- Email: [email protected]
Plastic pollution affects American lobsters, Homarus americanus
Marine Pollution Bulletin 138 (2019) 545–548
Contents lists available at ScienceDirect
Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Note
Plastic pollution affects American lobsters, Homarus americanus Potocka Marta
a,b,⁎
b
, Bayer Robert C. , Potocki Mariusz
T
c,d
a
Department of Antarctic Biology, Institute of Biochemistry and Biophysics Polish Academy of Sciences, Pawińskiego St. 5a, 02-106 Warsaw, Poland Lobster Institute, University of Maine, 5722 Deering Hall 144, Orono, ME 04469, USA Climate Change Institute, University of Maine, Orono, ME 04469, USA d School of Earth and Climate Sciences, University of Maine, Orono, ME 04469, USA b c
A R T I C LE I N FO
A B S T R A C T
Keywords: American lobster Homarus americanus Plastic pollution Ingested plastics
This paper provides the first record of ingestion of plastic debris by American lobster, Homarus americanus. Plastics particles, identified as rubber pieces, were found in the stomachs of 3 from 17 individuals of lobsters kept in laboratory conditions. Debris had evidence of cuts, what suggest they were actively consumed.
1. Introduction The impact of plastic pollution on the marine environment is one of the most studied topics in recent years (Law, 2017; Andrady, 2011; Gall and Thompson, 2015; Eriksen et al., 2014: Bergmann et al., 2017). Plastic debris has been found in the oceans worldwide and global analysis reported a quarter of a billion metric tons of plastic suspended in the oceans (Cózar et al., 2014; Eriksen et al., 2014). Several potential impacts of plastic debris on marine wildlife were recognized, such as: i). injury, trapping, or drowning through entanglement, ii). internal injury, obstruction of the gut, accumulation of plastic material in the gut, damaging or clogging gills, iii). it can also act as a substrate means of transport for rafting organisms or as a substrate/shelter for benthic animals on the seafloor, iv). or it can be an attractant to fish or other marine life (Law, 2017; Kiessling et al., 2015). Influence of chemicals, emitted from or associated with plastic, was also studied (Koelmans et al., 2014; Ogata et al., 2009). Altogether several hundreds of marine species have been recognized to be affected by plastics at sea, including marine mammals, sea turtles, seabirds, fish, and invertebrates, mostly through its ingestion (Laist, 1987; Hartwig et al., 2007; Teuten et al., 2007; Savoca et al., 2016; Wójcik-Fudalewska et al., 2016; Ory et al., 2018). The negative effect of plastic consumption was widely described, especially for seabirds and marine mammals, as one of the most dangerous threats to their populations (Wilcox et al., 2015). The ingestion of this debris might take place through active consumption as was observed in vertebrates (Wilcox et al., 2015), or through passive consumption and absorption of microplastic particles from water, sediment, or embedded in natural
food (Gobas, 1993). Both may cause false satiation and a decrease in the nutritional state (Welden and Cowie, 2016; Wilcox et al., 2015). Plastic ingestion by invertebrates has been recognized and is an interest of many researchers, but our knowledge of its impact on animals is still limited. Most research has been focused on the influence of microplastics and chemicals connected with it on invertebrates (i.e. Jacobs et al., 2012; Laufer et al., 2011, 2012; Murray and Cowie, 2011; Brennecke et al., 2015; Abbasi et al., 2018). Microplastics have been found in tissues of many commercially important marine invertebrates, such as mussels, oysters (Avio et al., 2015; Farrell and Nelson, 2013), fish, or prawns (Abbasi et al., 2018; Murray and Cowie, 2011). This paper reports the first observation of plastic debris in the stomach of American lobster, Homarus americanus. 2. Methods Observations presented in this paper were made during the experiment of gastrolith development in American lobster in July 2018 in Lobster Institute, University of Maine, Maine, USA. American lobsters, H. americanus from Gulf of Maine, Casco Bay area (Portland ME, USA) of the east coast of USA, were obtained from commercial fishermen in July 2018. Hard-shell lobsters were sourced from different boats but were caught on the same day and in the same area. Vigor index (tail strength, antenna movements, tail position and eye responses) was determined using the method described by Spanoghe, 1996 (0- dead, 1- moribund, 2-weak, 3- healthy, 4-very healthy, 5-aggressive), and only lobsters with vital index 4 and 5 were chosen for further experiments. Animals were ultrasounded with a
⁎ Corresponding author at: Department of Antarctic Biology, Institute of Biochemistry and Biophysics Polish Academy of Sciences, Pawińskiego St. 5a, 02-106 Warsaw, Poland. E-mail address: [email protected] (M. Potocka).
https://doi.org/10.1016/j.marpolbul.2018.12.017 Received 23 November 2018; Received in revised form 11 December 2018; Accepted 11 December 2018 0025-326X/ © 2018 Published by Elsevier Ltd.
Marine Pollution Bulletin 138 (2019) 545–548
M. Potocka et al.
portable ultrasound device (Aloka 500 V with 7.5 MHz probe) to determine the molting stage of animals via development of their gastroliths (Potocka et al., 2015). Animals with no evidence of gastroliths were chosen for further experiment. Selected animals (17 individuals), with a rubber band on each claw (5 individuals with two bands on each claw), were transported in coolers to the laboratory in the Lobster Institute at the University of Maine, Orono, ME, USA, where they were kept in a cold-water tank system (mesocosms with two tanks volume 250 l each). Water conditions were stable (S 32 PSU, T 13 °C and pH 8.1), and similar to the natural environment. All animals were measured (wet weight, carapace length). Animals were kept in laboratory conditions for 16 days, and not fed what was required for original experiment. After this period, all animals were dissected.
Table 1 Size (length/width) of rubber particles found in lobster's stomachs. Lobster no. 1
Lobster no. 2
Lobster no. 3
3 mm/10 mm
10 mm/6 mm 8 mm/9 mm
13 mm/9 mm 8 mm/8 mm 10 mm/8 mm 8 mm/6 mm 10 mm/10 mm 8 mm/5 mm
the stomachs of 3 specimens (Fig. 1, Table 1). Animals with plastic particles in stomachs were different than those which lost their bands during the experiment. Rubber bands on their claws were undamaged for the whole period of experiment. Rubber particles from lobster's stomachs were irregular in shape and had traces of cuts (Fig. 1). There was no other content of stomachs of studied animals.
3. Results Mean wet weight of animals was 586 g (SD = 107.1) and carapace length 88.9 mm (SD = 5.05). Ultrasound scanning didn't indicate any objects in the lobsters' stomachs. All lobsters in experimental tanks had undamaged rubber bands on the claws. During routine control of tanks, on the 3rd day of experiment, 4 animals without bands were noticed. Pieces of rubber bands were found in the tank, and removed. Lost bands on lobster's claws have been replaced. All animals were in a good condition (vital index 4 and 5) at the end of the experiment. After dissection, rubber band particles were found in
4. Discussion This is the first, to our knowledge, finding of plastics ingestion in American lobsters. Probably rubber particles were actively consumed during the experiment, which is suggested by cut traces on the rubber edges. Presence of plastics in decapods' stomachs were also recorded in Nephrops norvegicus (Murray and Cowie, 2011), but it was passively ingested with sediment. Another record of passive ingestion of nylon
Fig. 1. Rubber band particles found in American lobsters' stomachs. 546
Marine Pollution Bulletin 138 (2019) 545–548
M. Potocka et al.
filament was observed in shrimps, Plesionika narval (Bordbar et al., 2018). Microplastic can also be transferred in the tissues of crustaceans' prey, as it was found by Farrell and Nelson, 2013in crabs' digestive system. Incidental records of plastic pieces in American lobsters' stomachs were noted before (Scarrat, 1980; Elner and Campbell, 1987), but without any information on the ingestion route. Due to growing concerns of plastic pollution in the marine environment, more frequent observations of debris ingestion in crustaceans are expected. The implications of this phenomena on the physiology and ecology of lobsters are not well known, and they may have a serious influence on populations of these commercially and culturally important animals. It's still largely unknown how marine animals can mistake plastics for their natural food. Plastic debris, after exposure to saltwater, can be overgrown by epifauna or algae, and can emit the scent of food (Seymour et al., 2010). Furthermore, Savoca et al. (2016) indicated that biota growing on microplastics produce infochemicals, which can serve as an attractant to marine wildlife. Most marine crustaceans use chemical stimuli to find food (Pearson and Olla, 1977; Markowska et al., 2008a, 2008b; Kidawa et al., 2008; Kidawa et al., 2004; Derby et al., 2016; Atema and Steinbach, 2007). It is especially important for marine benthic decapods as they occur in low-light environment and feed at night (Zhou and Rebach, 1999; Kidawa et al., 2004). Lobsters are scavengers, but also eat fresh food such as crabs, mussels, or even plants. This kind of diet can explain rubber particles in their stomach. Pieces of rubber on the bottom of the tank resembled lobster's natural food, probably with some algae growing on them, probably emitted chemoattractant. We can suspect that in the natural environment plastic debris may also be mistakenly eaten by lobsters as natural food, especially when food amount is limited, as it occurred in our experiment. Furthermore, chemicals emitted from plastic debris may affect functioning of chemoreceptors, distorting information that animals receive from the environment (Blinova and Cherkashin, 2012). It may lead to changes in animals' behavior with further consequences for their survival. Consumption of bigger pieces of plastic can cause false satiation or even clog the gut, which may be lethal for most of the animals (Savoca et al., 2016). Smaller pieces, such as microplastic strands, may accumulate within crustacean tissues (Murray and Cowie, 2011), and can be further transferred to the next levels of food chain, also to humans (Kontrick, 2018). So far we know that alkylphenols, products used i.e. in plastic manufacture or petroleum recovery, were discovered in lobster's hemolymph (Jacobs et al., 2012) and they have serious negative influence on animals' physiology: larval survival and metamorphosis (Laufer et al., 2011) or shell hardening during molting (Laufer et al., 2012). Through a delay in the hardening response, pollutants such as alkylphenols may exacerbate shell disease, which can further influence, on the whole, lobster stocks (Laufer et al., 2005). Our observations, although noticed by accident, showed that the problem of plastic pollution also affects American lobsters and special attention should be paid to this issue. Further studies on its effect on large marine crustaceans are needed, as this knowledge may be vital in maintaining the sustainability and profitability of the lobster fishery.
Microplastics in different tissues of fish and prawn from the Musa Estuary, Persian Gulf. Chemosphere 205, 80–87. Andrady, A.L., 2011. Microplastics in the marine environment. Mar. Pollut. Bull. 62, 1596–1605. Atema, J., Steinbach, M.A., 2007. Chemical communication and social behavior of the lobster, Homarus americanus, and other Decapod Crustacea. In: Duffy, J.E., Thiel, M. (Eds.), Evolutionary Ecology of social and Sexual Systems: Crustaceans as Model Organisms. Oxford University Press, New York NY, USA, pp. 115–144. Avio, C.G., Gorbi, S., Milan, M., Benedetti, M., Fottorini, D., D'Errico, G., Pauletto, M., Bargelloni, L., Regoli, F., 2015. Pollutants bioavailability and toxicological risk from microplastics to marine mussels. Environ. Pollut. 198, 211–222. Bergmann, M., Tekman, M.B., Gutow, L., 2017. Marine litter: sea change for plastic pollution. Nature 544, 297. https://doi.org/10.1038/544297a. Blinova, N.K., Cherkashin, S.A., 2012. The olfactory system of crustaceans as a model for ecologo-toxicological studies. J. Evol. Biochem. Physiol. 48 (2), 155–165. Bordbar, L., Kapiris, K., Kalogirou, S., Anastasopoulou, A., 2018. First evidence of ingested plastics by a high commercial shrimp species (Plesionika narval) in the eastern Mediterranean. Mar. Pollut. Bull. 136, 472–476. Brennecke, D., Ferreira, E.C., Tarso, M.M., Costa, M., Appel, B., da Gama, B.A.P., Lenz, M., 2015. Ingested microplastics (> 100 μm) are translocated to organs of the tropical fiddler crab Uca rapax. Mar. Pollut. Bull. 96, 491–495. Cózar, A., Echevarría, F., González-Gordillo, J.I., Irigoien, X., Úbeda, B., Hernández-León, S., Palma, A.T., Navarro, S., García-De-Lomas, J., Ruiz, A., Fernández-De-Puelles, M.L., Duarte, C.M., 2014. Plastic debris in the open ocean. Proc. Natl. Acad. Sci. U. S. A. 111, 10239–10244. Derby, C.D., Kozma, M.T., Senatore, A., Schmidt, M., 2016. Molecular mechanisms of reception and perireception in crustacean chemoreception: a comparative review. Chem. Senses 41 (5), 381–398. https://doi.org/10.1093/chemse/bjw057. Elner, R.W., Campbell, A., 1987. Natural diets of lobster Homarus americanus from barren ground and macroalgal habitats off southwestern Nova Scotia, Canada. Mar. Ecol. Prog. Ser. 37, 131–140. Eriksen, M., Lebreton, L.C.M., Carson, H.S., Thiel, M., Moore, C.J., Borerro, J.C., Galgani, F., Ryan, P.G., Reisser, J., 2014. Plastic pollution in the world's oceans: more than 5 trillion plastic pieces weighing over 250,000 tons afloat at sea. PLoS One 9, e111913. Farrell, P., Nelson, K., 2013. Trophic level transfer of microplastics: Mytilus edulis (L.) to Carcinus maenas (L.). Environ. Pollut. 177 (1–3). Gall, S.C., Thompson, R.C., 2015. The impact of debris on marine life. Mar. Pollut. Bull. 92, 170–179. Gobas, F.A.P.C., 1993. A model for predicting the bioaccumulation of hydrophobic organic chemicals in aquatic food webs: application to Lake Ontario. Ecol. Model. 69, 1–17. Hartwig, E., Clemens, T., Hechroth, M., 2007. Plastic debris as nesting material in a Kittiwake (Rissa tridactyla) colony at the Jammerbugt, Northwest Denmark. Mar. Pollut. Bull. 54, 595–597. Jacobs, M., Laufer, H., Stuart, J., Chen, M., Pan, X., 2012. Endocrine-disrupting alkylphenols are widespread in the blood of lobsters from southern New England and adjacent offshore areas. J. Shellfish Res. 31 (2), 563–571. Kidawa, A., Markowska, M., Rakusa-Suszczewski, S., 2004. Chemosensory behaviour in the mud crab, Rhithropanopeus harrisii tridentatus, from Martwa Wisla estuary (Gdansk Bay, Baltic Sea). Crustaceana 77 (8), 897–908. Kidawa, A., Stepanowska, K., Markowska, M., Rakusa-Suszczewski, S., 2008. Fish blood as a chemical signal for Antarctic marine invertebrates. Polar Biol. 31, 519–525. Kiessling, T., Gutow, L., Thiel, M., 2015. Marine litter as habitat and dispersal vector. In: Bergmann, M., Gutow, L., Klages, M. (Eds.), Marine Anthropogenic Litter, pp. 141–180. Koelmans, A.A., Besseling, E., Foekema, E.M., 2014. Leaching of plastic additives to marine organisms. Environ. Pollut. 187, 49–54. Kontrick, A.V., 2018. Microplastics and human health: our great future to think about now. J. Med. Toxicol. 14 (2), 117–119. Laist, D.W., 1987. Overview of the biological effects of lost and discarded plastic debris in the marine environment. Mar. Pollut. Bull. 18, 319–326. Laufer, H., Demir, N., Pan, X., 2005. Shell disease in the American lobster and its possible relations to alkylphenols. N. Engl. Aquar. J. 05, 73–75. Laufer, H., Baclaski, B., Koehen, U., 2011. Alkylphenols affect lobster (Homarus americanus) larval survival, molting and metamorphosis. Int. J. Invertebr. Reprod. Dev. 56, 66–71. Laufer, H., Chen, M., Johnson, M., Demir, N., Bobbitt, J.M., 2012. The effect of alkylphenols on lobster shell hardening. J. Shellfish Res. 31, 555–562. https://doi.org/10. 2983/035.031.0215. Law, K.L., 2017. Plastics in the marine environment. Annu. Rev. Mar. Sci. 2017 (9), 205–229. Markowska, M., Janecki, T., Kidawa, A., 2008a. Field observation of spider crab Hyas araneus feeding behaviour in the Arctic fjord. Crustaceana 81 (10), 1211–1217. Markowska, M., Kidawa, A., Janecki, T., 2008b. Amino acids as a food signals for two Arctic decapods Hyas araneus and Eupagurus pubescens. Polish Polar Res. 29 (3), 219–226. Murray, F., Cowie, P.R., 2011. Plastic contamination in the decapod crustacean Nephrops norvegicus (Linnaeus, 1758). Mar. Pollut. Bull. 62, 1207–1217. Ogata, Y., Takada, H., Mizukawa, K., Hirai, H., Iwasa, S., et al., 2009. International Pellet Watch: global monitoring of persistent organic pollutants (POPs) in coastal waters. 1. Initial phase data on PCBs, DDTs, and HCHs. Mar. Pollut. Bull. 58, 1437–1446. Ory, N.C., Gallardo, C., Lenz, M., Thiel, M., 2018. Capture, swallowing, and egestion of microplastics by a planktivorous juvenile fish. Environ. Pollut. 240, 566–573. Pearson, W.H., Olla, B.L., 1977. Chemoreception in the blue crab, Callinectes sapidus. Biol. Bull. 153, 346–354. Potocka, M., Bayer, R., Stolarski, J., Bowden, T., 2015. The implementation of ultrasound
Acknowledgment The authors would like to thank Luke Holden from Luke's Lobster for lobsters' donation. The authors also would like to thank Dr. Timothy Bowden and Brian M. Preziosi from School of Food and Agriculture, Aquaculture Research Institute, University of Maine, Orono, ME for allow us to use the cold-water tank system, and Dr. James A. Weber from Department of Animal and Veterinary Sciences, University of Maine, Orono, ME, USA for allow us to use the ultrasound device. References Abbasi, S., Soltani, N., Keshavarzi, B., Moore, F., Turner, A., Hassanaghaei, M., 2018.
547
Marine Pollution Bulletin 138 (2019) 545–548
M. Potocka et al.
Teuten, E.L., Rowland, S.J., Galloway, T.S., Thompson, R.C., 2007. Potential for plastics to transport hydrophobic contaminants. Environ. Sci. Technol. 41, 7759–7764. Welden, N.A., Cowie, P.R., 2016. Environment and gut morphology influence microplastic retention in langoustine Nephrops norvegicus. Environ. Pollut. 214, 859–865. Wilcox, C., Van Sebille, E., Hardesty, B.D., 2015. Threat of plastic pollution to seabirds is global, pervasive, and increasing. PNAS 112 (38), 11899–11904. Wójcik-Fudalewska, D., Normant-Saremba, M., Anastacio, P., 2016. Occurrence of plastic debris in the stomach of the invasive crab Eriocheir sinensis. Mar. Pollut. Bull. 113 (1–2), 306–311. Zhou, T., Rebach, S., 1999. Chemosensory orientation of the rock crab Cancer irroratus. Journ. Chem. Ecol. 25, 315–329.
technique as a method to evaluate gastroliths development in American lobster, Homarus americanus. In: FRAM Science Days, Conference Papers, Tromso Nov. 2015. Savoca, M.S., Wohlfeil, M.E., Ebeler, S.E., Nevitt, G.A., 2016. Marine plastic debris emits a keystone infochemical for olfactory foraging seabirds. Sci. Adv. 2, e1600395. Scarrat, D.J., 1980. The food of lobsters. Can. Tech. Rep. Fish. Aquat. Sci. 954, 66–91. Seymour, J.R., Simo, R., Ahmed, T., Stocker, R., 2010. Chemoattraction to dimethylsulfoniopropionate throughout the marine microbial food web. Science 329, 342–345. Spanoghe, P.T., 1996. An Investigation of the Physiological and Biochemical Responses Elicited by Panulirus Cygnus to Harvesting, Holding and Live Transport. School of Biomedical Sciences, Curtin University, Perth, Western Australia (Doctoral thesis, 378 pp).
548
Contents lists available at ScienceDirect
Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Note
Plastic pollution affects American lobsters, Homarus americanus Potocka Marta
a,b,⁎
b
, Bayer Robert C. , Potocki Mariusz
T
c,d
a
Department of Antarctic Biology, Institute of Biochemistry and Biophysics Polish Academy of Sciences, Pawińskiego St. 5a, 02-106 Warsaw, Poland Lobster Institute, University of Maine, 5722 Deering Hall 144, Orono, ME 04469, USA Climate Change Institute, University of Maine, Orono, ME 04469, USA d School of Earth and Climate Sciences, University of Maine, Orono, ME 04469, USA b c
A R T I C LE I N FO
A B S T R A C T
Keywords: American lobster Homarus americanus Plastic pollution Ingested plastics
This paper provides the first record of ingestion of plastic debris by American lobster, Homarus americanus. Plastics particles, identified as rubber pieces, were found in the stomachs of 3 from 17 individuals of lobsters kept in laboratory conditions. Debris had evidence of cuts, what suggest they were actively consumed.
1. Introduction The impact of plastic pollution on the marine environment is one of the most studied topics in recent years (Law, 2017; Andrady, 2011; Gall and Thompson, 2015; Eriksen et al., 2014: Bergmann et al., 2017). Plastic debris has been found in the oceans worldwide and global analysis reported a quarter of a billion metric tons of plastic suspended in the oceans (Cózar et al., 2014; Eriksen et al., 2014). Several potential impacts of plastic debris on marine wildlife were recognized, such as: i). injury, trapping, or drowning through entanglement, ii). internal injury, obstruction of the gut, accumulation of plastic material in the gut, damaging or clogging gills, iii). it can also act as a substrate means of transport for rafting organisms or as a substrate/shelter for benthic animals on the seafloor, iv). or it can be an attractant to fish or other marine life (Law, 2017; Kiessling et al., 2015). Influence of chemicals, emitted from or associated with plastic, was also studied (Koelmans et al., 2014; Ogata et al., 2009). Altogether several hundreds of marine species have been recognized to be affected by plastics at sea, including marine mammals, sea turtles, seabirds, fish, and invertebrates, mostly through its ingestion (Laist, 1987; Hartwig et al., 2007; Teuten et al., 2007; Savoca et al., 2016; Wójcik-Fudalewska et al., 2016; Ory et al., 2018). The negative effect of plastic consumption was widely described, especially for seabirds and marine mammals, as one of the most dangerous threats to their populations (Wilcox et al., 2015). The ingestion of this debris might take place through active consumption as was observed in vertebrates (Wilcox et al., 2015), or through passive consumption and absorption of microplastic particles from water, sediment, or embedded in natural
food (Gobas, 1993). Both may cause false satiation and a decrease in the nutritional state (Welden and Cowie, 2016; Wilcox et al., 2015). Plastic ingestion by invertebrates has been recognized and is an interest of many researchers, but our knowledge of its impact on animals is still limited. Most research has been focused on the influence of microplastics and chemicals connected with it on invertebrates (i.e. Jacobs et al., 2012; Laufer et al., 2011, 2012; Murray and Cowie, 2011; Brennecke et al., 2015; Abbasi et al., 2018). Microplastics have been found in tissues of many commercially important marine invertebrates, such as mussels, oysters (Avio et al., 2015; Farrell and Nelson, 2013), fish, or prawns (Abbasi et al., 2018; Murray and Cowie, 2011). This paper reports the first observation of plastic debris in the stomach of American lobster, Homarus americanus. 2. Methods Observations presented in this paper were made during the experiment of gastrolith development in American lobster in July 2018 in Lobster Institute, University of Maine, Maine, USA. American lobsters, H. americanus from Gulf of Maine, Casco Bay area (Portland ME, USA) of the east coast of USA, were obtained from commercial fishermen in July 2018. Hard-shell lobsters were sourced from different boats but were caught on the same day and in the same area. Vigor index (tail strength, antenna movements, tail position and eye responses) was determined using the method described by Spanoghe, 1996 (0- dead, 1- moribund, 2-weak, 3- healthy, 4-very healthy, 5-aggressive), and only lobsters with vital index 4 and 5 were chosen for further experiments. Animals were ultrasounded with a
⁎ Corresponding author at: Department of Antarctic Biology, Institute of Biochemistry and Biophysics Polish Academy of Sciences, Pawińskiego St. 5a, 02-106 Warsaw, Poland. E-mail address: [email protected] (M. Potocka).
https://doi.org/10.1016/j.marpolbul.2018.12.017 Received 23 November 2018; Received in revised form 11 December 2018; Accepted 11 December 2018 0025-326X/ © 2018 Published by Elsevier Ltd.
Marine Pollution Bulletin 138 (2019) 545–548
M. Potocka et al.
portable ultrasound device (Aloka 500 V with 7.5 MHz probe) to determine the molting stage of animals via development of their gastroliths (Potocka et al., 2015). Animals with no evidence of gastroliths were chosen for further experiment. Selected animals (17 individuals), with a rubber band on each claw (5 individuals with two bands on each claw), were transported in coolers to the laboratory in the Lobster Institute at the University of Maine, Orono, ME, USA, where they were kept in a cold-water tank system (mesocosms with two tanks volume 250 l each). Water conditions were stable (S 32 PSU, T 13 °C and pH 8.1), and similar to the natural environment. All animals were measured (wet weight, carapace length). Animals were kept in laboratory conditions for 16 days, and not fed what was required for original experiment. After this period, all animals were dissected.
Table 1 Size (length/width) of rubber particles found in lobster's stomachs. Lobster no. 1
Lobster no. 2
Lobster no. 3
3 mm/10 mm
10 mm/6 mm 8 mm/9 mm
13 mm/9 mm 8 mm/8 mm 10 mm/8 mm 8 mm/6 mm 10 mm/10 mm 8 mm/5 mm
the stomachs of 3 specimens (Fig. 1, Table 1). Animals with plastic particles in stomachs were different than those which lost their bands during the experiment. Rubber bands on their claws were undamaged for the whole period of experiment. Rubber particles from lobster's stomachs were irregular in shape and had traces of cuts (Fig. 1). There was no other content of stomachs of studied animals.
3. Results Mean wet weight of animals was 586 g (SD = 107.1) and carapace length 88.9 mm (SD = 5.05). Ultrasound scanning didn't indicate any objects in the lobsters' stomachs. All lobsters in experimental tanks had undamaged rubber bands on the claws. During routine control of tanks, on the 3rd day of experiment, 4 animals without bands were noticed. Pieces of rubber bands were found in the tank, and removed. Lost bands on lobster's claws have been replaced. All animals were in a good condition (vital index 4 and 5) at the end of the experiment. After dissection, rubber band particles were found in
4. Discussion This is the first, to our knowledge, finding of plastics ingestion in American lobsters. Probably rubber particles were actively consumed during the experiment, which is suggested by cut traces on the rubber edges. Presence of plastics in decapods' stomachs were also recorded in Nephrops norvegicus (Murray and Cowie, 2011), but it was passively ingested with sediment. Another record of passive ingestion of nylon
Fig. 1. Rubber band particles found in American lobsters' stomachs. 546
Marine Pollution Bulletin 138 (2019) 545–548
M. Potocka et al.
filament was observed in shrimps, Plesionika narval (Bordbar et al., 2018). Microplastic can also be transferred in the tissues of crustaceans' prey, as it was found by Farrell and Nelson, 2013in crabs' digestive system. Incidental records of plastic pieces in American lobsters' stomachs were noted before (Scarrat, 1980; Elner and Campbell, 1987), but without any information on the ingestion route. Due to growing concerns of plastic pollution in the marine environment, more frequent observations of debris ingestion in crustaceans are expected. The implications of this phenomena on the physiology and ecology of lobsters are not well known, and they may have a serious influence on populations of these commercially and culturally important animals. It's still largely unknown how marine animals can mistake plastics for their natural food. Plastic debris, after exposure to saltwater, can be overgrown by epifauna or algae, and can emit the scent of food (Seymour et al., 2010). Furthermore, Savoca et al. (2016) indicated that biota growing on microplastics produce infochemicals, which can serve as an attractant to marine wildlife. Most marine crustaceans use chemical stimuli to find food (Pearson and Olla, 1977; Markowska et al., 2008a, 2008b; Kidawa et al., 2008; Kidawa et al., 2004; Derby et al., 2016; Atema and Steinbach, 2007). It is especially important for marine benthic decapods as they occur in low-light environment and feed at night (Zhou and Rebach, 1999; Kidawa et al., 2004). Lobsters are scavengers, but also eat fresh food such as crabs, mussels, or even plants. This kind of diet can explain rubber particles in their stomach. Pieces of rubber on the bottom of the tank resembled lobster's natural food, probably with some algae growing on them, probably emitted chemoattractant. We can suspect that in the natural environment plastic debris may also be mistakenly eaten by lobsters as natural food, especially when food amount is limited, as it occurred in our experiment. Furthermore, chemicals emitted from plastic debris may affect functioning of chemoreceptors, distorting information that animals receive from the environment (Blinova and Cherkashin, 2012). It may lead to changes in animals' behavior with further consequences for their survival. Consumption of bigger pieces of plastic can cause false satiation or even clog the gut, which may be lethal for most of the animals (Savoca et al., 2016). Smaller pieces, such as microplastic strands, may accumulate within crustacean tissues (Murray and Cowie, 2011), and can be further transferred to the next levels of food chain, also to humans (Kontrick, 2018). So far we know that alkylphenols, products used i.e. in plastic manufacture or petroleum recovery, were discovered in lobster's hemolymph (Jacobs et al., 2012) and they have serious negative influence on animals' physiology: larval survival and metamorphosis (Laufer et al., 2011) or shell hardening during molting (Laufer et al., 2012). Through a delay in the hardening response, pollutants such as alkylphenols may exacerbate shell disease, which can further influence, on the whole, lobster stocks (Laufer et al., 2005). Our observations, although noticed by accident, showed that the problem of plastic pollution also affects American lobsters and special attention should be paid to this issue. Further studies on its effect on large marine crustaceans are needed, as this knowledge may be vital in maintaining the sustainability and profitability of the lobster fishery.
Microplastics in different tissues of fish and prawn from the Musa Estuary, Persian Gulf. Chemosphere 205, 80–87. Andrady, A.L., 2011. Microplastics in the marine environment. Mar. Pollut. Bull. 62, 1596–1605. Atema, J., Steinbach, M.A., 2007. Chemical communication and social behavior of the lobster, Homarus americanus, and other Decapod Crustacea. In: Duffy, J.E., Thiel, M. (Eds.), Evolutionary Ecology of social and Sexual Systems: Crustaceans as Model Organisms. Oxford University Press, New York NY, USA, pp. 115–144. Avio, C.G., Gorbi, S., Milan, M., Benedetti, M., Fottorini, D., D'Errico, G., Pauletto, M., Bargelloni, L., Regoli, F., 2015. Pollutants bioavailability and toxicological risk from microplastics to marine mussels. Environ. Pollut. 198, 211–222. Bergmann, M., Tekman, M.B., Gutow, L., 2017. Marine litter: sea change for plastic pollution. Nature 544, 297. https://doi.org/10.1038/544297a. Blinova, N.K., Cherkashin, S.A., 2012. The olfactory system of crustaceans as a model for ecologo-toxicological studies. J. Evol. Biochem. Physiol. 48 (2), 155–165. Bordbar, L., Kapiris, K., Kalogirou, S., Anastasopoulou, A., 2018. First evidence of ingested plastics by a high commercial shrimp species (Plesionika narval) in the eastern Mediterranean. Mar. Pollut. Bull. 136, 472–476. Brennecke, D., Ferreira, E.C., Tarso, M.M., Costa, M., Appel, B., da Gama, B.A.P., Lenz, M., 2015. Ingested microplastics (> 100 μm) are translocated to organs of the tropical fiddler crab Uca rapax. Mar. Pollut. Bull. 96, 491–495. Cózar, A., Echevarría, F., González-Gordillo, J.I., Irigoien, X., Úbeda, B., Hernández-León, S., Palma, A.T., Navarro, S., García-De-Lomas, J., Ruiz, A., Fernández-De-Puelles, M.L., Duarte, C.M., 2014. Plastic debris in the open ocean. Proc. Natl. Acad. Sci. U. S. A. 111, 10239–10244. Derby, C.D., Kozma, M.T., Senatore, A., Schmidt, M., 2016. Molecular mechanisms of reception and perireception in crustacean chemoreception: a comparative review. Chem. Senses 41 (5), 381–398. https://doi.org/10.1093/chemse/bjw057. Elner, R.W., Campbell, A., 1987. Natural diets of lobster Homarus americanus from barren ground and macroalgal habitats off southwestern Nova Scotia, Canada. Mar. Ecol. Prog. Ser. 37, 131–140. Eriksen, M., Lebreton, L.C.M., Carson, H.S., Thiel, M., Moore, C.J., Borerro, J.C., Galgani, F., Ryan, P.G., Reisser, J., 2014. Plastic pollution in the world's oceans: more than 5 trillion plastic pieces weighing over 250,000 tons afloat at sea. PLoS One 9, e111913. Farrell, P., Nelson, K., 2013. Trophic level transfer of microplastics: Mytilus edulis (L.) to Carcinus maenas (L.). Environ. Pollut. 177 (1–3). Gall, S.C., Thompson, R.C., 2015. The impact of debris on marine life. Mar. Pollut. Bull. 92, 170–179. Gobas, F.A.P.C., 1993. A model for predicting the bioaccumulation of hydrophobic organic chemicals in aquatic food webs: application to Lake Ontario. Ecol. Model. 69, 1–17. Hartwig, E., Clemens, T., Hechroth, M., 2007. Plastic debris as nesting material in a Kittiwake (Rissa tridactyla) colony at the Jammerbugt, Northwest Denmark. Mar. Pollut. Bull. 54, 595–597. Jacobs, M., Laufer, H., Stuart, J., Chen, M., Pan, X., 2012. Endocrine-disrupting alkylphenols are widespread in the blood of lobsters from southern New England and adjacent offshore areas. J. Shellfish Res. 31 (2), 563–571. Kidawa, A., Markowska, M., Rakusa-Suszczewski, S., 2004. Chemosensory behaviour in the mud crab, Rhithropanopeus harrisii tridentatus, from Martwa Wisla estuary (Gdansk Bay, Baltic Sea). Crustaceana 77 (8), 897–908. Kidawa, A., Stepanowska, K., Markowska, M., Rakusa-Suszczewski, S., 2008. Fish blood as a chemical signal for Antarctic marine invertebrates. Polar Biol. 31, 519–525. Kiessling, T., Gutow, L., Thiel, M., 2015. Marine litter as habitat and dispersal vector. In: Bergmann, M., Gutow, L., Klages, M. (Eds.), Marine Anthropogenic Litter, pp. 141–180. Koelmans, A.A., Besseling, E., Foekema, E.M., 2014. Leaching of plastic additives to marine organisms. Environ. Pollut. 187, 49–54. Kontrick, A.V., 2018. Microplastics and human health: our great future to think about now. J. Med. Toxicol. 14 (2), 117–119. Laist, D.W., 1987. Overview of the biological effects of lost and discarded plastic debris in the marine environment. Mar. Pollut. Bull. 18, 319–326. Laufer, H., Demir, N., Pan, X., 2005. Shell disease in the American lobster and its possible relations to alkylphenols. N. Engl. Aquar. J. 05, 73–75. Laufer, H., Baclaski, B., Koehen, U., 2011. Alkylphenols affect lobster (Homarus americanus) larval survival, molting and metamorphosis. Int. J. Invertebr. Reprod. Dev. 56, 66–71. Laufer, H., Chen, M., Johnson, M., Demir, N., Bobbitt, J.M., 2012. The effect of alkylphenols on lobster shell hardening. J. Shellfish Res. 31, 555–562. https://doi.org/10. 2983/035.031.0215. Law, K.L., 2017. Plastics in the marine environment. Annu. Rev. Mar. Sci. 2017 (9), 205–229. Markowska, M., Janecki, T., Kidawa, A., 2008a. Field observation of spider crab Hyas araneus feeding behaviour in the Arctic fjord. Crustaceana 81 (10), 1211–1217. Markowska, M., Kidawa, A., Janecki, T., 2008b. Amino acids as a food signals for two Arctic decapods Hyas araneus and Eupagurus pubescens. Polish Polar Res. 29 (3), 219–226. Murray, F., Cowie, P.R., 2011. Plastic contamination in the decapod crustacean Nephrops norvegicus (Linnaeus, 1758). Mar. Pollut. Bull. 62, 1207–1217. Ogata, Y., Takada, H., Mizukawa, K., Hirai, H., Iwasa, S., et al., 2009. International Pellet Watch: global monitoring of persistent organic pollutants (POPs) in coastal waters. 1. Initial phase data on PCBs, DDTs, and HCHs. Mar. Pollut. Bull. 58, 1437–1446. Ory, N.C., Gallardo, C., Lenz, M., Thiel, M., 2018. Capture, swallowing, and egestion of microplastics by a planktivorous juvenile fish. Environ. Pollut. 240, 566–573. Pearson, W.H., Olla, B.L., 1977. Chemoreception in the blue crab, Callinectes sapidus. Biol. Bull. 153, 346–354. Potocka, M., Bayer, R., Stolarski, J., Bowden, T., 2015. The implementation of ultrasound
Acknowledgment The authors would like to thank Luke Holden from Luke's Lobster for lobsters' donation. The authors also would like to thank Dr. Timothy Bowden and Brian M. Preziosi from School of Food and Agriculture, Aquaculture Research Institute, University of Maine, Orono, ME for allow us to use the cold-water tank system, and Dr. James A. Weber from Department of Animal and Veterinary Sciences, University of Maine, Orono, ME, USA for allow us to use the ultrasound device. References Abbasi, S., Soltani, N., Keshavarzi, B., Moore, F., Turner, A., Hassanaghaei, M., 2018.
547
Marine Pollution Bulletin 138 (2019) 545–548
M. Potocka et al.
Teuten, E.L., Rowland, S.J., Galloway, T.S., Thompson, R.C., 2007. Potential for plastics to transport hydrophobic contaminants. Environ. Sci. Technol. 41, 7759–7764. Welden, N.A., Cowie, P.R., 2016. Environment and gut morphology influence microplastic retention in langoustine Nephrops norvegicus. Environ. Pollut. 214, 859–865. Wilcox, C., Van Sebille, E., Hardesty, B.D., 2015. Threat of plastic pollution to seabirds is global, pervasive, and increasing. PNAS 112 (38), 11899–11904. Wójcik-Fudalewska, D., Normant-Saremba, M., Anastacio, P., 2016. Occurrence of plastic debris in the stomach of the invasive crab Eriocheir sinensis. Mar. Pollut. Bull. 113 (1–2), 306–311. Zhou, T., Rebach, S., 1999. Chemosensory orientation of the rock crab Cancer irroratus. Journ. Chem. Ecol. 25, 315–329.
technique as a method to evaluate gastroliths development in American lobster, Homarus americanus. In: FRAM Science Days, Conference Papers, Tromso Nov. 2015. Savoca, M.S., Wohlfeil, M.E., Ebeler, S.E., Nevitt, G.A., 2016. Marine plastic debris emits a keystone infochemical for olfactory foraging seabirds. Sci. Adv. 2, e1600395. Scarrat, D.J., 1980. The food of lobsters. Can. Tech. Rep. Fish. Aquat. Sci. 954, 66–91. Seymour, J.R., Simo, R., Ahmed, T., Stocker, R., 2010. Chemoattraction to dimethylsulfoniopropionate throughout the marine microbial food web. Science 329, 342–345. Spanoghe, P.T., 1996. An Investigation of the Physiological and Biochemical Responses Elicited by Panulirus Cygnus to Harvesting, Holding and Live Transport. School of Biomedical Sciences, Curtin University, Perth, Western Australia (Doctoral thesis, 378 pp).
548