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The frequency of ingested plastic debris and its effects
on body condition of Short-tailed Shearwater (Puffinus
tenuirostris) pre-fledging chicks in Tasmania, Australia
Hannah R. Cousin
A,C
, Heidi J. Auman
A
, Rachael Alderman
B
and Patti Virtue
A
A
Institute for Marine and Antarctic Studies, University of Tasmania, Private Bag 129, Hobart, Tas. 7001, Australia.
B
Department of Primary Industries, Parks, Water and Environment, GPO Box 44, Hobart, Tas. 7001, Australia.
C
Corresponding author. Email: hrcousin@utas.edu.au, hancuz@bigpond.com
Abstract. In recent years, there have been increasing reports of ingestion of marine plastic debris in seabirds. Our aim was
to assess the frequency and effects of ingested plastic debris in pre-fledging Short-tailed Shearwaters (Puffinus tenuirostris)
in Tasmania. We conducted necropsies of 171 Shearwater chicks, confiscated after illegal poaching, to determine the
presence of plastic debris in the proventriculus and ventriculus. We also examined whether there was a correlation between
body condition (based on body mass and fat-scores) and quantity of plastic ingested (by count and weight). We recorded 1032
ingested plastic particles, consisting of industrial plastic (31%) and user plastic (69%). Most of the Shearwater chicks (96%)
contained plastic debris with a mean of 148.1 mg per bird (s.e. 8.1). Most plastic was found in the ventriculus. Light-coloured
plastic dominated (63.8%), with the rest medium (22.1%) and dark (14.1%) plastics. We found that total mass of ingested
plastic was not significantly related to body condition, or fat-scores or mass individually. Our study highlights the prevalence
of plastic pollution in apparently healthy Shearwater chicks and underscores concern regarding the effects of increasing
marine pollution on a global scale.
Additional keywords: industrial plastic, marine debris, nurdles, plastic colour, plastic pollution, user plastic.
Received 9 September 2013, accepted 9 August 2014, published online 2 February 2015
Introduction
Scientists have documented the effects of plastic pollution on
wildlife since the 1920s (Gudger 1922), with many reports of
effects on marine mammals, seabirds and marine reptiles (Carr
1987; Fowler 1987; Bjorndal et al.1994; Henderson 2001; Cadée
2002; Auman et al.2003; Page et al.2004; Gilman et al.2010;
Carey 2011a). An increasing number of polypropylene- and
polyethylene-based plastic particles, in the form of pre-produc-
tion pellets, known as industrial plastic or nurdles, and fragments
of manufactured plastics, known as user plastic, have been
detected in the marine environment (Rios et al.2007). Because
their size and colour may appear similar to prey species, marine
wildlife may misidentify both nurdles and user-plastic debris as
prey and ingest them accidentally. As the demand for plastic
products increases, particularly for disposable and single-use
items, more debris is likely to infiltrate rivers and oceans (Rios
et al.2007; Barnes et al.2009).
Plastic particles are not only being ingested directly by surface
feeding but also via secondary predation in the food web. Studies
also suggest that ingestion of plastic is more of an inter-gener-
ational event than a singular occurrence, with plastic debris being
transferred to the next generation through parental feeding
(Auman et al.1997; Barbieri 2009; Boerger et al.2010; Carey
2011a).
Procellariformes are likely to ingest plastic owing to their
foraging strategies. Many larger species feed by surface-seizing
(Ryan and Jackson 1987; Auman et al. 1997,2003; Ryan 2008;
Barbieri 2009; Avery-Gomm et al.2012) whereas smaller species
are pursuit feeders (Prince et al.1994; Hedd et al.1997; Huin and
Prince 1997). Several species of shearwater have been recorded
with plastic in their digestive systems, including Wedge-tailed
(Ardenna pacifica), Sooty (Puffinus griseus), Manx (P. puffinus),
Great (P. gravis) and Short-tailed (P. tenuirostris) Shearwaters
(Furness 1983,1985; Vlietstra and Parga 2002; Pierce et al.2004;
Barbieri 2009; Carey 2011a; Tanaka et al.2013; Verlis et al.
2013). The incidence of plastic ingestion in Short-tailed Shear-
waters is one of the highest reported in seabirds (Vlietstra and
Parga 2002).
The Short-tailed Shearwater is an abundant burrow-nesting
species that breeds solely within Australia, mainly on small
islands of Tasmania, and which undertakes a circum-Pacific
migration (Skira 1986; Wooller et al.1990; Bradley et al.
1991). The species is reasonably well studied, with some colonies
studied since 1947 (Bradley et al.1991). Short-tailed Shearwaters
typically breed annually. They begin breeding from 5–8 years of
age and may live for 30 years or more (Wooller et al.1990).
A single egg is laid in November, chicks hatch in January and
have a rearing period of ~2.5 months before fledging in early April
CSIRO PUBLISHING
Emu,2015, 115,6–11
http://dx.doi.org/10.1071/MU13086
Journal compilation BirdLife Australia 2015 www.publish.csiro.au/journals/emu
(Serventy and Curry 1984; Wooller et al.1990; Yamashita et al.
2011). During the breeding period (November–April), the for-
aging range of adult Shearwaters extends from coastal Tasmania
to Antarctic waters (Weimerskirch and Cherel 1998; Carey
2011b; Einoder et al. 2011). During the austral summer, prey
includes both Australian and Antarctic euphausiids as well as fish,
squid and other crustacean species (Hamer et al.1997; Weimers-
kirch and Cherel 1998; Vlietstra and Parga 2002). During the non-
breeding period (May–September), they travel to the North
Pacific Ocean, venturing into the subarctic Bering Sea (Vlietstra
and Parga 2002). Because of their abundance, extensive distri-
bution and frequency of recorded plastic ingestion, Short-tailed
Shearwaters are an ideal indicator species for plastic accumula-
tion in the oceans (Vlietstra and Parga 2002; Avery-Gomm et al.
2012).
Previous studies of ingestion of plastic debris in Procellar-
iiformes have used beachcast birds, for which the cause of death
could not be established and carcasses could not therefore be
considered a healthy subset of the population (Pierce et al.2004;
Barbieri 2009; Carey 2011a). These studies could not, therefore,
determine links between plastic ingestion and health. In our study,
we aimed to determine the amount and frequency of plastic
debris in a large, random sample of healthy pre-fledging Short-
tailed Shearwaters and then investigated whether this affected
their body condition.
Methods
Location
We obtained a sample of 171 Short-tailed Shearwater chicks from
the Clifton Beach colony (–425902200S, 1473101800 E), a coastal
reserve 25 km south-east of Hobart, Tasmania, Australia. Fresh
carcasses taken in opportunistic illegal harvesting were seized by
the Tasmanian Department of Primary Industries, Parks, Water
and Environment in April 2012. Considering the body-weights
(146–698 g) and extent of downy plumage moult (0–95%), we
estimated that the chicks were 3–7 weeks before fledging at the
time of collection (Oka 1989), and therefore deemed them as a
random and healthy sample from the breeding colony.
Dissection
Birds were stored in a freezer at 20C before dissection in
March 2013. Necropsies followed methods outlined in Auman
et al. (1997). We measured wing-chord, percentage of downy
plumage and total body-weight to examine any differences in
morphometric traits that might correlate with the presence and
mass of plastic in birds. Weight was measured on a Masscal scale
(model 323, accuracy 1 g). In cases where carcasses were
beheaded (n= 53), we weighed individual heads of the remaining
chicks and added the average mass to the decapitated specimens.
Wing-chord was measured with a ruler from metacarpal joint to
the end of the tenth primary. We made a visual estimate of the
percentage of downy plumage on the dorsal (including head and
neck) and ventral (including chin and throat), with each side 50%
of the total coverage of downy plumage.
Using surgical scissors, a small horizontal incision was made
just above the cloaca on the ventral side of the body. A cut was
then made up the chest cavity, from posterior to anterior, to access
the digestive tract.
We estimated a pectoral muscle-score of 0–3 (0, no muscle; 1,
low levels of muscle; 2, moderate levels of muscle; 3, well
muscled) and a fat-score of 0–3 (as muscle-score, with 0 = no
fat to 3 = high fat) of both subcutaneousand visceral fat, following
methods of van Franeker (2004). The digestive system was
removed for easier analysis with one cut made just above the
cloaca and a second just under the caudal tip of the heart muscle,
cutting ventrally through the oesophagus. Upon extraction of the
digestive tract, observations were made on the condition of the
liver, heart and lungs; any sign of discolouration or haemorrha-
ging was noted.
Protocol for plastic sampling
Previous studies on seabirds have sampled only the proventric-
ulus and ventriculus; to obtain comparable results, we followed
this protocol, which aligned with the methods of Auman et al.
(1997). These two sections of the stomach were assessed
separately; contents of each were washed with fresh water and
air-dried in a Petri dish. Following Auman et al. (1997), the
proventricular lining was examined for any perforations or
lacerations that may have been caused by the ingested plastic
fragments.
The contents of the proventriculus and ventriculus were
weighed with a Mettler Toledo balance (accuracy 0.0001 g).
Samples were categorised as organic matter, plastics and prey
items. Plastics were then categorised as industrial plastic, user
plastic or other, following Ogi (1990), Vlietstra and Parga (2002)
and Carey (2011a) to allow comparison between this and previ-
ous studies. To determine the prevalence of various colours of
plastics, we initially followed the classifications of colour of
Vlietstra and Parga (2002) and Carey (2011a). However, because
many pieces of plastic did not match these colour categories, we
added 11 colours to the classification: clear, white-yellow, peach,
light green, light blue and pink were added to the light colour
category; orange, olive-green and turquoise were added to the
medium category; and dark grey and dark red-brown were added
to the dark category.
Statistical analyses
Statistical analyses were conducted in R version 2.14.2 (R
Development Core Team 2011) and significance level for all
tests was set at a<0.05. Both non-parametric and parametric tests
were used to assess statistical significance between morphometric
measurements and plastic loads. Pearson’s Chi-square test with
Yate’s continuity correction and log-likelihood ratios (non-
parametric) were used as a precursor to any significance (Vlietstra
and Parga 2002; Yamashita et al.2011), which was later tested
and verified with an analysis of variance (ANOVA) (parametric).
Results
Of the 171 birds, 96% had ingested plastic debris, with a mean
plastic mass of 148.1 mg per bird (s.e. 8.1 mg) or 155.4mg per
bird containing plastic (s.e. 8.0). Seven birds had no plastic within
either the proventriculus or ventriculus. A total of 1032 pieces of
plastic was collected, weighing 25.32 g. On average, each bird
contained 6.03 0.3 (s.e.) pieces of plastic, with a range of 1–30
plastic pieces per bird. Mean body-mass was 503.2 g 6.94 g s.e.
(range 146–698 g), mean wing-chord 26.7 cm 0.09 cm s.e.
Effects of plastic ingestion on body condition Emu 7
(range 21.5–29.0 cm) and mean percentage of downy plumage
was 31% 2.0% s.e. (range 0–95%).
The most abundant type of plastic, by number of fragments,
was user plastic (68.9%) followed by industrial plastic nurdles
(31.0%),with little other plastic (one rubber O-ring) (0.09%)
(Table 1). The majority of plastic debris was found in the
ventriculus (89%, or 924 pieces) (Table 1). The largest number
of plastic fragments found within one bird was 30 pieces, all in
the ventriculus (11 industrial and 19 user). The retrieved plastic
included rounded and worn, irregular and sharp-edged fragments
ranging in length from 1 to 20 mm.
In terms of light, medium and dark colours, light-coloured
plastic (63.76%) was most prevalent, followed by medium col-
ours (22.09%) and dark colours (14.15%) (Table 2). Of the
individual colours identified, yellow-brown (23.06%), white-
yellow (16.47%) and brown (13.18%) were the most commonly
ingested (Table 2).
There was no correlation between total mass of plastic
ingested and any of the morphometric traits measured: body
mass (P= 0.642), wing-chord (P= 0.599) or percentage of downy
plumage (P= 0.469). On average, the fledglings had high scores
(3) for both subcutaneous and visceral fat and also for pectoral
muscle. There was also no correlation between total mass of
plastic and either pectoral muscle-score (P= 0.756) or subcuta-
neous fat-score (P= 0.342). Although not statistically significant,
a weak correlation between ingested plastic load and visceral fat-
score (P= 0.0967) is suggestive of a link between the amount of
plastic ingested and visceral fat around the intestine (Fig. 1).
Body-mass was positively correlated with pectoral muscle-
score, and subcutaneous and visceral fat-scores (all P<0.001).
Table 1. Number and proportion of each type of plastic in the proventriculus and ventriculus of fledgling Short-tailed Shearwaters (total = 1032 pieces)
Industrial plastic User plastic Other plastic
Proventriculus Ventriculus Proventriculus Ventriculus Proventriculus Ventriculus
Number of pieces 18 302 89 622 1 0
Proportion of total (%) 1.7% 29.2% 8.6% 60.2% 0.09% 0%
Overall proportion of each type of plastic 31.0% 68.9% 0.09%
Table 2. Number and proportion of plastic particles of different colour
in the proventriculus and ventriculus of Short-tailed Shearwater chicks
Colour Number of pieces %
Light
Clear 9 0.87
White 101 9.79
White-yellow 170 16.47
Yellow 78 7.56
Yellow-brown 238 23.06
Peach 4 0.39
Light green 44 4.26
Light blue 3 0.29
Grey 10 0.97
Pink 1 0.09
Sub-total 658 63.76
Medium
Brown 136 13.18
Blue 4 0.39
Orange 16 1.55
Green 12 1.16
Olive-green 15 1.45
Red 19 1.84
Turquoise 26 2.52
Sub-total 228 22.09
Dark
Dark grey 5 0.48
Dark blue 1 0.09
Dark green 17 1.65
Dark red 10 0.97
Dark red-brown 61 5.91
Black 52 5.04
Sub-total 146 14.15
Total 1032 100
0.6 (a)
(b)
(c)
0.4
0.2
0
012
Pectoral muscle-score
Subcutaneous fat-score
Visceral fat-score
3
0123
0123
0.6
0.4
Ingested plastic load (g)
0.2
0
0.6
0.4
0.2
0
Fig. 1. Relationship between plastic load (weight of plastic (g)) and:
(a) pectoral muscle-score; (b) subcutaneous fat-score; and (c) visceral fat-
score. Muscle and fat were scored from 0 to 3: 0, no muscle or fat; 1, low levels
of muscle or fat; 2, moderate levels of muscle or fat; 3, high levels of muscle or
fat. Box-plots show the range of plastic loads, and black dots the median
weight of plastic weight in each fat score.
8Emu H. R. Cousin et al.
Wing-chord and percentage of downy plumage were strongly
positively correlated with body-mass (P<0.001).
In addition to plastic, other gut contents in the proventriculus
and ventriculus included wood, stones, squid beaks and a rarely
found isopod, Anuropus sp. (family Anaropidae; G. Poore and
N. Bruce, pers. comm., 2013).
Discussion
Observations of wildlife casualties from entanglement in and
ingestion of plastic debris are increasing around the world. Sea-
birds in particular are facing greater exposure to this threat as
levels of marine plastic pollution increase (Barnes et al.2009).
Short-tailed Shearwaters are one species of seabird that could be
exposed to this increasing threat, owing to their foraging range
spanning the northern and southern hemispheres and several
oceans. The results of our study, reporting a 96% incidence of
plastic-debris ingestion in Short-tailed Shearwater chicks from a
reasonably remote area and before they fledge, are a significant
concern, particularly in the context of global marine pollution.
The results of our study are comparable to those of Carey
(2011a) on Phillip Island, Victoria. Those beachcast Short-tailed
Shearwater fledglings had ingested an average 113 mg of plastic
per bird compared with our Tasmanian pre-fledging chicks with
148 mg per bird. We also found, as did Carey (2011a), that user
plastic was the most commonly ingested plastic, with the
majority of the plastic particles located in the ventriculus and a
high proportion of light-coloured plastic debris ingested. Adult
Short-tailed Shearwaters in the Bering Sea (Vlietstra and Parga
2002) had similar plastic loads, of 6.9 pieces per bird compared
with the 6.0 pieces per bird of our study.
Given the extensive foraging range of this species and the fact
that the retention time of plastics in seabirds is poorly understood,
but may be 6 months or more (Day et al.1985; Ryan 1989), it is
not possible to say whether the plastic debris in this study was
ingested in local Tasmanian or more distant waters. Previous
studies have shown that adults do forage around southern Aus-
tralia and into Antarctic waters during the breeding season, with
foraging trips averaging 1–2 days (Weimerskirch and Cherel
1998; Carey 2011b; Einoder et al. 2011). It is therefore likely that
the Clifton Beach chicks are receiving plastics from the southern
hemisphere (Raymond et al.2010).
Short-tailed Shearwaters are considered an ideal indicator
species of plastic accumulation in the oceans (Vlietstra and Parga
2002; Avery-Gomm et al.2012). Although 96% of the chicks in
this study contained plastic debris, we found no evidence that
plastic ingestion was effecting the physical health of Shearwater
chicks from this Tasmanian population. The natural diet of these
birds includes squid beaks and fish bones so their digestive system
is likely to be robust enough to cope with sharp objects. Given
the flexibility of the proventriculus and ventriculus, we would not
expect to find obvious perforations resulting from small pieces of
plastic. No statistically significant correlations between plastic
load and body condition were observed, nor were there any
reductions in body fat or mass of these birds that could be
contributed to ingested plastic. Additionally, the proventricular
linings of the 171 fresh carcasses showed no punctures, lacera-
tions or ulcerations potentially owing to ingested plastic debris.
Given the rather small amounts of plastic in each bird and their
normal diet including squid this is not surprising. No deaths have
been directly attributed to proventricular damage in several
hundred freshly dead Laysan Albatross necropsied between
1993 and 2000, and this species is reported to have the heaviest
plastic loads of all seabirds (Auman et al. 1997; H. J. Auman, pers.
obs.).
Analyses of plastic items ingested by seabirds often show a
non-random selection, presumably because they match the col-
ours of their prey (Ryan 1987; Cooper et al.2004). The prevalence
of light colours, particularly white, white-yellow, yellow-brown
and brown found in Short-tailed Shearwaters resembles prey
species found in the North Pacific Ocean, in particular the
euphausiids (Vlietstra and Parga 2002). Although the numbers
of white plastic pieces reported here are lower than those found
in birds from the Bering Sea (Vlietstra and Parga 2002), there
appears to be a greater proportion of yellow-brown plastics in
birds in waters around Tasmania. This shift in colour predomi-
nance could be a result of a change in prey species closer to
breeding grounds. However, some staining of plastic fragments
within the digestive system of the birds is also possible.
Owing to the various chemicals added to plastics during their
production, there is some risk of toxicological effects from
ingesting plastics, because it has been suggested that chemicals
derived from plastics may leach from ingested plastic into seabird
tissues. Polybrominated diphenyl ethers (PBDE) congeners,
originating in flame retardants, have been found in Short-tailed
Shearwater adipose tissue yet not found in their prey items
(Tanaka et al.2013). Polychlorinated biphenyls (PCB) have been
positively correlated with ingested plastics in at least eight species
of Procellariiformes (Ryan et al.1988; Colabuono et al.2010).
Potential toxicological effects as a result of ingested plastics are
still being elucidated and the effects of many contaminants,
including heavy metals, on seabirds are currently not known
(Yamashita et al.2011). We recommend future research on the
toxicological effects of plastics to discern the long-term effects of
ingested plastic debris on seabird populations.
Acknowledgements
This research project was conducted under the Tasmanian Department of
Primary Industries, Parks, Water and Environment (DPIPWE) permit number
TFA13039. Gratitude goes to laboratory assistants Skye-Louise Lawler,
Tamara Bartholomew, Natalie Bool, Marion Foucher and Nicole Hellessey.
Thanks also to Kris Carlyon for facilitating the collection of the Shearwaters
from the DPIPWE, Simon Witherspoon and Mark Hindell for their statistical
advice, Kerry Swadling, and Gary Poore and Niel Bruce (Museum Victoria,
Melbourne) for identification of the unknown isopod. We also thank two
reviewers who improved this manuscript.
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Effects of plastic ingestion on body condition Emu 11
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