Oil spill impacts on mangroves: Recommendations for ... · ing death and sublethal impacts (Swan et...

Marine Pollution Bulletin 109 (2016) 700–715

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Marine Pollution Bulletin

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Oil spill impacts on mangroves: Recommendations for operationalplanning and action based on a global review

Norman C. Duke ⁎James Cook University, TropWATER Centre, Townsville, QLD, Australia

⁎ Corresponding author.E-mail address: [email protected].

Figure frontispiece. Shipping accidents cause most o

http://dx.doi.org/10.1016/j.marpolbul.2016.06.0820025-326X/© 2016 Elsevier Ltd. All rights reserved.

a b s t r a c t
a r t i c l e i n f o
Article history:Received 6 January 2016Received in revised form 20 June 2016Accepted 22 June 2016Available online 1 July 2016

Mangrove tidal wetland habitats are recognised as highly vulnerable to large and chronic oil spills. This review ofcurrent literature and public databases covers the last 6 decades, summarising global data on oil spill incidentsaffecting, or likely to have affected, mangrove habitat. Over this period, there have been at least 238 notable oilspills alongmangrove shorelinesworldwide. In total, at least 5.5million tonnes of oil has been released intoman-grove-lined, coastal waters, oiling possibly up to around 1.94 million ha of mangrove habitat, and killing at least126,000 ha of mangrove vegetation since 1958. However, there were assessment limitations with incompleteand unavailable data, as well as unequal coverage across world regions. To redress the gaps described here inreporting on oil spill impacts on mangroves and their recovery worldwide, a number of recommendations andsuggestions are made for refreshing and updating standard operational procedures for responders, managersand researchers alike.

© 2016 Elsevier Ltd. All rights reserved.

Keywords:MangrovesOil spillsImpactsPollutionMonitoringRisk managementStandard operational procedurerecommendations

il spills that threaten mangrove and tidal wetland habitats, as with the 2007 oil spill in Port Curtis, Queensland, Australia.

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701N.C. Duke / Marine Pollution Bulletin 109 (2016) 700–715

1. Introduction

Mangroves are highly vulnerable to oil spills because oil deposits onsensitive plant surfaces, affecting soils and dependant marine life caus-ing death and sublethal impacts (Swan et al., 1994, Duke et al., 1999,Duke and Burns, 2003; NOAA, 2014). This disruption affects ecosystemservices of mangroves, like fisheries production and shoreline protec-tion worldwide. Oil spill impacts also persist for decades, and they canoccur at any time, at any location. So, for as long as oil is extracted andtransported around the world, the risks are ever present. Therefore, itis essential to be prepared where possible with prior risk assessmentsand surveys of baseline shoreline condition, along with database re-cords of earlier impacts and instances of recovery. There is an urgentneed, for example, to quantify impact severity in a standard way,starting with relatively simple parameters like: area of tree death; esti-mated volume of oil reaching mangrove habitat; and, areas of potentiallethal and sublethal impacts. This article reviews current literature, andlists a number of key recommendations and guidelines for improvinglonger term management and monitoring of mangroves affected bylarge oil spills.

2. Diverse and vulnerable mangrove assemblages

Tidal wetlands consist of forested mangrove woodlands, thick man-grove and saltmarsh shrubbery, low dense samphire plains, andmicrolagal covered saltpans (Tomlinson, 1994; Duke, 2011). In the tro-pics, mangroves are often the dominant shoreline ecosystem comprisedchiefly offlowering trees and shrubs uniquely adapted to coastal and es-tuarine tidal conditions (also see Spalding et al., 2010). They form dis-tinctly dense structured habitat of verdant closed canopies fringingcoastalmargins and tidal waterways of equatorial, tropical and subtrop-ical regions of theworld. Normally, but not exclusively, these vegetationassemblages grow in soft sediments above mean sea level in the inter-tidal zone of sheltered coastal environments and estuarine margins.Mangroves are well-known for their morphological and physiologicaladaptations, copingwith salt, saturated anoxic soils and regular tidal in-undation; notably with specialised attributes like: exposed air-breath-ing roots above ground; extra, above-ground stem support structures;salt-excreting leaves; low water potentials and high intracellular saltconcentrations to maintain favorable water relations in saline environ-ments; and viviparous water-dispersed propagules. With such survivaltraits, these habitats have key roles in coastal productivity and connec-tivity, often supporting high biodiversity and biomass not possible inupland vegetation, especially in more arid regions.

Mangroves are recognised as an economic and biological resourcewith a number of highly beneficial ecosystem services (Mukherjee etal., 2014, Duke and Schmitt, 2015). These include fisheries (nursery,habitat and aquaculture), ecotourism and recreation, shoreline protec-tion, coastal water quality buffering (‘coastal kidneys’), coastal primaryproduction and pollution abatement ranking highly. It is of concern thatthese services have been seriously under-valued in recent decadesreflected in natural habitat replacement, alteration and general degra-dation associated with inadequate management of coastal areas (Dukeet al., 2007; Richards and Friess, 2016). Mangroves collectively face anumber of primary threats with habitat loss caused by direct and indi-rect human pressures coupled with global climate change. Along withreclamation and changes to hydrological flows, pollution damage is spe-cifically identified as amajor threat tomangrove ecosystemsworldwide(Hensel et al., 2010). Such pressures have all contributed to an overalldeterioration of the adaptive resilience of mangrove plants, adverselylimiting their ability to respond and adapt to current human and naturalpressures (cs. Lovelock et al., 2015).

Mangroves and tidal wetlands are ancient ecosystems, havingevolved over at least 60 million years. During this time, the earth, sealevel and climate have changed dramatically. Mangroves today, com-prised of plants and animals, are the survivors of changes through the

millennia. As such, these ecosystems have well-developed strategiesfor survival in their capacity for dealing with change. Today, as tidalwetlands ecosystems respond to change, they rely on their inherentadaptive capacities (eg., Duke et al., 1998a). Where sea levels hadrisen and fallen in the past, current occurrences of intact mangrovestands, are tangible evidence of their resilience and abilities for success-ful restoration, migration and re-establishment. However such abilitiesare finite, and they cannot be taken for granted. In this context, it is co-gent that mangrove communities around the world are currently in de-cline both in area and function. The causes appear related in large part tothe combination of on-going ‘natural’ influences, coupled with an ever-growingmenace of direct and indirect human pressures (Duke, 2014a).

Despite such pressures and limitations, there exists a highly diverseand thriving number of plant types within mangrove stands (Duke,2014b, Duke and Schmitt, 2015). And, awell-recognised benefit ofman-grove habitats are their habitat role between shoreline andmarine envi-ronments where their biodiversity and structure uniquely provideshelter, protection from erosion, as well as food for a number of terres-trial andmarine species, like juvenile fishes (e.g. Meynecke et al., 2008).The forested stands are known also for their traditional forest products,including timber for construction and local energy demands (e.g.Walters, 2005). Despite these uses, and others, unique wetland forestsare known only in a few instances for being managed in a sustainableway. Around the world, these habitats are considered wild and uncon-trolled compared to upland plants used in urban, city, industrial park-lands and forestry plantations. Never the less, unmanaged mangrovesoccur alongmany heavily populated shorelines where they provide sig-nificant, but often unrecognized services, like shoreline protection, nu-trient plus carbon sinks, fisheries benefits, as well as providing distinctaesthetic improvements to otherwise drab mud banks, flotsum rubbishand constructed walls.

In summary, mangrove habitats are seriously influenced by a num-ber of often deterministic ‘natural’ factors including: tidal inundation;sea water and broad salinity fluctuations; exposure at times to severewinds, waves and currents; variations over longer periods to overallsea level changes; and, growth in unconsolidated sediments with fre-quent instances of severe erosion and burial deposition. In recent centu-ries, there are added significant pressures of severe physical damage byhuman trampling, replacement with expanding human development,and pollution (Duke, 2014a). All these have notable and profound influ-ences on the distribution, functioning andwell-being of mangrove hab-itat. Few other natural ecosystems are subject to such an array of severeabiotic influences, as listed above, including oil pollution.

3. The influence of oil spills on mangroves

Mangrove communities are particularly susceptible to damage fromlarge oil spills (also see: Proffitt, 1997; Hensel et al., 2010, Lewis et al.,2011, Santos et al., 2011).When oil is released into coastal and estuarinewaters and washed ashore, it deposits on sensitive surfaces exposedduring the regular daily ebb and flow of tidal waters. This includes thesediments that thinly cover the highly sensitive fine feeding roots ofmangrove trees. Once deposited, oil mostly adheres and rarely moves,having adsorbed to oleophilic surfaces of plants and animals alike.Only in incidences where oil volumes are very large does it refloat andcontinue to spread in a significant way with subsequent tidal flushing.In each case, oil coats breathing surfaces ofmangrove roots, stems, seed-lings, and surrounding sediments, as well as fauna present in burrowsand root hollows.When smotheredwith oil, shorter plants and animals,die mostly within days. By contrast, taller mature trees and shrubbery,oiled only on their exposed roots and sediments, might persist for sixor more months before dying. Plants are accordingly smothered,poisoned and starved by oil spills; and the lighter the oils are, themost damaging they are (Duke and Burns, 1999, 2003; Michel andRutherford, 2014).

702 N.C. Duke / Marine Pollution Bulletin 109 (2016) 700–715

These differences between lethal responses and their quantificationare very informative, but there are also sublethal responses to consider.The sublethal responses are rarely ever quantified (cs. Duke et al., 1997)but they are often very important since they help us better understandand define overall impacts and possible recovery trajectories. So, whileoil type and concentration levels have a primary influence on the im-pacts observed, it is the responses of mangrove biota to all influentialfactors that better define their recovery potential, and the longer termfate of oil-impacted habitat. For these reasons, and that deposited oiloften becomes less visible after a few days and weeks, it is strongly rec-ommended that deposited oil be surveyed and mapped accurately atthe time when the spill is taking place, or very soon afterwards.

There are also further influential variables affecting habitatresponses, like differences in the sensitivity of individualmangrove spe-cies to oil and dispersed oil (Duke et al., 1998b; Duke and Burns, 2003;Lewis et al., 2011). In Australian studies, mangrove species were testedin planthouse trials where species showed a range of sensitivities fromhighest in Aegiceras corniculatum and Avicennia marina, to lesser levels

Fig. 1. Schematic diagram depicting the effecAdapted from Duke et al. (1999) and NOAA (

in Rhizophora stylosa and Ceriops tagal. The more sensitive specieswere thosewith greater salt excretion strategies as their likely co-relatedphysiological character. Duke and Burns (1999) further concluded thatsediment type was also important where those plants in more poroussediments were more vulnerable than those growing in fine clay mud.In addition, oil types were ranked by increasing impact on plants, fromleast sensitive: Bunker C fuel oil; Arabian light crude; Gippsland lightcrude; Thevenard crude; to Woodside condensate, the most harmful. Ingeneral, impact level rankings corresponded to oil density, where lightoils were more harmful than dense heavy oils. Oil toxicity trials werenotably made during field trials and post-spill studies, and not duringspill incidents (Swan et al., 1994).

In field situations, oil-impacted mangrove ecosystems follow a rea-sonably ordered set of condition states with primary, secondary and re-sidual effects, leading to recovery and/or loss. The schematic modelpresented in Fig. 1, shows key trajectories followed by oil-affectedman-grove plants, including: undisturbed (left side, green) to either recovery(orange); and permanent loss from deterioration (lower right, pink).

ts of large oil spills on mangrove habitat.2014).


Note, the short term effects where some trees die while others surviveoiling.

The longer termeffects occur over decadeswith habitat either recov-ering via successful recruitment, or lost permanently in a cycle of pro-gressive degradation and deterioration. Because of the propensity ofoil to clump, especially in cooler conditions, the areas oiled are oftenpatchy. The result can be a combination of both oiled and unoiledpatches occurring in close proximity. Accordingly, responses can be var-iable and complicated. Some recovery of unoiled undisturbed patchescan be quite rapid (less than one year) with virtually undetected long-term effects. The fate of oiled patches however may follow one of twooverall possible trajectories – one to recovery, and the other to deterio-ration and loss. These latter trajectories of recovery or loss further de-pend on the severity of oiling, and the severity of any subsequentdamaging events.

Where oiling results in sublethal damage only, then recovery can berapid (1–5 years) since affected trees only need to recover their canopyfoliage, and regain their associated fauna. But, where trees die, the re-covery process will take much longer (5–25 years or more), involvingseedling recruitment, establishment, and the growth of replacementplants to maturity with propagation. Such recovery processes are diffi-cult to achieve in this physically dynamic and demanding environment.Bymost accounts, tree growth tomaturity can take at least 25–30 years.Assessment protocols set out in the recommended operational guide-lines below have been developed for assessments of both the extentand severity of impacts, and the status of recovery/degradationprocesses.

The aimhas been to characterize and quantify the key characteristicsof any incident under consideration, with severity measures of impactand condition status in rehabilitation, for any time during or after anoil spill. For example, Da Silva et al. (1997) identified an apparent out-come of continuing habitat deterioration where there was no progresstowards recovery, while mangrove recruitment after oiling became ex-tremely vulnerable to subsequent episodic events like hurricanes andother human-caused disturbances. By contrast, other authors (Lewis,1982; Lamparelli et al., 1997; Kadafa, 2012a) when describing impacttrajectories have taken a positive view, where comparable stages andtimelines progress along a trajectory to full recovery of habitat. Unfortu-nately, this is not always the case, and there appears to be a growingnumber of impacted sites showing little or no recovery.

Fig. 2.Mangrove habitat zones (green shading) and shipping risk routes (blue tracks;Wikimedoccur. This is representative of the 238 or so, reported oil spill incidents recordedbetween1958 amangroves occur almost exclusively along intertidal shoreline margins, so their extent is restriAdapted from Duke (2011).

4. Past incidences of larger oil spills affecting mangroves

Oil pollution incidents, as accidental or deliberate spillages, are thechief way oil reaches mangrove habitat, especially those in high riskcoastal areas like ports, refineries and busy transport corridors. Since1958, there have been at least 238 notable incidents of larger oil spillsreported as affecting or threatening mangrove habitats worldwide(see Fig. 2; Table 1; Supplementary Data). Data on these spills havebeen sourced from a number of incident reports, but particularly fromfive exemplary online databases listing selections of marine spill inci-dents (AMSA, CEDRE, NOAA, ITOPF and the Nigerian Oil Spill Monitor,2016). Unfortunately, none of these sources list all spills affecting man-grove habitat. And, asmentioned in the recommendations, their contentand access might also be usefully improved upon because many inci-dents were in the vicinity of mangrove habitat but these were mostlyleft unreported. Regardless, data gathered from these sources hasgreat value in this compilation, as compared and listed in the Supple-mentary Data Tables 1 to 3. This first comprehensive review draws onpublished research survey results, technical publications as well asthese online databases.

The distribution of reported incident locations (Fig. 2) generallymatch the global distribution of mangrove habitat (green shadedareas; see Duke, 2011) – demonstrating that oil spills occur very widelyaffecting mangroves where ever this habitat occurs. Four types of oilspills are represented including: pipeline ruptures; vessel incidents;shore tank facility disruptions; and, well head damage. Sites of majorexperimental field trials include those in Port Curtis, Australia in1995–1998 (also see Fig. 5). Some open water incidents within themangrove area have not been included since they occurred appreciablyoffshore andwere considered unlikely to have impactedmangrove hab-itats since they are restricted to intertidal shorelines. In each case, thechoice to include each incident wasmade based on local circumstances,including distance offshore, when no observations were made aboutimpacts on specific shoreline mangrove habitats.

Understandably, there was a notable concentration of incidents inareas of both high vessel traffic and extraction sources, like the ArabianSea, the Gulf of Mexico, South eastern Brazil, and the Niger Delta. How-ever, the wider distributions dominate, and oil-affected mangrovescould be found in all 6 global sub-regions. This occurrence is explainedby the bulk of spill incidents having occurred during the transport of

ia Commons, 2016), describemajor spill incidents (black astericks) only wheremangrovesnd 2016 (see Table 1, SupplementaryData Table 3; compiled frommultiple sources). Note:cted to enclosed margins of islands and continents within green shaded areas.


oil, with shipping accidents accounting for at least 54%. The othercauses, like leakages from pipelines, shore tanks and well heads,accounted for the rest.

The region of least incidents was the West American sub region inthe Atlantic East Pacific. And, the area with the greatest concentrationof reported incidents was the East American region.While the reportingfrom the latter region (cs. mostly NOAA, 2016) was especially inclusiveand detailed, this greater level of reporting provides a challenge to otherregions. Perhaps the region of most deficient information was WestAfrica where public reporting of oil spills was far less rigorous (Odeyemiand Ogunseitan, 1985; Kadafa, 2012a) despite a seemingly first ratereporting service with the Nigerian Oil spill Monitor (2016). This meantthat it was harder to get a balanced and uniform global comparison, andthere are important observations stemming from this review. Firstly, itwas cogent that reported spill numbersworldwidewould be significantlygreater should the same amount of reporting have beenmadeworldwideas those covered by NOAA and the other databases. And, having said that,an international database that collated reports equally from all over theworld is a tangible goal. But this needs a greater commitment withencouragement for global organizations to collaborate, either supportingand contributing to a single database, or using shared regional databasesthat apply and link comparable reporting standards and maintain public,open accessibility.

While it may also be partly an artifact of progressively improvedreporting, it is more likely that the overall number of incidents had in-creased much as shown, from 7 in the 1960s, to 59 in the 2000s. This

Table 1A summary table of reported oil spill incidents having actual and likely impacts on mangrovemeasures of under-estimated impacts (representing b17% of incidents were observations wesources are listed in the Supplementary Data Table 3.

1958–1969 1970–1979 1980–198

Larger incident locations (number)World total 7 28 39East Africa 2 5 4Indo-Malesia 0 1 0Australasia 0 3 8IWP global region 2 9 12West America 0 1 1East America 5 16 22West Africa 0 2 4AEP global region 5 19 27

Total oil spill threatSpillage (tonnes) 83,832 1,685,234 852,043Mean (tonnes/spill) 11,976 60,187 21,847

Spill incident type (number)Pipeline 0 2 6Vessel 6 18 20Shore Tank 1 4 9Well Head 0 4 4Other 0 0 0

Mangrove oiled* (ha)World total 49 172 11,910Sites Measured * 1 9 9Sites Observed, not measured 2 6 4Likely, unconfirmed 4 13 26% sites oiled 42.9 53.6 33.3Studied incidents 1 8 8Field trials 0 0 3

Mangrove oil-dead, reported* (ha)World total 49 37 6528East Africa 0 0 0Indo-Malesia 0 20 0Australasia 0 5 2IWP global region 0 25 2West America 0 0 0East America 49 12 88West Africa 0 0 6438AEP Global Region 49 12 6525% dead of oiled 33.3 60.0 76.9

coincides with a growing global demand for oil. Over this period, thenumber of incidents steadily increased in 4 of the 6 global sub regionswith apparent decreases in East Africa and Australasia, (Table 1; Fig.3). The types of spill events were mostly vessel-related with collisions,fires, holing and sinkings. Pipeline ruptures and damage to shore tankfacilities make up about 34% of incidents while accidents on offshorewell heads account for the remaining 9%. A lack of reporting and assess-ment of the impact and death ofmangrove vegetation greatly under-es-timates the likely full extent of impacts on this habitat.

A number of reports have documented the death and/or damage ofmangrove vegetation associated with released oil (NOAA, 2014). Mostreport overall oil volumes released into the environment. In total, overthe last 6 decades, N5.5 million tones of oil were spilled into coastal wa-ters where mangroves occur. This equates to around 23,216 tonnes perspill. Volumes of oil released appearmaintained at a high rate with littlechange overall over half a century (see Fig. 4), as reflected especially insubregions: East America, West Africa, Indo Malesia and Australasia.Slight decreaseswere observed in the 2 other subregions ofWest Amer-ica and East Africa.

The latter region of East Africa was affected by a number of war inci-dents that damaged refineries and storage tanks, as those in Iran andKuwait affecting the Arabian Sea in the 1990s. These are some of thelargest releases of oil inmodern times, with the damage in Kuwait caus-ing the loss of around 1.5 m tonnes of crude oil during 1991 – (Böer,1993; El-Nemr, 2006; CEDRE, 2016; Webecoist, 2016; NOAA, 2016).Mangroves were affected, but the areas of oiling or tree death were

habitats worldwide over the last 6 decades from the 1958 to 2016. Asterisks (*) mark there available). See Fig. 2, for global regions represented. Individual incidents and multiple

9 1990–1999 2000–2009 2010–2016 Total

56 59 49 2383 1 2 172 5 8 16

14 7 5 3719 13 15 700 2 0 4

31 39 28 1416 5 6 23

37 46 34 168

1,735,425 393,205 775,773 5,525,51230,990 6664 15,832 23,216

11 14 16 4932 31 21 1288 6 5 332 5 6 213 3 1 7

12,328 2962 665 28,08611 7 6 4312 6 6 3633 46 37 15941.1 22.0 22.4 35.97 4 1 291 0 0 4

12,215 216 32 19,0770 0 0 00 1 0 218 15 0 308 16 0 520 0 0 0

13 0 0 16112,195 200 32 18,66512,208 200 32 19,026

39.1 46.2 9.1 44.1

Fig. 3. Numbers of larger oil spill incidents affecting and likely to have affected mangrovehabitats worldwide for 6 global sub-regions during the last 6 decades (Table 1;Supplementary Data).


unreported. Other large spills occurred in East America due to seriousaccidents on two offshore well heads in the Gulf of Mexico, with theIxtoc 1 well releasing around 1 m tonnes in 1979 (Hooke (1997);CEDRE, 2016; NOAA, 2016; ITOPF, 2016; Webecoist, 2016), and theDeepwater Horizon well head releasing around 760,000 tonnes in2010 (Khanna et al., 2013; CEDRE, 2016; Webecoist, 2016; NOAA,2016; Nixon et al., 2016). Each of these very large spills oiled mangrovehabitat, but no reports describe the areas oiled or whether mangrovevegetation died after oiling. This lack of assessment and reportingfrom these very large spills makes it difficult to further evaluate the se-verity of such spills on mangrove habitat.

As noted, reporting was generally lacking for the region of West Af-rican shorelines of Angola, and particularly Nigeria where there werevery high concentrations of oil extraction infrastructure – as numerouswell heads and inter-connected piping (Odeyemi and Ogunseitan,1985; Kadafa, 2012a, 2012b; Nigerian Oil Spill Monitor, 2016; see Sup-plementary Data). While few prior reviews of world oil spill damageto mangroves refer to these instances, a number of documents werefound describing the relatively large number of incidents reported inthis review. Mangroves have been affected by numerous oiling inci-dents throughout the Niger Delta since at least 1979, until the presentday (Odeyemi and Ogunseitan, 1985; Seenreport, 2008; Twumasi andMerem, 2006; Adeyemo et al., 2009; Kadafa, 2012a; FAO, 2010;Eoearth, 2010; The Guardian, 2010, 2011; UNEP, 2011; Shell, 2015;BBC, 2015; Oil Spill Intelligence Report, 2016). The amounts of oil re-leased, although not always clearly quantified, were unusually largecompared to elsewhere in the world. For instance, where this global re-view lists 238 incidents of oil spills since 1958 affecting mangrovesworldwide, in the Niger Delta there appears to have been that numberof incidents each year over the same time period (Odeyemi andOgunseitan, 1985; Kadafa, 2012a).

Fig. 4. Released oil spill volumes (tonnes) of larger oil spill incidents affecting and likely to have(Table 1; Supplementary Data).

A brief outline for each decade confirms the on-going situation inNigeria (see Nigerian Oil Spill Monitor, 2016, for overall information).In the 1970s, mangroves were reportedly oiled in 783 incidents(Odeyemi and Ogunseitan, 1985; Tolulope, 2004; Ukoli, 2005;Twumasi and Merem, 2006; Kadafa, 2012a). In the 1980s, 11,210 ha ofmangroves were reportedly oiled in 2015 incidents (Ekekwe, 1983;Snowden and Ekweozor, 1987; Thorhaug, 1992; Tolulope, 2004; Ukoli,2005; Nwilo and Badejo, 2005; Twumasi and Merem, 2006; Aghalinaand Eyinla, 2009; Adeyemo et al., 2009; Kadafa, 2012a; NOAA, 2016).In the 1990s around 12,195 ha were reportedly oiled in 4024 incidents(Adeyemo et al., 2009; Twumasi and Merem, 2006; Kadafa, 2012a;Eoearth, 2010; Human Rights Watch, 2016). In the 2000s mangroveswere reportedly oiled in 117 incidents (Adeyemo et al., 2009; FAO,2010; Eoearth, 2010; The Guardian, 2010, 2011; Kadafa, 2012a; Shell,2015; BBC, 2015). From 2010 to 2016, mangroves were reportedlyoiled in 5 larger incidents (Huffington Post, 2010; UNEP, 2011;Sciencythoughts, 2013; Wikipedia, 2014; The Guardian, 2015; Oil SpillIntelligence Report, 2016).

All together, these oil releases in the Niger Delta reportedly amountto around 100,000 t each decade with likely severe damage caused tolocal mangroves as well as to the human communities that depend onthem (Kadafa, 2012a). This amount of oil released equates to around27% of that threatening mangroves worldwide. To this date, only theBodoWest study of spills from pipeline sabotage (UNEP, 2011) has ad-equately verified and described clear impacts on mangroves. But, moreis needed to document the apparently severe and chronic incidentsacross the Niger Delta.

For allworld regions (Fig. 2), the total amounts of oil released in eachof the 6 sub regions are shown in Fig. 4 for each decade since 1958. Notethat the amounts of oil released inWest Africa were maintained, as de-scribed above. As they stand, these levels matched those in the EastAmerican with lesser amounts in Indo Malesia. There were small de-clines in the Australiasian, East African and West American regions.

These differ from the trends with increasing number of incidents re-gionally and globally over the last 60 years (Fig. 3). Total oil volumes re-leased and likely to impact on mangrove habitat, range from 393,205 to1,735,425 tonnes per decade.While thesemeasures are generally usefulfor overall quantification of incident severity, they have been less usefulin quantifying the incident impacts on mangrove habitat. More directmeasures are needed, like the areas of mangrove oiled, and the areasof mangrove tree death.

5. Oiledmangrove habitat – ameasureof lethal and sublethal impact

Of the total amounts of oil released, only a portion is likely to impacton mangrove habitat. Much of the free oil may distribute elsewhere be-fore reaching vulnerable mangrove shorelines. Released floating oil canevaporate and degrade, be diverted using booms, or even recoveredusing skimmers whilst at sea. A more direct measure of likely impacts

affected mangrove habitats worldwide for 6 global sub-regions during the last 6 decades


on mangrove habitat is the amount of oil reaching mangroves, and thearea of mangrove oiled. This measure best defines and describes thesubsequent responses of mangrove vegetation to both lethal and suble-thal damage.

For the incidents reported, only 43 out of 238 (18.1%) were quanti-fied for the amounts of mangrove habitat actually oiled (Table 1). Thistotal area of oil-affected mangrove was around 28,000 ha. But, becausethis figurewas derived from only a subset of incidents, the total amountoiled is expected to have been around 5 times greater – up to around155,000 ha.

To help quantify the measures of impact shown in the broadlysourced data used in this review, it was convenient to categorise threelevels of mangrove oiling where: ‘Site Measured’ quantified those inci-dents where oiled areasweremeasured (noted above); ‘Sites Observed,not measured’ – were the sites with mangroves observed as oiled, butnot measured; and, ‘Likely, unconfirmed’ – were those sites likely tobe oiled since mangroves are known in that locality, but not reportedas oiled. The three categories of oiled mangrove incident reports weretabulated across all 6 decades in Table 1.

The percentage ‘Likely, unconfirmed’ was overall around 67%. An-other 14% of incidents had the briefest of comments about mangrovesbeing oiled. So, without other accompanying details, the presence ofoiled mangroves was deduced sometimes from photographs andmaps in the incident reports. This meant that b20% of reports made de-finitive mention of the presence of mangroves in the vicinity, despitethe habitat being unilaterally recognised as highly vulnerable.

A review of available reports shows the ten largest areas of man-grove habitat damage (see Supplementary Data Table 2; noting sourcereferences there in). These rank the reported single incident impactsof oiled mangrove area for the countries represented with the largestspills first:

• Nigeria with the Funiwa 5 Well blowout in 1980 oiling 5107 ha;• Pakistanwith the Tasman Spirit sinking in 2003 oiling around 1000 ha;• Nigeria with the Pipeline rupture Bodo in 2008 oiling at least 1000 ha;• The Philippines with the Solar 1 sinking in 2006 oiling 650 ha;• Panama with the Texaco Refinery spill in 1986 oiling 377 ha;• Nigeria Pipeline sabotage, Bodo West in 2011 oiling 366 ha;• Brazil pipeline rupture near Sao Paulo in 1983 oiling around 300 ha;• Micronesian islands of Yap with the sinking of the Kyowa Violet in2002 oiling 300 ha; Indiawith sinking of theMSC Chitra in 2010 oilingaround 200 ha; and

• Australia with the holing of the Era in 1992 oiling 100 ha.

6. Dead mangroves – the lethal response of mangrove habitat tooiling

A specific and relatively easily deduced measure of impact on man-grove habitat is the area of dead mangrove vegetation post oiling (see,Duke and Burns, 2003). These data were available only from a relativelysmall number of reported incidents, just 36 incidents, or 15.1%of all 238.The total area of mangroves reportedly killed by oil spills was around19,077 ha for the subset of sites, extrapolated to around 126,338 hafor all incidents since 1958. There were a number of instances where aclear record was made of no mangroves having died. These consideredobservations of no lethal impact have been as important to this review,as those reports with measured areas of dead mangroves. Unlike othermeasures, the losses and damage to mangrove vegetation are both di-rectly related to the overall vulnerability of this environmental receptor.This severity measure is easily recognised, mapped and measured fromhistorical and current aerial/satellite imagery. In addition, change detec-tion assessments with appropriate field validation have been useful inquantifying losses and gains in other studies of vegetation cover, postimpact and post recovery (e.g., Duke et al., 1997).

The largest areas of mangrove habitat damage reported (see Supple-mentary Data Table 2; noting source references there in) were in theNiger Delta with: around 340 ha killed by the Funiwa 5 well head spillin 1980; 200 ha killed by theBodo pipeline rupture in 2008; and another32 ha killed by the Bodo West pipeline sabotage in 2011. Elsewhere inthe World, the largest areas of oil-dead mangroves range generallylower, with: 69 ha killed in Panama by the Texaco Refinery spill in1986; 49 ha killed in Panama by the Witwater sinking spill in 1968;20 ha killed in Indonesia with the sinking of the Showa Maru in 1975;12 ha killed in Puerto Rico with the Jet Fuel tank spill in 1999; 10.5 hakilled in Brazil by a Jet Fuel tank spill in 1999; 10 ha killed in Yap, Micro-nesia with the sinking of the Kyowa Violet in 2002; and another 6 hakilled in Puerto Rico by an earlier Jet Fuel tank spill in 1986.

These data of amounts (area) of mangrove death are perhaps themost cogent, simple measures of impact severity, as themeasures of le-thal habitat damage. They provide the means to quantify and comparerelative impacts from which we might later derive realistic estimatesof habitat recovery. Despite the great value of these data, and theirease of measurement, there have been relatively few reports recordingthese usefulmeasures. The inclusion of such keymeasured observationsin future reporting is one of the chief recommendations arising fromthis review.

7. Relationship betweenoiling and the amount ofmangrove damage

This review has drawn on a wide selection of marine oil spill inci-dents to gain amuch greater understanding of the variables and circum-stances influencing oil-impacted mangrove habitat, and its possiblerecovery. Further insights have been derived also from observationsand findings of experimental field trials (Supplementary Data Table3). The overall aim has been to document key lessons learnt, and to de-velop and support the revised list of recommendations, guidelines andstrategies for better informing and preparing responders, communityandmanagers faced with actual and potentially oil-damaged mangrovehabitat. Overall findings include the identification of knowledge gaps,and other useful deductions considered to be lessons learnt. One ofthese found that impact severity can be equated to the amount of lethaldamage. A further finding was an informative, emerging relationshipbetween the area of mangrove oiled (sublethal and lethal impacted)and the area of lethal impact.

These relationships have been derived from 7 well-studied spillsites, including (see Supplementary Data Table 3 for source references):

• the Texaco Refinery, Atlantic coast, Panama in 1986;• Zoe Colocotronis, Cabo Rojo, Puerto Rico in 1973;• World Encouragement, Botany Bay, New South Wales, Australia in1979;

• the Sao Paulo pipeline, Brazil in 1983;• Era, Spencer Gulf, South Australia in 1992;• Solar I, Iliolo, The Philippines in 2006; and,• the Bodo West pipeline sabotage, Niger Delta, Nigeria in 2011.

Thesemore detailed findings show that for a total of around 1900 haof mangroves oiled, there were around 123 ha of mangrove death, oraround 6.5%. So, for any given area of mangrove death, there might bea 15 times greater area of sublethal affected mangrove habitat. Thismeasure of sublethal damage (as decreased canopy densities) was fur-ther observed in Panama with assessments of the Texaco Refinery spill(Duke et al., 1997). In that incident, although there were no specificmeasurements of the area of oiled mangrove, the proportion of man-grove lethal damage was measured around 18% of the observed suble-thal damage. In this case, the area of sublethal damage measured fromlow density canopies was at least 5–6 times greater than the area ofdead mangroves. If the previous ratio of 6.5% were applied it meansthat N1000 ha were oiled, and the canopy damage observed


(~377 ha) was the area of more severe sublethal damage. In the sameway, the previous measure of oiled mangroves above is likely also tobe much greater based on the area of dead mangroves measured. Sothe total amount of oiled mangrove in all incident sites around theworld is more likely to have been around 1900,000 ha since 1958.

Replicated field trials (Fig. 5) were conducted in central Queenslandto further test dispersant use and bioremediation treatments (Duke etal., 2000). Oils were weathered and applied at a pre-determined rateof 5 l·m−2, based on field observations from hydrocarbon samplingfrom actual oil spill sediments in Panama (Duke et al., 1997). The im-pacts of Gippsland light crude and Bunker C fuel oil on mature standsof Rhizophora stylosa were assessed over at least 18 months post oilingin each case. With the application of light crude oil, around half of thetrees in each plot died within 6–12 months, compared to control plots.By contrast, there were no significant differences with the applicationof the heavier fuel oil between plots.

These findings suggest that tree death occurred only after exceedinga defined threshold concentration of oil present in sediments. And, thatthere was a relational link between the area of dead and dying man-grove trees and the oil type and volume (concentration) required tokill mature vegetation. Although precise dosage levels can be refined,this current estimate provides a tangible measure by which to extrapo-late first order estimates of released oil volume based on observed areasof tree death – or vice versa. This has already been usefully applied in fo-rensic post-incident investigations and legal considerations with a casein Nigeria (BBC, 2015; Shell, 2015; The Guardian, 2015; The MaritimeExecutive, 2015).

Of further critical importance, therewas also a notable order ofmag-nitude difference between recovery periods of lethal impacted(deforested) habitat (Fig. 1) taking multiple decades for re-establish-ment (with seedling establishment, growth and development, plus re-establishment of animals), compared with months and years for recov-ery of sublethal impacted habitat (as mostly for re-establishment of an-imals). This section outlines such vulnerabilities of mangrove habitat inrelation to large oil spills, taking into account important geophysical andtemporal variables. These are important for predicting the likely impactof spills on mangroves in any given circumstance.

The loss of keystone individual plants of mangrove communities islikely to have substantial consequences for tidal wetland habitats. Mi-croclimate is altered with the absence of canopy, resulting in increasedtemperatures and lower humidity. Physical habitat is lost for plants andanimals that attach to mangrove stems and roots. Sediment can also belostwhenmangrove roots decay and become detached over large areas.Any loss of sediment, especially at the seaward edge of a mangrove, willrepresent a significant impediment to the re-establishment of the hab-itat (Duke, 2001).

Fig. 5. Field trials tested the resilience mature mangrove stands to oil and dispersantduring 1995–1998 in Port Curtis, near Gladstone (Fig. 2).

These observations describe two distinct levels of impact, with onebeing easily quantifiable and available. These are considered essentialto both quantify such variables with each incident, and to learn moreabout how mangroves respond to the presence of petroleum on theirroots, and coating surrounding sediment surfaces. While oil on exposedfoliage is known to be lethal, the impacts on taller trees with oilingaround their trunks were more cryptic and previously uncertain. Theobserved dosage to sediments surrounding mature trees (noted abovefor the central Queenslandfield trials)was checked and found compara-ble to concentrations in sediments measured during accidental largespill events where trees died (Duke and Burns, 2003). Lower trial dos-age levels of 0.1 to 0.5 l per m2 resulted in smaller patchy impacts onvegetation and fauna, with no tree death (Duke et al., 2000).

8. Retention of oil in mangrove sediments

Oil can at times be retained within sediments of the intertidal zonefor decades following an oil spill. And, there may not always be harmfuleffects on plants, their growth or reproduction. Sediments deposited inintertidal habitats, especially mangroves, are often fine-grained, water-logged and rich in organicmatter. Thesemostly oleophilic properties fa-vour retention of oil and other contaminants via physical and chemicalprocesses (Lewis et al., 2011, Santos et al., 2011).

The abundance of burrows made by crabs and other fauna has beenshown to enhance the retention of oil at depth within intertidal sedi-ment (Duke et al., 2000; Culbertson et al., 2007, Hensel et al., 2010).Mudflats are less likely to accumulate oil relative to mangrove plantsgiven the lack of vegetation and debris to trap material, and their loca-tion lower in the intertidal zone where tidal flushing is regular. Also,as noted previously, oil in mangrove sediments degrades more rapidlyin places where there is greater tidal range and exposure (Burns et al.,1993, Burns et al., 2000).

Chronic impacts on mangroves have been observed across long pe-riods (up to decades) following oil spills, with the symptomsmost com-monly observed being: death of trees with seedling regeneration;defoliation and canopy thinning; leaf yellowing; reduced height growthof surviving trees and poor seedling establishment (Duke et al., 1997,Hensel et al., 2010, Lewis et al., 2011); plus, likely toxic response defor-mities and morphological changes such as pneumatophore branching(Duke et al., 2005), reduced lenticel numbers (Böer, 1993), and geneticmutations like variegated leaves and chlorophyll-deficient propagules(Duke and Watkinson, 2002).

Distinguishing both acute and chronic effects, aswell as the differentresponses from toxic or smothering impacts, are all important forpredicting the ecological consequences of any spill and for modelingsubsequent impact and recovery. Because of the often complex circum-stances surrounding any spill incident where the dynamic betweenlong-lived trees and short lived fauna are responding to an altered, com-plex and heterogeneous environment, it is understandably challenging.Additional controlled and replicated studies undertaken in realistic fieldsettings (seeDuke et al., 2000) are needed to address the important datagaps identified above. For instance, it is important to derive realisticdose-response data, and to follow longer term processes associatedwith the accumulation and breakdown of oil in sediment.

There are complex inter-relationships also amongst plants and ani-mals. And, it is clear that each depends on the other in significantways. So, a decline in the condition of either plants or animals will affectthewell-being of the other biota types (Cannicci et al., 2008). One readyexample is the influence of crabs as ecosystem engineers, with theirburrowing and soil bioturbation affecting sediment aeration, nutrientturnover, water exchange and leaching of salt within sediments. Crabsalso have a major influence on mangrove forest structure with their se-lective predation of propagules. Other examples include the beneficialrole of sessile sponges onmangrove roots preventing borer attack, stim-ulating rootlet growth, and enhancing nutrient uptake; and heat-


restricted weevil borers that severely limit propagule establishmentthat might also influence mature forest structure (Duke, 2001).

9. Recovery potential of oil-damaged habitat

Post spill assessments suggest that structural recovery of oil-dam-aged mangrove forests takes place over a period of at least 3 decades.For instance, an estimated time of recovery of 30–36 yearswas deducedfrom 16 oil spills affecting variousmangrove locations (Duke and Burns,1999). Based on the ranked recovery state phases described in Table 2,the previous incident data were re-assessed as part of this treatment.The recovery period relationship is re-affirmed, as displayed in Fig. 6.It must be emphasized however that this recovery only refers to forest

Table 2Mangrove forest recovery goes through6 phases and one negative state, based on structural regrIndicators of gap condition status have been adapted from Duke (2001). Faunal status, while unforest recovery vary due to the different trajectories of sublethal and lethal impacts.

Recovery phase ofgap

Recoverystatus %percent

Sub lethaltrajectory

Natural pre-damagestate

Referencecondition

Foliage dense with yellowing leaf numbers b10%.Seedling bank under closed mature canopy.

1. Recently oiled Positive1–10

Yellowing and loss of foliage in affected areas, andpresence of dead, low-placed seedlings. Somesurviving seedlings.

2. Recoverypreliminary

Positive11–30

Loss of foliage in affected areas, and presence of dead,low-placed seedlings.

3. Recoveryestablished

Positive31–50

Foliage density in recovery with new growth.Re-establishment seedling bank under re-establishedcanopies.

4. Recoveryprogressed

Positive51–70


5. Recoveryadvanced

Positive71–90


6. Structuralrecovery in finalstages ofcompletion.

Positive91–100

Normal foliage density with canopy closed. SiteMaximal Canopy Height unaffected. Presence ofseedling bank of 3–6 year old young plants, and anotable gap between mature canopy trees.

Possibledeteriorationstate postrecovery, likelyfrom phases 1 to 5

Negativecondition

Foliage absent in impacted gap area

structure, and not the dependant fauna. From other studies, it seemsthat recovery of fauna and full habitat recovery may take longer periodsthan recovery of forest structure alone (Salmo and Duke, 2010).

It seems that once the toxic components of spilled oil have dissipat-ed and broken down to more benign residual products, mangrovestands may re-establish in similar ways to non oil-impacted forests(see Duke, 2001). Erosion may also follow deforestation with tree deg-radation and subsequent dislodgement of root systems and soil binding.Elevation within the intertidal zone governs inundation regime, whichis critical for establishment and growth ofmangroveswith particular re-quirements that vary between species. Therefore, any loss of soil and el-evation via erosion will influence mangrove re-establishment (Lewis,2005). Instances have also been reported where dead trees and

owth from sublethal (marginal) and lethal (central, gap) impacts (also Fig. 1), respectively.doubtably important also, has not been included in this treatment. Actual times taken for

Lethal trajectory in gapLethal state representationin gap

Trees mostly alive throughout stand; occasional deadtrees and up to ~10% light gaps in ambient conditions.

Tree death (within 6–12 months after spill), deadseedlings and saplings. Trees with dead yellow leavesand small twigs present. Mostly dead seedlings.

Deterioration of dead trees missing small branchesand twigs. No appreciable recruitment, someseedlings.

Deterioration of dead trees missing large branches andupper stems. Establishment of additional seedlingrecruits in open areas.

Notable large stumps remain with some exposedroots. Saplings dominate in dense stands, in the forestgaps. Immature, low level canopy closure.

Reduced remnant dead stumps & wood sections.Canopy closure advanced. Notable thinning of saplingsand young seedlings present.

None or occasional remnant mature-sized stumps.Canopy closed. Damaged area Site Maximal CanopyHeight restored. Formation of seedling bank of 3–6year old recruits, notable class gap to mature canopy.

Dependent on state of gap degradation. Absence ofintegrated roots, living seedlings, saplings and youngtrees. Evidence of scouring.

Fig. 6. Recovery of mangrove forest structure killed during various oil spills (seeSupplementary Data Table 3). Recovery was quantified in terms of total above groundbiomass of mangrove stands before and after deforestation (see Table 2). The linearregression of ‘best fit’ shows a trend towards recovery of after around 3 decades(dashed line: r = 0.878; N = 7; P b 0.005). Note, this trend does not necessarilyrepresent full habitat recovery since faunal biota were not considered.

Fig. 7. Rates of annual recovery of mangrove forest structure influenced by different tidalranges (see Fig. 6; Supplementary Data Table 3). The linear regression of ‘best fit’ shows atrend where greater tidal range equates to greater rates of recovery (dashed line: r =0.827; N = 7; P b 0.005). Note, this trend does not necessarily represent completehabitat recovery since faunal biota were not considered.


dislodged roots have been carried away by waves and tides, causing asecond wave of mortality through scouring of newly-established plantsaround 6 years after the initial oil spill impact (Duke et al., 1997, Dukeand Burns, 1999). While oil-impacted, fringing mangroves on high en-ergy coastlines are at greatest risk (Duke and Burns, 1999), it is such ex-posed stands thatmaintain and support the integrity of the structurally-delicate inner stands. Re-establishment of these stands is critical butthere is little evidence demonstrating how this might happen. In anycase, it means that all mangrove stands are highly vulnerable to oilspills, and that lethal damage should be avoided at all costs!

Biotic and abiotic interactions with mangrove ecosystems are com-plex, and each spill has a different set of circumstances. Hence, somegeneralisations about the long-term term consequences of oil spills inmangroves are difficult to make. In summary, the primary factorsmost likely to influence recovery time are oil type (heavy versuslight), quantity, and oil condition (fresh and concentrated versusweathered and dispersed). High initial impacts are most likely wherefresh, light oils are involved, but also possible also with concentrated,heavy oils where they smother exposed surfaces (Duke et al., 1998b).Broadly applied dense oiling is also more likely to result in delayed re-covery than small patches of oiling over several hectares or less. Recov-ery clearly depends on biotic factors also, like the supply of propagulesfor colonization, and variations in species tolerances.

Furthermore, recovery may proceed more rapidly in areas of hightidal ranges where the effects of more flushing appears to break downdeposited oil faster (Burns et al., 1993, 2000). This is shown from thecurrently considered data in Fig. 7, which shows the relationship be-tween tidal range for particular incidents, and the estimated annual re-covery rates (Supplementary Data Table 3). The recovery rates varyfrom 3 to 6% per year for a tidal ranges varying from 0.6 to 3.9 m. Theimplications of these preliminary findings are that the application of ar-tificial flushing may be beneficially applied to accelerate the recovery ofat least the structural components of mangrove stands.

A number of management options exist to assist recovery of man-groves following an oil spill. These focus on accelerating the rate ofbreakdown of oil (via degradation and bioremediation) and plantingseedlings to assist natural regeneration. As a means for restoring man-grove cover, facilitating natural regeneration is generally preferredover planting as it is more cost-effective, and it can have a better out-come for structure and composition (Lewis, 2005). For oil spills, seed-ling re-establishment may only proceed once toxic compounds in

sediments have sufficiently diminished, as the agents causing harm. Fi-nally, if changes in elevation and alterations in tidal flow have occurredfollowing severe or prolonged damage, re-engineering may be neededto create suitable conditions for establishment and growth (Schmittand Duke, 2015). For areas that have been denuded of cover and debris,strategic planting or the positioning of artificial structures may assist tocapture and stabilise sediment and create nodes of advanced recovery(also see Gedan and Silliman, 2009).

In conclusion, on-going improvements for bettermanaging recoveryand rehabilitation of oil-impacted mangrove tidal wetland habitat, de-pends on the successful implementation of robust assessment andmon-itoring strategies and measures for gauging the success of interventionand mitigation efforts. These measures need to be ecologically soundwhile providing quantifiable, longer term comparisons of reliable, prac-tical and useful evaluations of habitat condition and health. While agreat deal of progress has beenmade in some aspects, the recommenda-tions that have arisen from these considerations are considered practi-cal and useful next level improvements in the sustainablemanagement of valuable but vulnerable tidal wetland habitatsworldwide.

10. Operational response guidelines for oil-damaged mangroves

As noted, there is a great need for standard reporting of each spill in-cident affecting mangroves. This includes sharing these findings in apublic forum. Standard descriptors start with: the area of oiled man-grove and surrounding sediments; as well as areas of oil impacted de-forestation. Finally, there is a need to promote rehabilitation ofdamaged areas, especially for areas deforested by oiling. With thesemeasures, it is understandably considered best practice to support nat-ural processes of natural seedling recruitment, and to promote plantgrowth generally. For instance, only if absolutely necessary, should sup-plemental planting be used to aid recovery and seedling re-establish-ment when stand integrity has not yet reached self-reliance.

Amore complete set of suggested actions are listed in Table 3, cover-ing the four key threat phase periods that make up a ‘Pre, During, Im-pact, Post’ (PDIP) Spill Response plan. It is notable, that this strategyreflects the nomenclature to be used by AMSA and CSIRO in the newAustralian National Oil Spill Monitoring Handbook. By way of furtherexplicit explanation, nine (9) key recommendations are also given forimproving the management of oil-damaged mangrove and tidal wet-land habitat. Further included are brief guidelines for responders to

Table 3Actions and response strategies for monitoring mangrove habitats impacted, or likely to be impacted, by large oil spills, as a set of recommended Standard Operational Procedures. Thetypes of responses, actions and their timing depend on the Threat Phase of the spill incident. The four Phases include: “Pre-Spill”, “During Spill Pre-Impact” and “During Spill Post-Impact”and “Post Spill”. Modified from Duke and Burns (1999). This describes the “Pre, During, Impact, Post“(PDIP) Spill Response Plan for the four (4) critical phases when oil spills threaten, orimpact on, mangrove and tidal wetland habitat.

Oil spill threat phase Operational monitoring actions Response measures Justification

Pre-spillBefore Spill Incident

Proactive preparedness – Training of personnel inhigh risk areas, equipment preparations, plus thecompilation of Reports, Data and the approval ofcurrent best practice Strategies for Monitoringand Assessment of Oiled Mangrove Habitat.• Feedback from prior incidents of monitoring,recovery and mitigation measures used.• Risk & Resource Assessments Minimization ofrisk at possible spill point sources, includingsafe ship handling practices.• Contingency Planning with the Compilation ofbest advice, equipment and personnel trainingfor effective rapid response.• Publication of a coastal resource atlas,identifying risk levels and habitat vulnerability.• Research into fate and effects of oils anddispersed oils on mangrove communities.• Regular re-assessment and updating ofresponse, cleanup and management protocols.• Maintenance of a contact list of mangrovemonitoring specialists.• Test likely products and strategies used inmitigation and cleanup.• Supply & Equipment Stockpiles developed.

Specific responses include:1) Oil spill database. Develop and support anational and/or regional database and atlas ofoil spill incidents affecting mangroves.2) Current contacts. A network of currentstakeholders, like the Australian Mangrove &Saltmarsh Network (www.amsn.net.au).3) Shoreline risk evaluation. Shoreline mappingusing latest satellite imagery; in combinationwith shoreline condition monitoring andassessments (like the Shoreline VideoAssessment Method) for the entire shorelinearea at risk.4) Standard operational procedures. Anapproved and agreed set ofprocedures/strategies for the monitoring andrehabilitation of oil damaged mangrove habitat,based on past incident experience, reports andresearch.5) Standard methods. Production of a series ofapproved Standard Assessment Methods, like:mangrove cleanup techniques; how torecognise mangrove recovery status, and agingdead tree decomposition; species identificationmaterial that are regionally relevant for plantsand animals.

This applies to unspecified threats from large oilspill incidents that may affect sensitive mangrovehabitat.It is essential best practice to be prepared usingthe best available resources and people.Preparedness need be applied at a National andregional level since major oil spills can occur atanytime and at any location.This ‘In between’ Phase is the best time toreview, discuss and approve a series ofdedicated, current best practice guides alongwith current best practice monitoringstrategies. It is also the time to prepare contactlists for particular specialists who can assistboth during the Rapid Response Phases, and themore considered post incident assessments.

During Spill pre-impact.Spill Incident TakingPlace - oil threatensmangrove habitat.

Oil threatening mangroves – reactive phaseimproved greatly by any prepared responsemeasures.• Urgent need for monitoring of mangrovehabitat to start with the Rapid Response Unitsduring the spill incident.• Prediction of Threat - Spatial & Temporal -Predict movement of oil and evaluate threats topotential stranding sites of oil along theshoreline.• Apply Contaminant Delay and DiversionStrategies - evaluate the range of responseoptions, including “do nothing but monitor theincident”.• Dispersant Application - review cleanup andcontainment techniques subject to habitat, oiltype, etc.• Recovery of Oil - Assess removal, disposal, andassisted degradation of oil.

Specific responses include:

1) Standard operational guidelines. Follow anyagreed and approved Monitoring AssessmentStrategies and Field Procedural Check Sheets.2) Standard reporting. Document Incidentcircumstances as recommended in publicallyavailable reports.3) Standard assessment methods. Specifically foridentification of: oil type (collect fresh samplesfrom source); oil volume released; oil volumesalvaged; locations likely to be oiled; type ofcorrective chemicals used, like dispersants;installation of booms; use of skimmers;document impacts on mobile marine and birdfauna; collect water quality data.4) Oil spill database. Add new and revisedinformation to the national oil spill databaseand atlas.

Oil spill current – or within 2 weeks.Oil not in mangroves but it threatens.

The primary aim at this phase is to protect sitesof sensitive mangrove habitat. To be effective,this requires a good knowledge of thewhereabouts of any particularly vulnerablehabitats, as well as the current climaticconditions (like wind direction, waves, storms,etc), and current movements.Responders also need to have an eye on thefuture with additional, targeted monitoring tofurther improve future responses (like thetrialing of cleaning techniques, innovativeproducts, etc).This includes the consideration andestablishment of incident specific influentialparameters – as listed in Response Items. Theseparticularly concern the locations of oildeposition, as well as reasonably accuratemeasures of habitat likely to be affected by oil.

During Spill post-impact.Spill Incident TakingPlace - oil depositedamongst mangroveplants and surroundingsediments.

Newly oiled mangrove - Reactive Phase improvedgreatly by any prepared response measures.• Urgent need for monitoring of mangrovehabitat to start with the Rapid Response Unitsduring the spill incident. There is only a veryshort period of days and weeks before vitalevidence is lost.• Habitat Affected - Shoreline Assessments -evaluation of affected habitat.• Remote Imagery & Mapping - before damage -evidence of canopy damage.• Infauna Assessment - assessment of infaunacondition.• Stranded Oil Assessment - map oil ‘hot spots -assessment of deposited oil


1) Standard operational guidelines. Follow anyagreed and approved Monitoring AssessmentStrategies and Field Procedural Check Sheets.2) Standard reporting. Document ongoingincident circumstances.3) Standard assessment methods. Specifically foridentification of: oil volume released (collect oilsample, floating/deposited on trees and onmud); map locations where oil deposited; noteoiled ‘hot spots’; document impacts on fauna;collect data and samples of each speciespresent; collect water quality data.4) Oil spill database. Add new and revisedinformation to the national oil spill databaseand atlas.

Oil spill current – or within 2 weeks.Oil in mangroves, coating exposed roots, soil &wildlife.

At this critical phase, it is essential to determinethe extent of likely and actual oil spill impactsrelated to both lethal and sublethal responsesby affected mangrove habit. This requires agood knowledge of the indicators by thoseundertaking the monitoring.It is essential during this phase to establish keycriteria that will frame all post spill assessmentreporting. For example, it is important to knowabout the extent of likely sublethal damage.This can only be determined if the extent ofoiled mangrove is mapped during this shortphase. Much of the visual evidence of broaderoiling disappears shortly after this phase.

Post spill.Oil Long Settled,Mangrove notablyImpacted, and/orRecovery Taking Place.

Previously oiled mangrove – opportunities toevaluate mitigation strategies, as well as thequantification of past impacts and any recoveryprocesses.

• Habitat Damage & Recovery Assessments -evaluation of damage, response and recovery of


1) Standard reporting. Document what is knownof the primary oil spill incident – along with anyintervening severe events, like cyclones, oradditional oil spills.2) Standard assessment methods. Specifically for

Oil spill much earlier –maybe last year or decadessince.

For this phase, it is essential to document whatcan be discovered about the earlier oil spillincident.Important parameters to add at this time


http://www.amsn.net.au

Table 3 (continued)

Oil spill threat phase Operational monitoring actions Response measures Justification

oiled habitat.• Remote Imagery & Mapping - after damage -evidence of longer term canopy damage.• Assessment of Associated Biota - condition ofmangrove infauna.• Oil in Sediment - analysis of residual oil insediments.• Assist in restoration of habitat where and ifnecessary.• Assessment of prior Restoration Interventions

identification of; visual presence of oil; collectwater samples; collect sediment samples for oilassessment; assess status of mangrove habitat –condition; structure, biodiversity; record deadtrees and status of decomposition;measure/sample presence of fauna, biomass,species, abundance.4) Oil spill database. Add new and revisedinformation to the national oil spill databaseand atlas. Especially reporting on recoverystatus, and how affected sites responded toapplied mitigation strategies.

include: the full extent of structural (lethal)damage (this would not have been evident atthe time of the spill); the extent of sublethaldamage to reproductive success & productivity;impacts on dependent animals, including localfisheries; review lessons learnt during theincident for reducing impacts of future spills.It is important at this phase to establishamounts of progress, if any, towards recovery.This requires those monitoring to have astandard set of robust indicators for rankinglevels of damage, and recovery. Such objectivemeasures are needed when comparingincidents, and to get more measuredevaluations of the effectiveness of priormitigation strategies.


large oil spills. The following points and recommendations are madebased on the prior studies and observations considered in this article.

11. Specific recommendations for monitoring oil-damagedmangroves

The history of oil spills affecting mangroves suggests that recoveryand rehabilitation generally takes at least 3 decades (as noted above),depending on climate, tidal range and geographic circumstances(Lewis et al., 2011; Duke, 2001; NOAA, 2014). However, sufficiently de-tailed studies of long term impacts are relatively few in number.What isrequired is more explicit reporting using a standard selection of key de-fining parameters.While an array of factors influence the outcome of anoil spill incident onmangrove stands, only a few parameters are neededto quantify impact severity and on-going changes towards recovery, ordegradation. By measuring these parameters, it should be possible toquantify overall impacts and timeframes for recovery.

This understanding would greatly improve the management of oil-damaged mangrove ecosystems. For example, oil type and the theamount of habitat oiled are key determinants of impact severity, andthe longer term responses. With this knowledge, responders might beable to more confidently apply targeted intervention with a reasonableexpectation of achieving certain outcomes and in reducing impacts. Thiscould include interventions like: the application of dispersants; the re-direction of oil deposits; the reduction to oil depositedwithinmangrovestands; enhanced flushing; and bioremediation. The following nine (9)recommendations outline a series of strategies intended to guide betterand more targeted responses that promote and accelerate recovery ofmangrove habitat affected by larger oil spills.

Recommendation 1: Follow a Pre, During, Impact, Post (PDIP) Re-sponse Plan (Table 3) to minimise impacts and costs associatedwith oil-damaged mangrove and tidal wetland habitat.

For overall management of large oil spill impacts on mangrove andtidal wetland habitat it is necessary to follow a plan like the allencompassing strategy of Pre, During, Impact, Post (PDIP) ResponsePlan, adapted from Duke and Burns (2003) and described in Table 3.

Recommendation 2: Report, record and make available publically,all relevant information about oil spill incidents where they impacton mangroves and tidal wetland habitat.

For relevant spill incidents, both past and present background infor-mation should be made available, collected and archived in a centralpublic repository. Full access to all relevant documents is essential ifthere are to be further improvements in future response actions. Thisdatabase could build on prior reviews of large oil spill incidents, likethose from around Australia (see Duke and Burns, 2003). It is importantto piece together, capture and link all relevant historical facts and obser-vations that might otherwise be lost.

Exemplary examples of existing databases include those mentionedin this review, including: AMSA (2016); CEDRE (2016); ITOPF (2016);NOAA (2016) and the Nigerian Oil Spill Monitor (2016). These modelresources could be improved uponwith:more defined content (cs. spe-cific geographic areas, incident types, etc), better search capabilities(like, mangroves affected), a wider range of standardized entry fields,andmultiple choice selections to help responders upload their observa-tions in a standard format.

Recommendation 3:Where possible, either as part of pre-spill con-tingency planning, or as part of rapid assessment pre-impact, it ishighly beneficial that baseline condition of the oil- threatenedman-grove shorelines be measured and evaluated using acceptedmethodologies, to support future ‘before and after impact’ com-parisons.Where this is not possible, appropriate comparative sitesneed to be established in suitable locations known to reflect aswell as can be determined, the pre-impact state of the impactedmangroves.

The ideal baseline monitoring of shorelines threatened by oil spillsneeds to be undertaken prior to an oil spill incident. But, since oil spillsare known to occur anywhere, as demonstrated in this review, it re-quires regional shorelines be fully surveyed beforehand. This appearsto present a difficult challenge, but there are solutions found in recentinnovations in shoreline surveillance. One is critical evidence capturedin high definition satellite imagery and data. Remote satellite mappingis extremely valuable in providing overall quantifications of habitattypes and locations, but there are limitations to its applicationwhichbe-comes obvious only when ground verification is found lacking.

An important recent compliment to satellite remote sensing is theShoreline Video Assessment Method (S-VAM) as used from eitherboat-based (Mackenzie et al., 2016) or low-level, aerial platforms(Duke et al., 2010). The S-VAM approach provides a unique, improvedperspective that allows quantification of shoreline processes as well aslikely impacting agents, like severe climatic events, storms, and large

Table 4A proposed standard list of information fields for reporting on large oil spill incidents, es-pecially those resulting inmangrove dieback and habitat loss. Modified and adapted fromDuke and Burns, 1999; NOAA, 2014.

Standard reporting oil spill incident database fields

Primary informationDate, or period, of spillDate/time of landings of oil by locationLocation, name and site coordinatesTidal range, tidal phase during oil landingsSite exposure condition – aspect, directionTypes of oilQuantities of oil releasedWeather conditions at the time and subsequentlyDescription of spill, details of incident, vessels involvedObservations/measurements/samples, slick observations

Spill responseDescription of response actionVolume of oil recoveredRemediation/mitigation strategies usedType and quantity of dispersant used

Sediment condition, physical site parametersSediment typeHydrocarbons in sedimentsCoastal features and water movements


oil spills. For instance, S-VAM aerial survey data was used to establishshoreline baseline condition, including mangroves, threatened duringthe offshore Montara oil spill incident off the north-west coast of Aus-tralia in 2009 (CEDRE, 2016; AMSA, 2016). A notable feature of thislow level aerial monitoringmethod is that it allowed not only establish-ment of baseline condition, but it also provided a permanent referencedatabase from which to evaluate future change along these shorelines.The future application of this method depends on two key contribu-tions: continued image acquisition through space and time; and, the de-velopment of a dedicated data management and display portal, calledShoreView. The former requires its adoption by coastal surveillanceagencies at a national scale, and the latter is under development forthe Port Curtis Port Alma Coastal Habitat Archive and Monitoring Pro-gram (Duke and Mackenzie, 2015). For those interested, the prototypePTTEP Montara ShoreView display portal is available for viewing at:http://203.101.224.239/.

Recommendation 4:Collect all descriptive data on large oil spills ina standardized, expanded format, especiallywhere spillsmight im-pact on mangrove and tropical saltmarsh habitat.

Biotic condition, impact assessmentArea and extent of mangrove oiled – time of landingExtent of mangrove deforestation – over one yearMangrove species affected – oil contactedOther mangrove biota affected – death of animalsStatus of plant condition, regrowth, recruitment

Remediation appliedNatural restoration, no intervention, location areasAssisted restoration, types and location of interventions

Habitat recovery assessmentMonitoring strategies conductedResearch investigations undertaken

Maps and remote sensing imageryField sketch maps and notesSatellite imagery, highest resolution, GIS layersAerial imagery flownHistorical imagery, background status, change detection

Image records and documentationPhotographic imagery archiveOfficial reports, publicationsPopular media, newspapers, websites

Contact person(s)/organisation(s), email, web sitesSpill management and clean-upImpact assessment/monitoring/researchRecovery monitoring and current statusSite access restrictions, authorities and delegations

It is recommended that some additional fields be considered forinclusion in future evaluation and monitoring guides. The value ofreports on oil spill incidents affectingmangroves could be greatly en-hanced by adding the suggested fields (see Duke and Burns, 2003), asfully detailed in Table 4. And, these would bemost useful if theywerefreely available as per Recommendation 1. The information fieldslisted expand slightly, but importantly, on those listed by NOAAand other organizations. The new observations made in this reviewsupport further useful post-spill deductions, for example, regardsextrapolated volumes of oil lost based on the area of oil-relateddieback.

Recommendation 5: Determine, using accepted methods, thetype, extent and concentrations of oil within the impacted areasof mangrove (cs., water surface, water column, sediment andmangrove surfaces and buried sediment) at both the time of oilingand at some period after initial oiling (i.e. 3–6months)when lethalimpacts are apparent, and the type, extent and severity of man-grove damage (e.g. severity of defoliation or deforestation) isknown.

The severity of damage caused by oiling ofmangrove habitat, shouldbe measured in terms of deforestation and habitat loss (the lethal im-pact), as well as sampling and measuring oil concentrations and oiltype and condition from contaminated sediments. These and otherinfluencing factors are needed in the making of a baseline assessment.There is further value in using the reported lethal dosage of 5 l.m−2 ofmature Rhizophora stands in Panama (Duke et al., 2000), to estimate ei-ther the area of mangroves likely killed by the known volume lost, orvice versa, to deduce the likely volume of oil from the area of deadman-groves. It follows that the area ofmangrove deathwould not be the onlya measure of impact, but this measure is a useful proxy for the amountof oil deposited inmangrove habitat. This allows impact/response asses-sors ameans to estimate theminimal volume of oil lost inmangroves, asthe amount it takes to cause anobserved area of tree death. Clearly, suchan estimate will be approximate, since there are other factors to consid-er, like oil type. The accuracy is expected to be improved as we learnmore from better andmore specific reporting, as noted in these Recom-mendations (2, 3 & 4).

Recommendation 6: Post-spill monitoring of mangrove reforesta-tion and the presence of hydrocarbons in sediments needs to beconducted over 3–4 decades to assess habitat recovery wheretrees have died.

Habitat rehabilitation from recruitment to canopy closure and mat-uration of previously deforested areas from oiling may take around35–50 years from the initial incident of first impact. Note that habitatcondition refers to the diversity and health of both plants and animals.Recovery rates are expected to be difficult to predict because there area number of influential factors like, tidal range, temperature and rainfall,coupled with site conditions of species assemblages, sediment type, siteexposure. There are also different residual oil effects, with their differingrates of degradation. A further notable factor often overlooked is theprior condition and resilience of mangroves before they had beenimpacted by a current incident. While it is essential where possible toestablish baseline condition, this recommendation requires the identifi-cation of adequate longer term funding and support through

http://203.101.224.239/

Table 5Once oil is within amangrove stand, the following is a brief list of options ranging from noaction, to varying forms of intervention (adapted from Hensel et al., 2010; NOAA, 2014).

Intervention action Comment

No action This is recommended for most affected areas.Booms and other barriers,including adsorbant booms andpillows

Can be effective but generally only for lowenergy settings and where advancedpreparation enables structures to bepositioned in advance of the spill comingashore.

Manual removal Most applicable for heavy oils as they can bepersistent and cause long term risks;however, trampling and other forms ofphysical damage are most likely to beunreasonably destructive.

Vacuuming Suitable only for the outer fringe of amangrove and/or in open stands, coarserather than fine sediment and heavier ratherthan light oil. Access by the necessary heavyequipment is a major limitation.

Flooding and flushing usingseawater

Designed to remove oil from sedimentsurface and from mangrove parts; mosteffective for light and medium oils, on areceding tide when oil is moving out of themangrove and if sediment will not bedisturbed. This type of intervention showsgreat promise since this method concurs withobserved more rapid oil degradation rates inareas of higher tidal ranges (see Burns et al.,2000; Duke et al., 2000; Fig. 7).

Cleaners & dispersants To assist tidal flow or flushing treatments todetach and dissolve oil from sediment andmangrove parts; however, some cleanersmay be toxic.

Bioremediation Promoting microbial breakdown of oilthrough nutrient addition and aeration;noted that this approach is yet to be fullyevaluated and nutrient addition cannegatively affect mangrove health. But seeDuke et al. (2000) for a successful trial ofbioremediation in Central Queensland andSantos et al. (2011) for a furthercomprehensive account.

Removal of oiled debris Appropriate when no further oil is likely toreach the shore (debris acts as a barrier),physical damage to mangroves can beminimised and the activity does not result insignificant habitat alteration (also see Duke etal., 1999).

Floating loose sorbents This includes dust or fibre sorbents, includingpersistent polymers (i.e. plastics banned inAustralia and other countries, for theirpersistence and negative influences), floatingorganic materials of little use (e.g. wool, haircoconut fibre, straw), or inorganic materials(e.g. zeolites, cat litter, plasma silicates).These may well sink and they are generallynot well researched. However, new productsand processes are imminent. For example, seethe AMSA (2016) Oil Spill Control AgentsRegister list. The product called OilZorb, as anexample with potential for better responseapplications in and about mangrove areas.


appropriate mechanisms starting with insurance and company clean-up obligations.

Recommendation 7: Mangroves along exposed foreshores andfringing the waters' edge are more vulnerable to damage and re-quire the highest level of protection.

Rates of recovery are largely influenced by site exposure wherethose in sheltered locations recover slowly while those in exposed loca-tionsmay have initially recovered quickly only to be subsequently killedby “driftwood scouring”. This degradation occurs after the roots of deadtrees have decomposed and become mobilised, after around 5–6 years,as observed in Panama (Duke et al., 1997). This occurrence appears toapply generally where trees die in exposed stands for various reasons(like severe stormwinds), and resulting in stand replacement and turn-over (Duke, 2001).

Recommendation 8:Post-spill monitoring of animals needs to con-tinue as part of habitat rehabilitation assessments for more thantwo years to adequately assess their recovery.

While mangrove trees take several months to die following a largespill (as for Recommendation 6), this contrasts with the impact on ani-mals which occurs within hours of the oil first settling after tide levelsfirst drop. During the following days, the habitat can smell ofdecomposing fauna, like those in Port Curtis after experimental oiling(Duke and Burns, 1999). The animals chiefly comprised small fish, shell-fish and crustaceans, including sesarmid crabs and pistol shrimps. How-ever, unlike the process for replacing trees taking decades, the crabs andother animals reported dead in the trials (Duke et al., 2000), had re-established in plots after 1–2months. However, it was notable that fau-nal activity levels remained relatively low compared to those in un-oiled plots after 2 years.

Longer term funding support is essential also for research andmon-itoring of animals affected by oil spills. Animals are essential for thehealth andwell-being ofmangrove vegetation, as shown in the complextrophic and functional relationships observed (cs., McIvor and Smith,1995).

Recommendation 9: Once oil enters a mangrove tidal wetland,very serious considerationmust bemade for ‘no action’where justabout any intervention will result in further habitat damage, liketrampling of sediments and seedlings, cutting away dead wood,sweeping up dead vegetation, planting seedlings, burning off oil,scraping up oiled surface sediments, and applying dispersants orother industrial chemicals. Cleanup access and procedures mustonly be applied where these intervention actions are proven notto cause harm to recovery processes.

Overall, the treatment of oil offshore is regarded as the preferred op-tion over the treatment of oil deposited within intertidal habitat. Thisapplies especially to mangroves where clean up is extremely difficultsince stands are often dense, remote and inaccessible. And, that theclean up intervention is most likely damaging in itself; for example,trampling, root breakage and other forms of physical impacts. Optionsfor treating oil offshore include mechanical containment and skimmerrecovery, agitation and mixing, dispersant use, and burning. However,chemical additives such as dispersants may have an impact on other

sensitive habitats like coral reefs, while burning can produce solid resi-due that can wash ashore and also contaminate the intertidal zone.

Should oil enter a mangrove stand then a decision must be made atthe time to act, or not, based on best available evidence of all extenuat-ing circumstances. Information reviewed by Hensel et al. (2010) pro-vides some well-founded suggestions for the cleanup of oil spilledwithin mangroves and associated intertidal habitats. A summary is pre-sented (Table 5) as an additional guide for making informed decisionsabout cleanup intervention. Of these, the most likely beneficial inter-vention appears to be gentle flushing (Fig. 7), since this simulates


greater tidal flushing with reported correlative benefits for more rapidlonger term recovery (Burns et al., 2000).

If there are any doubts about making an intervention, then such un-certainty must emphasis the need for more research and testing. It fol-lows that in making a decision to intervene, then that action should berigorously reviewed, monitored and tested to properly evaluate itsvalue and future merit in subsequent responses – compared to doingnothing. During a spill, is arguably the best time formaking selective tri-als and evaluations since there is both opportunity with experimentalconditions, and public support. Justification is readily made in the inter-ests of improving future responses, and in learning from past experi-ences and mistakes – all of which needs to be publically documentedand published.

Acknowledgements

I acknowledge assistance from the sub editor and an anonymousreviewer.

Appendix A. Supplementary data

Supplementary data to this article can be found online at http://dx.doi.org/10.1016/j.marpolbul.2016.06.082.

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