Kristina Lehnert
Elehna Bethune2
Ellen Schulz-Kornas
Ursula Siebert
Thomas M. Kaiser- 1Institute for Terrestrial and Aquatic Wildlife Research (ITAW), University of Veterinary Medicine Hannover, Foundation, Büsum, Germany
- 2Centre for Taxonomy and Morphology, Leibniz Institute for the Analysis of Biodiversity Change (LIB), Hamburg, Germany
- 3Department of Cariology, Endodontology and Periodontology, Leipzig University, Leipzig, Germany
Introduction: Marine mammals are apex predators in the marine environment and seals are known as opportunistic hunters which adapt to prey availability in their distribution range. Knowledge about harbour seal diet is a crucial baseline parameter to assess environmental change in marine ecosystems, however inferring diet composition in marine animals remains challenging. The harbour seal subpopulations in the German North Sea and Danish Kattegat region underwent strong population dynamics during the last centuries. In the 1960s/70s they had undergone declines due to hunting pressure and pollutant exposure and experienced mass mortalities caused by virus epidemics in 1988. The hunting bans and conservation measures implemented since then in different areas may have altered the dietary preferences and foraging ecology of harbour seal populations in the Danish Kattegat and the German Wadden.
Methods: In this study the tooth abrasion in harbour seals from two geographic regions is investigated to infer on their foraging ecology by taking advantage of dental microwear texture analysis (DMTA) in archived museum specimens. The upper dentition of 82 harbour seals originating from seal skulls collected during 1988 (German Wadden Sea) and the 1970/80s (Danish Kattegat) in museum archives were analysed using DMTA to infer dietary abrasiveness.
Results: Significant differences in dental microwear textures (DMT) between the Wadden Sea and Kattegat harbour seal groups were revealed. Danish Kattegat female harbour seals, and to a smaller extent Kattegat males, around the island of Hesselø displayed the roughest DMT reflecting a significantly higher intake of abrasives compared to the Wadden Sea harbour seals. The lack of significant DMT differences within the Hesselø subpopulation and the high variability of DMT in Hesselø females suggest a more generalistic foraging strategy as a response to high intra-specific competition in the protected area surrounding Hesselø.
Discussion: The slightly shifted DMT within Wadden Sea seals might be linked to a sexual segregation of foraging strategies in a larger, more resourceful North Sea habitat. DMTA is useful to reveal intra-specific foraging strategies in museum specimens from the past and different geographic regions. The novel technique opens new options to infer foraging dynamics in wildlife populations, taking advantage of valuable skeletal material from historic specimens in natural history collections, and offers new perspectives for non-invasive texture measurements on the dentition of live aquatic mammals. Information about foraging ecology of seal species related to anthropogenic stress in the past can inform current conservation and management in the face of environmental change.
1 Introduction
Since the 20th century, the population of harbour seals (Phoca vitulina Linnaeus, 1759) in North European waters has been highly impacted by anthropogenic influences. Increased hunting pressure in the early 20th century, motivated by subsistence, commerce or local bounties, led to a dramatic drop in seal numbers (Reijnders, 1980; Heide-Jørgensen and Härkönen, 1988). Additionally, as a result of industrialisation and urbanisation, the harbour seal population development was increasingly affected by pollution, disturbances and shifts in prey availability (Drescher et al., 1977; Reijnders, 1980; Reijnders, 1986). In the early 20th century, the harbour seal populations in Danish waters were dwindling due to intensive hunting, accelerated by a government-financed bounty system (1889–1927) (Olsen et al., 2018). As a result, harbour seals were mostly restricted to a few haul-out sites on Kattegat islands in 1930 (Søndergaard et al., 1976; Joensen et al., 1976). In the year 1951, a protected area for seals was established at Hesselø, a small island in the south-eastern Kattegat (Søndergaard et al., 1976; Joensen et al., 1976). During the next two decades, most of the harbour seal populations experienced a constant reduction in distribution and numbers, while Hesselø became the only breeding ground with a marked population increase (Joensen et al., 1976). Despite the protection, a number of harbour seals at Hesselø were killed for some years in the 1960s for the Zoological Museum in Copenhagen (Søndergaard et al., 1976). In a conservation story of success, the Hesselø stock increased from 250 individuals in the late 1960s to over 500 individuals in 1975 (Søndergaard et al., 1976). With the introduction of the Game Act in 1967, harbour seals in Danish waters were protected during the reproductive season (June to August) until the final implementation of a complete hunting ban on harbour seals in 1977 (Joensen et al., 1976; Olsen et al., 2010). The harbour seals of the German Wadden Sea experienced a lower hunting pressure than in the Kattegat. Whereas the Danish bounty system encouraged any citizen to hunt seals, the Federal Hunting Act of 1958 entitled only appointed game keepers to cull the seal population (Hoffmeyer, 1962). Although seal hunting during pupping season has been forbidden in German waters since 1938 (Hoffmeyer, 1962), harbour seal numbers were impacted by hunting pressure and pollutant exposure, and as a response to low numbers, seal hunting was gradually prohibited. The harbour seal subpopulations of the German Wadden Sea have been protected since 1971/1973 (Lower Saxony/Schleswig-Holstein) and monitored since 1974 (Reijnders, 1980). In 1988, the first outbreak of phocine distemper virus (PDV) killed up to 60% of North Sea harbour seals (Dietz et al., 1989; Heide-Jørgensen et al., 1992; Härkönen et al., 2006). The impact on the harbour seal subpopulation in the German Wadden Sea was evident in aerial surveys with 4,900 adults counted in 1987 and 2,500 adults in 1989 (Brasseur et al., 2018).
Studying foraging in marine mammals is difficult due to their vagile behaviour and aquatic environment, and existing studies on diet composition have therefore focused mostly on indirect observations from hard parts retained in stomach contents, stable isotopes or, more recently, metabarcoding (Sievers, 1989; de La Vega et al., 2016; Boyi et al., 2022). Diet and distribution studies have shown that harbour seals typically are associated with coastal waters, forage at relatively shallow depths and are generalist and opportunistic feeders with a preference for foraging for demersal or benthic prey species (Härkönen, 1988; Olsen and Bjørge, 1995; Thompson et al., 1996; Andersen et al., 2007; Dietz et al., 2012; Sherman et al., 2016; Aarts et al., 2019). Under optimal conditions, harbour seals would adapt their foraging behaviour to local conditions, such as substrate, water depth and prey abundance (Sharples et al., 2012). However, it is yet unknown to what extent the foraging behaviour in the last century was affected by anthropogenic impact in the form of hunting and culling (Olsen et al., 2018). Without stomach content analyses, faecal or soft tissue samples, indirect proxies to reconstruct the harbour seals’ diet prior to the hunting ban from preserved skeletal remains in museum collections are crucial (Feddern et al., 2021; Kershaw et al., 2021). Dental microwear texture analysis (DMTA) using ISO parameters was established as a measure of dietary composition reflected by dietary abrasiveness (Schulz et al., 2010). DMTA measures the microscopic wear or abrasive patterns on teeth caused by various foods or sediment materials like grit (Arman et al., 2019). This method can be a valuable tool for inferring the diets of mammals and provides information on biomechanical properties of the food items ingested, like scaliness or exoskeletons of prey organisms, yet not about the actually ingested species themselves (Calandra and Merceron, 2016).
Incorporating intra-specific variation into DMTA became a promising tool in terrestrial mammals to improve the resolution of dietary reconstruction to reveal feeding ecology, e.g. in field voles from two Finish Lapland localities (Calandra et al., 2016), Australian tree-kangaroos (Arman et al., 2019) and rodents from the rainforest (Robinet et al., 2022), as well as the arctic habitats (Ungar et al., 2021), and revealed in chimpanzees the abrasive effect of dust (Schulz-Kornas et al., 2019) and seasonal dietary fluctuations (Stuhlträger et al., 2019, Stuhlträger et al., 2021). Differences in dental microwear texture (DMT) reflected village or pristine rainforest habitat in black rats in Madagascar and, by proxy, anthropogenic impact (Winkler et al., 2016). Furthermore, DMTA has since been successfully used to infer on the diet of various extant and recent carnivores, e.g. from wolves (Burtt and DeSantis, 2022; Schulz-Kornas et al, 2024), bears (Peigné and Merceron, 2019) and also on odontocetes (Purnell et al., 2017), which catch and hold on to their prey in a similar piercing bite like seals. Thus, DMTA has been established recently as a dietary proxy in aquatic environments and of feeding behaviour in pinnipeds (Bethune et al., 2021).
In this study, intra-specific variations in harbour seal tooth abrasion related to foraging behaviour and anthropogenic impacts are investigated. Two distinct seal subpopulations, the heavily hunted Kattegat subpopulation from the 1960s/1970s and the more protected Wadden Sea subpopulation of 1988, are comparatively analysed using DMTA. Among temporal and geographic differences between the two study areas, hunting pressure could influence habitat use and dietary composition in harbour seals from both areas, with significant differences between protected seals from 1988 in the Wadden Sea and harbour seals under hunting pressure between 1960 and 1972 at the Southern Kattegat region. As Danish harbour seals were restricted to a few insular haul-out sites before the hunting ban, it is speculated that access to some foraging grounds and prey items was limited and may have increased intra-specific competition, resulting in differences in dietary abrasiveness detectable via DMTA. We expected that the dietary abrasiveness was shaped by prey biomechanics—mainly size/shape (swallowability), toughness of the fish scales and exoskeletons (processability) and escape performance (catchability)—and foraging ground characteristics, e.g. sediment load due to turbulence in the water column of the respective ecosystem. DMTs of the Hesselø subpopulation are expected to be more variable, reflecting a higher variance in prey selection, including more abrasive foraging grounds and prey items, compared to Wadden Sea harbour seals.
2 Materials and methods
2.1 Specimen selection
This study focused on the upper dentition of skeletal material from harbour seal specimens of two subpopulations (Figure 1). The first subpopulation of harbour seals in this study consisted of Danish harbour seal specimens from Hesselø, a small island in the south-eastern Kattegat region, and specimens were collected between 1960 and 1972. The skeletal material is curated at the zoological collection of the Natural History Museum of Denmark in Copenhagen. Information on sex, age class (juvenile/adult), year of collection, total length and body weight is provided for each animal (Supplementary Table 1). A total of 16 Hesselø specimens were examined: eight females (♀H: one juvenile and seven adults) and eight males (♂H: two juveniles and six adults). The second subpopulation originated from the Wadden Sea, used in Bethune et al. (2021) to establish DMTA in pinnipeds. Those individuals were collected between June and October in the year 1988 along the German Wadden Sea coast during the first epizootic outbreak of the PDV. The German Wadden Sea harbour seals (♀WS, 41 females; ♂WS, 37 males) are curated at the osteological collection of the Zoological Institute of Kiel University, Germany. Information on sex, age at death, date and location of collection, as well as data on body length and weight, is available for each animal (Supplementary Table 1). For the specimens from the German Wadden Sea, age ranged from 5 to 16 years and was determined using cement layer analysis of canine teeth by Abt (2002). The upper permanent dentition of harbour seals consisted of the tooth classes according to the dental formula (I 3/2, C 1/1, P 4/4, M 1/1 = 34) (Jefferson et al., 1993) (Figure 2).
Figure 1. Map of the German Wadden Sea. The examined specimens were collected (a) during the summer/fall of 1988 along the coast of the German Wadden Sea (blue/green) and (b) at the Danish island Hesselø in the Danish southern Kattegat (red).
Figure 2. Harbour seal (Phoca vitulina) dentition and moulding process. (a) Skull in ventral and (b) lateral views showing the upper dentition. Tooth positions from mesial to distal: first postcanine (PC1), second postcanine (PC2), third postcanine (PC3) and fourth postcanine (PC4). Specimen 9343, curated at Leibniz Institute for the Analysis of Biodiversity Change, Hamburg, Germany. Moulding process on the buccal side of (c) PC2, PC3 and PC4 and (d) C and I3. The short wire is oriented towards cusp tip, and the long wire towards mesial. Specimen 30670, curated at the skeletal collection of the Zoological Institute, University of Kiel, Germany. Scale = 1 cm. (e) Buccal view of measurement area (coloured) on the third upper postcanine tooth of P. vitulina.
Since the DMT varies mostly in frontal tooth positions in harbour seals, all measurements for this study were made on the upper postcanine dentition using the second (PC2), third (PC3) and fourth postcanine teeth (PC4) (Figure 2). Parts of the data set from Bethune et al. (2021) were re-used for these three postcanine upper teeth and added equivalent new data for the Hesselø seals in the same tooth positions (Supplementary Table 1). Due to limited availability, a resulting small sample size and the missing age data of Hesselø seals, no wear differences between age groups or seasons were examined.
Since the premolar and molar teeth in pinnipeds are not clearly distinguishable, those teeth are often referred to as postcanine teeth (Hillson, 1986). Since the DMT in the frontal tooth positions of harbour seals has been found to differentiate between males and females (Bethune et al., 2021), all measurements were made on the postcanine dentition. Along the upper dentition, the following tooth positions were measured: second (PC2), third (PC3) and fourth postcanine teeth (PC4) (Figure 2).
2.2 Moulding
After cleaning the dentition with acetone, moulds of upper teeth were made using a high-resolution silicone (Provil Novo Light C.D.2 regular set; Type 3; Heraeus Kulzer, Dormagen, Germany) following the procedure outlined by Schulz et al. (2010). The silicone was applied on the main cusp of the postcanines on the straight surface between the maximum convexity at the cervical third and the tip (Figure 2) following the moulding procedure of Bethune et al. (2021) (for details, see Figure 2 in Bethune et al., 2021).
2.3 Data acquisition
Surface scans of enamel facets were conducted using the high-resolution disc scanning confocal microscope μsurf custom with a blue LED (470 nm) and a high-speed progressive-scan digital camera (984 × 984 pixels) (NanoFocus AG, Oberhausen, Germany) following the established protocol (Schulz et al., 2010), pre-processing and filtering following Schulz et al (2010), Schulz et al, 2013). Where possible, four non-overlapping measurement fields per facet with a square area of 160 μm2 were collected using a ×100 long distance objective (numerical aperture of 0.8, a resolution in x, y = 0.16 μm and z = 0.06 μm). Measurements with <95% surface points or a vertical displacement range of δz > 40 μm were rejected, as well as surface areas with defects or adherent dirt. The DMT was quantified by employing two methods: 1) scale-sensitive fractal analysis (SSFA; four parameters; Supplementary Table 2) using length-scale and area-scale fractal analyses (Ungar et al., 2003; Scott et al., 2006) and 2) three-dimensional surface texture analysis (3DST; 45 parameters; Supplementary Table 2) using standardised roughness (ISO 25178) and flatness (ISO 12781) parameters combined with non-standardised motif, furrows, direction and isotropy parameters (Schulz et al., 2010; Calandra et al., 2012). A full description of the 49 surface texture parameters used can be found in Supplementary Table 2. The analysis was conducted using μsoft analysis premium v.7.0.6672 software (NanoFocus AG, Oberhausen, Germany; a derivative of Mountains® Analysis software by Digital Surf, Besançon, France).
2.4 Statistics
Statistical analyses were carried out using the open-source software R version 2.15.1 (R Development Core Team, 2011) following the statistical procedure of Calandra et al. (2012). The R packages xlsx version 0.3.0 (Dragulescu, 2011), doBy version 4.5.9 (Højsgaard and Halekoh, 2013), grDevices version 2.15.1 (R Development Core Team, 2011) and R.utils version 1.9.11 (R Development Core Team, 2011) were used. All statistical tests were carried out using functions (Wilcox et al., 2005) that are included in the package WRS (Wilcox and Schönbrodt, 2010) (v. 0.12.1). All data were trimmed 15% in each tail to compensate for non-normality, and heteroscedastic tests were applied due to the heterogeneity of variances. The robust Welch–Yuen (Wilcox, 2003; Wilcox et al., 2005) omnibus test was performed to test for significant differences between groups and to control for type I error. Subsequently, the source of significant differences within the arithmetical means was determined using a heteroscedastic pairwise comparison test analogue to Dunnett’s T3 (Dunnett, 1980). In addition, to control for type II error, a heteroscedastic rank-based test based on Cliff’s method (Cliff, 1996) was applied for all pairs, in which the family-wise error was controlled via Hochberg’s method (Hochberg, 1988). The results were accepted if Cliff’s ordinal method and the combination of the Welch–Yuen test and Dunnett’s T3 test showed a significant output (p ≤ pcrit ≤ 0.05). Additionally, a factor analysis (FA) was performed using the open-source software R version 4.0.5 (R Development Core Team, 2021) following the statistical procedure of Stuhlträger et al. (2019) to compare the effect of sex and region. The R packages xlsx version 0.6.5 (Dragulescu and Arendt, 2020), doBy version 4.6.10 (Højsgaard and Halekoh, 2021), R.utils version 2.10.1 (Bengtsson, 2020), devtools version 2.4.1 (Wickham et al., 2021), ggplot2 version 3.3.3 (Wickham, 2016), factoextra version 1.0.7 (Kassambara and Mundt, 2020), rela version 4.1 (Chajewski, 2009) and ggfortify version 0.4.11 (Horikoshi and Tang, 2020) were used. Of the initial 49 3DST parameters, 21 (Asfc, FLTp, FLTq, FLTt, FLTv, mea, medf, meh, metf, nMotif, Sa, Smc, Smr, Sp, Sq, Sxp, Sz, Vmp, Vv, Vvc and Vvv) were selected for the final FA using a varimax rotation and the function “factanal”. The 3DST parameters were selected due to significant output detected using both Dunnett’s and Cliff’s tests, with no missing values and approximately normal distribution. The FA was justified as shown by the Kaiser–Meyer–Olkin measure of sampling adequacy (value > 0.5) using the function “paf” of the R package rela (Chajewski, 2009). A one-way ANOVA with a post-hoc Tukey’s honestly significant difference (HSD) test was conducted using FA scores of factors with eigenvalue ≥ 1.
3 Results
Significant differences in DMT of the studied harbour seal groups were found. Descriptive statistical values, including the mean and standard deviation (SD) for the surface texture parameters of both subpopulations, are given in Supplementary Table 3.
The upper dentition in females from Hesselø and the Wadden Sea (♀H vs. ♀WS) differed most distinctly in their microscopic wear pattern (23 out of 49 parameters). In comparison to that in the Wadden Sea females, the DMTs of Hesselø females were significantly more anisotropic (Asfc) with fewer motifs (nMotif), had higher texture profile (FLTp, FLTq, FLTt, FLTv, meh, metf, Sa, Smc, Smr, Sp, Sq, Sxp and Sz), were more voluminous (Sdv, Vm, Vmp, Vv, Vvc and Vvv) and showed a higher density of furrows (medf) (Table 1; Figure 3).
Table 1. Overview table of the statistically significant DMTA parameters.
Figure 3. Dental microwear texture in the upper dentition of Phoca vitulina. Boxplots of selected surface texture parameters measured along the upper dentition of P. vitulina specimens from Hesselø (♀ = coral and ♂ = light blue) and the German Wadden Sea (♀ = pink and ♂ = dark blue). Test statistics following the established protocol (Calandra et al., 2012), combining the Welch–Yuen test, the equivalent of Dunnett’s T3 test and Cliff’s method; significance levels: * p ≤ 0.05, ** p ≤ 0.01, and *** p ≤ 0.005. H, Hesselø; WS, Wadden Sea; ♀, females; ♂, males. For descriptions of parameters, see Supplementary Table 2.
Thirteen DMTA parameters revealed differences in the dental textures microwear of Hesselø females and Wadden Sea males (♀H vs. ♂WS). The DMTs of the Wadden Sea males were significantly flatter (FLTp, FLTq, FLTt, Sa, Smr, Sq and Sxp), more isotropic (Asfc) with more motifs (nMotif) and less voluminous (Vm, Vmp, Vv and Vvv) and had a lower density of furrows (medf) than those of the Hesselø females (Table 1; Figure 3).
The postcanine dentitions of Wadden Sea females and Hesselø males (♀WS vs. ♂H) differed in four DMTA parameters, with Hesselø males displaying a more anisotropic (Asfc) DMT with higher peaks (Sxp) and more voluminous valleys (Vvv) (Table 1; Figure 3).
No significant differences in DMTA parameters were detectable in the Wadden Sea sample (♀WS vs. ♂WS), in the Hesselø sample (♀H vs. ♂H) or between the males of both subpopulations (♂WS vs. ♂H) (Table 1; Figure 3).
The FA revealed three factors with eigenvalues ≥ 1, together explaining 83.3% of the total variance (Table 2). According to the factor loadings (Table 2), the parameters FLTq, FLTt, FLTv, Sa, Smc, Smr, Sq, Sxp, Vv, Vvc and Vvv contributed most to factor 1; Asfc contributed most to factor 3; all parameters had weak loadings (≤0.7) for factor 2. The more widespread Wadden Sea clusters in the FA were partially overlapping with the smaller Hesselø clusters (Figure 4). The separation between the Wadden Sea and Hesselø groups was mainly driven by factor 1. This indicated a dental microwear with higher profiles and more voluminous textures in the Hesselø group. ANOVA reported differences in the means of the groups (df = 3, F = 12.4, pANOVA ≤ 0.001) (Table 3). ANOVA reported differences in the means of the four groups (df = 3, F = 12.4, pANOVA ≤ 0.001) (Table 3). Tukey’s test with three factors revealed between-group differences for ♀H vs. ♀WS (pTukey ≤ 0.001) > ♀H vs. ♂WS (pTukey = 0.002) > ♀WS vs. ♂H (pTukey = 0.028) > ♀WS vs. ♂WS (pTukey = 0.044) (Figure 4b; Table 3), indicating that the Hesselø females have the roughest and most voluminous DMTs in the four groups.
Table 2. Factor loadings and principal component loadings for the group comparisons given for each DMTA parameter and factors with eigenvalues ≥ 1.
Figure 4. (a) Factor analysis and (b) Tukey’s test of upper teeth of Phoca vitulina comparing the Wadden Sea population to the Hesselø specimens. H, Hesselø; WS, Wadden Sea; ♀, females; ♂, males. Bold bars indicate significant differences. For descriptions of parameters, see Supplementary Table 2.
Table 3. Post-hoc Tukey’s test for the scores of factors 1, 2 and 3 of the factor analysis between groups.
4 Discussion
Spatial differences in dental microwear texture of harbour seals in two geographic areas revealed different foraging strategies in two harbour seal subpopulations in this study, which may be related to hunting pressure, which can influence movement behaviour and therefore habitat use and foraging ecology in wild carnivores (Stillfried et al., 2015). However, spatiotemporal differences between foraging habitats in the North and Baltic Sea ecosystems, as well as prey population dynamics and other anthropogenic impacts, may interact. We noted that the group differences in some of the DMT parameters of the seals have a similar range as compared to different diet types, ranging from sardines (low abrasive diets) to crawfish (exoskeletons, highest abrasive diets) in controlled feeding experiments in alligators, e.g. Asfc > 1 < 4 (Winkler et al., 2022). Within the limited comparability of different species and different instrument settings (Winkler and Kubo, 2025 in press, Kubo et al., 2025), we interpreted such a similarity with some caution but as first evidence indicating substantial and ecologically relevant dietary differences related to dietary abrasiveness between the harbour seal populations.
4.1 Foraging strategies of the Danish Kattegat population
Our results revealed that Hesselø females displayed the roughest DMT, indicating the highest intake of dietary abrasives. Additionally, Hesselø males displayed a slightly higher DMT than Wadden Sea females, probably reflecting a higher intake of abrasives. Those results are in line with our hypothesis that Kattegat Hesselø harbour seals may display a higher variance in prey selection with respect to the Wadden Sea individuals, as a result of a restricted habitat shaped by surrounding hunting pressure and therefore an increased reliance on more abrasive foraging grounds and prey items. This seems to be inapplicable for the entire Hesselø subpopulation, as no differences were detected between males from both areas, but a significantly higher intake of abrasives can be assumed for Hesselø females compared to Wadden Sea seals and for Hesselø males compared to Wadden Sea females. Since the DMTs of Hesselø males appeared similar to those of Wadden Sea males, it can be assumed that both habitats provided foraging opportunities with comparable dietary abrasives. It is possible that males in both subpopulations were able to feed on similar prey, occupying the same niche in both regions. The lack of significant differences within the Hesselø harbour seals hints at an overlap of foraging strategies in Hesselø. Considering the rougher texture and complex DMTs of Hesselø females as compared to Wadden Sea females, we proposed a strongly generalistic foraging strategy in both regions as a species dietary signal covering the wide range of DMT parameter values. For the Hesselø females, we linked the surface texture signature with a higher intake of abrasives in response to intra-specific competition for foraging grounds and prey. In fact, it remains for future studies to determine the source of abrasive particles and clarify in seal diets the exact impact of internal abrasive from dietary parts (fish scales and invertebrate exoskeletons) or external abrasives (sediments). When the harbour seal subpopulation at Hesselø increased during the 1960s/1970s, intra-specific competition for haul-out places and fish resources in this small protected area may have influenced foraging behaviour.
The increased predation surrounding Hesselø may have reduced prey abundance close to the island, an effect described by Birt et al. (1987) as Ashmole`s halo (Vance et al., 2021). Such a zone of depletion around Hesselø, combined with limited home ranges due to hunting pressure in neighbouring Danish waters, could have led to high intra-specific consumptive competition. However, also environmental conditions like sediment structure, salinity and other ecosystem characteristics like bathymetry may influence prey consumption in different time periods. Apart from hunting, anthropogenic impacts like fisheries and contaminant influx may have affected prey availability and foraging ecology. A mechanism for reducing intra-specific competition in harbour seals is the sexual segregation of foraging, as reported by several studies. According to a telemetric study of Baechler et al. (2002), male harbour seals at Nova Scotia, Canada, dove deeper and longer during the breeding season of 1989–1996 compared with females. Wilson et al. (2015) noted that female seals in the Wadden Sea between 2004 and 2006 stayed significantly longer underwater and foraged at shallower depths than males in the same region. Such sex-dependent differences in dive duration and swimming speed are considered a major contribution to minimising the effects of competing for prey. The differing observations of female dive depths in the mentioned studies suggest that the form of sexual segregation can differ between populations depending on local conditions and population dynamics. Thompson et al. (1998) reported that female harbour seals from Scotland during the breeding season displayed significantly shorter foraging trip durations and foraging ranges than males. This diving behaviour and movement patterns show that sexual segregation of foraging behaviour in harbour seals can take on locally different forms depending on environmental conditions and habitat constraints. However, at Hesselø, such a sexual segregation in habitat use by variable trip distance and duration was probably prevented by the small protected perimeter. Later movement studies conducted in the Skagerrak and Kattegat after the hunting ban (Härkönen and Harding, 2001; Dietz et al., 2012) revealed a striking segregation by age and sex in harbour seals, observing an increasing site fidelity in females, whereas dispersal rates in juveniles and adult males increased with age, supporting the findings in this study.
4.2 Foraging strategies of the German Wadden Sea population
The Wadden Sea specimens in our study show some sex-specific differences in their DMTs, which could imply a sexual segregation in foraging behaviour. In contrast to Hesselø and its limited perimeter of protection, the Wadden Sea provided large hunting-free foraging grounds, allowing for sexual segregation in habitat use or foraging behaviour, resulting in low or moderate intra-specific competition. The prey abundance in the wider Wadden Sea area may have led harbour seals to focus on preferred and less abrasive prey, e.g. juvenile fish, or less scaled species like sandeel and herring, leading to lower DMTs. This is supported by telemetry studies observing multi-day foraging trips in harbour seals away from coastal haul-out sites to the offshore North Sea with similar foraging rates during travelling and at offshore sites in the North Sea (Vance et al., 2021). Those findings suggest offshore trips to be an avoidance of intra-specific competition rather than a reliance on specific rich offshore foraging hotspots (Vance et al., 2021). Other studies have revealed that harbour seals around the Wadden Sea had a much larger home range than harbour seals from the Kattegat (Tougaard et al., 2008; Dietz et al., 2012). In conclusion, Wadden Sea seals in this study were able to overcome intra-specific competition by foraging in a wider area without anthropogenic stress, while Hesselø harbour seals had a more generalistic foraging strategy in a smaller habitat restricted by surrounding hunting pressure.
It remains unclear which specific internal or adherent abrasives caused the distinct DMTs in the studied harbour seals. Main abrasive agents in harbour seal diet may be scales of modern teleost fish and incidentally ingested sediment (Bethune et al., 2021). Furthermore, the effect of those abrasives should be amplified by repeated contact during the reduction of unwieldy, large prey. Therefore, a diet consisting of large prey species with ctenoid scales that burrow into the sediment, like flatfish, is considered highly abrasive, in contrast to a diet consisting of small pelagic fish with cycloid scales that cause less abrasion (Spinner et al., 2019).
4.3 Population comparison
The stomach content analyses conducted on the studied specimens (pers. com. M.T. Olsen) revealed that eight out of 16 stomachs contained otoliths of gadoids, affirming the ingestion of gadoids in half the specimens. The total absence of otoliths from other species in addition to gadoids may be explained by the bias of stomach content analyses: as digestion strongly influences the proportion and size of otoliths, fish species with larger otoliths may be over-represented in the stomachs, as the smallest otoliths degrade at a faster rate (Pierce and Boyle, 1991; Bowen and Iverson, 2013). The advent of metabarcoding analyses for deciphering the diet composition of aquatic predators has also shown that some soft-bodied prey taxa are underrepresented in hard part analyses (Boyi et al., 2022); therefore, in the existing studies, some relevant prey groups responsible for certain observed characteristic differences in texture may be missing. The dietary information pertaining to Hesselø harbour seals and the lack of comparable stomach content analyses from Wadden Sea seals limit conclusions drawn with respect to DMT patterns of specimens in this study. Diet composition analyses were conducted around Anholt, an island in the Southern Kattegat, located 55 km north of Hesselø (Härkönen, 1987a, Härkönen, 1988). According to otolith analyses from faecal samples, Anholt harbour seals fed on flat fish (75% by weight), codfish associated with the bottom (15.5%) and sandeels (9.3%) in the summer of 1980. In their sandy shore habitat surrounding the sandbanks, harbour seals preferred to feed on sea beds down to 30 m with scarce or lacking vegetation (Härkönen, 1988). The less diverse prey spectrum of seals in this area was attributed to a structurally simple habitat and the sharp halocline at 30 m, which restricted accessibility for some prey species in shallow waters (Härkönen, 1988). In the German Wadden Sea, harbour seals foraged on benthic flatfish (78.2% by weight), gadoids (7.8%), smelt (6.1%), bull-rout (4.2%) and gobies (2.1%), according to stomach content analyses between 1975 and 1984 (Behrends, 1985; Sievers, 1989). Therefore, harbour seal subpopulations from the Kattegat and from the Wadden Sea seem to have fed on similar prey. As for potentially ingested substrate, both regions are characterised by flat sandy sea beds with water depths up to 20 m (Härkönen, 1987b; Vance et al., 2021).
In the DMTA study of Winkler et al. (2019), low roughness (Asfc), density (medf) and depth of surface texture features in carnivorous Lepidosauria were linked to unidirectional puncturing of tissue without prey reduction behaviour. However, the higher complexity (Asfc) and higher density of surface texture features (medf) in herbivores, algaevores, frugivores, omnivores, insectivores and molluscivores seem to reflect a more pronounced oral food-processing behaviour and particle size reduction. When transferring those principles to the harbour seals in the current study, the Hesselø females displaying the highest DMT profile (high Asfc, medf and metf) should have performed the most pronounced prey handling in comparison to the Wadden Sea specimens. Thus, we assumed the high DMT profiles of Hesselø females—in relation to Wadden Sea specimens—to emanate from a) the increased ingestion of sediment while feeding on prey close to or burrowed into the sediment (flat fish and sand eels), b) an increased ingestion of coarser sediment and/or c) from foraging for more unwieldy prey, e.g. large gadoids or flat fish requiring prey reduction behaviour.
4.4 Anthropogenic impact of hunting
Since the implementation of hunting bans, the harbour seal subpopulations in Danish and German waters are recovering, despite the impact of several epidemics over the past 40 years. In 2019, the harbour seal subpopulation size at Hesselø was estimated to be 2,315 (Silva et al., 2021). According to a survey conducted in 2021, a total of 17,121 harbour seals were counted in the German Wadden Sea (Galatius et al., 2021). However, different management regimes operating 40 years ago still influence the current population structure, distribution and demography (Brasseur et al., 2018). The hunting of harbour seals has created an imbalance in the distribution of breeding females rooted in their high site fidelity, leading to regional variations in population recovery. Seemingly stable seal populations may experience a strong reliance on locally highly adapted foraging behaviour to compensate for prey competition within their colonies. Such populations are vulnerable to shifts in prey abundance by overexploitation and to fragmentation of foraging grounds by tourism or construction (Silva et al., 2021). Changes in environmental conditions, like water temperature, oxygenation and pH, may influence prey species abundance (Heße et al., 2024; Kappa et al., 2025), with more Lusitanian fish species migrating to the North and Baltic Sea regions (Boyi et al., 2022) due to climate change. A study on the effects of herring weight, birth rate of mature females and hunting pressure on grey seal abundance in Finnish waters confirmed that prey quality and decreased hunting pressure may have positively influenced birth rates (Kauhala et al., 2016), highlighting the effects of anthropogenic stress and prey availability on apex predators. Spatial differences in diet plasticity were also found in ringed seal and beluga whale arctic top predators by investigating stable carbon and nitrogen isotopes as a proxy for diet, supporting the findings of this study and reflecting the high degree of individual specialisation in the investigated ringed seals (Yurkowski et al., 2016). Anthropogenic influences, either disturbances or conservation measures, have a long-term effect on future harbour seal populations as a consequence of their longevity and their site fidelity during breeding. In the future, elucidating not only intra-specific but also interspecific competition between harbour, grey and ringed seals in the different Baltic Sea ecosystems, and with small odontocetes, would be crucial to determine the impacts of overfishing and prey depletion on threatened apex marine predators.
5 Conclusion
Significant differences in tooth microwear between harbour seals from two geographic regions exposed to different anthropogenic pressures were shown using DMTs. The newly established method was used successfully on historical seal skulls preserved in natural history museum collections. Variable patterns of abrasiveness reflected prey diversity and abundance as well as bottom and sediment structures in the Wadden Sea and Kattegat foraging grounds. Female harbour seals from Hesselø with higher DMTs probably displayed a more generalistic foraging strategy due to intra-specific competition. Harbour seals from the Wadden Sea, however, were able to avoid competition for food resources by dispersing in larger foraging grounds within protected German North Sea waters, as reflected by slightly shifted DMTs. This study showed DMTA to be a promising tool to elucidate intra-specific foraging strategies in harbour seals and opens new avenues for uncovering locally modified intra-specific dynamics in past seal subpopulations by analysing museum material. Future analyses using this non-invasive method in live aquatic mammals can elucidate foraging dynamics in current wildlife populations and help to assess conservation measures.
Data availability statement
The original contributions presented in the study are included in the article/Supplementary Material. Further inquiries can be directed to the corresponding author.
Ethics statement
Ethical approval was not required for the study involving animals in accordance with the local legislation and institutional requirements because Skeletal material from museum specimens was used in this study.
Author contributions
KL: Funding acquisition, Resources, Supervision, Validation, Writing – original draft, Writing – review & editing. EB: Data curation, Formal analysis, Investigation, Methodology, Visualization, Writing – original draft, Writing – review & editing. ES-K: Conceptualization, Data curation, Methodology, Supervision, Validation, Writing – review & editing. US: Funding acquisition, Project administration, Resources, Supervision, Writing – review & editing. TK: Conceptualization, Funding acquisition, Methodology, Resources, Supervision, Validation, Writing – review & editing.
Funding
The author(s) declared financial support was received for this work and/or its publication. Volkswagen Foundation (AZ 89911) funded this study within the framework of the program “Research in Museums”.
Acknowledgments
The authors thank the Volkswagen Foundation (AZ 89911) for funding this study within the framework of the program “Research in Museums”. We thank the former Center of Natural History (CeNak), Hamburg, Germany, for their financial support. We would like to express our gratitude to Günther B. Hartl and Renate Lücht (Zoological Institute of Kiel University, Germany), Daniel Klingberg Johansson (Natural History Museum of Denmark) and to Morten Tange Olsen (University of Copenhagen, Denmark) for access to the osteological collection and for providing stomach content information of Hesselø seals. Special thanks to Holger Krohn, University of Hamburg, for assisting with measuring the DMTsDMT. We acknowledge financial support by the Open Access Publication Fund of the University of Veterinary Medicine Hannover, Foundation.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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Supplementary material
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fmars.2025.1589549/full#supplementary-material
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Keywords: dental microwear texture analysis (DMTA), marine mammals, foraging ecology, historic diet composition, North Sea, Kattegat, conservation, anthropogenic stress
Citation: Lehnert K, Bethune E, Schulz-Kornas E, Siebert U and Kaiser TM (2025) Intra-specific foraging dynamics reveal anthropogenic impact on harbour seals (Phoca vitulina) in the Danish Kattegat and the German Wadden Sea. Front. Mar. Sci. 12:1589549. doi: 10.3389/fmars.2025.1589549
Received: 07 March 2025; Accepted: 24 November 2025; Revised: 17 November 2025;
Published: 16 December 2025.
Edited by:
Sarah Kienle, University of Rhode Island, United StatesReviewed by:
Karl Lundström, Swedish University of Agricultural Sciences, SwedenMagda Chudzinska, University of St Andrews, United Kingdom
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*Correspondence: Kristina Lehnert, S3Jpc3RpbmEubGVobmVydEB0aWhvLWhhbm5vdmVyLmRl