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Article

Can Hediste diversicolor Speed Up the Breakdown of Cigarette Butts in Marine Sediments?

by
Mercedes Conradi
1,
J. Emilio Sánchez-Moyano
1,*,
Francisco J. Rodríguez-Martín
1 and
Javier Bayo
2
1
Department of Zoology, Faculty of Biology, University of Seville, Av. Reina Mercedes s/n, 41012 Seville, Spain
2
Department of Chemical and Environmental Engineering, Technical University of Cartagena, Paseo Alfonso XIII 44, 30203 Cartagena, Spain
*
Author to whom correspondence should be addressed.
Appl. Sci. 2024, 14(11), 4409; https://doi.org/10.3390/app14114409
Submission received: 11 April 2024 / Revised: 14 May 2024 / Accepted: 15 May 2024 / Published: 23 May 2024
(This article belongs to the Special Issue Environmental Technology Applied to Pollution Research: Monitoring, Analysis and Remediation)
Browse Figures
Versions Notes

Abstract

:
Cigarette butts (CBs) are non-biodegradable harmful residues of synthetic origin and are widespread in marine environments around the world. Although environmental factors are often primarily responsible for the fragmentation of microplastics in the marine environment, biotic factors have recently been shown to be equally important in plastic debris. This study evaluates the role of the Hediste diversicolor polychaete in the fragmentation of CBs in the marine environment. Polychaetes were exposed to three concentrations of CB (0 (as the control), 0.25, and 1 butt L−1) at two different temperatures (15 °C and 23 °C) for 28 days. At each temperature, aquaria without polychaetes were used to study the effect of the burrowing activity of the polychaete on CB fragmentation. Toxicants analysed from exposed sediments increased their concentration in a dose-dependent manner to the CB concentration at a temperature of 15 °C but not at 23 °C. CBs did not directly decrease Hediste survival, but prolonged elevated temperatures increased the polychaetes’ susceptibility. The negative effects of CBs on burial success and burrowing behaviour could not be offset by the reduced start time caused by elevated temperatures. Regardless of temperature, both the weight loss and physical fragmentation of CBs buried in polychaete-contaminated sediments were significantly higher than those without Hediste, with no differences between the two concentrations tested. FTIR-ATR analysis used to evaluate CB degradation in relation to cellulose acetate decomposition showed a greater degradation of this compound in treatments with Hediste than in those without polychaetes (~2.75 times), but these differences were not significant. This study is a promising initial step for future research, as any factor that facilitates the fragmentation of this prevalent and hazardous waste must be carefully studied to extract the maximum benefit to help to reduce CBs in the marine environment.

1. Introduction

Due to the difficulty in collecting and subsequently treating them, cigarette butts (CBs) are the most abundant and dispersed garbage in the world [1] and the most abundant type of litter on beaches [2,3,4]. CBs on beaches not only generate large economic costs but also serious environmental problems, which is why this waste is considered an important social problem [5]. The economic cost is determined by its impact on tourism, a value that can be reduced by up to 97% due to dirt [6,7,8]. Thus, most countries invest heavily in keeping their coasts clean. But CB cleaning is not only expensive, it is also ineffective (30% recovered) [9,10], with CBs remaining in the environment even after cleaning, especially automatic cleaning, of the beaches [11]. The environmental cost is more difficult to determine. CBs represent a unique combination of physical and chemical contamination [12]; physical contamination because this trash sheds 100 small microfibrils per day [13], which marine organisms can feed on and transfer throughout the food chain [14,15,16] and chemical contamination because CBs can filter more than 7000 toxins into the environment, many of which have been shown to be dangerous for marine organisms (e.g., [17,18,19,20,21]). The effects of this chemical pollution are difficult to estimate in the marine environment, since CBs can not only leach toxicants into the seawater but can also adsorb toxicants from the ocean floor, depending on the concentrations available and relative to its degradation level (e.g., [22]).
Our current knowledge about CB biodegradation mechanisms and their efficiency is quite limited [23]. CBs are generally made of cellulose acetate (CA), a chemically modified natural polymer [24] widely used in the textile, plastic film, and packaging industries [25]. CA degrades slowly since its high degree of acetylation makes its degradation difficult in the natural environment [26,27]; thus, it remains in the environment for a long time. Although the decomposition of polymer material by physical forces of a mechanical nature is considered vital in the degradation process [28], recently, biotic factors have been considered equally important in this fragmentation [29,30]. For example, some isopods and polychaetes create thousands of microfibres when digging blocks of expanded polystyrene over a short period (days) [31,32]; thus, organisms can break down large polymers [33,34,35] at an even faster rate than abiotic processes [36] and/or can also alter their bioavailability by reducing their size and incorporating them into faeces and faecal matter [36,37,38,39].
Hediste diversicolor (O.F. Müller, 1776) is a common and ecologically important polychaete burrowing species in estuarine sedimentary habitats of European and North American coasts, where it plays an essential role as a bioturbation species that greatly influences the flux of organic matter, oxygen, and bacterial diversity in sediments [40]. For the first time, here, we tested whether the bioturbation created by this polychaete in marine sediments, the most likely final fate of CBs, can directly or indirectly favour mechanical fragmentation of this type of litter. To do this, we determined not only if Hediste can survive the different toxicants leached from CBs at summer and winter temperatures but also if CBs influence the burrowing activity of polychaetes and whether this activity influences directly or indirectly the mechanical fragmentation of CBs. We consider the broader definition of CB degradation that includes weight loss by the leaching of additives or part of the material with low molar mass [41].

2. Material and Methods

2.1. Study Area and Sample Collection

Natural sediment was collected at low tide from an intertidal zone in the Bay of Cádiz (southwestern Spain, 36°29′20″ N 6°15′50″ W) with well-identified sediment characteristics [42] and low contamination levels [43] to avoid collateral contamination. This sediment was sieved through a 0.5 mm mesh to remove fauna, stones, and large organic particles, transported to the laboratory, and stored at 5 ± 1 °C (in the dark) until the time of the experiment.
Hediste diversicolor individuals were collected at the beginning of October to avoid the reproductive season [44]. Specimens of similar weight (1.37 ± 0.24 g) and size (10.66 ± 0.49 cm) were selected to minimise differences in biological responses. In the laboratory, polychaetes (~400 individuals/m2) were placed in different aquariums for a 10-day acclimatisation period with the selected sediment (1/3 of the height of the aquarium) and artificial seawater (ASW-filtered freshwater with Tropic Marin SEA SALT, salinity 35). During the acclimatisation period, the organisms were kept under a constant photoperiod (12 h light: 12 h dark), temperature (15 ± 1 °C, a winter temperature close to values of the natural environment), continuous aeration, and ambient pH (pH 8.1). Polychaetes were fed with a commercial mixture every other day (Tropical Bionautic Flakes—protein 46.0%, fat 7.0%, fibre 3.5%, moisture 8.0%, phosphorus 0.4%) and at least 50% of the water was exchanged every three days. The leftover food was removed by a manual suction pump if it was seen on top of the sediment.

2.2. Experimental Design

Polychaetes were exposed to three concentrations of CB (0 (as the control), 0.25, and 1 butt L−1 equivalents, [14]) at 15 °C and 23 °C (mean seawater temperatures in winter and summer, respectively, in Cádiz; https://seatemperature.info/es/espana/cadiz-temperatura-del-agua-del-mar.html, access date: 1 September 2023) for a period of 28 days. Two different temperatures were used since this affects the burrowing activity of H. diversicolor sediments [40]. Therefore, there were six experimental conditions: (1) control (0 butt L−1 + winter temperature (15 °C); (2) control (0 butt L−1) + summer temperature (23 °C); (3) moderate CB contamination (0.25 butt L−1) + winter temperature (15 °C); (4) moderate CB contamination (0.25 butt L−1) + summer temperature (23 °C); (5) extreme CB contamination (1 butt L−1) + winter temperature (15 °C); (6) extreme CB contamination (0.25 butt L−1) + summer temperature (23 °C). For each condition, three aquaria (5 L in volume) with 600 g of sediment (1/3 of the height of the aquarium) were used with ten specimens per aquarium (density: ~400 individuals/m2) to evaluate mortality, burrowing activity, and CB fragmentation. Furthermore, three aquaria without polychaetes added were used at each temperature to study the effect of the burrowing activity of the polychaete on CB fragmentation.
To achieve the required temperature conditions, 18 aquaria were placed in a sealed thermostat-controlled 15 °C room, and another 18 aquaria were placed in a 23 °C water bath using an AquaMedic Titan 500 (Ab Aqua Medic GmbH, Bissendorf, Germany) closed cooling system connected to an AquaMedic Ocean Runner OR6500 pump. Once the sediment had settled in the experimental aquaria, the polychaetes were randomly placed in them and the temperature of those at 23 °C was increased by 0.5 °C per day. When this temperature was reached, the CBs were added by dropping them onto the surface of the water. The majority (~90%) fell immediately into the sediment, and only some remained floating for up to 2 h before sinking. The CBs were then manually buried in the sediment.
The brand ”Malboro” was used since it is the most popular and most-sold cigarette in Spain (https://www.hacienda.gob.es/es-ES/Areas%20Tematicas/CMTabacos/Paginas/EstadisticasCMT2023.aspx, access date: 10 January 2024). Cigarettes collected within one week of consumption were “naturally smoked” by 3 different individuals. The remaining tobacco was removed from these collected CBs, so the CBs consisted only of a filter wrapped in paper. Later, they were weighed, labelled, and individually stored at −20 °C until the start of the experiment [45].
Water quality was maintained by re-renewing the ASW twice a week, always replenishing less than 50% of the water to disturb as little as possible both the CBs and the polychaetes. During the first two weeks of the experiment, the temperature, pH, salinity, and level of dissolved oxygen (DO%) were measured 3 times a day (Hanna EDGE Multiparametric HI2020-02 (Hanna Instruments, Smithfield, VA, USA), accuracy ±0.002 pH at 0.001 pH resolution; ±0.01 to a resolution of 0.01) since previous work suggested that the toxicants leached from CB could change these characteristics of seawater [17]. After this time period, these parameters were measured twice a day, except for dissolved oxygen, which was measured once a week.

2.3. Sediment Contamination

At the end of the experiment, sediment samples from each aquarium and condition were dried at 60 °C until they reached a constant weight and were transported to the EU-accredited company INNOAGRAL (Seville, Spain) (https://www.innoagral.com, access date: 10 January 2024), where the most abundant alkaloids, nicotine [46], polycyclic aromatic hydrocarbons [17], and the heavy metals Cu and Zn [46,47] in the CB leachate were analysed.

2.4. Biological Parameters

Mortality: Determined weekly by dividing the number of dead individuals at the end of a given week by the number of live individuals at the beginning of that week, within each condition (0 CBL−1 + 15 °C; 0 CBL−1 + 23 °C; 0.25 CBL−1 + 15 °C; 0.25 CBL−1 + 23 °C; 1 CBL−1 + 15 °C; 1 CBL−1 + 23 °C). The number of live specimens was determined by sieving the sediments of each aquarium. Mortality was expressed as a percentage.
Burrowing activity: After 7, 15, and 28 days of exposure, thirty-six polychaetes (two per aquarium; six for each condition) were placed individually into a 150 mL beaker containing 5 cm of natural sediment from the sampling area and 100 mL of ASW to observe the burrowing activity. Burial was considered successful when the polychaetes were able to bury themselves completely within 45 min. The success rate was expressed as a percentage. The burrowing behaviour was considered as the time it took for individuals to start the burrowing process as soon as they were placed in the beaker, while the burial rate was considered as the total time it took the polychaetes to completely bury themselves in the sediment [40].

2.5. Physical Degradation of CBs

Physical degradation of the CBs was determined by the CB weight loss. The weight loss of each CB was calculated by the weight difference between day 0 and day 28:
% weight loss: [(m0 − mt)/m0] × 100
where m0 is the initial mass of the material (day 0) and mt is the mass at the end of the experiment (day 28) in g [48].
The degradation level was visually classified into four states defined similarly as in [49] but with slight modifications: (I) preserved paper and filter; (II) coated paper but considerably worn and discoloured, without the manufacturer’s identification and preserved filter; (III) only the plug-wrapped paper and filter, and (IV) only the fibres of the fat and compact filter, without any paper. The CBs were always washed twice in distilled water for 5 min and kept in a light-protected desiccator at 30 °C until a constant weight was reached. Each CB was weighed using a precision balance (±0.0001 g) [45].

2.6. Cigarette Filter Characterization and Degradation Tracking

The CBs were characterised by attenuated total reflexion Fourier-transform infrared spectroscopy (ATR-FTIR) [45].
To identify the functional groups and the molecular composition of the polymers, ATR-FTIR was used. Samples were compressed in a diamond anvil compression cell, and spectra were acquired with a Thermo Nicolet 5700 Fourier-transformed infrared spectrometer (Thermo Nicolet Analytical Instruments, Madison, WI, USA) fitted with a deuterated triglycine sulphate (DTGS) detector and KBr optics. The spectra were then evaluated using the Thermo Scientific OMNIC Specta software. An average of 20 scans (resolution of 16 cm−1 in the range of 400–4000 cm−1) was performed for each sample. The identification of the polymers was carried out thanks to different libraries of reference polymers such as Hummel Polymer and Additives (2011 spectra), Polymer Additives and Plasticisers (1799 spectra), Sprouse Scientific Systems Polymers from the ATR library (500 spectra), rubber composite materials (350 spectra), and other literature [50]. The standard criteria of [51] were followed for the percentage match (>60%) between the CB degradation state and the reference spectra.

2.7. Statistical Analysis

Differences between the concentrations of the selected CB-derived toxicants were statistically analysed using the PRIMER v6 software to perform univariate PERMANOVA based on Euclidean distance similarity matrices. Differences were considered significant for p-values less than 0.05.
To test whether temperature and CB contamination affect biological traits tested over time, statistical comparisons of the survival and burrowing activity of H. diversicolor were determined by repeated measures of analysis of variance in IBM SPSS 21, using time as a within-subject factor and temperature and CB concentrations as factors between subjects. Pillai’s trace was applied except when the sphericity assumption was violated (in this case, the Greenhouse–Geisser correction was used). Homogeneous groups for the factors were separated by a Tukey test, while the factors were separated by the Bonferroni test. In the case of significant interactions, multiple comparisons between factors were made using the Bonferroni test with the probability of a Type I error. Posteriorly, a Spearman correlation analysis was performed between biological traits and the sediment contamination level of each selected toxicant.
A two-way ANOVA was applied to establish whether the presence of H. diversicolor or temperature significantly affected the physical degradation of CB (weight and level of degradation), after verifying the homogeneity of variances (Levene test) and normality (Kolmogorov–Smirnov test).

3. Results

3.1. Physicochemical Parameters

The seawater parameters and mean values for the different treatments at both temperatures (15 °C and 23 °C) are presented in Table 1.
All toxicant concentrations showed significant differences in the sediments of the tested treatments, and there was an interaction between temperature and the concentration of CB. Regarding temperature, only Zn concentrations were different between those sediments exposed to 15 °C (winter temperature) compared with those exposed to 23 °C (summer temperature) (Table 2).
Sediments of the two CB concentrations tested without Hediste diversicolor (0.25 and 1 CBL−1 D treatments) had similar concentrations of heavy metals (Cu and Zn) and naphthalene at both temperatures, but Cu and Zn sediment concentrations at 0.25 CBL−1 were higher at 23 °C than at 15 °C (Figure 1). Similarly, the Zn concentration from the sediment without H. diversicolor at 23 °C was also higher from that at 15 °C. These treatments also had similar nicotine concentrations at 23 °C but not at 15 °C. Nicotine concentrations in sediments exposed to 0.25 CBL−1 were lower at the winter temperature than at the summer temperature (Figure 1C).
The Cu concentrations of the CB-contaminated sediments with polychaetes were significantly different from the control at 15 °C. However, only the control sediments and 0.25 CBL−1 had significantly different Cu concentrations at summer temperatures. Higher Cu and Zn concentrations were found in sediments exposed to 1 CBL−1 at 15 °C compared with those exposed at 23 °C (Figure 1A,B). However, the Zn concentration of the sediments containing 0.25 CBL−1 at 23 °C was higher than at 15 °C (Figure 1B). Except for the control and the 1 CBL−1 condition at 23 °C, the Zn concentrations in the sediment were different in all CB treatments tested at both temperatures. Nicotine concentrations were different between all H. diversicolor treatments at both temperatures and between CB concentrations at 15 °C compared with those at 23 °C (Figure 1C). A difference was found between the naphthalene concentrations of the two CB-contaminated sediments tested (0.25 and 1 CBL−1) at both temperatures (Figure 1D), and there were also differences between those two concentrations at 15 °C compared with those at 23 °C. According to the Spearman correlation analysis, nicotine concentrations showed a correlation with those of naphthalene (ρ = 0.68). None of the toxicants studied had different concentrations between the controls at 15 °C compared with those at 23 °C.

3.2. Biological Parameters

Although the two CB concentrations tested did not affect the survival of H. diversicolor, there was an interaction between this factor and time (p < 0.05, Table 3). As shown in Figure 2, the mortality of polychaetes exposed to CB increases with time, especially in those exposed to summer temperatures (23 °C). Indeed, both temperature (p < 0.001) and time (p < 0.0001) significantly reduced polychaete survival, with an interaction between these two factors. The survival of control polychaetes at 15 °C is significantly different from that of CB treatments after 21 days of exposure (p < 0.05). In contrast, the differences between control survival at 23 °C and the lower CB concentration tested are significant after 7 days of exposure. Hediste survivals of all treatments at 15 °C are significantly different from their respective treatments at 23 °C.
H. diversicolor exposed to CB concentrations at 23 °C reduced their burial success by 33% compared with controls after only 7 days of exposure. This reduction was maintained until day 21 of the experiment in polychaetes exposed to 0.25 CBL−1, while the difference between those exposed to 1 CBL−1 and the controls increased to 66% at 14 and 21 days of exposure. Indeed, regardless of time, both the CB concentration and temperature similarly affected the burial behaviour of Hediste, as there is no interaction between these two factors (Table 3). Polychaetes from both CB concentrations began to burrow into the sediment significantly later than those from the control throughout the experiment (Figure 3A). Except for those polychaetes that were unsuccessful in burrowing, the mean time needed to start digging was shorter for polychaetes at 23 °C. Temperature also affected the burial rate of H. diversicolor, as did exposure time (Table 3). On the contrary, CB concentrations did not affect the burial rate, although there is a trend for the time it takes for polychaetes to bury themselves to increase as the CB concentration in the water increases (Figure 3B).
Spearman correlations between the biological traits and chemical parameters were significant between the burrowing behaviour of polychaetes and naphthalene (−0.69).

3.3. Physical Degradation of the CBs

The presence of H. diversicolor significantly decreased the weight of the CBs such that all the CBs, regardless of treatment (0.25 or 1 CBL−1), had a lower final weight than those CBs from the treatments without polychaetes (D-0.25 CBL−1 and D-1 CBL−1) (Figure 4, Table 4). Tukey’s test clearly shows two homogeneous groups: one formed by the two concentrations of CBs without polychaetes and another by the two concentrations with polychaetes (p < 0.05). On the contrary, the temperature did not affect the final weight of the CBs, nor was there any interaction between this factor and the CBs (Table 4).
According to our classification of the different degradation states, the physical degradation of CB was significantly increased by polychaetes (Table 4). Therefore, 100% of the CBs of any treatment with H. diversicolor lacked both the paper coating and the plug wrap. In non-polychaete treatments, 66% of CBs still had all or most of the paper coating at 15 °C, while at 23 °C, 80% of the butts had the coating paper partially removed, and only 20% still had it. Despite this difference, there were no significant differences in the CB degradation level in the non-polychaete treatments with respect to temperature, nor was there any interaction between temperature and the treatments (Table 4). Cellulose acetate degraded an average of 0.53 ± 0.33% in those treatments without Hediste, and 1.46 ± 0.91% with Hediste, without statistically significant differences between both means (p = 0.346) (Figure 5A). The treatments carried out at 15 °C showed an average percentage of 1.45 ± 0.91% in the degradation of CA, and those carried out at 23 °C having an average of 0.54 ± 0.34%, without statistically significant differences between the two (p = 0.356) (Figure 5B). There were also no statistically significant differences in CA degradation between the 0.25 CBL−1 (1.02 ± 0.85%) and 0.50 CBL−1 (0.97 ± 0.28%) treatments (p = 0.960). The highest percentage of CA degradation was seen in those treated with CB at 15 °C (2.58 ± 1.72%), and the lowest percentage was for the treatment without polychaetes at 15 °C (0.32 ± 0.36%). The only treatment that showed statistically significant differences compared with the rest was the 0.25 CBL−1 treatment at 15 °C, with an average CA degradation value of 4.02 ± 3.57% compared with the remaining CB treatments, which had an average value of 0.56 ± 0. 22% (p = 0.014).

4. Discussion

It is now well established that CBs represent a significant source of pollutants in the environment. Upon contact with water, various organic and inorganic compounds are released from these CBs [12,17,18,19,52,53,54,55,56], rendering them bioavailable to aquatic life. The highest variability in terms of toxicant concentrations analysed in sediment occurred between treatments at 15 °C and 23 °C. Except for naphthalene at the highest concentration of CB studied (1 CBL−1), all contaminants increased their concentration in the sediment in a dose-dependent manner to the CB concentration at 15 °C. However, this relationship was disrupted at 23 °C, where the highest CB concentration consistently exhibited pollutant concentrations similar to that of the control or lower than those analysed in the 0.25 CBL−1 treatment (nicotine). While potentially toxic element leachates from CBs have been studied in various types of water [18,56], no studies have investigated the potential differences in leachates from this type of litter in seawater at different temperatures. The only experiment conducted aimed to determine the influence of temperature and relative humidity on the airborne chemicals emitted by CBs [57], showing that increased temperature led to the faster release of nicotine, triacetin, and other chemicals. However, temperature may also play a crucial role in determining the phase transfer and mobility of these pollutants, such as PAHs [58]. Although it would be interesting to determine whether temperature effectively affects the release of CB contaminants or their mobility, given the substantial increase in the CB presence on beaches in summer, this is not the primary focus of this study.
In this study, CB did not directly decrease the survival of H. diversicolor, but both time and temperature did increase its effects. While the survival of this polychaete upon exposure to different CB concentrations has not been previously studied, it has been shown that the lowest concentration at which the burrowing of H. diversicolor is affected by toxic CB leachates in seawater is 2 CBL−1 (LOEC for 96 h = 172 μgL−1 nicotine), with higher concentrations causing growth retardation and extensive DNA damage [59]. However, this work also found that this lower concentration was higher (LOEC for 96 h = 8 CBL−1; 694 ngml−1 nicotine) when polychaetes were exposed to CB microfibres in sediment, with no effect on the relative growth rate after 96 h and 28 days of exposure. Therefore, it is unsurprising that the concentrations tested in this study, 0.25 and 1 CBL−1, did not influence Hediste survival. However, summer temperatures did affect the survival of CB-exposed polychaetes, particularly at the highest concentration. Elevated temperatures could increase the susceptibility of marine invertebrates to contamination [60,61,62,63]. Although little is known about the effect of increased temperature on pollutant toxicity in polychaetes, higher temperatures have recently been shown to exacerbate the negative effects of marine acidification on H. diversicolor survival [40].
CBs can cause significant sublethal effects, such as behavioural changes and/or alterations in the reproductive performance of marine invertebrates [15]. Limited current data on the effect of CB on sediments indicate a reduction in benthic copepod reproduction of Nitokra sp. (0.1 and 0.01 CBL−1) [64], as well as decreased burrowing activity and growth of the polychaete Hediste diversicolor [59]. Similarly, our results show that CBs within sediment significantly prolonged the time taken by H. diversicolor to initiate burrowing (p < 0.05), with an initial difference of 6 days compared with the controls at 15 °C and 9 days at 23 °C (after 14 exposure days). The earthworm Eisena fetida avoided soil contaminated with CBs, and the avoidance rate positively correlated with CB concentration but negatively correlated with exposure time [65]. Burial success, like other energy-intensive activities, is favoured by warmer temperatures, as it activates metabolism in ectothermic animals [66], including Hediste diversicolor [67]. In fact, increased temperature altered the burrowing behaviour, shortening the time taken by the polychaete to initiate burrowing (Figure 3A control). Ref. [59] reported that burrowing times of H. diversicolor were more than 10 times longer when exposed to CB leachates with concentrations <2 CBL−1 but found no significant differences in the burial rate when exposed to CB microfibres in sediment. Occasionally, the negative effects of certain stressors, such as water acidification, on marine animals’ energetic activities or foraging can be offset by elevated temperatures [68]. However, if the negative impact of the stressor outweighs the increase in or acceleration of metabolism due to the temperature increase, a negative effect will be observed in the organism. Thus, the negative impact of CBs on the H. diversicolor burrowing behaviour at 23 °C was such that it was not only uncompensated for by the increase in temperature but also accompanied by a significantly decreased burial success rate (up to 66% in 1 CBL−1). Polychaetes that successfully buried themselves took longer to start the burying process as the CB concentration in sediment increased. A similar trend was observed with the burial rate at the two tested temperatures, although this was not significant. Similarly, [40] found that increased temperature potentiated the adverse effect of marine acidification on the initiation of H. diversicolor burrowing activity. However, in this study, burial rate increased with decreasing pH levels, especially at 25 °C; however, regardless of pH, a higher burial rate was observed at 25 °C compared with 15 °C.
Reduced burrowing activity not only affects the survival of the Hediste population, as they are exposed to predators for longer durations, but also affects the ecosystem due to the crucial ecological role of this polychaete in sediment bioturbation (i.e., [69,70,71]). However, until now, the potential role of this bioturbation in the fragmentation of residues as long-lasting in the environment as CBs had not been studied. Our results indicate that, regardless of temperature, both the weight and physical degradation of CBs buried in polychaete sediments exhibit significantly higher levels of fragmentation than those in contaminated sediments without H. diversicolor. No differences were observed between the weight loss or degradation levels of CBs at the two CB concentrations tested, which is likely due to polychaete mortality and the reduced burial success at 1 CBL−1 and 23 °C. Studies on CA degradation in different aqueous environments have also found that the effect of temperature is insignificant and that most of the weight loss occurs in the initial degradation steps [23]. Our data confirm that the initial step of the CB decomposition process (~30 days) involves mass loss (~15–20%; [72]), but the percentage of this loss was significantly higher in treatments with H. diversicolor, with many CBs losing 20–30% of their weight. In the only study conducted on the CB degradation status on tropical beaches, this mass loss corresponded approximately to degradation level I (0% mass loss with tobacco residues and preserved filter and paper coating;), II (15% mass loss without tobacco residues, preserved filter and paper coating, and manufacturer’s identification), and III (26% mass loss, no tobacco remains, and filter with paper coating but considerably worn and discoloured, without manufacturer’s identification) [49]. However, in our study, this would correspond to level III (only plug-wrap paper and filter preserved), although we have not considered level I as defined by these authors. Thus, 100% of the CBs from any treatment with H. diversicolor lacked both the paper coating and the plug wrap, while most CBs from the non-polychaete treatments retained all or most of the paper coating. These differences were also observed when FTIR-ATR analysis was used to assess CA decomposition (about 2.75 times greater in Hediste treatments compared with those without polychaetes), although these were not significant. Therefore, CB degradation is not linear and requires an extensive period to complete, indicating that this residue persists in the medium and interacts with both toxicants and the surrounding biota. However, this study serves as a promising initial step for future research with this polychaete to further explore whether H. diversicolor can be utilised as a bioremediator to facilitate the degradation of this prevalent and hazardous waste in marine environments.

Author Contributions

Conceptualization, M.C.; formal analysis, M.C. and J.E.S.-M.; writing—review and editing, M.C., J.E.S.-M., F.J.R.-M. and J.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Ethical review and approval were waived for this study due to our work describes research on invertebrates (polychaetes). According to European legislation (Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes, article 1.3 and 1.4) and Spanish national legislation (RD 53/2013, article 2.4), these animals are not subject to these regulations. Nevertheless, during the execution of the experiment, the 3 Rs were taken into account. Specifically, the minimum number of animals was used to obtain significant results. Additionally, to minimize the harm to the animals, they were maintained in conditions similar to their natural environment, with adequate substrate and food supply ad libitum. The specimens from the initial stock that were not used in the experiment were released in the same area from which they were collected. The specimens used in the experiment were anesthetized with menthol, sacrificed by immersion in liquid nitrogen, and preserved for later analysis.

Data Availability Statement

The raw data supporting the conclusions of this article will be made available by the authors on request.

Conflicts of Interest

The authors declare no conflict of interest.

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Applsci 14 04409 g001
Figure 1. Mean values (+SD) of the toxicant analysed in the sediment exposed to the different concentrations of CB (0 CBL−1, 0.25 CBL−1, 1 CBL−1 with Hediste diversicolor, and 0.25 CBL−1, 1 CBL−1 without polychaetes) at the two temperatures studied (15 °C, 23 ° C) for 28 days. (A) Cu concentration; (B) Zn concentration; (C) Nicotine concentration; (D) Naphthalene concentration. Significant differences among the CB concentrations are represented by different letters (uppercase letters for CB concentrations with polychaetes; lowercase letters for CB concentrations without polychaetes; letters without ′ for 15 °C treatment; letters with ′ for 23 °C treatment). Significant differences (p < 0.05) between the same concentration of CB at the two temperatures tested are represented by asterisks (*).
Figure 1. Mean values (+SD) of the toxicant analysed in the sediment exposed to the different concentrations of CB (0 CBL−1, 0.25 CBL−1, 1 CBL−1 with Hediste diversicolor, and 0.25 CBL−1, 1 CBL−1 without polychaetes) at the two temperatures studied (15 °C, 23 ° C) for 28 days. (A) Cu concentration; (B) Zn concentration; (C) Nicotine concentration; (D) Naphthalene concentration. Significant differences among the CB concentrations are represented by different letters (uppercase letters for CB concentrations with polychaetes; lowercase letters for CB concentrations without polychaetes; letters without ′ for 15 °C treatment; letters with ′ for 23 °C treatment). Significant differences (p < 0.05) between the same concentration of CB at the two temperatures tested are represented by asterisks (*).
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Applsci 14 04409 g002
Figure 2. Survival (%) of Hediste diversicolor exposed for 28 days to different CB concentrations (0 CBL−1, 0.25 CBL−1, 1 CBL−1) at the two temperatures studied: 15 °C (light color), 23 °C (dark color). Significant differences (p < 0.05) between CB concentrations and the control on the same date are represented by asterisks (*).
Figure 2. Survival (%) of Hediste diversicolor exposed for 28 days to different CB concentrations (0 CBL−1, 0.25 CBL−1, 1 CBL−1) at the two temperatures studied: 15 °C (light color), 23 °C (dark color). Significant differences (p < 0.05) between CB concentrations and the control on the same date are represented by asterisks (*).
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Figure 3. The burrowing activity (mean values + SD) of Hediste diversicolor at different CB concentrations (0 CBL−1, 0.25 CBL−1, 1 CBL−1) and at the two temperatures studied (15 °C, 23 °C) over 28 days. (A) Burrowing behaviour (seconds); (B) Burial rate (seconds). (*) Unsuccessful burial.
Figure 3. The burrowing activity (mean values + SD) of Hediste diversicolor at different CB concentrations (0 CBL−1, 0.25 CBL−1, 1 CBL−1) and at the two temperatures studied (15 °C, 23 °C) over 28 days. (A) Burrowing behaviour (seconds); (B) Burial rate (seconds). (*) Unsuccessful burial.
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Figure 4. Weight (g; maximum, mean, and minimum) of the CBs without Hediste diversicolor (left) and with these polychaetes (right) exposed to two different CB concentrations: 0.25 CBL−1, 1 CBL−1 and at the two temperatures studied: 15 °C (blue dots), 23 °C (red dots) for 28 days.
Figure 4. Weight (g; maximum, mean, and minimum) of the CBs without Hediste diversicolor (left) and with these polychaetes (right) exposed to two different CB concentrations: 0.25 CBL−1, 1 CBL−1 and at the two temperatures studied: 15 °C (blue dots), 23 °C (red dots) for 28 days.
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Figure 5. Examples of the FTIR spectra for cellulose acetate degradation: (A) Treatment with (black line) and without (green line) Hediste diversicolor; (B) Treatment with H. diversicolor at 15 °C (blue line) and 23 °C (red line).
Figure 5. Examples of the FTIR spectra for cellulose acetate degradation: (A) Treatment with (black line) and without (green line) Hediste diversicolor; (B) Treatment with H. diversicolor at 15 °C (blue line) and 23 °C (red line).
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Table 1. Artificial seawater (ASW) conditions (mean ± SD) at 15 °C and 23 °C during the 30 days of the experiment in each treatment. Average pH (NBS), salinity (PSU), temperature (°C), dissolved oxygen (DO %). D, treatments without H. diversicolor.
Table 1. Artificial seawater (ASW) conditions (mean ± SD) at 15 °C and 23 °C during the 30 days of the experiment in each treatment. Average pH (NBS), salinity (PSU), temperature (°C), dissolved oxygen (DO %). D, treatments without H. diversicolor.
pHTemperatureSalinityDO
15 °CControl8.13 ± 0.0914.99 ± 0.1335.38 ± 0.09131.79 ± 7.6
0.25 CBL−18.13 ± 0.0814.97 ± 0.1335.39 ± 0.11131.64 ± 9.3
1 CBL−18.12 ± 0.0914.96 ± 0.1335.39 ± 0.12134.10 ±6.7
D-0.25 CBL−18.14 ± 0.0814.94± 0.1635.47 ± 0.11129.75 ± 6.6
D-1 CBL−18.15 ± 0.0814.96 ± 0.1635.44 ± 0.11130.64 ± 6.5
23 °CControl8.11 ± 0.0823.15 ± 0.3135.42 ± 0.12126.62 ± 11.4
0.25 CBL−18.12 ± 0.1023.15 ± 0.3635.45 ± 0.08125.60 ± 10.1
1 CBL−18.11 ± 0.1023.15 ± 0.3635.44 ± 0.09127.29 ± 10.6
D-0.25 CBL−18.11 ± 0.0923.17 ± 0.3435.50 ± 0.11128.36 ± 10.4
D-1 CBL−18.13 ± 0.0923.15 ± 0.3635.49 ± 0.10129.40 ± 9.8
Table 2. PERMANOVA results for the Cu, Zn, naphthalene and nicotine concentrations in the sediments exposed to different CB concentrations (0 CBL−1, 0.25 CBL−1, 1 CBL−1 with Hediste diversicolor, and 0.25 CBL−1, 1 CBL−1 without polychaetes) at the two temperatures studied (15 °C, 23 °C) for 28 days. Sum square (SS); mean square (MS); degrees of freedom (df); ns = nonsignificant.
Table 2. PERMANOVA results for the Cu, Zn, naphthalene and nicotine concentrations in the sediments exposed to different CB concentrations (0 CBL−1, 0.25 CBL−1, 1 CBL−1 with Hediste diversicolor, and 0.25 CBL−1, 1 CBL−1 without polychaetes) at the two temperatures studied (15 °C, 23 °C) for 28 days. Sum square (SS); mean square (MS); degrees of freedom (df); ns = nonsignificant.
dfSSMSPseudo-Fp
CuCB430.417.6231.860.001
Temperature10.300.301.26ns
CB × Temperature423.775.9424.810.001
Res6214.820.24
Total7171
ZnCB438.789.69253.20.001
Temperature16.886.88179.70.001
CB × Temperature425.416.35165.910.001
Res622.373.828 × 10−2
Total7171
NaftaleneCB437.239.3126.560.001
Temperature10.450.451.28ns
CB × Temperature411.442.868.160.001
Res6221.730.35
Total7171
NicotineCB329.159.7238.450.001
Temperature16.32 × 10−26.32 × 10−20.25ns
CB × Temperature326.458.8234.890.001
Res5213.140.25
Total5969.14
Table 3. Results of the three-factor repeated-measures ANOVA for the mortality, burrowing behaviour, and burial rate of Hediste diversicolor exposed to the different CB concentrations (0 CBL−1, 0.25 CBL−1, 1 CBL−1) and at the two temperatures studied (15 °C, 23 °C) for 28 days. Sum square (SS); mean square (MS); degrees of freedom (df); ns = nonsignificant.
Table 3. Results of the three-factor repeated-measures ANOVA for the mortality, burrowing behaviour, and burial rate of Hediste diversicolor exposed to the different CB concentrations (0 CBL−1, 0.25 CBL−1, 1 CBL−1) and at the two temperatures studied (15 °C, 23 °C) for 28 days. Sum square (SS); mean square (MS); degrees of freedom (df); ns = nonsignificant.
dfSSMSFp
Mortality rateTime1.328496.728496.7021.910.0001
Time × CBs2.631324.991324.993.420.0440
Time × Temperature1.326205.386205.3816.000.0001
Error (Time)42387.77170.20--
CBs2.007430.713715.363.500ns
Temperature1.0019,181.8719,181.8718.100.0010
Error1414,843.521070.25--
Burrowing behaviorTime2.4524,14024,140.291.65ns
Time × CBs4.4067,741.3813,010.802.30ns
Time × Temperature2.4028,048.5511,436.801.90ns
Error (Time)56205,169.385975.56--
CBs2.0058,063.4029,031.704.700.0270
Temperature1.0036,200.2836,200.285.900.0290
Error1485,485.626106.18--
Burial rateTime2.00119,836.1557,548.403.600.0370
Time × CBs4.2054,932.3154,932.310.84ns
Time × Temperature2.1042,614.3820,464.521.30ns
Error (Time)56458,695.558190.99--
CBs2.0023,835.4711,917.730.82ns
Temperature1.0077,088.4077,088.405.320.0370
Error1420,2705.3314,478.95--
Table 4. Results of two-factor ANOVAs for the CB weight loss and degradation level at the different CB concentrations (0 CBL−1, 0.25 CBL−1, 1 CBL−1 with Hediste diversicolor, and 0.25 CBL−1, 1 CBL−1 without polychaetes), and at the two temperatures studied (15 °C, 23 °C) after 28 days. Sum square (SS); mean square (MS); degrees of freedom (df); ns = nonsignificant.
Table 4. Results of two-factor ANOVAs for the CB weight loss and degradation level at the different CB concentrations (0 CBL−1, 0.25 CBL−1, 1 CBL−1 with Hediste diversicolor, and 0.25 CBL−1, 1 CBL−1 without polychaetes), and at the two temperatures studied (15 °C, 23 °C) after 28 days. Sum square (SS); mean square (MS); degrees of freedom (df); ns = nonsignificant.
dfSSMSFp
Weigth lossCB316,426.655475.556.260.0001
Temperature1450.76450.761.1370.248
CB × Temperature3597.90199.301.1370.298
Error228719.28396.33-
Total3026,412.62--
Degradation
level		CB324.538.1838.550.0001
Temperature10.190.190.890.345
CB × Temperature30.530.170.38 0.487
Error224.670.21
Total30350
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Conradi, M.; Sánchez-Moyano, J.E.; Rodríguez-Martín, F.J.; Bayo, J. Can Hediste diversicolor Speed Up the Breakdown of Cigarette Butts in Marine Sediments? Appl. Sci. 2024, 14, 4409. https://doi.org/10.3390/app14114409

AMA Style

Conradi M, Sánchez-Moyano JE, Rodríguez-Martín FJ, Bayo J. Can Hediste diversicolor Speed Up the Breakdown of Cigarette Butts in Marine Sediments? Applied Sciences. 2024; 14(11):4409. https://doi.org/10.3390/app14114409

Chicago/Turabian Style

Conradi, Mercedes, J. Emilio Sánchez-Moyano, Francisco J. Rodríguez-Martín, and Javier Bayo. 2024. "Can Hediste diversicolor Speed Up the Breakdown of Cigarette Butts in Marine Sediments?" Applied Sciences 14, no. 11: 4409. https://doi.org/10.3390/app14114409

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