a global review of marine turtle entanglement in

18
ENDANGERED SPECIES RESEARCH Endang Species Res Vol. 34: 431–448, 2017 https://doi.org/10.3354/esr00865 Published December 11 INTRODUCTION Marine plastic pollution Anthropogenic materials, the majority of them plas- tic, are accumulating on the surface of the oceans, in the water column and on the seabed (Thompson et al. 2004). The durability of plastic means that it may per- sist for centuries (Barnes et al. 2009). It is estimated that 4.8 to 12.7 million tonnes of plastic waste could be entering the marine environment annually (Jambeck et al. 2015). Over 700 marine species have been demonstrated to interact with marine plastic pollution (Gall & Thompson 2015), which presents a risk to ani- © The authors 2017. Open Access under Creative Commons by Attribution Licence. Use, distribution and reproduction are un- restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com *These authors contributed equally to this work **Corresponding author: [email protected] REVIEW A global review of marine turtle entanglement in anthropogenic debris: a baseline for further action Emily M. Duncan 1,2,3, *, Zara L. R. Botterell 1, *, Annette C. Broderick 1 , Tamara S. Galloway 2 , Penelope K. Lindeque 3 , Ana Nuno 1 , Brendan J. Godley 1, ** 1 Marine Turtle Research Group, Centre for Ecology and Conservation, University of Exeter, Penryn TR10 9FE, UK 2 Biosciences, College of Life and Environmental Sciences, Geoffrey Pope Building, University of Exeter, Stocker Road, Exeter EX4 4QD, UK 3 Marine Ecology and Biodiversity, Plymouth Marine Laboratory, Prospect Place, West Hoe, Plymouth PL1 3DH, UK ABSTRACT: Entanglement in anthropogenic debris poses a threat to marine wildlife. Although this is recognised as a cause of marine turtle mortality, there remain quantitative knowledge gaps on entanglement rates and population implications. We provide a global summary of this issue in this taxon using a mixed methods approach, including a literature review and expert opinions from conservation scientists and practitioners worldwide. The literature review yielded 23 reports of marine turtle entanglement in anthropogenic debris, which included records for 6 species, in all ocean basins. Our experts reported the occurrence of marine turtles found entangled across all species, life stages and ocean basins, with suggestions of particular vulnerability in pelagic juve- nile life stages. Numbers of stranded turtles encountered by our 106 respondents were in the thou- sands per year, with 5.5% of turtles encountered entangled; 90.6% of these dead. Of our experts questioned, 84% consider that this issue could be causing population level effects in some areas. Lost or discarded fishing materials, known as ‘ghost gear’, contributed to the majority of reported entanglements with debris from land-based sources in the distinct minority. Surveyed experts rated entanglement a greater threat to marine turtles than oil pollution, climate change and direct exploitation but less of a threat than plastic ingestion and fisheries bycatch. The challenges, research needs and priority actions facing marine turtle entanglement are discussed as pathways to begin to resolve and further understand the issue. Collaboration among stakeholder groups such as strandings networks, the fisheries sector and the scientific community will facilitate the development of mitigating actions. KEY WORDS: Conservation · Entanglement · Ghost fishing · Marine debris · Plastic pollution · Sea turtle · Strandings OPEN PEN ACCESS CCESS Contribution to the Special ‘Marine pollution and endangered species’

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Page 1: A global review of marine turtle entanglement in

ENDANGERED SPECIES RESEARCHEndang Species Res

Vol. 34: 431–448, 2017https://doi.org/10.3354/esr00865

Published December 11

INTRODUCTION

Marine plastic pollution

Anthropogenic materials, the majority of them plas-tic, are accumulating on the surface of the oceans, inthe water column and on the seabed (Thompson et al.

2004). The durability of plastic means that it may per-sist for centuries (Barnes et al. 2009). It is estimatedthat 4.8 to 12.7 million tonnes of plastic waste could beentering the marine environment annually (Jambecket al. 2015). Over 700 marine species have beendemonstrated to interact with marine plastic pollution(Gall & Thompson 2015), which presents a risk to ani-

© The authors 2017. Open Access under Creative Commons byAttribution Licence. Use, distribution and reproduction are un -restricted. Authors and original publication must be credited.

Publisher: Inter-Research · www.int-res.com

*These authors contributed equally to this work**Corresponding author: [email protected]

REVIEW

A global review of marine turtle entanglement in anthropogenic debris:

a baseline for further action

Emily M. Duncan1,2,3,*, Zara L. R. Botterell1,*, Annette C. Broderick1, Tamara S. Galloway2, Penelope K. Lindeque3, Ana Nuno1, Brendan J. Godley1,**

1Marine Turtle Research Group, Centre for Ecology and Conservation, University of Exeter, Penryn TR10 9FE, UK2Biosciences, College of Life and Environmental Sciences, Geoffrey Pope Building, University of Exeter, Stocker Road,

Exeter EX4 4QD, UK3Marine Ecology and Biodiversity, Plymouth Marine Laboratory, Prospect Place, West Hoe, Plymouth PL1 3DH, UK

ABSTRACT: Entanglement in anthropogenic debris poses a threat to marine wildlife. Althoughthis is recognised as a cause of marine turtle mortality, there remain quantitative knowledge gapson entanglement rates and population implications. We provide a global summary of this issue inthis taxon using a mixed methods approach, including a literature review and expert opinionsfrom conservation scientists and practitioners worldwide. The literature review yielded 23 reportsof marine turtle entanglement in anthropogenic debris, which included records for 6 species, in allocean basins. Our experts reported the occurrence of marine turtles found entangled across allspecies, life stages and ocean basins, with suggestions of particular vulnerability in pelagic juve-nile life stages. Numbers of stranded turtles encountered by our 106 respondents were in the thou-sands per year, with 5.5% of turtles encountered entangled; 90.6% of these dead. Of our expertsquestioned, 84% consider that this issue could be causing population level effects in some areas.Lost or discarded fishing materials, known as ‘ghost gear’, contributed to the majority of reportedentanglements with debris from land-based sources in the distinct minority. Surveyed expertsrated entanglement a greater threat to marine turtles than oil pollution, climate change and directexploitation but less of a threat than plastic ingestion and fisheries bycatch. The challenges,research needs and priority actions facing marine turtle entanglement are discussed as pathwaysto begin to resolve and further understand the issue. Collaboration among stakeholder groupssuch as strandings networks, the fisheries sector and the scientific community will facilitate thedevelopment of mitigating actions.

KEY WORDS: Conservation · Entanglement · Ghost fishing · Marine debris · Plastic pollution · Sea turtle · Strandings

OPENPEN ACCESSCCESS

Contribution to the Special ‘Marine pollution and endangered species’

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Endang Species Res 34: 431–448, 2017

mals through ingestion, entanglement, degradation ofkey habitats and wider ecosystem effects (Nelms et al.2016). Megafauna such as marine turtles with complexlife histories and highly mobile behaviour are particu-larly vulnerable to its impacts (Schuyler et al. 2014).

Entanglement in marine litter

Entanglement in plastic debris is recognised as amajor risk for many marine species (Laist 1987, Vegter et al. 2014). This has become sufficiently highprofile that the European Union’s Marine StrategyFramework Directive (MSFD) Technical Subgroupon Marine Litter has announced that it will develop adedicated monitoring protocol for its next report(MSFD GES Technical Subgroup on Marine Litter2011). Entanglement has the potential to cause arange of fatal and non-fatal impacts such as seriouswounds leading to maiming, amputation, increaseddrag, restricted movement or choking (Votier et al.2011, Barreiros & Raykov 2014, Lawson et al. 2015).

Types of marine debris causing entanglement

The debris causing this entanglement falls into 2broad categories. Firstly, hundreds of tons of fishinggear are lost, abandoned or discarded annually,forming ‘ghost gear’ which passively drifts over large distances, sometimes indiscriminately ‘fishing’ mar-ine organisms (Macfadyen et al. 2009, Wilcox et al.2013). This gear is commonly made of non-bio -degradable synthetic material that will persist in themarine environment, potentially become biofouledby marine organisms and act as a fish aggregatingdevice (FAD), attracting both grazers and predatorssuch as marine turtles (Filmalter et al. 2013, Wilcox etal. 2013). It is important to distinguish here between‘entanglement’ and ‘bycatch’. Bycatch can be de -fined as unselective catch of either unused or unman-aged species during fishing, with a particular focuson ‘active’ gear, whereas ghost gear can be definedas equipment of which the fisher has lost operationalcontrol (Smolowitz 1978, Davies et al. 2009). There-fore, here we consider animals caught in passiveghost fishing gear as entangled, not bycaught. Sec-ondly, there have also been reports of entanglementin litter from land-based sources (Chatto 1995, Ben-tivegna 1995, Santos et al. 2015). In this review we donot include bycaught turtles — only those that havebecome entangled in passive anthropogenic debrissuch as ghost gear or land-based debris.

Current knowledge gaps regarding turtle entanglement

Despite turtle entanglement being recognised asone of the major sources of turtle mortality in north-ern Australia and the Mediterranean, there is a quan-titative knowledge gap with respect to the entangle-ment rates and possible implications in terms of globalpopulations (Casale et al. 2010, Wilcox et al. 2013,Camedda et al. 2014, Gilman et al. 2016). A re cent lit-erature review by Nelms et al. (2016) returned only 9peer-reviewed publications on marine debris entan-glement and turtles (Bentivegna 1995, Chatto 1995,López-Jurado et al. 2003, Casale et al. 2010, Santos etal. 2012, Jensen et al. 2013, Wilcox et al. 2013, 2015,Barreiros & Raykov 2014). Of these, 7 were focusedon ghost fishing gear, highlighting the distinct lack ofknowledge of entanglement in debris from land-based sources. Even fewer of these studies focusedon the potential variable susceptibility among lifestages or species, with only one paper, Santos et al.(2012), reporting that the majority of entangled oliveridley turtles Lepidochelys olivacea on the Brazilianislands of Fernando de Noronha and Atol das Rocaswere sub-adults and adults.

Research rationale in terms of marine turtles and pollution

In terms of global research priorities for sea turtleconservation and management, understanding theimpact of pollution is considered of high importance(Hamann et al. 2010, Rees et al. 2016). To evaluatethis effectively, the impact of anthropogenic debris,specifically, must be considered at a species and pop-ulation level. Additionally, it is important to under-stand the variation in entanglement rates among species and life stages to better evaluate vulnerabil-ity and the frequency of interactions with differentdebris types (Nelms et al. 2016). Once these havebeen established, opportunities for delivering effec-tive education and awareness can be given or othermitigation planned (Vegter et al. 2014).

Here, we define marine turtle entanglement as‘the process under which a marine turtle becomesentwined or trapped within anthropogenic materi-als.’ We sought to include discarded fishing gear(ghost fishing) as well as land-based sources. Theaim of this study was to (1) review existing, andobtain new, reports of the occurrence and global spa-tial distribution of marine turtle entanglement; (2)gain insights into patterns of species, life stage and

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Duncan et al.: Marine turtle entanglement

debris type involved across entanglement cases; and(3) glean an insight into the change in prevalence ofmarine debris entanglement over time. To addressthese, a mixed methods approach was employed, in -volving a literature review and an elicitation of ex -pert opinions. Given the difficulty of acquiring robuststandardised data, this review is intended to high-light the value of mixed methods as a first step tounderstand complex conservation issues, and to pro-vide suggestive yet relevant indications as to thescale of the threat of entanglement to marine turtles.

MATERIALS AND METHODS

Literature review

In January 2016 and again in June 2017 (during themanuscript review process), all relevant literaturewas reviewed that may have contained records ofmarine turtle entanglement. ISI Web of Knowledge,Google Scholar and the Marine Turtle Newsletter(www.seaturtle.org) were searched for the terms ‘en -tanglement’, ‘entrapment’, ‘ensnare’ or ‘ghost fishing’and ‘turtle’. The first 200 results were viewed, withresults very rarely fulfilling the criteria after the first20; spurious hits were ignored and all relevant refer-ences were recorded and investigated.

Elicitation of expert opinions

During the period 1–30 April 2016, an online ques-tionnaire survey was conducted to investigate 3 maintopics of interest: (1) the occurrence and global spa-tial distribution of sea turtle entanglement; (2) spe-cies, life stage and debris type involved; and (3) thechange in entanglement prevalence over time. Atotal of 20 questions requiring both open and closedresponses from a range of experts were used toobtain insight into the scale of marine turtle entan-glement. We clearly explained to the respondents thedefinition of ‘marine turtle entanglement’ specific tothis study. Grid-like responses and Likert scales,offering potential answers from a range of ordinaloptions, were used to aid in achieving a quantitativeassessment of the issues (Elaine & Seaman 2007) (seeBox S1 in the Supplement at www. int-res. com/articles/ suppl/ n034 p431 _ supp. pdf).

Potential participants for this questionnaire wereidentified from lead authorship of papers compiled inthe recent review on the effects of marine plasticdebris on turtles from Nelms et al. (2016), and our

review due to their involvement in research into marine debris. From reviewing the few publishedreports, it was apparent that governmental strandingnetworks, sea turtle rescue and rehabilitation centresand conservation projects may also hold many un -published records of entanglement occurrence. Acomprehensive list of such organisations from sea -turtle.org (www.seaturtle.org/groups/; accessed 24March 2016) was used to find more expert contacts toparticipate in the questionnaire. Additionally, con-sidering the aim of attaining an appropriate numberof respondents while avoiding potential samplingbiases due to researchers’ personal networks and per-ceptions about the issue (Newing 2011), we employedrespondent-driven sampling; this purposive sam-pling approach involves requesting those directlycontacted to recruit additional participants amongcolleagues, peers and other organisations that mayhave knowledge of additional records of marine turtle entanglement.

From this first questionnaire, an initial report wasproduced and sent to the expert respondents (n =106) to share the results and thoughts that arose fromthe first questionnaire. This included 8 initial figuresproduced from the data given by respondents in theoriginal questionnaire to aid feedback of our results(these were draft versions of Figs. 2, 3 & 4). Followingthis, during the period 24 May to 30 June 2016, a fol-low-up questionnaire survey was conducted with theexpert participants of the first questionnaire surveywho were then invited to comment and answer 10open and closed questions (see Box S2 in the Supple-ment). This aimed to further understand the chal-lenges, future requirements (both research and prior-ity actions) and perceptions of the likelihood ofpopulation level effects of marine turtle entangle-ment. In this second questionnaire, respondentswere asked to comment on our initial results and toprovide suggestions on future knowledge gains andactions. Their answers were categorised using aninductive approach; summary themes were identi-fied through the process of directly examining thedata (Elo & Kyngäs 2008), instead of having pre-defined categories.

RESULTS

Literature review

Our literature search yielded 23 reports regardingentanglement in multiple species of marine turtles,the majority of which were peer-reviewed publica-

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Endang Species Res 34: 431–448, 2017

tions (n = 17) with additional grey literature reports(n = 6). Species included loggerhead Caretta caretta(n = 7), green Chelonia mydas (n = 7), leatherbackDermochelys coriacea (n = 5), hawksbill Eretmo -chelys imbricata (n = 5), olive ridley Lepido chelys oli-vacea (n = 9) and flatback Natator depressus (n = 2).There were no records for Kemp’s ridley Lepi-dochelys kempii (Table 1). Of these publications, 18reported entanglement due to ghost fishing or fish-eries materials and 7 recorded entanglement in land-based plastic debris; 7 publications reported the sizerange and life stage of the entangled turtles. Thesepublications highlighted a range of impacts of entan-glement, such as serious wounds leading to maiming,amputation or death, increased drag, restrictedmovement or choking that were further illustrated byphotographs from collaborating experts (Fig. 1).

Elicitation of expert opinions

Survey response rates and demographics

From an estimated pool of ca. 500 potential contacts,the ‘Marine Turtle Entanglement Questionnaire’ wasreceived and completed by a total of 106 expert re-spondents from 43 countries. However, due to theanonymous nature of the survey and the potentialaugmentation from the use of respondent-driven sam-pling, it is not possible to determine how many ofthose initially contacted took part in the survey. Allocean basins were covered; the respondents’ mainoceanic region of work was given as: Atlantic (34.8%;n = 39), Pacific (18.9%; n = 20), Caribbean (25.5%;n = 27), Mediterranean (9.4%; n = 10) and Indian(9.4%; n = 10). Respondents experienced a wide

434

Fig. 1. Impacts of marine turtle entanglement: (a) live leatherback turtle entangled in fishing ropes which increases drag,Grenada 2014 (photo: Kate Charles, Ocean Spirits); (b) drowned green turtle entangled in ghost nets in Uruguay (photo:Karumbe); (c) live hawksbill turtle entangled in fishing material constricting shell growth, Kaeyama Island, Japan 2001 (photo:Sea Turtle Association of Japan); (d) live hawksbill turtle with anthropogenic debris wrapped around front left flipper con-stricting usage of limb which could lead to amputation and infection, Kaeyama Island, Japan 2015 (photo: Sea Turtle Associa-

tion of Japan). All photos used with express permission

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Duncan et al.: Marine turtle entanglement 435

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Endang Species Res 34: 431–448, 2017

range in the number of annual stranding cases in theirrespective study sites (annual maxima given in thesurvey; mean ± SE = 239.9 ± 71.7, range = 0 to 4100,n = 97) but in total, through addition of the respon-dents’ answers, they are responsible for at tending anestimated 23 000 stranded turtles yr−1. Respondentsalso generally had many years of ex perience dealingwith and reporting marine turtle strandings (range = 2to 42 yr, mean ± SE = 15.6 ± 1.1, n = 98), confirmingthem as having relevant ex perience to answer thesurvey. The second follow-up questionnaire sent to allrespondents (n = 106) received 63 responses with re-spondents from 31 countries.

Rates of entanglement

A majority of respondents (84.3%; n = 101) hadencountered cases in which turtles were entangled inanthropogenic debris. When broken down by spe-cies, the proportion of stranded turtles that wereentangled did not differ significantly (Kruskal-Wallis:χ2 = 4.59, df = 6, p = 0.59) (Fig. 2a). There was a lowpercentage incidence for all species, with the grandmedian rate of 5.5%, although there was consider-able inter- and intraspecific variation, with incidencesin different responses ranging from 0 to 95.5%. Interms of the proportion of marine turtles alive whenfound entangled, there were significant interspecificdifferences (Kruskal-Wallis: χ2 = 19.62, df = 6, p =0.003). The proportion found alive (grand median =9.4%) was significantly higher in green (25.5%) andloggerhead (15.5%) turtles than in all other species(5.5%) (Fig. 2b).

Entanglement rates also differed amongst life stagesfor each species. Whilst respondents indicated thatall life stages of each species had been affected byentanglement, the results suggested adults weremost impacted in leatherback and olive ridley turtles,whereas for the remaining species respondents indi-cated a higher rate of entanglement in juveniles(pelagic and neritic; Fig. 3).

When considering this issue over time (over the last10 yr), a similar proportion of respondents (35.8% of106) thought the prevalence of entanglement hadincreased or remained the same, while the remainderthought it had decreased (8.5%) or were unsure(19.8%). Among those respondents that noted anincrease, some (n = 4) suggested that this may becaused by an increase in reporting and awareness,while others (n = 9) indicated the development ofcoastal fishing activities might be a factor. Whenasked to consider a shorter time period (the last 5 yr),

the majority of respondents believed that the pre -valence of entanglement they had experienced hadremained stable (51.9%), whilst the others thought ithad increased (29.2%), decreased (3.8%) or were notsure (15.1%).

Entanglement materials

The majority of entanglements recorded were withlost/discarded fishing gear (Fig. 4). A clear distinc-tion was made between ‘active’ and ‘lost/discarded’

436

0

20

40

60

80

100

CC CM DC EI LK LO NDSpecies

% a

live

0

20

40

60

80

100a

bCC CM DC EI LK LO ND

% e

ntan

gled

Fig. 2. Inter-species comparison of the proportion of: (a)stranded individuals found entangled and (b) individualsfound alive when discovered entangled. Violin plots showthe kernel density of data at different values. Median (blackdot) with interquartile range boxplot (black/white) andgrand median (black dashed line). Turtle species abbrevia-tions: CC: loggerhead Caretta caretta; CM: green Cheloniamydas; DC: leatherback Dermochelys coriacea; EI: hawks-bill Eretmochelys imbricata; LK: Kemp’s ridley Lepidochelyskempii; LO: olive ridley Lepidochelys olivacea; ND: flatback

turtle Natator depressus

Page 7: A global review of marine turtle entanglement in

Duncan et al.: Marine turtle entanglement

fishing gear to try and separate incidents due tobycatch and subsequent stranding from those causedby ghost fishing. The number of responses on theoccurrence of ghost fishing (GF) through discardedfishing debris (rope, net and line) was generallyslightly higher than for bycatch (BC) through activegear.

A smaller percentage of respondents specifiedcases of turtle entanglement in land-based sources,from polythene sheeting (n = 71), woven sacks (n =72) and non-fishing rope/twine (n = 68). But in only afew incidences were these said to be common oc -currences (polythene sheeting [n = 3], woven sacks[n = 4], non-fishing rope/twine [n = 7]). Respondentswere asked to comment on the occurrence of ‘other’

entangling materials (n = 54) and to provide exam-ples (n = 20) that caused turtle entanglement. Thisincluded debris from land-based sources (plastic -balloon string, canned drink ‘6-pack’ rings, kitestring, plastic chairs, plastic packaging straps, wood -en crates and weather balloons) and debris fromother maritime activities (boating mooring line, an -chor line and discarded seismic cable).

Scale of issue

In order to obtain further insights into the potentialscale of this issue, respondents to the second surveywere asked whether they thought entanglement inanthropogenic debris is causing population-level ef-fect in marine turtles. Of the 63 respondents, 84.1%thought that this was probable, very likely or definite(see Fig. S1 in the Supplement). There was no signif-icant difference in scaled responses by ocean basin(Kruskal-Wallis: χ2 = 1.82, df = 4, p = 0.77). In order toassess the relative importance of different threats ac-cording to experts, we also sought the experts’ opin-ions on how they thought entanglement in anthro-

437

Fig. 3. Inter-specific comparison of the breakdown of entan-gled sea turtle species by life stage. Black: pelagic juveniles(PJ); white: neritic juveniles (NJ); light grey: juveniles (JV);dark grey: adults (AD); see Fig. 2 for species abbreviations.Flatback turtles were only categorised into juvenile or adultclasses with advice from species experts. Sea turtle skull fig-ures used with permission of WIDECAST; original artwork

by Tom McFarland

0 20 40 60 80 100

L/DF net

L/DF line

A/F line

L/DF rope

A/F net

A/F rope

Other

Poly sheet

Woven sacks

Non-F rope/twine

n = 54

n = 71

No. of responses

n = 72

n = 68

n = 75

n = 81

n = 78

n = 79

n = 86

n = 81

Fig. 4. Entangling materials. L/DF: lost/discarded fishing;A/F: active fishing; Non-F: non fishing; Poly sheet: poly -ethylene sheeting. Black: common (10% or more of cases);grey: sometimes (less than 10% of cases); white: never. Notall participants categorised each material; total number ofresponses for each material shown on the right of the graph

Page 8: A global review of marine turtle entanglement in

Endang Species Res 34: 431–448, 2017

pogenic debris compared to other threats to marineturtles (i.e. ‘plastic ingestion’, ‘oil pollution’, ‘fisheriesbycatch’, ‘direct exploitation’ and ‘climate change’).Although between 6.35 and 25.4% were unsure,there was a strong opinion that plastic ingestion andfisheries bycatch were greater threats, and that oilpollution, climate change and direct exploi tationwere less severe threats than entanglement (Fig. 5).

Challenges, priority actions and research needs

Respondents to the second survey converged on alimited number of themes when considering thechallenges, research needs and priority actions with -in marine turtle entanglement. The challenges toaddressing the issue (115 suggestions) could begrouped into 5 major categories: law and enforce-ment (23.5%; n = 27); sources and spatial extent ofentanglement materials (24.3%; n = 28); educationand innovation (24.3%; n = 28); understanding thefull extent of the threat (18.3%; n = 21); and humanresponse to entangled turtles (9.6%; n = 11) (Table 2).Seven major research areas were suggested by re -spondents (91 suggestions): more specific reportingand monitoring or a common database (23.1%; n =21); mapping the threat/spatio-temporal hotspots(31.9%; n = 29); identifying entanglement materialsand sea turtle inter actions (24.2%; n = 22); under-standing post-release mortality and physical effects(3.3%; n = 3); socio-economic impacts (4.4%; n = 4);innovation of new replacement materials (6.6%; n =6); and demographic risk assessments (6.6%; n = 6)(Table 3). Priority actions (n = 121 suggestions) thatrespondents believe would help re duce turtle entan-glement were grouped into 5 major areas: educa-tion/stakeholder engagement (31.4%; n = 38); fish-eries management and monitoring (26.4%; n = 32);research (5%; n = 6); law and enforcement (20.7%;n = 25); and development of alternative materials andmethods (16.5%; n = 20) (Table 4).

DISCUSSION

Global distribution

Our review and elicitation of expert opinions de -monstrate that marine turtle entanglement is an issueoperating at a global scale, occurring in all species,throughout their geographic range. We sought toanswer key knowledge gaps surrounding the issue ofturtle entanglement in marine debris as previously

highlighted by Vegter et al. (2014) and Nelms et al.(2016). Difficulties in investigating these knowledgegaps are in part due to a lack of robust data. Thishighlights the importance of using mixed methods toaccess expert opinion to gain an insight into thisglobal threat. The growing use of expert knowledgein conservation is driven by the need to identify andcharacterise issues under limited resource availabil-ity, and the urgency of conservation decisions (Mar-tin et al. 2012).

Acknowledging the incomplete coverage of our es-timates, given the mean estimated number of strand-ings and mortality rates, in the order of 1000 turtlesdie annually as a result of entanglement in the areasmonitored by our respondents. These levels arelikely a profound underestimation of the scale of thisissue as the coverage of these actors is far from com-prehensive. Second, it is well known that not all deadturtles strand (Epperly et al. 1996, Sasso & Epperly2007), especially small and pelagic animals, andthere can also be decay of entangled animals. Addi-tionally, some of our respondents commented thatdetection of stranded animals may be further con-founded due to take of stranded animals for humanconsumption.

438

Fig. 5. Responses to comparison of other threats faced bymarine turtles compared to entanglement (n = 63). Black:greater than entanglement; grey: similar threat; white: less

than entanglement; striped: unsure

Page 9: A global review of marine turtle entanglement in

Duncan et al.: Marine turtle entanglement 439

Ch

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Page 10: A global review of marine turtle entanglement in

Endang Species Res 34: 431–448, 2017440

Res

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= 9

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rd n

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n w

ater

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in

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igh

pre

ssu

re o

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nal

an

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por

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tify

ing

an

d m

app

ing

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nd

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even

t oc

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, su

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s ta

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ore

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ls

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ng

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pin

g p

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of d

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s

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nd

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n s

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ats

(e.g

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g a

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fee

din

g

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on, p

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of m

arin

e tu

rtle

g

rou

nd

s) w

ith

are

as o

f h

igh

deb

ris

con

cen

trat

ion

(e.

g. c

onve

rgen

ce z

ones

)’

m

igra

tion

s an

d t

he

char

acte

riza

tion

of

fish

erie

s d

istr

ibu

tion

s

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cale

s. H

otsp

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tan

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men

t m

ater

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an

d

2

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tud

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g s

ea t

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beh

avio

ur

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ral

(for

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r sh

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trai

ts i

n d

iffe

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t tu

rtle

sp

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s or

se

a tu

rtle

in

tera

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ns

an

d t

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r in

tera

ctio

ns

pop

ula

tion

s th

at m

ay t

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e vu

lner

able

to

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ng

lem

ent’

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vest

igat

e th

e b

ehav

iou

ral

char

acte

rist

ics

of t

he

turt

les

that

lea

d t

o th

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trap

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fis

hin

g g

ear

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h a

vie

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o im

pro

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Endang Species Res 34: 431–448, 2017

Species differences

Although there was no interspecific difference inthe incidence of entanglement, most peer-reviewedpublications featured olive ridley turtles, with someexperts reporting high incidences of entanglementfor this species. Stelfox et al. (2016) noted that oliveridley turtles accounted for the majority of sea turtlesidentified as entangled (68%; n = 303), and this couldbe for the following reasons. Firstly, this species,which often exhibits mass nesting in the hundreds ofthousands of individuals, is highly numerous, and atparticularly high densities in some areas, leading toentanglement hotspots (Jensen et al. 2006, Koch etal. 2006, Wallace et al. 2010a). Secondly, the oliveridley forages along major oceanic fronts which areknown to aggregate marine debris (Polovina et al.2004, McMahon et al. 2007). Finally, their generalistfeeding behaviour potentially attracts them to feedopportunistically on biofouled marine debris such asghost gear (Stelfox et al. 2016).

Life stages

Entanglement was reported to occur in all lifestages (pelagic juveniles, neritic juveniles and adults)across all species (the exception being flatback tur-tles which have no pelagic juveniles; Hamann et al.2011). Perhaps of greatest concern is the signal ofhigh entanglement incidence in the pelagic juvenilestage: despite the general inaccessibility of samplingthis life stage, they are still appearing as strandedentangled. The currents that transport hatchlings tooceanic convergence zones are also now recognisedas concentrating floating anthropogenic debris, cre-ating the capacity for an ecological trap for theseyoung turtles, whether it be through ingestion orentanglement (Nelms et al. 2016, Ryan et al. 2016).Many respondents considered that entanglementcould be having a population level effect; a distinctpossibility if this there is a large impact on this crypticlife stage and on pelagic foraging adults (Mazaris etal. 2005).

Entangling materials

Respondent data highlighted that the majority ofentanglements were the result of fishery-basedmaterial and other maritime activities. The issue ofghost fishing featured highly, with numerous res -ponses reporting entanglement within lost/discarded

gear. This gear is often lost, abandoned or discardedwhen it becomes derelict, attracting scavengers andacting as FADs (Gilman 2011). Subsequently, speciessuch as marine turtles become entangled within thegear, perhaps encouraged by this process of ‘self-baiting’ (Matsuoka et al. 2005).

Change in fishing practice

The issue of ghost fishing appears to have wors-ened since the 1950s, as the world’s fishing indus-tries have replaced their gear, which was originallymade of natural fibres such as cotton, jute andhemp, with synthetic plastic materials such asnylon, poly ethylene and polypropylene. Manufac-tured to be resistant to degradation in water meansthat once lost, it can remain in the marine environ-ment for decades (Good et al. 2010). Furthermore,there has also been a shift in the type of syntheticnets being selected; for example, fishers in part ofSoutheast Asia now increasingly favour superfinenets. Al though this can help increase catches, thetwine thinness means that they break easily and aredifficult to repair once damaged (Stelfox et al.2016). The incidences of entanglement caused bythis form of pollution in our expert surveys indicatesthat this source of mortality for marine turtles mir-rors that in marine mammals and sea birds, whichhas increased substantially over the last century(Tasker et al. 2000, Good et al. 2010, McIntosh et al.2015).

Differentiation from bycatch

It is quite plausible that ghost fishing may be work-ing synergistically alongside bycatch, but because ofits more cryptic nature this means that understand-ing its role in marine turtle mortality is much moredifficult. Bycatch is better understood. For example,the analysis of catch rates in the Mediterraneanallowed for the estimation of 132 000 captures and44 000 incidental deaths per year (Casale 2011). Like-wise, cumulative analysis of catch rates in US fish-eries estimated a total of 71 000 annual deaths priorto the establishment of bycatch mitigation methods.Since these measures were implemented, mortalityestimates are ~94% lower (4600 deaths yr−1) (Fink -beiner et al. 2011). This highlights the importance ofinformed estimates to monitor the success of mitiga-tion methods. In addition to bycatch mortality esti-mates, spatial and temporal patterns of bycatch inci-

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dences can be identified. Using onboard observerdata, Gardner et al. (2008) found seasonal changes incatch distributions of loggerhead and leatherbackturtles in the North Atlantic, with patterns of spatialclustering from July to October. Analysed on a globalscale, Wallace et al. (2010b) were able to highlightregion− gear combinations requiring urgent actionsuch as gillnets, longlines and trawls in the Mediter-ranean Sea and eastern Pacific Ocean. Generatingsuch estimates of catch rates and spatial/temporalpatterns for entanglement are not yet possible due tothe lack of quantitative information.

Land-based plastic entanglements

The domination of fisheries-based materials in theresults does not mean that land-based plastics arenot a source of entanglement. The increased input ofplastic debris from terrestrial run-off means thatthese interactions are only likely to increase (Jam-beck et al. 2015). Our literature search and ‘other’materials stated by respondents contained a varietyof items causing entanglement that could be de -creased by reduction of use, replacement with moredegradable alternatives and better waste manage-ment and recycling. The prevalence of these materi-als in the marine environment will very much de -pend on future waste governance, especially in thosecountries that generate the most plastic waste (Jam-beck et al. 2015). A future technological solutionwhich is currently being investigated or adopted inhigh plastic-generating countries such as Thailandand India is the pyrolysis of plastics. This processproduces fuel from waste plastic, a better alternativeto landfill and a partial replacement of depleting fossil fuels (Wong et al. 2015).

Caveats

It is important to recognise the biases associatedwith using stranding animals for data collection.Within and between stranding sites there are differ-ences in turtle foraging ecology, life stages andproximity to human habitation (Bolten 2003, Rees etal. 2010), and therefore they are exposed to differentlevels and types of potential entangling materials.Individual turtles therefore may not represent ahomogeneous group in terms of entanglement oc -currence within that population (Casale et al. 2016).Additionally, recovered carcasses represent an un -known fraction of at-sea mortalities, with physical

oceanography (e.g. currents) and biological factors(e.g. decomposition) affecting the probability andlocation of carcass strandings (Hart et al. 2006).However, examining reports of stranded animalsrepresents a vital opportunity for research and canprovide insights into the impacts of anthropogenicthreats which would otherwise go undetected(Chaloupka et al. 2008, Casale et al. 2010). In addi-tion, stranding information aids with the assessmentof harder-to-access life stages, yielding key infor-mation on the risk to specific resident populationsand contributing to building a worldwide perspec-tive for conservation issues (Chaloupka et al. 2008,Casale et al. 2016). Indeed, this was the aim of ourstudy: using stranding data from expert respondentsto gain an initial indication of the estimated magni-tude of this threat.

Surveying experts can be a powerful tool for ob -taining insights on particular topics not widelyknown by others (Martin et al. 2012). Expert knowl-edge and opinions may be the result of training,research, skills and personal experience (Burgman etal. 2011a). In this study, we sought the opinions ofconservation scientists and practitioners with experi-ence in marine turtle entanglement and strandings.Due to the purposive sampling nature of our ap -proach, we aimed to identify people with relevantexperiences instead of focusing on obtaining a ran-dom selection of representatives; this is a widelyused practice when undertaking social surveys thatfocus on particular subgroups or specialists (Newing2011). Nevertheless, expert knowledge and opinionsare also known to be subject to biases, includingoverconfidence, accessibility and motivation (see e.g.Burgman et al. 2011b and Martin et al. 2012). In theabsence of empirical data to validate our findings,this remains as simply suggestive but neverthelessrelevant information in terms of identifying a poten-tially important conservation issue and providing rel-ative indications of the scale of entanglement as athreat to sea turtles.

Future actions and recommendations

Ghost fishing

Issue and policy. Presently, a large knowledgegap exists regarding effects of ghost fishing. Whilethere has been some progress in documenting thefrequency of loss from passive gear such as gillnets, little is known about loss from active gears; effectivemethodology to estimate the persistence of types of

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gear such as trawl nets has yet to be developed(Gilman et al. 2013). While it would be optimal toswitch all gear to more biodegradable materials,synthetic materials will continue to be used withinfisheries for the foreseeable future. This is an issuethat has been highlighted in policy by the Food andAgriculture Organization (FAO), who recommendthe identification, quantification and reduction ofmortality caused by ghost fishing by implementingthis into fisheries management plans, increasing sci-entific information and developing mitigation strate-gies; but this appears still to be in its infancy(Gilman et al. 2013). This is also reflected in man-dates within the International Maritime Organisa-tion (IMO) and International Convention for Preven-tion of Pollution from Ships (MARPOL Annex V)(Stelfox et al. 2016).

Need for a global database and spatial hotspotidentification. Undoubtedly a common global meta-database recording the spatial distribution and abun-dance of possible entangling ghost gear as well asincidences of marine turtle entanglement incorporat-ing a unit of effort metric would assist in quantifyingthe mortality due to ghost gear that is needed to in -form policy (Nelms et al. 2016). A recent global re -view (dominated by the Atlantic and Pacific oceans)on marine megafauna by Stelfox et al. (2016) re -ported a total of 5400 individuals of 40 species thathad been associated with ghost gear between 1997and 2015. They suggested this was a great underesti-mate due to lack of capacity to record incidence.Such data could feed into one of the major researchpriorities emphasised by respondents; modellingspatio-temporal hotspots of entanglement. An inno-vative study by Wilcox et al. (2013) used beach cleandata and models of ocean drift to map the spatialdegree of threat posed by ghost nets for marine tur-tles in northern Australia and map areas of high risk.With the input of more specific marine location dataon ghost gear and the advocacy of the use of everimproving modelling, this could provide a powerfultool in the future.

Education and stakeholder engagement

Local initiative to reduce debris causing entangle-ment. On a more local and regional scale, many ini-tiatives are being brought into place to encourage areduction in the amount of ghost gear/plastic debrisentering the ocean and combat discarding at sea byworking closely with community education andengagement; another highlighted topic by our re -

spondents. There are numerous examples: the seaturtle conservation program in Bonaire has started a‘Fishing Line Project’ (www.bonaireturtles. org/ wpp/what-we-do/fishing-line-project) working with vol-unteers to train them on how to remove discardedline and nets from coral reefs, and the ZoologicalSociety of London’s ‘Net-works’ (www.net-works.com)initiative has established a supply chain for discardedfishing nets from artisanal fishing communities in thePhilippines to a carpet manufacturing company. Withfurther replication of such community-based projectsand stakeholder engagement, especially with arti-sanal fisheries awareness, the potential exists to starttargeting hotspots of marine vertebrate entangle-ment directly.

Stranding networks training. Another set of stake-holders which will be important to engage arestranding networks. Responses to entangled turtlescan often be slow, and respondents commented thatmany are not trained in the correct protocols tosafely remove entangling materials. If strandingnetworks were fully trained in a standardised proto-col for removal, the techniques could then bepassed on through educational training programmesto the fishing community, quickening the responseto such incidences. This is already beginning tohappen for bycatch cases; Sicilian fisherman nowactively volunteer to take part in the rescue of tur-tles in difficulty and are trained in contacting thecompetent authorities for the transfer of turtles tothe nearest recovery centres. This level of involve-ment by workers in the fishery sector was stressedand encouraged through both effective educationactivity and specific targeted study campaigns(Russo et al. 2014).

Future research avenues into marine turtle entanglement

Respondents raised the issue of post-release mor-tality and the importance of behavioural researchinto the interactions between marine turtles andpotential entangling materials present in the marineenvironment. The prominence of this has been em -phasised within other taxa; for example, post-release mortality can result from long-term chroniceffects of injuries in pinnipeds even after the entan-glement has been removed (McIntosh et al. 2015).Furthermore, it has been argued that some colonialseabirds released from entangling plastic would notsurvive without human intervention (Votier et al.2011).

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To validate the success of release protocols afterentanglement incidents (as mentioned above), tech-niques could be employed from other areas of mar-ine turtle research. Satellite telemetry has alreadybeen used in a multitude of ways to provide infor-mation on conservation issues facing marine turtles;a number of studies have used this technique toconsider post-release mortality after bycatch fish-eries interactions (reviewed in Jeffers & Godley2016). Deploying tagged turtles that have beeninvolved in entanglements could aid in the under-standing of survival after these events as well assimultaneously providing information on the loca-tion of sea turtles, feeding into information on en -tanglement hotspots to target mitigation actions.The benefits of utilising such techniques have beenillustrated in other endangered species facing en -tanglement, such as studying mortality of silky sharksCarcharhinus falciformis in the Indian Ocean; esti-mates derived from satellite tracking showed thatmortality due to entanglement was 5 to 10 timesthat of known bycatch mortality and provided evi-dence for a call advising immediate managementintervention (Filmalter et al. 2013).

Other research methods and ideas could be modi-fied from the study of plastic debris ingestion by seaturtles. Studies are currently underway to under-stand the selective mechanisms that lead to ingestionof plastic pieces (Schuyler et al. 2014, Nelms et al.2016). For instance, a study by Santos et al. (2016)used Thayer’s law of countershading to assess differ-ences in the conspicuousness of plastic debris to inferthe likelihood that visual foragers (sea turtles) woulddetect and possibly ingest the plastic fragments. Sim-ilar studies could be conducted to comprehend theunderlying behavioural and physiological mecha-nisms that influence turtles to approach potentialentangling materials when encountering them with -in the marine environment.

Similarly, comprehending how important the levelof biofouling on this synthetic debris is in contribut-ing to the likelihood of entanglement will be impor-tant. Total fish catches by monofilament gillnets inTurkey was lower, as a result of accumulating detri-tus and biofouling increasing the visibility of the netsin the water column (Ayaz et al. 2006). Furthermore,the level of biofouling could indicate the age of ghostgear entangling marine turtles. Retrieved lost/dis-carded fishing gears are usually found fouled bymacro-benthic organisms, so if a relationship be -tween soak time and biofouling level could be established, these organisms could provide a validmethodology to age the gear and enable better esti-

mates of ‘catches’ made by the respective net (Sal-danha et al. 2003).

Finally, it will be important to undertake demo-graphic studies, calculating rates of entanglement,especially for specific populations that are known tobe particularly vulnerable to a combination of otheranthropogenic threats. For species such as pinni -peds, which are less elusive (hauling out on land)than marine turtles, the literature describes differentmethods. For example, a proportion de rived from acount of entangled individuals from a sub-sample oran estimate of the total population (Raum-Suryan et al.2009, McIntosh et al. 2015), or more recently, the useof mixed-effects models to obtain a prediction of thetotal number of seals entangled per year, by examin-ing changes in entanglement rates over time and thepotential drivers of these detected trends (McIntoshet al. 2015). However, this can only be achieved ifreporting and recording such incidences in marineturtles improves in efficacy and standardisation.

CONCLUSIONS

Further research may show that the issue is moreone of animal welfare than of substantive conserva-tion concern to many marine turtle populations. It isclear, however, that entanglement with anthro-pogenic plastic materials such as discarded fishinggear and land-based sources is an under-reportedand under-researched threat to marine turtles. Col-laboration among stakeholder groups such as strand-ings networks, fisheries and the scientific communitywill aid in providing mitigating actions by targetingthe issue of ghost fishing, engaging in education andproducing urgently needed research to fill knowl-edge gaps.

Acknowledgements. The authors thank all respondents ofthe questionnaires for their invaluable knowledge andinsights regarding this issue. We are grateful to Karen Eck-ert of WIDECAST for granting access to turtle graphics.E.M.D. received generous support from Roger de Freitas,the Sea Life Trust and the University of Exeter. B.J.G. andA.C.B. received support from NERC and the Darwin Initia-tive, and B.J.G. and P.K.L. were funded by a University ofExeter — Plymouth Marine Laboratory collaboration awardwhich supported E.M.D. We acknowledge funding to T.S.G.from the EU Seventh Framework Programme under GrantAgreement 308370, and P.K.L. and T.S.G. received fundingfrom a NERC Discovery Grant (NE/L007010/1). This workwas ap proved by the University of Exeter, CLES ethics com-mittee (Ref. 2017/1572). The manuscript was greatlyimproved by the input of the editor and 2 anonymousreviewers.

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Editorial responsibility: Rory Wilson, Swansea, UK

Submitted: February 22, 2017; Accepted: September 22, 2017Proofs received from author(s): November 28, 2017