Science of the Total Environment 496 (2014) 257–263
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Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv
Fish oil disrupts seabird feather microstructure and waterprooﬁng Lora A. Morandin a, Patrick D. O'Hara b,c,⁎ a b c
1212 Juno St., Victoria, BC, Canada V9A 5K1 Canadian Wildlife Service, Environment Canada, Institute of Ocean Sciences, 9860 W. Saanich Rd., Sidney, BC, Canada V8L 4B2 Department of Biological Sciences, University of Victoria, Box 3020, Station CSC, Victoria, BC, Canada V8W 3N5
H I G H L I G H T S • • • • •
Little is known about effects of ﬁsh and other edible oils on seabirds. We conducted lab experiments and interviewed wildlife response experts. Lab experiments showed ﬁsh oil signiﬁcantly disrupted feather microstructure. Feathers exposed to ﬁsh oil absorbed water and oil indicating loss of waterprooﬁng. Experts agreed that ﬁsh oil is harmful to seabirds and requires intervention.
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Article history: Received 24 March 2014 Received in revised form 7 July 2014 Accepted 8 July 2014 Available online xxxx Editor: Mark Hanson Keywords: Marine pollution Fish oil Edible oil Seabirds Shipping Feather microstructure
a b s t r a c t Seabirds and other aquatic avifauna are highly sensitive to exposure to petroleum oils. A small amount of oil is sufﬁcient to break down the feather barrier that is necessary to prevent water penetration and hypothermia. Far less attention has been paid to potential effects on aquatic birds of so called ‘edible oils’, non-petroleum oils such as vegetable and ﬁsh oils. In response to a sardine oil discharge by a vessel off the coast of British Columbia, we conducted an experiment to assess if feather exposure to sheens of sardine oil (ranging from 0.04 to 3 μm in thickness) resulted in measurable oil and water uptake and signiﬁcant feather microstructure disruption. We designed the experiment based on a previous experiment on effects of petroleum oils on seabird feathers. Feathers exposed to the thinnest ﬁsh oil sheens (0.04 μm) resulted in measurable feather weight gain (from oil and water uptake) and signiﬁcant feather microstructure disruption. Both feather weight gain and microstructure disruption increased with increasing ﬁsh oil thickness. Because of the absence of primary research on effects of edible oils on sea birds, we conducted interviews with wildlife rehabilitation professionals with experience rehabilitating sea birds after edible oil exposure. The consensus from interviews and our experiment indicated that physical contact with ﬁsh and other ‘edible oils’ in the marine environment is at least as harmful to seabirds as petroleum oils. Crown Copyright © 2014 Published by Elsevier B.V. All rights reserved.
1. Introduction It is well-known that petroleum oil discharges in oceans have negative impacts on seabirds (e.g., Leighton, 1991; Jenssen, 1994; Stephenson, 1997; Giese et al., 2000; Irons et al., 2000; Wiese and Robertson, 2004; Votier et al., 2005). Feather fouling from as little as 10 ml of petroleum oil can cause penetration of water and oil, result in loss of buoyancy, and signiﬁcantly reduce thermoregulation in aquatic avifauna; these effects are particularly lethal in colder climates and for surface feeders and diving birds (Hartung, 1967; McEwan and Koelink, 1973; Levy, 1980; Lambert et al., 1982; Jenssen and Ekker, 1991; Camphuysen, 1998). Indeed, based on observations made in the ﬁeld and results reported by O'Hara and Morandin (2010), trace quantities of oil impact feather ⁎ Corresponding author. Tel.: +1 250 363 6545. E-mail address: [email protected]
http://dx.doi.org/10.1016/j.scitotenv.2014.07.025 0048-9697/Crown Copyright © 2014 Published by Elsevier B.V. All rights reserved.
integrity and water prooﬁng ability. There is evidence that some marine birds, particularly those that spend some time on land, are able to ‘selfclean’ petroleum oil, without intervention from humans (Camphuysen, 2011); however, this likely does little to offset the large proportion of birds that are not able to recover on their own. Much less is known about effects on seabirds of other types of oil such as ﬁsh and vegetable oils (sometimes termed ‘non-petroleum oils’, ‘non-petrogenic oils’, or ‘edible oils’; we use the term edible oils throughout this paper, referring mainly to ﬁsh- and vegetable-based oils). We are aware of no previous studies measuring sensitivity of seabird feathers or whole birds to edible oils. It is vital to understand how edible oils impact feathers and birds since there is a perception that edible oils may be less detrimental to marine life than petroleum oils. However, observations of impacts of edible oils on seabirds suggest that they are as harmful, or more harmful than petroleum oils (Berry, 1976; McKelvey et al., 1980; Rigger, 1997; Bucas and Saliot, 2002).
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Many types of edible oils are formally recognized as harmful by The International Convention for the Prevention of Pollution from Ships (MARPOL; http://www.imo.org/About/Conventions/ListOfConventions/ Pages/International-Convention-for-the-Prevention-of-Pollution-fromShips-(MARPOL).aspx), which is reﬂected in national legislation (e.g., Canada: Canada Shipping Act: http://laws-lois.justice.gc.ca/eng/acts/C10.15/; U.S.: U.S. Environmental Protection Act http://www2.epa.gov/ emergency-response/vegetable-oils-and-animal-fats#frp). Indeed, in the U.S., the Environmental Protection Agency denied a request by various trade associations to amend restrictive Facility Response Plan rules and further differentiate between petroleum and edible oils in terms of potential environmental consequences in a worst case scenario (Federal Register 62 (202): 54508–54543: http://www.gpo.gov/fdsys/ granule/FR-1997-10-20/97-27261). Despite clear legislation and upper level policy however, these oils and their impacts often are overlooked by response and enforcement personnel because edible oils are considered non-toxic, disregarding that the oil–feather interaction typically is the main reason for acute effects of oil exposure on marine birds. Feathers are important for both insulation and buoyancy on water; feather microstructure, made up of barbs and barbules, creates an interwoven mesh structure with trapped air, which results in a waterproof barrier (Stephenson, 1997). It is this microstructure and the oleophilic nature of the structure that result in the water repellency of feathers (Rijke, 1970). A compromise of feather integrity can result in water penetrating plumage, displacing the layer of insulating air, which may result in hypothermia and death. In water birds, the structure within and between feathers is adapted to the speciﬁc (high) surface tension of unpolluted water (Swennen, 1978). In addition to disrupting the feather microstructure, oil and other materials lower surface tension of water resulting in feathers being less able to resist penetration (Swennen, 1978; Stephenson, 1997; Stephenson and Andrews, 1997). Studies on the effects of petroleum oils on feather microstructure are sparse yet show that oils and other pollutants disrupt feather microstructure by collapsing the interlocking structure of barbs, barbules, and hooks, resulting in the penetration of water and oil, displacing air (Hartung, 1964; Jenssen and Ekker, 1988; Jenssen, 1994; O'Hara and Morandin, 2010). Evidence linking ﬁsh and other edible oils with negative impacts on feathers and whole birds is largely anecdotal at this point. Consequently, management and enforcement policy often overlooks edible oils in addressing potential ecological consequences associated with discharged oil. This study was initiated in response to a July, 2010 discharge of approximately 940 l of crude sardine oil, into the marine environment from a vessel 220 km west of Vancouver Island. The discharge and resultant sheen was observed by a Transport Canada National Aerial Surveillance Program (NASP) aircraft and was reported to be approximately 25 km2 with a silver grey appearance (pers. comm. Ralph Hilchie, NASP; incident report to enforcement agencies for both Transport Canada and Environment Canada). The effects of this spill on wildlife were not directly measured at the time. This study is composed of two main components: 1. An experiment to assess the impacts of ﬁsh oil on seabird feather microstructure, and water and oil uptake with varying surface oil thicknesses; and 2. Interviews with researchers, rehabilitation professionals, and veterinarians on their experiences with seabirds and edible oils. For the experiment portion, we adapted a protocol from a previous experiment we conducted on petroleum oils (O'Hara and Morandin, 2010). In the previous experiment, we found that there was a signiﬁcant weight increase in feathers exposed to crude oil sheens 3 μm and greater, and a signiﬁcant change in feather microstructure with crude oil sheens of 0.1 μm and greater. We expected that ﬁsh oil would cause a similar feather microstructure disruption and weight gain as petroleum oil, with the thinnest sheens causing no measurable effect, and an increasing disruption and weight gain with increasing sheen or slick thickness. The purpose of the interviews was to establish the extent to which whole birds are affected by exposure to ﬁsh oil and their ability to preen these oils out.
Because edible oils are less toxic to seabirds, an ability to rapidly and efﬁciently preen the oils from feathers would support the case for edible oils being less harmful than generally toxic petroleum oils. 2. Feather exposure experiment 2.1. Materials and methods Upper breast feathers were sampled from 10 frozen common murre (Uria aalge) and 10 rhinoceros auklet (Cerorhinca monocerata) carcasses collected from ﬁsheries incidental take in British Columbia waters. Carcasses were stored in a freezer at −10 °C. Unprocessed, crude sardine oil was acquired from Investigations (Environment Canada) from the Vancouver Port reception facility that received crude ﬁsh oil from the vessel associated with the discharge event documented by the NASP and described in the introduction to this study. The ﬁsh oil was stored in a clean brown glass bottle in a refrigerator at approximately 3 °C. Fish oil treatments were chosen to encompass the thickness corresponding to a silver or grey sheen, which was the observed colour of the sardine oil slick observed by the NASP; a silver/grey sheen corresponds to 0.04 μm to 0.3 μm for petroleum oil on seawater. However, these sheen and slick thicknesses are estimated based on a visual assessment of colours calibrated for petroleum oils, and this technique may not be accurate for estimating the thickness of other oils. We chose four treatment levels of 1) control: no oil added, 2) low estimate silver/grey: 0.04 μm, 3) mid-estimate silver/grey sheen: 0.1 μm, and 4) rainbow colour sheen: 3.0 μm (http://response.restoration.noaa.gov/ sites/default/ﬁles/OWJA_2012.pdf). These sheen thicknesses also corresponded to the thicknesses of petroleum oil used in O'Hara and Morandin (2010). Initially we included a ﬁfth treatment level, a positive control of 25 μm thickness; however, preliminary tests showed that this thickness completely saturated the feathers with oil and there was no calculable amalgamation index (see below). Sheen treatments were created by calculating the amount of oil required to create the designated thickness given the surface area of the Petri dish using the formula, volume of oil added = πr2x (where r = radius of the Petri dish, and x = oil thickness). Seawater was cooled in the refrigerator to approximately 10 °C to simulate typical summer seawater surface temperatures off the coast of Vancouver. 140 ml Petri dishes were ﬁlled with 77 ml (5 mm height) of the cooled seawater. One replicate of each treatment was prepared at a time, so that there were four dishes prepared at once, and appropriate volumes of oil (based on formula above) were pipetted onto the surface using a calibrated micropipette. In each experimental round of four Petri dishes, dishes were randomly assigned to an oil treatment and dishes were used from left to right. After oil was deposited on the surface of the seawater, it was gently stirred with the tip of the pipette. Before being exposed to the oil sheen, a feather was picked up by the calamus (Fig. 1) with clean tweezers and weighed on a Scaltec SBC 22 analytical balance (Heilingenstadt, Germany, accuracy class I) to 0.0001 g. The feather was placed with the convex side up on a microscope slide and photographed under 60× magniﬁcation. Two images were taken on each side of the rachis for a total of four images of each feather. Image locations were chosen semi-randomly, in areas that did not contain large anomalies such as splits between barbs (Fig. 2). The feather was then placed on the water, in the centre of the Petri dish, convex side down, for 15 s. The feather was swiped three times across the surface of the water, the full diameter of the Petri dish, and then left stationary on the water surface for an additional 15 s. The feather was weighed a second time and then again placed onto a glass slide, convex side up, leaving the convex feather surface untouched after treatment. During this process, the feather was grasped by the calamus only, with no disturbance of the barbs and barbules other than the treatment. The process was repeated 10 times (rounds) for each species with washed and freshly prepared Petri dishes. For each of the 10 treatment rounds per species, a different individual bird
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Fig. 1. Feather microstructure. Diagram by J. Clowater.
was used, so that there were 10 individuals used from each species, and four feathers that were collected from each individual. Feathers collected from each individual were randomly assigned to one of the four treatments, and four post-treatment pictures were taken from each feather resulting in a total of 40 post-treatment images per treatment, per species. Proportional feather weight increase [(post-treatment weight − pre-treatment weight) / pre-treatment weight] was compared among treatments using a mixed model ANOVA with treatment, species, and the interaction as main effects, and individual bird and feather as random factors. A barbule amalgamation index (AI) was calculated for each image following O'Hara and Morandin (2010) in order to quantify clumping of barbules resulting from exposure to oiled water. This may be similar to the feather microstructure ‘derangement’ described by
Hartung (1967) following feather immersion in petroleum oil slicks. On each image, we measured a 0.8 mm section of ramus and counted the number of barbules with hooks (from herein referred to as barbules) originating from this section. We then counted the number of barbules in each ‘clump’ (touching each other) and calculated AI as mean barbules per clump (Table 1 and Fig. 3). Higher AI values indicate greater numbers of barbules per clump, resulting in larger gaps or holes through which water and oil can penetrate. Pre-treatment amalgamation was scored in order to have a baseline in which to compare amalgamation of barbules from treated feathers. Because pre-treatment amalgamation had very little variability, feather amalgamation scoring was only done for 64 images (4 images, from each of four feathers, from each of four birds). Barbule AI was ﬁrst compared between the sub-sample of pretreatment common murre feathers (four common murre individuals, four feathers from each individual, and four pictures per feather for a total of 64 pre-treatment, scored images) and post-treatment common murre images in order to assess if there were differences between pretreatment AI and post treatment AI for each of the oil thickness treatment levels. We were particularly interested in whether the control treatment of no oil disrupted feather microstructure compared to feathers that had no treatment exposure. The expectation was that pre-treatment AI would not differ from control or 0.04 μm treatment AI, but would be different from all other treatments. If this were the case, the analysis would show that exposure to the control treatment (no oil, only sea water) or ‘barely visible sheen’ of 0.04 μm did not impact feathers in terms of AI. Pre-treatment AI was compared to post treatment AI using a mixed model ANOVA in the statistical package SAS (SAS, 1999) with treatment as the main effect and individual, feather, and photo as random effects, followed by comparison of means among treatment levels. Following the pre-analysis, we removed the pre-treatment subsample and compared AI among treatments using a mixed model ANOVA (SAS, 1999) with treatment and species, and the interaction as main effects, and individual, feather, and picture as random factors. For all ANOVA analyses, a Poisson or negative binomial distribution link function was used when data were not normally distributed, and F-values were reported with numerator (ﬁrst) and denominator (second) degrees of freedom as subscripts. All t-values were also reported with degrees of freedom as subscripts. P-values of less than 0.05 were considered signiﬁcant. All reported means and graphs were based on non-transformed data.
Fig. 2. Four pictures were taken on each feather (red squares), before and after treatment exposure, with the locations chosen semi-randomly, with two pictures on each side of the rachis. Areas that had anomalies such as large splits between adjacent barbs were avoided. This picture is of a feather after exposure to a 0.1 μm sardine oil sheen. (For interpretation of the references to color in this ﬁgure legend, the reader is referred to the web version of this article.)
There was no species by treatment interaction on feather weight gain or effect of species on weight gain, and we therefore analysed weight gain for feathers collected from both species together. There was a signiﬁcant effect of oil thickness (treatment) on weight gain (F3,54 = 84.57, P b 0.0001), with progressively greater weight gain with each increase in sheen thickness (Fig. 4). Proportional weight gain for all treatments, except the control treatment, was signiﬁcantly greater than zero (P b 0.0001). Amalgamation index (AI) from the sub-sample of pre-treatment images was not different from control treatment AI (± SE) (AI pretreatment 1.36 (0.04) and control AI 1.35 (0.03); t204 = 0.11, P = 0.910). However, pre-treatment AI was lower than AI from all other treatments (P b 0.01 for all three other comparisons). There was a signiﬁcant interaction between bird species and treatment for AI and therefore we analysed AI data from the two species separately. For common murres, there was a signiﬁcant difference in AI among treatments (F3,141 = 95.11, P b 0.0001), with an increase in AI with increasing oil thickness (Fig. 5). For rhinoceros auklets, there also was a signiﬁcant increase in AI with increasing oil thickness but with a larger increase in AI for the 3 μm treatment (F3,141 = 95.57, P b 0.0001; Fig. 6). Of note, for
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Table 1 Amalgamation index calculations corresponding to the four pictures in Fig. 3. These four feathers were from the same common murre, but exposed to different sardine oil sheen thicknesses. The value in the “Trt” column is the thickness of the sardine oil on seawater (μm) that the feather was exposed to. “Barbules” indicate the total number of barbules in the 0.8 mm section that was assessed, and “AI” is the amalgamation index calculated as the number of barbules in the 0.8 mm section divided by the number of barbule groups. For 0.1 μm AI = 25 / 7 in this example. Trt
0 0.04 0.1 3
1 1 4 4
1 1 3 3
1 2 3 2
1 1 6 7
2 1 4 17
2 2 3
1 2 2
both species, AI was signiﬁcantly greater than the control treatment even at the thinnest sheen of 0.04 um.
2.3. Experimental discussion Sardine oil sheens on seawater caused measurable disruption to feathers both in weight gain and barbule clumping (measured by amalgamation index; AI). Weight gain was proportional to the thickness of the ﬁsh oil that the feather was exposed to, indicating that harm to seabirds could be proportional to the quantity and/or thickness of discharges. The oil and water uptake likely is due to the decreased surface tension of the water caused by the ﬁsh oil (Stephenson, 1997; Stephenson and Andrews, 1997) and the disruption of feather microstructure creating larger spaces between barbules (Hartung, 1967; Rijke, 1970). Somewhat surprisingly, even the thinnest sheens we tested (0.04 μm) caused measurable and signiﬁcant oil and water uptake by feathers. In our previous study with petroleum oils, there was no significant increase in feather weight gain in comparison to the control treatment for oil thickness of less than 3 μm (O'Hara and Morandin, 2010). Similarly, AI was signiﬁcantly greater at the lowest treatment level of ﬁsh oil (0.04 μm) than AI in the control treatment, whereas for crude oil and synthetic drilling ﬂuid, AI was not greater than the control when feathers were exposed to 0.04 μm sheens (O'Hara and Morandin, 2010).
32 30 25 33
1.2 1.6 3.6 6.6
In terms of AI therefore, ﬁsh oil (current experiment) impact to seabird feathers was greater than that of crude oil (O'Hara and Morandin, 2010). While there have been no other experimental studies, to our knowledge, that assess the impact of edible oils on seabirds or compare impacts of edible to petroleum oils, published observational studies have provided evidence that edible oil causes as much immediate, acute harm to seabirds as petroleum oils, despite the fact that edible oils are not internally toxic. For example, rapeseed oil spills in Vancouver Harbour have caused signiﬁcant seabird death, in some cases causing greater mortality than similar sized, and larger, petroleum spills (McKelvey et al., 1980; Smith and Herunter, 1989). Similarly, a large soybean oil spill in the Mississippi river killed an estimated 4000 birds (Anonymous, 1963). The lack of toxicity of edible oils however, may result in fewer long-term, sub-lethal effects as petroleum oil. Published reports on effects of ﬁsh oil in marine environments are similarly sparse as other edible oils, yet they also indicate dramatic, negative effects to seabirds. Close to 6000 oiled birds were killed at Bird Island, 240 km north of Cape Town, South Africa when ﬁsh oil was released from an efﬂuent pipe of a ﬁsh-processing factory a few hundred metres from the island (Anonymous, 1974). In the same year, over 4500 Cape Cormorants were killed by anchovy oil discharged from wetprocessing at a ﬁsh plant and ship holds during an anchovy run on the coast of Namibia (Berry, 1976). Death was thought to be due to the oil causing ﬂightlessness and subsequent starvation, and exposure to cold
Fig. 3. Photos of common murre feather barbs after exposure to different thicknesses of crude sardine oil on seawater: a. 0 μm (control); b. 0.04 μm; c. 0.1 μm; and d. 3 μm. Each picture is a unique feather but from the same bird. Red lines superimposed on the rachi show the 0.8 mm section where amalgamation index was calculated. See Table 1 for barbule scoring and amalgamation index calculations corresponding to these images. (For interpretation of the references to color in this ﬁgure legend, the reader is referred to the web version of this article.)
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Proportional weight gain
2 2 0 0.00
Oil thickness (µm)
Oil thickness (µm) Fig. 4. Proportional weight gain of feathers before and after exposure to varying thicknesses of crude sardine oil. All treatments were signiﬁcantly different from each other (P b 0.05).
Fig. 6. Amalgamation index for rhinoceros auklet feathers exposed to various thicknesses of sardine oil sheens on seawater. All treatments were signiﬁcantly different from each other (P b 0.01).
from loss of insulation due to feather oiling. Further, anecdotal evidence indicates that even small quantities of ﬁsh oil can result in the loss of water repellency in ducks (Fabricius, 1956) and captive pelagic seabirds (Swennen, 1978). The reported marine bird mass mortality from ﬁsh and other edible oils, along with the current experimental evidence of water and/or oil uptake and feather derangement when exposed to even the thinnest ﬁsh oil, strongly suggests that ﬁsh oil discharges are at least as harmful to seabird plumage and seabird mortality as are petroleum oils.
with effects of exposure to edible oils on wildlife. As well, we interviewed an ecological researcher who had authored one of the few publications on the effects of ﬁsh oil on seabirds in the ﬁeld (see Michelle Bradshaw below). Wildlife rehabilitation experts were identiﬁed for interviews by means of referral from other wildlife experts or through an online discussion forum for Seabirds.net. In the discussion forum, Michelle Bradshaw polled the Seabirds.net community for information and observations regarding seabirds interacting with ﬁsh oil, and we followed up with individual respondents and their referrals. Our interviews focused on two principal questions:
3. Interviews with researchers, rehabilitation professionals, and veterinarians
1) Are marine birds sensitive to exposure to ﬁsh oils? 2) Are marine birds capable of recovering feather form and function before succumbing to the adverse effects of exposure?
Our experimental results suggest that feather microstructure is highly sensitive to exposure to ﬁsh oil, as it is for petroleum oils and likely any other types of oily substance. However, translating oil–feather interaction into effects on the whole organism is problematic because ﬁsh oil is edible and birds may be able to preen out the oil before any lasting physiological effects. Given the absence of published information on the effects of exposure to edible oils on whole marine bird organisms, we approached rehabilitation professionals and wildlife veterinarians as this group of professionals was most likely to have experience dealing 10
• Michelle Bradshaw nee Du Toit (Port Elizabeth Museum, South Africa) • Dr. Nola Parsons (SANCCOB, South Africa) • Dr. Sherri Cox (University of Guelph and the Toronto Wildlife Centre, Canada) • Monte Merrick (Bird Ally X, USA) • Deborah Jaques (Paciﬁc EcoLogic, USA) • Chris Battaglia and Jenny Schlieps (Focus Wildlife, Canada and USA) • Dr. Michael Ziccardi (University of California, Davis, Oiled Wildlife Care Network, USA) 3.1. Are marine birds sensitive to exposure to ﬁsh oils?
The following people were interviewed by phone or email:
Oil thickness (µm) Fig. 5. Amalgamation index for common murre feathers exposed to various thicknesses of sardine oil sheens on seawater. All treatments were signiﬁcantly different from each other (P b 0.01).
All interviewees agreed that marine birds are highly sensitive to exposure to ﬁsh oil (and all other oily substances). In all cases of ﬁsh oiling that were discussed, stricken birds were linked to ﬁsh oil by coincidental observations, and from appearance (i.e., colour, presence of ﬁsh scales) and odour of fouled feathers. In Namibia, high numbers of fouled Cape Gannets (Morus capensis) were observed in areas where birds had been seen ﬂoating and feeding around ﬁshery vessels that were processing ﬁsh while at-sea (Michelle Bradshaw). Stricken birds have been observed and captured for rehabilitation in areas where birds had been feeding under or near offal disposal pipes from ﬁsh processing plants (USA, Namibia, and South Africa: Michelle Bradshaw, Jenny Schlieps), and oiled birds had to be rescued from open tubs used to store ﬁsh offal for disposal from ﬁsh processing plants (California USA: Jenny Schlieps, Monte Merrick, and see for an example “Eureka Fish Oil, November 22, 2006”: http://www.humboldt.edu/mwcc/pastspills. html). A large number of oiled birds were recovered in Monterey Bay
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(California, USA) following a dump of rancid ﬁsh in October 1997 (Michael Ziccardi, and see L.A. Times archived article: http://articles. latimes.com/1997/oct/26/news/mn-46929). Also in California, large numbers of pelicans and other marine birds have been observed fouled with ﬁsh oil from offal pipes from ﬁsh processing tables that are publicly available in many marinas (Monte Merrick, Deborah Jaques: Jaques, 2013; Merrick, 2013). During the pre-release conditioning phase (as per Oiled Wildlife Care Network terminology), seabirds are often kept in warm water therapy pools or outdoor diving pools where they are fed ﬁsh. It is well established within the wildlife rehabilitation community that fats from food ﬁsh can create a buildup of oil on the surface of the pools' seawater causing re-oiling of birds and even mortality if birds are not re-cleaned. Because of this, recovery pools are constructed so that the surface water can be constantly ﬂushed with fresh seawater in order to remove any residue ﬁsh oil from food ﬁsh and faeces (Monte Merrick, Nola Parsons, Jenny Schlieps) and in some cases, polypropylene ﬁlters are used to remove ﬁsh oils (Michael Ziccardi). Indeed, one of the biggest challenges for rehabilitation centres is access to a large quantity of fresh water, and maintaining the recovery pools free of ﬁsh oil slicks is one of the main reasons that access to fresh water is so important (Jenny Schlieps). In some cases, ﬁsh with lower fat content is provided as food to prevent the formation of ﬁsh oil slicks at the water surface. However, providing ﬁsh with lower fat content can compromise the recovery of birds under care, and for this reason the decision to provide ﬁsh with less fat is complicated, involving the consideration of conservation status of birds under care, the quantity of stricken birds, and capacity of the response organizations to provide adequate care (Monte Merrick). 3.2. Are marine birds capable of recovering feather form and function before succumbing to the adverse effects of exposure? Self-recovery of feather form and function following exposure to ﬁsh oil or other edible oils appears to be difﬁcult despite the lack of toxicity. In Namibia, Michelle Bradshaw observed that few, if any, Cape Gannets were able to self-recover feather structure and function, particularly if the oil was mixed with guano. She noted that soaked gannets required approximately 3 days to “dry out” if they were able to return to shore. However, even if the birds were able to dry out over the three days, most birds become soaked again as soon as they returned to their feeding areas. Although ﬁsh oil is far less toxic than petroleum oils, it appears that birds cannot preen out ﬁsh oil. Standard rehabilitation protocol includes a form of triage during large events, prioritizing bird care when all birds cannot be washed at the same time. Bird Ally X, which is a non-proﬁt organization of wildlife care practitioners in California has resorted to triage during several of the ﬁsh oil fouling events, and birds were maintained up to three days before cleaning occurred. In none of these deferred cases were the birds able to clean themselves before being attended to by rehabilitators (Monte Merrick). Rehabilitation experts agree that in many cases ﬁsh oil (and other “edible” oils) is at least as difﬁcult to remove as petroleum oils, and can be more difﬁcult in some cases. Monte Merrick also noted that vegetable oils often require higher heat for effective removal, which can compromise the recovery of the birds under care. In the rancid ﬁsh dump case in Monterey Bay, very few of these birds were released (most were euthanized) because the Oiled Wildlife Care Network found it too difﬁcult to clean the birds sufﬁciently, largely because of the tacky consistency of the contaminant (Michael Ziccardi). Although information presented in this section is largely anecdotal, it is striking how consistent the observations were, that marine birds are sensitive to exposure to ﬁsh and other edible oils. As well, all agreed that exposure to ﬁsh oil necessitates intervention, suggesting that birds are no more able to preen and self-recover feather form and function as they are for petroleum oils.
4. Overall discussion and conclusions Although there is little information published on the effects of ﬁsh oil, it is clear that marine birds are highly sensitive to exposure to these and other edible oils. Serious and probably lethal consequences can occur for individual birds exposed to small amounts of ﬁsh oil. Our work experimentally shows that feathers are signiﬁcantly impacted when exposed to even barely visible, thin sheens of 0.04 μm of ﬁsh oil. Indeed, feathers appeared to be more vulnerable to ﬁsh oil than to crude oil with similar sheen thicknesses. The impact of ﬁsh oil is well-known in the rehabilitation community of experts, with wellestablished protocols to prevent oiling from food fed to captive birds. Although there is some anecdotal information linking physiological effects of exposure to ﬁsh oils and other edible oils, the primary mechanism of impact likely is by means of compromising the feather boundary that prevents water penetration and subsequent hypothermia. In this study we show experimentally how trace amounts of ﬁsh oil interact with feathers, providing a mechanism for how exposure to thin ﬁsh oil sheens causes disruption to feather microstructure and allows water and oil to penetrate the feather boundary. Expert opinion from our interviews establishes the link between feather disruption and ﬂuid uptake with effects on the whole organism, and further, that birds are unable to recover themselves following exposure even to trace amounts of ﬁsh oil. Experiments with live birds are necessary to explore sensitivity to these non- or less-toxic edible oils. The measurements of physiological stress, behavioural changes that affect ﬁtness (i.e., excessive preening in place of foraging), and ability to recover (i.e., remove substance and recover buoyancy and thermal regulation) would be some useful areas to explore. In addition, a comprehensive evaluation of ﬁsh oil discharges in marine waters and frequency of bird exposure and fouling would provide valuable information in order to assess the magnitude and extent of the problem. It is important to note that this report does not address species' vulnerability to exposure, which can vary among species and seasons. Species vulnerability depends on a number of factors including seasonal distribution and foraging mode. For example, surface feeders may be more likely to encounter a surface slick than a diver, because they tend to spend disproportionately more time at the surface (King and Sanger, 1979; Camphuysen, 1989; Williams et al., 1995). A species' population vulnerability to exposure may increase during the breeding season when they aggregate close to shore near their breeding colonies (O'Hara and Morgan, 2006). An additional consideration for edible oils is potential attractive qualities. Although an area where ﬁsh oil has been discharged may not previously have been frequented by seabirds, ﬁsh oil can attract individuals of some species from hundreds of kilometres away. Procellariform, or “tube-nosed” seabirds (i.e., albatrosses, petrels, and shearwaters) use their incredible olfactory capabilities to forage over 1000's of kilometres of patchily distributed prey (Warham, 1996; Nevitt et al., 2004). In an experiment conducted in the Antarctic, procellarids were highly associated with vegetable oil slicks scented with Herring oil (Nevitt et al., 2004). It is also fairly a common practice among ecotourism companies to “chum” the waters (i.e., introduce ﬁsh offal/oils) to attract seabirds to their observation platforms. In Canada, the discharge of a deleterious substance in an area frequented by migratory birds is considered illegal according to the Migratory Bird Convention Act. These ecotourism practices should be considered inadvisable based on the results of our experimental work, and what is generally well-understood in rehabilitation community regarding impacts on marine birds from exposure to ﬁsh and vegetable oils. Furthermore, policies surrounding disposal of ﬁsh offal should be evaluated and modiﬁed to reduce the likelihood of exposure to seabirds. We conclude that ﬁsh and potentially other edible oils are as harmful to marine birds as petroleum oils and therefore should not be regulated less stringently than petroleum oils simply because they are ‘edible’. Further, the potential for edible oils to attract seabirds rather than
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repelling them, as has been noted for some petroleum oil spills, necessitates rapid and thorough clean-up and rehabilitation response. Policy for support of enforcement activities is necessary in order to identify and prevent discharges of edible oils, particularly in circumstances where the discharge could concentrate as slicks at the water surface. Acknowledgements This study was supported by funds provided by Environment Canada. We owe Dr. John Dower (Department of Biology, University of Victoria) our gratitude for providing us with lab space and equipment. We thank Ken Morgan, Doug Bertram, and Laurie Wilson (Environment Canada) for providing access to their frozen birds, as well as to Owain McKibbon for providing us with further samples. Jarrott Brochez and Angela Walker (Investigations, Environment Canada) acquired crude sardine oil samples from the anonymous reception facility in Vancouver Harbour. We are indebted to numerous members of the wildlife response and rehabilitation community that provide their time and support for this project, particularly during the interview stage (Chris Battaglia, Deborah Jaques, Monte Merrick, Jenny Schlieps, and Drs. Sherri Cox, Nola Parson, and Michael Ziccardi). O'Hara was provided with in-kind support by the Institute of Ocean Sciences (Department of Fisheries and Oceans) during this study. References Anonymous. Oil spills affecting the Minnesota and Mississippi rivers, winter 1962–1963. Public Health Service, US Department of Health, Education and Welfare; 1963. p. 1–40. Anonymous. Fish oil kills seabirds, 28. African Wildlife; 1974. p. 24–5. Berry HH. Mass mortality of Cape Cormorants, caused by ﬁsh oil, in the Walvis Bay region of South West Africa. Madoqua 1976;9:57–62. Bucas G, Saliot A. Sea transport of animal and vegetable oils and its environmental consequences. Mar Pollut Bull 2002;44:1388–96. Camphuysen CJ. Beached bird surveys in the Netherlands 1915–1988; seabird mortality in the southern North Sea since the early days of oil pollution. Technisch Rapport Vogelbescherming, 1. Amsterdam: Werkgroep Noordzee; 1989. p. 322. Camphuysen CJ. Beached bird surveys indicate decline in chronic oil pollution in the North Sea. Mar Pollut Bull 1998;36:519–26. Camphuysen CJ. Seabirds and chronic oil pollution: self-cleaning properties of gulls, Laridae, as revealed from colour-ring sightings. Mar Pollut Bull 2011;62:514–9. Fabricius E. What makes plumage waterproof? Zoologisk Revy 1956;18:71–83. Giese M, Goldsworthy SD, Gales R, Brothers N, Hamill J. Effects of the Iron Baron oil spill on little penguins (Eudyptula minor). III. Breeding success of rehabilitated oiled birds. Wildl Res 2000;27:583–91. Hartung R. Some effects of oils on waterfowl. Ann Arbor, MI: University of Michigan; 1964. Hartung R. Energy metabolism in oil-covered ducks. J Wildl Manag 1967;31:798–804.
Irons DB, Kendall SJ, Erickson WP, McDonald LL, Lance BK. Nine years after the Exxon Valdez oil spill: effects on marine bird populations in Prince William Sound, Alaska. Condor 2000;102:723–37. Jaques, D, 2013. Brown Pelicans and ﬁsh waste handling conﬂicts in northern California harbors, Summer 2012. Paciﬁc Eco Logic report to the Kure/Stuyvesant Trustee Council, p. Unpubl. 20 pp. [email protected]
Jenssen BM. Review article — effects of oil pollution, chemically treated oil, and cleaning on the thermal balance of birds. Environ Pollut 1994;86:207–15. Jenssen BM, Ekker M. A method for evaluating the cleaning of oiled seabirds. Wildl Soc Bull 1988;16:213–5. Jenssen BM, Ekker M. Dose dependent effects of plumage-oiling on thermoregulation of common eiders Somateria mollissima residing in water. Polar Res 1991;10:579–84. King JG, Sanger GA. Oil vulnerability index for marine oriented birds. In: Bartonek JC, Nettleship DN, editors. Conservation of marine birds of northern North America; 1979. p. 227–39. Lambert G, Peakall DB, Philogene BJR, Engelhardt FR. Effect of oil and oil dispersant mixtures on the basal metabolic-rate of ducks. Bull Environ Contam Toxicol 1982;29: 520–4. Leighton FA. The toxicity of petroleum oils to seabirds; an overview. In: White J, editor. The effects of oil on wildlife. Hanover, PA: Sheridan Press; 1991. p. 43–57. Levy EM. Oil pollution and seabirds — Atlantic Canada 1976–77 and some implications for northern environments. Mar Pollut Bull 1980;11:51–6. McEwan EH, Koelink AFC. Heat production of oiled mallards and scaup. Can. J. Zool. (Revue Canadienne De Zoologie) 1973;51:27–31. McKelvey RW, Robertson I, Whitehead PE. Effect of non-petroleum oil spills on wintering birds near Vancouver. Mar Pollut Bull 1980;11:169–71. Merrick M. Reducing injury to brown pelicans in northern California harbors. Bird Ally X; 2013 [p. 12 pp. [email protected]
]. Nevitt G, Reid K, Trathan P. Testing olfactory foraging strategies in an Antarctic seabird assemblage. J Exp Biol 2004;207:3537–44. O'Hara PD, Morandin LA. Effects of sheens associated with offshore oil and gas development on the feather microstructure of pelagic seabirds. Mar Pollut Bull 2010;60: 672–8. O'Hara PD, Morgan KH. Do low rates of oiled carcass recovery in beached bird surveys indicate low rate of ship-source oil spills? Mar Ornithol 2006;34:133–40. Rigger D. Edible oils: are they really that different? International Oil Spill Conference; 1997. Rijke AM. Wettability and phylogenetic development of feather structure in water birds. J Exp Biol 1970;52:469–79. SAS. SAS for Windows Version 8.0. SAS Institute Inc. Cary, NC 1999. Smith DW, Herunter SM. Birds affected by a canola oil spill in Vancouver Harbour, February, 1989. Spill Technol Newsl 1989;14:3–5. Stephenson R. Effects of oil and other surface-active organic pollutants on aquatic birds. Environ Conserv 1997;24:121–9. Stephenson R, Andrews CA. The effect of water surface tension on feather wettability in aquatic birds. Can J Zool (Revue Canadienne De Zoologie) 1997;75:288–94. Swennen C. Keeping pelagic seabirds in captivity. Ibis 1978;120:112–3. Votier SC, Hatchwell BJ, Beckerman A, McCleery RH, Hunter FM, Pellatt J, et al. Oil pollution and climate have wide-scale impacts on seabird demographics. Ecol Lett 2005;8: 1157–64. Warham J. The behaviour, population biology and physiology of the petrels. London: Academic Press; 1996. Wiese FK, Robertson GJ. Assessing seabird mortality from chronic oil discharges at sea. J Wildl Manag 2004;68:627–38. Williams JM, Tasker ML, Carter IC, Webb A. A method of assessing vulnerability to surface pollutants. Ibis 1995(Suppl. 141):147–52.