Incidental ingestion of meso- and macro-plastic debris by benthic and demersal fish

Accepted Manuscript Incidental ingestion of meso- and macro-plastic debris by benthic and demersal fish.

López-López, Lucía, Preciado, Izaskun, González-Irusta, José Manuel, Arroyo, Isabel, Punzón, Antonio, Serrano, Alberto PII: DOI: Reference:

S2352-2496(17)30042-3 https://doi.org/10.1016/j.fooweb.2017.12.002 FOOWEB 74

To appear in: Received date: Revised date: Accepted date:

11 August 2017 20 December 2017 20 December 2017

Please cite this article as: López-López, Lucía, Preciado, Izaskun, González-Irusta, José Manuel, Arroyo, Isabel, Punzón, Antonio, Serrano, Alberto , Incidental ingestion of mesoand macro-plastic debris by benthic and demersal fish.. The address for the corresponding author was captured as affiliation for all authors. Please check if appropriate. Fooweb(2017), https://doi.org/10.1016/j.fooweb.2017.12.002

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ACCEPTED MANUSCRIPT Incidental ingestion of meso- and macro-plastic debris by benthic and demersal fish. López-López, Lucía1, Preciado, Izaskun1, González-Irusta, José Manuel1, Arroyo, Nina Larissa1,Muñoz, Isabel1, Punzón, Antonio1, Serrano, Alberto1 1

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Spanish Institute of Oceanography. Promontorio de San Martín s/n.39004 Santander, Spain.

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ACCEPTED MANUSCRIPT Abstract We examine the ingestion of meso- and macro-plastics by teleost fish and elasmobrachs with benthic- demersal dwelling habits, analysing the occurrence of this litter type on the diet of 39 of these species over the North-western Iberian Shelf Sea between 1999

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and 2016. Plastic consumption seems to be incidental, occurring only in 7 of the 39 species examined, and in a very low proportion (<0.3% of individuals in all cases). The

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highest rates were found among benthic feeding elasmobranchs, including Leucoraja

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naevus, Scyliorhinus canicula and Galeus spp., the two latter being opportunistic scavengers. While our study rules out a high occurrence of meso- and macro- plastics in

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benthic fauna, the presence of micro-plastics in the diet of these species is still a major

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concern, as the deep sea is possibly a natural sink for these litter particles. Keywords: Marine litter, teleosts, elasmobranchs, diet, continental shelf, Southern Bay

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of Biscay

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ACCEPTED MANUSCRIPT Marine environments are increasingly being polluted by litter as its input rate in the sea largely exceeds its degradation time. This is particularly true for plastic litter, which degrades exceptionally slowly due to its high stability and durability, two of the main reasons for its industrial relevance (Zheng et al., 2005). Indeed, plastics constitute the bulk of marine litter worldwide (reviewed in Derraik, 2002) and are considered a major

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threat to ecosystems (Depledge et al., 2013; Pham et al., 2014) with multipleimpacts on

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marine fauna. For example, after ingestion, products derived from plastic degradation in

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the digestive tract may translocate to the animal's fluids (Browne et al., 2008), and organic pollutants adsorbed on the surface of litter items may also get released

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(Teutenet al., 2007, Rios et al., 2010, Rochman, 2015). Micro-plastics have been found in the dietsof pelagic, demersal and benthic fish and elasmobranchs (Lusher et al., 2013,

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Neves et al., 2015, Bellas et al., 2016, Alomar and Deudero, 2017) and are also ingested by zooplankton (Cole et al., 2013, Setälä et al., 2014), possibly impacting a wide range

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of ecological processes (Galloway et al., 2017). The ingestion of meso- and macro-

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plastics, has been extensively reported in pelagic top predators (e.g., Markaida and Sosa-Nishizaki, 2010, Williams et al., 2011, de Stephanis et al., 2013, van Frankener

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and Law, 2015), which may increase satiation and/or obstruct their intestinal tract, often with fatal consequences (reviewed in Gall and Thompson, 2015). Conversely, ingestion

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of meso- and macro-plastics by demersal and benthic species, has been rarely reported and is considered to be infrequent (Anastasopoulou et al., 2013, Deudero and Alomar, 2015).

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Figure 1. Map of the North-western Iberian Shelf Sea, showing the location of all sampling hauls in the period 1999-2016 (open points) and plastics ingestion incidents (solid points) and the 100, 200 and 500 isobaths.

We analysed the occurrence of meso- (5-25 mm) and macro-plastics (>25 mm) (EC

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JRC, 2013) in the diet of 39 benthic-demersal teleost fish and elasmobranchs sampled

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along the North-western Iberian Shelf Sea (NISS) between 1999 and 2016. Sampling was carried out during bottom trawl oceanographic surveys (DEMERSALES surveys-

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under ICES IBTSWG standardisation, ICES, 2010). The surveys follow a randomly stratified sampling design in five geographical sectors and three depth ranges: 70-120

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m., 120-200mand 200-500 m (for a complete description of the survey design see Sánchez and Serrano, 2003). After each haul, 10 individuals of each target species were set aside for an extended biological sampling. The sampling effort was higher for Lepidorhombus bosccii, Lepidorhombus whiffiagonis and Merluccius merluccius, which were split into different size ranges based on ontogenetic changes in their diet. Thus, except for these three species, the total number of individuals sampled may reflect its frequency of occurrence in the environment. As part of the extended biological

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ACCEPTED MANUSCRIPT sampling, stomach content volume was registered and prey were measured when possible. Marine litter items, in the size range of the main prey pool for each predator, were also systematically identified in three categories, i.e. plastics, wood or metal, and their relative volume estimated as part of the total stomach volume. As wood can have both natural and anthropogenic origin, and no metal debris was detected, our study

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focuses on plastic ingestion.

Mean prey size ± Prey size range Nºguts with SE(mm) (mm) plastics (%)

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Nº fish analysed

PREDATOR SPECIES

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Table 1. Predator species analysed between 1999 and 2016, indicating prey size and the number of stomachs in which meso- and macro-plastic was identified.

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40 ± 2

34 - 52

0

Callionymus lyra

2116

9±1

1 - 117

0

Chelidonichthys cuculus

3503

20 ± 0

1 - 390

1 (0,03 %)

Chelidonichthys gurnardus

2853

24 ± 1

1 - 205

0

1019

36 ± 2

2 - 356

0

412

11 ± 1

2 - 73

0

7007

49 ± 1

1 - 380

1 (0,01 %)

130

106 ± 19

24 - 220

0

756

44 ± 2

7 - 120

0

725

21 ± 1

1 - 120

0

2962

41 ± 1

3 - 270

3 (0.10 %)

3618

25 ± 1

1 - 180

0

25914

22 ± 0

1 - 226

0

6753

42 ± 1

1 - 324

0

34

49 ± 11

5 - 132

0

Leucoraja naevus

381

31 ± 2

2 - 184

1 (0.26 %)

Lophius budegassa

505

111 ± 6

5 - 450

0

Lophius piscatorius

1382

100 ± 4

5 - 520

0

63

95 ± 55

4 - 271

0

16164

99 ± 1

1 - 570

0

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Chelidonichthys lucerna Chelidonichthys obscurus

Deania calcea Etmopterus spinax

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Conger conger

Galeus spp.

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Gaidropsaurus macrophthalmus

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Helicolenus dactylopterus Lepidorhombus boscii

Lepidorhombus whiffiagonis Leucoraja circularis

Lythognathus mormyrus Merluccius merluccius

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Aphanopus carbo

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ACCEPTED MANUSCRIPT 39 ± 1

1 - 215

2 (0,02 %)

990

74 ± 2

2 - 250

0

Mullus surmuletus

1298

19 ± 1

1 - 267

0

Pagellus acarne

1917

19 ± 11

1 - 215

0

Pagellus bogaraveo

174

18 ± 3

2 - 41

0

Pagellus erythrinus

370

24 ± 4

1 - 212

0

Phycis blennoides

1828

22 ± 1

2 - 180

0

Raja clavata

2705

28 ± 1

1 - 285

0

Raja montagui

1421

30 ± 1

1 - 270

0

Scorpaena loppei

104

19 ± 2

4 - 65

0

Scorpaena scrofa

51

41 ± 7

8 - 160

0

9981

32 ± 1

2 - 485

7 (0.07 %)

115 ± 13

18 - 265

0

29 ± 7

2 - 127

0

49

70 ± 18

10 - 231

0

1488

15 ± 1

1 - 174

0

3076

21 ± 0

2 - 221

1 (0.03 %)

2062

18 ± 1

1 - 216

0

1346

80 ± 3

2 - 493

0

Scyliorhinus canicula Scymnodon ringens

49 284

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Spondyliosoma cantharus Trachyscorpia cristulata

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Trigla lyra

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Zeus faber

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Trisopterus luscus Trisopterus minutus

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Molva macrophthalma

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10575

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Micromesistius poutassou

Plastic debris was identified in only 16 individuals from the 116,076 analysed over the

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1999-2016 period (0.014%, Table 1). Litter ingestion was recorded in 7 of the 39studied species (Table 1); the highest incidence occurring within the benthic shark and ray group (Table 1). The ray Leucoraja naevus showed the highest consumption (0.26%, 1 occurrence), followed by Galeus spp. (0.10%,3 occurrences) and Scyliorhinus canicula (0.07%, 7 occurrences).These elasmobranchs are essentially benthic feeders and the two latter are known to be opportunistic scavengers (Olaso et al., 1998, Madurell et al., 2003, Olaso et al., 2005; Anastasopoulou et al., 2013b).

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ACCEPTED MANUSCRIPT The categories of meso- and macro-plastics, ranging between 5-25 mm and >25 mm, respectively (EC JRC, 2013), coincide with the mean prey size identified for all predators (Table 1). The relative volume of the plastic litter ingested was highly variable and was found with other food remains in 11 out of the 16 individuals (Table 2). Plastic ingestion was scattered both in time and space (Fig. 1 and Table 2), showing no clear

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trends, but the low incidence of litter recorded prevented us from undertaking any

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further analyses.

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Table 2. Details of the 16 incidentsof plastic ingestion by benthic-demersal between 1999-2016. Relative litter volume refers to the litter volume in relation to total stomach contents (100% meaning the stomach contained only litter). PREDATOR SPECIES

1,2

20%

Scyliorhinus canicula

54

0,65

10%

2002

Conger conger

27

0,1

100%

2002

Scyliorhinus canicula

58

0,5

10%

2006

Micromesistius poutassou

12

0,1

100%

2007

Leucoraja naevus

52

0,5

33%

2008

Galeus spp.

30

0,3

100%

2008

Galeus spp.

32

1,8

90%

2009

Micromesistius poutassou

24

0,3

100%

Scyliorhinus canicula

26

0,3

10%

Scyliorhinus canicula

33

0,12

4%

2009

Trisopterus luscus

21

<0,1

1%

2010

Galeus spp.

36

0,5

100%

2014

Chelidonichthys cuculus

25

0,1

5%

2015

Scyliorhinus canicula

47

1,2

30%

2016

Scyliorhinus canicula

42

5

50%

2009

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2009

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2001

48

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Scyliorhinus canicula

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2001

PREDATOR LITTER RELATIVE SIZE (cm.) VOLUME (cc) LITTER VOLUME

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YEAR

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ACCEPTED MANUSCRIPT The low values of ingestion of meso- and macro-plastics in benthic- demersal teleosts and elasmobranches may be due to several causes. Comparing our results with those of pelagic predators (e.g., Markaida and Sosa-Nishizaki, 2010, Williams et al., 2011, de Stephanis et al., 2013, van Frankener and Law, 2015), the incidence of meso- and macro- plastic litter in the benthic- demersal community was considerably lower. While

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this result could be derived from the lower abundance of macro-plastic in deep-sea

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environments compared with floating plastics, behavioural and/or physiological causes

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should also be considered. Marine fauna rely on different senses for prey detection depending on the habitat they dwell in. While pelagic predators seem to rely

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preferentially on visual cues and the lateral line, benthic predators depend mostly on olfactory cues (Wagner et al., 2002). In addition, the resemblance of litter items to

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pelagic fauna may confuse pelagic predators (e.g., plastic bags can be mistaken with jellyfish by marine turtles, Mrosovsky, 1981), but litter items have generally little

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resemblance to benthic prey. Therefore, plastics may not be identified as food for most

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benthic- demersal predators. It is noteworthy that benthic sharks are responsible for most of the plastic ingestion incidents; in addition to their inferior mouth and

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opportunistic diet other specificities of their feeding behaviour could be involved in their higher rates of plastic ingestion. Other studies have pointed to the ingestion of

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metal debris by benthic elasmobranchs (e.g. Anasasopoulou et al., 2013a),who would be attracted to this type of litter because of their electro-sensory system (Moss, 1984), however, we did not find any metal item in the stomach contents in our samples. Global patterns of marine litter distribution are also fundamental to explain these results, as the severity of litter pollution differs among regional seas. Regarding benthic litter, the NISS seems to be one of the least polluted European shelves (Lopez- Lopez et al., 2017). Indeed, higher values of occurrence of meso- and macro- plastic litter in 9

ACCEPTED MANUSCRIPT benthic- demersal fish and elasmobranchs have been reported over the Mediterranean Sea (Madurell, 2003, Anastasopoulou et al., 2013a).For example, Galeus melastomus ingested on average between 3-13 % of litter within its diet volume, while the benthic shark Etmopterus spinax, which did not show any plastic ingestion in our study, consumed on average between 6-8% of litter by volume in deep-sea Mediterranean

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waters (Madurell, 2003, Anastasopoulou et al., 2013a). Many other benthic-demersal

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species are known to include marine litter in their diet in small quantities (reviewed in

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Deudero and Alomar, 2015), but this may include micro-plastics and be a result of prey digestion (secondary consumption) rather than direct consumption (Au et al., 2017).

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Indeed, evidence of the occurrence of micro-plastics in the diet of marine fauna is increasing (Cole et al., 2013, Lusher et al., 2013, Setälä et al., 2014, Neves et al., 2015,

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Bellas et al., 2016, Alomar and Deudero, 2017).

Recent studies suggest that litter entering the marine environment does not accumulate

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in the sea surface, pointing to the sea bottom as one of the potential sinks for the litter (e.g. van Frankener and Law, 2015). Indeed, the deep ocean can be regarded as a longterm sink for marine plastics, as degradation times slow down due to the low

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hydrodynamism, reduced solar radiation (EC JRC, 2013), and the absence of biota able

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to degrade these substances (Nauendorf et al., 2016). Our results support the hypothesis that the ingestion of meso- and macro-plastics is incidental in the North-western Iberian Shelf Sea. However, the ingestion of micro-plastics by benthic feeding species in deep environments and its possible transfer through the food web should not be disregarded. Indeed, evidence of plastic fibers in the diet of deep sea organisms is accumulating (Taylor et al., 2016, Alomar and Deudero, 2017) and should be further investigated. Acknowledgements

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ACCEPTED MANUSCRIPT This work is based on data collected during the IBTS “Demersales” (1999-2016) framed within the ERDEM project.We are thankful to the crew of the R/V Cornide de Saavedra and R/V Miguel Oliver and to all colleagues who participated in these surveys, particularly those contributing to the trophic ecology team.

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