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Increased Incidence of Entanglements and Ingested Marine Debris in Dutch Seals from 2010 to 2020

: In recent decades, the amount of marine debris has increased in our oceans. As wildlife interactions with debris increase, so does the number of entangled animals, impairing normal behavior and potentially affecting the survival of these individuals. The current study summarizes data on two phocid species, harbor ( Phoca vitulina ) and gray seals ( Halichoerus grypus ), affected by marine debris in Dutch waters from 2010 to 2020. The ﬁndings indicate that the annual entanglement rate (13.2 entanglements/year) has quadrupled compared with previous studies. Young seals, particularly gray seals, are the most affected individuals, with most animals found or sighted with ﬁshing nets wrapped around their necks. Interestingly, harbor seals showed a higher incidence of ingested debris. Species differences with regard to behavior, foraging strategies, and habitat preferences may explain these ﬁndings. The lack of consistency across reports suggests that it is important to standardize data collection from now on. Despite increased public awareness about the adverse environmental effects of marine debris, more initiatives and policies are needed to ensure the protection of the marine environment in the Netherlands. Entanglements could be caused by a single piece of debris (89.7%) or by several pieces (5.5%) (e.g., ﬁshing net and wrapping plastic). In seven cases, no information was reported about the origin of the debris (4.8%) (Figure 5).


Introduction
During the last few decades, the environmental effects of marine debris have become more and more apparent [1][2][3][4]. Marine debris is defined as "any persistent, manufactured, or processed solid material that is directly or indirectly, intentionally or unintentionally, disposed of or abandoned into the marine environment" [5]. This classification of debris includes diverse materials such as plastics, metals, fabrics, and petroleum. Currently, debris made of plastic poses the biggest environmental threat due to the material's slow degradation and widespread access [4,6]. However, thanks to the results of multiple scientific reports, several policy changes are being developed and implemented worldwide. One example is the 2008 Marine Strategy Framework Directive (MSFD) by the European Union (EU) which, according to descriptor10 Marine Litter, "requires EU Member States to ensure that properties and quantities of marine litter do not cause harm to the coastal and marine environment" [7]. Although society has become increasingly aware of the problems caused by litter, large quantities still end up in the marine environment.
Marine debris can cause a variety of environmental effects. According to Kuo and Huang [8], the impact of marine debris can be divided into three categories: injury or death of marine wildlife, harm to marine ecosystems, and effects on human lives and properties.
Conservationists are particularly concerned with the direct impacts on wildlife [9]. Over a period of 18 years (1997 to 2015), researchers observed a 49% increase in the number of aquatic species that were either entangled in or had ingested marine debris [3,10]. The list The animals were found either dead or alive. Dead animals were either disposed of (i.e., advanced decomposition state) or brought to one of the rehabilitation centers for post-mortem examination. For the animals found alive, one of three possible actions were taken: (1) no action, if the animal could not be caught nor any other action could be taken at that moment; (2) released on site, if the animal could be caught, freed from the entangled debris, presented none to very mild wounds, and could be released immediately afterwards; or (3) brought into rehabilitation, if the animal could be caught and presented moderate to severe wounds that required further medical treatment. In situations where the survival of the individual was compromised due to medical reasons, euthanasia was performed by a licensed veterinarian, first sedating the animal and then injecting pentobarbital sodium (100 mg/kg) intravenously [26]. No animals were euthanized for the purpose of this study.
Reports were grouped by species, age, and sex [27]. The encounters were from the two phocid species found in the Netherlands, gray seals and harbor seals. The individuals reported comprised all age classes (pups, juveniles, and adults) and both sexes. Age determination was performed based on body size, condition of dentition, presence or absence of lanugo, and shape of the head [28]. Animals were classified as pups when the estimated age was less than four weeks old (i.e., 26 days old). We chose this threshold because the average lactation period is 26 days for both species [29,30]. Juveniles are independent, non-sexually mature animals which include weaners (<1 year old), yearlings (1-2 years old), and subadults (<3 years old). Pups were not included in the juvenile category because, during the lactation period, they are still dependent on their mothers for food. Males and females of both native species reach sexual maturity at the age of 3; hence, animals were classified as adults if they were estimated to be more than 3 years of age [30]. Age and sex were reported as unknown if the individuals were far away from the observer or if they were lying on their abdomen, or swimming. The same was true for dead animals who were in an advanced state of decomposition.
The entanglement was described in more detail, including the type (external or ingested), location (e.g., where on the body), the origin of debris (from boating/fishing industry or of other origin), and lesions caused. The entanglement type was reported as external when the material was found around (part of) the body, and as ingested when the material was found in the digestive tract. Debris that originated from the boating/fishing industry included, among others, fishing lines, nets, hooks, and ropes. Marine debris of other origin could include textiles, domestic or industrial plastics, etc. Unfortunately, due to the lack of consistency while reporting the type of material the debris was made of (i.e., metal, plastic, fabric, etc.), and the lesions caused by marine debris, no further data analysis was performed regarding the type of material or the severity of the animal's wounds.
Data was analyzed in R version 4.1.0 (RStudio version 1.4.1717). Only summary statistics, including absolute counts and percentages, were performed. We also looked at yearly and geographical trends. Yearly trends were analyzed by reporting the number of strandings per year from 2010 to 2020. We also looked at yearly entanglement trends, separating those per stranding location, age, sex, and origin of the entangled debris. Lastly, we computed, for both species, the yearly entanglement rates, expressed as a percentage, by dividing the number of reported entanglements by the number of animals counted during the molting period [23]. Geographical trends were analyzed by compiling the WGS 84 satellite coordinates of all reported strandings and creating a map to show their distribution in the Netherlands. The proportion of strandings in each mainland province (Zeeland, South Holland, North Holland, Friesland, and Groningen) and each of the Wadden islands (Texel, Vlieland, Terschelling, Ameland, and Schiermonnikoog) was indicated using color coding.

Results
Entangled seals were observed every year during the studied time period (2010-2020). A total number of 145 entanglements with marine debris were reported, of which the majority were gray seals (81.4%). The average yearly number of reported entanglements was 13.2 reports per year (10.7 for gray seals; 2.5 for harbor seals). Overall, the numbers of yearly strandings were rather stable at the start of the study, with around seven reports per year. However, from 2017 onwards, there was a gradual increase in reported strandings, with a clear spike after 2018 (Figure 1a). ments was 13.2 reports per year (10.7 for gray seals; 2.5 for harbor seals). Overall, the numbers of yearly strandings were rather stable at the start of the study, with around seven reports per year. However, from 2017 onwards, there was a gradual increase in reported strandings, with a clear spike after 2018 (Figure 1a).
Entanglement rates varied yearly in both species. On average, yearly entanglement rates for gray and harbor seals were 0.3% and 0.04%, respectively, suggesting that gray seals are entangled more frequently. For gray seals, entanglements were seen every year, with the lowest entanglement rate being 0.03% in 2012; and the highest being 0.6% in 2019. For harbor seals, the lowest entanglement rates were in 2013 and 2016 when no entanglements were reported. The highest entanglement rate was 0.14% in 2019. In the Netherlands, entanglements occurred more frequently on the Wadden islands (70.3%) as opposed to the mainland (29.7%). Gray seals were stranded 2.8 times more frequently on the Wadden islands than on the mainland, but harbor seal strandings seemed to occur at almost the same frequency in both locations ( Figure 1b). Due to the variability in the number of reports per year, we could not reliably compare yearly stranding rates based on location. However, the general trend per year did not seem to vary much: entangled gray seals were found more frequently on the Wadden islands, and it was equally likely to find entangled harbor seals on the islands than on the mainland (see Figures S1 and S2 in the Supplementary Materials). Entanglement rates varied yearly in both species. On average, yearly entanglement rates for gray and harbor seals were 0.3% and 0.04%, respectively, suggesting that gray seals are entangled more frequently. For gray seals, entanglements were seen every year, with the lowest entanglement rate being 0.03% in 2012; and the highest being 0.6% in 2019. For harbor seals, the lowest entanglement rates were in 2013 and 2016 when no entanglements were reported. The highest entanglement rate was 0.14% in 2019.
In the Netherlands, entanglements occurred more frequently on the Wadden islands (70.3%) as opposed to the mainland (29.7%). Gray seals were stranded 2.8 times more frequently on the Wadden islands than on the mainland, but harbor seal strandings seemed to occur at almost the same frequency in both locations (Figure 1b). Due to the variability in the number of reports per year, we could not reliably compare yearly stranding rates based on location. However, the general trend per year did not seem to vary much: entangled gray seals were found more frequently on the Wadden islands, and it was equally likely to find entangled harbor seals on the islands than on the mainland (see Figures S1 and S2 in the Supplementary Materials).
From the 145 reports, 15 animals were found dead and 130 were found alive. For 30 of the individuals found alive, no action could be taken at the moment of the encounter (e.g., they could not be caught). There were 41 animals released on-site from their entanglements (this applied to external entanglements only), and 59 were caught and transported to one of the rehabilitation centers. Three animals died while being transported to rehabilitation, and eight died or were euthanized during the rehabilitation process. The cause of death of these eight individuals was not always related to the severity of the lesions caused by the entanglement; in some cases, a concomitant disease (e.g., parasitic pneumonia) was the most likely cause of death. The remaining 48 animals were released back into the wild after a period in rehabilitation. Overall, the survival rate for animals accepted into rehabilitation was 85.7% ( Figure 2). rehabilitation, and eight died or were euthanized during the rehabilitation process. The cause of death of these eight individuals was not always related to the severity of the lesions caused by the entanglement; in some cases, a concomitant disease (e.g., parasitic pneumonia) was the most likely cause of death. The remaining 48 animals were released back into the wild after a period in rehabilitation. Overall, the survival rate for animals accepted into rehabilitation was 85.7% ( Figure 2). We checked for age and sex differences in the number of reported entanglements. We found that juveniles comprised more than 67% of the sample, suggesting that animals of a younger age are more affected by marine debris (Figure 3). There were no noticeable sex differences in the two seal species. Age and sex trends were similar across the years (see Figures S1 and S2 in Supplementary Materials). We checked for age and sex differences in the number of reported entanglements. We found that juveniles comprised more than 67% of the sample, suggesting that animals of a younger age are more affected by marine debris (Figure 3). There were no noticeable sex differences in the two seal species. Age and sex trends were similar across the years (see Figures S1 and S2 in Supplementary Materials).  External entanglements (93.8%) were more common than debris ingestion (4.8%). two cases, the animals presented both an external entanglement and ingestion of deb (1.4%). The results showed that gray seals were mostly affected by external entanglemen (98.3%), whereas harbor seals showed a higher incidence of ingested debris (22.2%) wh compared with gray seals. External entanglements located around the neck of the anim were more common (69%) than those located in other body parts (e.g., flippers or hea (Figure 4). In some cases, the animals were affected by the entanglement at two differe body sites. External entanglements (93.8%) were more common than debris ingestion (4.8%). In two cases, the animals presented both an external entanglement and ingestion of debris (1.4%). The results showed that gray seals were mostly affected by external entanglements (98.3%), whereas harbor seals showed a higher incidence of ingested debris (22.2%) when compared with gray seals. External entanglements located around the neck of the animal were more common (69%) than those located in other body parts (e.g., flippers or head) (Figure 4). In some cases, the animals were affected by the entanglement at two different body sites.
(98.3%), whereas harbor seals showed a higher incidence of ingested debris (22.2%) when compared with gray seals. External entanglements located around the neck of the animal were more common (69%) than those located in other body parts (e.g., flippers or head) (Figure 4). In some cases, the animals were affected by the entanglement at two different body sites. The majority of entanglements were caused by marine debris which originated from the boating/fishing industry (83.4%), such as fishing nets, ropes, fishing lines, fishing hooks, etc. From the marine debris in this category, fishing nets (88.4%) were the most abundant. In 12% of the reported entanglements, the debris had a different origin (i.e., The majority of entanglements were caused by marine debris which originated from the boating/fishing industry (83.4%), such as fishing nets, ropes, fishing lines, fishing hooks, etc. From the marine debris in this category, fishing nets (88.4%) were the most abundant. In 12% of the reported entanglements, the debris had a different origin (i.e., frisbee, clothing, potato net, rubber band, tarpaulin, etc.). Debris from fishing/boating was reported every year, whereas debris from other origins was not (see Figures S1 and S2 in the Supplementary Materials). Entanglements could be caused by a single piece of debris (89.7%) or by several pieces (5.5%) (e.g., fishing net and wrapping plastic). In seven cases, no information was reported about the origin of the debris (4.8%) ( Figure 5).

Discussion
The results of our study show that (i) the number of entangled seals incr the last years, (ii) gray seals are more affected by marine debris than harbor se most affected animals were juveniles, (iv) gray seals suffer more from externa ments (i.e., around the neck) and harbor seals ingest debris more frequently, an marine debris causing entanglements, such as fishing nets, comes from the fishi industry.

Discussion
The results of our study show that (i) the number of entangled seals increased over the last years, (ii) gray seals are more affected by marine debris than harbor seals, (iii) the most affected animals were juveniles, (iv) gray seals suffer more from external entanglements (i.e., around the neck) and harbor seals ingest debris more frequently, and (v) most marine debris causing entanglements, such as fishing nets, comes from the fishing/boating industry.

Yearly Trends
Our study reports on 145 cases of phocids affected by marine debris from 2010 to 2020 in the Netherlands. We compared our results with two previous studies on reported entanglements around the Dutch coast: Osinga and colleagues [15] reported 77 strandings of animals affected by marine debris from 1979 to 2008 (2.7 strandings per year); the 2010 SCP internal communication [25] reported 54 strandings over a 25-year period from 1985 to 2010 (2.2 strandings per year). This study (13.2 stranding per year) found that the number of yearly entanglements seems to have quadrupled since these reports were written, representing a clear and significant increase in the number of animals entangled in marine debris. It is important to note, however, that Osinga and colleagues [15] only reported strandings of dead animals, whereas this study and the 2010 SCP internal communication [25] reported on both live and dead strandings. Moreover, our study reports on strandings from all three Dutch rehabilitation centers, whereas the two previous studies only reported stranding data from SCP; hence, the current numbers must be interpreted with caution when comparing with the two previous studies.

Number of Entanglements
When comparing species, we found that the incidence of entanglements in gray seals is more than four times higher than that in harbor seals (Figure 2), even though, in 2016, the Dutch population of harbor seals was three times as large as the population of gray seals [23,31]. Our results are in line with those of the 2010 SCP internal communication [25], which reported a 2.6-fold higher incidence of entanglements in gray seals than in harbor seals, but contradict the results of Osinga and colleagues [15], who reported a 3.5-fold higher likelihood of entanglement in harbor seals. Nevertheless, the results obtained by Osinga and colleagues [15] should be interpreted with caution because most of the cases they reported were categorized as inferred by-catch. They defined inferred by-catch as dead animals found without a net and without external physical evidence of contact with fishing gear, but which always met all the following criteria: (1) fish (remains) in the stomach or intestines, (2) good nutritional condition, (3) no other significant pathological findings, and (4) the presence of lung edema. We believe that such cases do not necessarily suggest by-catch, because no further histopathological examination of carcass tissues was performed, potentially missing acute diseases without clear macroscopic alterations such as acute bronchopneumonia, cardiovascular problems, and septicemia, among others. This suggests that the higher incidence of reported entanglements in harbor seals was likely over-represented by Osinga and colleagues [15]. We thus propose that future studies only include cases of confirmed by-catch to avoid possibly inflating the number of reported entanglements, as conducted in the current report.
Comparing our results with previously published data, we found that, regardless of the location, gray seals still suffer more from entanglements than harbor seals [32,33]. Our gray seal yearly entanglement rate (0.3%) was considerably lower than the entanglement rates (3.6-5.0%) reported in the United Kingdom [34]. Similarly, our yearly entanglement rate for harbor seals (0.04%) was lower than rates (0.05-0.09%) reported in California in the mid-1980s [35]. However, these results should be interpreted with caution because none of the studies used the same methodology for reporting entanglements (e.g., only looking at haul-out sites) and calculating yearly entanglement rates.

Stranding Distribution
Gray seal breeding grounds are located on the islands of Vlieland, Terschelling, and the sandbanks in between both islands [36], which corresponds to the locations with higher stranding rates in this study (Figure 1b). Gray seals are known for their playful behavior [37,38]. They generally forage in deeper waters further away from their haul-out sites and eat larger prey [36,39]. The combination of playful behavior and foraging prefer-ences may bring gray seals closer to active fishing grounds, increasing the number of interactions with fisheries, and subsequently increasing the likelihood of becoming entangled.
Harbor seals were stranded more frequently on the coastlines of South Holland and North Holland. However, we cannot explain this particular finding as their distribution along the Dutch coast is relatively homogeneous [39]. The higher incidence of ingested debris, such as fishing lines and hooks, found in harbor seals may be explained by their preference to forage in shallower waters and eat smaller-sized prey that is often targeted by recreational fishing [39].
In the Netherlands, the habitat of both species is constantly affected by anthropogenic activities, such as fishing [23,24]. In fact, Hastie and colleagues [40] showed that gray seals take foraging decisions based on the amount of fish available and the risks associated with sound exposure (i.e., aversiveness to anthropogenic noise). These behavioral changes may affect their foraging efficiency, potentially increasing the number of interactions with fishing boats and causing an increased risk of entanglement [40,41].

Age Differences
We find that juveniles of both species are more affected by marine debris than adults or pups ( Figure 2). Young pinnipeds, particularly gray seals, tend to be more playful and curious than older individuals [20,37,38,42]. Juveniles tend to swim further away from their known haul-out locations to avoid competition with older individuals and explore new feeding grounds [43,44]. These age-related behavioral differences may explain the higher incidence of entanglements found in younger animals. Young animals are also the most affected by entanglements in other European locations, such as Ireland [32] and Germany [33].

Type of Entanglement
For both species, the most common external entanglements were located around the neck ( Figure 3). However, this type of entanglement may have been over-represented in this study because these occurrences are easier to spot from boats or from the beach. To establish that an animal has ingested debris, further diagnostic procedures, such as radiography, are required. This could potentially have contributed to an under-representation of ingested debris.

Origin and Type of Debris
The most common material found causing entanglements originated from fishing activities, particularly fishing nets ( Figure 4). This aligns with findings of the last Marine litter Wadden Sea Quality Status Report [4], which states that the majority of litter items found on beaches, such as plastic nets and ropes, are frequently used for fishing. Marine debris can be diverse, but because of its properties (resistant, durable, flexible, accessible, etc.), plastic debris is the most abundant [4,6,17]. In fact, five out of the nine seals that ingested marine debris in our study had swallowed fishing lines made of a synthetic plastic material called nylon. The direct effects of swallowed fishing line have been described before [12,20]; however, a potential indirect effect should be considered. Over time, large pieces of plastic can break down into smaller pieces due to the effect of waves, currents, and sunlight [45]. These small plastic particles, known as microplastics, can act as anchors for certain pollutants and toxins (e.g., persistent organic pollutants-POPs-or bis-phenol A). If these plastics are ingested, the pollutants they hold can leach out of them [45]. Once inside of an organism, these toxic substances accumulate in its body tissues because they cannot be metabolized. Individuals may suffer from a range of impairments, including endocrine disruption, growth inhibition, and impaired reproduction [1,[46][47][48][49]. Moreover, the body tissue concentration of environmental pollutants increases at higher levels in the trophic food chain in a process known as biomagnification [50]. Seals, which are the apex predators of the Wadden Sea, are thus likely already exposed to higher levels of pollutants [49]. It is, however, unknown whether the ingestion of plastic debris further accelerates the uptake of environmental pollutants in seal body tissues.
In addition to the composition of the debris, the shape of the debris may also play a role in the incidence of entanglements. Debris that resembles the shape of a seal's prey could trigger a foraging behavior, potentially increasing the number of interactions with the debris, and consequently, the chances of becoming entangled. For example, the shape of a rope may resemble a sand eel (typical prey of gray and harbor seals [51,52]).

Data Collection Standardization
Although not all entangled animals are in need of rehabilitation, some entanglements may result in lesions that require medical treatment, as demonstrated by the case of a young gray seal (see the Supplementary Materials). The survival of such affected individuals is dependent on the quality of the intensive care provided, emphasizing the importance of rehabilitation efforts. Unfortunately, due to the lack of consistency among stranding reports, no further analysis was conducted based on the severity of the wounds. Forney and colleagues [53] developed a classification system of the severity of entanglement injuries in marine mammals, which we tried to apply in this study. According to this approach, the majority of our reported cases fell into the serious injury category, but we found that if immediate action could be taken and the entangled marine debris was removed on-site, serious injuries could be completely avoided. With this in mind, the authors have adapted Forney et al.'s [53] classification system based on our experience in seal rehabilitation. In doing so, we propose a comprehensive and standardized method for reporting and classifying entangled animals, which will facilitate data collection and improve on-site decision-making (see the Supplementary Materials).

Conclusions
In conclusion, we have shown that the numbers of entanglement cases are rapidly increasing around the Dutch coast. There may be several reasons for the increasing numbers of reported entanglements found in this study. First, the observed increase may be directly related to increased interactions with marine debris due to the higher abundance of waste found in our oceans [4,10,17,21,22]. Despite both gray and harbor seals having healthy populations in the Wadden Sea [23], the combined effects of anthropogenic threats, such as the increased abundance of marine debris, higher levels of environmental pollution (e.g., noise and microplastics), and increased interactions with fisheries, could, in the long run, become an important risk to the survival of these populations. There is thus an urgent need to keep developing public programs and implement governmental policies which aim to protect the marine environment. For example, initiatives such as the "Bins on Boats" are proving very successful in reducing the amount of boat-generated litter [54]. Second, the recent advice issued by the Scientific Advisory Committee on the rehabilitation of seals in the Netherlands states that "injured animals are to be assisted or rehabilitated if the injuries have been caused by direct human activities" [31], potentially resulting in increased public awareness of how local marine wildlife may be affected by environmental debris. Third, the heightened will to help animals in need combined with the widespread use of new technologies in recent years, such as smartphones and social media (e.g., WhatsApp), may have facilitated contact with rehabilitation centers, increasing the number of reported entanglements. Although public awareness is increasing and policies aimed at protecting the Dutch marine environment are being developed and implemented, it is currently unknown whether these efforts will be enough to ensure healthy and sustainable populations of gray and harbor seals in the years to come.