Harbor porpoise displacement by a solitary bottlenose dolphin in the Baltic Sea

Abstract

Top predators affect ecosystems by controlling prey populations both directly through consumption and indirectly through fear (Brown et al., 1999; Suraci et al., 2016). The threat of predation affects the foraging and spatial behavior of prey species and can even drive emigration from areas with higher predation risk (Bowlby et al., 2023; Jorgensen et al., 2019; Suraci et al., 2016).

Harbor porpoises (Phocoena phocoena) are the smallest and one of the most abundant and widely distributed cetaceans in the Northern Hemisphere (Bjørge & Tolley, 2018). From what we know, the main predators of harbor porpoises are killer whales Orcinus orca (Cosentino, 2015), white sharks Carcharodon carcharias (Arnold, 1972), and gray seals Halichoerus grypus (Leopold, 2015); in some regions they are also killed/harassed by common bottlenose dolphins (Tursiops truncatus) without further consumption (Cotter et al., 2012; Jepson & Baker 1998; Ross & Wilson, 1996; Wilkin et al., 2012).

In contrast to their popular image as the iconic “smiling dolphin,” bottlenose dolphins can exhibit marked aggressiveness. Agonistic interactions have been reported not only between adult males (Parsons et al., 2003), but also by males directed towards females (Scott et al., 2005) and calves (Kaplan et al., 2009; Robinson, 2014). Moreover, bottlenose dolphins often behave aggressively towards other cetacean species, particularly those of smaller size, including Guiana dolphins (Sotalia guianensis, Wedekin et al., 2004), short-beaked common dolphins (Delphinus delphis, Puig-Lozano et al., 2020), Atlantic spotted dolphins (Stenella frontalis, Herzing & Johnson, 1997; Puig-Lozano et al., 2020), and Commerson's dolphins (Cephalorhynchus commersonii, Coscarella & Crespo, 2009). However, the most commonly reported target of bottlenose dolphin interspecific aggression is the harbor porpoise.

Bottlenose dolphin aggression towards harbor porpoises was originally reported from the Moray Firth, Scotland (Ross & Wilson, 1996). Four violent dolphin-porpoise interactions were witnessed, and most porpoises stranded in that area were observed to have multiple skeletal fractures and damaged internal organs. Similar cases were noticed in Cardigan Bay, Wales (Jepson & Baker, 1998) and in Monterey Bay, California (Cotter et al., 2012; Wilkin et al., 2012).

Behavioral observations potentially offer insights into the underlying motivations driving attack behavior. Cotter et al. (2012) found that in all cases where the sex of attacking dolphins in California was identified, the aggressors were always males. As most attacks occurred at the height of the breeding season it was suggested that “porpicide” (porpoise killing) was a form of aggressive play in frustrated males with high testosterone levels, limited access to receptive females, and was possibly related to infanticide practices observed in bottlenose dolphins. Some ecological hypotheses have also been suggested, including prey competition and feeding interference, but the support for them has been weak due to the little dietary overlap between the species (Cotter et al., 2012; Jacobson et al., 2015).

In areas where harbor porpoises are regularly attacked by bottlenose dolphins, porpoises avoid spatio-temporal overlap with dolphins. A study in California (where the two species habitats overlap) showed that the acoustic activity of porpoises was lower when dolphins were present than when they were absent (Jacobson et al., 2015). Nuuttila et al. (2017) found the fine-scale temporal partitioning between the species in Cardigan Bay at three levels: seasonal, with more porpoises in winter and dolphins in summer; diel, with more porpoises at night and more dolphins shortly after sunrise; and tidal, with more dolphins during ebb and more porpoises at slack water. Williamson et al. (2022) reported a spatiotemporal segregation of porpoises and dolphins in Moray Firth, with porpoises staying more offshore than dolphins and less likely to occur prior to dolphin detections. However, it is unknown whether these patterns arise from individual experience with dolphins, local tradition of dolphin avoidance or instinct.

Harbor porpoises are the only native cetacean species in the Baltic Sea and Inner Danish waters (Benke et al., 1998), therefore these porpoise populations do not normally experience dolphin aggression. Bottlenose dolphins are known to enter the Baltic Sea occasionally and stay there for periods from months to years, causing a temporary threat to porpoises. For example, in 2016, a solitary male bottlenose dolphin stayed in Schleswig-Holstein area of the Baltic Sea for three months, and several stranded porpoises with unusual blunt force trauma were found during that period (Gross et al., 2020). There were also several videos in the social media of dolphins harassing porpoises in the Little and Great Belt during that time. Nevertheless, there is no resident dolphin population that could pose permanent danger to porpoises, keeping them in constant fear and vigilance. When a new dolphin appears in the Baltic Sea, most porpoises do not have previous experience with this species that would warn them of the potential danger. It is not known whether porpoises have an instinctive fear of dolphins and dolphin sounds. Therefore, it is not obvious how presence of a dolphin would affect the distribution and behavior of porpoises: whether they will avoid the area inhabited by the dolphin, or whether they will continue to use it in a normal way.

Invasive predators are one of the most important causes of species declines worldwide (Doherty et al., 2016). Even though dolphins do not consume killed porpoises and therefore they are not predators in the strict sense, they can affect porpoise populations in the same way as predators affect their prey. It is therefore important to monitor the effects of dolphin presence on the local population of harbor porpoises. Even though these species are known to coexist in many places, dolphins' colonization of new areas can potentially have far reaching implications for naive porpoises. In this study, we report the results of passive acoustic monitoring of an area in the western Baltic Sea where a solitary male bottlenose dolphin resided for 3.5 years. The dolphin was reported killing harbor porpoises at least twice, in August 20201 and 2022.2 We determined whether the presence of the dolphin affected the spatial distribution of harbor porpoises in the area occupied by the dolphin.

The study was conducted in the waters south of the island of Funen, Denmark (Figure 1). A solitary bottlenose dolphin settled in Svendborgsund (a channel between the islands Funen and Tåsinge, with both sides encompassing the harbor of the town Svendborg) in September 2019. The dolphin was nicknamed Delle by the locals, but later it was matched to the photoidentification catalog from Moray Firth, Scotland (University of Aberdeen, 2019) as individual #1022 nicknamed Yoda. According to the catalog, the dolphin was a subadult male born in 2007.

According to reports by local observations reported on social media such as the Danish Facebook pages Vores delfin i Svendborgsund and Delles venner, it used a restricted area in Svendborgsund. The dolphin was often seen in Svendborg harbor and in the area around Svendborgsund Bridge and sometimes further west in the channel all the way to Rantzauminde village. It was never reported from locations outside the channel during his stay in this area. It left the area on the April 8, 2023, when it was spotted in Nyborg, which is approximately 30 km north from Svendborg. On April 23, Delle was seen in Trawemünde, Germany where it spent approximately 3 weeks. After that it was occasionally seen in other locations at German Baltic coast, and at the time of writing it had not been observed again in Denmark.

To assess the presence of porpoises before Delle's arrival, we used citizen science data obtained through Smartphone app Marine Tracker that was developed by Martin Slusarczyk Hubel from the University of Southern Denmark. The app allows the public to report the encounters with harbor porpoises around Funen. The app was launched in April 2019 and has so far collected more than 6,000 observations considered trustworthy around Funen (Jakobsen et al., 2024). We used the app data on porpoise sightings from April to August 2019. We did not use data from September 2019 and onwards as these may include sightings of Delle, as many people may not be able to discern a dolphin from a porpoise. The citizen science data indicated that before the dolphin settled in Svendborg, sightings of harbor porpoises were common in Svendborgsund, as well as in areas west of Tåsinge and in Faaborg (Figure 2).

The presence of the dolphin and porpoises over the course of this study in December 2022–September 2023 was assessed using six F-PODs (Chelonia Ltd., 2020). The F-PODs are new generation click detectors, the successors of the C-PODs. F-PODs have higher detection rates than C-PODs and were reportedly better for monitoring fine-scale behaviors (Todd et al., 2023).

The F-PODs were deployed close to Svendborg in the area used by the dolphin, as well as west of Tåsinge Island and off Faaborg where Delle was not observed (Figure 1). The F-PODs were deployed in locations 1–6 (Figure 1) on December 8, 2022, and retrieved on February 14 and 15, 2023. On April 9, 2023, we deployed F-PODs in locations 1, 2a, 3a, 7 and 8, and on June 4, 2023, in location 4 in Faaborg. On July 8, 2023, we retrieved F-PODs from locations 7 and 8, and on September 27, from locations 1, 2a, 3a and 4. A total of 1,161 full days of data was obtained with the F-PODs. Locations 2a and 3a had slightly different positions than locations 2 and 3 for logistical reasons, but the data from locations 2 and 2a as well as 3 and 3a were pooled for modeling purposes (see below).

It has been shown that the position of a click logger in the water column affects the number of detections: significantly more harbor porpoise clicks were detected at the click loggers moored in the water column, closer to the surface, compared with those near the seabed (Alonso & Nuuttila, 2014). Therefore, all our F-PODs were moored in the same position close to the seabed at similar depths of approximately 9–10 m.

To analyze the data, we used the F-POD software (Chelonia Ltd., 2022). F-PODs record the center frequency, frequency trend, duration, intensity, and bandwidth of clicks in the frequency range 20–160 kHz. F-POD software subsequently analyzes the recorded click trains and classifies them into three categories: narrow-band high frequency clicks of porpoises, lower wide-band clicks of other cetaceans (in our case represented only by Delle), or clicks from boat sonars. The output indicates the level of confidence (low, moderate, or high) in classification. To minimize the risk of including a significant number of false positive detections, only click trains with high and moderate level of confidence in classification were used in our analyses. The error rate of F-POD automatic classification has been shown to be extremely low: the fraction of porpoise false positives was less than 0.1% and for dolphins the corresponding error rate was 0.97% (Ivanchikova & Tregenza, 2023). The F-POD software allowed us to inspect the occurrence of clicks from different categories visually, as well as export the data for the subsequent statistical analysis.

We used acoustic data to quantify porpoise and dolphin presence in the study area. Detections of echolocation click trains were recorded as a count of detection-positive minutes (DPM, minutes containing at least one click train) in each day. Statistical analysis of porpoise detections was conducted using generalized additive mixed models (GAMM) with logarithmic link function and negative binomial distribution to account for overdispersion. The response variable was the total number of porpoise DPM per day. Explanatory variables included dolphin presence, dolphin DPM per day, season, temperature, and boat sonar DPM per day. Dolphin presence was a binary variable (yes/no) that had a value “yes” in locations 1–3 for all days during the winter deployment, no matter whether dolphin click trains were registered during that day or not, and a value “no” for all other locations and seasons. The motivation for adding this variable was the fact that porpoise presence can be more related to the mere fact of potential dolphin presence in the area, rather than to his immediate level of acoustic activity. Location was included in the model as a random variable. Location 2a was pooled with location 2, and location 3a was pooled with location 3 for the modeling purposes, because these locations were separated only by a few kilometers distance and had similar features. To select the best model, we sequentially removed the variables from the model and calculated Akaike's information criterion (AIC) for each model (Burnham & Anderson, 2002). The model with the lowest AIC was selected as the best model. Statistical analyses were carried out in R (R Core Team, 2023) using R packages mgcv, gamm, and nlme.

Porpoise DPM varied substantially across the locations and in time (Figure 3). Dolphin detections were often registered during the winter in locations 1 and 2 (Svendborg harbor and Svendborgsund), and to much lesser extent in location 3 (channel east of Svendborg harbor), suggesting uneven usage of the area by the dolphin. Dolphin clicks were registered in either location 1 or 2 in all but one days during the winter deployment, confirming the reports from the locals of the daily dolphin presence in the area (Figure 3).

The final GAMM included the variables dolphin presence, dolphin DPM per day, season and boat sonar DPM per day. The temperature variable was dropped based on the AIC value. After dropping the temperature variable AIC of the model decreased by 29 units. Dropping any of the other variables increased AIC, therefore they were retained in the final model. All variables in the final model were significant (dolphin presence: F = 132.344, df = 1, p < .0001; dolphin DPM per day: F = 6.378, df = 1, p < .05; season: F = 24.416, df = 2, p < .0001; boat sonar DPM per day: F = 15.94, df = 2.45, p < .0001).

Dolphin presence was the most significant variable in the model. There were fewer harbor porpoise acoustic detections in locations where and when the dolphin regularly occurred (Figures 3 and 4). Some of this difference can be attributed to seasonal variation. However, the differences in porpoise detections between winter and summer seasons were much less pronounced in the location 4 in Faaborg where the dolphin never occurred, than in Svendborg locations (1, 2/2a, and 3/3a) where the dolphin was present during the winter (Figures 3 and 4).

Boat sonars had pronounced effect on porpoise detections, but it was unclear to what extent it was caused by porpoise avoidance of boats and to what extent by the masking effect of the sonars on porpoise detections by F-PODs. Svendborg harbor (location 1) had one or two orders of magnitude higher levels of boat sonar DPMs per day than other locations (Figure 4), which probably contributed to the low levels of porpoise acoustic detections there in the spring and summer after the dolphin left the area. Variation in winter porpoise detections across three locations in Faaborg (4–6) were also likely related to the differences in boat sonar occurrence.

Porpoise detections increased in some locations in August–September. However, as it was observed both in the locations where the dolphin was present (1 and 3a) and absent (4) during the winter, it is possible that this increase was caused by environmental factors rather than delayed porpoise recovery after the dolphin's departure.

The results of our study demonstrate that harbor porpoise acoustic detections substantially decreased in the area inhabited by the bottlenose dolphin. Over the course of a 2-month investigation during the winter, when the dolphin was observed in Svendborgsund, our data recorded significantly reduced instances of acoustic detections of porpoises in three deployment locations (1–3) where the bottlenose dolphin regularly occurred, compared to nearby Faaborg where the dolphin was not observed (locations 4–6; Figure 3). Citizen science data collected prior to the dolphin's arrival also demonstrate that porpoises were common both in Svendborg and Faaborg.

Subsequent to the departure of the bottlenose dolphin from the area in the spring and summer, we observed an increase in the number of porpoise detections in both Svendborgsund (locations 1, 2a, and 3a) and Faaborg (location 4), suggesting seasonal shift in porpoise presence. Nevertheless, the decrease in winter porpoise detections was substantially more pronounced in Svendborgsund than in Faaborg (Figures 3 and 4), which could be attributed to the combined effects of season and dolphin absence.

An important limitation of our study is that all detections (except for the citizen science data) were made acoustically, so if an animal remained silent, its presence went undetected. Therefore, we were unable to resolve whether harbor porpoises were responding to bottlenose dolphin presence by leaving the area or by reducing vocal activity to avoid detection. Observations of porpoise reactions to 15 kHz pinger tone playbacks showed that they can both change their acoustic behavior and leave the area (Elmegaard et al., 2023). Four of the six porpoises in that study decreased their click rate while one porpoise substantially increased the click rate during the exposure; five out of six animals increased distance to sound source while increasing swimming effort. Future investigations could significantly benefit from supplementing acoustic monitoring of dolphin impacts on porpoises with visual observations, biologging studies and eDNA analysis.

We found that in the GAMM, the variable “dolphin presence” was substantially more significant than the variable “dolphin DPM.” “Dolphin presence” was a binary variable that reflected the possible dolphin presence in locations 1–3 during the winter and the absence of dolphin in the winter in Faaborg and in the summer in all locations. “Dolphin DPM” was the number of detection positive minutes of the dolphin click trains per day. Therefore, “dolphin DPM” reflected the immediate acoustic presence of the dolphin, while “dolphin presence” indicated the potential presence of the dolphin in the area. The fact that “dolphin presence” explained more variation in porpoise acoustic detection than “dolphin DPM” implies that the mere fact of potential dolphin presence in the area held greater significance for porpoises than his immediate level of acoustic activity. Porpoises avoided the area around Svendborg not only in response to acoustic indications of the dolphin's presence, but also during periods, at times lasting several days, when no acoustic cues suggested the immediate presence of the dolphin. This behavior is particularly evident at location 3, where dolphin detections were infrequent; nonetheless, porpoises demonstrated avoidance patterns similar to those observed at the other two locations.

This phenomenon is akin to the concept of a “landscape of fear” (Laundré et al., 2010). According to this concept, the presence of predators that constrain habitat choice gives rise to a “landscape of fear” shaped by spatial variation in the predators' occurrence, which can have far reaching ecological implications. The risk of predation affects the spatial and foraging behavior of prey, which in turn can alter the whole ecosystem through trophic cascade (Suraci et al., 2016). Besides, the frightened prey eats less, and the mere presence of predators may affect the trophic chain by decreasing the pressure of their prey on the lower trophic levels (Suraci et al., 2016).

Harbor porpoises are not consumed by bottlenose dolphins, therefore, one can argue that strictly speaking they cannot be considered the dolphins' prey. However, as porpoises are being killed by the dolphin, from a porpoise perspective there is no difference whether it is consumed afterwards or not. Besides, indirect effects can regulate not only the predator–prey interactions, but also the interactions among co-occurring top predators when the shared resources are not necessarily limited in terms of abundance. Interference competition rather than competition for food was suggested to be a limiting factor for a leopard (Panthera pardus) population overlapping in distribution with tiger (Panthera tigris) territories (Odden et al., 2010). Brief visits from killer whales displaced white sharks from Farallon Islands, disrupting shark feeding behavior and decreasing shark predation pressure on pinnipeds (Jorgensen et al., 2019).

Alien predators are more dangerous than native predators because prey are often naïve to the hunting tactics of novel alien predators (Salo et al., 2007). In areas where dolphin and porpoise ranges naturally overlap, their segregation is established over a long period of co-existence. Porpoises can learn to adjust their area usage patterns to avoid dolphins from their mothers, or they can develop instinctive avoidance mechanisms. In areas where dolphins do not normally occur, porpoises need to relay either on personal experience of interactions with dolphins, or on the instinctive predator avoidance mechanisms.

In our study porpoises avoided the area around Svendborg where the dolphin occurred, despite their limited or virtually nonexistent prior experience with dolphins. There are two plausible hypotheses to account for this behavior. First, given that the dolphin spent more than 3 years in Svendborgsund by the time of our study, it is conceivable that porpoises may have commenced avoiding the area following aggressive interactions with the dolphin, albeit surviving these agonistic encounters. It remains a possibility that the dolphin caused fatalities in only a few instances, while in other cases, it engaged in aggressive pursuits that resulted in nonlethal injuries. However, there were no reports of harmless chases by the local observers, and all reported interactions were characterized as exceedingly aggressive and most likely fatal to the porpoises involved.

Alternatively, it is possible that harbor porpoises have an instinctive fear of dolphins and dolphin sounds, which could account for their avoidance of Svendborgsund. In this scenario, porpoises would exhibit avoidance behaviors in response to the mere presence of dolphin sounds, without any direct interspecies interactions taking place. Such a behavioral mechanism could explain why pingers that are attached to gill nets where they regularly emit dolphin-like sounds, are so efficient in reducing bycatch (Larsen & Eigaard, 2014).

Furthermore, it is plausible that porpoises demonstrate caution when confronted with any new unfamiliar sounds. Research on other marine mammals supports this notion, as demonstrated by Deecke et al. (2002), who reported that harbor seals Phoca vitulina exhibited avoidance responses to unfamiliar killer whale vocalizations but did not react to familiar, nonthreatening calls produced by fish-eating killer whales.

Our data suggest that porpoise presence in Svendborgsund recovered to levels comparable to Faaborg and western Tåsinge (where the dolphin did not occur) just a few days after the dolphin left the area (except for the location 1 in Svendborg harbor, where porpoise click trains could have been masked by an order of magnitude higher levels of boat sonar occurrence, Figure 4). This fast recovery can be related to the seasonal changes in porpoise occurrence, as the dolphin left Svendborgsund in early April, when many new porpoises not aware of the dolphin presence were probably arriving to the area following their seasonal migration patterns. Unfortunately, we cannot estimate how soon the local porpoises that were keeping away from Svendborgsund because of the dolphin presence started using the area again after its departure. Nevertheless, we can claim that the habitat was colonized by porpoises almost immediately after the dolphin left, suggesting that dolphin presence only affects porpoises in real time and does not have long-lasting effects on porpoise habitat exclusion. A similar pattern was demonstrated by Kindt-Larsen et al. (2019) who found that porpoises returned to the area during silent periods of pingers running on 23 hr on/off cycles.

Understanding how alien predators affect their prey is a significant conservation objective. It is important both to identify and protect prey species at risk, and to ensure efficient and targeted management of the problem (Salo et al., 2007). The results of our study are crucial for predicting the ecological implications of bottlenose dolphin range expansion in the eastern North Atlantic. In the last years, bottlenose dolphins are often seen in areas of Europe where they have not normally occurred. In Denmark, a group of bottlenose dolphins (some of them being immediate relatives of the Svendborg's dolphin) currently inhabit the western entrance of Limfjord near the town of Thyborøn.

Even a small number of novel top predators can cause significant shifts in local biodiversity and trophic chains. For example, in South Africa two male killer whales that started preying upon sharks caused a major change in their distribution over a few years (Towner et al., 2022). This killer whale pair was first documented in False Bay in 2015, preying upon sevengill sharks, which led to their disappearance from a large aggregation site in False Bay (Engelbrecht et al., 2019). In 2017, the same killer whale pair started preying upon large white sharks in Gansbaai, displacing them from that area (Towner et al., 2022). This in turn decreased white shark predation on Cape fur seals (Arctocephalus pusillus), leading to physiological and behavioral changes in this species (Hammerschlag et al., 2022).

More effort is needed to monitor the effects of dolphin presence on the local population of harbor porpoises and its consequences for the ecosystem. The recent SCANS-IV survey showed that the estimate of harbor porpoises in Belt Sea was considerably lower than the estimates for 2016, although the data had a high level of uncertainty that did not allow to detect a trend in abundance (Gilles et al., 2023). Our findings strongly suggest that harbor porpoises may be influenced by the presence of bottlenose dolphins in two ways. First, the lethal bottlenose dolphin attacks could potentially lead to a direct reduction in the population of harbor porpoises. The second potential impact pertains to the creation of a “landscape of fear” leading to the reduction in fitness as a result of exclusion from suitable habitat. Even though the numbers of bottlenose dolphins in Denmark appear to be too low to cause significant effects, it is vital to recognize that even a small number of novel top predators can cause far reaching ecological implications. Moreover, future scenarios may involve an increase in the number of dolphins in the area, driven by immigration from other regions, in response to climatic shifts and ecological transformations in the North Atlantic.

Olga A. Filatova: Data curation; formal analysis; investigation; methodology; visualization; writing – original draft; writing – review and editing. Ivan D. Fedutin: Conceptualization; investigation; methodology; resources. Freja Jakobsen: Methodology; resources. Lotte Kindt-Larsen: Resources. Magnus Wahlberg: Conceptualization; funding acquisition; resources; supervision.