doi:10.3402/polar.v34.25718


R E S E A R C H / R E V I E W A R T I C L E

Haematological values of three Antarctic penguins:
gentoo (Pygoscelis papua), Adélie (P. adeliae) and
chinstrap (P. antarcticus)
Andrés E. Ibañez,1 Roberto Najle,2 Karen Larsen,2 Marcela Pari,3 Amalia Figueroa3 & Diego Montalti1

1
Ornithology Section, Vertebrate Zoology Division, Faculty of Natural Sciences and Museum, La Plata National University, Paseo del Bosque s/n,

B1900FWA-La Plata, Buenos Aires, Argentina
2

Laboratory of Cellular Biology, Faculty of Veterinary Sciences, Centro de la Provincia de Buenos Aires National University, B7000GHG Tandil,

Buenos Aires, Argentina
3

Laboratory of Clinical and Biochemical Analysis, Interzonal Hospital Luisa C. de Gandulfo, B1832GVK Lomas de Zamora, Buenos Aires, Argentina

Keywords

Antarctic; haematology; physiology;

Pygoscelis; penguins; serum biochemistry.

Correspondence

Andrés E. Ibañez, Ornithology

Section, Vertebrate Zoology Division,

Faculty of Natural Sciences and Museum,

La Plata National University, Paseo del

Bosque s/n, B1900FWA-La Plata,

Buenos Aires, Argentina.

E-mail: aeibanez@fcnym.unlp.edu.ar

Abstract

It is established that haematological and biochemical parameters provide im-

portant data to assess the physiological condition and health status of wild

birds. To undertake conservation physiology or ecophysiology work, it is

therefore essential to establish baseline physiological parameters and how

these parameters change with age and life history events. In this work, we

determined and compared baseline haematology and serum biochemistry

between adults and chicks of three Antarctic penguin species of the genus

Pygoscelis: gentoo (P. papua), Adélie (P. adeliae) and chinstrap (P. antarcticus).

Differences in adults among species were observed in haemoglobin and

biochemical parameters such as total proteins, glucose and alkaline phospha-

tase activity. In addition, differences between adults and chicks in haematocrit,

haemoglobin, total proteins and glucose concentration were determined.

Moreover, we evaluated the electrophoretic protein profiles between adults

and chicks of the genus Pygoscelis, and a conserved protein pattern was

observed among species and ages in the genus. Altogether, the results suggest

that biochemical and haematological differences among pygoscelids may be

related to the nutritional status and energetic expenditure during breeding as

well as their feeding habits and development stage.

Haematology and plasma or serum biochemical para-

meters can provide extremely important information

about health status and autecology of free-living verte-

brates (Balasch et al. 1974; Cooke et al. 2013). These

analyses consider current nutritional, immune and stress

status, but also different seasonal processes related with

moult and breeding behaviour. Increasing evidence

indicates that specific responses against environmental

factors may be taxon specific (Cooke et al. 2013). The

determination of these parameters provides information

about the longer-term physiological and ecological pro-

cesses affecting individuals or populations (Ardia 2006).

In a nutritional context, body condition typically refers to

vertebrates’ stored fat (and protein) reserves (Schulte-

Hostedde et al. 2005), which are critical in many acti-

vities and processes influencing fitness, such as long-

distance migration and reproductive success (Lill et al.

2013). Therefore, establishing reference values and how

these values change with age and different life history

events is essential for future conservation efforts.

Migratory birds are exposed to extreme metabolic

demands that, together with other factors, such as envi-

ronmental pollution, stressful situations, physical activity,

quality and availability of food resources or health status,

can induce changes in plasma biochemistry and haema-

tology (Sturkie & Griminger 1986; Studds & Marra 2005).

Furthermore, all these factors together with human

disturbance in breeding sites can limit the individual’s

condition, impeding its ability to migrate, breed and

survive (Studds & Marra 2005; Carlini et al. 2007).

Polar Research 2015. # 2015 A.E. Ibañez et al. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0
International License (http://creativecommons.org/licenses/by-nc/4.0/), permitting all non-commercial use, distribution, and reproduction in any medium, provided the
original work is properly cited.

1

Citation: Polar Research 2015, 34, 25718, http://dx.doi.org/10.3402/polar.v34.25718

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Antarctic birds are important members of the Antarctic

ecosystem, in terms of total biomass and of interaction

with the environment. Of particular importance are the

penguins, including the three species of the genus

Pygoscelis: gentoo (P. papua), Adélie (P. adeliae) and chin-

strap (P. antarcticus), whose breeding range extends south

of 608S. In penguins, haematological research has been
carried out mainly on blood respiratory properties (Lenfant

et al. 1969; Milsom et al. 1973; Nicol et al. 1988; Rosa

et al. 1993) and on changes in plasma nutrients and meta-

bolites during fasting in breeding season (Cherel, Leloup

et al. 1988; Cherel, Robin et al. 1988; Ghebremeskel et al.

1989; Ghebremeskel et al. 1991; Ghebremeskel et al.

1992; Merino & Barbosa 1997; Vleck & Vleck 2002).

Notwithstanding the great attention given to penguins

because their special adaptations to environmental con-

ditions, there are little reported data about normal

haematology and plasma biochemistry of members of

the Pygoscelis genus (Merino & Barbosa 1997; Najle et al.

2006). Moreover, comparisons of haematological refer-

ence values of adults and chicks of the genus have not

been reported, although it is well established in other

birds that development and life history play substantial

roles in changing blood chemistry and haematology

(Wolf et al. 1985; Moreira dos Santos Schmidt et al.

2007). It would be of interest to know whether patterns

of haematological ageing observed in other birds are also

seen in penguins, as this group is ecologically divergent

from most of the world’s birds (Williams 1995).

The aim of this study was to establish reference

haematological and blood biochemical parameters of

the three Antarctic pygoscelid penguins*gentoo, Adélie

and chinstrap*using wild birds. In addition, compari-
sons between adults and chicks of three species were

analysed.

Materials and methods

Study area

The study was conducted on Potter Peninsula on King

George Island, South Shetland Islands, Antarctica

(62815’0’’S, 58840’0’’W; Fig. 1). The official site name and
its latitudinal and longitudinal position were obtained

from the SCAR-MarBIN Portal at www.scarmarbin.be/

gazetteer.php?p�details&id�13542. When this work was
carried out (15 December 2010 to 15 February 2011), the

three species were breeding sympatrically and a total of

14 554 pairs of Adélie penguin, 2325 pairs of gentoo

penguin and 265 pairs of chinstrap penguin were

present. Of note, on King George Island there are eight

scientific bases with hundreds of scientists working

throughout the year. Also, ongoing and continual move-

ment of aircraft and ships in the area has the potential to

contribute to the anthropogenic effects in these zones

(Rakusa-Suszczewski 1998; Vodopivez & Curtosi 1998;

dos Santos et al. 2005).

Sample collection

Blood samples were collected by venipuncture of the

brachial vein from adults (26 gentoos, 18 Adélies and 15

chinstraps) and chicks (17 gentoos, 16 Adélies and 18

chinstraps) of similar age (15�20 days). Peripheral blood

Fig. 1 Study area showing the sampling site, Potter Peninsula in King George Island, South Shetland Islands, Antarctica.

Haematological values of three Antarctic penguins A.E. Ibañez et al.

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www.scarmarbin.be/gazetteer.php?p=details&id=13542
www.scarmarbin.be/gazetteer.php?p=details&id=13542
www.scarmarbin.be/gazetteer.php?p=details&id=13542
www.scarmarbin.be/gazetteer.php?p=details&id=13542
www.scarmarbin.be/gazetteer.php?p=details&id=13542
www.scarmarbin.be/gazetteer.php?p=details&id=13542
www.scarmarbin.be/gazetteer.php?p=details&id=13542
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was obtained using a single 5-ml syringe and a 23-gauge

needle. Blood samples (approximately 3 ml) were taken

immediately, within two minutes after bird capture, to

avoid changes in biochemical and haematological para-

meters due to stress associated to handling (Fowler

1999). Then the sample was divided and deposited in

different test tubes depending on subsequent procedures.

Briefly, 1 ml of fresh blood was used to determine

haematocrit, sedimentation rate, haemoglobin, glucose

and electrolytes. On the other hand, 2 ml of blood were

used to obtain serum. For this, blood was incubated

overnight at 48C and then clotted samples were centri-
fuged for 10 min at 400 � g. Finally, harvested serum was
frozen at �208C until determinations were performed in
the laboratory. In some cases, blood volumes obtained

were small and as a consequence some procedures were

applied to all species, but some were only applied to

gentoo penguins. Haemolysis was not detected in the sera

obtained. During the sample collection, each bird was

banded with a numbered band to avoid re-sampling.

Haematological and biochemical analysis

Haematological and biochemical analyses were carried

out on blood samples obtained from adults and chicks

of gentoo, Adélie and chinstrap penguins. Haematocrit,

haemoglobin, erythrocyte sedimentation, biochemical

metabolites (glucose, total lipid and proteins, urea,

creatinin), alkaline phosphatase activity and ion concen-

tration (Na
�

, K
�

, Cl
�

, Ca
�2

, P
�3

and Mg
�2

) were

measured.

The haematocrit percentage value was determined by

the micromethod, haemoglobin level using the cyan-

methaemoglobin method (Drabkin & Austin 1935) and

the standard sedimentation value of erythrocytes was

calculated in heparinized blood by standing blood verti-

cally in a Westergren pipette for 60 min. Glucose con-

centration was estimated using the ortho-toluidine method

in a spectrophotometer at 505 nm (Nikkila & Hyvärinen

1962). In serum, lipid concentration was determined

using the sulfo-phospho-vanillin method in a spectro-

photometer at 510 nm (Frings & Dunn 1970). Total pro-

teins were quantified by the Lowry method. Electrolyte

concentrations were determined using different assays:

sodium (100�200 mEq/L), chloride (50�150 mEq/L) and
potassium (2�10 mEq/L) with a Konelab 60I Prime
selective ion analyser (Wiener, Rosario, Argentina), cal-

cium (0�10 mg/dl) and magnesium (0�15 mg/dl) with
the colourimetric method (Konelab 60I Prime) and

phosphorus (0�60 mg/dl) with the ultraviolet method
(Konelab 60I prime). Urea, alkaline phosphatase and

creatinine were determined by the chemiluminescence

method using an Architect i1000SR Immunoassay Ana-

lyzer (Abbot Diagnostics, Santa Clara, CA, US). All

determinations were done in triplicate.

Agarose gel electrophoresis

Protein fractions (albumin, a-, b-, g-globulins) and A/G
ratio were studied in serum samples (10 ml) from adults
and chicks. Agarose gel electrophoresis was performed

using a semi-automated Hydrasys device (Sebia Electro-

phoresis, Lisses, France). After that, gels were stained

with 0.2% Amido Schwartz solution. An electrophoretic

profile of each sample was obtained and analysed using

PHORESIS software.

Fig. 2 Haematological values of gentoo (Pygoscelis papua), Adélie (P.

adeliae) and chinstrap (P. antarcticus) penguins. (a) Haematocrit values

are represented as mean (9SE)% of haematocrit in adults (A) and chicks

(C). (b) Mean (9SE) haemoglobin concentration (g/dl) in adult penguins.

Sample sizes are given in brackets. Significance values are represented

by single (pB0.05), double (pB0.01) and triple (pB0.001) asterisks.

A.E. Ibañez et al. Haematological values of three Antarctic penguins

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Statistical analysis

Statistical analysis and plotting were performed using

GraphPad Prism 4 software (GraphPad, San Diego, CA).

Normality and homogeneity of variances were tested

using Kolmogorov-Smirnov and Levene tests. Data were

analysed using one-way ANOVA with Bonferroni’s post-

hoc test. For age comparisons in each species, data were

analysed using a paired t-test. F ratio and t values are

shown in the results, and a p-value less than 0.05 was

considered significant. Results in tables were expressed as

mean9SD, while in bar charts as mean9SE for each

study group.

Results

Haematocrit values from Pygoscelis penguins (adults and

chicks) are shown in Fig. 2a. No differences were

determined in haematocrit values among adult gentoo,

Adélie and chinstrap penguins (gentoo versus Adélie

p �0.320, F �1.443; gentoo versus chinstrap p �0.268,
F �1.732; Adélie versus chinstrap p �0.188, F �2.371).
In contrast, differences were found when comparing

adults and chicks. Haematocrit values in adult gentoo,

Adélie and chinstrap penguins were 1.33, 1.47 and 1.40

times higher than chicks, respectively (gentoo pB0.001,

t �8.048; Adélie pB0.001, t �6.233; chinstrap pB0.001,
t �9.237).

Differences in haemoglobin concentration were ob-

served among species in adults. Gentoo showed higher

values than the other species (gentoo versus Adélie

p �0.038, F �6.714; gentoo versus chinstrap p �0.0097,

F �13.429; Fig. 2b). In the case of gentoos, haemoglobin
value was also determined in chicks (20.7 g/dl 91.6) and

the results indicated significantly higher values in adults

(pB0.001; t �7.562). In addition, the erythrocyte sedi-
mentation rate in adult gentoo penguins was 1.45 mm/h

after 60 min.

Statistically significant differences in serum glucose

concentration were found among species. Chinstrap

penguins showed higher values than the other species

under study (versus Adélie p �0.0018, F �28.37; versus
gentoo p�0.0008, F�39.69), while glucose level in Adélie
was higher than in gentoo (p �0.0009, F �35.14). Mea-
sured total lipid concentrations showed no differences

(Table 1).

Gentoo adult penguins showed higher protein concen-

tration than Adélie and chinstrap (p �0.026, F�8.238).
Furthermore, age variation in this parameter was found

in gentoo and chinstrap penguins, being higher in adults

(gentoo adults versus chicks pB0.01, t �3.149; chinstrap
adults versus chicks pB0.001, t �4.92; Table 1).

Reference serum metabolites (urea, creatinin, alkaline

phosphatase, sodium, potassium, chloride, calcium, phos-

phorus and magnesium) for the three Pygoscelis penguin

species are shown in Table 1.

The serum protein electrophoretic profile was deter-

mined in the species studied in this work in adults and

chicks. In all cases, proteins were scattered at least in four

peaks corresponding to albumin (Alb), a-globulins (a1
and a2), b-globulin and g-globulin. We did not observe
differences in the serum globulin fraction. In addition,

there was a fusion of a1- and a2-globulin fractions in
samples of the three species, in both adults and chicks.

Table 1 Serum biochemical reference values for gentoo (Pygoscelis papua), Adélie (P. adeliae) and chinstrap (P. antarcticus) penguins. Mean (9 SD)

and sample size (n) of serum biochemistry values are given. Superscript letters a(pB0.05), b(pB0.01) and c(pB0.001) indicate statistically significant

differences between species, and single (pB0.05), double (pB0.01) and triple (pB0.001) asterisks indicate significant differences between ages.

nd: not determined.

Gentoo Adélie Chinstrap

Adults Chicks Adults Chicks Adults Chicks

(n) 22 17 21 16 18 18

Serum biochemistry Mean9SD Mean9SD Mean9SD

Proteins (g/dl) 3.7190.42
a,

** 2.4790.74 4.3990.6 4.2090.43 3.4691.1
a,

*** 2.2090.87

Lipids (g/l) 8.391.7 nd 7.990.8 nd 8.390.9 nd

Glucose (mg/dl) 201.2921
c,

* 193.0920.71 285.6946
b

nd 321.3915.3
b,c,

*** 227912.86

Urea (mg/dl) 10.592.12a 11.2592.5 15.890.07a 18.6791.15 1395.65 13.6795.03

Creatinine (mg/dl) 0.4390.05 0.4790.01 0.3390.30 0.5590.09 0.3490.28 0.3890.27

Alk. phosphatase (mg/dl) 108915.56 108.7930.35 120953.55 87.67923.59 7197.07* 138911.31*

Sodium (mEq/l) 142.596.36 15299.055 130920.22 141.795.68 164.7930.6 151.791.52

Potassium (mEq/l) 2.590.42b 3.5790.25 19.0591.76b 15.8793.33 6.2392.09b 2.790.34

Chloride (mEq/l) 98.593.53 114.3912.09 125.394.04 11790 131.3938.7 11194.35

Calcium (mg/dl) 3.291.41 3.4290.80 5.291.31 3.5391.01 3.2392.04 3.7691.00

Phosphorus (mg/dl) 5.3590.21
b

4.8591.34 13.0492.67
b

16.893.1 5.2391.66 4.5390.32

Magnesium (mg/dl) 2.290.28 1.4590.62 2.2690.30 2.290.34 1.490.98 1.5690.58

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Finally, the A/G ratio was similar among pygoscelid

adults and lower than chicks (Fig. 3, Table 2).

Discussion

Haematocrit values determined for the three Pygoscelis

species were similar to those previously described for

these penguins and other migratory birds (Milsom et al.

1973; Myrcha & Kostelecka Myrcha 1980). No differ-

ences were observed in haematocrit among adults, but

significant age-related differences were identified. This

agrees with the observation that haematocrit value is

different for each stage of development, and is associated

with physiological processes such as haematopoiesis,

which occurs during late embryonic growth and the

early post-hatching period. As young animals grow, there

is a trend to raise the production of red blood cells, which

increases haematocrit value (Fair et al. 2007). Haemo-

globin values were similar to those previously reported

for pygoscelids (Milsom et al. 1973). Gentoo penguins

showed higher haemoglobin levels in comparison with

Adélie and chinstrap, potentially related to gentoo

penguins being able to dive deeper distances for longer

periods than the other species (Williams 1995). The

adult�chick differences observed in haematological
values (haematocrit and haemoglobin-only in gentoo)

are in line with expectations. Adults should have a higher

oxygen affinity to support adult behaviours such as long

continuous diving and swimming (Culik et al. 1994).

Gentoo penguins showed lower glucose concentration

than Adélie and chinstrap penguins. The glucogenic

mechanisms in gentoo penguin are likely to be important

because of its feeding habits (Aguilera et al. 1993).

Gentoo penguins feed inshore and are deep divers, and

have both greater average prey size and body mass than

the other two species. However, values reported here for

the penguin species were lower than those described

previously (Aguilera et al. 1993).

Lipid concentration is related to nutritional status in

free-living birds (Jenni-Eiermann et al. 2002). Serum

lipid values were similar to those previously described for

these species. In addition, among adult penguins lipids

were similar, and this may be because these species have

the similar diets which are constituted of krill and fish

with high fat content (Reinhardt & Van Vleet 1986;

Williams 1995).

Gentoo penguins showed higher protein concentration

than Adélie and chinstrap penguins, and also age-related

differences were identified in gentoo. In addition, some

studies have found chick birds to have higher protein

levels than adults, whereas others have found the

opposite (Dawson & Bortolotti 1997). This could provide

an avenue for future research as it would be interesting

to know what proteins make up these differences (e.g.,

immunological, homeostatic regulation, growth regula-

tion) and what the ecological and fitness roles are for

changing protein concentrations across ages. Studies of

grown birds have been unable to detect age differences.

Protein electrophoresis is an invaluable diagnostic tool

to assess the avian physiological status by determining

the relative and total amounts of albumin, a-, b-, and g-
globulin fractions. Variations in these fractions are related

to inflammatory processes, age and nutritional status

Fig. 3 Determination of Pygoscelis serum protein fraction by native

agarose gel electrophoresis. Serum samples from gentoo (Pygoscelis

papua), Adélie (P. adeliae) and chinstrap (P. antarcticus) adults and

chicks were assessed in native agarose gel electrophoresis. Using

PHORESIS software, by densitometric analyses four peaks were

determined in each sample corresponding to albumin, a (a1 and a2), b
and g fractions.

Table 2 Blood serum proteins in gentoo (Pygoscelis papua), Adélie (P. adeliae) and chinstrap (P. antarcticus). Values of albumin, a1a2-globulins,
b-globulins, g-globulins and A/G ratio are represented as mean (9SD) protein fraction (%) in adult and chick penguins. Samples sizes are given
in parentheses.

Gentoo Adélie Chinstrap

Adults (3) Chicks (4) Adults (3) Chicks (3) Adults (3) Chicks (3)

Fraction (%) Mean9SD Mean9SD Mean9SD

Albumin 48.6593.18 52.1598.11 48.7391.55 51.1791.92 46.4394.70 54.4592.19

a1a2-Globulins 29.492.82 27.1594.93 31.5392.67 30.993.20 33.1797.55 28.3593.18
b-Globulins 12.5591.20 10.9894.37 12.2391.57 10.4392.21 14.2391.46 11.292.54
g-Globulins 9.490.84 9.7291.67 7.590.0 7.591.65 6.16793.6 692.82
A/G ratio 0.9590.12 1.1390.35 0.9590.05 1.04790.08 0.8790.16 1.1990.10

A.E. Ibañez et al. Haematological values of three Antarctic penguins

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(Grasman et al. 2000). We observed a conserved protein

pattern among Pygoscelis species and ages, which reflects

the close taxonomic relationship of these species. Adults

showed lower A/G ratio values than chicks. This ob-

servation in adults could be a consequence of the ener-

getic costs during breeding, as well because of chronic

infection or acute disease, as was reported by others (Ots

et al. 1998). Moreover, the fusion observed in a1- and a2-
globulin fractions was previously described in gentoo and

Adélie, as a physiologic response to infectious agents and

organic compounds in the environment (Najle et al.

2006).

Interestingly, the baseline biochemical values observed

in this work differ and were lower in comparison with

those previously reported (Aguilera et al. 1993), in

particular concentrations of protein, glucose, urea, crea-

tinine, alkaline phosphatase, electrolytes and protein

fraction patterns. A possible explanation for this is that

serum metabolites or proteins may vary in response to

specific nutritional, pathological or environmental condi-

tions. Supporting our thoughts on this, previous works

reported that in different Antarctic regions where human

activities were significative, modifications in baseline plasma

biochemical parameters and immunoglobulin levels were

induced in Pygoscelis species (Barbosa et al. 2007; Carlini

et al. 2007). Sample collection was performed from breed-

ing colonies on King George Island, a site with high

anthropogenic pressure (Harris 1991; Carlini et al. 2007).

Therefore, we believe that the environment could be

exerting pressure, modifying baseline serum biochemistry

as a physiological adaptation, although further work

comparing King George Island populations with other

less disturbed colonies is needed to confirm this.

In this work, we established haematological and serum

biochemical reference values for wild Antarctic Pygoscelis

adult and chick penguins. While we acknowledge that

sample sizes for some species are small, we consider that

the reference values reported here represent basic

physiological information from which future compari-

sons and interpretations can be made. Altogether, this

information contributes to our knowledge of physiology

and their overall health status of these species. Once

reference values are established, clinical evaluations,

ecological physiology and veterinary care will be im-

proved, and this will substantially aid in future conserva-

tion efforts.

Acknowledgements

The fieldwork was supported by the Argentine Antarctic

Institute, and the protocol of ethical conditions under

which this research was carried out was approved by the

Program of Environmental Management and Tourism

(Argentine Antarctic Institute, Argentine Ministry of

Foreign, International Commerce and Worship). We

also thank the editors and reviewers for their helpful

critiques and comments for improving this manuscript.

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Citation: Polar Research 2015, 34, 25718, http://dx.doi.org/10.3402/polar.v34.25718 7
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http://www.polarresearch.net/index.php/polar/article/view/25718
http://dx.doi.org/10.3402/polar.v34.25718