otoliths and bones regularly occur in the

analyzed ornithogenic sediments some guano samples did

not provide any kind of dietary remains Polito et al (2002)

reported the occurrence of feathers in Cape Bird organic

levels without dietary remains which may reflect their

deposition at the time when the area was used by penguin

only to molt and not to nest Stratigraphic and geomor-

phologic features of our samples indicate their nesting site

origin confirmed by the presence of eggshell fragments

collected at the same level suggesting that penguins were

nesting A small number of breeding penguins could be

responsible for the paucity of remains or erosion processes

may have accounted for otolith loss We can also hypoth-

esize that the lack of prey remains could be a shift to a

prevalent non-fish diet Considering in fact that krill is not

maintained in the soils guano samples without fish remains

could reflect a tendency towards a prevalent krill-based

paleodiet At present time Adelie penguin diet switching

between fish and krill may reflect changes in the foraging

setting in relation to environmental and ecological features

Several authors indicated particular climate and marine

conditions (ie sea-ice extension and persistence) as cause

of penguin dietary fluctuation between fish and krill

(Ainley et al 1998 Olmastroni et al 2000 cfr Ainley

2002 Ainley et al 2003) But Ainley et al (2006) in a

more recent study suggested also that feeding competition

among penguins and cetaceans rather than change in

sea-ice cover can better explain the annual switch in the

penguinsrsquo prey items

If the temporal distribution of DR samples versus NDR

ones revealed no significant differences some consider-

ations on their spatial distribution could be made In certain

locations including Inexpressible Island Cape Hickey and

Depot Island NDR guano samples prevail over those

containing fish remains (Table 1) In these cases particular

local marine conditions or other ecological factors as well

as foraging competition with other predators could have

resulted in different krill availability andor consumption

(cfr Ainley et al 2006) Occurring in earlier periods at

Inexpressible Island (5058ndash3900 BP) and later at Cape

Hickey (4075ndash1985 BP) and at Dunlop Island (3100ndash2020

BP) it is not possible to define a common paleoenviron-

mental factor that explains this pattern at the regional scale

At Inexpressible Island for example between 6000 and

4000 BP Adelie penguins shared ice-free coastal terrain

with elephant seals (Hall et al 2006) Thus it is possible

that in this area feeding competition due to this coeval

Polar Biol

123

occupation led penguins to change their diet by targeting

primarily krill which may be eaten only occasionally by

elephant seals (Daneri and Carlini 2002 van den Hoff et al

2003) Even if not revealed by the spatial and temporal

distribution of our samples different sea ice regimes

(Olmastroni et al 2004a b) andor mega icebergs calving

(Arrigo et al 2002) might have had an effect at local scale

These events in fact are known to play an important role on

penguin life cycle and they have been reported to occur in

the past (cfr Shepherd et al 2005)

Although Holocene climatic and environmental changes

have clearly affected the VL coast as indicated by Adelie

penguin colonization history (Baroni and Orombelli

1994a Lambert et al 2002 Emslie et al 2003 Hall et al

2006) over the past 7000 years the Ross Sea ecosystem

seemed to be a relatively stable ecosystem with P ant-

arcticum being the most important fish component in the

Adelie penguin diet for several thousand years The

present study provides the most detailed Adelie penguin

paleodiet records for this area These records may supply

new insights into the past feeding penguin behavior in

the VL coastal area and on a larger scale about the

ecological conditions of the Ross Sea ecosystem during

the Holocene

Acknowledgments This work was executed within the framework

of the Italian National Program on Antarctic Research (PNRA) and

was financially supported by joint research programs in geology at

the University of Pisa The authors thank Fabrizio Ciampolini

(University of Siena) for scanning electron micrographs Silvano

Focardi head of the laboratories at the Department of Environ-

mental Science (University of Siena) where the morphometric

analyses were performed David Lambert Grant Ballard and one

anonymous referee greatly improved an earlier version of the

manuscript

References

Ainley DG (2002) The Adelie penguin bellwether of climate change

Columbia University Press New York

Ainley DG Wilson PR Barton KJ Ballard G Nur N Karl B (1998)

Diet and foraging effort of Adelie penguins in relation to pack-

ice conditions in the southern Ross Sea Polar Biol 20311ndash319

doi101007s003000050308

Ainley DG Ballard G Barton KJ Karl BJ Rau GH Ribic CA

Wilson PR (2003) Spatial and temporal variation of diet within a

presumed metapopulation of Adelie penguins Condor 10595ndash

106 doi1016500010-5422(2003)105[95SATVOD]20CO2

Ainley DG Ballard G Dugger KM (2006) Competition among

penguins and cetaceans reveals trophic cascade in the Western

Ross Sea Antarctica Ecology 872080ndash2093 doi1018900012-

9658(2006)87[2080CAPACR]20CO2

Arrigo KR van Dijken GL Ainley DG Fahnestock MA Markus T

(2002) Ecological impact of a large Antarctic iceberg Geophys

Res Lett 291104 doi1010292001GL014160

Baroni C (1994) Notes on late-glacial retreat of the Antarctic ice sheet

and Holocene environmental changes along the Victoria Land

Coast Mem Natl Inst Polar Res (Jpn) C 5085ndash107

Baroni C Hall BL (2004) A new Holocene relative sea-level curve for

Terra Nova Bay Victoria Land Antarctica J Quat Sci 19377ndash

396 doi101002jqs825

Baroni C Orombelli G (1991) Holocene raised beaches at Terra

Nova Bay Victoria Land Antartica Quat Res 36157ndash177

doi1010160033-5894(91)90023-X

Baroni C Orombelli G (1994a) Abandoned penguin rookeries

as Holocene paleoclimatic indicators in Antarctica Geology

2223ndash26 doi1011300091-7613(1994)0220023APRAHP[23CO2

Baroni C Orombelli G (1994b) Holocene glacier variations in Terra

Nova bay area (Victoria Land Antartica) Antarct Sci 6497ndash

505 doi101017S0954102094000751

Barrett JE Virginia RA Hopkins DW Aislabie J Bargagli R

Bockheim JG Campbell IB Lyons WB Moorhead DL Nkem

JN Sletten RS Steltzer H Wall DH Wallenstein MD (2006)

Terrestrial ecosystem processes of Victoria Land Antarctica

Soil Biol Biochem 383019ndash3034 doi101016jsoilbio2006

04041

Berkman PA Forman SL (1996) Pre-bomb radiocarbon and the

reservoir correction for calcareous marine species in the

Southern Ocean Geophys Res Lett 23363ndash366 doi101029

96GL00151

Bjorck S Hakansson H Olsson S Ellis-Evans C Humlum O Lirio

JM (1996) Late Holocene palaeoclimatic records from lakes

sediments on James Ross Island Antarctica Palaeogeogr

Palaeoclimatol Palaeoecol 113195ndash220 doi1010160031-

0182(95)00086-0

Bochenski Z (1985) Remains of subfossil birds from King George

Island (South Shetland Islands) Acta Zool Cracov 29109ndash116

Chappell MA Shoemaker VH Janes DN Bucher TL Maloney SK

(1993) Diving behavior during foraging in breeding Adelie

penguins Ecol USA 741204ndash1215

Daneri GA Carlini AR (2002) Fish prey of southern elephant seals

Mirounga leonine at King George Island Polar Biol 25739ndash743

Eastman JT (1993) Antarctic fish biology evolution in a unique

environment Academic Press San Diego

Emslie SD (1995) Age and taphonomy of abandoned penguin

rookeries in the Antarctic Peninsula region Polar Rec (Gr Brit)

31409ndash418

Emslie SD (2001) Radiocarbon dates from abandoned penguin

colonies in the Antarctica peninsula region Antarct Sci

13289ndash295 doi101017S0954102001000414

Emslie SD McDaniel JD (2002) Adelie penguin diet and climate

change during the middle to late Holocene in northern Margue-

rite Bay Antarctic Peninsula Polar Biol 25222ndash229

Emslie SD Patterson WP (2007) Abrupt shift in d13C and d15N

values in Adelie penguin eggshell in Antarctica Proc Natl Acad

Sci USA 10411666ndash11669 doi101073pnas0608477104

Emslie SD Woehler EJ (2005) A 9000-year record of Adelie penguin

occupation and diet in the Windmill Islands East Antarctica

Antarct Sci 1757ndash66 doi101017S0954102005002427

Emslie SD Fraser W Smith RC Walker W (1998) Abandoned

penguin colonies and environmental change in the Palmer

Station area Anvers Island Antarctic Peninsula Antarct Sci

10257ndash268 doi101017S0954102098000352

Emslie SD Berkman PA Ainley DG Coats L Polito M (2003) Late-

Holocene initiation of ice-free ecosystems in the southern Ross

Sea Antarctica Mar Ecol Prog Ser 26219ndash25 doi103354

meps262019

Emslie SD Coats L Licht K (2007) A 45000 year record of Adelie

penguins and climate change in the Ross Sea Antarctica

Geology 3561ndash64 doi101130G23011A1

Hall BL Baroni C Denton GH (2004) Holocene relative sea-level

history of the Southern Victoria Land Coast Antarctica Glob

Planet Chang 42241ndash263 doi101016jgloplacha200309004

Polar Biol

123

all samples In fact the age distribution of the samples

confirms that fish remains increased in samples dated

between 2000 and 4000 BP a period that includes the time

lag defined as the lsquolsquopenguin optimumrsquorsquo by Hall et al (2006)

(Fig 3)

Fish species different from P antarcticum composed a

very small percentage of the organic material sorted in the

ornithogenic sediment Species other than silverfish

occurred only at southern latitudes between 74420 and

77140S When included in the logistical model (c) the

presenceabsence of other fishes was significantly

explained by the latitude alone (Table 3) and the model

correctly reclassified 797 of the samples

Prey size classes in ornithogenic soils

A morphometric analysis of 380 Antarctic silverfish

otoliths showed that the mean silverfish SL was

6723 plusmn 2347 mm (range 4018ndash18267) Furthermore

our data indicate that 8289 of the silverfish eaten by

Adelie penguins belonged to the 40ndash80 mm length class

(Fig 4)

There was no significant difference in the distribution of

the size classes of P antarcticum according to age of the

samples Grouping colonies according to a north to south

gradient samples from the northern colonies (n = 70 mean

7139 plusmn 23007 mm) contained longer Antarctic silverfish

compared to the southern colonies (n = 310 mean

66285 plusmn 23508 mm) this difference appears to be sig-

nificant (U MannndashWhitney = 782850 Z = -3521

P = 0000)

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 74420 and

77140S (866) The abundance in guano samplersquos

availability during this period may be a consequence of the

great spread of Adelie penguin colonies recorded for the

VL between 2300 and 4000 BP and indicated as the lsquolsquopen-

guin optimumrsquorsquo (cfr Baroni and Orombelli 1994a Hall

et al 2006)

Table 3 Logistic models testing the effect of latitude and age on the

presenceabsence in the ornithogenic samples of models a b c

Variable B Wald statistic df P

Model a) Latitude -0840 0140 1 0709

Age of samples 0000 2701 1 0100

Constant 7914 0223 1 0637

Model b) Latitude 0032 0017 1 0896

Age of samples 0000 5463 1 0019

Constant -0651 0001 1 0972

Model c) Latitude 0653 3757 1 0050

Age of samples 0000 0010 1 0921

Constant -50665 3955 1 0047

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-uragramma antarcticum) (n = 79 16 with other species and 63

without)

Significant effects are indicated

Fig 3 Samples with fish remains (DR) (n = 65 black bars) and

samples with P antarcticum (n = 46 light bars) grouped for each

1000 years (from 320 to 7200 BP) NDR samples of the period are

reported in parentheses The time periods of occupational history for

Victoria Land as described by Hall et al (2006) are reported in the

background

Pleuragramma antarcticum

0

5

10

15

20

25

30

0 10 20 30 40 50 60 70 80 90 100 110 120 130 140 150 160 170 180

SL classes (mm)

Fre

qu

ency

of

occ

urr

ence

(

)

Fig 4 Antarctic silverfish size class distribution in ornithogenic

samples For each class the lower limit (mm) is reported

Polar Biol

123

Except for fish otoliths and bones no other dietary

remains were recovered in this study although Polito et al

(2002) identified several squid beaks in organic sediments

at Ross Island One possible explanation for the lack of

squid remains in our sample could be the lower preserva-

tion of the cephalopod beak compared to fish otoliths

(Emslie and McDaniel 2002) or it is possible that squid did

not contribute to the diet of Adelie penguins in the inves-

tigated period and locations Assuming that Adelie

penguins are still feeding upon the same preys since the

Holocene recent literature reports that squid are preyed

during the summer in East Antarctica and the Weddell Sea

but have not been reported for the Ross Sea (cfr Ainley

2002) In this region two krill species (Euphausia superba

and E crystallorophias) and fish compose the Adelie

penguin diet mixed together in different proportions

(Ainley 2002 Olmastroni et al 2000)

Temporal and spatial variation of prey

Taxonomic identification of fish otoliths indicated P ant-

arcticum as the most eaten prey throughout the investigated

period The abundance of Antarctic silverfish remains

identified in this study agrees with previous paleodietary

investigations in the Antarctica Peninsula East Antarctica

and in the southern Ross Sea region (Emslie and McDaniel

2002 McDaniel and Emslie 2002 Polito et al 2002

Emslie and Woehler 2005) 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 50ndash75 by mass to the Adelie penguin diet even

exceeding crystal krill (E crystallorophias) consumption

in the southern Ross Sea (Ainley 2002 Ainley et al 2003)

Only a very low percentage of remains belongs to other

fish genera The interspecific variation in samples found

exclusively at southern latitudes was probably a conse-

quence of the fact that those samples composed 866 of

the total and contained 96 of the recovered otoliths The

low percentage of occurrence of lsquolsquoother speciesrsquorsquo in our

samples is not surprising Adelie penguins primarily forage

in the continental shelf waters surrounding Antarctica

which are characterized by a very low ichthyic biodiversity

(cfr Ainley 2002) Most unidentifiable fish otoliths

retrieved in the older guano samples maybe related to

sediment transformation processes (such as pedogenesis

and diagenesis) However since many of the best-pre-

served P antarcticum otoliths come from the older guano

samples preservation factors appear here to be related

more to acidic digestion processes rather than to the sample

age or to erosion action through time This is also

supported by the dry and cold condition of Antarctic

environment where the arid climate and low temperatures

slow the damage action of soil processes on organic

remains

Latitude did not significantly affect the mean relative

abundance of Antarctic silverfish indicating that in the past

this species represented an important food source for

penguin breeding throughout the VL coast This prey

species has fluctuated in importance over the past

6000 years (Fig 3) This pattern seems to agree with Hall

et al (2006) who delineated the Adelie penguin and ele-

phant seal occupation history for the VL coast Decreasing

periods of silverfish remains in the present study (Fig 3

1000ndash2000 and 5000ndash6000 BP) correspond approximately

to the seal optimum (1100ndash2300 BP) and to the coeval

occupation (ie contemporary occupation by both species)

(4000ndash6000 BP) reported by Hall et al (2006) Both of

these periods were characterized by a sea ice decrease in

the Ross Sea particularly severe during the most recent

period On the other hand our data show an increase in the

silverfish remains abundance in the past 1000 years and

during the lsquolsquopenguin optimumrsquorsquo this latter being the highest

value among all the investigated periods The lsquolsquopenguin

optimumrsquorsquo and the most recent ages were characterized by

higher sea ice in the Ross Sea region producing a more

fitting habitat for the sea ice obligate Adelie penguin (Hall

et al 2006) The shifts in the presence of fish remains and

in particular of P antarcticum might also represent chan-

ges in Antarctic silverfish population according to the sea

ice advance and retreat (Eastman 1993) Zane et al (2006)

used mitochondrial DNA sequencing to hypothesize that a

demographic expansion that occurred for P antarcticum

during a cooling period (last glaciation peak 111000ndash

126000 BP) suggesting a strong link between this species

(and its prey cfr Smetacek and Nicol 2005) and paleo-

climatic regime shifts

Nevertheless Antarctic silverfish is characterized by a

strong trophic flexibility and adaptability (Eastman 1993

Zane et al 2006) and at present compose the main part of

the diet of marine predators which are also ice-avoiding

species that prefer open water such as elephant seals

(Daneri and Carlini 2002) For this reason we hypothesize

that rather than indicating a decrease in silverfish avail-

ability the shifts in abundance of P antarcticum in the

present study could reflect a higher number of fish remains

in samples as a consequence of a higher number of birds

attending the colonies during periods with more sea ice

Prey size selection

Despite their dense structures fish otoliths are exposed to

variable mechanical and chemical abrasions on calcium

carbonate in the digestive tracts of predators The

Polar Biol

123

susceptibility of fish otoliths (and bones) to digestive ero-

sion appears to change widely taxon by taxon (Harkonen

1986 Pierce et al 1993 Tollit et al 1997) Furthermore in

the ornithogenic soils continuous freezethaw action

through time and sediment transformation processes can

contribute to the consumption and damage of otoliths

These erosive processes act on otolith morphological fea-

tures and size and can lead to non-detection of some prey

categories or of some individuals in a prey category and to

underestimation of prey body size Nevertheless the rela-

tive frequency and size of prey estimated from the hard

remains found in guano samples are valuable and are very

likely the only available information on the kind of prey

consumed

Juvenile P antarcticum with a 40ndash80 mm standard

length range (conforming to juvenile age classes 1 and

2 Hubold and Tomo 1989) are the most-represented

individuals in the VL sediments McDaniel and Emslie

(2002) recognized this prevalence in Northern Marguerite

Bay (Antarctic Peninsula) although with a wider value

range (1582ndash1874 mm) and higher mean SL (10819 plusmn

2553 mm) Juvenile P antarcticum occur primarily at

depths of 50ndash400 m and are well accessible to penguin

capture since their normal foraging depths range between 3

and 98 m (Chappell et al 1993) When analyzing the

temporal distribution of P antarcticum SL significant

differences were not found throughout the investigated

period In Northern Marguerite Bay (Antarctic Peninsula)

(McDaniel and Emslie 2002) some variations within mean

silverfish SL have been recognized among different time

periods but these did not result in a predictable temporal

pattern in accord with past climate change although

Holocene climatic environmental changes are well docu-

mented in both the Antarctic Peninsula and the Ross Sea

region (Bjorck et al 1996 Ingolfsson et al 1998 Baroni

and Orombelli 1991 1994b Baroni and Hall 2004 Hall

et al 2004 2006) The absence of temporal variations of

the silverfish size over the past 7000 years reflects a cer-

tain stability in penguin foraging habits which is also

confirmed by modern diet data on the species predated (crf

Ainley 2002) and on the prey size (Olmastroni et al 2004a

b) No significant temporal variation in prey size was

found The significant difference in silverfish mean size

between the northern and southern colonies was not due to

the amount of older thus more eroded otoliths in the

southern samples In fact the percentage of recent otoliths

for the north and south colonies remains very similar for

the 0ndash1000 period (20 and 1967) and furthermore

northern samples contain higher percentages of older

(period 4000ndash6000) otoliths with respect to the south area

(6713 and 4806 respectively) Therefore although the

difference accounts only for a mean value of 511 mm we

can hypothesize that at least in the past penguins breeding

in colonies located north of the Drygalski ice tongue were

feeding on slightly larger Antarctic silverfish

Sample without fish remains are they evidence

of a dietary shift

Although fish otoliths and bones regularly occur in the

analyzed ornithogenic sediments some guano samples did

not provide any kind of dietary remains Polito et al (2002)

reported the occurrence of feathers in Cape Bird organic

levels without dietary remains which may reflect their

deposition at the time when the area was used by penguin

only to molt and not to nest Stratigraphic and geomor-

phologic features of our samples indicate their nesting site

origin confirmed by the presence of eggshell fragments

collected at the same level suggesting that penguins were

nesting A small number of breeding penguins could be

responsible for the paucity of remains or erosion processes

may have accounted for otolith loss We can also hypoth-

esize that the lack of prey remains could be a shift to a

prevalent non-fish diet Considering in fact that krill is not

maintained in the soils guano samples without fish remains

could reflect a tendency towards a prevalent krill-based

paleodiet At present time Adelie penguin diet switching

between fish and krill may reflect changes in the foraging

setting in relation to environmental and ecological features

Several authors indicated particular climate and marine

conditions (ie sea-ice extension and persistence) as cause

of penguin dietary fluctuation between fish and krill

(Ainley et al 1998 Olmastroni et al 2000 cfr Ainley

2002 Ainley et al 2003) But Ainley et al (2006) in a

more recent study suggested also that feeding competition

among penguins and cetaceans rather than change in

sea-ice cover can better explain the annual switch in the

penguinsrsquo prey items

If the temporal distribution of DR samples versus NDR

ones revealed no significant differences some consider-

ations on their spatial distribution could be made In certain

locations including Inexpressible Island Cape Hickey and

Depot Island NDR guano samples prevail over those

containing fish remains (Table 1) In these cases particular

local marine conditions or other ecological factors as well

as foraging competition with other predators could have

resulted in different krill availability andor consumption

(cfr Ainley et al 2006) Occurring in earlier periods at

Inexpressible Island (5058ndash3900 BP) and later at Cape

Hickey (4075ndash1985 BP) and at Dunlop Island (3100ndash2020

BP) it is not possible to define a common paleoenviron-

mental factor that explains this pattern at the regional scale

At Inexpressible Island for example between 6000 and

4000 BP Adelie penguins shared ice-free coastal terrain

with elephant seals (Hall et al 2006) Thus it is possible

that in this area feeding competition due to this coeval

Polar Biol

123

occupation led penguins to change their diet by targeting

primarily krill which may be eaten only occasionally by

elephant seals (Daneri and Carlini 2002 van den Hoff et al

2003) Even if not revealed by the spatial and temporal

distribution of our samples different sea ice regimes

(Olmastroni et al 2004a b) andor mega icebergs calving

(Arrigo et al 2002) might have had an effect at local scale

These events in fact are known to play an important role on

penguin life cycle and they have been reported to occur in

the past (cfr Shepherd et al 2005)

Although Holocene climatic and environmental changes

have clearly affected the VL coast as indicated by Adelie

penguin colonization history (Baroni and Orombelli

1994a Lambert et al 2002 Emslie et al 2003 Hall et al

2006) over the past 7000 years the Ross Sea ecosystem

seemed to be a relatively stable ecosystem with P ant-

arcticum being the most important fish component in the

Adelie penguin diet for several thousand years The

present study provides the most detailed Adelie penguin

paleodiet records for this area These records may supply

new insights into the past feeding penguin behavior in

the VL coastal area and on a larger scale about the

ecological conditions of the Ross Sea ecosystem during

the Holocene

Acknowledgments This work was executed within the framework

of the Italian National Program on Antarctic Research (PNRA) and

was financially supported by joint research programs in geology at

the University of Pisa The authors thank Fabrizio Ciampolini

(University of Siena) for scanning electron micrographs Silvano

Focardi head of the laboratories at the Department of Environ-

mental Science (University of Siena) where the morphometric

analyses were performed David Lambert Grant Ballard and one

anonymous referee greatly improved an earlier version of the

manuscript

References

Ainley DG (2002) The Adelie penguin bellwether of climate change

Columbia University Press New York

Ainley DG Wilson PR Barton KJ Ballard G Nur N Karl B (1998)

Diet and foraging effort of Adelie penguins in relation to pack-

ice conditions in the southern Ross Sea Polar Biol 20311ndash319

doi101007s003000050308

Ainley DG Ballard G Barton KJ Karl BJ Rau GH Ribic CA

Wilson PR (2003) Spatial and temporal variation of diet within a

presumed metapopulation of Adelie penguins Condor 10595ndash

106 doi1016500010-5422(2003)105[95SATVOD]20CO2

Ainley DG Ballard G Dugger KM (2006) Competition among

penguins and cetaceans reveals trophic cascade in the Western

Ross Sea Antarctica Ecology 872080ndash2093 doi1018900012-

9658(2006)87[2080CAPACR]20CO2

Arrigo KR van Dijken GL Ainley DG Fahnestock MA Markus T

(2002) Ecological impact of a large Antarctic iceberg Geophys

Res Lett 291104 doi1010292001GL014160

Baroni C (1994) Notes on late-glacial retreat of the Antarctic ice sheet

and Holocene environmental changes along the Victoria Land

Coast Mem Natl Inst Polar Res (Jpn) C 5085ndash107

Baroni C Hall BL (2004) A new Holocene relative sea-level curve for

Terra Nova Bay Victoria Land Antarctica J Quat Sci 19377ndash

396 doi101002jqs825

Baroni C Orombelli G (1991) Holocene raised beaches at Terra

Nova Bay Victoria Land Antartica Quat Res 36157ndash177

doi1010160033-5894(91)90023-X

Baroni C Orombelli G (1994a) Abandoned penguin rookeries

as Holocene paleoclimatic indicators in Antarctica Geology

2223ndash26 doi1011300091-7613(1994)0220023APRAHP[23CO2

Baroni C Orombelli G (1994b) Holocene glacier variations in Terra

Nova bay area (Victoria Land Antartica) Antarct Sci 6497ndash

505 doi101017S0954102094000751

Barrett JE Virginia RA Hopkins DW Aislabie J Bargagli R

Bockheim JG Campbell IB Lyons WB Moorhead DL Nkem

JN Sletten RS Steltzer H Wall DH Wallenstein MD (2006)

Terrestrial ecosystem processes of Victoria Land Antarctica

Soil Biol Biochem 383019ndash3034 doi101016jsoilbio2006

04041

Berkman PA Forman SL (1996) Pre-bomb radiocarbon and the

reservoir correction for calcareous marine species in the

Southern Ocean Geophys Res Lett 23363ndash366 doi101029

96GL00151

Bjorck S Hakansson H Olsson S Ellis-Evans C Humlum O Lirio

JM (1996) Late Holocene palaeoclimatic records from lakes

sediments on James Ross Island Antarctica Palaeogeogr

Palaeoclimatol Palaeoecol 113195ndash220 doi1010160031-

0182(95)00086-0

Bochenski Z (1985) Remains of subfossil birds from King George

Island (South Shetland Islands) Acta Zool Cracov 29109ndash116

Chappell MA Shoemaker VH Janes DN Bucher TL Maloney SK

(1993) Diving behavior during foraging in breeding Adelie

penguins Ecol USA 741204ndash1215

Daneri GA Carlini AR (2002) Fish prey of southern elephant seals

Mirounga leonine at King George Island Polar Biol 25739ndash743

Eastman JT (1993) Antarctic fish biology evolution in a unique

environment Academic Press San Diego

Emslie SD (1995) Age and taphonomy of abandoned penguin

rookeries in the Antarctic Peninsula region Polar Rec (Gr Brit)

31409ndash418

Emslie SD (2001) Radiocarbon dates from abandoned penguin

colonies in the Antarctica peninsula region Antarct Sci

13289ndash295 doi101017S0954102001000414

Emslie SD McDaniel JD (2002) Adelie penguin diet and climate

change during the middle to late Holocene in northern Margue-

rite Bay Antarctic Peninsula Polar Biol 25222ndash229

Emslie SD Patterson WP (2007) Abrupt shift in d13C and d15N

values in Adelie penguin eggshell in Antarctica Proc Natl Acad

Sci USA 10411666ndash11669 doi101073pnas0608477104

Emslie SD Woehler EJ (2005) A 9000-year record of Adelie penguin

occupation and diet in the Windmill Islands East Antarctica

Antarct Sci 1757ndash66 doi101017S0954102005002427

Emslie SD Fraser W Smith RC Walker W (1998) Abandoned

penguin colonies and environmental change in the Palmer

Station area Anvers Island Antarctic Peninsula Antarct Sci

10257ndash268 doi101017S0954102098000352

Emslie SD Berkman PA Ainley DG Coats L Polito M (2003) Late-

Holocene initiation of ice-free ecosystems in the southern Ross

Sea Antarctica Mar Ecol Prog Ser 26219ndash25 doi103354

meps262019

Emslie SD Coats L Licht K (2007) A 45000 year record of Adelie

penguins and climate change in the Ross Sea Antarctica

Geology 3561ndash64 doi101130G23011A1

Hall BL Baroni C Denton GH (2004) Holocene relative sea-level

history of the Southern Victoria Land Coast Antarctica Glob

Planet Chang 42241ndash263 doi101016jgloplacha200309004

Polar Biol

123

Except for fish otoliths and bones no other dietary

remains were recovered in this study although Polito et al

(2002) identified several squid beaks in organic sediments

at Ross Island One possible explanation for the lack of

squid remains in our sample could be the lower preserva-

tion of the cephalopod beak compared to fish otoliths

(Emslie and McDaniel 2002) or it is possible that squid did

not contribute to the diet of Adelie penguins in the inves-

tigated period and locations Assuming that Adelie

penguins are still feeding upon the same preys since the

Holocene recent literature reports that squid are preyed

during the summer in East Antarctica and the Weddell Sea

but have not been reported for the Ross Sea (cfr Ainley

2002) In this region two krill species (Euphausia superba

and E crystallorophias) and fish compose the Adelie

penguin diet mixed together in different proportions

(Ainley 2002 Olmastroni et al 2000)

Temporal and spatial variation of prey

Taxonomic identification of fish otoliths indicated P ant-

arcticum as the most eaten prey throughout the investigated

period The abundance of Antarctic silverfish remains

identified in this study agrees with previous paleodietary

investigations in the Antarctica Peninsula East Antarctica

and in the southern Ross Sea region (Emslie and McDaniel

2002 McDaniel and Emslie 2002 Polito et al 2002

Emslie and Woehler 2005) 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 50ndash75 by mass to the Adelie penguin diet even

exceeding crystal krill (E crystallorophias) consumption

in the southern Ross Sea (Ainley 2002 Ainley et al 2003)

Only a very low percentage of remains belongs to other

fish genera The interspecific variation in samples found

exclusively at southern latitudes was probably a conse-

quence of the fact that those samples composed 866 of

the total and contained 96 of the recovered otoliths The

low percentage of occurrence of lsquolsquoother speciesrsquorsquo in our

samples is not surprising Adelie penguins primarily forage

in the continental shelf waters surrounding Antarctica

which are characterized by a very low ichthyic biodiversity

(cfr Ainley 2002) Most unidentifiable fish otoliths

retrieved in the older guano samples maybe related to

sediment transformation processes (such as pedogenesis

and diagenesis) However since many of the best-pre-

served P antarcticum otoliths come from the older guano

samples preservation factors appear here to be related

more to acidic digestion processes rather than to the sample

age or to erosion action through time This is also

supported by the dry and cold condition of Antarctic

environment where the arid climate and low temperatures

slow the damage action of soil processes on organic

remains

Latitude did not significantly affect the mean relative

abundance of Antarctic silverfish indicating that in the past

this species represented an important food source for

penguin breeding throughout the VL coast This prey

species has fluctuated in importance over the past

6000 years (Fig 3) This pattern seems to agree with Hall

et al (2006) who delineated the Adelie penguin and ele-

phant seal occupation history for the VL coast Decreasing

periods of silverfish remains in the present study (Fig 3

1000ndash2000 and 5000ndash6000 BP) correspond approximately

to the seal optimum (1100ndash2300 BP) and to the coeval

occupation (ie contemporary occupation by both species)

(4000ndash6000 BP) reported by Hall et al (2006) Both of

these periods were characterized by a sea ice decrease in

the Ross Sea particularly severe during the most recent

period On the other hand our data show an increase in the

silverfish remains abundance in the past 1000 years and

during the lsquolsquopenguin optimumrsquorsquo this latter being the highest

value among all the investigated periods The lsquolsquopenguin

optimumrsquorsquo and the most recent ages were characterized by

higher sea ice in the Ross Sea region producing a more

fitting habitat for the sea ice obligate Adelie penguin (Hall

et al 2006) The shifts in the presence of fish remains and

in particular of P antarcticum might also represent chan-

ges in Antarctic silverfish population according to the sea

ice advance and retreat (Eastman 1993) Zane et al (2006)

used mitochondrial DNA sequencing to hypothesize that a

demographic expansion that occurred for P antarcticum

during a cooling period (last glaciation peak 111000ndash

126000 BP) suggesting a strong link between this species

(and its prey cfr Smetacek and Nicol 2005) and paleo-

climatic regime shifts

Nevertheless Antarctic silverfish is characterized by a

strong trophic flexibility and adaptability (Eastman 1993

Zane et al 2006) and at present compose the main part of

the diet of marine predators which are also ice-avoiding

species that prefer open water such as elephant seals

(Daneri and Carlini 2002) For this reason we hypothesize

that rather than indicating a decrease in silverfish avail-

ability the shifts in abundance of P antarcticum in the

present study could reflect a higher number of fish remains

in samples as a consequence of a higher number of birds

attending the colonies during periods with more sea ice

Prey size selection

Despite their dense structures fish otoliths are exposed to

variable mechanical and chemical abrasions on calcium

carbonate in the digestive tracts of predators The

Polar Biol

123

susceptibility of fish otoliths (and bones) to digestive ero-

sion appears to change widely taxon by taxon (Harkonen

1986 Pierce et al 1993 Tollit et al 1997) Furthermore in

the ornithogenic soils continuous freezethaw action

through time and sediment transformation processes can

contribute to the consumption and damage of otoliths

These erosive processes act on otolith morphological fea-

tures and size and can lead to non-detection of some prey

categories or of some individuals in a prey category and to

underestimation of prey body size Nevertheless the rela-

tive frequency and size of prey estimated from the hard

remains found in guano samples are valuable and are very

likely the only available information on the kind of prey

consumed

Juvenile P antarcticum with a 40ndash80 mm standard

length range (conforming to juvenile age classes 1 and

2 Hubold and Tomo 1989) are the most-represented

individuals in the VL sediments McDaniel and Emslie

(2002) recognized this prevalence in Northern Marguerite

Bay (Antarctic Peninsula) although with a wider value

range (1582ndash1874 mm) and higher mean SL (10819 plusmn

2553 mm) Juvenile P antarcticum occur primarily at

depths of 50ndash400 m and are well accessible to penguin

capture since their normal foraging depths range between 3

and 98 m (Chappell et al 1993) When analyzing the

temporal distribution of P antarcticum SL significant

differences were not found throughout the investigated

period In Northern Marguerite Bay (Antarctic Peninsula)

(McDaniel and Emslie 2002) some variations within mean

silverfish SL have been recognized among different time

periods but these did not result in a predictable temporal

pattern in accord with past climate change although

Holocene climatic environmental changes are well docu-

mented in both the Antarctic Peninsula and the Ross Sea

region (Bjorck et al 1996 Ingolfsson et al 1998 Baroni

and Orombelli 1991 1994b Baroni and Hall 2004 Hall

et al 2004 2006) The absence of temporal variations of

the silverfish size over the past 7000 years reflects a cer-

tain stability in penguin foraging habits which is also

confirmed by modern diet data on the species predated (crf

Ainley 2002) and on the prey size (Olmastroni et al 2004a

b) No significant temporal variation in prey size was

found The significant difference in silverfish mean size

between the northern and southern colonies was not due to

the amount of older thus more eroded otoliths in the

southern samples In fact the percentage of recent otoliths

for the north and south colonies remains very similar for

the 0ndash1000 period (20 and 1967) and furthermore

northern samples contain higher percentages of older

(period 4000ndash6000) otoliths with respect to the south area

(6713 and 4806 respectively) Therefore although the

difference accounts only for a mean value of 511 mm we

can hypothesize that at least in the past penguins breeding

in colonies located north of the Drygalski ice tongue were

feeding on slightly larger Antarctic silverfish

Sample without fish remains are they evidence

of a dietary shift

Although fish otoliths and bones regularly occur in the

analyzed ornithogenic sediments some guano samples did

not provide any kind of dietary remains Polito et al (2002)

reported the occurrence of feathers in Cape Bird organic

levels without dietary remains which may reflect their

deposition at the time when the area was used by penguin

only to molt and not to nest Stratigraphic and geomor-

phologic features of our samples indicate their nesting site

origin confirmed by the presence of eggshell fragments

collected at the same level suggesting that penguins were

nesting A small number of breeding penguins could be

responsible for the paucity of remains or erosion processes

may have accounted for otolith loss We can also hypoth-

esize that the lack of prey remains could be a shift to a

prevalent non-fish diet Considering in fact that krill is not

maintained in the soils guano samples without fish remains

could reflect a tendency towards a prevalent krill-based

paleodiet At present time Adelie penguin diet switching

between fish and krill may reflect changes in the foraging

setting in relation to environmental and ecological features

Several authors indicated particular climate and marine

conditions (ie sea-ice extension and persistence) as cause

of penguin dietary fluctuation between fish and krill

(Ainley et al 1998 Olmastroni et al 2000 cfr Ainley

2002 Ainley et al 2003) But Ainley et al (2006) in a

more recent study suggested also that feeding competition

among penguins and cetaceans rather than change in

sea-ice cover can better explain the annual switch in the

penguinsrsquo prey items

If the temporal distribution of DR samples versus NDR

ones revealed no significant differences some consider-

ations on their spatial distribution could be made In certain

locations including Inexpressible Island Cape Hickey and

Depot Island NDR guano samples prevail over those

containing fish remains (Table 1) In these cases particular

local marine conditions or other ecological factors as well

as foraging competition with other predators could have

resulted in different krill availability andor consumption

(cfr Ainley et al 2006) Occurring in earlier periods at

Inexpressible Island (5058ndash3900 BP) and later at Cape

Hickey (4075ndash1985 BP) and at Dunlop Island (3100ndash2020

BP) it is not possible to define a common paleoenviron-

mental factor that explains this pattern at the regional scale

At Inexpressible Island for example between 6000 and

4000 BP Adelie penguins shared ice-free coastal terrain

with elephant seals (Hall et al 2006) Thus it is possible

that in this area feeding competition due to this coeval

Polar Biol

123

occupation led penguins to change their diet by targeting

primarily krill which may be eaten only occasionally by

elephant seals (Daneri and Carlini 2002 van den Hoff et al

2003) Even if not revealed by the spatial and temporal

distribution of our samples different sea ice regimes

(Olmastroni et al 2004a b) andor mega icebergs calving

(Arrigo et al 2002) might have had an effect at local scale

These events in fact are known to play an important role on

penguin life cycle and they have been reported to occur in

the past (cfr Shepherd et al 2005)

Although Holocene climatic and environmental changes

have clearly affected the VL coast as indicated by Adelie

penguin colonization history (Baroni and Orombelli

1994a Lambert et al 2002 Emslie et al 2003 Hall et al

2006) over the past 7000 years the Ross Sea ecosystem

seemed to be a relatively stable ecosystem with P ant-

arcticum being the most important fish component in the

Adelie penguin diet for several thousand years The

present study provides the most detailed Adelie penguin

paleodiet records for this area These records may supply

new insights into the past feeding penguin behavior in

the VL coastal area and on a larger scale about the

ecological conditions of the Ross Sea ecosystem during

the Holocene

Acknowledgments This work was executed within the framework

of the Italian National Program on Antarctic Research (PNRA) and

was financially supported by joint research programs in geology at

the University of Pisa The authors thank Fabrizio Ciampolini

(University of Siena) for scanning electron micrographs Silvano

Focardi head of the laboratories at the Department of Environ-

mental Science (University of Siena) where the morphometric

analyses were performed David Lambert Grant Ballard and one

anonymous referee greatly improved an earlier version of the

manuscript

References

Ainley DG (2002) The Adelie penguin bellwether of climate change

Columbia University Press New York

Ainley DG Wilson PR Barton KJ Ballard G Nur N Karl B (1998)

Diet and foraging effort of Adelie penguins in relation to pack-

ice conditions in the southern Ross Sea Polar Biol 20311ndash319

doi101007s003000050308

Ainley DG Ballard G Barton KJ Karl BJ Rau GH Ribic CA

Wilson PR (2003) Spatial and temporal variation of diet within a

presumed metapopulation of Adelie penguins Condor 10595ndash

106 doi1016500010-5422(2003)105[95SATVOD]20CO2

Ainley DG Ballard G Dugger KM (2006) Competition among

penguins and cetaceans reveals trophic cascade in the Western

Ross Sea Antarctica Ecology 872080ndash2093 doi1018900012-

9658(2006)87[2080CAPACR]20CO2

Arrigo KR van Dijken GL Ainley DG Fahnestock MA Markus T

(2002) Ecological impact of a large Antarctic iceberg Geophys

Res Lett 291104 doi1010292001GL014160

Baroni C (1994) Notes on late-glacial retreat of the Antarctic ice sheet

and Holocene environmental changes along the Victoria Land

Coast Mem Natl Inst Polar Res (Jpn) C 5085ndash107

Baroni C Hall BL (2004) A new Holocene relative sea-level curve for

Terra Nova Bay Victoria Land Antarctica J Quat Sci 19377ndash

396 doi101002jqs825

Baroni C Orombelli G (1991) Holocene raised beaches at Terra

Nova Bay Victoria Land Antartica Quat Res 36157ndash177

doi1010160033-5894(91)90023-X

Baroni C Orombelli G (1994a) Abandoned penguin rookeries

as Holocene paleoclimatic indicators in Antarctica Geology

2223ndash26 doi1011300091-7613(1994)0220023APRAHP[23CO2

Baroni C Orombelli G (1994b) Holocene glacier variations in Terra

Nova bay area (Victoria Land Antartica) Antarct Sci 6497ndash

505 doi101017S0954102094000751

Barrett JE Virginia RA Hopkins DW Aislabie J Bargagli R

Bockheim JG Campbell IB Lyons WB Moorhead DL Nkem

JN Sletten RS Steltzer H Wall DH Wallenstein MD (2006)

Terrestrial ecosystem processes of Victoria Land Antarctica

Soil Biol Biochem 383019ndash3034 doi101016jsoilbio2006

04041

Berkman PA Forman SL (1996) Pre-bomb radiocarbon and the

reservoir correction for calcareous marine species in the

Southern Ocean Geophys Res Lett 23363ndash366 doi101029

96GL00151

Bjorck S Hakansson H Olsson S Ellis-Evans C Humlum O Lirio

JM (1996) Late Holocene palaeoclimatic records from lakes

sediments on James Ross Island Antarctica Palaeogeogr

Palaeoclimatol Palaeoecol 113195ndash220 doi1010160031-

0182(95)00086-0

Bochenski Z (1985) Remains of subfossil birds from King George

Island (South Shetland Islands) Acta Zool Cracov 29109ndash116

Chappell MA Shoemaker VH Janes DN Bucher TL Maloney SK

(1993) Diving behavior during foraging in breeding Adelie

penguins Ecol USA 741204ndash1215

Daneri GA Carlini AR (2002) Fish prey of southern elephant seals

Mirounga leonine at King George Island Polar Biol 25739ndash743

Eastman JT (1993) Antarctic fish biology evolution in a unique

environment Academic Press San Diego

Emslie SD (1995) Age and taphonomy of abandoned penguin

rookeries in the Antarctic Peninsula region Polar Rec (Gr Brit)

31409ndash418

Emslie SD (2001) Radiocarbon dates from abandoned penguin

colonies in the Antarctica peninsula region Antarct Sci

13289ndash295 doi101017S0954102001000414

Emslie SD McDaniel JD (2002) Adelie penguin diet and climate

change during the middle to late Holocene in northern Margue-

rite Bay Antarctic Peninsula Polar Biol 25222ndash229

Emslie SD Patterson WP (2007) Abrupt shift in d13C and d15N

values in Adelie penguin eggshell in Antarctica Proc Natl Acad

Sci USA 10411666ndash11669 doi101073pnas0608477104

Emslie SD Woehler EJ (2005) A 9000-year record of Adelie penguin

occupation and diet in the Windmill Islands East Antarctica

Antarct Sci 1757ndash66 doi101017S0954102005002427

Emslie SD Fraser W Smith RC Walker W (1998) Abandoned

penguin colonies and environmental change in the Palmer

Station area Anvers Island Antarctic Peninsula Antarct Sci

10257ndash268 doi101017S0954102098000352

Emslie SD Berkman PA Ainley DG Coats L Polito M (2003) Late-

Holocene initiation of ice-free ecosystems in the southern Ross

Sea Antarctica Mar Ecol Prog Ser 26219ndash25 doi103354

meps262019

Emslie SD Coats L Licht K (2007) A 45000 year record of Adelie

penguins and climate change in the Ross Sea Antarctica

Geology 3561ndash64 doi101130G23011A1

Hall BL Baroni C Denton GH (2004) Holocene relative sea-level

history of the Southern Victoria Land Coast Antarctica Glob

Planet Chang 42241ndash263 doi101016jgloplacha200309004

Polar Biol

123

susceptibility of fish otoliths (and bones) to digestive ero-

sion appears to change widely taxon by taxon (Harkonen

1986 Pierce et al 1993 Tollit et al 1997) Furthermore in

the ornithogenic soils continuous freezethaw action

through time and sediment transformation processes can

contribute to the consumption and damage of otoliths

These erosive processes act on otolith morphological fea-

tures and size and can lead to non-detection of some prey

categories or of some individuals in a prey category and to

underestimation of prey body size Nevertheless the rela-

tive frequency and size of prey estimated from the hard

remains found in guano samples are valuable and are very

likely the only available information on the kind of prey

consumed

Juvenile P antarcticum with a 40ndash80 mm standard

length range (conforming to juvenile age classes 1 and

2 Hubold and Tomo 1989) are the most-represented

individuals in the VL sediments McDaniel and Emslie

(2002) recognized this prevalence in Northern Marguerite

Bay (Antarctic Peninsula) although with a wider value

range (1582ndash1874 mm) and higher mean SL (10819 plusmn

2553 mm) Juvenile P antarcticum occur primarily at

depths of 50ndash400 m and are well accessible to penguin

capture since their normal foraging depths range between 3

and 98 m (Chappell et al 1993) When analyzing the

temporal distribution of P antarcticum SL significant

differences were not found throughout the investigated

period In Northern Marguerite Bay (Antarctic Peninsula)

(McDaniel and Emslie 2002) some variations within mean

silverfish SL have been recognized among different time

periods but these did not result in a predictable temporal

pattern in accord with past climate change although

Holocene climatic environmental changes are well docu-

mented in both the Antarctic Peninsula and the Ross Sea

region (Bjorck et al 1996 Ingolfsson et al 1998 Baroni

and Orombelli 1991 1994b Baroni and Hall 2004 Hall

et al 2004 2006) The absence of temporal variations of

the silverfish size over the past 7000 years reflects a cer-

tain stability in penguin foraging habits which is also

confirmed by modern diet data on the species predated (crf

Ainley 2002) and on the prey size (Olmastroni et al 2004a

b) No significant temporal variation in prey size was

found The significant difference in silverfish mean size

between the northern and southern colonies was not due to

the amount of older thus more eroded otoliths in the

southern samples In fact the percentage of recent otoliths

for the north and south colonies remains very similar for

the 0ndash1000 period (20 and 1967) and furthermore

northern samples contain higher percentages of older

(period 4000ndash6000) otoliths with respect to the south area

(6713 and 4806 respectively) Therefore although the

difference accounts only for a mean value of 511 mm we

can hypothesize that at least in the past penguins breeding

in colonies located north of the Drygalski ice tongue were

feeding on slightly larger Antarctic silverfish

Sample without fish remains are they evidence

of a dietary shift

Although fish otoliths and bones regularly occur in the

analyzed ornithogenic sediments some guano samples did

not provide any kind of dietary remains Polito et al (2002)

reported the occurrence of feathers in Cape Bird organic

levels without dietary remains which may reflect their

deposition at the time when the area was used by penguin

only to molt and not to nest Stratigraphic and geomor-

phologic features of our samples indicate their nesting site

origin confirmed by the presence of eggshell fragments

collected at the same level suggesting that penguins were

nesting A small number of breeding penguins could be

responsible for the paucity of remains or erosion processes

may have accounted for otolith loss We can also hypoth-

esize that the lack of prey remains could be a shift to a

prevalent non-fish diet Considering in fact that krill is not

maintained in the soils guano samples without fish remains

could reflect a tendency towards a prevalent krill-based

paleodiet At present time Adelie penguin diet switching

between fish and krill may reflect changes in the foraging

setting in relation to environmental and ecological features

Several authors indicated particular climate and marine

conditions (ie sea-ice extension and persistence) as cause

of penguin dietary fluctuation between fish and krill

(Ainley et al 1998 Olmastroni et al 2000 cfr Ainley

2002 Ainley et al 2003) But Ainley et al (2006) in a

more recent study suggested also that feeding competition

among penguins and cetaceans rather than change in

sea-ice cover can better explain the annual switch in the

penguinsrsquo prey items

If the temporal distribution of DR samples versus NDR

ones revealed no significant differences some consider-

ations on their spatial distribution could be made In certain

locations including Inexpressible Island Cape Hickey and

Depot Island NDR guano samples prevail over those

containing fish remains (Table 1) In these cases particular

local marine conditions or other ecological factors as well

as foraging competition with other predators could have

resulted in different krill availability andor consumption

(cfr Ainley et al 2006) Occurring in earlier periods at

Inexpressible Island (5058ndash3900 BP) and later at Cape

Hickey (4075ndash1985 BP) and at Dunlop Island (3100ndash2020

BP) it is not possible to define a common paleoenviron-

mental factor that explains this pattern at the regional scale

At Inexpressible Island for example between 6000 and

4000 BP Adelie penguins shared ice-free coastal terrain

with elephant seals (Hall et al 2006) Thus it is possible

that in this area feeding competition due to this coeval

Polar Biol

123

occupation led penguins to change their diet by targeting

primarily krill which may be eaten only occasionally by

elephant seals (Daneri and Carlini 2002 van den Hoff et al

2003) Even if not revealed by the spatial and temporal

distribution of our samples different sea ice regimes

(Olmastroni et al 2004a b) andor mega icebergs calving

(Arrigo et al 2002) might have had an effect at local scale

These events in fact are known to play an important role on

penguin life cycle and they have been reported to occur in

the past (cfr Shepherd et al 2005)

Although Holocene climatic and environmental changes

have clearly affected the VL coast as indicated by Adelie

penguin colonization history (Baroni and Orombelli

1994a Lambert et al 2002 Emslie et al 2003 Hall et al

2006) over the past 7000 years the Ross Sea ecosystem

seemed to be a relatively stable ecosystem with P ant-

arcticum being the most important fish component in the

Adelie penguin diet for several thousand years The

present study provides the most detailed Adelie penguin

paleodiet records for this area These records may supply

new insights into the past feeding penguin behavior in

the VL coastal area and on a larger scale about the

ecological conditions of the Ross Sea ecosystem during

the Holocene

Acknowledgments This work was executed within the framework

of the Italian National Program on Antarctic Research (PNRA) and

was financially supported by joint research programs in geology at

the University of Pisa The authors thank Fabrizio Ciampolini

(University of Siena) for scanning electron micrographs Silvano

Focardi head of the laboratories at the Department of Environ-

mental Science (University of Siena) where the morphometric

analyses were performed David Lambert Grant Ballard and one

anonymous referee greatly improved an earlier version of the

manuscript

References

Ainley DG (2002) The Adelie penguin bellwether of climate change

Columbia University Press New York

Ainley DG Wilson PR Barton KJ Ballard G Nur N Karl B (1998)

Diet and foraging effort of Adelie penguins in relation to pack-

ice conditions in the southern Ross Sea Polar Biol 20311ndash319

doi101007s003000050308

Ainley DG Ballard G Barton KJ Karl BJ Rau GH Ribic CA

Wilson PR (2003) Spatial and temporal variation of diet within a

presumed metapopulation of Adelie penguins Condor 10595ndash

106 doi1016500010-5422(2003)105[95SATVOD]20CO2

Ainley DG Ballard G Dugger KM (2006) Competition among

penguins and cetaceans reveals trophic cascade in the Western

Ross Sea Antarctica Ecology 872080ndash2093 doi1018900012-

9658(2006)87[2080CAPACR]20CO2

Arrigo KR van Dijken GL Ainley DG Fahnestock MA Markus T

(2002) Ecological impact of a large Antarctic iceberg Geophys

Res Lett 291104 doi1010292001GL014160

Baroni C (1994) Notes on late-glacial retreat of the Antarctic ice sheet

and Holocene environmental changes along the Victoria Land

Coast Mem Natl Inst Polar Res (Jpn) C 5085ndash107

Baroni C Hall BL (2004) A new Holocene relative sea-level curve for

Terra Nova Bay Victoria Land Antarctica J Quat Sci 19377ndash

396 doi101002jqs825

Baroni C Orombelli G (1991) Holocene raised beaches at Terra

Nova Bay Victoria Land Antartica Quat Res 36157ndash177

doi1010160033-5894(91)90023-X

Baroni C Orombelli G (1994a) Abandoned penguin rookeries

as Holocene paleoclimatic indicators in Antarctica Geology

2223ndash26 doi1011300091-7613(1994)0220023APRAHP[23CO2

Baroni C Orombelli G (1994b) Holocene glacier variations in Terra

Nova bay area (Victoria Land Antartica) Antarct Sci 6497ndash

505 doi101017S0954102094000751

Barrett JE Virginia RA Hopkins DW Aislabie J Bargagli R

Bockheim JG Campbell IB Lyons WB Moorhead DL Nkem

JN Sletten RS Steltzer H Wall DH Wallenstein MD (2006)

Terrestrial ecosystem processes of Victoria Land Antarctica

Soil Biol Biochem 383019ndash3034 doi101016jsoilbio2006

04041

Berkman PA Forman SL (1996) Pre-bomb radiocarbon and the

reservoir correction for calcareous marine species in the

Southern Ocean Geophys Res Lett 23363ndash366 doi101029

96GL00151

Bjorck S Hakansson H Olsson S Ellis-Evans C Humlum O Lirio

JM (1996) Late Holocene palaeoclimatic records from lakes

sediments on James Ross Island Antarctica Palaeogeogr

Palaeoclimatol Palaeoecol 113195ndash220 doi1010160031-

0182(95)00086-0

Bochenski Z (1985) Remains of subfossil birds from King George

Island (South Shetland Islands) Acta Zool Cracov 29109ndash116

Chappell MA Shoemaker VH Janes DN Bucher TL Maloney SK

(1993) Diving behavior during foraging in breeding Adelie

penguins Ecol USA 741204ndash1215

Daneri GA Carlini AR (2002) Fish prey of southern elephant seals

Mirounga leonine at King George Island Polar Biol 25739ndash743

Eastman JT (1993) Antarctic fish biology evolution in a unique

environment Academic Press San Diego

Emslie SD (1995) Age and taphonomy of abandoned penguin

rookeries in the Antarctic Peninsula region Polar Rec (Gr Brit)

31409ndash418

Emslie SD (2001) Radiocarbon dates from abandoned penguin

colonies in the Antarctica peninsula region Antarct Sci

13289ndash295 doi101017S0954102001000414

Emslie SD McDaniel JD (2002) Adelie penguin diet and climate

change during the middle to late Holocene in northern Margue-

rite Bay Antarctic Peninsula Polar Biol 25222ndash229

Emslie SD Patterson WP (2007) Abrupt shift in d13C and d15N

values in Adelie penguin eggshell in Antarctica Proc Natl Acad

Sci USA 10411666ndash11669 doi101073pnas0608477104

Emslie SD Woehler EJ (2005) A 9000-year record of Adelie penguin

occupation and diet in the Windmill Islands East Antarctica

Antarct Sci 1757ndash66 doi101017S0954102005002427

Emslie SD Fraser W Smith RC Walker W (1998) Abandoned

penguin colonies and environmental change in the Palmer

Station area Anvers Island Antarctic Peninsula Antarct Sci

10257ndash268 doi101017S0954102098000352

Emslie SD Berkman PA Ainley DG Coats L Polito M (2003) Late-

Holocene initiation of ice-free ecosystems in the southern Ross

Sea Antarctica Mar Ecol Prog Ser 26219ndash25 doi103354

meps262019

Emslie SD Coats L Licht K (2007) A 45000 year record of Adelie

penguins and climate change in the Ross Sea Antarctica

Geology 3561ndash64 doi101130G23011A1

Hall BL Baroni C Denton GH (2004) Holocene relative sea-level

history of the Southern Victoria Land Coast Antarctica Glob

Planet Chang 42241ndash263 doi101016jgloplacha200309004

Polar Biol

123

occupation led penguins to change their diet by targeting

primarily krill which may be eaten only occasionally by

elephant seals (Daneri and Carlini 2002 van den Hoff et al

2003) Even if not revealed by the spatial and temporal

distribution of our samples different sea ice regimes

(Olmastroni et al 2004a b) andor mega icebergs calving

(Arrigo et al 2002) might have had an effect at local scale

These events in fact are known to play an important role on

penguin life cycle and they have been reported to occur in

the past (cfr Shepherd et al 2005)

Although Holocene climatic and environmental changes

have clearly affected the VL coast as indicated by Adelie

penguin colonization history (Baroni and Orombelli

1994a Lambert et al 2002 Emslie et al 2003 Hall et al

2006) over the past 7000 years the Ross Sea ecosystem

seemed to be a relatively stable ecosystem with P ant-

arcticum being the most important fish component in the

Adelie penguin diet for several thousand years The

present study provides the most detailed Adelie penguin

paleodiet records for this area These records may supply

new insights into the past feeding penguin behavior in

the VL coastal area and on a larger scale about the

ecological conditions of the Ross Sea ecosystem during

the Holocene

Acknowledgments This work was executed within the framework

of the Italian National Program on Antarctic Research (PNRA) and

was financially supported by joint research programs in geology at

the University of Pisa The authors thank Fabrizio Ciampolini

(University of Siena) for scanning electron micrographs Silvano

Focardi head of the laboratories at the Department of Environ-

mental Science (University of Siena) where the morphometric

analyses were performed David Lambert Grant Ballard and one

anonymous referee greatly improved an earlier version of the

manuscript

References

Ainley DG (2002) The Adelie penguin bellwether of climate change

Columbia University Press New York

Ainley DG Wilson PR Barton KJ Ballard G Nur N Karl B (1998)

Diet and foraging effort of Adelie penguins in relation to pack-

ice conditions in the southern Ross Sea Polar Biol 20311ndash319

doi101007s003000050308

Ainley DG Ballard G Barton KJ Karl BJ Rau GH Ribic CA

Wilson PR (2003) Spatial and temporal variation of diet within a

presumed metapopulation of Adelie penguins Condor 10595ndash

106 doi1016500010-5422(2003)105[95SATVOD]20CO2

Ainley DG Ballard G Dugger KM (2006) Competition among

penguins and cetaceans reveals trophic cascade in the Western

Ross Sea Antarctica Ecology 872080ndash2093 doi1018900012-

9658(2006)87[2080CAPACR]20CO2

Arrigo KR van Dijken GL Ainley DG Fahnestock MA Markus T

(2002) Ecological impact of a large Antarctic iceberg Geophys

Res Lett 291104 doi1010292001GL014160

Baroni C (1994) Notes on late-glacial retreat of the Antarctic ice sheet

and Holocene environmental changes along the Victoria Land

Coast Mem Natl Inst Polar Res (Jpn) C 5085ndash107

Baroni C Hall BL (2004) A new Holocene relative sea-level curve for

Terra Nova Bay Victoria Land Antarctica J Quat Sci 19377ndash

396 doi101002jqs825

Baroni C Orombelli G (1991) Holocene raised beaches at Terra

Nova Bay Victoria Land Antartica Quat Res 36157ndash177

doi1010160033-5894(91)90023-X

Baroni C Orombelli G (1994a) Abandoned penguin rookeries

as Holocene paleoclimatic indicators in Antarctica Geology

2223ndash26 doi1011300091-7613(1994)0220023APRAHP[23CO2

Baroni C Orombelli G (1994b) Holocene glacier variations in Terra

Nova bay area (Victoria Land Antartica) Antarct Sci 6497ndash

505 doi101017S0954102094000751

Barrett JE Virginia RA Hopkins DW Aislabie J Bargagli R

Bockheim JG Campbell IB Lyons WB Moorhead DL Nkem

JN Sletten RS Steltzer H Wall DH Wallenstein MD (2006)

Terrestrial ecosystem processes of Victoria Land Antarctica

Soil Biol Biochem 383019ndash3034 doi101016jsoilbio2006

04041

Berkman PA Forman SL (1996) Pre-bomb radiocarbon and the

reservoir correction for calcareous marine species in the

Southern Ocean Geophys Res Lett 23363ndash366 doi101029

96GL00151

Bjorck S Hakansson H Olsson S Ellis-Evans C Humlum O Lirio

JM (1996) Late Holocene palaeoclimatic records from lakes

sediments on James Ross Island Antarctica Palaeogeogr

Palaeoclimatol Palaeoecol 113195ndash220 doi1010160031-

0182(95)00086-0

Bochenski Z (1985) Remains of subfossil birds from King George

Island (South Shetland Islands) Acta Zool Cracov 29109ndash116

Chappell MA Shoemaker VH Janes DN Bucher TL Maloney SK

(1993) Diving behavior during foraging in breeding Adelie

penguins Ecol USA 741204ndash1215

Daneri GA Carlini AR (2002) Fish prey of southern elephant seals

Mirounga leonine at King George Island Polar Biol 25739ndash743

Eastman JT (1993) Antarctic fish biology evolution in a unique

environment Academic Press San Diego

Emslie SD (1995) Age and taphonomy of abandoned penguin

rookeries in the Antarctic Peninsula region Polar Rec (Gr Brit)

31409ndash418

Emslie SD (2001) Radiocarbon dates from abandoned penguin

colonies in the Antarctica peninsula region Antarct Sci

13289ndash295 doi101017S0954102001000414

Emslie SD McDaniel JD (2002) Adelie penguin diet and climate

change during the middle to late Holocene in northern Margue-

rite Bay Antarctic Peninsula Polar Biol 25222ndash229

Emslie SD Patterson WP (2007) Abrupt shift in d13C and d15N

values in Adelie penguin eggshell in Antarctica Proc Natl Acad

Sci USA 10411666ndash11669 doi101073pnas0608477104

Emslie SD Woehler EJ (2005) A 9000-year record of Adelie penguin

occupation and diet in the Windmill Islands East Antarctica

Antarct Sci 1757ndash66 doi101017S0954102005002427

Emslie SD Fraser W Smith RC Walker W (1998) Abandoned

penguin colonies and environmental change in the Palmer

Station area Anvers Island Antarctic Peninsula Antarct Sci

10257ndash268 doi101017S0954102098000352

Emslie SD Berkman PA Ainley DG Coats L Polito M (2003) Late-

Holocene initiation of ice-free ecosystems in the southern Ross

Sea Antarctica Mar Ecol Prog Ser 26219ndash25 doi103354

meps262019

Emslie SD Coats L Licht K (2007) A 45000 year record of Adelie

penguins and climate change in the Ross Sea Antarctica

Geology 3561ndash64 doi101130G23011A1

Hall BL Baroni C Denton GH (2004) Holocene relative sea-level

history of the Southern Victoria Land Coast Antarctica Glob

Planet Chang 42241ndash263 doi101016jgloplacha200309004

Polar Biol

123

Hall BL Hoelzel AR Baroni C Denton GH Le Boeuf BJ Overturf

B Topf AL (2006) Holocene elephant seal distribution implies

warmer-than-present climate in the Ross Sea Proc Natl Acad Sci

USA 10310213ndash10217 doi101073pnas0604002103

Harkonen TJ (1986) Guide to the Otoliths of the Bony Fishes of the

Northeast Atlantic Danbui ApS Hellerup p 256

Heine JC Speir TW (1989) Ornithogenic soils of the Cape Bird

Adelie penguin rookeries Antarctica Polar Biol 1089ndash99 doi

101007BF00239153

Hubold G Tomo AP (1989) Age and growth of Antarctic Silverfish

Pleuragramma antarcticum Boulanger 1902 from the southern

Weddell Sea and Antarctica Peninsula Polar Biol 9205ndash212

doi101007BF00263768

Ingolfsson O Hjort C Berkman PA Bjorck S Colhoun E Goodwin

ID Hall B Hirakawa K Melles M Moller P Prentice ML

(1998) Antarctic glacial history since the last glacial maximum

an overview of the record on land Antarct Sci 10326ndash344 doi

101017S095410209800039X

La Mesa M Eastman JT Vacchi M (2004) The role of notothenioid

fish in the food web of the Ross Sea shelf waters a review Polar

Biol 27321ndash338 doi101007s00300-004-0599-z

Lambert DM Ritchie PA Millar CD Holland B Drummond AJ

Baroni C (2002) Rates of evolution in ancient DNA from Adelie

penguins Science 2952270ndash2273 doi101126science1068105

Leopold M Van Damme C Van Der Veer H (1998) Diet of

cormorants and the impact of cormorant predation on juvenile

flatfish in the Dutch Wadden Sea J Sea Res 4093ndash107 doi

101016S1385-1101(98)00028-8

Liu X Li H Sun L Yin X Zhao S Wang Y (2006) d13C and d15N in

the ornithogenic sediments from the Antarctic maritime as

palaeoecological proxies during the past 2000 year Earth Planet

Sci Lett 243424ndash438 doi101016jepsl200601018

Lorius C Jouzel J Ritz C Merlivat L Barkov NI Korotkevich YS

Kotlyakov VM (1985) A 150000-year climatic record from

Antarctic ice Nature 316591ndash596 doi101038316591a0

McDaniel JD Emslie SD (2002) Fluctuations in Adelie penguin prey

size in the mid to late Holocene northern Marguerite Bay

Antarctic Peninsula Polar Biol 25618ndash623

Michel RFM Schaefer CEGR Dias LE Simas FNB de Melo Benites

V de Sa Mendonca E (2006) Ornithogenic Gelisols (Cryosols)

from Maritime Antarctica pedogenesis vegetation and carbon

studies Soil Sci Soc Am J 701370ndash1376 doi102136sssaj

20050178

Olmastroni S Corsolini S Pezzo F Focardi S Kerry K (2000) The

first 5 years of ItalianndashAustralian joint programme on the Adelie

penguin an overview Ital J Zool (Modena) 67(supplement 1)

141ndash145 doi10108011250000009356369

Olmastroni S Pezzo F Bisogno I Focardi S (2004a) Interannual

variation in the summer diet of Adelie penguin (Pygoscelisadeliae) at Edmonson Point CCAMLR working group on

ecosystem monitoring and management WG-EMM 0438 Siena

12ndash23 July 2004

Olmastroni S Pezzo F Volpi V Focardi S (2004b) Effects of weather

and sea-ice on the reproductive performance of the Adelie

penguins at Edmonson Point Ross Sea CCAMLR Sci 1199ndash

109

Petit JR Basile I Leruyuet A Raynaud D Lorius C Jouzel J

Stievenard M Lipenkov VY Barkov NI Kudryashov BB Davis

M Saltzman E Kotlyakov V (1997) Four climate cycles in

Vostok ice core Nature 387359ndash360 doi101038387359a0

Pierce GJ Boyle PR Watt J Grisley M (1993) Recent advances in

diet analysis of marine mammals Symp Zool Soc Lond 66241ndash

261

Polito M Emslie SD Walker W (2002) A 1000-year record of Adelie

penguin diets in the southern Ross Sea Antarct Sci 14327ndash332

doi101017S0954102002000184

Shepherd LD Millar CD Ballard G Ainley DG Wilson PR Haynes

GD Baroni C Lambert DM (2005) Microevolution and mega-

icebergs in the Antarctic Proc Natl Acad Sci USA 10216717ndash

16722 doi101073pnas0502281102

Simas FNB Schaefer CEGR Melo VF Albuquerque-Filho MR

Michel RFM Pereira VV Gomes MRM da Costa LM (2007)

Ornithogenic cryosols from maritime Antarctica phosphatiza-

tion as a soil forming process Geoderma 138191ndash203 doi

101016jgeoderma200611011

Smetacek V Nicol S (2005) Polar ocean ecosystems in a changing

world Nature 437362ndash368 doi101038nature04161

Speir TW Cowling JC (1984) Ornithogenic soils of the Cape Bird

Adelie penguin rookeries Antarctica 1 Chemical properties

Polar Biol 2199ndash205 doi101007BF00263625

Spellerberg IF (1970) Abandoned penguin colonies near Cape Royds

Ross Island Antarctica and 14C dating of penguin remains N Z

J Sci 13380ndash385

Stonehouse B (1970) Recent climatic change in Antarctica suggested

from 14C dating of penguin remains Palaeogeogr Palaeoclimatol

Palaeoecol 7(34)1ndash343

Syroechkovsky EE (1959) The role of animals in primary soil

formation under conditions of pre-polar region of the globe

(exemplified by the Antarctic) Zool J 381770ndash1775

Tabachnick BG Fidell LS (1996) Using multivariate statistics Harper

Collins New York

Tatur A Myrcha A (1989) Soils and vegetation in abandoned penguin

rookeries (maritime Antarctic) Polar Biol 2181ndash189

Tollit DJ Steward MJ Thompson PM Pierce GJ Santos MB Hughes

S (1997) Species and size differences in the digestion of otoliths

and beaks implications for estimates of pinniped diet compo-

sition Can J Fish Aquat Sci 54105ndash119 doi101139

cjfas-54-1-105

Ugolini FC (1972) Ornithogenic soils of Antarctica In Llano GA

(ed) Antarctic terrestrial biology Am Geophys Union Antarct

Res Ser 20181ndash193

Vacchi M La Mesa M Dalu M Macdonald J (2004) Early life stages

in the life cycle of Antarctic silverfish Pleuragramma antarct-icum in Terra Nova Bay Ross Sea Antarct Sci 16299ndash305 doi

101017S0954102004002135

van den Hoff J Burton H Davies R (2003) Diet of male southern

elephant seals (Mirounga leonina L) hauled out at Vincennes

Bay East Antarctica Polar Biol 2627ndash31

Williams R McEldowney A (1990) A guide to the fish otoliths from

waters off the Australian Antarctic Territory Heard and Macquire

Islands ANARE Res Notes 75 Antarctic Division Australia

Zane L Marcato S Bargelloni L Bortolotto E Papetti C Simonato

M Varotto V Patarnello T (2006) Demographic history and

population structure of the Antarctic silverfish Pleuragrammaantarcticum Mol Ecol 154499ndash4511 doi101111j1365-294X

200603105x

Zhu R Sun L Yin X Xie Z Liu X (2005) Geochemical evidence for

rapid enlargement of a gentoo penguin colony on Barton

Peninsula in the maritime Antarctic Antarct Sci 1711ndash16 doi

101017S0954102005002373

Polar Biol

123