1 Emma Lowe

Impacts of boat activity on Cardigan Bay (Tursiops truncatus) behaviour and their implications for the future Emma Lowe BSc (Hons) Marine Biology Stage 4

Project Advisor: Dr Clare Embling

2 Emma Lowe

Impacts of boat activity on Cardigan Bay bottlenose dolphin (Tursiops truncatus) behaviour and their implications for the future

Emma Lowe

Project Advisor: Dr Clare Embling 3 Emma Lowe

Abstract

Tursiops truncatus are a characteristic, social species that prefer coastal habitats, consequently come into contact with human activity. Cardigan Bay is subject to high levels of boat traffic during the summer months as tourism peaks, and there is increasing demand for dolphin watching trips. Bay is a small bay located on the Southern end of Cardigan Bay, and is a site often frequented by dolphins as feeding and nursing grounds. It is therefore questioned whether this intense vessel activity in New Quay bay is impacting the dolphins in terms of their behaviour. It was discovered that dolphins showed more staying behaviours, involving long dives and irregular surfacing when boats were present compared to when boats were absent (X2 = 17.1, d.f. = 6, p = 0.00876). These findings suggest that boat occurrence significantly affects dolphin behaviour. Other studies have reported similar results, with boat traffic causing short-term behavioural changes. The longer term implications of these behaviours would merit further study; however may involve site avoidance, reductions in biological fitness and lower breeding rates. Furthermore these impacts may be detrimental to the population of T. truncatus in Cardigan Bay, which are protected by the implementation of a Special Area of Conservation (SAC). This study suggests that further work is carried out to estimate the extent of damage being done to bottlenose dolphin populations via behavioural changes instigated by boat presence, and that stricter regulations are implemented in the code of conduct of the SAC to ensure effective protection of the species.

Keywords: Bottlenose dolphin, behaviour, human impacts, boat activity, ecology, Special Area of Conservation

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Introduction

Human vessel activities in the marine environment and their wide-ranging impacts on marine life have long been a cause for concern across the globe, notably influencing local megafauna and disrupting delicate ecosystems (Torres et al. 2011). Simply vessel presence in an environment has been observed to have significant effects on marine mammals, heavily influencing their behaviour and disturbing their regular patterns and activities (Lusseau et al. 2009, Richter et al. 2006). Marine mammals are impacted by boats on a large scale and in vastly different ways, from negative interactions with fisheries involving bycatch (Read, 2008), to interference with underwater acoustics (Erbe et al. 2002), and simply by disrupting natural behaviours (Blane & Jaakson 1994). This is observed on a global scale, in a number of cetacean species. As the tourism industry develops the demand for dolphin watching trips increases, putting more strain on marine mammals as they are increasingly disturbed by boats invading their habitat (Bejder et al. 1999, Ribeiro et al. 2005).

The bottlenose dolphin (Tursiops truncatus) is widely distributed and well-studied species in regions from Sarasota Bay in Florida to the Shannon Estuary in Ireland (Gregory & Rowden 2001). As a coastal dwelling species bottlenose dolphins are often subject to the effects of human activity, arguably the most of the odontocetes (Nowacek & Wells 2001). The semi-resident population found in Cardigan Bay, along the West coast (Wood 1998), is uniquely protected and has been frequently observed in the area from the 1920’s (Bristow & Rees 2001). In common with other coastal populations, the bottlenose dolphins of Cardigan Bay are specific to this site, identified as their home range (Hudson 2005), making it vitally important to their survival and success that their habitat is productive and remains undamaged (Ingram & Rogan 2002). Habitat protection via the use of reserves has shown to be effective for the conservation of megafauna. Conversely megafauna are useful indicators of ecosystem and trophic level health via both bottom-up, and top-down control, and are increasingly used for the design of these reserves (Heithaus et al. 2008, Hooker & Gerber 2004).

The Cardigan Bay bottlenose dolphins are observed most in the area from April through to October (Dunn et al. 2012, Gregory & Rowden 2001, Simon et al. 2010), however are not seen often during the winter months and tend to move offshore into the (Pierpoint et al. 2009). The number of dolphins present in the area peaks during the summer season (Bristow 2004, Pierpoint et al. 2009), and although calves are born all year round calving numbers are at their highest during the warmest months (Connor et al. 1996, Hudson 2005). Dolphins are regularly seen 15km from the coast (Gregory & Rowden 2001) mainly between Cardigan and in West Wales. This population although semi-resident, has been described as fluid as the individuals in the population differ annually, with some individuals disappearing for seasons at a time before returning (Bristow & Rees 2001). New Quay has been noted as one of the many favoured sites of the bottlenose dolphins (Gregory & Rowden 2001), and it is used as a feeding and nursing ground (Simmonds et al. 2013).

Cardigan Bay and Pen Llŷn a’r Sarnau have protected status as a Special Area of Conservation (SAC) by the EU Habitats directive, as part of the Natura 2000 (Fig. 1). The aim of this is to protect the bottlenose dolphins in the area, as well as sand banks and cobble reefs which are important features of the bay at risk from fishing activities; most notably scallop dredging for Pecten maximus (Hinz et al. 2010, Simon et al. 2010). This protected habitat stretches across 1000km2, over Cardigan Bay, and Pen Llŷn a’r Sarnau (Veneruso & Evans 2012). Despite the protection of Cardigan Bay concerns are 5 Emma Lowe

high regarding damage done to the habitat by commercial fisheries, which may have knock-on effects on the dolphins in the bay (Bear 2012, Pirotta et al. 2013, Smith 2012). Scallop dredging in particular has been singled out, due to destruction of the seabed and changes to the habitat being made (Robinson et al. 2001), which in turn causes disruption to the dolphins’ food chain. Additionally, a fish factory is located on New Quay headland, which releases discards into the water below, interfering with the local trophic levels, having potential implications for the dolphins (Denton 2012).

Fig. 1: Cardigan Bay’s location in the United Kingdom, and the area designated as an SAC where this study was based

Cardigan Bay is also subject to high levels of boat traffic, which peaks during the summer months coinciding with the peak in dolphin presence (Pierpoint et al. 2009). High numbers of tourist wildlife watching boats, fishing trips, commercial fishing vessels, recreational vessels such as canoes/kayaks, sail boats, and privately owned motorboats operate in the bay throughout daylight hours. A distinctive threat is posed to the dolphins here, in the form of disturbance, leading to behavioural changes (Lusseau et al. 2006) and site avoidance (Bejder et al. 1999, Kruse 1991). Disturbance poses potential impacts on the behaviour of these species, and as bottlenose dolphins are fairly long-lived, and this population is semi-resident, certain individuals may be repeatedly exposed to human activities. If these individuals feel threatened by boat activities they may become more sensitive to 6 Emma Lowe

vessel presence and exhibit avoidance behaviours (Constantine et al. 2004, Williams et al. 2006). This is particularly important for mother-calf pairs, as calves are born in the summer months, when boat activities are at their peak, which may impact their behaviour and long-term health, especially if it results in longer dives to avoid boats (Janik & Thompson 2006). An additional consideration is the population function as a whole, as vital behaviours are disrupted as dolphins have to exert time and energy avoiding these boats (Nowacek & Wells 2001). This may lead to less time for mothers to nurse their calves (Stensland & Berggren 2007), a decrease in reproductive output as socializing time is reduced (Lusseau 2004) and a decrease in biological fitness as energy budgets are interrupted by the need to avoid disturbances by boats (Bejder et al. 1999, Gregory & Rowden 2001).

As bottlenose dolphins are protected in areas worldwide to encourage their conservation, it is vitally important that we ensure that the measures being taken to protect this species are effective (Barros & Wells 1998). It is crucial that the local protection is effective at ensuring their conservation and protection as this is Britain’s largest breeding population of bottlenose dolphins. The findings of this study will be used to evaluate the effectiveness of measures in place to protect the bottlenose dolphins of Cardigan Bay, with a focus on investigating whether the local code of conduct effectively protects the species from disturbance via vessel activities (Bejder et al. 2006b, Nowasek & Wells 2001). Additional stress being applied to these dolphins by boat presence and changes to behaviour may have severe implications, potentially pushing them away from their habitat as they become increasingly disturbed (New et al. 2013, Lusseau 2005, Williams et al. 2006). The long-term impacts that may imprint on the dolphins are unknown, which makes it even more important to ensure that they are receiving adequate protection by the SAC from further stress and interference (Sini et al. 2005).

What this study aims to do, firstly, is to determine the impacts this boating activity may have on dolphin presence in the bay, which will contribute to the discovery of whether there is any short- term site avoidance occurring. Secondly, it will investigate whether boat activity in the bay impacts the behaviour of the dolphins; whether they exhibit some behaviour types more than others when in the presence or absence of boats. Finally, it will determine whether certain types of boat produce a behavioural response in the dolphins more than others. This will ascertain whether particular boats have more stressful and potentially detrimental impacts on the dolphins. Furthermore, this information could contribute to evidence supporting greater emphasis on the code of conduct. Other factors, such as sea state are also considered to allow for the elimination of bias in the data during particular environmental conditions. This study could support the view that there needs to be a more authoritative and rigorous form of controlling the behaviour of local vessels than a voluntary code of conduct. The work carried out aims to contribute to the work determining the best way forward to ensure that the bottlenose dolphins of the Cardigan Bay SAC are receiving appropriate and thorough protection.

The hypothesis this study is based on is that bottlenose dolphins will exhibit more reserved behaviours, involving long dives and milling in the area, and less active and characteristic behaviours such as leaping and lunging when boats are present compared to when they are absent.

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Methodology

Study site

Based on data between 2001 and 2007, the bottlenose dolphin population of Cardigan Bay is made up of between 121 and 210 individuals (Pierpoint et al. 2008). New Quay Bay was the study site used, which is a shallow bay, located in Cardigan Bay on the West coast of Wales, facing out to the Irish Sea towards the West and bound by land on the other three sides (Fig. 2). Cardigan Bay is a sheltered habitat with a depth on average around 40m (Evans, 1995). New Quay bay is comprised of a heterogenous seabed, with sediment made up of primarily gravel and stones, with sand in the bay, and behind the shelter of the harbour wall, and accumulated on the beach in front of the wall, between the wall and the headland further down the coast (Barnes 2011, Fig. 2). In deeper waters further out into there is sediment made up of stones and sand, showing primarily fine sediment, however towards the cardinal marker 1km away from the wall into the bay, the benthos is

Fig 2: Line diagram of the study area, and location of data collection.

comprised of rock, sand and weed, which provides a more complex, three dimensional habitat for the local ecosystem.

8 Emma Lowe

Vessel activities in the area

Various kinds of vessels run in New Quay bay almost all year round – however the peak of vessel activity is in the summer months, where visitor passenger boats (VPB) i.e. tourist and trip boats, are able to utilise good weather conditions and high levels of tourists and run around the clock during daylight hours, which were between 05:56 and 06:23 sunrise, and 20:36 and 20:02 sunset throughout August. 13 VPB boats operate in the bay, along with 6 commercial fishing boats, and there are 180 moorings for private boats in the bay. New Quay is a popular site in terms of fishing, and there are distinct fishing seasons that lead to recreational and commercial fishermen travelling to New Quay specifically to fish for species such as whelks (most notably Buccinum undatum), scallops (Pecten maximus) and herring (Clupea harengus).

Data collection

Data for this study were collected by volunteers of Cardigan Bay Marine Wildlife Centre (CBMWC), which enabled a more rigorous study of the bottlenose dolphins’ behaviour than already carried out by the CBMWC. Watches were carried out by volunteers in 2 hour shifts, usually from 9am until 5pm but occasionally starting at 7am and ending at 7pm. A watch in this context is the act of standing on land at a specific location, and consistently scanning the bay for marine mammals and observing the area attentively, both by eye and with the aid of binoculars. Watches were performed from New Quay harbour wall, which extended out into New Quay Bay, Cardigan Bay, West Wales (Fig. 1), where a volunteer would stand and watch for dolphin activity in New Quay harbour looking out at Cardigan Bay, with the aid of a pair of Nikon Waterproof Binoculars Sporter EX 8x42.

Volunteers were fully trained in data collection for land-based surveys prior to the beginning of the survey work, and all had backgrounds and experience in scientific data collection. Data was collected daily from 1st of August – 4th of September 2015, with trial runs being held on the 30th and 31st of July to test the effectiveness of the data collection sheets. August was chosen as the study period as the annual peak of vessel activity in the bay is during this month (Hudson, 2014).

A separate land survey sheet (See Fig. 1, Appendix) was used to record environmental conditions every 15 minutes, which were; Time, date, 15 minute period of the survey (designated letters A-H), sea state (using the Beaufort scale 0-6+), general weather conditions (a key provided to match weather conditions to a number), wind direction (a compass was used to determine from which direction the wind was blowing), species sighted, sighting location with the use of maps of the survey area, where the estimated location of the animal was plotted. Groups of dolphins studied were defined as individuals within 100 meters of one another (Barnes 2011) and exhibiting similar behaviours, showing social interaction between one another considerably more than with other individuals in adjacent areas (Irvine et al. 1981).

The study area extended roughly 2km out to sea, a cardinal marker was used to measure 1km from the harbour wall, and roughly a further kilometre was included in the survey area. Other landmarks such as terrestrial features that lined up and buoys were used to estimate distance.

Behaviour of dolphin groups was collected every 5 minutes, where a sighted group of dolphins were consistently observed and their behaviours noted down using the behaviour key (Fig. 2, Appendix). The main behaviours observed involved staying behaviours, such as milling at the surface and 9 Emma Lowe

carrying out dives, travelling behaviours where the dolphins were consistently heading in a direction, and fast-moving behaviours, including leaping, chasing fish at the surface, tail slapping and lunging (see Fig. 2 of Appendix for more details).

These behavioural codes were noted every 5 minutes on a separate data sheet (See Fig. 3, Appendix), and it was also noted whether the group of dolphins were within 300m of a boat during that 5 minute period, or not. Being within 300m of a boat was classed as a boat encounter. The total number of boats in the survey area was also noted every 5 minutes. If a group of dolphins did experience a boat encounter, additional data was required (Table 1) with use of the key provided and a map of the area with sections numbered 1-8. If more than one group of dolphins experienced a boat encounter, the first to have one was the group that was monitored closely and had additional information noted about it; this allows identification of which group this additional information is in reference to.

Table 1: Additional information collected when a group of dolphins experienced a boat encounter, i.e. a boat came within 300m of the group.

Parameter measured How measured/example How many boats within 300m Boat count of vessels within 300m Boat type Motorboat/ Sail boat/ Visitor Passenger Obeyed code of conduct? Yes, slowed gradually and stopped Group location Which grid on the map they were located in Immediate reaction by dolphins Tail slapping/ Deep dive/ leaping Which dolphin group experienced encounter G1/ G2 etc.

A maximum of 5 different groups of dolphins were recorded during the survey, as it would become difficult to effectively monitor more groups than this at one time, and reliability of the results would therefore be jeopardized. The number of dolphins in each group was also noted down.

Statistical analysis

Due to the data being count data, chi-square analyses were the most appropriate method for statistical analysis.

Dolphin presence and absence versus boat presence and absence in the total survey area were plotted, and a chi-squared analysis of the data was carried out, with the use of Microsoft Excel. The raw data was put into proportion, along with the expected values, and plotted onto a bar chart for visualisation (Fig. 3).

GLM analysis of dolphin presence absence, boat presence absence, and sea state in the total survey area was carried out using Minitab 7 software.

A chi-square analysis was executed on the data involving dolphin behaviour, and boat presence and absence. Each behaviour type was treated as a different category, and put against boat presence or absence in a chi-square table. 10 Emma Lowe

The same statistical test was then used to compare observed and expected values in terms of boat type, and dolphin behaviour, which involved boats being within 300m of the dolphins. This raw data was plotted on a bar chart showing the proportion of time dolphins spent exhibiting each behaviour when experiencing a boat encounter with different boat types (Fig. 4, appendix). The code for each boat type is also explained in the appendix (Fig. 5, appendix).

The additional data collected when dolphins experienced a boat encounter was not statistically analysed for the purpose of keeping this study focussed on boat occurrence. However the detailed nature of this additional information does provide scope for further study, and investigation into and identification of precise parameters causing behavioural changes in bottlenose dolphins.

Results

A total of 2373 observations were made, where each observation was a 5 minute watch period, collected from August 1st to September 4th 2015. Data was collected between the hours of 7am to 7pm, equating to 197.75 hours’ worth of effort, during all tidal states and weather conditions except for in cases of extreme weather.

Dolphin and boat presence

There was a significant effect of boat presence on dolphin presence (X2=55.4, d.f.=3, p=<0.0001, n=2373). There were significantly more dolphins present in the bay when boats were also present than expected shown by Table 2. There were also fewer observations of dolphins when boats were absent than expected. When boats were present in the bay there were fewer observation periods without dolphins present than expected, so dolphins were present more in the bay alongside boats than predicted by the expected values.

Table 2: Observed and expected data of dolphin presence/absence and boat presence/absence

Conditions Observed Expected No dolphins, no boats 396 332.7 Dolphins, no boats 57 120.3 No dolphins, boats 1349 1410.3 Dolphins, boats 571 509.7

A general linear model showed that both boat presence and sea state significantly impact dolphin presence/absence (Dolphin occurrence ~ Boat occurrence + Sea state, p= 0.005, <0.0001). Dolphin presence was shown to be impacted by Beaufort sea states 1-4, however there was no significant relationship between dolphin presence and sea state when at sea states 5 and 6. Sightings rates were reduced as sea state increased, shown by Table 1, appendix. This however can be explained by the difficulty to spot cetaceans at sea states of this magnitude (Barco et al. 1999, Forney 2000).

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Dolphin behaviour

Fig. 3 shows that long dives (S3) were carried out less than expected when boats were not present in the bay. Fast circling, tail slapping and lunging behaviours (S6) were displayed less than expected when boats were present, and in proportion this behaviour was displayed the least when boats were present. S3 behaviours were observed more in the bay when boats were present than expected, in proportion. There was little difference between observed and expected values for travelling behaviours T1 and T2, however differences were seen in T3 rapid travelling, where without boats present there were no observations of this behaviour at all, however this behaviour was observed only very occasionally overall in the sheltered bay of a survey area. Table 4 shows the corresponding codes and behaviours used in the experiment.

Fig. 3: The observed and expected proportion values of dolphin behaviour with and without boats present.

Dolphin behaviour was shown to be significantly impacted by boat occurrence (X2 = 17.1, d.f. = 6, p = 0.00876). This showed that the observed amount dolphins carry out various behaviours with and without boat present in the survey area are significantly different to what was expected (Table 3). These results back up the pattern that is shown by the proportion data, where staying and long dive behaviours (S3) are observed more than expected with boats present, and less than expected without boats present in the bay. Additionally, S6 behaviours (see Table 4) are observed less than expected with boats present, and almost twice as much as expected when boats are absent from the survey area. Behaviours S3 and S6 are of greatest value in this study, as they represent a high contrast in behaviour dependant on boat occurrence, and they achieve expected values over the value of 5.The other values have limited value and trustworthiness due to their corresponding expecting values being below 5.0. 12 Emma Lowe

Table 3: Observed and expected dolphin behaviours with and without boats present

Behaviour With Boats Without Boats Observed Expected Observed Expected S2 44 49.1 10 4.9 S3 336 324.6 21 32.4 S4 3 2.7 0 0.3 S6 68 74.6 14 7.4 T1 43 43.6 5 4.4 T2 76 75.5 7 7.5 T3 1 0.9 0 0.1

Table 4: Codes used in the study and the bottlenose dolphin behaviours they represent

Code Corresponding behaviour S2 Staying – slow circling, milling around (mingling) at the surface S3 Staying – long dives, potentially foraging at depth S4 Chasing prey at surface, fish seen S6 Staying – fast circling (mingling) at surface, leaps, tail slaps or lunges T1 Travel – regular surfacing, all animals keep same, consistent heading making determined progress T2 Travel – long dives, surfacing at irregular intervals, thought to be searching for prey while on the move T3 Travel – rapid progress with forward leaps or otherwise splashy surfacing

Additional data

A chi-squared test was also run on data on boat type and behaviour, however obtained a result that showed boat type did not significantly impact dolphin behaviour (X2 = 28.353, d.f. = 30, p = 0.552). Fig. 4, appendix, shows this raw data, in proportion.

Discussion

Dolphin occurrence, sea state and boat occurrence

The relationship between sea state and dolphin presence may be partially explained by the fact that dolphin sightings are significantly reduced above sea states of 3 on the beaufort scale, due to reduced ability to see dorsal fins in choppier conditions (Barco et al. 1999, see Table 1., appendix). However the result that there are significantly fewer dolphins observed in the bay when there are boats present is indicative that boats are having a negative impact on the dolphins; they are actively avoiding the bay when there are boats present. This could eventually lead to long-term site avoidance of New Quay Bay, if there is short-term avoidance of the area. Lusseau’s study from 2005 13 Emma Lowe

looking at Tursiops truncatus in New Zealand demonstrates similar results; dolphins were shown to avoid the site of heavy boat traffic when there is a particularly great amount of vessel activity (Lusseau 2005).

Differences in behaviour with boats present and absent

Bottlenose dolphins were shown to carry out staying behaviours with long dives significantly more in the presence of boats than without boats. This could mean that when boats are nearby, they are spending their time primarily underwater, where they are less exposed, as they feel threatened. This has been also observed in a number of other studies, where dolphins increase the length of their dives and time spent underwater in the presence of boats, and breathing and surfacing rate is seen to significantly decrease (Hastie et al. 2003). Hastie et al.’s work also showed that synchronous breathing in individuals in a group of dolphins significantly increased in the presence of boats, this could be indicative of some kind of defence mechanism against the anthropogenic disturbances the dolphins are faced with. When exposed to boat traffic, Tursiops species have been shown to increase their dive duration and this is widely treated as a behavioural trait associated with avoidance (Seuront & Cribb 2011).

When boats were absent from the bay, bottlenose dolphins were shown to carry out splashy and active behaviours, involving staying, fast circling, mingling at the surface, leaps, tail slaps or lunges, more regularly than when boats were present. They also display more playful and outgoing behaviours that may make them more vulnerable when there are not boats around compared to when boats are in the area, showing that they’re more comfortable displaying these behaviours when boat traffic is relatively quieter, and able to carry out usual behaviours that are disrupted in the presence of vessels (Steckenreuter at al. 2012).

Other literature report that bottlenose dolphins exhibit widely ranging behavioural responses to boat activities, from increasing swimming speed and directly avoiding boats (Bejder at al. 2006), to being attracted to and interacting with vessels (Gregory & Rowden 2001). Attraction to boats was also observed in New Zealand where Hector’s dolphins approached boats within the first 10-50 minutes of them entering the bay (Bejder et al. 1999). Some studies have even shown bottlenose dolphin indifference to the presence of boats, where they have become acclimated to vessels being nearby for so long that they no longer respond behaviourally to this disturbance (Acevedo 1991, Hudson 2005). However the results of this study contradict reported positive reactions or indifference to boat presence, as the dolphins behave in an elusive and reserved manner around the boats in Cardigan Bay. Hastie et al.’s study from 2003 reinforces the notion that boats are a negative disturbance to dolphins, and alludes to bottlenose dolphins seeing boats as a threat. Bottlenose dolphins were shown to respond to boat presence by increasing their breathing synchrony and by becoming a more tightly packed group (Hastie et al. 2003), a behaviour also observed by other studies (Steckenreuter et al. 2012). This compact formation has been suggested as an antipredatory behavioural response, as they are more prepared to respond to danger (Bejder et al. 2006a, Lusseau 2006). Bejder et al’s study (1999) supports this theory, where Hector’s dolphins form tighter groups in the presence of boats, which has been associated with dolphins being threatened or in danger, so that they provide enhanced protection on an individual scale (Bejder et al. 1999).

These various responses can cause significant short term implications for these marine mammals; widely explored by a number of studies where the impacts of boat presence are distinctively 14 Emma Lowe

impacting dolphin behaviour (Lusseau et al. 2006). However long-term implications of these of these behavioural responses are poorly understood and difficult to predict in terms of the health of populations of bottlenose dolphins and other cetaceans in the future (Lemon et al. 2006). An example of this is an increase in the amount of time spent underwater and less regular surfacing around boats, which could have physiological impacts on the population (Hastie et al. 2003). Mother and calf pairs would be most vulnerable to these impacts due to the requirement of newborns and calves to breathe more frequently than adult individuals (Hastie et al. 2003). Additional stress placed on the calves of these slow growing and maturing species, along with their low fecundity rate may have detrimental effects on the population as a whole (Currey at al. 2009, Seuront & Cribb 2011). Avoidance of high volumes of vessel activities could also eventually cause some site avoidance, in the short term and potentially long-term. A study on Killer Whales (Orcinus orca) in British Columbia found that orcas made direct heading for open water when approached by boats, out of the narrow Johnstone strait to less restrictive waters where they may potentially avoid vessels (Kruse 1991). The Indo-Pacific dolphin Tursiops aduncus off the south coast of Zanzibar also displayed a negative response to boat traffic; when boats were present female dolphins and their calves showed direct avoidance behaviour by increasing travelling (Stensland & Berggren 2007). There is concern that these behavioural responses eventually lead to site avoidance, and displacement of dolphins from their local ranges (Bejder et al. 1999). Additionally, Lusseau’s report (2004) noted that boat presence reduced the time dolphins spent socializing, which has previously been closely linked to the fecundity of dolphin populations. This suggests that an increase in boat disturbance of dolphin groups may decrease the overall reproductive output of the population, and decrease rates of pregnancy as breeding success is reduced (Bejder et al. 1999, Lusseau 2004).

Some studies have alluded to consequences in terms of the wellbeing of mother and calf pairs, such as a decrease in time available for mothers to nurse their calves as they are spending more of their time avoiding boat traffic (Stensland & Berggren 2007). This reinforces the concern that mother and calf pairs are most at risk to the costs of disturbance by heavy boat traffic. Bejder et al. (1999) also suggested that there may be long-term costs in terms of biological fitness, where dolphins have to exert a great amount of time avoiding boats, as their critical energy budgets become interrupted by high use of avoidance strategies (Bejder et al. 1999).

Conversely, long diving and staying behaviours, with inconsistent surfacing patterns could be associated with foraging, so it may be that the dolphins are simply feeding at that time, and underwater for longer and surfacing less regularly as they are in pursuit of prey. However, the shallow nature of the bay makes this unlikely, as it would be more likely to see the dolphins splashing at the surface if they were feeding (Gregory & Rowden 2001). This additional theory however is supported by the work of Engas et al. (1995), where dolphins could be responding to boats by spending more time underwater and diving deeply due to prey aggregations as a result of boat presence. Engas et al. (1995) found that cod (Gadus morhua), and herring (Clupea harengus), both school together into dense and organised clusters, and swim towards the seabed in response to boat engine noise. This may reflect the way dolphins appear more reserved around boats; they are simply spending more time foraging. As these fish are able to hear and respond to boat engine noise over vast distances, just having boats within the survey area may have instigated a response in the behaviour of these fish, which would then have a knock-on impact on dolphin behaviour as they respond opportunistically to this sudden influx of prey aggregations, and spend more time foraging in response to this food source. Dolphins have a wide range of prey species (Pesante et al. 2008, 15 Emma Lowe

Santos et al. 2001) hence it is widely believed that they feed opportunistically, which supports the argument that they would exploit a temporary rich food source. The behaviours observed in Cardigan Bay when boats were present however also involved a great amount of milling in the area along with irregular surfacing, which has been noted by Steckenreuter at al. (2012) as behaviour increased four times in the presence of boats compared to their absence (Steckenreuter at al. 2012). The array of evidence supporting behavioural changes in bottlenose dolphins in response to boats as a threat overwhelms the argument making it more plausible that they are negatively responding directly to boat presence (Bejder et al. 2006a, Hastie et al. 2003, Ingram & Rogan 2003, Lusseau 2006, Lusseau et al. 2006). This reinforces the idea that boats are causing high levels of disturbance to bottlenose dolphins, causing changes to natural, regular behaviours, with implications for populations that we can only estimate (Constantine 2001, Ingram & Rogan 2003, Lusseau & Higham 2004).

Conclusions and recommendations for Cardigan Bay as a SAC

As boats have been shown to impact bottlenose dolphin, correct and appropriate protection for this species is crucial. The protected status of Cardigan Bay as a SAC does allow boats to oprate in the area, as long as they adhere to the Marine Code of Conduct. This dictates that boats may not approach within 100m of dolphins or speed towards them, must slow down to a minimum speed and make no sudden or erratic changes in course and not attempt to touch, feed or swim with marine mammals in the area (Ceredigion County Council Department of Environmental Services and Housing 2015). However it is questionable whether this is providing sufficient protection for the dolphins. Concerns were raised by Nowacek & Wells where it was suggested that boat traffic causing behavioural changes and associated implications such as changes in breathing, is technically a form of harassment, as their usual behaviours are disrupted (Nowack & Wells 2001). The indisputable fact that there is a distinct difference in the way Tursiops truncatus behaves when around boats compared to when boats are not present illustrates that boats are having an impact on their behaviour and therefore population health (Stensland & Berggren 2007). This suggests that heavy boat traffic in Cardigan Bay could be unsustainable in the future, as the tourism industry grows in New Quay levels of boat traffic are likely to increase to meet growing demands for dolphin watching trips (Currey et al. 2009).

It is reflective of other studies that dolphins are responding to these vessels in the bay as a threat, and will respond accordingly to what they precieve as a danger to them (Bejder et al. 2006a, Lusseau 2006). These responses however when exhibited too regularly, are in fact a threat to the wellbeing of the dolphins, and so their being induced increasingly by the presence of boats may lead to detrimental impacts on the population (Lemon et al. 2006). It is consequently recommended that additional studies are carried out to consistently monitor dolphin behaviour in response to boat traffic, to ensure a thorough understanding of the extent of the impacts of boat disturbance in New Quay. Further work could investigate parameters recorded in this study however were not examined, such as relationship between whether boats adhere to the code of conduct, and dolphin behaviour. Findings such as these, along with more rigorous investigations into the impacts of boats on dolphin behaviour, as well as monitoring over entire seasons, will allow an informed decision to be made in terms of protecting this local population in the long term. However, a precautionary approach should be adopted in terms of site management, and stricter measures implemented in the code of conduct to ensure minimum impacts to the dolphins (Currey et al. 2009), as simply a 16 Emma Lowe

voluntary code of conduct may not be enough to motivate boats operating in the area to adhere to the rules in place. Correct operation of vessels around marine mammals is the very least that can be done at the present time to ensure minimal disturbance; however this study and other work highlights that there is an issue with boat traffic and its impact on bottlenose dolphins, which requires further investigation and careful monitoring as the outcomes and long term implications can not yet be predicted.

Acknowledgements

I would like to give a massive thank you to Sarah Perry of Cardigan Bay Marine Wildlife Centre for all of her tremendous help throughout the making of this project. I am also very grateful to the CBMWC volunteers who helped with the data collection throughout the month of August; including Rhian Forrest, Masa Svent, James Clarke, Michael Naylor, Rhiannon Nichol, Laura Evans and Samantha Patek, along with everyone else at CBMWC for all of their help. Additionally I am very grateful to Dr Clare Embling for all of her help and guidance as my advisor for this project. Finally I would like to thank my family, Sam and Matt for their unfailing support throughout all of my work.

Cited Literature

Acevedo A (1991) Interactions between boats and bottlenose dolphins, Tursiops truncatus, in the entrance to Ensenada De La Paz, Mexico. Aquat Mamm 17:120-124.

Bailey H, Thompson P (2010). Effect of oceanographic features on fine-scale foraging movements of bottlenose dolphins. Mar Ecol Prog Ser 418:223-233.

Barco S, Swingle W, Mlellan W, Harris R, Pabst D (1999) LOCAL ABUNDANCE AND DISTRIBUTION OF BOTTLENOSE DOLPHINS (TURSIOPS TRUNCATUS) IN THE NEARSHORE WATERS OF VIRGINIA BEACH, VIRGINIA. Mar Mamm Sci 15:394-408.

Barnes C (2011) Social structure of bottlenose dolphins (Tursiops truncatus) in Cardigan Bay, Wales. BSc dissertation, School of Science and Technology, Plymouth University, Plymouth, Devon

Barros NB, Wells RS (1998) Prey and Feeding Patterns of Resident Bottlenose Dolphins (Tursiops truncatus) in Sarasota Bay, Florida. J Mammal 79:1045-1059.

Bear C (2012) Assembling the sea: materiality, movement and regulatory practices in the Cardigan Bay scallop fishery. Cult Geogr 20:21-41.

Bejder L, Dawson S, Harraway J (1999) RESPONSES BY HECTOR'S DOLPHINS TO BOATS AND SWIMMERS IN PORPOISE BAY, NEW ZEALAND. Mar Mamm Sci 15:738-750.

Bejder L, Samuels A, Whitehead H, Gales N (2006)a Interpreting short-term behavioural responses to disturbance within a longitudinal perspective. Anim Behav 72:1149-1158. 17 Emma Lowe

Bejder L, Samuels A, Whitehead H, Gales N, Mann J, Connor R, Heithaus M, Watson-Capps J, Flaherty C, Krutzen M (2006)b Decline in Relative Abundance of Bottlenose Dolphins Exposed to Long-Term Disturbance. Conserv Biol 20:1791-1798.

Blane JM, Jaakson R (1994) The Impact of Ecotourism Boats on the St Lawrence Beluga Whales. Environ Conserv 21:267-269.

Bristow T, Glanville N, Hopkins J (2001) Shore-based monitoring of bottlenose dolphins (Tursiops truncatus) by trained volunteers in Cardigan Bay, Wales. Aquat Mamm 27:115-120.

Bristow T, Rees EIS (2001) Site fidelity and behaviour of bottlenose dolphins (Tursiops truncatus) in Cardigan Bay, Wales. Aquat Mamm 27:1-10.

Cairns DK (1987) Seabirds as Indicators of Marine Food Supplies. Biol Oceanogr 5:261-271.

Ceredigion County Council Department of Environmental Services and Housing, (2015) Ceredigion Marine Code, Ceredigion.

Ceredigion County Council, the Countryside Council for Wales, Environment Agency Wales, North Western and Sea Fisheries Committee, Coast National Park Authority, Pembrokeshire County Council, South Wales Sea Fisheries Committee and Dŵr Cymru Welsh Water and EC LIFE-Nature Programme., (2008). Cardigan Bay Special Area of Conservation (SAC) Management Scheme. Ceredigion, 18-27.

Connor R, Smolker R, Richards A, Mann J (1996) Patterns of Female Attractiveness in Indian Ocean Bottlenose Dolphins. Behaviour 133:37-69.

Constantine R (2001) INCREASED AVOIDANCE OF SWIMMERS BY WILD BOTTLENOSE DOLPHINS (TURSIOPS TRUNCATUS) DUE TO LONG-TERM EXPOSURE TO SWIM-WITH-DOLPHIN TOURISM. Mar Mamm Sci 17:689-702.

Constantine R, Brunton D, Dennis T (2004) Dolphin-watching tour boats change bottlenose dolphin (Tursiops truncatus) behaviour. Biol Conserv 117:299-307.

Currey R, Dawson S, Slooten E (2009) An approach for regional threat assessment under IUCN Red List criteria that is robust to uncertainty: The Fiordland bottlenose dolphins are critically endangered. Biol Conserv 142:1570-1579.

Currey R, Dawson S, Slooten E, Schneider K, Lusseau D, Boisseau O, Haase P, Williams J (2009) Survival rates for a declining population of bottlenose dolphins in Doubtful Sound, New Zealand: an information theoretic approach to assessing the role of human impacts. Aquat Conserv 19:658-670.

Denton J (2012) Bottlenose dolphin (Tursiops truncatus) abundance in Cardigan Bay, Wales, in relation to shellfish factory discards. BSc Dissertation, University, Swansea, Wales.

Dunn J, Still R, Harrop H (2012) Britain's Sea Mammals. Princeton: Princeton University Press.

Engås A, Misund O, Soldal A, Horvei B, Solstad A (1995) Reactions of penned herring and cod to playback of original, frequency-filtered and time-smoothed vessel sound. Fish Res 22:243-254. 18 Emma Lowe

Erbe C (2002) UNDERWATER NOISE OF WHALE-WATCHING BOATS AND POTENTIAL EFFECTS ON KILLER WHALES (ORCINUS ORCA), BASED ON AN ACOUSTIC IMPACT MODEL. Mar Mamm Sci 18:394-418.

Forney K (2000) Environmental Models of Cetacean Abundance: Reducing Uncertainty in Population Trends. Conserv Biol 14:1271-1286.

Furness RW, Tasker ML (2000) Seabird-fishery interactions: quantifying the sensitivity of seabirds to reductions in sandeel abundance, and identification of key areas for sensitive seabirds in the North Sea. Mar Ecol Prog Ser 202:253-264.

Hastie G, Wilson B, Tufft L, Thompson P (2003) BOTTLENOSE DOLPHINS INCREASE BREATHING SYNCHRONY IN RESPONSE TO BOAT TRAFFIC. Mar Mamm Sci 19:74-084.

Heithaus M, Frid A, Wirsing A, Worm B (2008) Predicting ecological consequences of marine top predator declines. Trends Ecol Evol 23:202-210.

Hinz H, Scriberras M, Benell JD, Kaiser MJ (2010) Assessment of offshore habitats in the Cardigan Bay SAC. Fisheries & Conservation Report, Bangor University, 11-254.

Hooker S, Gerber L (2004) Marine Reserves as a Tool for Ecosystem-Based Management: The Potential Importance of Megafauna. BioScience:27.

Hudson T (2005) Bottlenose dolphin (Tursiops truncatus) response to vessel activity in New Quay Bay. MSc thesis, School of Ocean Sciences, Bangor University, Bangor, Wales.

Ingram S, Rogan E (2003) Bottlenose dolphins (Tursiops truncatus) in the Shannon Estuary and selected areas of the west-coast of Ireland. Report to the National Parks and Wildlife Service, Ireland, 28.

Irvine AB, Scott MD, Wells RS, Kaufmann JH (1981). Movements and activities of the Atlantic Bottlenose Dolphin, Tursiops truncatus, near Sarasota, Florida. Fish Bull 79:671-688.

Janik V, Thompson P (2006) CHANGES IN SURFACING PATTERNS OF BOTTLENOSE DOLPHINS IN RESPONSE TO BOAT TRAFFIC. Mar Mamm Sci 12:597-602.

Kruse S (1991) The Interactions between Killer Whales and boats in Johnstone Strait, B.C. In: Pryor K, Norris K, (ed) Dolphin Societies: Discoveries and Puzzles, 1st ed. Berkeley and Los Angeles: University of California Press, California, p 149-159.

Lemon M, Lynch T, Cato D, Harcourt R (2006) Response of travelling bottlenose dolphins (Tursiops aduncus) to experimental approaches by a powerboat in Jervis Bay, New South Wales, Australia. Biol Conserv 127:363-372.

Lusseau D (2004) The hidden cost of tourism: detecting long-term effects of tourism using behavioural information. Ecol Soc 9:1-10.

Lusseau D (2005) Residency pattern of bottlenose dolphins Tursiops spp. in Milford Sound, New Zealand, is related to boat traffic. Mar Ecol Prog Ser 295:265-272. 19 Emma Lowe

Lusseau D (2006) THE SHORT-TERM BEHAVIORAL REACTIONS OF BOTTLENOSE DOLPHINS TO INTERACTIONS WITH BOATS IN DOUBTFUL SOUND, NEW ZEALAND. Mar Mamm Sci 22:802-818.

Lusseau D, Bain D, Williams R, Smith J (2009) Vessel traffic disrupts the foraging behavior of southern resident killer whales Orcinus orca. Endang Species Res 6:211-221.

Lusseau D, Higham J (2004) Managing the impacts of dolphin-based tourism through the definition of critical habitats: the case of bottlenose dolphins (Tursiops spp.) in Doubtful Sound, New Zealand. Tourism Manage 25:657-667.

Lusseau D, Slooten L, Currey R (2006) Unsustainable Dolphin-watching Tourism in Fiordland, New Zealand. TME 3:173-178.

New L, Harwood J, Thomas L, Donovan C, Clark J, Hastie G, Thompson P, Cheney B, Scott- Hayward L, Lusseau D (2013) Modelling the biological significance of behavioural change in coastal bottlenose dolphins in response to disturbance. Funct Ecol 27:314-322.

Nowacek SM, Wells RS (2001) Short-term effects of boat traffic on Bottlenose Dolphins, Tursiops truncatus, in Sarasota Bay, Florida. Mar Mamm Sci 17:673-688.

Pierpoint C, Allan L, Arnold H, Evans P, Perry S, Wilberforce L, Baxter J (2009) Monitoring important coastal sites for bottlenose dolphin in Cardigan Bay, UK. J Mar Biol Assoc UK 89:1033- 1043.

Pirotta E, Laesser B, Hardaker A, Riddoch N, Marcoux M, Lusseau D (2013) Dredging displaces bottlenose dolphins from an urbanised foraging patch. Mar Pollut Bull 74:396-402.

Read A (2008) The looming crisis: interactions between marine mammals and fisheries. J Mammal 89:541-548.

Ribeiro S, Viddi F, Freitas T (2005) Behavioural Responses of Chilean Dolphins (Cephalorhynchus eutropia) to Boats in Yaldad Bay, Southern Chile. Aquat Mamm 31:234-242.

Richter C, Dawson S, Slooten E (2006) IMPACTS OF COMMERCIAL WHALE WATCHING ON MALE SPERM WHALES AT KAIKOURA, NEW ZEALAND. Mar Mamm Sci 22:46-63.

Robinson S, Bernier S, MacIntyre A (2001) The impact of scallop drags on sea urchin populations and benthos in the Bay of Fundy, Canada. Hydrobiologia 465:103-114.

Santos M, Pierce G, Reid R, Patterson I, Ross H, Mente E (2001) Stomach contents of bottlenose dolphins (Tursiops truncatus ) in Scottish waters. J Mar Biol Assoc UK 81:873-878.

Seuront L, Cribb N (2011) Fractal analysis reveals pernicious stress levels related to boat presence and type in the Indo–Pacific bottlenose dolphin, Tursiops aduncus. Physica A 390:2333- 2339.

Simmonds M, Green M, James V, Eisfeld S, Lott R (2013) Assessing the Cardigan Bay bottlenose dolphin SACs. ECOS 34:46-55. 20 Emma Lowe

Simon M, Nuuttila H, Reyes-Zamudio MM, Ugarte F, Verfub U, Evans PGH (2010) Passive acoustic monitoring of bottlenose dolphin and harbour porpoise, in Cardigan Bay, Wales, with implications for habitat use and partitioning. J Mar Biol Assoc UK 90:1539-1545.

Sini M, Canning S, Stockin K, Pierce G (2005) Bottlenose dolphins around Aberdeen harbour, north-east Scotland: a short study of habitat utilization and the potential effects of boat traffic. J Mar Biol Assoc UK 85:1547.

Smith H (2012) Population dynamics and habitat use of bottlenose dolphins (Tursiops aduncus), Bunbury, Western Australia. Ph.D. Dissertation, Murdoch University, Perth, Australia.

Steckenreuter A, Möller L, Harcourt R (2012) How does Australia’s largest dolphin-watching industry affect the behaviour of a small and resident population of Indo-Pacific bottlenose dolphins? J Environ Manage 97:14-21.

Stecker M (2016) Map of the United Kingdom. (image) Available at: http://mstecker.com/pages/uk_fp.htm (Accessed 19 Mar. 2016).

Stensland E, Berggren P (2007) Behavioural changes in female Indo-Pacific bottlenose dolphins in response to boat-based tourism. Mar Ecol Prog Ser 332:225-234.

Torres L, Thompson D, Bearhop S, Votier S, Taylor G, Sagar P, Robertson B (2011) White-capped albatrosses alter fine-scale foraging behavior patterns when associated with fishing vessels. Mar Ecol Prog Ser 428:289-301.

Veneruso G, Evans PGH (2012) Bottlenose Dolphin and Harbour Porpoise Monitoring in Cardigan Bay and Pen Llŷn a’r Sarnau Special Areas of Conservation. CCW Monitoring Report No. 95, p 66.

visitMyHarbour (2015) New Quay: Chart of New Quay Bay. Available: http://www.visitmyharbour.com/harbours/wales-nw-england/new- quay/chart/F2771306A8CC1/chart-of-new-quay-bay. Last accessed 4th Aug 2015.

Williams R, Trites A, Bain D (2006) Behavioural responses of killer whales (Orcinus orca) to whale-watching boats: opportunistic observations and experimental approaches. J Zool 256:255-270.

Williams R, Lusseau D, Hammond P (2006) Estimating relative energetic costs of human disturbance to killer whales (Orcinus orca). Biol Conserv 133:301-311.

Wood C (1998) Movement of bottlenose dolphins around the south-west coast of Britain. J Zool 246:155-163.

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Appendix

Fig. 1: The data collection sheet used for collecting environmental data and general sightings information 22 Emma Lowe

Fig. 2: Key to the codes of various behaviours and conditions potentially observed during a watch 23 Emma Lowe

Fig. 3: Table used to collect data on dolphin behaviour whilst on watch 24 Emma Lowe

Table 1: The number of observations (5 minutes watches) of each sea state achieved

Sea State (Beaufort scale) Number of observations 0 0 1 882 2 783 3 264 4 294 5 144 6 6

Fig. 4: The various behaviours shown by dolphins when experiencing an encounter with different boat types, in proportion

25 Emma Lowe

Table 2: Codes used and their corresponding boat type

Code used Boat Type VPB Visitor Passenger Boat C Canoe/Kayak SAIL Any boat under sail MB Motor boat SB Speed boat/ RIB CF Commercial Fishing vessel