Discussion

The total number of marine species with documented records of either entanglement and/or ingestion has doubled with an increase from 267 species in Laist (1997) to 557 species in this new review (Table 4.3 and Online Supplements). The increase in number of affected species is substantial in all groups. The documented impact for marine turtles increased from 86 to 100 % of species (now 7 of 7 species), for marine mammals from 43 to 66 % of species (now 81 of 123 species) and for seabirds from 44 to 50 % of species (now 203 of 406 species). Among marine mammals the percentage of affected whales increased from 37 to 68 % of species (now 54 of 80 species) and seals from 58 to 67 % of species (now 22 of 32 species) (see Table 4.3).

Laist (1997) addressed groups such as fish and invertebrates only marginally, so comparative figures in such groups (Tables 4.1, 4.2, 4.3) are currently of less use. We may have missed sources, and recently publications have been published at such high frequency that we cannot guarantee completeness as given in full in the online supplement, with derived data in Table 4.4.

We have stopped our additions to the online supplement and thus to derived tables on the 9th of December 2014. We welcome documentation on missed or new records of entanglement or ingestion for future updates. It remains important to continue such documentation of species affected by marine debris. However, given sufficient time and research effort, all species of marine organisms will get documented examples of interaction with marine debris. Any species can become the victim of entanglement. Furthermore, the filter-feeding habits of many lower trophic levels, and secondary ingestion by higher trophic levels, make it almost unavoidable that any species in the marine food web will at some stage pass at least some plastic debris through the intestinal tract.

As a consequence, to improve on current knowledge, future assessments of deleterious effects of debris on marine life require comparable standardized data on frequency of occurrence, ingestion quantifi and categorisation of ingested debris. It is only through study of the various impacts (including frequency and quantity) on

Table 4.3 Number of species with documented records of entanglement in, and/or ingestion of marine debris

Species group

Laist (1997)

This study

Spp. total

Species affected

Spp. total

Species affected

(n)

(n)

(%)

(n)

(n)

(%)

Seabirds

314

138

43.9

406

203

50.0

Anseriformes (marine ducks)

1

13

5

38.5

Gaviiformes (divers)

5

4

80.0

Sphenisciformes (penguins)

16

6

38.0

18

9

50.0

Procellariiformes (tubenoses)

99

63

64.0

141

85

60.3

Podicipediformes (grebes)

19

2

10.0

23

6

26.1

Pelecaniformes, suliformes, phaethontiformes (pelicans, gannets and boobies, tropicbirds)

51

17

33.3

67

27

40.3

Charadriiformes (gulls, skuas, terns, auks)

122

50

41.0

139

67

48.2

Marine mammals

115

49

43

123

81

65.9

Mysticeti (baleen whales)

10

6

60.0

13

10

76.9

Odontoceti (toothed whales)

65

22

34.0

65

44

66.2

Phocidae (true seals)

19

8

42.0

19

9

42.1

Otariidae (eared seals)

14

11

79.0

13

13

100.0

Sirenia (sea cows, dugongs)

4

1

25.0

5

3

60.0

Mustelidae (otters)

1

1

100.0

2

1

50.0

Ursidae (polar bears)

1

1

100.0

Turtles

7

6

85.7

7

7

100.0

Sea snakes

0

62

2

3.2

Fish

60

32,554

166

0.6

Invertebrates

9

159,000

98

0.1

All species

267

557

Marine birds, mammals and turtles

436

193

44.3

536

291

54.3

Species associated with smothering

22

Comparative summary with the earlier major review by Laist (1997). See notes in captions of Tables 4.1 and 4.2. Numbers of species affected and group percentages are not a simple sum of Tables 4.1 and 4.2 because many species suffer from entanglement as well as ingestion. For details, see the Online Supplement

different species and their interactions, combined with dedicated observational or experimental studies, that we can ultimately gain areal understanding of the many deleterious impacts of marine plastic debris on wild populations. A number of recommendations can be made to assist collection of comparable high-quality data sets:

• Accurate data on frequency of occurrence of entanglement or ingestion of debris require a proper a priori protocol, staff that has experience with identifying (symptoms of) marine debris and adequate samples sizes.

• Concerning frequency of entanglement in debris, protocols for assessment are

complicated by the distinction between interaction with active fishing gear and

Table 4.4 Number of species of major groups of marine organisms with documented records of marine debris impacts in natural habitats, separately for entanglement or ingestion and in combination (search closed 9th December 2014)

Species group

Species (n)

Entanglement (n)

Entanglement (%)

Ingestion (n)

Ingestion (%)

Total species affected (n)

Total species affected (%)

Seabirds

406

103

25.4

164

40.4

203

50.0

Anseriformes

13

5

38.5

1

7.7

5

38.5

Anatidae (marine ducks)

13

5

38.5

1

7.7

5

38.5

Gaviiformes

5

3

60.0

3

60.0

4

80.0

Gaviidae (divers, loons)

5

3

60.0

3

60.0

4

80.0

Sphenisciformes

18

6

33.3

5

27.8

9

50.0

Spheniscidae (penguins)

18

6

33.3

5

27.8

9

50.0

Procellariiformes

141

24

17.0

84

59.6

85

60.3

Diomedeidae (albatrosses)

21

12

57.1

17

81.0

17

81.0

Procellariidae (petrels, shearwaters, prions)

92

10

10.9

55

59.8

56

60.9

Hydrobatidae (storm petrels)

24

2

8.3

10

41.7

10

41.7

Pelecanoididae (diving petrels)

4

0

0.0

2

50.0

2

50.0

Podicipediformes

23

6

26.1

0

0.0

6

26.1

Podicipedidae (grebes)

23

6

26.1

0

0.0

6

26.1

Phaethontiformes

3

0

0.0

2

66.7

2

66.7

Phaethontidae (tropicbirds)

3

0

0.0

2

66.7

2

66.7

Pelecaniformes

8

4

50.0

2

25.0

5

62.5

Pelecanidae (pelicans)

8

4

50.0

2

25.0

5

62.5

Suliformes

56

16

28.6

12

21.4

20

35.7

Fregatidae (frigatebirds)

5

0

0.0

1

20.0

1

20.0

Sulidae (gannets, boobies)

10

6

60.0

5

50.0

8

80.0

Species group

Species (n)

Entanglement (n)

Entanglement (%)

Ingestion (n)

Ingestion (%)

Total species affected (n)

Total species affected (%)

Phalacrocoracidae (cormorants, shags)

41

10

24.4

6

14.6

11

26.8

Charadriiformes

139

39

28.1

55

39.6

67

48.2

Chionidae (sheathbills)

2

0

0.0

1

50.0

1

50.0

Scolopacidae (phalaropes)

3

0

0.0

2

66.7

2

66.7

Laridae (gulls, noddies, skimmers, terns)

102

28

27.5

32

31.4

42

41.2

Stercorariidae (skuas)

7

2

28.6

6

85.7

6

85.7

Alcidae (murres, guillemots, murrelets, auks, auklets, puffins)

25

9

36.0

14

56.0

16

64.0

Marine mammals

123

51

41.5

62

50.4

81

65.9

Mysticeti

13

9

69.2

7

53.8

10

76.9

Balaenidae (right whales)

4

3

75

2

50

3

75.0

Neobalaenidae (pygmy right whales)

1

1

100

1

100

1

100.0

Eschrichtiidae (gray whales)

1

1

100

0

0

1

100.0

Balaenopteridae (rorquals)

7

4

57.1

4

57.1

5

71.4

Odontoceti

67

16

23.9

40

59.7

44

65.7

Physeteridae (sperm whales)

1

1

100

1

100

1

100.0

Kogiidae (dwarf and pygmy sperm whales)

2

1

50

2

100

2

100.0

Pontoporiidae (La Plata river dolphins)

1

0

0

1

100

1

100.0

Monodontidae (narwhals, belugas)

2

1

50

0

0

1

50.0

Table 4.4 (continued)

Species group

Species (n)

Entanglement (n)

Entanglement (%)

Ingestion (n)

Ingestion (%)

Total species affected (n)

Total species affected (%)

Phocoenidae (porpoises)

6

2

33.3

4

66.7

4

66.7

Delphinidae (oceanic dolphins)

34

10

29.4

19

55.9

22

64.7

Ziphiidae (beaked whales)

21

1

4.8

13

61.9

13

61.9

Pinniped

33

22

66.7

12

36.4

22

66.7

Phocidae (true seals)

19

9

47.4

4

21.1

9

47.4

Otariidae (eared seals)

13

13

100

8

61.5

13

100.0

Sirenia

5

2

40

3

60

3

60.0

Trichechidae (manatees)

2

1

50.0

2

100.0

2

100.0

Dugongidae (dugongs)

2

1

50

1

50

1

50.0

Carnivora

3

2

66.7

0

0.0

2

66.7

Mustelidae (otters)

2

1

50

0

0

1

50.0

Ursidae (polar bears)

1

1

100

0

0

1

100.0

Turtles

7

7

100.0

7

100.0

7

100.0

Carettinae

3

3

100.0

3

3.0

3

100.0

Cheloniidae

3

3

100.0

3

3.0

3

100.0

Dermochelyidae

1

1

100.0

1

1.0

1

100.0

Sea snakes

62

2

3.2

0

0.0

2

3.2

Hydrophiidae (sea snakes)

62

2

3.2

0

0.0

2

3.2

Fish

32,554

89

0.27

92

0.28

166

0.51

Elasmobranchii

692

21

3.03

18

2.60

30

4.34

Hexanchiformes (frill and cow sharks)

6

1

16.67

0

0.00

1

16.67

Orectolobiformes (carpet sharks)

44

0

0.00

1

2.27

1

2.27

Species group

Species (n)

Entanglement (n)

Entanglement (%)

Ingestion (n)

Ingestion (%)

Total species affected (n)

Total species affected (%)

Lamniformes (mackerel sharks)

16

6

37.50

5

31.25

7

43.75

Charcharhiniformes (ground sharks)

282

11

3.90

8

2.84

14

4.96

Squaliformes (bramble, sleeper, dogfish sharks)

129

1

0.78

3

2.33

4

3.10

Myliobatiformes (stingrays)

215

2

0.93

1

0.47

3

1.40

Holocephali

50

1

2.00

0

0.00

1

2.0

Chimaeriformes (chimaeras)

50

1

2.00

0

0.00

1

2.0

Actinopterygii

22,916

67

0.29

74

0.32

135

0.6

Amiiformes (bowfins)

1

1

100.00

0

0.00

1

100.0

Anguilliformes (eels, morays)

906

1

0.11

0

0.00

1

0.11

Clupeiformes (herrings)

390

2

0.51

2

0.51

3

0.77

Siluriformes (cat fish)

3589

2

0.06

3

0.08

4

0.11

Osmeriformes (smelts)

319

1

0.31

0

0.00

1

0.31

Salmoniformes (salmons)

215

4

1.86

1

0.47

5

2.33

Stomiiformes (light fish, dragon fish)

413

0

0.00

3

0.73

3

0.73

Aulopiformes (grinners)

255

0

0.00

1

0.39

1

0.39

Myctophiformes (lantern fish)

215

0

0.00

12

5.58

12

5.58

Lampriformes (velifers, tubeeyes, ribbon fish)

24

0

0.00

3

12.50

3

12.50

Gadiformes (cod-like)

614

2

0.33

7

1.14

8

1.30

Batrachoidiformes (toad fish)

82

2

2.44

0

0.00

2

2.44

Lophiiformes (angler fish)

353

0

0.00

1

0.28

1

0.28

Table 4.4 (continued)

Species group

Species (n)

Entanglement (n)

Entanglement (%)

Ingestion (n)

Ingestion (%)

Total species affected (n)

Total species affected (%)

Atheriniformes (silversides)

338

0

0.00

1

0.30

1

0.30

Cyprinodontiformes (rivulines, killi fish, live bearers)

1249

1

0.08

0

0.00

1

0.08

Beloniformes (needle fish)

254

0

0.00

1

0.39

1

0.39

Zeiformes (dories)

33

0

0.00

1

3.03

1

3.03

Scorpaeniformes (scorpion fish, flatheads)

1622

18

1.11

5

0.31

23

1.42

Perciformes (perch-like)

10,837

20

0.18

29

0.27

47

0.43

Pleuronectiformes (flatfish)

778

11

1.41

4

0.51

14

1.80

Tetraodontiformes (puffers, file fish)

429

2

0.47

0

0.00

2

0.47

Invertebrates

159,000

92

0.06

6

0.004

99

0.06

Crustacea

67,000

46

0.07

3

0.00

49

0.07

Echinodermata

7000

21

0.30

0

0.00

21

0.30

Mollusca

85,000

25

0.03

3

0.00

29

0.03

All species*

344

331

557

*Exclusive 22 species associated with smothering, see online supplement 2

interaction with marine debris. For example, even for experts using standard protocols, it is difficult to distinguish whether wounds are caused by entanglement in active or derelict fishing gear, even when remains of nets or similar are found on the body. Some suggestions are being developed concerning entanglement rates in ghost nets or for bird entanglement in synthetic materials used for nest construction (MSFD-TSGML 2013).

• For ingestion, in addition to frequency of occurrence ('incidence') it is recom-

mended to collect data on quantities of ingested debris not only on the basis of numbers of items but also by mass of categories.

• In such ingestion records, as a minimum it is recommended to separate industrial

plastics (pellets) from consumer-waste plastics (see Table 4.5). The latter if possible can be further specifi following the categorisation recommended for ingestion by birds, mammals and fi according to the EU Marine Strategy Directive (MSFDTSGML 2013), that is into categories of sheetlike, threadlike, foamed, hard fragmented, and other synthetic items, plus categories of non-plastic rubbish.

• For averaged data, information should be provided as 'population averages' with

standard error of the mean. Population averages are calculated with the inclusion of individuals without ingested plastics. Additional data can be maximum levels observed, or proportions of animals exceeding a particular limit [such as the 0.1-g critical limit in the Ecological Quality Objective for plastic ingestion by northern fulmars (Van Franeker et al. 2011)] (see Table 4.5). We emphasize this explicit use of population averages because in quite a few of the publications checked for this review averages had been calculated just over those individuals that had plastic, often not specifying that zero values had been omitted.

• Negative species results (e.g. Avery-Gomm et al. 2013; Provencher et al. 2014) are

also relevant but again should be based on an adequate sample size of animals studied according to a proper protocol. Thus, records of absence of debris for an individual sample should be as fi as those on presence. From experience in our own research group, we know of claims on absence or near absence of plastics in stomachs or guts of several species of which diets were studied, but without dedicated methods or data recording for marine debris (including zeros). Once proper methods were established for laboratory procedures and data recording, each of those species was found to contain debris regularly (e.g. Bravo-Rebolledo et al. 2013).

• Examples of protocols for ingested debris in intestinal tracts of larger organisms

can be found in e.g. MSFD-TSGML (2013), with further information for ingestion by marine birds in Van Franeker et al. (2011) and marine turtles in Camedda et al. (2014). Standard protocols for marine mammals, invertebrates have not yet been established in detail but may largely follow those for seabirds and turtles. In general, these studies consider debris of ≥1 mm by using sieves with such mesh size.

• Only when using the above approaches on frequency of occurrence (proportion of

animals in populations affected) and gravity of interaction (quantity of ingested material; damage level from entanglement), it becomes possible to design experimental or other dedicated studies that allow estimates of the true impact of plastic ingestion on wildlife populations. This relates to both the physical and chemical types of impacts, and will ultimately require model predictions using demographic characteristics of the species involved (Criddle et al. 2009).

Table 4.5 Recommended mode of data presentation for ingested plastic debris, using the example of plastics ingested by northern fulmars in different subregions of the North Sea (modified from Van Franeker and the 'Save the North Sea Fulmar' study group, 2013)

Regions

Industrial granules

User plastics

Total plastics

2007–2011

period

Sample (n)

Incidence (%)

Average number n ± se

Average mass g ± se

Incidence (%)

Average number n ± se

Average mass

g ± se

Incidence (%)

Average number n ± se

Average mass

g ± se

Geome tric mean mass

EcoQO (%) (over

0.1 g)

Scottish Islands

121

47

1.3 ± 0.2

0.03 ± 0.00

90

21.2 ± 3.0

0.32

± 0.06

90

22.5 ± 3.0

0.35

± 0.06

0.091

58

East England

51

75

4.2 ± 0.9

0.09 ± 0.02

98

42.2 ± 6.2

0.26

± 0.06

98

46.4 ± 6.7

0.35

± 0.07

0.154

76

Channel area

72

82

7.1 ± 1.6

0.15 ± 0.03

99

44.6 ± 8.0

0.39

± 0.06

99

51.7 ± 9.3

0.54

± 0.08

0.278

86

SE North Sea

493

57

3.1 ± 0.6

0.07 ± 0.01

94

24.9 ± 1.8

0.29

± 0.04

95

28.0 ± 2.1

0.36

± 0.04

0.105

60

Skagerrak

79

53

3.4 ± 0.8

0.07 ± 0.02

94

49.2 ± 14.9

0.24

± 0.04

94

52.6 ± 15.5

0.31

± 0.05

0.105

56

North Sea total

816

58

3.3 ± 0.4

0.07 ± 0.01

94

29.5 ± 2.0

0.30

± 0.03

95

32.8 ± 2.2

0.37 ±

0.03

0.115

62

Given are sample size, percentage of individuals with ingested material (incidence or frequency of occurrence), and population averages (including zero values) with standard error (se) for both number of items (n) and mass. These are specified for industrial plastics and consumer waste separately, and in total. Added to total plastics in this example are geometric mean mass and EcoQO performance that is the percentage of fulmars that had more than the critical level of 0.1 g of total plastic in the stomach

It will take considerable time and effort to collect these data and conduct dedicated studies before firm conclusions can be drawn on the level of detrimental impact of marine plastic debris on wildlife. However, in our opinion the suffering and death of individuals, in combination with the likelihood of higher-level population effects, indicates the need for a rapid reduction of input of plastic debris into the marine environment. If wildlife problems are not convincing: recent studies show that chemical and physical impacts are likely to occur in marine food webs (e.g. Van Cauwenberghe and Janssen 2014; Rochman et al. 2013, 2014), which implies potential impacts on human end consumers (Galloway 2015).

Long-term studies on seabirds have shown that measures to reduce loss of plastics to the environment do have relatively rapid effects. After considerable attention to the massive loss of industrial pellets to the marine environment in the early 1980s, improvements in production and transport methods were reflected in a visible result in the marine environment within one to two decades: several studies from around the globe showed that by the early 2000s the number of industrial granules in seabird stomachs had approximately halved from levels observed in the 1980s (Van Franeker and Meijboom 2002; Vlietstra and Parga 2002; Ryan 2008; Van Franeker et al. 2011; Van Franeker and Law 2015). These examples indicate that it is possible to reduce deleterious impacts from marine plastic debris on marine wildlife in shorter time frames than the longevity of the material might suggest.

Acknowledgments We are very grateful for the language corrections made by Dan Turner. We thank two anonymous reviewers and the editorial team for their constructive comments and suggestions, which contributed to considerable improvements in the manuscript.

 
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