A retrospective study was carried out using lung tissue samples fixed in 10% buffered formalin between 2000 and 2017 and kept in the Institute of Animal Health Tissue Bank. Formalin-fixed lung samples were cut into thin sections (≤1 mm) to ensure the proper penetration of OsO4. Post-fixation with OsO4 is needed as lipids are soluble in the processing solvents used to embed the tissues in paraffin. The sections were then washed with running tap water for 20 min followed by 10 min in distilled water. Next, the sections were immersed in 1% OsO4 aqueous solution (sonication was previously used to dissolve the commercial crystalline OsO4) within hermetically sealed bottles on a shaker inside a chemical hood. Then, the sections were rinsed in running tap water for 30 min and immersed in 1% periodic acid until the dark osmicated tissues were uniformly cleared (Abramowsky et al., 1981). Samples were washed for 30 min with tap water, and rinsed three times with distilled water. Then, the samples were routinely processed and embedded in paraffin-wax, sectioned at 5 µm-thick, treated with picric acid (1% in ethanol 96%) for 24 h to remove excess formalin pigment (Abramowsky et al., 1981), and counterstained with hematoxylin and eosin (HE). Finally, slides were mounted in DPX mounting medium. Tissue sections as blubber and rete mirabile (which have abundant adipocytes), were used as positive controls (treated with OsO4) and negative controls (non-treated with OsO4) to validate the technique.

#### Microscopic Analysis

All lung sections were evaluated for the presence/absence of fat emboli, as well as the area occupied by those emboli within lung vessels using light microscopy (Olympus BX51).

Each lung tissue section was divided in "N" number of 100× magnified microscopic fields (MF) (Ocular: 10× and Objective: 10×). A Bootstrap analysis was carried out to determine the number of 100 MFs ("n") that needed to be studied for each tissue section (**Table 2**). We considered a good estimation of the true value if the total bound error was below 8%. Depending on the total tissue section area the Bootstrap analysis yielded results between 14 and 20 100 MFs. These fields were randomly selected and photographed using an Olympus XC30 camera (Olympus Soft Imaging Solutions GmbH©, Johann-Krane-Weg 39, D-48149 Münster) (**Table 2**). Fields containing pleura (adipocytes are normally present in the pleura of sperm whales) (**Figure 1B**), and/or largediameter bronchi/bronchioles (empty spaces) were discarded to ensure a similar parenchyma size comparison between the different fields.

The software ImageJ (1.48v, Wayne Rasband, National Institute of Health, United States) was used to determine the area occupied by fat emboli, in pixels, in each of the photographs. Each of the 100 MFs' photographs has a total area of 1,920,000 pixels. Fat emboli are recognized as black droplets primarily in the lumen of capillaries and smalland medium-size arteries. The software ImageJ allows the quantification of areas of a certain color automatically, or the quantification of selected areas manually.  As a result, for each animal, we ended up having an "n" number of 100 MFs (photographs), each of them with an area in pixels occupied by fat emboli.

#### Analysis for the Validation of the Osmium Tetroxide Technique as a Complementary Diagnostic Tool for Ship-Strikes

The 25th, 50th, 75th, and 90th percentiles of the areas (pixels) occupied by fat emboli in the "n" 100 MFs studied were calculated for each animal (**Table 3**). As fat emboli were also present in a few lungs of the "control group," a classification and regression tree (CART) was developed to obtain a cut-off value from which the probability of association with ship-strike is high. This procedure classifies data using a sequence of if–then rules. The basis of the decision tree algorithms is the binary recursive partitioning of the data. The most discriminative variable is first selected to partition the data set into child nodes. The splitting continues until some stopping criterion is reached. The tree was constructed according to the following algorithm: in the first stage, the tree grows until all cases are correctly classified, and in the second stage, we used the tenfold cross-validation method of successive pruning (Breiman et al., 1984). Finally, the tree that minimized the error measurement (deviance) was chosen. Then, the low and high-probability categories obtained were compared using the exact Fisher test. The sensitivity

TABLE 1 | Epidemiological and biological data of the sperm whales included in the present study with evidence of ship strike.

Age: N, Neonate; C, Calf; J, Juvenile; S, Subadult; A, Adult. Stranding location: N, North; S, South; E, East; W, West; NE, Northeast; NW, Northwest; SE, Southeast; SW, Southwest; T, Tenerife; GC, Gran Canaria; F, Fuerteventura; L, Lanzarote; H, El Hierro; LG, La Gomera. Decomposition code: 1, Very fresh; 2, Fresh; 3, Moderate autolysis; 4, Advanced autolysis; 5, Very advanced autolysis. Body condition: 1, Very poor; 2, Poor; 3, Fair; 4, Good; NE, Not Evaluated.

"N" is the total number of 100 MFs analyzed in the lung tissue section; and "n" is the number of microphotographs that should be captured to achieve <8% error bound.

and specificity were estimated by means of 95% confidence intervals (95% CI).

expressed as medians and interquartile ranges (IQR = 25th–75th percentile) (**Table 3**).

### Exploration of Association Between Trauma-Related Variables and Fat Emboli Severity

Categorical variables were expressed as frequencies and percentages, and continuous variables, like fat emboli areas, were

The variables age, presence/absence stomach food content and degree of digestion of the ingesta, presence of fractures and stranding location were compared between both groups using the Chi-square (χ2) test or the exact Fisher test for percentages; and the Wilcoxon test for independent data for the medians (**Table 3**).

The variables age, sex, body condition, presence/absence and degree of digestion of the stomach food content, trauma location

adipocytes in the pleura (arrows) (Bar = 200 µm).  For this aim, a linear analysis was carried out. The variables introduced in the model were age (calf/not calf), sex, body condition, presence/absence and degree of digestion of the stomach food content, trauma location and presence/absence of fractures. Then, a selection of variables based on the Akaike information criteria was performed.

Data were analyzed using the R package, version 3.3.1 (R Development Core Team, 2016).

 Fat emboli ranged from 67 to 59773 pixels, and were seen circulating in medium and small caliber intrapulmonary arteries and/or obliterating arterioles and capillaries, both in fresh and decomposed specimens (**Figure 3**). None but two of eight "control" sperm whales had detectable fat emboli (**Figure 1A**). Those two animals (cases 21 and 24) had rare isolated OsO4 positive fat emboli (<650 pixels) in arterioles (**Table 3**).

Calves were "significantly" (p = 0.003) more likely to be involved in ship-strikes than other age categories. As well, the presence of fractures was "significantly" associated to ship-strikes p = 0.003. Other variables studied like the stranding location (island) or the presence/absence and degree of digestion of the ingesta, were not significantly different between both groups (**Table 3**). An association between trauma-related variables and fat emboli severity could not be established.

When assessing the probability of ship strike based on the fat emboli area, significant differences between non-strike and strike groups started to be seen in the 50th-percentile values, but the

TABLE 3 | Categorical variables studied expressed as frequencies and percentages or continuous, expressed as medians and interquartile ranges (IQR = 25th–75th percentile).

In the last column, P-value <0.05 was considered as statistically significant difference between ship-strike and non-ship strike groups.

FIGURE 2 | Vessel strike-related injuries in sperm whales (Physeter microcephalus) stranded in the Canary Islands. (A) Presence of a deep incision in the right flank of the animal, caudal to the pectoral fin, with soft tissue exposure, abdominal perforation and evisceration and costal fractures, case 4. (B) Complete amputation of the vertebral column at the level of the last thoracic vertebrae, case 14.

highest discriminant power between both groups corresponded to the fat emboli area's value of the 75th-percentile (**Table 3**). The CART indicates that if the value of the 75th-percentile fat emboli area is greater than 140 pixels in the animal studied (cutoff value), the probability of having been hit by a vessel is high, and so the animal is assigned to the strike group. If the value of the area occupied by fat emboli in the 75th-percentile is lower than 140 pixels, and the animal is a calf, it is also assigned to the strike group. If none of the previous conditions are met, the animals are assigned to the non-strike group (p < 0.001) (**Table 3** and **Figure 4**). The sensitivity and the specifity were 89% (52–100; 95% CI) and 100% (78–100; 95% CI), respectively.

FIGURE 4 | Result of the classification and regression tree to determine the cut off for ship-strike probability of the studied sperm whales. A high or low probability of ship strike was established according to: first, the fat emboli-P75 value and secondly, being a calf or not a calf.  Its sensitivity is 89% (95% CI = 52–100%) and its specificity 100% (95% CI = 78–100%).

### Factors Related to Ship Strikes in the Canary Islands

Most sperm whales with evidence of ship-strike were calves (10/16; 62.5%), followed by juveniles (3/16; 18.75%), adults (2/16; 12.5%) and subadults (1/16; 6.25%). All the adults/subadults included in this study were females.

Most of the animals with evidence of ship strike appeared floating or stranded along the east coast of Tenerife (56.25%), followed by the east coast of Gran Canaria (18.75%), east coast of Fuerteventura (12.5%), and finally east coast of El Hierro (6.25%) and west coast of Lanzarote (6.25%) (**Figure 5**).

### DISCUSSION

### Presence of Fat Embolism and Its Significance in Ship Strikes

The lack of detectable fat emboli in lung tissue of most control sperm whales suggests that fat embolism is not a physiological or common finding in lungs of stranded sperm whales. In addition, the presence of abundant OsO4-positive fat emboli in most sperm whales with evidence of ship-strike indicates an association with trauma. The etiology of fat emboli in the blood stream may be trauma- or non-trauma related (Glover and Worthley, 1999). Trauma conditions may include marrow-containing bone fractures or adipocyte-rich soft tissue injuries (Watson, 1970; Fulde and Harrison, 1991;

Gupta and Reilly, 2007). Both possibilities likely coexisted in our cases with evidence of ship-strike. The presence of fat emboli in the lung microvasculature indicates that the animal was alive at the moment of the strike and that cardiovascular collapse did not ensue immediately with successful pulmonary irrigation for an unknown period of time.

In addition to fat emboli, other typical findings of antemortem ship strike in cetaceans include subcutaneous, muscular and/or internal hemorrhage with hematoma formation, organ contusion and/or rupture with bleeding, e.g., in airways, in gastrointestinal tract, and edema in various organs mainly due to increased hydrostatic pressures, increased permeability due to hypoxia and vascular disruption (Campbell-Malone et al., 2008; Moore et al., 2013). Traumatic injuries on the dorsum are usually considered as antemortem or perimortem as carcasses tend to float with the ventral or lateral side upward, making a dorsal strike of a carcass unlikely (Laist et al., 2001; Campbell-Malone et al., 2008). On histopathologic examination, the presence of inflammatory response, hemorrhage or edema (Campbell-Malone et al., 2008; Moore et al., 2013), as well as acute, monophasic myocyte (segmentary, discoid) degeneration, contraction band necrosis, and/or fragmentation of the myofibers in the skeletal muscle (Sierra et al., 2014) support antemortem trauma.

Nevertheless, when working with decomposed carcasses it is not always feasible to assess many of the ship strike evidences described above. It is in these cases, where the detection of fat emboli in the lungs has proven to be a valuable and reliable confirmatory diagnostic tool, allowing us to conclude that, at least, 83% of the studied stranded sperm whales in the Canary Islands with evidence of ship strike were alive at the moment of the strike.

All the same, the methodology for fat emboli detection is not devoid of certain limitations that may lead to an underestimation of fatal vessel strikes, such as the slanted and arbitrary sampling of lung tissue. Kinra and Kudesia (2004), suggested that fat emboli are not homogenously distributed along lung tissue. Although different lung areas, including cranial, medial, and caudal samples from both lungs should be routinely collected during the necropsy, there is not a specific sampling protocol to accurately assess lung fat emboli. Thus, results from small lung portions taken arbitrarily should be carefully interpreted as they may not be representative of the whole tissue.

Microscopically, the severity of fat embolism has been traditionally assessed using a simple scale based on the number of emboli encountered in the tissue section studied (Saukko and Knight, 2004). Here we proposed and evaluated fat emboli area as a better estimator to assess fat emboli severity since the same number of emboli in two different lung histological sections may occupy different areas, and the one with the largest area occupied, would be a more severe case.

The rule developed for our samples based on the area occupied by fat emboli allowed us to discriminate between sperm whales that suffered strikes from those that died due to other causes, even when fat emboli was present in some animals of the control group (Cases 21 and 24). In these two cases, there was a blunt trauma of unknown origin. Possible etiologies included intra- or interspecific interactions or a potential livestranding event (Díaz-Delgado et al., 2018). Intra-/interspecific traumatic interactions are frequent among cetaceans, and may result in blunt traumas where internal hemorrhages and/or bone fractures may occur (Arbelo et al., 2013; Díaz-Delgado

et al., 2018). In the case of sperm whales, they have been observed being attacked by killer whales (Orcinus orca) or male sperm whales fighting with each other (Whitehead, 2009).

When relating the severity of fat embolism and the severity of the trauma a general positive correlation was established by Emson (1958) based on the type and number of bones fractured of 100 patients who died after injury. On the contrary, we did not find any association between variables related to trauma (i.e., presence of fractures or location of the trauma) with fat embolism severity. This could be due to the low sample size, heterogeneous distribution of fat emboli, methodological bias, immediate cardiovascular collapse with none or little pulmonary irrigation post-trauma (sudden death), or to the fact that the strike occurred post-mortem. Fatal lesions, often involving direct cardiovascular trauma with or without rupture of large vessels (hypovolemic shock) and/or severe neurogenic dysfunction, may cause an abrupt death, leading to immediate cease of the blood, and could explain the absence of fat emboli in different body organs, including the lung. This has been documented in aircraft fatalities, were extensive injuries were associated with lower grades of fat embolism (Mason, 1962), or no emboli at all in disintegration cases (Kinra and Kudesia, 2004), showing the importance of intact circulation for the formation of fat emboli. We surmise rapid cardiovascular collapse could explain lack of detectable fat emboli in three of our cases (cases 7, 10, and 13). These animals presented severe injuries, including abdominal evisceration or caudal amputation (Díaz-Delgado et al., 2018).

### Factors Related to Ship Strikes in the Canary Islands

All the sperm whales included in this study, were either female adults/subadults, or juveniles or calves, of any sex. This is in agreement with the fact that sperm whale females and their progeny composed the main groups present all year round in Canarian waters, which are considered nursery and breeding areas (André, 1997).

The fact that young animals are not fully adapted to dive and need to spend more time at surface, together with their relatively slow swimming speed compared to adults, may explain their higher vulnerability to ship strikes (Papastavrou et al., 1989; Laist et al., 2001; Whitehead, 2009). Mothers with recent calves (cases 6 and 7) may be also at higher risk as they will spend more time in the surface with their offspring.

A previous study estimated the absolute abundance and density of sperm whales in Canarian waters, and concluded that the species would not be able to sustain the current level of strikes (Fais et al., 2016). This impact is aggravated by the female philopatry in the Canaries, as they are not genetically connected to west North Atlantic populations (Alexander et al., 2016), and by the number of calves and reproductive females affected by strikes.

Most struck sperm whales appeared in the east coast of Tenerife, in agreement with previous studies (André, 1997; Carrillo and Ritter, 2010; Ritter, 2010). A major explanation for this is that the channel between Tenerife and Gran Canaria is a prime habitat for sperm whales in the Canaries (André, 1997; Fais et al., 2016), as well as an area with a high maritime traffic density, dominated by fast and high speed ferries (Ritter, 2010). An overlap between most of the sperm whales' stranding locations and fast-ferry transects was also observed in the present study.

To conclude, this study provided compelling histochemical evidence of fat emboli as a reliable confirmatory diagnostic tool of ante-mortem ship-strike even in decomposed sperm whale carcasses. Our results demonstrated that most of the sperm whales with evidence of ship-strike and stranded in the Canaries were alive at the moment of the strike. However, this may be an underestimation as cases where immediate cardiovascular collapse (sudden death) occur, may lack detectable fat emboli in the lungs. A final diagnosis of antemortem ship-strike may considerably benefit from fat emboli detection in lung tissue, particularly when other trauma-related gross and microscopic findings are not evident.

Some future directions may include the study of fat emboli distribution within the lungs to determine if some areas are more affected by fat emboli, and based on the results, the development of a homogenized lung sampling protocol to detect fat emboli. Alternative techniques to osmium tetroxide, which is extremely toxic, should be developed to study lipids histologically. Lipid composition analyses of fat emboli may contribute to a better understanding of its pathogenesis in these animals.

Some mitigation measures have been implemented in other locations and have proven to be effective, such as a mandatory vessel-speed restriction in the United States East Coast (Conn and Silber, 2013), the establishment of Traffic Separation Schemes (TSS) in the Bay of Fundy (Vanderlaan et al., 2008) or the proposal of recommended Areas To Be Avoided (ATBA) like the Roseway Basin Area (Vanderlaan and Taggart, 2009). Similarly, mitigation measures to reduce ship-strike mortalities and guarantee the survival of the sperm whales' population in Canarian waters should be further explored and implemented.

#### DATA AVAILABILITY

All datasets generated for this study are included in the manuscript and/or the supplementary files.

### ETHICS STATEMENT

All animals included in the present study were dead, either floating offshore or stranded in the coast. Required permission for the management of stranded cetaceans was issued by the environmental department of the Canary Islands' Government and the Spanish Ministry of Environment. No experiments were performed on live animals.

#### AUTHOR CONTRIBUTIONS

fmars-06-00379 July 2, 2019 Time: 17:43 # 9

AF: conceptualization. MArb, ES, YBdQ, JD-D, CS-S, RP-L, and MArr: sampling. MArr: laboratory analyses. PS, MArr, and YBdQ: data analyses. AF: funding. MArr: writing. All authors: review and editing. YBdQ and AF: supervision.

#### FUNDING

This study was funded by the National Project CGL2015/71498P and the Canary Islands Government, which has funded and provided support to the stranding network. MArr was funded by the University Professor Formation fellowship from the Spanish Ministry of Education (FPU; 15/02265). YBdQ was funded by

#### REFERENCES

a postdoctoral fellowship from the University of Las Palmas de Gran Canaria. JD-D was the recipient of a postdoctoral fellowship by the São Paulo Research Foundation (FAPESP; Grant #2017/02223-8).

#### ACKNOWLEDGMENTS

The authors thank the Electronic Microscopy Service in the Faculty of Health Sciences (University of Las Palmas de Gran Canaria), all the members and volunteers of the Cetacean Stranding Network, Marisa Tejedor and associated nongovernmental organizations: SECAC and Canary Conservation. The authors also thank Ana María Alfonso for technical assistance. MArb is also a co-corresponding author.

whales. Conserv. Biol. 23, 1467–1474. doi: 10.1111/j.1523-1739.2009. 01329.x

**Conflict of Interest Statement:** The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2019 Arregui, Bernaldo de Quirós, Saavedra, Sierra, Suárez-Santana, Arbelo, Díaz-Delgado, Puig-Lozano, Andrada and Fernández. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

# Monitoring of Marine Mammal Strandings Along French Coasts Reveals the Importance of Ship Strikes on Large Cetaceans: A Challenge for the European Marine Strategy Framework Directive

#### Edited by:

Joshua Nathan Smith, Murdoch University, Australia

#### Reviewed by:

Caterina Lanfredi, Consorzio Nazionale Interuniversitario per le Scienze del Mare (CoNISMa), Italy Francine Kershaw, Natural Resources Defense Council, United States

#### \*Correspondence:

Hélène Peltier<EMAIL_ADDRESS><EMAIL_ADDRESS>
#### Specialty section:

This article was submitted to Marine Conservation and Sustainability, a section of the journal Frontiers in Marine Science

Received: 07 February 2019 Accepted: 18 July 2019 Published: 31 July 2019

#### Citation:

Peltier H, Beaufils A, Cesarini C, Dabin W, Dars C, Demaret F, Dhermain F, Doremus G, Labach H, Van Canneyt O and Spitz J (2019) Monitoring of Marine Mammal Strandings Along French Coasts Reveals the Importance of Ship Strikes on Large Cetaceans: A Challenge for the European Marine Strategy Framework Directive. Front. Mar. Sci. 6:486. doi: 10.3389/fmars.2019.00486 Hélène Peltier1,2 \*, Alain Beaufils3 , Catherine Cesarini4 , Willy Dabin1 , Cécile Dars1,2 , Fabien Demaret1,2, Frank Dhermain5 , Ghislain Doremus1 , Hélène Labach5 , Olivier Van Canneyt1 and Jérôme Spitz1

1 Observatoire Pelagis, UMS 3462, Université de La Rochelle – CNRS, La Rochelle, France, 2 ADERA, Pessac, France, 3 Association CHENE, Allouville-Bellefosse, France, 4 Cétacés Association Recherche Insulaire, Corte, France, 5 Groupe d'Etude des Cétacés de Méditerranée, Sausset-les-Pins, France

The incidence of marine traffic has risen in recent decades and is expected to continue rising as maritime traffic, vessel speed, and engine power all continue to increase. Although long considered anecdotal, ship strikes are now recognized as a major threat to cetaceans. However, estimation of ship strike rates is still challenging notably because such events occurred generally far offshore and collision between large ships and whales go often unnoticed by ship crew. The monitoring of marine mammal strandings remain one the most efficient ways to evaluate the problem. In France, a national coordinated network collected data and samples on stranded marine mammals since 1972 along the Mediterranean and Atlantic French coasts. We examined stranding data, including photography and necropsy reports, collected between 1972 and 2017 with the aim to provide a comprehensive review of confirmed collision records of large whales in France. During this period, a total of 51 ship strike incidents were identified which represents the 1st identified causes of mortality for large whale in France. It has increased since 1972 with seven records during the 1st decade to reach 22 stranded animals observed between 2005 and 2017. This issue appears particularly critical in the Mediterranean Sea where one in five stranded whales showed evidence of ship strike. This review of collision records highlights the risk of a negative impact of this anthropogenic pressure on the dynamic of whale populations in Europe, suggesting that ship strike rates could not allow achieving the Good Environmental Status of marine mammal populations required by the European Marine Strategy Framework Directive.

Keywords: ship strikes, fin whales, sperm whales, strandings, monitoring, MSFD

### INTRODUCTION

fmars-06-00486 July 30, 2019 Time: 15:35 # 2

Marine traffic exerts a growing pressure on marine megafauna. Ships and other sea-faring vessels cause chemical pollution, modification of habitats and animal behavior (including through noise disturbance) as well as direct injuries through collisions with animals (Pirotta et al., 2018). Although long considered anecdotal, ship strikes are now recognized as a major threat to cetaceans (Kraus et al., 2005; Douglas et al., 2008). Any vessel type may be involved in ship strikes, including tankers, cargo or cruise ships, ferry boats, whale watching vessels, and sailing vessels (Laist et al., 2001; Ritter, 2012). Ship strikes occur worldwide and have been reported in at least 11 large whale species (Laist et al., 2001). Several hotspots have been identified across the world where ship strikes seriously threaten the conservation status of whale populations, e.g., northern right whales in the Western North Atlantic, blue whales around Sri Lanka and fin whales in the Mediterranean Sea (Cates et al., 2017). The incidence of ship strikes has risen in recent decades and is expected to continue rising as maritime traffic, vessel speed, and engine power all continue to increase (Laist et al., 2001; Douglas et al., 2008).

A thorough understanding of the incidence and future threat of ship strikes is of major importance for large cetacean conservation but is challenging to achieve. Relatively little is known about the geographic distribution of ship strikes and the magnitude of their impact. The scarcity of direct reports and relevant data makes it challenging to provide quantitative indicators of absolute mortality at sea. The best source of information available on ship strike fatalities is the examination of stranded cetaceans (Laist et al., 2001).

Understanding the pressures faced by marine wildlife and implementing plans to mitigate them are crucial to achieving and maintaining a Good Environmental Status (GES) of European waters - the aim of the Marine Strategy Framework Directive (MSFD, 2008/56/EC). Good Environmental Status is defined as "the environmental status of marine waters where these provide ecologically diverse and dynamic oceans and seas which are clean, healthy and productive". In order to understand the future threat of anthropogenic pressures, like the "extraction of, or mortality/injury to, wild species, (by commercial and recreational fishing and other activities)" (2008/56/EC, Annex III), we need to study their impact on populations in the past and present, and project the observed trends into the future. For cetaceans, this requires the efficient monitoring of populations and the development of quantitative indicators that reveal the degree to which human activities impact these populations (Santos and Pierce, 2015; Authier et al., 2017).

We review five decades of whale stranding data collected along the French coasts in order to document the importance of ship strikes on populations of large whales and provide baseline data for future assessments. This is a step toward the development of a ship strike mortality indicator, which would serve as a means to better understand the importance of ship strikes in European waters in the future and identify ways to mitigate them in context of GES achievement through the MSFD.

#### MATERIALS AND METHODS

Stranding data was collected by the French National Stranding Network following standardized observation and sampling protocols set in place in the 1980s. This network is made up of around 400 trained volunteers distributed along the coasts of mainland France. Examination protocols include taking external measurements, photographs, and observations of all stranded cetaceans. According to the accessibility and the decomposition status of carcasses, tissues are regularly but not systematically sampled and examined (blubber, skin, internal organs, muscles, and skeleton).

Ship strike was determined as the cause of death if animals were recovered on ship bows or behind propellers, or with strong evidence of ship strikes. Evidence of ship strike includes: deep propeller cuts, significant bruising, oedema, internal bleeding radiating from a specific impact site, fractures and ship paint marks (Jensen and Silber, 2004; Douglas et al., 2008).

Observation effort has been stable since the late 1980s (Authier et al., 2014), so trends can therefore be interpreted with greater confidence for the last three decades. The earlier stranding records (1972–1982) must be carefully interpreted.

Because of low number of records, data were collated in histograms by 10-year intervals to improve the understanding of trends. Spatially, results are described following different marine sub-areas used in MSFD: the Western Mediterranean Sea (WMS), the Bay of Biscay (BB), the Celtic Sea (CS) and the Channel and North Sea area (CNS).

### RESULTS

#### Species Composition of Strandings

A total of 396 large whale strandings were recorded in France between 1972 and 2017, of which 51 (12.9%) were diagnosed as being caused by ship strikes (details provided in **Supplementary Table S1**). Balaenopterids represented 79.5% of the total strandings, 315 in total, and sperm whales represented the remaining 81 strandings (20.5%). Ship strike incidents included 39 fin whales (76.5%), 4 minke whales (7.8%), 2 humpback whales (3.9%), 4 sperm whales (7.8%) and 2 unidentified baleen whales (3.9%). Of the fin whales killed by ship strikes, 16 were males, 13 females, and 9 were not identifiable. The average length of males was 14.6 m (± 3.5 m) and 16.1 m (± 2.6 m) for females.

Due to the high representation of fin whales in the total sample of ship strike events (83% of balaenopterids), all balaenopterids (fin whales, minke whales, humpback whales, and unidentified balaenopterids) were collated for analysis.

#### Temporal Trends

The total number of strandings have increased over the last 46 years for sperm whales in the Atlantic Ocean and Mediterranean Sea as well as balaenopterids in the Atlantic Ocean. Strandings of balaenopterids in the Mediterranean Sea increased steadily until the last decade during which the number of strandings slightly decreased (**Figure 1**).

as a proportion of all strandings are indicated.

Evidence of ship strikes were only reported for sperm whales in the last decade, while balaenopterid strikes are documented as early as 1972 and increased over the decades: a total 18 baleen whale strikes were reported along French coasts between 2005 and 2017 (**Figure 1**). The proportion of balaenopterid strandings caused by ship strike per decade was variable in the Mediterranean Sea (22.5% ± 7.3%) and increased over the decades along the Atlantic coast. The proportion of total strandings caused by ship strikes remained stable over the decades. Ship strike induced strandings occurred throughout the year but more frequently between the months of July and November (67% of ship strike strandings) (see **Supplementary Table S1**).

#### Geographic Distribution of Ship Strikes

Strandings due to ship strike were more frequent along the Mediterranean coast than the Atlantic coast (**Figure 2**). 28 whales were struck and found stranded in the Mediterranean Sea (including 24 fin whales, one humpback whale and three sperm whales) compared to 21 whales in Atlantic Ocean and English Channel (15 fin whales, four minke whales, one humpback whale, and one sperm whale). The majority of ship strikes reported on the Mediterranean coast were recovered on the eastern part of the Gulf of Lion and the Ligurian Sea (97%), an area which includes the Pelagos Sanctuary.

#### DISCUSSION

Ship strikes were the predominant anthropogenic cause of death identified in large cetaceans along both Atlantic and Mediterranean coasts. This is in line with the results of studies in other parts of the world that report a direct correlation between the global increase of shipping activity, engine power, and vessel speed (Laist et al., 2001; Ritter, 2012; Cates et al., 2017). Vessel speed correlates positively with the probability of ship strikes and the severity of injuries (Vanderlaan and Taggart, 2007; Douglas et al., 2008; Ritter, 2012; Conn and Silber, 2013).

The increase of large whale strandings does not appear to be related to an increase in public awareness or reporting pressure, at least for the last three decades during which observation effort was stable. Temporal changes in strandings are therefore likely due to changes in cetacean abundance and distribution, and/or changes in the intensity of pressures (Peltier et al., 2012).

High densities of large cargo vessels in major shipping routes create a serious risk of ship strikes. The Ushant Traffic Separation

Scheme in the English Channel and the Mediterranean Sea are two of the most important waterways of the world (Lloyds Maritime and Intelligence Unit, 2008). Individuals injured in these shipping routes may, however, strand great distances from the location they were struck or never strand at all. One study described a fin whale carcass being dragged over 1100 km by a cruise ship after a ship strike (Laist et al., 2001). Therefore, despite stranding data being the best source of information available to determine ship strike incidence, the degree to which they are representative of actual ship strikes is limited and the threat of ship strikes may be under- or overestimated based on stranding numbers.

Based on their known distribution, fin whale densities were expected to be highest on the continental slope of the BB and the oceanic area of the Pelagos Sanctuary in the summer months, and absent in the English Channel (Laran et al., 2017a,b). The relative number of ship strikes in the English Channel may have been over-estimated: animals injured in adjacent areas of the Atlantic Ocean may have drifted to shores along the English Channel. Ship strikes in the BB may have been underestimated: the majority of collisions would likely have occurred in the dense shipping routes far from the coast beyond the continental shelf. Animals that stranded along the shores of the BB after collisions in these parts would have drifted long distances to the shores. The bad drift conditions in the BB in summer (Peltier et al., 2013) (when whale density and therefore collision risk is high) could have prevented some carcasses from reaching the coast at all. Moreover, because of the long travel time coupled with the aggravated decomposition of the carcass after blunt force trauma, the animals could have reached the shores in too bad a state to be able to identify evidence of ship strike.

Fin whales are of particular concern in French Mediterranean waters. A recent study estimated that the fin whale population

in the French Mediterranean Sea numbered only 2,500 individuals [CI 95% = 1472–4310] (Laran et al., 2017a) in the summer. The small population is characterized by limited gene flow (Palsbøll et al., 2004) and is thus particularly vulnerable to anthropogenic pressures (Panigada et al., 2006; Panigada and Notarbartolo di Sciara, 2012).

Aguilar et al. (1988) reported fin whale sexual maturity at a size of 17.4 m for females and 18.5 m for males. The majority of fin whales that stranded following a ship strike had not yet reached maturity: eight of the 13 females and 15 of the 16 males. Immature fin whales seem to be more vulnerable to ship strikes than mature animals, a result that is supported by the findings other studies (Laist et al., 2001; Panigada et al., 2006; Douglas et al., 2008). Laist et al. (2001) also reported that a high proportion (75%) of northern right and humpback whale fatalities due to ship strikes were calves and juveniles. Immature whales may be more naïve to ships and spend more time surfacing when vessels are in the vicinity.

Scientists need to identify the main pressures within each MSFD component in order to develop monitoring schemes and indicators to assess the condition of European marine environments, to evaluate the efficiency of mitigation measures, and to recover GES. A challenge for the second MSFD 6 years cycle will be to complete the currently used set of indicators (focused on cetacean abundance and distribution, bycatch, and contaminant issues) to allow for a broader assessment of species and the pressures they face, especially large whales (e.g., ship strikes). The development of quantitative indicators to monitor the levels and the impacts of ship strikes on large whale populations is vital for future cetacean studies under the MSFD. Such indicators could document the criteria on biodemographic parameters (called D1C3), which require estimating mortality rates.

In the context of the next GES assessment in 2024, the proper assessment of ship strike mortality on cetacean populations in European waters through the MSFD requires: (1) the stimulation of transboundary collaboration at a basin scale to collect enough standardized data over a large enough area to be relevant for such large and mobile species (Authier et al., 2017), and (2) the development and use of quantitative indicators and thresholds adapted to the low occurrence of ship strike records. Overcoming these challenges would be an important step in integrating ship strike risk and impact in the future assessment of GES for cetaceans.

#### ETHICS STATEMENT

This work was carried out in the respect of European regulation regarding the use of stranded dead cetacean for scientific and conservation purposes. The authors have therefore adhered to general guidelines for the ethical use of animals in research, the legal requirements in Europe. No living animals were used for this study, only dead cetaceans found stranded along European coasts by several organisations were considered. No samples were used for this study.

### AUTHOR CONTRIBUTIONS

HP performed the analyses and wrote the manuscript. WD, CD, FDe, GD, and OVC coordinated the French stranding network and collected the stranding data. AB, CC, FDh, and HL collected the stranding data. JS supervised and corrected the manuscript.

### FUNDING

The Observatoire Pelagis is funded by the French ministry in charge of the environment, the French Agency for the Biodiversity, and Communauté d'Agglomération de la Ville de La Rochelle.

### ACKNOWLEDGMENTS

We warmly thank all the members of the French National Stranding Network for their continuous effort in collecting the stranding data. In particular, we thank all the volunteers who examined the whales: Stéphane Auffret (Ocarium), MNH Le Havre, Université de Corse, CROSSMED, Eric Poncelet (CRMM), Jean-Roch Meslin (RNE 17), M. Capoulade (SNCM), Laurence Micout (GECEM), Pascal Jasek (GECEM), Jean-Louis Cyrus (MHN Marseilles), Fabrice Roda (ONCFS), CMNF, LPA Calais, Thierry Jauniaux (Marin), Nowosad, Douanes du Havre, Françoise Passelaigue (GECEM), Joël Pourreau (RNE 44), Navire Mega Express, Navtex, NGV Liamone, NGC Asco, Vincent Ridoux (Observatoire), Prefecture Maritime de Cherbourg, Prefecture Maritime de la Manche, Franck Dupraz (GECEM), Gérard Gautier (Aérobaie), Stephane Beillard (ONCFS), Ludivine Martinez (Observatoire Pelagis), Gilles Le Guillou (La Maison de l'Estuaire), OCEAMM, Catherine Retore (GECEM), Parc Marin Côte Bleue, Anthony Le Doze (Syndicat Mixte Gâvres Quiberon), François Gabillard (GMN), Laurence Gonzalez (Observatoire Pelagis), André Agullo (ONCFS), Alain Cauzid-Esperandieu (ONCFS), Caroline Gioan (GECEM), Virginie Garcia-Rog (ONCFS), Jean-Jacques Boubert (RN Banc d'Arguin), Roland Mirtain (RNE 33), Fréderic Blondy (ONCFS), Gaëlle Jaffre (Syndicat Mixte Gâvres Quiberon), Marie Kerdavid (Syndicat Mixte Gâvres Quiberon), Pierre Moisson (CARI), Thomas Abiven (ONCFS), François Lescuyer (RN Camargue), Silke Befeld (RN Camargue), Jérémy Nemoz (Seaquarium), Jean-Baptiste Senegas (Seaquarium), Laure Prevost (CHENE), and Damien Le Guillou (CHENE).

### SUPPLEMENTARY MATERIAL

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fmars.2019. 00486/full#supplementary-material

TABLE S1 | Details of the 51 large whale strandings with evidence of lethal ship strikes along the coasts of mainland France for different marine sub-areas between 1972 and 2017. Total numbers par MSFD reporting cycles according to marine sub-regions are presented [number of individuals (reporting cycle)].

### REFERENCES

fmars-06-00486 July 30, 2019 Time: 15:35 # 6

**Conflict of Interest Statement:** The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2019 Peltier, Beaufils, Cesarini, Dabin, Dars, Demaret, Dhermain, Doremus, Labach, Van Canneyt and Spitz. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

# The Assessment and Management of Marine Pest Risks Posed by Shipping: The Australian and New Zealand Experience

#### Keith R. Hayes1 \*, Graeme J. Inglis2 and Simon C. Barry3

1 CSIRO Data61, Hobart, TAS, Australia, 2 National Institute of Water and Atmospheric Research Ltd., Riccarton, New Zealand, 3 CSIRO Data61, Canberra, ACT, Australia

#### Edited by:

Jessica Redfern, Southwest Fisheries Science Center (NOAA), United States

#### Reviewed by:

Hanno Seebens, Senckenberg Biodiversity and Climate Research Centre, Germany Kevin Alexander Hovel, San Diego State University, United States

> \*Correspondence: Keith R. Hayes<EMAIL_ADDRESS>
#### Specialty section:

This article was submitted to Marine Conservation and Sustainability, a section of the journal Frontiers in Marine Science

Received: 23 April 2019 Accepted: 19 July 2019 Published: 06 August 2019

#### Citation:

Hayes KR, Inglis GJ and Barry SC (2019) The Assessment and Management of Marine Pest Risks Posed by Shipping: The Australian and New Zealand Experience. Front. Mar. Sci. 6:489. doi: 10.3389/fmars.2019.00489 Ships have been translocating species around the world for hundreds of years but attempts to understand and manage this issue date back only three decades. Here we review the assessment and management of risks from vessel biofouling and ballast water over this time period from an Australian and New Zealand perspective. We detail a history of successes and failures at the science-policy interface that include international guidelines for biofouling management and the recent ratification of a ballast water convention. We summarize the efficacy and costs of current treatment options, and highlight the practical challenges and policy implications of managing the diffuse and succinct bio-invasion risks that shipping creates pre- and post-border. We then use the lessons learnt over the last 30 years to recommend a future empirical strategy.

Keywords: marine pest, risk assessment, monitoring, ballast water, biofouling

### INTRODUCTION

The role of ballast and biofouling as vectors for the translocation of species globally has been known for over 60 years (Elton, 1958; Medcof, 1975). The magnitude of the consequences for human health, the economy and environment, however, was not widely publicized until the mid-1980s (Carlton, 1985; William et al., 1988). At this time, and in the decade that followed, the gravity of the problem was underlined by the introduction of Cholera to Peru (McCarthy and Khambaty, 1994), the global increase in the frequency, intensity and distribution of paralytic shellfish poisoning (Hallegraeff and Bolch, 1992), the role of the Atlantic comb jelly Mnemiopsis leidyi in the collapse of the Black Sea ecosystem (Shiganova, 1998), the economic and environmental impacts of the zebra mussel Dreissena polymorpha (Holland, 1993), and a growing awareness that the number of species being translocated around the globe was much larger than previously realized (Carlton, 1992).

The international community was initially quick to respond to the marine pest threat. In 1991 the Marine Environment Protection Committee (MEPC), a subcommittee of the International Maritime Organization (IMO), adopted the International Guidelines for Preventing the Introduction of Unwanted Aquatic Organisms and Pathogens from Ships Ballast Water and Sediment Discharges (**Figure 1**). Progress after that was significantly slower. The MEPC guidelines began a series of international efforts to manage ballast water. It took 13 years, however, before the International Convention for the Control and Management of Ships' Ballast Water and Sediments

was adopted by the IMO in 2004, and another 13 years before the convention was ratified in September 20171 .

Policies that seek reasonable assurance of a net benefit must balance the often readily quantifiable costs of management against the more uncertain economic, environmental and health benefits. Scientific risk assessment is often used to help find this balance. Whilst some cost-benefit calculations for ballast water management suggested clear net benefits (World Wildlife Fund, 2009), uncertainty around this process contributed to the delay between recognizing the ballast water threat and managing it.

The principle of risk versus return is implicit in the ballast water convention. A key component is regulation A-4 which lays out the nature of exemptions that can be given to vessels. These require the application of defined risk analysis methods which are described in Guideline G7, significant elements of which reflect thinking and approaches that were originally developed in Australia and New Zealand. Both countries were leaders in introducing controls to manage the risks posed by introduced marine species. This was supported by their well-developed terrestrial biosecurity systems and island status which reduces certain complications faced by other jurisdictions.

The recent ratification, and entry into force, of the convention provides an impetus to review current knowledge around the risk-based management of marine pests. In the 15 years since the convention was adopted, Australian and New Zealand authorities have gained significant practical experience in applying different risk assessment techniques, and theoretical developments in estimating risk have taken place. This paper performs that review. It considers risk management for threats posed by both hull fouling and ballast water and for completeness considers the risk-based management of both domestic and international ballast water. We first review the Australian and New Zealand experience of using risk-based approaches, and then propose a conceptualization of the problem that is consistent with the convention but respects the relevant uncertainties and knowledge. We close by discussing the implications of this conceptualization and recommend future research directions.

#### RISK ASSESSMENT AND MANAGEMENT

#### Ballast Water

At the outset of the marine pest issue, scientists and regulators naturally looked to existing analogs for guidance on how risk assessment for marine pest introductions might be conducted. Many analysts (including ourselves) turned to three situations that, at least initially, looked analogous to the problem of risk assessment for marine pest incursions via ballast water and biofouling: (i) assessing the pre-border risk posed by accidental introductions of pests of agricultural production systems, including aquaculture; (ii) the risk of spread and impacts following post-border outbreaks of pests in these systems; and (iii) pre-border assessments of the incidental risks posed by deliberate introductions of biocontrol agents.

With exception of biocontrol agents, where assessment requirements and guidelines were developed relatively late (Barratt et al., 2010), risk guidelines and procedures were well established for each of the other situations, and this material often carried the imprimatur of respected national and international organizations (Kohler and Stanley, 1984; Kellar, 1993; Morley, 1993; Office International des Epizooties, 1996; Food and Agricultural Organization, 2006).

A common feature of these guidelines and procedures was that each adopted a species-specific perspective to the risk assessment problem, advocating that each assessment be treated on a case-bycase basis, using the characteristics of the species and receiving environment to guide the assessment process. Unsurprisingly, species-specific approaches for risk assessment of pests associated with biofouling and ballast water were identified as a possible approach to vector management, in-keeping with international expectations for trade.

There were, nevertheless, some misgivings about this approach at the time. Public submissions to a 1996 New Zealand government discussion paper on proposed regulatory approaches for the management of ballast water and biofouling highlighted the lack of detailed information available to underpin species-specific assessments, including on the species likely to be transported into New Zealand, the prospects for their establishment and likely consequences (New Zealand Government, 1998).

In the absence of this information, the Government supported a precautionary approach which assumed that all ballast discharges from vessels entering New Zealand could contain unwanted species, and in May 1998, New Zealand was among the first countries to implement mandatory requirements for ballast water management that reflected the three management actions – mid-ocean exchange preferably 200 nautical miles from land and in water over 200 m deep, onboard treatment, or discharge to an on-shore facility – identified in the 1991 IMO guidelines, without any provisions for exemption based on risk assessment (McConnell, 2002). Australia implemented similar mandatory requirements for international ballast water in July 2001 (**Figure 1**), but also sought to offer exemptions based on a species-specific, risk-based, Decision Support System, supported by a target-species list and port baseline surveys (McConnell, 2002; Hayes and Sliwa, 2003; Campbell et al., 2007) due to concerns about the feasibility and cost of midocean exchange, particularly for domestic voyages between Australian ports.

Species-specific methods were not the only approach advocated for biofouling and ballast water risk assessment. Carlton et al. (1995) raised the notion that environmental distance could act as a proxy for probability of survival, suggesting that translocations of ballast water between saline and fresh water, and between polar and tropical, environments would be safe because of the severe environmental dissimilarity between source and recipient regions. Hilliard and Raaymakers (1997) extended this idea and proposed a method of assessing ballast water risks based almost entirely on the environmental distance between the source and recipient ports measured with 37 variables, rather than just temperature and salinity.

1http://www.imo.org/en/About/Conventions/ListOfConventions/Pages/ International-Convention-for-the-Control-and-Management-of-Ships'-Ballast-Water-and-Sediments-(BWM).aspx

Considerations and recommendations for how to conduct risk assessments using both species-specific approaches and environmental matching, for journeys within and between bioregions, were eventually published by Barry et al. (2008). Early drafts of this document were shared with members of some of the national delegations to the MEPC, and the overall approach and recommendations were taken up in the IMO G7 Guidelines for ballast water risk assessment (Marine Environment Protection Committee [MEPC], 2007). The guidelines provided for three types of assessments – environmental matching, species-specific and species' biogeography – and were subsequently revised in 2017 to include the concept of "Same Risk Area" to recognize the possibility of species-specific, low risk scenarios where target species are already present in all ports within an area or had a high probability of establishing in all locations via natural dispersal (Marine Environment Protection Committee [MEPC], 2017).

Importantly, when the IMO guidelines were released only one (mid-ocean exchange) of the three management options identified by the guidelines was practically available because no shipboard treatments were available globally and no shorebased reception facilities were approved in either Australia or New Zealand. There was therefore some trepidation among Australian and New Zealand officials at this time that each country's trading partners might not accept blanket regulation on ballast water discharges because of the possible ramifications for trade (New Zealand Government, 1998). Many other countries, however, adopted similar regulations (Bailey, 2015) and midocean exchange quickly became standard practice, routinely performed by international vessels whenever journey conditions permitted. According to information provided to the Australian Decision Support System, for example, virtually all international vessels arriving in Australia were able to complete mid-ocean exchange in accordance with the guidelines.

A strong rationale for risk-based exemptions from the blanketmanagement described in the guidelines remained, however, for vessels undertaking short coastal journeys between ports within the same nation, or in other regions such as the North Sea and Baltic Sea, where it was not possible to meet the D-1 performance standard because there was not enough time, depth or distance to perform 95% volumetric exchange of ballast in water 200 m deep and/or more than 200 nautical miles from shore (Behrens et al., 2005; David et al., 2013). In Australia, target species risk-based management shifted focus to domestic ballast water transfers, culminating in the Australian Domestic Ballast Water Risk Assessment tool2 .

#### Biofouling

Biofouling threats were originally conceived as arising primarily from fouling organisms that accumulated over time on a vessel's hull. Biofouling increases frictional drag which adversely impacts the vessel's performance (Schultz et al., 2011), hence it is standard practice for marine coatings to be applied to vessel hulls at intervals of between 18 months to 5 years to prevent corrosion and retard biofouling growth (Almeida et al., 2007). Coatings are tailored to the operational profiles of different vessel types to maximize performance and to extend the time the vessel can remain in the water.

Empirical analysis of vessel biofouling confirms that the amount of fouling material on submerged surfaces is correlated

2http://www.agriculture.gov.au/biosecurity/avm/vessels/ballast#quick-domesticballast-water-risk-assessment-tool

to the number of days since the vessel was last cleaned and antifouled and the pattern of use of the vessel, including how often it is used and any significant periods of lay-up, but the effect of the last two factors may vary according to vessel type, the type of anti-fouling paint used, and how good the coating application was (Floerl et al., 2005; Davidson et al., 2009; Inglis et al., 2010; Lacoursière-Roussel et al., 2012; Lane et al., 2019).

Biofouling on the hulls of commercial and recreational vessels can be managed if owners apply anti-fouling coatings that suit their vessel's operational profile, and perform regular maintenance in accordance with the manufacturers specifications (Davidson et al., 2016). Biofouling, however, is not evenly distributed over the hull, but tends to be most abundant in areas where the anti-fouling coatings are damaged or degraded and in recesses that are protected from the drag created by the vessel moving through the water ("niche areas") (Hayes, 2002). On modern merchant vessels, these niche areas can comprise up to 27% of the wetted surface area of a vessel (Moser et al., 2017) and contain >80% of the biofouling on a vessel (Coutts and Dodgshun, 2007; Inglis et al., 2010).

Concerns about vessel biofouling risks and the problem of niche area fouling were raised by Australia, New Zealand and Friends of the Earth International in 2005 at the 54th session of the IMO MEPC. In 2007, the MEPC approved the development of international measures for minimizing the transfer of invasive aquatic species through biofouling as a new high priority item in the work program of the Bulk Liquids and Gases Sub-Committee. The resulting Guidelines for the Control and Management of Ships' Biofouling to Minimize the Transfer of Invasive Aquatic Species (Marine Environment Protection Committee [MEPC], 2011) were subsequently adopted by MEPC for commercial vessels in 2011 [MEPC.207(62)] and recreational craft in 2012 (MEPC.1/Circ.792).

The MEPC biofouling guidelines present best practice for choosing, applying and maintaining anti-fouling systems for vessels and include recommendations for regular inwater inspection and cleaning of problem areas, training and record keeping. Member States were requested to take urgent action to apply the guidelines and to report back to MEPC on experience gained through their implementation (MEPC.1/Circ.811). Although voluntary, the guidelines do not preclude individual States from applying other mandatory measures to provide additional protection from invasive biofouling species within their jurisdiction.

In 2004, the New Zealand government commissioned a multi-year research survey of over 500 international merchant, recreational, passenger, fishing, and slow-moving vessels to characterize the biofouling risks associated with arriving vessels (Inglis et al., 2010; Piola and Conwell, 2010). The survey showed that most vessels (>70%) from all the major types examined conveyed some biofouling into New Zealand on arrival. Over 65% of the 187 biofouling species identified in the study were non-indigenous to New Zealand and >70% of them had not yet established in New Zealand (Inglis et al., 2010).

This research was used, with other sources of information, to inform a qualitative import risk analysis of vessel biofouling (Bell et al., 2011), which eschewed a species-specific approach in favor of analysis of risks from 20 broad taxonomic groupings of biofouling organisms. This was due to: (i) the large number of species that had been recorded from studies of biofouling worldwide (>2000); (ii) the relatively poor quality of information available on their global distributions, ecology and potential impacts; and, (iii) the difficulty in predicting from this large species pool which species may be problematic. Twelve of the 20 taxonomic groups that were assessed contained species adjudged to present non-negligible risks to New Zealand's marine ecosystems and for which risk management measures could be justified. This finding, and the need for a simple, streamlined clearance procedure for vessels at the border, meant that a precautionary approach was again proposed, with any macroorganisms found on the hull of an arriving vessel considered to be risk organisms (Bell et al., 2011).

Following the risk assessment recommendations, the New Zealand government initially proposed an Import Health Standard that required vessels arriving into New Zealand to meet a clean hull standard that was defined as having "no visible aquatic organisms on the hull, including niche areas, except as a slime layer". The practicality of the clean hull standard, however, was subsequently questioned during consultation because even well-maintained vessels will accumulate some biofouling while operational (Inglis et al., 2010).

The Import Health Standard was revised and released in May 2014 as a Craft Risk Management Standard with an initial 4-year lead-in period before becoming mandatory in 2018 (Ministry for Primary Industries, 2018). The "Clean hull" requirement was altered to allow some macro-fouling with the amount depending on the intended length of stay within New Zealand waters. These allowances were explicitly described as biofouling thresholds within the standard. Vessels intending to remain in New Zealand for more than 21 days or which intended to visit areas not designated as "Places of First Arrival" are permitted to have no more than a slime layer and goose barnacles present on any area of the hull and niches. Vessels visiting Places of First Arrival and intending to remain in New Zealand for less than 21 days are permitted an additional allowance of some early-stage macro-fouling, specifically macroalgae, barnacles, tubeworms and bryozoans. The standard specifies thresholds for the maximum allowable size (in the case of macroalgae), cover and richness of these four taxonomic groups on the wind/water line, general hull area and niches, with justification for these thresholds described by Georgiades and Kluza (2017).

Subsequent debate about the Craft Risk Management Standard has been mostly directed at the biofouling thresholds and their practicality. This debate, however, overlooks the sections of the standard that outline a range of acceptable measures for meeting the "Clean hull" standard (section 2.3). These include continual maintenance of the vessel in accordance with the MEPC 2011 biofouling guidelines, cleaning within 30 days of arrival in New Zealand, the application of approved treatments or submission of a Craft Risk Management plan that outlines steps taken to reduce risk sufficiently to meet the standard. In practice most vessels resort to these other forms of acceptable evidence to demonstrate compliance with the standard rather than the biofouling thresholds.

In Australia progress on managing biofouling lagged behind ballast water because: (i) it was considered, at least initially, to be adequately managed in commercial vessels by extant management practices; (ii) at least partially managed in the recreational sector by extant practice, and; (iii) because the stakeholder groups in the recreational sector are more diffuse and therefore more difficult to represent within the biosecurity governance arrangements of the time.

In 2011, Hewitt et al. (2011) completed a qualitative assessment of the likelihood of entry, establishment and impacts of more than 1781 individual biofouling species. They then identified 56 Species of Concern that were not currently known to be present in Australia, had a high probability of arriving in Australian waters as biofouling on international vessels and had the potential to cause unacceptable impacts to environmental, economic, social/cultural or human health values. Western Australia and the Northern Territory had corresponding schedules listing Species of Concern that currently include 82 and 44 species, respectively, (Northern Territory of Australia, 2009).

The Commonwealth Government of Australia subsequently released a Regulatory Impact Statement for consultation (Price Waterhouse Coopers, 2011) that proposed new regulations, whereby commercial and recreational vessels would be assessed using an online tool to assess biofouling risk. Vessels assessed as "high" or "extreme" risk would be subject to restrictions on the time they could operate at any one port (48 h), at a series of ports (8 days total) or within Australian waters (14 days). If the vessel was unable to conduct its business within these restrictions it would be required either to leave Australian waters or be subject to a hull inspection to determine if any quarantine pests (Species of Concern) were present.

In 2015, a national review of arrangements for marine biosecurity highlighted significant concerns among stakeholders about the species-based risk assessment and approach to biofouling regulation. High among these concerns were the costs of developing and maintaining lists of Species of Concern, the evidential basis for assessing risk and the administrative burden to vessel operators of implementing this regime. The review recommended biofouling requirements for international vessels that were more closely aligned to the (Marine Environment Protection Committee [MEPC], 2011) guidelines and to the approaches taken by New Zealand and California. A new Regulatory Impact Statement, issued in April 2019, reflects this outcome. It proposes three regulatory options for consideration, with the preferred option being the requirement for vessels to implement vessel-specific biofouling management practices consistent with the Marine Environment Protection Committee 2011 guidelines (Australian Government Department of Agriculture and Water Resources, 2019). These practices require vessels to develop and maintain a Biofouling Management Plan and BioFouling Record Book, without which vessels will be targeted for inspection on arrival and required to provide evidence that their biofouling risks had been "appropriately managed." The regulations also provide for a 5 year soft-start period, starting in September 2020, during which vessels without a BioFouling Management Plan may use other options, including treating or cleaning the hull and niche areas less than 30 days prior to arrival, to demonstrate effective biofouling management.

At a state level currently, only Western Australia and the Northern Territory have formal policies on biofouling. Vessels arriving to Western Australia ports from outside the state are required to ensure that marine pests and diseases are not being carried in biofouling and inspectors accredited by the West Australian Department of Fisheries routinely inspect vessels. This Department also maintains a voluntary, online risk assessment tool3 that allows operators of commercial vessels, non-trading, petroleum and commercial fishing vessels to assess the biofouling risk associated with any planned international or interstate movements, and thereby assist in the endorsement of any planned activities with the relevant state agencies.

### EFFICACY AND COSTS

#### Ballast Water Exchange

Shipboard studies of ballast water exchange show that the efficiency of volumetric exchange can vary from 66% to more than 99%, depending on ship type and method of exchange (Ruiz and Reid, 2007; Molina and Drake, 2016). Using the empty-refill method, exchange efficiencies typically exceed 98%, but if not managed correctly this method can create hazards for the vessel including instability and excessive shear forces on the hull (Endresen et al., 2004). Although safer, the flowthrough method can result in much lower exchange efficiencies because of mixing between the influent and effluent water (Noble et al., 2016). Meta-analysis of empirical studies shows that concentrations of zooplankton are reduced by both methods of ballast water exchange by between 34 and 100%, with higher variability in outcomes for protists, bacteria and virus-like particles (Molina and Drake, 2016).

Ballast water exchange involves two types of costs: (i) the cost of operating the pumps, including fuel, energy, labor, and maintenance; and, (ii) the opportunity costs associated with slowing ship speed or diversion to areas that meet the D1 Standard of the Ballast Water Management Convention. The pumping costs depend on the type and size of the vessel, the ballast tank configuration and the method of exchange. Arthur et al. (2015b) estimate the average operational cost of exchange for vessels entering Australia at between USD \$0.017 and \$0.029 per tonne, with an average cost per vessel of USD \$2790 for bulk carriers and USD \$2020 for other vessel types. The total annual cost of ballast water exchange by vessels entering Australia was estimated at USD \$29.3 million (Arthur et al., 2015b).

Costs associated with delay or diversion will vary according to the length of voyage and ship's ballast water capacity. For most vessels traveling to New Zealand from other overseas ports these are not likely to be significant because most routes allow sufficient time to perform exchange in suitable areas. For shorter, coast-wise voyages, however, they can be significant. For example, mandatory diversion of ships traveling between Australian ports to areas that are at least 50 nautical miles from the coast and

3https://vesselcheck.fish.wa.gov.au/

200 meters deep (i.e., less stringent than the D-1 standard) has been estimated to cost more than USD \$46 million per year (CIE, 2007).

#### Ballast Water Management Systems

To comply with Regulation D-3 of the Ballast Water Convention, ballast water management systems must have Type-approval from the Flag State administration. Type approval requires both land-based and shipboard testing of performance relative to the D-2 discharge standard (IMO, 2018a). As at January 2019, 14 administrations had advised Type approval of 76 ballast water management systems, 29 of which used active substances involving chemical or biological treatment (IMO, 2019). Although manufacturers continue to refine their systems to improve performance, a 2010 review of available technologies showed variable efficiency in removing dinoflagellates, phytoplankton and zooplankton from ballast water (Tsolaki and Diamadopoulos, 2010). Physical separation techniques (filtration and cyclonic separation) reduced concentrations by between 8 and 95% of original values. Mechanical treatments (ultraviolet, heat treatment and electric pulse applications) were generally more effective at reducing phytoplankton and zooplankton (reductions of 40% to more than 95% relative to controls) but less effective at treating dinoflagellate cysts (6–40% reductions). Treatments with active substances had the greatest efficacy, generally achieving reductions in excess of 80% across a range of organisms (Tsolaki and Diamadopoulos, 2010). Vessels entering the coastal waters of the United States are increasingly reporting the use of ballast water management systems but as of December 2015, 20 months before the Convention entered into force, they accounted for less than 2% of all ballast water discharged in the United States per month, (Davidson et al., 2017) whereas all ships must now meet the D-2 standard by the 8th September 2024.

The costs associated with ballast water management systems vary according to the type of system, vessel type and size, and whether it is to be installed on a new build or retrofitted to an existing vessel. King et al. (2012) reviewed information provided by vendors for a range of system types and ship types. Purchase prices of the units ranged between USD \$640,000 and \$947,000. Estimated costs of installation varied from USD \$27,000 to \$70,000 for new builds, depending on vessel type, and from USD \$48,000 to \$173,000 for retrofits. For most systems, the annual operating costs for maintenance were typically between USD \$9,000 and \$17,000, depending on vessel type and size, but technologies that used active substances had a much wider range (USD \$31,000–\$296,000) because the use of chemicals varied widely between different ship types and sizes.

#### Biofouling

In contrast to ballast water, there does not appear to be any comprehensive analysis of the compliance levels or efficacy of the Marine Environment Protection Committee 2011 biofouling guidelines. Guidance released in 2013 specified a range of performance measures for evaluation and a questionnaire pro forma to aid in the review (IMO, 2013). The MEPC has recently committed to review the guidelines in 2020–2021 based on these measures (IMO, 2018b). Data is emerging, however, in New Zealand. In 2015, the Ministry of Primary Industries initiated surveys of bio fouling on 40 arriving vessels to assess compliance with the (then voluntary) Craft Risk Management Standard. Thirty-nine vessels (greater than 95% of all arrivals) had some biofouling in niche areas and 16 (40%) were noncompliant with the short-stay biofouling thresholds (Kluza, 2018). Since the standard came into force in 2018, New Zealand authorities have taken action against 14 high-risk vessels, representing less than 1% of all arrivals. Six of these vessels were ordered to leave New Zealand waters within 24 h, while the others faced restrictions on the number of ports they could visit.

Section 7 of the MEPC biofouling guidelines recommends cleaning, maintenance and periodic inspection of ships to remove biofouling, which implies costs to vessel owners, operators and relevant authorities. Although technologies exist for in-water cleaning of vessels, most do not contain and capture material removed during the cleaning process so that biological material and contaminants from the anti-fouling coatings are released into the surrounding environment (Morrisey and Woods, 2015). As a result, in-water cleaning is banned or tightly regulated in many jurisdictions. The cost of removing the vessel to dry dock and applying anti-fouling coatings ranges from around USD \$100,000 per vessel weighing up to 5,000 tonnes to over USD \$464,000 per vessel (for vessels >200 meters in length) and may take 5–7 days with average opportunity costs per vessel per day of USD \$4,400 for bulk vessels, USD \$9,600 for general cargo vessels and USD \$11,200 for container vessels (Branson, 2012; Inglis et al., 2012).

Cost estimates for inspection regimes are currently more difficult to come by in part because there are no internationally agreed protocols for inspection and documentation of biofouling. The Australian 2019 Regulatory Impact Statement for biofouling management estimates that the additional dive time needed to add biofouling considerations to the scheduled class survey, inwater inspections (that occur on average once every 2.5 years) will cost AUD \$667, whereas specific in-water biofouling inspections are estimated to cost AUD \$7,000 per vessel (Australian Government Department of Agriculture and Water Resources, 2019). The statement also estimates that the regulatory burden of developing and maintaining a vessel's biofouling Management Plan and biofouling Record Book will be approximately AUD \$15 per vessel per year.

### PRACTICAL CHALLENGES AND THEIR IMPLICATIONS

Risk assessments for ballast water and biofouling face a number of similar challenges, with biofouling presenting additional difficulties because unlike ballast water, whose source can be determined relatively precisely, biofouling can be acquired from multiple locations during a vessel's in-service period, making its source pools harder to identify. Some of these challenges where foreshadowed by Simberloff (2006), and several others identified by Barry et al. (2008).

### Environmental Variables, Distance and Invasion Risk

Two primary problems occur with environmental matching: the choice of environmental variables, and the distance metric itself. Firstly, the analysis by Hilliard and Raaymakers (1997), and the GloBallast risk assessments that subsequently adopted this approach (for example Clarke et al., 2004) include a large number of variables in the distance calculation. Barry et al. (2008), however, demonstrate that introducing any environmental variables into the calculation that are not truly predictive of introduction or establishment success creates noise which diminishes the signal of the true predictive distance.

Secondly, environmental distance is not currently well calibrated with any of the potential ballast water risk assessment endpoints of survival, establishment or impact. Several studies use environmental distance to identify donor regions that may act as sources of successful invaders, or incorporate environmental distance into parameters of invasion models (see for example Keller et al., 2011; Seebens et al., 2013), but the empirical relationship between distance and survival or establishment of non-native species has not, in our opinion, been adequately determined. Furthermore, as Ruiz et al. (2013) demonstrate the relationship between these variables and historical introductions may no longer be discernible, and without systematic surveys the relationship into the future will remain obscured by uncertainty about the date of location, the source of inoculation and the responsible vector.

#### Data Needs and Saturation of Species-Specific Assessment

The primary problems associated with species-specific risk assessment are: (i) the potential for the risk assessment to identify all vessels as high risk (i.e., offer no potential for low risk outcomes) as more and more species potentially transported by the vector are added to the assessment - a process that we refer to as "saturation," (ii) the target species data needs and potential complexity of the modeling task; and, (iii) the availability and currency of information on the distribution of non-native species.

An analysis of an early proposal to develop a riskbased Decision Support System for international ballast water discharges in Australia showed that saturation can occur quite rapidly: 97% of international arrivals were deemed to be high risk with a target species list that was at that time restricted to only 12 species. This was largely due to the lack of information on the presence or absence of the target species in the international donor ports. In the absence of this information the risk assessment took a conservative approach and assumed target species were present, and risk reductions were not forthcoming in other parts of the assessment process.

Saturation did not occur, however, in the analysis of domestic ballast water translocations because the target list was smaller (reduced from 12 to 9), the Australian port baseline surveys (Campbell et al., 2007) and literature (for example Sliwa et al., 2008) provided better data on the distribution of non-native species in Australian ports, and risk reductions were forthcoming in the survival probability models that the assessment used.

The collation of data on the distribution and ecology of non-native species around the world (Katsanevakis and Roy, 2015) provides a growing information platform that can be used to populate parameters in species-specific risk assessment, such as the probability that the donor port contains a target pest. The number of different regional databases, only some of which are actively maintained, presents challenges, however, and the cost of acquiring information on the infection status of port, and maintaining the currency of this information, could become an important impediment to the long-term maintenance of species-specific risk assessments because: (i) as data ages the status of donor ports becomes increasingly uncertain; and, (ii) defensible (conservative) approaches to uncertainty lead to saturation.

Simberloff (2006) highlights a number of difficulties with species-specific approaches to invasion risk, in particular the data requirements, suggesting "Knowledge on most species is simply in-sufficient to enable more than educated guesses about the likelihood that a species will establish and impacts it might cause." Assessing the invasion risk of the Pacific oyster (Crassostrea gigas) through ballast water or biofouling highlights the data and modeling complexities that can arise: The risk assessment supporting the Australian ballast water Decision Support System minimizes the complexity of the modeling task by choosing a survival endpoint over the alternatives of establishment or impact (Hayes, 2003), on the grounds that the latter endpoints required more complex models, and for species deemed a priori to be environmental pests the probability of survival was sufficiently close to stakeholders' concerns to allow decision makers to make management decisions.

The probability of survival was assessed by simulating a species completing its life-cycle, and comparing the temperature tolerance at life-stage against simulated time series of daily temperature extremes in ports across Australia (Hayes et al., 2007, 2008). For sub-tidal species, the data and calculations proved tractable and have since been improved following an independent review (Arthur et al., 2015c). For inter-tidal species, such C. gigas, however, the analysis hit significant impediments. Firstly, the daily temperature regime experienced by inter-tidal organisms is substantially different to that of sub-tidal organisms because of their periodic exposure to the interacting elements of sunlight, wind speed and air temperate. Secondly, the body temperature of inter-tidal organisms is also influenced by body size and shape (Helmuth, 2002). These factors substantially raise the number of uncertain parameters in what was otherwise a relatively simple survival model. Whilst interest in these types of biophysical models is increasing in order to predict the effects of climate change (Levy et al., 2015), the data required to develop these types of models for target species is likely to be prohibitive.

#### Port Surveys

Species-specific risk assessments also require good information on the distribution of target species. Section 6.4.8 of the IMO G7 guidelines, for example, stipulates "if a target species is already present in the recipient port, it may be reasonable to

exclude that species from the overall risk assessment for that port unless that species is under active control." In effect, if all of the species that a vessel is assessed as being high risk against are already present (and not being actively controlled) in the recipient port, then the vessel defaults to low risk. Obviously, this approach makes no provision for species other than the target species, but it is based on the reasonable expectation that treatment costs should not be imposed on vessels if they are translocating species to locations where they already exist.

Section 6.4.8 can be problematic because of the high degree of power it imposes on the validity and currency of port survey information. In 1995 Australia embarked on a series of port baseline surveys following the "CRIMP protocols" (Hewitt and Martin, 1996, 2001). By 2005, 39 Australian ports had been surveyed to an accredited standard with these protocols, and the results entered into a National Port Survey Database (McEnnulty et al., 2005). The protocols were used extensively in New Zealand and elsewhere in the world, and have been the most widely implemented method of baseline survey for invasive species (Campbell et al., 2007).

The Australian baseline surveys helped define the distribution of non-native species in Australia. The surveys, however, are relatively expensive, and require a very high level of taxonomic expertise to successfully post-process the samples that are collected (Bishop and Hutchings, 2011). For example, only about 27% of the 15,412 taxonomic records in the Australian National Port Survey Database include a complete species name. The remaining records represent identifications to the level of Genus only (McEnnulty et al., 2005).

Australia responded to the requirement to maintain upto-date records of the distribution on non-native species in its ports by developing a set of port monitoring guidelines that stipulated not only which ports should be regularly monitored but also to what standard (Australian Government Department of Agriculture Fisheries and Forestry, 2010a,b). The guidelines identified 18 ports around Australia as the minimum required to form an effective National Monitoring System.

Many of these ports, however, are large, complex regions that are difficult to sample for reasons such as low visibility and/or strong currents. Furthermore, the sample sizes and hence costs of sampling these locations to a standard with high statistical power proved to be too high (reportedly between AUD \$175,000 and AUD \$355,000), to repeat on a regular basis, and only 5 of the 18 locations, together with seven other locations, were surveyed to the recommended standard.

A lack of clearly understood objectives among stakeholders, together with the high cost of the surveys, coinciding with a significant reduction in resources allocated to marine pest research and development in Australia at this time, stalled the implementation of the National Monitoring System, and as part of a wider review of Australia's marine biosecurity systems (Australian Government Department of Agriculture and Water Resources, 2015), it was recommended that the system be abandoned and replaced with a surveillance system

based on cheaper methods designed with clearer objectives (Arthur et al., 2015a).

One of the cheaper methods recommended by Arthur et al. (2015a) – the use of eDNA probes based on species-specific primers – holds promise but requires extensive testing to determine the relationship between presence and abundance of pests in the environment and the availability of eDNA to sample. Currently these probes may suffer high rates of false negatives (at the survey level), because eDNA is not sampled even though the species is present (Wood et al., 2018). These types of probes are also, by construction, speciesspecific which again raises the prospect of an inevitably restricted target list. eDNA probes based on meta-barcoding may offer the opportunity for "screening level" assessments of multispecies assemblages, but these probes are currently beset with challenges in the supporting infrastructure (i.e., incomplete sequence databases) and analytical pipelines that render them prone to high rates of false positives and false negatives (Ammon et al., 2018). The other method suggested by Arthur et al. (2015a) – sampling only in areas where ballast water is discharged or loaded – are unproven, and in large ports with significant circulation due to strong currents or tidal ranges may not be beneficial.

In 2001 New Zealand embarked on a national series of port baseline surveys based on the CRIMP protocols, and by 2007 had completed 43 surveys, including repeat surveys of 13 ports and 3 international marinas. The baselines surveys ended in 2007 and were considered at the time to provide a good indication of the then current distribution of nonindigenous species. In 2002 New Zealand also commenced with a series of targeted (species-specific) surveys initially designed to provide early detection of 7 high risk species. Surveys are now implemented in 11 harbors nationally every 6 months at an annual cost of approximately NZ \$2 million (Arthur et al., 2015a). A risk-based stratification of environments within each harbor is used to prioritize allocation of sample effort based on the likely distribution of founding populations of the primary target species (Inglis et al., 2006). These surveys adopt a more pragmatic approach to the problem of achieving a high statistical power (sensitivity) and use survey methods that are generic, quick and efficient to implement, with minimal processing of samples postcollection. Provisional identification of target species occurs in the field with only specimens of target and unrecognized taxa being retained for verification by taxonomic experts. In this way, relatively large sample sizes and coverage can be achieved in each survey at low sample cost. Because the surveys are principally focused on specific taxa, other groups of organisms (e.g., pelagic species, fish and benthic invertebrates) are not well sampled. The sensitivity of an individual survey varies among target species and is optimized across them using a risk-based Stochastic Scenario Tree model (Martin et al., 2007; Morrisey et al., 2012). For some species the per-survey sensitivity is less than the standards typically used to provide Proof of Freedom in veterinary and disease surveillance systems and, in these cases, the New Zealand surveys use Bayesian temporal discounting to provide Proof of Freedom based on non-detection in repeat, ongoing surveys.

### FUTURE APPROACHES TO MARINE PEST RISK ASSESSMENT AND MANAGEMENT

Many of the current approaches to marine pest risk assessment are based on the conceptualization that risk can be resolved at the species level, with detailed and sufficiently accurate assessments of individual risks. This view is realistic in certain circumstances. In aquaculture systems, for example, the number of identified pests is typically limited and therefore the knowledge base required to implement species-specific assessment is potentially manageable. This approach is also assisted by the similarity of aquaculture production systems internationally, so that knowledge developed in one location will readily translate to other locations. Moreover, aquaculture systems will have a commercial imperative and financial base to fund the required research and to balance the costs and benefits.

The utility of species-specific approaches is also clear in managing post-border incursions. A key example would be attempting to eradicate an invasive species. In this case the threat is identified and knowledge can be developed from direct observations of the species' behavior in its native and/or previously introduced range. In the case of post-border management, previous experience with arthropods suggests that taxon-specific information can be used to develop specific control plans and thereby improve the probability of successful eradication (Tobin et al., 2014). In developing response plans for specific target species, it is useful to cover a range of functional groups so that a response plan can be adapted easily for an incursion by an unexpected, but functionally similar species.

Pre-border, species-specific approaches to manage invasive species that pose a potential threat to environmental values are more problematic for several reasons. Firstly, the suite of potential invasive species is large but their distribution and ability to invade is poorly known. In addition, our ability to predict impact is limited, relying either on the species behavior in other non-native locales, or theoretical predictions as to the outcomes of the (potentially very) complex interactions between the species and the receiving environment. The Australian and New Zealand experience is that the inherent uncertainty and magnitude of this task can lead to policy impasses: there is potentially some level of risk in all vessels movements but its magnitude is uncertain. Hence any stakeholder can interpret it in a way that is consistent with their position. Moreover, currently there is no agreed way of determining a threshold of acceptable risk.

If we accept that species-specific approaches will not provide a practical basis for managing pre-border environmental pests we need to consider alternatives. Our starting point is to accept that all translocation pathways potentially carry some risk of environmental impact. If mitigation of this risk via a treatment was effectively cost free we would mandate it and the risk would be managed. In reality the costs of mitigation can be high. Hence there is a need to trade off the costs of mitigation versus the potential impact on the environment in a transparent and rational way.

Theory and experimental trials indicate that removing biological material, via ballast water exchange, ballast water treatment or increasingly stringent hull and niche area cleaning, will reduce inoculation pressure and therefore invasion risk (Bailey, 2015; Molina and Drake, 2016). In the limit, the elimination of all biological material on or contained in a vessel will achieve zero invasion risk. Thus we can conceptually rank treatments in terms of the amount of biological removed. It is important, however, that any such procedure accounts for operational conditions and distinguishes between application of a treatment - i.e., the management endpoint - and the actual amount of total biological inputs that are removed i.e., the biological endpoint. Empirical analysis of the efficacy of ballast water exchange in Chesapeake Bay, for example, illustrates that operational parameters, such as changing trade patterns, can lead to an overall increase in inoculation pressure despite implementation of the management endpoint (Carney et al., 2017).

The key question is how stringent management activities should be in order to mitigate the risk to an acceptable level. Intuitively we believe that a biological threshold exists, we just are uncertain about where it is. Adaptive policy settings and the use of expert panels to define the settings and monitor performance against them are increasingly important means for dealing with complex systems with uncertain management outcomes (Walker et al., 2001). Our key observation is that if we impose a management action, based on expert opinion for example, then we must monitor its biological efficacy, observe the number of incursions that occur and adjust the action if this rate is unacceptable. In this way, we analyze the system outcomes across all species rather than a bottom up assessment of individual species. Evaluation and monitoring of performance at the system level, measured in a way that is meaningful to decision makers, provides the key feedback to assess how well risk has been mitigated (Amendola, 2002).

In essence we propose that a treatment standard is defined that is underpinned and enforced by a rigorous compliance monitoring system. Adherence to this standard potentially results in ecological, economic and social impacts on the jurisdiction due to the establishment of new marine pests. These changes are detected by the system monitoring and that is used by management to assess the acceptability of the rate and nature of these changes. If these changes are unacceptable (because the standard is not stringent enough) the standard is modified.

In practice we recognize several practical challenges. Firstly, setting an expert based threshold involves pragmatism and can appear ad hoc. The alternative, however, may be that no action is taken at all while more information is sought to reduce uncertainty. Unfortunately, some of these uncertainties may be irreducible. The proposal converts the problem into one that can collect explicit data (e.g., incursions) to assess performance. This provides a more transparent basis to explore costs and benefits of a system. The threshold can also be tailored to different sectors and jurisdictions where needed. To break any impasse about the practicality of the approach, the threshold could be aligned

to outcomes that are achievable with current best practice and technology in the first instance, and then modified as further information became available.

Secondly, the proposed approach require effective compliance and compliance monitoring is therefore a key component of the system. As noted, compliance monitoring should consider both management and biological endpoints, and could be targeted at the highest risk vessels based on (for example) environmentalmatching risk assessment (Barry et al., 2015). We stress that the estimate of risk referred to here relates to the relative risk the vessel may pose, compared to all other vessels. This is a simpler task than assessing absolute risk.

Thirdly, the proposed approach relies on monitoring ecosystem outcomes. This is arguably the most significant challenge. The appropriate level of system monitoring is not solely a science issue but should also reflect the information needs of decision makers. At one extreme a jurisdiction could rely on passive monitoring to provide information about the impacts of new incursion on marine systems. Passive monitoring would rely on members of the public or industry to identify significant impacts as and when they become significant enough to be detected, and also relies on the media and/or government agencies to champion the issue and raise public awareness. Such a strategy, however, exposes jurisdictions to a number of threats such as creeping baselines (Papworth et al., 2009) and potentially an inability to identify incursions until they occupy large areas and are thereby costlier or impractical to eradicate (Tobin et al., 2014). Nonetheless, we believe this is the default approach in many jurisdictions.

At the other extreme, a jurisdiction could use detailed monitoring at a large number of sites to provide an information base for decision making. As discussed previously, detailed surveys in complex port environments are currently expensive and have been hard to justify to funders so careful consideration of the purpose and design of monitoring is needed. This is an area that we believe requires additional attention. The New Zealand experience is that this challenge can be met with a pragmatic approach to survey sensitivity that relies on repeat surveys conducted by a core team who become familiar with the system and are thereby able to identify unusual occurrences. This approach, however, still costs approximately NZ \$180,000 per port per year. It remains to be seen if the New Zealand experience could be scaled up to Australia but we believe this is worth further examination.

Finally, an adaptive, standard-based approach implies that the standard could change, and this could result in cost increases (or decreases) as industry moves to a more (or less) stringent standard. Such an approach also requires a standard that ideally: (i) can be assessed, at least in principle, by non-specialists to assist compliance and minimize associated costs; and (ii) describes what an acceptable level of biological contamination is - i.e., what is an acceptable level of fouling or acceptable concentration of organisms of different size classes in ballast water.

This type of standard is prescribed by the IMO D2 Ballast Water Treatment standards and is a feature of the New Zealand Craft Risk Management Standard for hull fouling (Georgiades and Kluza, 2017). The development of such a standard has the advantage of providing an unambiguous definition of what is and is not acceptable that can be directly related to observed environmental outcomes. The proposed biofouling management regime in Australia, which follows the MEPC guidelines, however, has moved away from this approach toward a standard based on a management endpoint not a biological endpoint. This could make it more difficult for an adaptive regime to respond to new information on incursion rates.

In a globalized world it is obviously helpful if standards are consistent world-wide. The ballast water convention is a clear example that, given time, a biological standard, and the technology needed to implement it, can be adopted around the world. The long lead times for international consensus mean that it is important that a similar approach for biofouling commence as soon as possible. In the interim countries can still apply their own standards consistent with their country-specific acceptable level of protection as defined by the World Trade Organization. Different countries are free to apply their own standards as long as they apply equally to all vessels and are, therefore, not trade restrictive.

The adaptive approach outlined above is consistent with the risk management measures adopted by countries for terrestrial biosecurity threats. For example, the importation of soil is tightly controlled in Australia, not on the basis of speciesspecific assessment but instead by a recognition that soil is a potential vector for a large number of organisms and is therefore unacceptable. Similarly, there are standards applied to the required cleanliness of shipping containers rather than relying on species-specific assessments.

In marine systems where the pathways are capable of sampling from a large species pool and where there is large uncertainty about which species will be transported and prosper in any given region, a species based approach to preborder risk assessment will not scale well because it becomes impractical as the number of species to be assessed rises. This problem is compounded by the potentially large range of values that are held in marine environments (environmental, social and cultural) and uncertainty in how introduced species may affect them.

Species-specific approaches can, however, help sharpen thinking and preparedness and should not therefore be discarded altogether. Species with a well-established track record of invasion and impact should be identified as unwanted, and they provide an opportunity to refine post-border preparedness - i.e., develop species-specific tactics for detection, eradication and control. If these tactics can be also be developed with a view to how they might be adapted to incursions by unknown/unanticipated species, by example considering the functional group that high profile invaders belong to, then this will improve a jurisdictions ability to respond to new incursions quickly as they are detected.

#### AUTHOR CONTRIBUTIONS

All authors listed have made a substantial, direct and intellectual contribution to the work, and approved it for publication.

#### REFERENCES

fmars-06-00489 August 6, 2019 Time: 14:28 # 11

comparative study between Canada and New Zealand. Biol. Invasions 14, 2301–2314. doi: 10.1007/s10530-012-0230-230

MAF Biosecurity New Zealand Technical Paper No: 2010/11. Wellington: MAF Biosecurity New Zealand.

eradication programs. Biol. Invasions 16, 401–414. doi: 10.1007/s10530-013- 0529-525

**Conflict of Interest Statement:** GI is employed by NIWA. NIWA undertakes the Marine High Risk Site Surveillance program under contract to biosecurity New Zealand.

The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2019 Hayes, Inglis and Barry. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

# Lessons From Placing an Observer on Commercial Cargo Ships Off the U.S. West Coast: Utility as an Observation Platform and Insight Into Ship Strike Vulnerability

#### Kiirsten Regina Flynn\* and John Calambokidis

Cascadia Research Collective, Olympia, WA, United States

#### Edited by:

Joshua Nathan Smith, Murdoch University, Australia

#### Reviewed by:

Allison Henry, Northeast Fisheries Science Center (NOAA), United States Jeanne Shearer, Duke University, United States

> \*Correspondence: Kiirsten Regina Flynn<EMAIL_ADDRESS>
#### Specialty section:

This article was submitted to Marine Conservation and Sustainability, a section of the journal Frontiers in Marine Science

Received: 01 May 2019 Accepted: 25 July 2019 Published: 14 August 2019

#### Citation:

Flynn KR and Calambokidis J (2019) Lessons From Placing an Observer on Commercial Cargo Ships Off the U.S. West Coast: Utility as an Observation Platform and Insight Into Ship Strike Vulnerability. Front. Mar. Sci. 6:501. doi: 10.3389/fmars.2019.00501 Ship strikes of whales are a growing concern around the world and especially along the U.S. West Coast, home to some of busiest ports in the world and where ship strikes on a number of species including blue, fin, and humpback whales have been documented. This trial program examined the feasibility, logistics, industry cooperation, and effectiveness of placing an observer on board a commercial ship. An experienced marine mammal observer went on five voyages, spanning over 8 days on ships operating between U.S. West Coast ports. Daylight observations were conducted over 68 h and covered over 1300 nm as ships transited between three ports [Seattle, Oakland, and LA/Long Beach (LA/LB)]. Sightings of large whales were reported on all (n = 42), totaling an estimated 57 individuals that included humpback, blue, fin, and beaked whales. Close encounters of large whales occurred (on one occasion a near miss, estimated at 40 m, of two humpbacks), and on another, a ship chose to alter course to avoid whale sightings in its path identified by the observer. All ships personnel cooperated and voluntarily aided in the observations even after initial skepticism by some crew about the program. While most effort on mitigating ship strikes along the U.S. West Coast has focused on shipping lanes, the vast majority of these sightings occurred outside these lanes and on the transit routes, emphasizing the need for added attention to these areas. This experiment demonstrates the effectiveness and promise of observations from ships providing critical information on whale locations at risk to ship strikes.

Keywords: ship strike, ship observers, blue whales, humpback whales, fin whales, shipping lanes

## INTRODUCTION

Ship strike of large whales have become an issue of growing concern worldwide and along the U.S. West Coast in particular (Redfern et al., 2013; Rockwood et al., 2017). The eastern North Pacific Ocean (ENP) and specifically coastal waters of the U.S. West Coast are utilized by a number of threatened or endangered large whales including blue whales, fin whales and two

(Mexico and Central America) distinct population segments (DPS) of humpback whales (Carretta et al., 2017). Ship traffic along the U.S. West Coast operate from major ports including those in the north based in Washington and British Columbia that transit out the Strait of Juan De Fuca, those based in San Francisco Bay including Oakland, Richmond, and San Francisco and in the Southern California Bight (SBC) home to Los Angeles/Long Beach (LA/LB), one of the world's largest ports. Ships transiting to and from these ports can go through five west coast National Marine Sanctuaries (NMS), areas identified as biologically important areas (BIAs) for the endangered blue and humpback whales, and for high densities of feeding gray whales (Calambokidis et al., 2015). With large ports and large commercial vessels transiting through these rich marine areas, comes the potential for ship strikes (Redfern et al., 2013; Rockwood et al., 2017; Moore et al., 2018).

Ship strikes of blue, fin, humpback, and gray whales have been frequently documented along the U.S. West Coast (Laist et al., 2001; Douglas et al., 2008; Rockwood et al., 2017) and second only to entanglements in the leading cause of human caused mortality to large whales along the U.S. West Coast (Carretta et al., 2017). Blue and fin whales appear to be particularly susceptible to ship strike mortality along the U.S. West Coast (Berman-Kowalewski et al., 2010; McKenna et al., 2015) though Monnahan et al. (2015) question whether ship strikes threaten the recovery of eastern North Pacific blue whales. Mitigation efforts increased after detection of seven blue whale carcasses triggered an unusual mortality event in 2007 (Abramson et al., 2009), and four of those deaths were attributed to vessel strikes (Berman-Kowalewski et al., 2010). In 2009, the Channel Islands National Marine Sanctuary (CINMS) recommended shipping lane changes (Abramson et al., 2009), which were put into place in 2013. In 2011, the National Oceanic and Atmospheric Administration's (NOAA) Office of Marine Sanctuaries also established a Joint Working Group (JWG) to assess ship and whale interactions including ship strike and acoustic impacts in the Gulf of the Farallones and Cordell Bank, to create a list of recommended mitigation measures (Joint Working Group, 2012). The JWG concluded that in order to reduce lethal ship strikes, a reduction in the co-occurrence of ships and whales had to occur. In their 2012 report, their recommendations included modification of shipping lanes, creation of dynamic management areas (DMA) in regions of high whale concentrations, education and outreach initially engaging and informing the commercial industry, and the creation of a real time monitoring and whale sighting network with commercial ship participation (Joint Working Group, 2012).

Placing dedicated marine mammals observers on board vessels has been proposed as an effective method for getting sighting information and helping to avoid collisions with large whales (Weinrich, 2004; ACCOBAMS, 2005; David et al., 2005; Weinrich et al., 2010; Gende et al., 2011; Couvat and Gambaiani, 2013). We report on a pilot program putting an observer on ships transiting between U.S. West Coast ports to document sightings along these routes, help quantify the threat to whales from ships and also evaluate the feasibility of using these platforms as an expanded source of sighting reports which were all part of the recommendations of the JWG.

#### MATERIALS AND METHODS

With the assistance of the Pacific Merchant Shipping Association, we worked with two shipping companies that transit between ports on the U.S. West Coast. While many ships using U.S. West Coast ports including the ships we worked with transit to more distant ports including Hawaii and Asia, we only sought transits between U.S. ports. All trips were conducted by the senior author, an experienced marine mammal observer and a licensed captain with professional experience in the maritime industry, which was valuable in negotiating with the companies with assurances she would not disrupt ship operations. The bridge height of commercial vessels is set up to provide the vessel operators the most unobscured 360◦ view possible for safe operations regardless of the position of the bridge (forward, mid, or aft). Ships we worked with included vessels with both forward and mid-aft bridges (**Figure 1**), for the latter the height of the containers carried on the ships never extends above the bridge height but did partially obscure visibility directly in front of the ship.

Shipping companies and the ship's officers agreed to provide access to the vessel bridge to the observer during all daylight hours. Ship passages occurred from May to September, periods of known occurrence of feeding baleen whales off the U.S. West Coast. Specific voyages were selected based on the vessel having the highest likelihood of being in a shipping channel during the most amount of daylight hours to allow for either entering or exiting shipping lanes into San Francisco and LA/LB, California (**Table 1**).

The observer was on effort approximately 4 h at a time during all daylight hours in all conditions, with 30-min breaks in between observation periods. Environmental (Beaufort, visibility, cloud cover, and precipitation) and effort data were recorded at the beginning and end of each on-effort period and any time conditions changed. During on-effort periods, continuous scans of the horizon were made from the bow to approximately 60◦ port and starboard with the naked eye and occasionally with a 7 × 50

FIGURE 1 | Examples of ship configurations and views from ships that were part of this study including a ship with a forward bridge, voyages (3–5) (top) and a ship with a mid-aft bridge (bottom) during voyages 1 and 2.

TABLE 1 | Voyage numbers, dates of travel and ship specifications of ride-alongs.

reticle compass binoculars. Species identification and behavior determination was aided with the help of binoculars. The sighting position and distance from ship of the whales was estimated for 5 of the 6 voyages, using the ship's GPS position, reticle reading of the whale's position below the horizon, angle off of ship's bow in 10◦ increments and height above the water. Group size and behavior if known was also recorded for any marine mammal. Data were collected both on an app based platform, SpotterPro, on a tablet (to test and demonstrate such a system to the crew) as well as on datasheets or a laptop. During observational watches, engagement with the crew offered informal discussions and educational opportunities for both crew and observer.

### RESULTS AND DISCUSSION

#### Sighting Locations

A total of 42 large whale sightings of an estimated 57 individuals were made during 68 h and 1,387 nm of observation effort during five voyages spanning 8 days as ships transited between U.S. West Coast ports (**Tables 2**, **3**). While 60% of large whale sightings were of unconfirmed species identity (species sometimes too distant even with the binoculars to identify), those that were identified included humpback, blue, fin and beaked whales (**Table 3**). Large whales were sighted on all five voyages representing six of the 8 days observations were made. Two days without sightings were the shortest days (2 and 5.5 h of observation). Even though sighting conditions varied widely and included some very poor weather (45 + knots of wind at one time and 25 foot seas) the bridge height above the water still provided good visibility. In addition to large whales there were also sightings of pinnipeds and small cetaceans.

The majority (76%, 32 out of 42) of the large whale sightings were on coastal ship transit routes along the coast outside the designated traffic separation lanes leading to major ports (**Figure 2** and **Table 3**). Average ship speed while traveling coastally and outside traffic separation schemes ranged from 18 to 23 kts while inside the designated shipping lanes speed was slower, 11–18 kts (**Table 2**).There were six close encounters with large whales on five of the six trips with four of these outside the shipping lanes and two in the lanes. A sighting was deemed a close encounter if the whale was estimated to be less than 300 m from the vessel. One of these (outside the lanes) was considered a near miss (estimated at 40 m) of two humpback whales.

Our results demonstrate the potential large role that ships traveling along the coast may play in ship strikes and how most of the risk for these ships may be outside of the designated shipping lanes near ports (versus ships that head offshore toward principal destinations in Asia after leaving the shipping lanes). Most of the focus of management efforts on the designated shipping lanes around major ports (San Francisco and Los Angeles/Long Beach). Our findings are consistent with encounter models of ships and whales that demonstrated a majority of strikes likely occur outside the designated traffic separation lanes even though the rate may be highest in the lanes (Rockwood et al., 2017).

### Experience Working on Vessels and Feasibility for Future Use

There was a high degree of cooperation from ship's personnel to the observer. Once introduced to and educated on the topic of whale strikes and explanations of the presence of a marine mammal observer not being a regulatory professional, all ships personnel on the bridge assisted and aided in the sightings, even when the observer was off effort. This cooperation came where there was initial skepticism by some crew on sighting whales with several crew saying they had never seen a whale while on watch on the bridge and were surprised at the amount of sightings detected on our trip, while others indicated that they see whales often and maneuver around them periodically. During down times on the bridge, discussions with crew included the feasibility of their recording sightings without a dedicated marine mammal observer and the best ways to achieve this. There was a repeated suggestion by crew that this could best be achieved by integrating marine mammal observations and recording into existing reports they already were conducting. Even though a poster to help identify whales and report sightings had been circulated to shipping companies operating out of LA/LB, it was not present on most vessels and in the cases where present crew seemed unfamiliar with it.

On two occasions, the ship's crew took initiative to alter course to avoid whales informing the observer of their intent. One of these involved some distant sightings in the ships path that prompted a small course alteration so they were no longer dead ahead and the other, the mate employed hand steering to avoid a closer sighting of a whale. Though not requested by the observer, these responses could have been influenced by our presence. Observations of whales directly ahead on board the vessels with a mid-aft bride were more difficult since the bow was over 180 m ahead of the observer position and containers blocked the view immediately in front of the vessel as seen in **Figure 1**.

This pilot study was more successful than anticipated both verifying the value of ships as an observation platform and

#### TABLE 2 | Dates, region, and on-effort length, sighting conditions, and speed of ship ride-alongs.

TABLE 3 | Numbers of sightings and individuals of large whales, inside and outside shipping channels.

FIGURE 2 | Tracks and sighting locations of voyages 1–5. (A) shows an overview of all ships tracks and sightings and (B–D) show detail of specific areas including shipping lanes shown in red and region outlined in white.

showing the frequency of encounters of large whales for vessels transiting along the coast. This is consistent with findings in other areas regarding the value of dedicated marine mammal observers placed on board ferries and cruise ships (Gende et al., 2011; Harris et al., 2012; Williams et al., 2016). Weinrich et al. (2010) demonstrated that observers aboard fast ferries detected whales faster and at larger distances than the crew. Commercial vessels bridge height above the sea surface, the wide field of view, all designed for safe operations and the ships stability, make an excellent marine mammal viewing platform. While our

visual observations were limited to daylight conditions, other approaches (e.g., infrared) could be used to expand this to nighttime periods when whales are closer to the surface and more vulnerable to ship strikes (Calambokidis et al., in press).

### CONCLUSION

Our findings demonstrated:

These findings have resulted in plans to conduct future trips with observers to improve sample size (planned for 2019–2021) with an ultimately goal of having ship personnel conduct their own observations and reporting.

#### DATA AVAILABILITY

The datasets generated for this study are available on request to the corresponding author.

#### REFERENCES

#### AUTHOR CONTRIBUTIONS

Both authors conceived and designed the study, revised the manuscript, and read and approved the submitted version of the manuscript. KF collected the data and wrote the first draft of the manuscript. JC designed the data analysis.

#### FUNDING

This work was supported by NOAA (Contract: AB-133F-12-SE-1069). Writing and analysis were supported by NOAA's Section 6 grant to the Washington Department of Fish and Wildlife (NA 16NMF 4720061).

#### ACKNOWLEDGMENTS

The authors would like to thank John Berge, Vice President, Pacific Merchant Shipping Association (PMSA), for his assistance with making connections with commercial shipping industry, and Michael Carver, Cordell Bank National Marine Sanctuary, for support of the project. Gratitude also goes to all ship's personnel and specifically to Colin Murray and Ryan Connolly with American President Lines (APL) and Reps: Kevin Krick, Senior Director – Security/Environment for APL; Erik Frisk, APL; APL M/V Thailand Captain, Daniel Parr; APL M/V Singapore Captain, George Werdann; Matson Reps: Captain, John F. Cronin; Matson: M/V Mokihana Captain, Tom Crawford; M/V Mokihana Captain, Jim Hill; M/V Manoa Captain, Peter Webster; and M/V Manoa Captain, Jeff Idema.

**Conflict of Interest Statement:** The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2019 Flynn and Calambokidis. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

# The Role of Slower Vessel Speeds in Reducing Greenhouse Gas Emissions, Underwater Noise and Collision Risk to Whales

#### Russell Leaper\*

International Fund for Animal Welfare, London, United Kingdom

Reducing speeds across shipping fleets has been shown to make a substantial contribution to effective short term measures for reducing greenhouse gas (GHG) emissions, working toward the goal adopted by the International Maritime Organization (IMO) in April 2018 to reduce the total annual GHG emission by at least 50% by 2050 compared to 2008. I review modeling work on GHG emissions and also on the relationships between underwater noise, whale collision risk and speed. I examine different speed reduction scenarios that would contribute to GHG reduction targets, and the other environmental benefits of reduced underwater noise and risk of collisions with marine life. A modest 10% speed reduction across the global fleet has been estimated to reduce overall GHG emissions by around 13% (Faber et al., 2017) and improve the probability of meeting GHG targets by 23% (Comer et al., 2018). I conclude that such a 10% speed reduction, could reduce the total sound energy from shipping by around 40%. The associated reduction in overall ship strike risk has higher uncertainty but could be around 50%. This would benefit whale populations globally and complement current efforts to reduce collision risk in identified high risk areas through small changes in routing.

#### Edited by:

David Peel, Commonwealth Scientific and Industrial Research Organisation (CSIRO), Australia

#### Reviewed by:

Mark Peter Simmonds, University of Bristol, United Kingdom Piers Dunstan, CSIRO Oceans and Atmosphere, Australia

#### \*Correspondence:

Russell Leaper<EMAIL_ADDRESS>
#### Specialty section:

This article was submitted to Marine Conservation and Sustainability, a section of the journal Frontiers in Marine Science

Received: 24 January 2019 Accepted: 29 July 2019 Published: 16 August 2019

#### Citation:

Leaper R (2019) The Role of Slower Vessel Speeds in Reducing Greenhouse Gas Emissions, Underwater Noise and Collision Risk to Whales. Front. Mar. Sci. 6:505. doi: 10.3389/fmars.2019.00505

#### Keywords: speed, GHG, emissions, underwater noise, ship strike

## INTRODUCTION

In April 2018, the International Maritime Organization (IMO) adopted an initial strategy on the reduction of greenhouse gas (GHG) emissions from ships. The target is to reduce the total annual GHG emissions by at least 50% by 2050 compared to 2008 values, while at the same time pursuing efforts toward phasing them out entirely. The strategy lists candidate short term measures to reduce GHG emissions in order to meet the agreed targets. IMO has developed the Energy Efficiency Design Index (EEDI) which requires that new ships become increasingly more energy efficient according to the year in which they were built. This is the only legally binding energy efficiency regulation for international shipping and only applies to new builds. This means that in order to reach the IMO 2050 target, measures for improving operational efficiency of existing ships will also be required. One element of the strategy is to "consider and analyze the use of speed optimization and speed reduction as a measure, taking into account safety issues, distance traveled, distortion of the market or to trade and that such measure does not impact on shipping's capability to serve remote geographic areas" (IMO, 2018). It has been suggested that speed reduction is perhaps the only short-term regulatory option capable of achieving the necessary reductions in GHG emissions to meet IMO targets (CSC, 2017).

Here, I consider the implications of speed optimization and reduction not only for GHG emissions but for two further environmental impacts of shipping: ship strike risk to whales and underwater noise. Collisions between cetaceans and ships occur worldwide where vessel activities overlap with cetacean habitat. Collisions can cause damage to vessels and lead to injury and/or death of cetaceans. In response to this threat, the IMO issued guidance on minimizing the risk of ship strikes to cetaceans (IMO, 2009) in 2009. The impacts of underwater noise from shipping have also become increasingly recognized. IMO agreed to guidelines for the reduction of underwater noise from commercial shipping to address adverse impacts on marine life in 2014 (IMO, 2014).