Limited ingestion, rapid egestion and no detectable impacts of microbeads on the moon jellyfish, Aurelia aurita
Introduction
Since the first disposable plastic shopping bag was introduced in the 1960s, plastics have become indispensable in people's daily lives. An estimated 8.3 billion metric tons of plastics have been manufactured globally (Geyer et al., 2017) and >5.25 trillion particles of plastics are estimated to float in the global oceans (Eriksen et al., 2014). By 2060, it is estimated that 265 million tons of mismanaged plastic will be generated annually with 91% finding its way into the ocean (Lebreton and Andrady, 2019).
Larger pieces of plastic discarded in the ocean eventually disintegrate into tiny particles (≤5 mm) called microplastics (Kershaw, 2015). Some microplastics also originate as virgin microplastics that are manufactured at a small size, such as the microbeads used in facial cleansers and various cosmetics (Cole et al., 2011). The proliferation of microplastics in the oceans means that most marine biota will now regularly encounter microplastic particles. Indeed, >690 marine species globally have been reported to ingest or become entangled by marine debris, with 92% of that debris being plastics (Gall and Thompson, 2015).
The impacts of microplastic ingestion, however, are variable with both adverse and no effects being documented. For example, up to 50% of the energy reserves of the marine worm Arenicola marina were reduced after four-weeks exposure to microplastics (Wright et al., 2013) and the body mass and metabolic rates of the langoustine Nephrops norvegicus were reduced after eight months of exposure to microplastics (Welden and Cowie, 2016). In contrast, Jovanović et al. (2018) reported that the tissues of the gastrointestinal tract of the fish Sparus aurata were not harmed by microplastics after 45 h exposure. Likewise, the larvae of the sea urchin Tripneustes gratilla egested microplastics within 7 h of ingestion, with no adverse effects reported (Kaposi et al., 2014).
Jellyfish ingest small particles such as zooplankton and fish eggs, and have high clearance rates (Titelman and Hansson, 2006). Jellyfish, therefore, have potential to ingest large quantities of microplastics. Jellyfish are abundant in marine environments (Lucas et al., 2014) and a play significant role in pelagic carbon and nutrient cycling (Pitt et al., 2009) and exert both top-down (grazing) and bottom-up (nutrient excretion) influences on zooplankton and phytoplankton communities (West et al., 2009). Jellyfish also provide numerous ecosystem services (Graham et al., 2014). For example, they are prey for vulnerable species of turtle (Houghton et al., 2006) and protect juvenile fish and other symbionts from predators (Lynam and Brierley, 2007; Rajkumar et al., 2014). Purcell and Decker (2005) suggested that jellyfish could be a keystone organism in plankton food webs. Thus, microplastic impacts on jellyfish could have cascading ecosystem outcomes.
Studies of the potential influence of microplastics on jellyfish are just beginning to emerge. For example, Sun et al. (2017) reported that “jellyfish” ingested microplastics but the species of medusae were not identified. In addition, Macali et al. (2018) reported macroplastics in the gastrovascular cavity of the semaestome jellyfish Pelagia noctiluca and hypothesised that jellyfish could facilitate the transfer of plastics to higher trophic levels. Recently, Costa et al. (2020) measured how newly liberated ephyrae of the moon jellyfish, Aurelia sp. responded when exposed to polyethylene microbeads at a range of concentrations (0.01–10 mg/L). The ephyrae ingested microbeads and experienced reduced pulsation rates and mobility even at the lowest concentration of microbeads (0.01 mg/L). All microbeads, however, detached from the ephyrae within 72 h and ephyrae fully recovered when transferred to uncontaminated seawater
Aurelia sp. is widely distributed in the world's oceans (Lucas, 2001) and frequently form spectacular blooms (Dong, 2019). Medusae of Aurelia aurita tend to feed on small, non-swimming prey (Graham and Kroutil, 2001) and have high clearance rates (Riisgård and Madsen, 2011), and so are likely to capture and potentially ingest large amounts of microplastics. A study, therefore, to assess the effects of microplastic ingestion on the medusae stage is needed. Since the gastroderm of jellyfish is very thin (one cell thick), the digestive tracts of jellyfish may be particularly susceptible to abrasion and injury from microplastics, which may, in turn, affect their physiology and overall fitness.
Here we determined rates of ingestion and egestion of polystyrene microbeads by A. aurita medusae and measured their physiological (respiration rate) and physical (histopathology) effects on the jellyfish. We hypothesised that ingestion of microbeads would increase respiration rates of the jellyfish and cause physical damage to their gastrodermal tissue.
Section snippets
Materials and methods
Eighty-four medusae (mean size ~3.5 cm ± 0.5 bell diameter) of the moon jellyfish Aurelia aurita were obtained from the commercial aquarium Underwater World, Sunshine Coast, Queensland. The medusae were acclimatised to laboratory conditions for seven days. During acclimation, medusae were maintained in a 50 L kreisel tank, and fed 10 ml of Artemia nauplii (~30 individual ml−1) three times daily. Prior to all experiments, medusae were starved for 4 h to ensure their guts were evacuated (
Ingestion experiment
Microbeads were observed associated with all structures of the jellyfish during the experiment (Fig. 1). Most microbeads were observed on the oral arms, exumbrella and tentacles within 1–2 h of initial exposure. Microbeads were also ingested (i.e. appeared within the manubrium and gastric pouches) within 1–2 h of exposure, and the maximum number of microbeads within gastric pouches occurred at 16 h (Mean number of microbeads = 2 ± 1.61 particles). With the exception of one microbead on the oral
Discussion
Aurelia sp. medusae had a very poor capture efficiency for microbeads. They ingested only small numbers of the captured microbeads, and microbeads were not retained in the digestive tract and were egested within 8 h of consumption. Moreover, our hypotheses that the ingestion of microbeads would increase respiration rates of the jellyfish and abrade their gastrodermal tissue were not supported and no physiological or physical effects on A. aurita medusae were detected.
The most microbeads found
Conclusion
Medusae of the moon jellyfish, Aurelia aurita can capture and ingest virgin polystyrene microbeads, albeit at low efficiency. The medusae, however, did not retain the polystyrene microbeads within their gastric structures and egested them within 8 h, indicating the ability to recognise them as “non-food particles”. Moreover, microbead ingestion had no significant impacts on A. aurita respiration rates and caused no visible damage to the tissues of the gastric pouches. Virgin microbeads,
CRediT authorship contribution statement
Phuping Sucharitakul:Writing - original draft, Conceptualization, Methodology, Investigation.Kylie A. Pitt:Writing - review & editing, Supervision.David T. Welsh:Methodology, Writing - review & editing, Supervision.
Acknowledgement
The first author is supported by Griffith University Postgraduate Research Scholarship and Griffith University International Postgraduate Research Scholarship. We thank staff at Underwater World, Queensland for providing medusae and staff at Sea World for technical support.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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2022, Marine Environmental ResearchCitation Excerpt :Cnidocytes of cnidarians contain mechanoreceptors and chemoreceptors (Albert, 2011) and Aurelia aurita selectively ingests particles based on taste (Archdale and Anraku, 2005), so microbeads lacking chemical cues may not be recognised as food. Nematocysts of polyps and ephyrae of Sanderia malayensis failed to discharge when exposed to microbeads (Eom et al., 2022) and the extremely low capture efficiency of virgin microbeads in laboratory studies (Costa et al., 2020a; Sucharitakul et al., 2020) is consistent with medusae failing to identify microplastics as food. Indeed, Aurelia aurita appears to only ingest virgin microbeads when live prey (Artemia nauplii) is present (Romero-Kutzner et al., 2022).