Ecological Effects of Microplastics on Marine Food Webs

 The accelerated use of plastics and their by-products during the last century has resulted in the increased contamination of animal habitats. The consummation – a modern societal issue which poses the challenge of harmonizing the convenience of plastic in daily life with the expectancy of causing ecological harm. Plastics are synthetic polymers which are used for their flexibility and durability however, it is these specific characteristics that make plastics desirable,  which  also make them a pollutant in the marine environment. In aquatic surroundings, plastics are subjected to a process of weathering and fragmentation. This is as a result of the combined action of winds, UV exposure and abrasion, which breakdown the macrodebris into substantially smaller nanodebris. This breakdown of primary plastics results in microplastics – miniscule fragments less than 5mm in size (Browne et al 2008), and facilitates their uptake by marine biota into the food chain – which is not without its consequences .  Food webs are an important ecological concept, used to represent the flow of energy from one group of feeding organisms to another, inclusive of all the food chains in a community (Smith and Smith 2009). This essay will briefly explain the divergent routes through which microplastics infiltrate the marine food chain, examine the effects of the bioaccumulation and transfer across different trophic levels and conclude that although ecological ramifications on marine food webs and ecosystems have been documented, it is still a vastly understudied and not yet conclusive topic.

  Microplastics are found in marine ecosystems worldwide, from deep ocean sediments to coastal habitats and in areas as remote  as the poles (Obbard et al 2014). Because of the breadth and severity of the problem, the EC’s Marine Strategy Framework Directive have highlighted microplastics as a pollutant of global concern. Plastic pollution originates from land-based sources, as well as the fishing and shipping industries, which contribute markedly to the release and redistribution of microplastics. Microplastic litter consists of plastics manufactured to be of a microscope size (primary sources), for example cosmetic exfoliates and pre-production pellets (Napper et al 2015), and fragments derivational of the degradation process of greater plastic debris (secondary sources). More recently, Napper and Thompson (2015) examined the washing of clothes made of synthetic materials, such as; polyester, polyester-cotton blend and acrylics as an important origin of microscopic fibres emancipating into the environment. Their results concluded a 6kg wash cycle of such fabrics released up to 728,789 microscopic fibres, making it a considerable contributor.

  Plastics lack biodegradability, or more simply, they cannot be broken down by living organisms and are therefore resistant to microbial attack. Their short time of subsistence in nature is instrumental in the fact that evolution has not yet designed new enzyme structures which are accomplished in breaking down these synthetic polymers (Mueller 2006).   Correspondingly, owing to their small size and bioavailability, microplastics have been reported in biota throughout the world’s oceans, including zooplankton, fish, turtles and marine mammals, such as whales and sharks, crabs and seabirds (Outi et al 2018).  Food webs in the marine environment consist of a diversity of these organisms, each group commanding distinct niches and retaining divergent feeding strategies. It is this diversity which accounts for the numerous potential pathways for the transport of microplastics and their subsequent interference with biologically mediated ecological processes. Infiltration can occur via several routes, Outi et al (2018) evaluate the four main routes in their study: inhalation, ingestion, entanglement and trophic transfer. Organisms may unintentionally capture microplastics as food whilst filter or deposit feeding, mistake them for prey when foraging or ingest prey which already contain the microplastics, resulting in the trophic transfer.

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  At the base of the aquatic food web, phytoplankton serve as the vital primary producers. These single-celled plants, bacteria and algae harvest sunlight through photosynthesis and convert it to chemical energy for herbivorous consumers such as zooplankton. Bhattacharya et al (2010) were the first to examine the implications of exposure of PVC (polyvinyl chloride) microplastics on several algae species. They found that in Skeletonema costatum, growth was inhibited by 39.7% and in Chlorella,photosynthesis was affected in terms of reduced chlorophyll production when exposed to plastics 1 $\mu$

m in size. In both species studied, reactive oxygen species (ROS) generation was induced. Reactive oxygen species are a natural by-product of the normal metabolism of oxygen, however increase dramatically during times of environmental stress, potentially damaging cell structures (Devasagayam et al 2004). It was identified that due to the positive charge of cellulose, the retention of the negatively charged beads of plastic was expedited due to electrostatic attraction. Contrarily, when exposed to microplastics of 1mm in size there were no documented effects. This suggests that the smaller the size, the greater the toxicity.Lyakurwa (2017) reported that in Rhodomonas baltica exposure resulted in food replacement and subsequent loss of motility. It is important to examine these interactions between phytoplankton and microplastics in order to understand the impacts on biota via the consumption, such as on zooplankton and other herbivorous consumers.

  Zooplankton possess a vital role in the marine ecosystem as they consist of both primary consumers and the juvenile stage of copious commercially relevant species. These heterotrophic drifting organisms range in size from microscopic to large species, such as jellyfish. They form an integral component of the lower food chain due to the fact they are consumed by larger marine animals. Outi et al (2018) carried out several experiments with species from the Baltic Sea, to ascertain their potential to ingest microplastics. Using fluorescent polystyrene microspheres 10 $\mu$

m in size, they were able to conclude that all taxa studied (copepods, cladocerans, rotifers, polychaete larvae and ciliates) ingested the microspheres. These results are likely a consequence of the indiscriminate feeding modes exhibited by zooplankton, such as filter feeding, resulting in prey being non-selectively fed upon. Cole et al (2013) examined the direct impacts of microplastic ingestion by zooplankton and found organisms to have small plastics manifesting both internally and externally. Live copepods, after exposure, exhibited polystyrene beads aggregated within the alimentary canals and amidst the setae of antennules, furca, swimming legs and joints of external appendages. Effects such as these on appendages, which pose pivotal roles in the function and behaviour of organisms, may have further reverberations on locomotion, feeding and mating. Algal ingestion rate of the copepods was examined, to deduce any effects on feeding, and in the case of Centropages typicus, was found to be significantly reduced. It was hypothesised that increased gut retention times likely gave the copepods a false sense of satiation, hence reducing feeding rate. There is a requisite to fully understand effects at this lower trophic level as such organisms provide an essential food source for higher trophic biota.

   The juvenile stages of larger animals, such as some species of fish, as well as small fish, jellyfish and crustaceans all employ zooplankton as a food source. Together these organisms make up the next trophic level of the marine food web, collectively termed the first level carnivorous consumers. Second and third level carnivorous consumers include large species of fish and some species of squid and octopus respectively. At the top of the trophic pyramid there are the top carnivorous predators, such as sharks and dolphins, though not all top predators live in the sea. Birds such as Pelicans, Albatross, Penguins and Skua are all important top predators. Microplastics can infiltrate these phyla either indirectly or directly. Predator species may feed on prey species which have already digested microplastics, resulting in indirect transfer, or microplastics could be absorbed via the direct uptake of particles from the water column and sediments. Megafauna such as baleen whales and basking sharks are filter feeders, taking in hundreds and even thousands of cubic metres of water a day, filtering it for plankton. Inadvertently, these species are also taking up indigestible microplastics (Elitza et al 2018).

 To examine potential food web transfer, Outi et al (2018) provided mysid shrimps with zooplankton which had already ingested the microspheres. On examination of the shrimps’ intestines, the presence of zooplankton with microspheres was noted, thus forming the first study to highlight the potential of microplastic transfer from one trophic level to a higher taxon within that level. This denoted that there are both direct and in-direct implications of microplastic ingestion at the primary consumption level. It is worth noting that although the possibility of trophic transfer has been established, most studies to date have involved low level trophic organisms. Subjecting large marine mammals to laboratory experiments is not without ethical constraints. However, Nelms et al (2018) overcame these limitations by sampling the faeces of captive grey seals, Halichoerus grypus, which were fed on wild-caught Atlantic mackerel, Scomber scombrus. Microplastics were visualized in the majority of samples, thus  highlighting the transfer of plastics from prey to predator at higher trophic levels.

   Microplastics are multiple stressors in the marine environment, bearing the ability to affect marine biota from both the physical nature of the plastic if ingested and by the transfer of chemicals associated with plastics, including persistent organic pollutants (POP’s) and endocrine disruptor chemicals (EDC’s). Persistent organic pollutants are environmental contaminants which are not easily degraded in the environment, therefore can be biomagnified up the marine food web (Mackay and Fraser 2000). Endocrine disrupting chemicals are exogenous substances which interfere with the normal functioning of the endocrine (hormone) system (Bergman et al 2013). Many persistent organic pollutants also have endocrine disrupting properties to which the marine biota are exposed, such as phthalates in plastics. Alterations in behaviour and physiology have been documented, as well as influences on the health of organisms such as those on: feeding, reproduction, energetic reserves, growth and survival.  New evidence suggests that because of this transfer, microplastics are also influencing higher levels of biological organisation. Sussarellu et al (2016) documented population shifts and altered behaviour impacting upon the ecological function of keystone species.  Pacific oysters, Crassotrea gigas, were chosen to study the effects of exposure to polystyrene (one of the most commonly used plastic polymers). Oysters are not only of economic importance as a seafood, they also have an important ecological role as a keystone species – they improve water quality by filter-feeding and provide an important habitat for other organisms. Their study concluded that exposure had impacts on feeding, absorption efficiency, gamete quality and fecundity, as well as effecting the growth of offspring.

Though few toxicity studies have been conducted using microplastic vectors, it is an area of scientific concern which does demand more attention. The marine environment is exposed to a vast range of anthropogenic pollutants, including POP’s and EDC’s. During the manufacturing process, additives known as “plasticisers”, are often added to the plastics to increase the life of the plastic. For example, polybrominated diphenyl ethers can be added to provide resistance to heat, nonylphenol for resistance to oxidative damage and triclosan for protection against microbial damage (Browne et al 2007).These are not only a concern as they extend the degradation time of the plastic, but they also pose the risk of introducing toxic chemicals to biota.

  For normal reproduction, development and immune-system function, the endocrine system is crucial (Colborn et al 1993). Toxins which disrupt these processes can be introduced to organisms via the ingestion of microplastics. In large longer-living species, these toxins have the potential to bioaccumulate over decades, in turn disrupting the normal function of the endocrine system and possibly altering reproductive fitness. Frequently used additives, such as polybrominated diphenyl ethers, phthalates and the constituent monomer bisphenol A are distinguished endocrine disruptors (Talsness et al 2009). Once the hormonal system has been disrupted, morphological issues have been noted in organisms at developmental stages and sexual disruption in adults. Genotoxic damage in mussel haemocytes and intersex conditions have been associated with phthalates from plastics (Oehlmann et al 2009).  Plastic additives and pollutants were recently discovered in the muscle of basking sharks, blubber of fin whales and skin of whale sharks (Fossi et al 2017). Moreover, processes such as maternal offloading, as evaluated by Kady et al (2018), represent an additional pathway that such chemicals can accumulate across the food web.  Each of these effects has the potential to harm species at both individual and population level.

  Currently, there are no conclusive answers when it comes to microplastics, their associated contaminants and how they interact physiologically and chemically with organisms at divergent trophic levels. The lack of absolute evidence does not however connote lack of effect. Ultimately, humans are at the top of the marine food chain, so the risks they pose via their consumption need to be seriously contemplated. Marine seafood was sampled from markets for sale for in Indonesia in a recent study (Rochman et al 2015). Of those sampled, 28% of fish and a staggering 55% of all species were found to have anthropogenic debris in their guts. In marine animals, the potential to evoke a biological response to microplastics either physically or chemically has been exhibited. This could mean that microplastics also have the potential to effect humans, via the consumption of such marine biota. Whether that be by means of physical damage or via the increase of exposure to hazardous chemicals associated with the plastics. It is also worth consideration that if the adverse impacts on wildlife end up substantial enough to bring about population declines, there comes the risk that certain food sources humans exploit in the marine environment could also lose their security. To determine such risks and those to human health, science has the huge task of first, exploring exactly how prevalent microplastics are in species across the marine food web, and secondly, expanding current knowledge on disadvantageous induced by their consumption.

  What is known, is that microplastics are accumulating in ocean gyres worldwide. The aggregation of microplastic debris has bestowed a supplementary marine habitat where biological interactions are taking place. This new habitat and its ecological implications remain areas of research which are still emerging – only a small fraction of marine taxa have been studied in regards to microplastics and their biological effects. By their very nature plastics show high resistance to aging and minimal degradation. The process of fragmentation through sunlight, wave and wind action is inevitable in the marine environment. It is therefore to be expected that due to these qualities, even if the input of plastics into the oceans was to cease entirely today, the quantity of microplastics in the oceanic environment could very well increase, as plastics become smaller over time. Correspondingly, this would lead to an escalation of effects on marine biota and eventually humans.. Further exploration on this fructifying issue will hopefully give rise to the development of better methods for controlling and reducing marine litter and its subsequent effects on marine life.  

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