Origins and Biological Accumulation of Small Plastic Particles 
in Fur-seal Scats from Macquarie Island

Ambio Vol. XXXII, No. 6, 2003

Cecilia Eriksson¹ and Harry Burton²

1 Mary St, Hobart, Tasmania 7000, Australia horatio@bigpond.comcecilia.eriksson@bigpond.com
²Australian Antarctic Division, Kingston, Tasmania, Australia harry_bur@antdiv.gov.au

Abstract

One hundred and sixty four plastic particles (mean length 4.1 mm) recovered from the scats of fur seals (Arctocephalus spp.) on Macquarie Island were examined. Electron micrographs of 41 of the plastic particles showed that none could be identified as plastic pellet feedstock from their shapes. Commonly, such pellets are cylindrical and spherical. Instead, all the 164 plastic particles from the seal scats were angular particles of seven colours (feedstock particles are normally opaque or white) and could be classified into two categories: i) Fragmented along crystal lines and likely to be the result of UV breakdown and ii) Worn by abrasion (where striations were clearly visible) into irregular shapes with rounded corners. White, brown, green, yellow and blue were the most common colours. In composition, they came from five polymer groups; polyethylene 93%, polypropylene 4%, poly(1-Cl-1-butenylene) polychloroprene 2%, melamine-urea (phenol) (formaldehyde) resin 0.5% and cellulose (rope fibre) 0.5%. The larger groups are buoyant with a specific gravity less than that of sea-water. These small plastic particles are formed from the breakdown of larger particles (fragments). Their origin seems to be from the breakdown of user plastics washed ashore and ground down on cobbled beaches. Certainly most particles (70%) had attained their final form by active abrasion. It is hypothesised that the plastic particles were washed out to sea and then selected by size and consumed by individuals of a pelagic fish species, Electrona subaspera, who in turn were consumed by the fur seals. Thus the particles were accumulated both by the fish and the seals in the usual process of their feeding.

The accumulation of plastic debris in the oceans and on beaches all over the world has been observed and reported for at least three decades with frequent publication from 1970 into the late 1980s (1). Amongst this marine debris, small plastic pellets from industrial feedstock especially, but also small fragments, were observed early on (2-7). Although measures were enforced to limit the input of plastic to the sea already in 1988 (8), plastic debris continued to appear in great densities in surface waters (9), on beaches (10) and even on the ocean floor (11-13). It is now recognised that much of that plastic originated from terrestrial sites as well as from vessels and quantities are difficult to estimate (14). It is therefore not surprising to find numbers of plastic items on geographically remote islands such as the Pitcairn Islands (15), Bird Island, South Georgia (16), New Zealand’s subantarctic islands (17,18) and Macquarie and Heard Islands in the Southern Ocean (19,20) and even at some beaches on the Antarctic Peninsula (21,22).

Neuston net sampling in sea surface waters for plastics, has been carried out in coastal areas, areas highly frequented by tankers and fishing vessels, and in areas away from such activities. Small plastic particles were found in all these areas. While Ryan (23) reported a mean density of 3 600 plastic particles km^-2 on the sea surface off South Africa, Day et al. (24) found numbers up to 0.3 x 106 plastic particles km-2 in the North Pacific east of Japan. In 2001 Moore et al. (25) described a mean abundance of 0.3 x 106 and a maximum of almost 1 x 106 plastic particles km-2 in the North Pacific central gyre. As well as feedstock, it was recognised that remnants of manufactured plastic products (user plastic) found in the marine environment also result from plastic product break down. This break down probably occurs through wave action and ultraviolet light acting both at sea and with grinding from rocks and sand on beaches. This conclusion was supported by the abundance of small plastic particles, mainly fragments, being correlated with the abundance of larger plastic items in the sea (26,27, 24). Also, Moore et al. (25) found that most of the plastic fragments they sampled were thin films (described as similar to the plastic used in sandwich bags), mono-filament line, and miscellaneous fragments.

A large number of publications reported on plastic particles, pellets as well as fragments, of sizes < 1 cm appearing in seabird digestive systems from all oceans. So far 111 (36%) species of seabirds worldwide have been found to ingest marine debris of which most is plastic (28). Some aspects of small plastic particles in sea birds, i.e. number of feedstock and/or user-plastic, size, colour, density, and chemical composition are well documented. Plastics have been found in turtles (29-31), juvenile and adult fish (2,4), the Southern Ocean opah fish Lampris immaculatus (32), sea snails (5), tuna (33), and whales (34,35), but little is known of the paths of these particles through the marine ecosystem.

Plastic particles were first seen in fur seal scats from Macquarie Island in 1990 (D. Johnson and H. Burton, unpubl. data). When studying the diet of Otarid seals at Macquarie Island, Goldsworthy et al. (36) and McMahon et al. (37) reported that they found scats, from fur seals and Hooker Sea Lions respectively, to contain small plastic particles ca 1 mm in diameter. The plastic particles were found in association with otoliths of the fish Electrona subaspera in all these seal species. Our study has looked further into the origin of similar small plastic particles in fur seal (Arctocephalus spp.) scats on Macquarie Island with collections from 1991 and 1997.

Methods

Collection of scat samples and extraction of plastic particles

Scats from the Antarctic fur seal Arctocephalus tropicalis and/or Antarctic fur seal A. gazella were collected in two periods, 1990/1991 and 1996/1997, at Secluded Beach and Goat Bay, North Head Peninsula, Macquarie Island (54°30'S 158°57'E). The beach at Secluded Bay is ~ 250 m long and that of Goat Bay ~ 50 m. Sampling was done from late November until early April while the seals were ashore in numbers sufficient to produce at least a few scats per visit to the beach. Scats were collected from between the grass tussocks just above the high-tide zone then frozen and later broken apart with water in a series of two sieves with mesh diameter of 1 mm and 0.5 mm mesh as described in Goldsworthy et al. (36). Thus plastic micro-litter, < 0.5 mm (14), was not retained. Plastic particles were stored dry in small plastic bags. Free plastic pieces were rarely observed in the tussock areas where the scats were collected; and so the inclusion of plastics from the ground together with scats is judged to be extremely unlikely.

Size measurements were done on all plastic particles extracted from seal scats in 1996/1997 with a Sigma Scan Pro image analysis system. Maximum length and “maximum width” (the latter being somewhat more subjective) were determined. Thickness was not measured but was always less than the maximum width. A subjective estimate of maximum length was made by eye on samples from 1990/1991. Colour was defined subjectively upon inspection by the senior author.

The scanning electron microscope (SEM) was a JEOL JSM-840. The plastic particles from 1990/91 were photographed at ~ 10 kVA, a low energy current, after being sputter-coated with ~ 21 nm thickness of gold while they were held on brass stubs by double-sided adhesive tape. The time each specimen was held in the SEM chamber was kept short because the hot electron beam in high vacuum distorted the specimens after a minute.

Chemical composition was determined for all plastic particles found in seal scats and also for all (no selections were made) plastic objects in flotsam collected regularly on Sandell Bay beach on Macquarie Island. The flotsam had been collected monthly during November 1998 to March 1999. Very thin sections were cut from seal scat plastic particles (after they were measured) and flotsam plastic with a fine dissecting knife and analysed by placing the fragments under an infrared microscope attached to a BRUKER IFS 66 FTIR. Spectral transmission data was collected over the range 700 to 4800 reciprocal centimetres. Special note was made from the transmission data of the degree of oxidation of the plastic. The samples were subjectively graded into one of three (low, medium or high oxidation) categories.

In this paper we present data only for scat samples that contained plastic particles. A total of 164 plastic particles were found in 145 seal scats. In the year 1990/1991 the number of plastic particles in the 45 scats was always one per scat and in the year 1996/1997 85% of the 100 scat samples contained 1 particle/scat, 12% had 2 particles/scat, 2% had 3 particles/scat and 1% had 4 particles/scat.

Scanning electron micrographs of 41 particles from 1990/1991 showed that 39% were fragmented along “crystal” lines. Nearly all (98%) had an irregular form and were worn by abrasion into shapes with some rounded edges (Figs 1 A, B). About one third of the particles had at least one sharp edge, and 70% had clearly visible wear striations from abrasion. Lengths of the plastic particles extracted from seal scats were only measured in 1996/1997 and generally ranged from 2 to 5 mm (89% of 119 particles) but could be up to 30 mm long. The mean length was 4.1 mm (Fig. 2), the mean width was 1.9 mm. A subjective estimate of maximum length for the 1990/1991 samples would be that they were similarly sized to the 1996/1997 particles. All particles (except one cellulose fibre) had similar relative dimensions (shapes) although individual circumferences were very irregular. The distribution of the ratio of length/width (shape) was tightly clumped (Fig 3).

Colour frequencies of plastic particles in seal scats as well as in flotsam were generally similar (Table 1). White, brown, blue, green and yellow were the most common colours among plastic particles in seal scats. In flotsam white, blue and green were most common and yellow and red were common.

All particles from seal scats (45 particles from 1990/1991 and 119 from 1996/1997) were analysed for chemical composition (Table 2). The particles came from five major polymer groups. Polyethylene comprised 93%, polypropylene 4%, poly(1-Cl-1-butenylene) polychloroprene 2%, melamine-urea (phenol) (formaldehyde) resin 0.5% and cellulose 0.5%. All the 163 flotsam objects collected from Sandell Bay beach in the year 1998/99 were analyzed for chemical composition. Polyethylene comprised 48% of the objects, polypropylene 18%, polyethylene terephthalate (PET) 11%, polystyrene 16%, casein 3.3%, polyester resin? 2.5%, polyester resin + glass fibres 3.3%, and < 1% in each of polyamid resin or nylon like, polystyrene co acrylonite co urethane, ester resin phenol modified alkyd, polyester urethane, and PVC and polyethylene co-vinyl acetate.

Plastic ingestion is known in a small number of marine mammals but is far more commonly reported from birds (eg 28, 38). It is possible to have sample sizes of hundreds of specimens of birds examined in a single study (39). Sample sizes of seals are commonly much smaller. Otarid seals have been reported to be entangled in marine debris, especially plastic strapping on beaches and trawl nets (40), however ingestion of plastic is rarely reported. Goldsworthy et al. (36) and McMahon et al. (37) both found plastic particles while investigating diets of fur seals and Hooker sea-lions at Macquarie Island. All three species had been feeding on Electrona subaspera which is a very numerous myctophid fish species in the region (41). Indeed, Merilees (42) has reported a mass stranding of thousands of individuals of this species on the shores of Macquarie Island. E. subaspera was by far the most numerous diet item in all fur seal scats (36).

Goldsworthy et al. (36) collected 138 scat samples from fur seals on Macquarie Island in 4 months, and of these, ~ 4% (mean of four months) contained plastic with a maximum of 15 % during one month. Thus plastic particles in the scats were found regularly. This is an unexpected result for a region far distant from sources that supply large quantities of plastic. However the number is still smaller than that of particles, 6.6 per bird, found in the North Pacific (39). It seems that the birds directly ingested the plastic particles themselves. There is little possibility that the seals directly ingested plastic particles with a mean size of ~ 4 mm. A plastics concentrating stage, such as a fish, is vital in explaining how these particles come to be found in seal scats in such numbers. In fact Carpenter et al. (2) found, when collecting small (0.1 to 2 mm) plastic spherules in the coastal waters of New England by oblique plankton tows, identical spherules in several fish species. These fish species ranged in size between 4.6 to 327 mm and each contained one spherule per fish. Minimum estimates of the concentration factors of plastic particles from the fish to the seals in our study lie upwards from 22 to 160 times. Theses estimates are calculated assuming 4% of scats contained one plastic particle, a mean number of fish per scat was 44.4/2 (2 otoliths from each fish) and the maximum observed number of fish per scat was 319/2 as described by Goldsworthy et al. (36). These are minimum estimates because digestion of otoliths (and thus loss of otoliths from the sample) was an active process. Approximately 98% of the otoliths were eroded (36). Thus concentration factors could be > 160 and so one plastic particle could be expected in a range of ~ 450 to 4000+ fish. The accumulation of plastics up the food-web is a purely physical one. The process has the same trophic basis as the accumulation of some pesticides in marine mammals (43). For the plastics are also materials which are consumed inadvertently and are of purely human origin.

The particles were extremely sorted in size and formed a unimodal distribution (Fig. 2) and had a shape ratio (length/maximum width) that was largely constant (Fig. 3). The shape ratio range varied from 1 to 18 (fibre); but the mean ratio was 2.6 (ovoid) (Fig. 3). These narrow ranges of particle parameters suggest selectivity of a precise kind. Such discrimination could be provided through consumption by a surface feeding fish whose normal diet items are of the same size range. E. subaspera is an omnivore of length up to 127 mm (44), which is the major diet item of fur seals and whose close congeneric E. carlsbergi is also an important diet item of penguins at Macquarie Island (45,46). E. carlsbergi is known to consume copepods inter alia and migrate to the surface near dusk from a depth of  80 to 140 m (44). The diet and habits of E. subaspera are likely to be similar. The size range of copepods in these waters is from 1-9 mm (47), which overlaps the size distribution of 95% of the plastic particles we found in the scats.

Abrasion, fragmentation and oxidation of particles

The scanning electron micrographs of the plastic particles from the scats of fur seals show 70% of the particles had clear abrasion marks (Fig. 1A). Thus most particles had attained their final form by active abrasion. The explanation for this that occurs to us is that these particles were actively ground against sharp and hard surfaces such as crystals in rocks. This abrasion could have happened on active cobbled beaches or in the digestive tracts of the seals. We favour the first explanation as the softer otoliths in the scats, also subject to the digestive process, did not have similar abrasion marks. Apart from being abraded, 34% of the particles also had partly sharp and angular forms. The oxidation of all plastic particles was evident from the analysis and it is likely that ultra violet (UV) light had played a part in promoting fragmentation at sea (48,49). Signs of crazing, chalking, discolouration and embrittlement (50), similar to what was found on plastic pellets by Gregory (51), were found in 39% of our particles. Most colours included particles with similar proportions of high, medium and low oxidation rating (52). However the white particles (52% of the total, Table 1B) had many more cases of low and medium oxidation rating, compared to high (52). This suggests that either this colour was more resistant to oxidation than the others or that the particles had been exposed for a shorter period. The first explanation is surprising as colours darker than white are reported (53) to be more resistant to UV degradation as the pigments can act as UV light absorbers (54,48) with the light energy then being dissipated as heat before it can contact the degradation-initiating centres of the polymers. Although low temperatures can cause embrittlement in polymers (55) Andrady (56) showed in experiments with polymers exposed to sunlight on land and floating on cool sea-water that low temperatures generally limited the degradation rates. Thus the particles in our study seemed more formed by abrasive processes than by chemical processes of polymer degradation.

The colours of particles from both seals and from beach washed flotsam were quite similar (Table 1). The approximately 10 times higher frequency of brown in particles from seal scats, compared to the colours of flotsam, is likely to be due to faecal staining. Plastic flipper tags on the rear flippers of southern elephant seals (Mirounga leonina) on Macquarie Island were observed commonly to be stained brown.

The similarity in colour distribution in particles from scats and in flotsam is consistent with the particles being selected by size at night whilst the colours were obscure to unidentifiable, but the size and outline being very clear, to a fish feeding from below the surface. The congruence in colours of these small plastic particles and beach flotsam (Table 1) suggests that the particles are formed from the breakdown of the larger flotsam pieces into smaller and smaller fragments. The small particles from seal scats therefore have not originated as plastic pellet feedstock which have quite limited colour frequencies (7).

Comparison of polymer group frequencies between seal and flotsam plastics

The categories of polymers found in the seal scats were essentially the same as those found in the beach flotsam (52). The differences were in the absence of polymers with a specific gravity > 1.02 which is the value for sea-water. While polyethylene and polypropylene were dominant in both groups, there were fewer plastic groups represented in the seal plastics (Table 2). This is evidence for the entry of plastic particles into the food-chain following a period of suspension in sea-water. For an important characteristic in determining their presence is likely to be specific gravity; as the “missing” plastic groups from the seal scats have specific gravities greater than sea-water. The constituent pieces would sink once their parent buoyant structures, which brought them to the beach, were broken up into smaller fragments. A good example of this effect is shown with soft-drink bottles made of PET. PET was found regularly on the beach as whole capped bottles but was never found in the seal scats as particles.

It is hypothesised that most small plastic particles (< 10 mm) found in seal scats from Macquarie Island originated from plastic flotsam that had been washed out to sea after their parent materials were washed ashore and broken down on shorelines. The particles did not originate as raw plastic feedstock pellets. Some of the particles were later consumed by individuals of a night-feeding pelagic fish, E. subaspera. Some of these individuals, in turn, were consumed by fur seals feeding near Macquarie Island. This biological accumulation of small plastic pieces through the near-island oceanic food-web is akin, by inadvertent consumption of anthropomorphic materials, to that of the accumulation of some pesticides through other marine mammal food-webs.

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57. We thank Susan Robinson and Simon Goldsworthy for the collection of the plastic particles and their cleaning from the scats, Gerry Nash for the electron micrographs and Graham Rowbottom for expert advice and supervision for the plastics analyses. Karen Wilson measured the size of some of the samples and John van den Hoff produced the final figures and gave very useful comments on the paper draft. We also benefited from discussions with Martin Riddle and Martin Schultz.

Table 1. Colours of plastic particles and flotsam (A, numbers of items; n = sample size; B percent of items).

A			green	blue*	yellow	white	brown	red	clear	pink	orange	black	n
Seals 1991		6	7	8	8	13	3	0	0	0	0	45
Seals 1997		18	17	17	46	18	2	1	0	0	0	119
Seals total		24	24	25	54	31	5	1	0	0	0	164
Flotsam total		19	34	10	85	3	8	0	1	1	2	163

B			green	blue*	yellow	white	brown	red	clear	pink	orange	black
Seals 1991		13	15	17	17	29	7	0	0	0	0
Seals 1997		15	14	14	38	15	1.6	0.8	0	0	0
Seals total		15	15	15	33	19	3	0.6	0	0	0
Flotsam total		12	21	6.1	52	1.8	4.9	0	0.6	0.6	1.2
*blue and purple (purple only in flotsam)

Table 2. Polymer type in seal scat particles and flotsam and specific gravity of the polymers (source http://www.polymerweb.com/_misc/specgrav2html and http://www.tfmconsultants.com/Density%20of%20Polymers.html).

					   Numbers of samples .
Polymer type				   Flotsam 	 Seals 	Specific gravity
Polyethylene				   76		151	0.79-0.97
Polypropylene				   28		7	0.90-0.92
Polyethylene/Polypropylene		   		1	
Polyamid resin or Nylon like		   1			1.01-1.02
Poly(1-Cl-1buteneylene) polychloroprene			3	
Melamine-urea (phenol)(formaldehyde) resin 		1	1.47-1.52
Cellulose 				   		1	
Polyethylene terephthalate (PET)	   18			1.34-1.39
Polystyrene (unexpanded)		   26			1.04-1.09
Casein based glue			   2			1.35
Polystyrene co acrylonitrile co urethane   1			1.08-1.1
Polyester resin				   4			1.37-1.38
Ester resin phenol modified alkyd	   1			>1.2
Polyester urethane			   1			1.1-1.25
Polyester resin + glass fibers		   2			 >1.35
PVC and polyethylene co-vinyl acetate	   1			1.37-1.39
Sea water				   1.02
Total					   161		164	

Figures

Figure 1. Electron micrograph examples of two classes of particle shape and wear patterns. A. Particle with rounded edges and striations. B. Particle with sharp edges and cleavage lines.

Figure 2. Frequency of particle numbers in each 1 mm length category. The first compartment holds particles from 0-1 mm, the second compartment 1-2 mm etc.

Figure 3. The frequency distribution of particle shapes (length/width).

Mindfully.org note: 
Many thanks to the journal Ambio and Cecilia Eriksson, a co-author, for permission to post this important paper.