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Isotopic niches reveal the
trophic structure of the cetacean
community in the oceanic
waters around the Azores
Myriam Lebon
1
*, Ana Colac¸o
1
, Rui Prieto
1
, Irma Cascão
1
,
Cla
´udia Oliveira
1
, Marta Tobeña
1
, Yann Planque
2,3
,
Je
´ro
ˆme Spitz
2,3
and Mo
´nica A. Silva
1
1
Institute of Marine Sciences - OKEANOS & Institute of Marine Research - IMAR, University of the
Azores, Horta, Portugal,
2
Observatoire Pelagis, Unité d'Appui et de Recherche (UAR) 3462 - La
Rochelle Universite
´- Centre National de la Recherche Scientifique (CNRS), La Rochelle, France,
3
Centre d’Etudes Biologiques de Chize
´, UMR 7372 La Rochelle Universite
´- CNRS, La Rochelle, France
Introduction: The oceanic waters around the Azores host a high diversity of
cetaceans, with 28 species of toothed and baleen whales present year-round or
seasonally. This high cetacean biodiversity likely plays an important role in the
structure, functioning and productivity of the ecosystem, and may increase
trophic redundancy, thus contributing to food web resilience to disturbances.
Methods: Here we used stable isotope (d
13
C and d
15
N) analysis to characterize
trophic niches, assess niche overlap, describe the trophic structure and discuss
potential redundancy in the cetacean community. Using 407 samples from 12
species, we estimated Standard Ellipse Areas and overlaps between species and
used a hierarchical clustering analysis to identify trophic guilds.
Results and discussion: d
13
C and d
15
N values ranged from -20.53 to -15.46‰
and from 7.78 to 14.41‰respectively, suggesting the use of diverse habitats and
resources among cetacean species. Clustering analysis revealed that species
were grouped into four trophic guilds, segregated mainly by trophic position (TP):
a low-TP guild with three zooplanktivore baleen whales, a mid-TP guild with
micronektivores, a high-TP guild with micronekton and nekton consumers, and a
cluster with only Pseudorca crassidens. There was significant isotopic niche
overlap between one pair of species within each guild, indicating some potential
for trophic redundancy in the community. Yet, these pairs also showed some
form of spatial or temporal partitioning, suggesting that mechanisms promoting
species coexistence could play a key role in structuring the cetacean community
in the region and in its ecological role.
KEYWORDS
stable isotopes, marine mammals, trophic niches, trophic guild, foraging, Azores,
oceanic islands
Frontiers in Marine Science frontiersin.org01
OPEN ACCESS
EDITED BY
Guillermo Luna-Jorquera,
Universidad Cato
´lica del Norte, Chile
REVIEWED BY
Joan Gime
´nez,
Spanish National Research Council (CSIC),
Spain
Maelle Connan,
Nelson Mandela University, South Africa
*CORRESPONDENCE
Myriam Lebon
myriam.io.lebon@uac.pt
RECEIVED 25 August 2023
ACCEPTED 17 April 2024
PUBLISHED 03 May 2024
CITATION
Lebon M, Colac¸oA,Prieto R, Cascão I,
Oliveira C, Tobeña M, Planque Y, Spitz J and
Silva MA (2024) Isotopic niches reveal the
trophic structure of the cetacean community
in the oceanic waters around the Azores.
Front. Mar. Sci. 11:1283357.
doi: 10.3389/fmars.2024.1283357
COPYRIGHT
© 2024 Lebon, Colac¸o, Prieto, Cascão,
Oliveira, Tobeña, Planque, Spitz and Silva. This
is an open-access article distributed under the
terms of the Creative Commons Attribution
License (CC BY). The use, distribution or
reproduction in other forums is permitted,
provided the original author(s) and the
copyright owner(s) are credited and that the
original publication in this journal is cited, in
accordance with accepted academic
practice. No use, distribution or reproduction
is permitted which does not comply with
these terms.
TYPE Original Research
PUBLISHED 03 May 2024
DOI 10.3389/fmars.2024.1283357
1 Introduction
Apex and large-bodied marine predators such as cetaceans play
important roles in ecosystem structure, function and productivity.
Despite their relatively low abundance compared to other taxa, they
can have disproportionate influence on food web structure, exerting
top-down controls on prey populations through direct
consumption and non-consumptive interactions (Baum and
Worm, 2009;Estes et al., 2016). Cetaceans can also influence
nutrient dynamics, by releasing nutrient-rich waste in surface
waters, transporting nutrients within and across ecosystems
through their extensive movements, and transferring nutrients
from deep waters to the surface and vice-versa (Roman and
McCarthy, 2010;Roman et al., 2014;Doughty et al., 2016;
Ratnarajah et al., 2018;Gilbert et al., 2023). However, cetaceans
are a very diverse group, and species’traits (e.g., morphological,
physiological, behavioral characteristics) determine their trophic
niche and interactions in the food web, which, in turn, govern their
contribution to energy and nutrient flows in the ecosystem (Laigle
et al., 2018). Knowledge of the trophic structure of cetacean
assemblages is therefore fundamental to understand the ability of
this community to fill diverse niches and contribute to the diversity
of trophic interactions, and to determine how species are
distributed among distinct trophic groups. Such knowledge can
provide insights into the breadth of functions of the cetacean
community as a whole in key ecosystem processes, as well as to
the extent to which different species share similar ecological roles.
The Azores (Portugal) is the most remote archipelago in the
North Atlantic, distancing about 1000 nm from continental Europe
and 3000 nm from North America. Despite being oligotrophic, the
region is characterized by dynamic ocean processes which interact
with high seafloor complexity creating nutrient pulses that
stimulate productivity and attract many marine megafauna
species (Afonso et al., 2020). The waters around the Azores host a
high diversity of cetaceans, with 28 species documented, including
species that are present year-round (e.g., Delphinus delphis,Tursiops
truncatus,Grampus griseus,Stenella coeruleoalba,Physeter
macrocephalus,Ziphius cavirostris,Mesoplodon bidens,M.
densirostris), seasonal visitors (e.g., Balaenoptera musculus,B.
physalus,B. borealis,Stenella frontalis,Hyperoodon ampullatus),
and regular visitors with no clear seasonality (e.g., Globicephala
macrorhynchus,Pseudorca crassidens,Megaptera novaeangliae,B.
acutorostrata,Orcinus orca), in addition to other less frequently
sighted species (Silva et al., 2014). The community comprises
species that typically occupy different feeding guilds: small
dolphins that feed on a variety of epipelagic micronekton, toothed
whales that consume meso- to bathypelagic prey, and baleen whales
that prey on zooplankton and small fish (Silva et al., 2014), likely
plays an important role in the local food web (Morato et al., 2016)
and may contribute significantly to the supply of nutrients in this
nutrient-depleted region (Gilbert et al., 2023). Furthermore, the
existence of several species with potentially similar trophic ecologies
could contribute to higher trophic redundancy within predator
guilds, thereby increasing food web resilience to environmental or
anthropogenic disturbances (Sanders et al., 2018). However, our
understanding of the ecological role of the cetacean community in
this oceanic region is limited by the lack of empirical knowledge of
their feeding habits in the area. Such information is typically
obtained from the analysis of stomach contents of stranded or
bycaught cetaceans, both of which are rare in the region
(Silva et al., 2014).
Stable isotope analysis (SIA) has been widely used to
reconstruct the diet and trophic ecology of populations and
interactions within communities (Boecklen et al., 2011). In the
marine system, bulk carbon (d
13
C) and nitrogen (d
15
N) stable
isotope values are the most commonly used isotopes, because
d
13
C values fluctuate mainly with primary carbon sources, giving
information on the origin of food resources (e.g., d
13
C values tend to
decrease from coastal and benthic sources to offshore and pelagic
sources), while d
15
N increases by 2-4‰at each trophic level, mostly
reflecting the trophic position of consumers within a particular
ecosystem (DeNiro and Epstein, 1978;Carlier et al., 2015). d
13
C and
d
15
N are also increasingly used to characterize isotopic niches
(Newsome et al., 2017) as a proxy of ecological niches
(Hutchinson, 1957,1978), and different metrics have been
proposed to quantify niche width, diversity, overlap and describe
trophic structure at the species or community level (Layman et al.,
2007). One advantage of SIA is that it can be performed using small
samples of skin tissue collected from live animals, thereby
circumventing the lack of stomach samples. Another advantage is
that the isotope composition provides dietary information
integrated over days to a few months, depending on the tissue
turnover rate (Crawford et al., 2008), whereas stomach content
analysis (SCA) gives information on recently ingested prey. Indeed,
although skin turnover rate is unknown for most species, full
incorporation of stable isotopes from prey into skin tissue in
cetaceans has been estimated to take 2.5 to 6 months (reviewed in
Wild et al., 2018). Because stable isotope data from cetacean skin
reflects diet over several months, it provides a time-integrated
description of trophic niches and of the community structure,
that contrasts with the snapshot view provided by SCA.
In this study, we determined the d
13
C and d
15
N composition
of the skin of 12 species of cetaceans (four baleen whales, six
delphinids, one beaked whale and the sperm whale) sampled off
the Azores to: 1) characterize their isotopic niche (used as a proxy
of trophic niche), identify trophic guilds within the community
and assess inter- and intra- guild variability in niche
characteristics, and 2) measure isotopic niche overlap among
species to better understand resource partitioning and trophic
redundancy within the cetacean community. We predict that the
community is divided into distinct trophic guilds, driven mainly
by variation in d
15
N values associated with differences in feeding
habits between species. Within each guild, we expect higher niche
overlap among species known to be spatially or temporally
segregated, and lower niche overlap among species that coexist
in the same area and time. Compared to species present year-
round, seasonal visitors and migratory species should have wider
niche spaces, reflecting a higher diversity of basal sources. Finally,
we discuss the potential importance of trophic redundancy within
the cetacean community in light of the current knowledge of the
spatiotemporal distribution and abundance of each species in
the area.
Lebon et al. 10.3389/fmars.2024.1283357
Frontiers in Marine Science frontiersin.org02
2 Materials and methods
2.1 Sample collection and processing
We analyzed 407 skin samples from 12 species collected
between 2002 and 2019 off the archipelago of the Azores,
Portugal (Figure 1). Of these, 392 samples were obtained from
free-ranging live animals using biopsy darts fired from a crossbow,
and 15 samples were from fresh carcasses of stranded animals
(decomposition codes 1 and 2 according to Van Canneyt et al.
(2015);Supplementary Table S1). Samples collected from live
animals were stored in Eppendorf tubes in a cooler until being
transferred to a -80°C freezer, while samples from strandings were
immediately stored at -80°C. All samples had information on date,
time, geographic position, as well as approximate (biopsy samples)
or exact (samples from strandings) body length of the sampled
individual. Most samples from B. musculus (n=17), B. physalus
(n=42) and B. borealis (n=39) have already been analyzed by
Silva et al. (2019).
2.2 Stable isotope analysis
The presence of lipids in samples usually results in more
negative d
13
C values because lipids are depleted in
13
C compared
to the proteins contained in the skin. To avoid this bias, lipids
can be extracted from samples. Although results were
inconsistent, Ryan et al. (2012) found that d
15
N can also, to a
lesser extent, be affected by lipid-extraction, and the authors
suggest measuring d
13
C in lipid-extracted tissue and d
15
Nin
non-extracted tissue. Other studies that examined the effect of
lipid-extraction on d
15
N revealed decreases, increases or no
changes in d
15
N(Post et al., 2007;Wilson et al., 2014;
Gimenez et al., 2017). Because biopsy skin samples were also
used for genetic analyses, the amount of tissue was not sufficient
to analyze each isotope on different sub-samples. Therefore, both
d
13
C and d
15
N were measured in lipid-extracted samples. This
method was selected to ensure consistency with prior studies
which have used the same samples and maintaining coherence
within the existing literature.
FIGURE 1
Locations of biopsy and stranding skin samples collected (n=407) from 12 cetacean species (each different point colors) between 2002 and 2019 in
the archipelago of the Azores (Portugal). Symbols indicate the taxonomic group: squares = Mysticeti, circles = Delphinidae, triangles = Ziphiidae,
diamonds = Physeteridae. Bathymetry lines are every 200 m. See Table 1 for abbreviated name of species.
Lebon et al. 10.3389/fmars.2024.1283357
Frontiers in Marine Science frontiersin.org03
Lipids were extracted from the skin using a 2:1 chloroform:
methanol solution and washed using 15 Wwater, and lipid-
extracted samples were stored in Eppendorf tubes without water
at -80°C. Samples were then freeze-dried for 48 hours and manually
ground until a homogeneous fine powder was obtained. Powder
samples of approximately 1 mg were analyzed through and isotope
ratio mass spectrometer (University of New Hampshire Stable
Isotope Laboratory, Marinova, IsoAnalytics, Centres Cientı
fics i
Tecnològics of the University of Barcelona (CCiT-UB), precision
always <0.3 ‰for d
13
C and <0.4 ‰for d
15
N). Carbon and nitrogen
stable isotope values are expressed as din ‰relative to the Vienna
Pee Dee Belemnite (PDB) standard and atmospheric nitrogen
(AIR), respectively. For samples with a mass C:N higher than 3.5
after lipid extraction (n=22), d
13
C values were mathematically
corrected using the equation from Post et al. (2007).
2.3 Data analysis
Prior to analysis, skin d
13
C values were corrected to account for
the Suess effect -0.026‰per year (Körtzinger et al., 2003).
Studies on the effects of decomposition on skin isotopic ratios of
cetaceans have provided contrasting results. While Payo-Payo et al.
(2013) did not detect any significant changes in either d
15
Nord
13
Cin
the skin of S. coeruleoalba after 62 days at ambient temperature,
Burrows et al. (2014) showed that Orcinus orca skin was significantly
enriched in
15
Nand
13
C after 3 days at 20°C, and continued to increase
up to 14 days, reaching values 6.4‰higher in d
15
Nand1‰higher in
d
13
C. Although samples from animals showing signs of decomposition
were not included in the analysis, we performed an outlier analysis to
identify any potential bias due to decomposition. We used the
Mahalanobis distance (MD) to calculate the distance between each
d
13
C-d
15
N pair in the bivariate plot space and the centroid of the cloud
encompassing all samples (Ghorbani, 2019). Individual distances were
then compared to a chi-squared distribution with two dependent
variables: d
13
Candd
15
N. If the MD was greater than the threshold
defined at the 99% confidence interval of the chi-square distribution,
the individual was considered an outlier. The analysis was conducted in
the rstatix package (Kassambara, 2023). No sample was considered an
outlier, therefore, isotopic measurements from biopsy and stranding
samples were pooled for further analysis. For two species (M. bidens
and S. coeruleoalba), only samples from stranded animals were
available, which made the comparison with biopsy samples
impossible. All samples from these two species were collected from
fresh specimens with no evident signs of decomposition, and we chose
to keep these data for a more comprehensive analysis of the trophic
ecology of the cetacean community off the Azores. Nevertheless, results
for these species should be interpreted with caution.
Differences in d
13
C and d
15
N between species were assessed
using Generalized Linear Mixed Models (GLMMs), as data were not
normally distributed (Shapiro-Wilk test results Supplementary
Table S2). Separate models were fit for each isotope, using species
as a fixed effect, and year and season as random effects, to account
for potential temporal variability in isotope compositions. The
significance of differences in d
13
C and d
15
N between species was
determined by pairwise comparisons of the estimated marginal
means, adjusted for multiple comparisons by Bonferroni
corrections. GLMMs were fit using the lme4 package (Bates et al.,
2015) and pairwise comparisons with the emmeans package
(Lenth, 2022).
We used Layman metrics (Layman et al., 2007) to characterize
species’isotopic niche spaces, determine the distribution of sampled
individuals within those niches, and compare niche characteristics
between species. For each species, six metrics were computed: d
15
N
range, d
13
C range, total area (TA), mean distance to centroid (CD),
mean nearest neighbor distance (NND) and standard deviation of
nearest neighbor distance (SDNND). The range of d
15
N and d
13
C
(in ‰) provides information on the trophic length and diversity of
basal resources for each species, respectively. TA is a measure of
niche width (in ‰²), while CD (in ‰) is a proxy for niche diversity.
Individual similarity and evenness in distribution within the species
d
15
N-d
13
C niche space are estimated by the NND and the SDNND
(both in ‰), respectively (low NND indicates high density or
clustering of individuals within the niche space, and low SDNND
indicates more even distribution of individuals within the niche
space). All metrics were calculated using the SIBER package
(Jackson et al., 2011) in R. Estimates of d
13
C and d
15
N ranges and
TA are especially affected by extreme values and therefore highly
sensitive to sample size (Jackson et al., 2011). To reduce the bias
caused by small sample sizes and uneven number of samples
between species, we bootstrapped all the metrics with replacement
(n=10 000) using the boot package (Canty and Ripley, 2022).
To estimate species’isotopic niche size and overlaps between
species we calculated Bayesian ellipses (SEA
B
)usingthe
‘bayesianOverlap’function in SIBER package (Jackson et al.,
2011). SEA
B
were calculated as the mean of the 4000 replicates of
basic Standard Ellipse Areas (SEA), which contain approximately
40% of the data for each species (modes ± SE in Supplementary
Table S3)(Jackson et al., 2011). Then, for every pair of 4000 SEA
B
generated by the model, we calculated the mean (and 95% credible
intervals) proportion of the ellipse of species A overlapping in the
ellipse of species B (i.e., the area of overlap/area of species B) and
vice versa.
Finally, we used a hierarchical clustering to define trophic guilds
within the community. A dissimilarity matrix was done using the
Euclidean distance between mean d
13
C and d
15
N values of each
species, and clusters were determined using the Ward’s method.
The optimal number of clusters was assessed using the Jaccard
similarity coefficient (hereafter Jaccard index, JI) which ranges from
0 to 1, with values ≤0.6 indicating an unstable cluster, values
between 0.6-0.75 indicating a pattern in the data, and those ≥0.75
a stable cluster (Hennig, 2023). Analyses were performed using the
packages stats (R Core Team, 2022) and fpc (Hennig, 2023)inR.
All analyses were done in R version 4.2.2 (R Core Team, 2022).
3 Results
A total of 407 skin samples from 12 cetacean species were
included in the trophic niche analyses. These species showed a wide
range of d
15
N (from 7.78‰to 14.41‰) and d
13
C values (from
-20.53‰to -15.46‰)(Table 1;Figure 2).
Lebon et al. 10.3389/fmars.2024.1283357
Frontiers in Marine Science frontiersin.org04
3.1 Intra- and interspecific variation in
stable isotope values and isotopic niches
GLMM results showed that season and year of sampling had no
significant effect on the isotopic composition of species (Supplementary
Tables S4 and S5). Pairwise tests (Supplementary Table S6)showed
significant differences in stable isotope values between several species,
except for M. bidens and M. novaeangliae,forwhichnearlyalltests
were non-significant, likely due to the small sample size. The Mysticeti
B. borealis,B. musculus and B. physalus had the lowest d
15
Nofall
sampled cetaceans (Table 1) and pairwise tests indicated that
differences to other species were statistically significant
(Supplementary Table S6). The three Balaenoptera species all differed
significantly in d
13
C: B. borealis were more enriched in
13
C, followed by
B. musculus and by B. physalus, which had the lowest d
13
Cvaluesofall
cetaceans, whereas their d
15
N values were similar.
P.crassidens had significantly higher values of d
13
C than P.
macrocephalus and T. truncatus, and these three species along with
G. macrorhynchus had significantly higher d
15
N relative to other
species but did not differ from each other. D. delphis showed
significant differences in d
15
N with all other species of
odontocetes except S. frontalis and M. bidens.
FIGURE 2
Mean Bayesian Standard Ellipse Area (SEA
B
) for the cetacean
community of the Azores. See Table 1 for abbreviated name of
species. Symbols indicate the taxonomic group: squares = Mysticeti,
circles = Delphinidae, triangles = Ziphiidae, diamonds = Physeteridae.
TABLE 1 Mean (± SD) and range of d
13
C and d
15
N (expressed in ‰) for 12 cetacean species used in the analysis.
Species Taxonomic
group Abr N Year
d
13
Cd
15
N
Presence in the Azores
Mean
±SD
Min-
Max
Mean
±SD
Min-
Max
Balaenoptera
borealis
Mysticeti Bbo 39 2005
–2019
-17.53
± 0.96
-19.56
–-15.80
9.06 ± 0.53 7.78
–10.27 Spring –early summer
Balaenoptera
musculus
Mysticeti Bmu 24 2008
–2019
-18.83
± 0.89
-19.76
–-16.33
9.16 ± 0.70 8.03
–11.03 Spring –early summer
Balaenoptera
physalus
Mysticeti Bph 127 2002
–2017
-19.37
± 0.50
-20.53
–-17.29
9.37 ± 0.61 8.3
–11.92
January –October (peak in May
–June)
Megaptera
novaeangliae
Mysticeti Mno 4 2010–
2017
-19.31
± 0.41
-19.55
–-18.70
10.42
± 0.76
9.39
–11.12 No seasonal pattern
Delphinus delphis Delphinidae Dde 69 2005
–2009
-18.33
± 0.44
-19.24
–-16.96
10.66
± 0.66
8.99
–12.87
Year-round but decrease in
summer and autumn
Stenella
coeruleoalba
Delphinidae Sco 7 2002
–2018
-18.15
± 0.39
-18.51
–-17.41
11.85
± 0.77
10.96
–13.01 Transient
Stenella frontalis Delphinidae Sfr 61 2005
–2013
-18.3
± 0.45
-18.96
–-16.86
11.00
± 0.59
9.97
–13.18 Early May –October
Mesoplodon bidens Ziphiidae Mbi 4 2009 -17.66
± 0.18
-17.86
–-17.46
11.68
± 0.06
11.63
–11.77 Summer
Globicephala
macrorhynchus
Delphinidae Gma 10 2004
–2014
-16.82
± 0.52
-17.49
–-15.89
12.33
± 0.52
11.7
–13.11 No seasonal pattern –Transient
Pseudorca
crassidens
Delphinidae Pcr 5 2009 -15.9
± 0.3209
-16.16
–-15.46
13.30
± 0.41
12.73
–13.71 Transient
Physeter
macrocephalus
Physeteridae Pma 42 2008
–2019
-17.26
± 0.3905
-17.78
–-16.16
12.84
± 0.47
11.54
–14.22 Year-round
Tursiops truncatus Delphinidae Ttr 15 2005
–2014
-17.51
± 0.4678
-18.26
–-16.86
12.53
± 0.70
11.51
–14.41 Year-round
Number of samples (N), sampling years (Year), taxonomic group and abbreviated name (Abr) are indicated for each species. Presence of each species in the Azores is based on Silva et al. (2014).
Lebon et al. 10.3389/fmars.2024.1283357
Frontiers in Marine Science frontiersin.org05
Baleen whales B. borealis,B. musculus and B. physalus displayed
the widest ranges in d
13
C(Figure 3A), the largest niche widths (TA)
(Figure 3C) and the greatest core niches (SEA
B
estimates) of all
studied cetaceans (Figure 4). Along with D. delphis,B. physalus also
showed one of the highest d
15
N ranges (Figure 3B). Conversely, M.
bidens, P. crassidens,M. novaeangliae and S. coeruleoalba, the
species with fewer samples (≤7), generally displayed low ranges in
both isotopes and small niche widths (Figures 3A,B). G.
macrorhynchus also showed one of the lowest d
15
N ranges and
niche widths. Amongst all species, Odontocetes S. frontalis,T.
truncatus and P. macrocephalus showed intermediate values in
niche width and d
13
C and d
15
N ranges, with S. frontalis showing
slightly higher values in all metrics relative to the other two species
(T. truncatus and P. macrocephalus). With the exception of B.
borealis,B. musculus and M. bidens, credible intervals of SEA
B
of the
remaining species largely overlapped (Figure 4). Compared to the
previously discussed Layman metrics, niche diversity (CD) varied
less across all species, with the highest diversity recorded in two
baleen whales (B. borealis and B. musculus), and the lowest in the
Ziphiidae species M. bidens (Figure 3D). M. novaeangliae
(Mysticeti), S. coeruleoalba and P. crassidens (Delphinidae)
showed the lowest degree of clustering (higher NND) and
strongest uneven distribution of individuals (higher SDNND)
A
B
DEF
C
FIGURE 3
Distribution of Layman metrics (A) d
13
C range, (B) d
15
N range, (C) TA (Total Area), (D) CD (Centroid Distance), (E) NND (Nearest Neighbor Distance),
(F) SDNND (Standard Deviation of Nearest Neighbor Distance) of the Azores cetacean community by species estimated by bootstrapping with n=10
000 replicates. Distributions are showed by boxplots. The lower and upper hinges correspond to the first and third quartiles (the 25th and 75th
percentiles), the bar inside represents the median, and the whiskers extend to 1.5 * IQR (Inter-Quartile Range). Dots represent outliers (i.e., data
beyond the whiskers). See Table 1 for abbreviated name of species.
FIGURE 4
Density plots of Bayesian Standard Ellipse Areas (SEA
B
)(in‰²)
showing the credible intervals at 50% (dark boxes), 75% (intermediate
boxes) and 95% (light boxes), and mode values of SEA
B
(white dot).
Species are ordered by mode values. Sample sizes for species are
indicated below each box. See Table 1 for abbreviated species names.
Lebon et al. 10.3389/fmars.2024.1283357
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within niche space, although variability in both metrics was very
high (Figures 3E,F). Density of individual packing and evenness in
individual distribution was greater in B. physalus,D. delphis,S.
frontalis and P. macrocephalus.
3.2 Trophic guilds in the
cetacean community
The hierarchical clustering analysis classified the 12 cetacean
species into four clusters: Cluster 1 contained three baleen whale
species (B. borealis,B. musculus,B. physalus), Cluster 2 included
two small dolphins (D. delphis, S. frontalis) and the last baleen
whale species M. novaeangliae, Cluster 3 comprised three
delphinids (G. macrorhynchus, T. truncatus, S. coeruleoalba), one
Physeteridae P. macrocephalus, and the Ziphiidae M. bidens, while
P. crassidens formed a separate cluster. The Jaccard index (JI)
suggests that assignment of species to some of these clusters
should be taken with caution, with cluster 1 and 3 being stable
(JI=0.75 and JI=0.76, respectively), clusters 2 indicating a pattern
(JI=0.70) and cluster 4 being unstable (JI=0.55) (Supplementary
Figure S1).
3.3 Interspecific overlap in isotopic niches
The highest overlaps were observed for two baleen whales: B.
physalus SEA
B
in the SEA
B
of B. musculus (62.7%, 95% CI: 17.3,
100), followed by two delphinids S. frontalis and D. delphis (55.8%,
95% CI: 22.2, 90.1 and 47.4%, 95% CI: 18.8, 76.7), and P.
macrocephalus in T. truncatus (45%, 95% CI: 0, 91.3) (Table 2).
Interestingly, while overlaps between the two latter pairs were
approximately symmetrical, the overlap between B. physalus and
B. musculus was clearly asymmetrical (Table 2). The remaining
pairwise overlaps were notably lower. In Cluster 1, niche overlaps
ranged from 0% (B. physalus - B. borealis) to 18.4% (95% CI: 0, 49.8;
B. borealis in B. musculus), with B. musculus showing the highest
overlaps of all whales (Table 2). Mysticeti from Cluster 1 also
overlapped with M. novaeangliae, the largest overlap being B.
physalus in M. novaeangliae (13%, 95% CI: 0, 69.7). In Cluster 2,
overlaps between the baleen whale M. novaeangliae and the
delphinids were low. In Cluster 3, S. coeruleoalba overlapped in
T. truncatus (17.1%), and M. bidens showed relatively high overlaps
in T. truncatus (13.6%) and S. coeruleoalba (19.1%), but credible
intervals indicate high uncertainty in these estimates (95% CI: 0,
100 in both cases) (Table 2). Lastly, P. crassidens showed a greater
overlap in G. macrorhynchus niche than in other species (7%, 95%
CI: 0, 64.4).
4 Discussion
We present here the first assessment of the trophic structure of
the Azorean community of cetaceans, as revealed by the analysis of
stable isotopes of 12 species representing the most important
taxonomic groups present, and diverse ecological and functional
traits. Results show that these species occupy a broad range of
isotopic niches, indicating that these species feed at various trophic
levels and in habitats with diverse basal resources. Our work
suggests that cetacean species can be grouped into four distinct
trophic guilds, revealing resource partitioning between some species
and potential trophic redundancy between others, allowing a better
understanding of intra and inter-guild trophic interactions, and
offering new insights into the ecological role of the community.
4.1 Community trophic structure and inter-
guild niche partitioning
Niche partitioning is a key mechanism to reduce competition
among coexisting species and plays a major role in driving the
composition, diversity and structure of communities
(HilleRisLambers et al., 2012). Niche partitioning may take
several forms, including resource partitioning, where species feed
on different food or prey items, spatial partitioning, where species
exploit different areas or habitats, and temporal partitioning, where
species differ in foraging times at daily or seasonal scales (Schoener,
1974). As predicted, resource partitioning plays an important role
in the trophic structure of the cetacean community in the Azores
and in driving the organization of species into multiple guilds.
Trophic differentiation between guilds was largely determined by
differences in trophic position (TP), indicating strong dietary
divergence between guilds through feeding on prey at different
trophic levels. This does not mean that all species use the same
foraging habitats and spatial partitioning does not occur locally.
However, in oceanic systems, especially those located at lower
latitudes such as the Azores, variability in baseline d
13
C values at
small spatial scales is generally low (Magozzi et al., 2017), making it
difficult to detect consumption of different local basal food
resources. This also means that substantial deviation in d
13
C
values from the ~1‰d
13
Cenrichmentateachtrophiclevel
observed for some species (e.g., B. borealis, M. novaeangliae,P.
crassidens) indicates feeding on carbon isoscapes very distinct from
that of the Azores region (see next section). Variation in isotopic
baselines between feeding areas can also influence the d
15
N
composition of species’skin and contribute to differences in
estimated TP, and we discuss potential biases in more detail when
describing species’niches. Nevertheless, the relative position of
species within the community described here is consistent with that
reported for other areas.
The hierarchical cluster analysis indicated that the cetacean
community consists of four trophic clusters. These are a low-TP
cluster with all Balaenoptera species (B. borealis,B. musculus and B.
physalus), a mid-TP cluster with one baleen whale (M.
novaeangliae) and two small dolphins (D. delphis and S.
frontalis), a high-TP cluster including one small (S. coeruleoalba)
and two larger delphinids (T. truncatus,G. macrorhynchus), a
beaked whale (M. bidens)andthespermwhale(P.
macrocephalus), and a fourth cluster occupying the highest TP
formed only by P. crassidens. Of these, only the high-TP and the
low-TP clusters can be considered a meaningful and stable cluster,
based on the Jaccard coefficient. The mid-TP cluster should be
Lebon et al. 10.3389/fmars.2024.1283357
Frontiers in Marine Science frontiersin.org07
viewed with caution as species’assignment to this cluster might be
unreliable, while the separate cluster formed by P. crassidens might
be entirely spurious. Despite these uncertainties, clusters identified
in this study are in broad agreement with the trophic clusters and
feeding habits of these species reported in other areas (Kenney,
1985), where the low-TP cluster likely represents zooplanktivores,
the mid-TP cluster represents micronektivores, the high-TP
comprises both micronekton and nekton piscivores and
teuthivores, and the P. crassidens cluster representing large
nekton consumers. Gavrilchuk et al. (2014) and MacKenzie et al.
(2022) also reported that M. novaeangliae occupied a higher trophic
position than the Balaenopterid whales. Amongst the odontocetes,
smaller dolphins like D. delphis,S. frontalis and S. coeruleoalba are
at lower trophic positions than T. truncatus and G. macrorhynchus
(Bode et al., 2022), while P. crassidens and P. macrocephalus
generally occupy the highest trophic positions in the community
(Bisi et al., 2013;Bode et al., 2022).
Clearly, species occupying different trophic guilds are unlikely
to show substantial trophic overlap. Indeed, overlap in isotopic
niches between species from different guilds was generally low
(<8%), with the exception of overlaps between M. novaeangliae
and two other baleen whales from the low-TP guild (B. musculus
and B. physalus), and between S. coeruleoalba and other dolphins
from the mid-TP guild (D. delphis and S. frontalis). This is not
surprising, given than these baleen whale and dolphin species have
similar morphological, behavioral and ecological traits (size, feeding
TABLE 2 Mean (bold) and 95% credible intervals (inside brackets) of pairwise overlaps in Bayesian ellipses (in %) calculated on SEA
B
.
Species
B (row) Bbo Bmu Bph Dde Mno Sfr Mbi Pma Sco Ttr Gma Pcr
Species
A (column) Cluster 1 Cluster 2 Cluster 3 Cluster
4
Bbo
Cluster1
18.4
[0,
49.8]
00
1.4
[0,
22.4]
000000 0
Bmu
14.5
[0,
40.2]
29.2
[8.4,
50.4]
0.8
[0,
7.8]
8
[0,
45.2]
0
[0, 0.2] 00
0.2
[0,
0.7]
00 0
Bph 0
62.7
[17.3,
100]
0.2
[0,
2.5]
13
[0,
69.7]
000
0.3
[0, 0] 00 0
Dde
Cluster2
0
2.6
[0,
23.2]
0.2
[0, 3]
10.5
[0,
72.7]
47.4
[18.8,
76.7]
0.3
[0,
4.5]
0
11.3
[0,
67.7]
0.5
[0,
5.9]
0.5
[0,
5.2]
0
Mno
1.4
[0,
20.7]
13.1
[0,
67.8]
10.5
[0,
53.5]
6.3
[0,
42.7]
4.2
[0,
32.7]
0.1
[0,
0.2]
0
3
[0,
36.8]
0.2
[0, 0]
0.1
[0, 0] 0
Sfr 0
0.2
[0,
0.8]
0
55.8
[22.2,
90.1]
8.5
[0,
69.7]
0.5
[0,
6.3]
0
21.7
[0,
84.9]
2.1
[0,
23.9]
1.1
[0,
15.8]
0
Mbi
Cluster3
0.2
[0, 0]
0.2
[0, 0]
0.1
[0, 0]
4.4
[0,
81.9]
1.5
[0,
7.6]
7.3
[0,
92.3]
2.7
[0,
51.5]
19.1
[0,
100]
13.6
[0,
100]
8.3
[0,
99.5]
0.4
[0, 0]
Pma 0000
0.2
[0, 0] 0
0.2
[0,
3.8]
6.6
[0,
65.6]
45
[0,
91.3]
8.5
[0,
48.2]
1.7
[0, 27.1]
Sco 00.3
[0, 1]
0.2
[0, 0]
7.2
[0,
41.1]
3.1
[0,
37.1]
12.6
[0,
47.5]
0.8
[0,
5.6]
3.1
[0,
29.9]
17.1
[0,
71.2]
3
[0,
30.3]
0.3
[0, 0]
Ttr 000
0.3
[0,
3.9]
0.5
[0, 0]
1.3
[0,
14.3]
0.6
[0,
5.6]
30.7
[0,
64.9]
20.3
[0,
80.6]
5.6
[0, 42]
1.1
[0, 17.3]
Gma 000
0.5
[0,
5.5]
0.3
[0, 0]
0.9
[0,
13.7]
0.6
[0,
6.1]
8.4
[0,
47.6]
5.5
[0,
61.1]
8.1
[0,
61.7]
5
[0, 47]
Pcr
Cluster4
0000
0.1
[0, 0] 00
1.9
[0,
30.7]
0.6
[0, 0]
1.8
[0,
29.7]
7
[0,
64.4]
Proportion of area of species A (column) overlapping area of species B (row) in each row. Highlighted cells are the largest overlaps in each cluster. See Table 1 for abbreviated name of species.
This table must be read by row, ex: The percentage of the niche of Bmu overlapping in the niche of Mno is 8%; the opposite is 13.1%. Mean (bold) and 95% credible intervals (inside brackets) of
pairwise overlaps in Bayesian ellipses (in %) calculated on SEAB.
Lebon et al. 10.3389/fmars.2024.1283357
Frontiers in Marine Science frontiersin.org08
strategy, dive depths, migration) and in other locations are known
to share common food resources and often overlap in isotopic
niches (Gavrilchuk et al., 2014;Gaspar et al., 2022;MacKenzie et al.,
2022). Nevertheless, M. novaeangliae and S. coeruleoalba feed at
higher trophic levels than the other species in their respective guilds,
and resource competition should be reduced, as long as resources
are not limited. On the other hand, there was a high degree of
overlap in isotopic niches between some pairs of species within the
same guild. Intra-guild niche overlap is discussed below in the
context of trophic redundancy.
4.2 Inter- and intra-specific variation in
niche characteristics within trophic guilds
4.2.1 Low-trophic position
The Mysticeti B. musculus,B. physalus and B. borealis occupied
the lowest trophic positions, consistent with their known preference
for zooplankton prey (Smith et al., 2015;Skern-Mauritzen et al.,
2022). Large differences in d
13
C between the three species indicate
the use of distinct habitats before reaching the sampling area (Silva
et al., 2019). As already noted by Silva et al. (2019),B. physalus and
B. borealis also differed significantly in d
15
N values, suggesting a
greater contribution of higher trophic level prey to the diet of B.
physalus than that of B. borealis. While differences in isotopic
baselines could have contributed to accentuate the difference in
d
15
N between the two species, these results agree with diet studies
based on SCA, which show that B. physalus feeds mainly on
euphausiids but also consume a variety of small schooling fish,
whereas B. borealis feeds primarily on lower-trophic level calanoid
copepods (Sigurjonsson and Vı
kingsson, 1997).
In agreement with our predictions, these migratory baleen
whales had the widest isotopic niches and the widest ranges in
d
13
C values, which clearly indicates use of multiple carbon sources.
Nevertheless, there were considerable interspecific differences in
niche characteristics. B. musculus and B. borealis had larger niches
(SEA
B
) and higher niche diversity (CD) than B. physalus
(Figures 3D and 4) and these differences were primarily driven by
their wide range in d
13
C values and to a lesser extent by variation in
d
15
N. Conversely, B. musculus and B. borealis showed lower degree
of clustering (NND) and more uneven distribution (SDNND) of
individuals within the niche space relative to B. physalus. Taken
together these results indicate that, within the population of B.
musculus and of B. borealis, different individuals exploited distinct
habitats along the coast-open ocean gradient in baseline d
13
C values
(or varied in time spent foraging in different baselines), suggesting
higher plasticity in foraging habitat use in these species. On the
other hand, B. physalus showed larger variations in d
15
N (3.62‰;
the largest of all species) than in d
13
C (3.20‰), indicating
exploitation of a wider range of feeding resources than B.
musculus and B. borealis. In addition, B. physalus had the lowest
NND and SDNND among all cetaceans, suggesting restricted inter-
individual variability in diet and foraging habitats, regardless of age
class, although we cannot ignore potential effects from sample size
as highlighted by Layman et al. (2007).
4.2.2 Mid-trophic position
Estimates of isotopic niche size and Layman metrics of M.
novaeangliae should be viewed with caution as they are likely biased
by low sample size (Jackson et al., 2011). Still, the presence of M.
novaeangliae in this guild, rather than in the low-TP guild, is in
agreement with previous studies that indicate a greater reliance on
higher trophic level prey, in particular small schooling fish,
compared to other baleen whales (Johnson and Davoren, 2021).
D. delphis and S. frontalis dolphins had very similar niche
characteristics and sizes (Figures 3 and 4). Samples from both
species (D. delphis and S. frontalis) were collected mainly in July and
August, and skin isotopic incorporation for dolphins has been
estimated at 180 ± 71 days (Gimenez et al., 2016). Therefore,
isotopic compositions in our study correspond to prey and
habitats from winter and spring. D. delphis is found year-round
in the Azores, while S. frontalis only occurs from late spring to early
autumn (Silva et al., 2014). d
13
C values of S. frontalis therefore
reflect carbon sources from various habitats. However, both species
have extremely similar d
13
C values, which suggests that the habitat
used by S. frontalis before reaching the sampling area is comparable
to the Azores: an oceanic environment depleted in
13
C. Seasonality
in sightings suggests that S. frontalis may move between the Azores,
Madeira and the Canary Islands (Querouil et al., 2010;Silva et al.,
2021). These oceanic Macaronesian archipelagos share similar
oceanographic characteristics, potentially leading to comparable
carbon baselines. This is supported by previous studies that also
failed to detect significant differences in muscle isotope values of D.
delphis and S. frontalis from the three archipelagos (Moreira et al.,
2018;Bode et al., 2022).
d
15
N ranges of D. dephis and S. frontalis were amongst the
largest and d
13
C ranges were intermediate between those of
Balaenoptera whales and other cetaceans. As with B. physalus, the
wide range of d
15
N values suggests high intraspecific diet plasticity.
Knowledge of the feeding habits of both species in the Azores is
scarce but in other areas they are known to be generalist predators
that can feed on a variety of epipelagic, mesopelagic and benthic
fishes, squids, and invertebrates (Perrin, 2009;Herzing and Perrin,
2018;Peters et al., 2020). In addition, both species displayed high
levels of clustering (NND) and even distribution (SDNND) of
individuals within the respective niches (Figure 3), indicating that
all individuals fed on similar isotopic sources and habitats.
4.2.3 High- trophic position
This guild is the most diverse in terms of the number and traits
of species, encompassing both small and large delphinids and
toothed whales. Although species within this guild occur year-
round off the Azores (T. truncatus,S. coeruleoalba,P.
macrocephalus and M. bidens) or visit the region regularly (G.
macrorhynchus), the distribution range of individual groups may
extend beyond this area. In fact, photo-identification data has
documented movements of individuals of T. truncatus,G.
macrorhynchus and P. macrocephalus between the Macaronesian
archipelagos (Alessandrini, 2016;Alves et al., 2018;Dinis et al.,
2021;Ferreira et al., 2022), and it is possible they occasionally
venture outside Macaronesia. Similarly to what was observed for S.
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Frontiers in Marine Science frontiersin.org09
frontalis, however, species within this guild showed relatively low
d
13
C values, but also narrow ranges of d
13
C values, indicating they
foraged mainly in oceanic waters. The only exception was G.
macrorhynchus that was slightly enriched in
13
C relative to other
guild members, suggesting a greater contribution of food from
coastal and/or more productive food webs.
The inclusion of S. coeruleoalba in this guild seems somewhat
surprising. Pairwise tests indicated that d
15
NvaluesofS.
coeruleoalba only differed from those of P. macrocephalus
(Supplementary Table S6), suggesting that it feeds at a trophic
level similar to all other species in the guild. Bode et al. (2022) also
separated the delphinids from Macaronesia into two groups based
on significant differences in their trophic position, with S.
coeruleoalba belonging to the high trophic position group along
with G. macrorhynchus, G. griseus and T. truncatus, while D. delphis
and S. frontalis belonged to the low trophic position group. As in
our study, S. coeruleoalba occupied a trophic position lower than P.
macrocephalus. In the Bay of Biscay, S. coeruleoalba feeds on prey
from oceanic, neritic and coastal habitats, and consume more
cephalopods than D. delphis (Spitz et al., 2006) but other studies
in the North east Atlantic reported higher reliance on mesopelagic
fish, namely myctophids (Ringelstein et al., 2006;Archer, 2018).
Stomach contents of M. bidens stranded in the Azores were also
dominated by myctophids (Pereira et al., 2011), and d
15
N values of
this species were very similar to those of S. coeruleoalba, although
the range in d
15
N was narrower, it had a smaller niche and lower
niche diversity. However, it is important to stress that sample size
for M. bidens was very small (n=4) and three out of four samples
came from the same group, which could explain the reduced
variability in nitrogen values in this species. Compared to other
species in this guild, G. macrorhynchus showed a narrower range of
d
15
N values (1.41‰), suggesting a rather specialized diet, albeit
some degree of individual variability in niche space. This agrees
with the known feeding habits of the species that preys almost
exclusively on oceanic cephalopods, mainly on ommastrephid
squids (Clarke, 1996;Fernandez et al., 2009). Still, sample size for
this species was also small (n=10) and results should be taken
with caution.
T. truncatus are known to be opportunistic predators and
consume a wide range of locally abundant pelagic and benthic
prey (Rossman et al., 2015;Gimenez et al., 2016), whereas off the
Azores P. macrocephalus mostlyfeedsonsquidsfromthe
Octopoteuthidae and Histiotheuthidae families (Clarke et al.,
1993). Despite dietary differences, the two species did not differ
significantly in isotope values and their niche sizes were similar. In
addition, both species showed considerable variability in d
15
N
values and relatively high trophic diversity (Figure 3), although
the delphinid (T. truncatus) had higher values of SDNND,
indicating a more uneven distribution of individuals within the
niche space than P. macrocephalus. This could indicate some degree
of individual dietary specialization within this generalist species
(Wells and Scott, 2009;Neri et al., 2023). Sex-related and
ontogenetic differences in diet composition have been reported in
other areas (Lopez, 2003;Knoff et al., 2008;Neri et al., 2023) and
could help explaining these results. Alternatively, or in combination
with this hypothesis, differences in residence and habitat use
patterns between different groups (Silva et al., 2008)canalso
influence their diet composition, as island-associated groups may
have increased access to coastal and benthic prey relative to
transient dolphins. Future studies should examine individual
differences in stable isotope composition of this and other
cetacean species.
4.2.4 Pseudorca crassidens
Compared to the other species, P. crassidens showed a highly
enriched
13
C composition, corresponding to more coastal or
benthic environments. The distribution and movements of P.
crassidens in the Northeast Atlantic are poorly documented,
making it impossible to identify the origin of their carbon source.
Our results suggest that P. crassidens feeds at higher trophic levels
than all other studied species. While these results could be due to P.
crassidens feeding on distinct d
15
N baselines, they are consistent
with the known diet of this species. Indeed, P. crassidens feeds on a
variety of fish and squid, but occasionally target large predatory fish
like tuna and even dolphins (Baird, 2009). Such dietary diversity
could partly explain the low degree of packing and uneven
distribution of samples within the species’niche, but the small
sample size precludes drawing any definitive conclusions.
4.3 Intra-guild niche overlap and
trophic redundancy
Trophic redundancy occurs when multiple species have similar
feeding ecologies and consume the same types of resources within
an ecosystem. It is generally assumed that such species have similar
ecological roles in the community or ecosystem (Paine, 1980).
Trophic redundancy can enhance ecosystem stability and
resilience potential, reducing the cascading effects of natural and
anthropogenic disturbance and biodiversity loss (Borrvall et al.,
2000;Sanders et al., 2018). Indeed, if several species occupy the
same or similar roles, this may ensure against the loss of ecosystem
functioning following changes in species diversity or abundance
(Yachi and Loreau, 1999).
We found significant overlap between one pair of species within
each guild (with the obvious exception of the guild containing only
P. crassidens), suggesting some degree of trophic redundancy within
the cetacean community (Table 2). Within the low-TP guild, B.
physalus niche significantly overlapped with that of B. musculus
(62.7%), similarly to what has been reported in other areas
(Gavrilchuk et al., 2014;Garcı
a-Vernet et al., 2021). These baleen
whales undertake long-distance seasonal migrations and their
isotope values likely reflect foraging across multiple habitats along
their migration. In particular, the high variability in d
13
C values in
B. musculus suggests that some individual whales foraged in more
13
C-enriched environments, while others mainly exploited
13
C-
depleted habitats, exhibiting stable isotope compositions very
similar to those of B. physalus (Figure 2). While these results
point to some degree of spatial segregation between the species,
they also suggest strong niche overlap between part of the
populations. Consequently, where B. musculus and B. physalus
coexist spatially and temporally, such as off the Azores (Visser
Lebon et al. 10.3389/fmars.2024.1283357
Frontiers in Marine Science frontiersin.org10
et al., 2011), they might support similar functions, thus increasing
ecosystem redundancy. Baleen whales consume large quantities of
prey and egest their remains in the photic zone. Predation by baleen
whales in the Azores may be of great importance in recycling
limiting nutrients to primary producers, thus stimulating ecosystem
productivity, as well as in maintaining the energy flow and species
composition in the food-web (Roman et al., 2014).
In the mid-TP guild, the isotopic niches of D. delphis and S.
frontalis showed a high degree of overlap (47.4-55.8%). In addition,
the two species did not differ in carbon or nitrogen stable isotope
values (Supplementary Table S6). D. delphis and S. frontalis also
have overlapping spatial distributions in the Azores (Tobeña et al.,
2016) but they are temporally segregated in the area, as sighting
rates of D. delphis decrease in spring and summer, when S. frontalis
occurs in the area (Silva et al., 2014). Therefore, D. delphis and S.
frontalis occupy similar niches and may perform similar ecological
roles but during distinct periods, indicating they have
complementary rather than redundant roles. These results also
illustrate how intra-guild niche partitioning can influence species’
demography locally and determine the structure and role of the
community. It remains unclearhowchangesinthetemporal
distribution of one species would affect the other species
distribution, and whether this could lead to their ecological role
being temporally vacant.
Surprisingly, the niche of P. macrocephalus overlapped
considerably with that of T. truncatus (45%), despite the slightly
higher trophic position of P. macrocephalus. As mentioned above,
the two species have strikingly different diets, although this
indicates that their preferred prey items should have similar
isotopic values. Both species are present year-round and exploit
similar areas in the Azores, but T. truncatus forages mostly within
the epipelagic layer, whereas P. macrocephalus feeds in waters
deeper than 700 m depth (Oliveira et al., 2022). The two species
could feed on prey undergoing diel vertical migration, therefore
having access to the same prey at different depths and times of the
day, explaining the similarity in stable isotope values. While both
species are locally abundant throughout the year, and their
contribution to nutrient recycling and food-web interactions is
potentially large (Gilbertetal.,2023), it’sunlikelytheyplay
similar roles in the ecosystem.
It should be stressed that accounting only for the characteristics
of species’isotopic niches and disregarding the species’traits and
strength of interactions among species, when analyzing trophic
redundancy might lead to oversimplified interpretations. Indeed,
the intensity of niche overlaps and functional redundancy may also
be a function of species abundance, diving behavior and daily
feeding patterns. To overcome this limitation, food-web models
could be used to provide a more comprehensive representation of
trophic links and strength of interactions and examine impacts of
different cetacean species on ecosystem structure and function.
5 Conclusions
This study is the first to describe the isotopic niches of cetaceans
in the Azores. We have investigated intraspecificniche
characteristics of the twelve studied species, including habitat and
resource use and specialization. Our results suggest the presence of
four distinct trophic guilds in the community, and we discuss niche
overlaps amongst species belonging in the same guild, in a context
of trophic redundancy and ecological roles in the ecosystem.
However, further research is needed to understand species’
niches and the structure of this community. For example, sexual
and ontogenetic differences in isotopic compositions should be
further explored to investigate their potential influence in
intraspecific variability in trophic niches and in interspecific niche
overlap. Differences in energetic demands, foraging abilities, or
habitat use patterns between individuals with distinct traits (e.g.,
bodysize,sex,reproductivestatus) may result in substantial
differences in diet composition and/or segregation in feeding
areas (Laigle et al., 2018). Although previous studies on the same
species reported limited differences in stable isotopes between sexes
(Ruiz-Cooley et al., 2004;Silva et al., 2019;Peters et al., 2020), and
while we excluded samples from calves known to have higher d
15
N
values (Borrell et al., 2016), the effects of sex, age class (adult vs. sub-
adult) and reproductive status on size and characteristics of each
species’niche remain unknown. Additionally, the use of other
isotopes as additional dimensions could contribute to better
understand the partitioning of species. For example, sulfur and
hydrogen isotopes can provide additional information on species
habitat use and the origin of sources (Peterson and Fry, 1987), while
oxygen can be used to retrace migration (Clementz and Koch,
2001), and mercury can inform on foraging depth (Besnard
et al., 2021).
Data availability statement
The raw data supporting the conclusions of this article will be
made available by the authors, without undue reservation.
Ethics statement
The animal study was approved by The Regional Directorate for
the Environment, the Regional Directorate for Sea Affairs, and the
Regional Directorate for Maritime Policies, of the Regional
Government of the Azores (Fieldwork and sample collection were
conducted under permits LMAS-DRPM/2023/02, LMAS-DRAM/
2021/12, LMAS-DRAM/2020/06, LMAS-DRAM/2018/06, 80/2017/
DRA, 37/2016/DRA, 30/2015/DRA, 34/2014/DRA, 20/2013/DRA,
31/2012/DRA, 51/2011/DRA, 16/2010/DRA, 20/2009/DRA, 76/
2007/DRA, 4/2006/DRA, 7/2005/DRA). The study was conducted
in accordance with the local legislation and institutional requirements.
Author contributions
ML: Conceptualization, Data curation, Formal analysis,
Methodology, Writing –original draft, Writing –review &
editing. AC: Investigation, Writing –review & editing. RP:
Resources, Writing –review & editing. IC: Resources, Writing –
Lebon et al. 10.3389/fmars.2024.1283357
Frontiers in Marine Science frontiersin.org11
review & editing. CO: Resources, Writing –review & editing. MT:
Resources, Writing –review & editing. YP: Writing –review &
editing, Formal analysis. JS: Conceptualization, Methodology,
Supervision, Writing –review & editing. MS: Conceptualization,
Data curation, Funding acquisition, Methodology, Investigation,
Project administration, Resources, Supervision, Writing –original
draft, Writing –review & editing.
Funding
The author(s) declare financial support was received for the
research, authorship, and/or publication of this article. This study
was supported by projects SUMMER (H2020-BG-2018-2, GA
817806), funded by the EU, and MISTIC SEAS 3 (110661/2018/
794676/SUB/ENV.C2), funded by the Directorate General
Environment of the European Commission. Data collection was
supported by the Portuguese Science & Technology Foundation
(FCT) and the Azorean Science & Technology Fund (FRCT)
through TRACE -PTDC/MAR/74071/2006, MAPCET -M2.1.2/F/
012/2011 and FCT Exploratory -IF/00943/2013/CP1199/CT0001
(FEDER, COMPETE, QREN, POPH, ESF, Portuguese Ministry for
Science and Education, OP Azores 2020). ML was supported by
FRCT and DRCT through M3.1.a/F/006/2021 and M1.1.C/
PROJ.EXPLORATO
RIOS/010/2022. MAS, AC and RP were
supported by the OP AZORES2020 through Fund 01-0145-
FEDER-1279 000140 “MarAZ Researchers: Consolidate a body of
researchers in Marine Sciences in the Azores”of the EU. AC was
further supported by FCT through project (10.54499/
2021.00101.CEECIND/CP1669/CT0001), IC by FCT-IP Project
UIDP/05634/2020, and CO by Biodiversa+, the European
Biodiversity Partnership under the 2021-2022 BiodivProtect joint
call for research proposals, co-funded by the European Commission
(GA N°101052342) and the Regional Government of the Azores,
through the Regional Fund for Science and Technology (FRCT),
under the project EUROPAM -European Spatial-Temporal Large
Scale Sea Noise Management & Passive Acoustic Monitoring of
Marine Megafauna (ref. 488). JS was supported by SUMMER
(H2020-BG-2018-2, GA 817806) and the French Environmental
Ministry. OKEANOS is funded by FCT under projects UIDB/
05634/2020 and UIDP/05634/2020, and by the Regional
Government of the Azores through the initiative to support the
Research Centres of the University of the Azores and through
project M1.1.A/REEQ.CIENTIFICO UI&D/2021/010. Publication
fees were covered by grant M1.1.C/PROJ.EXPLORATO
RIOS/010/
2022 from DRCT.
Acknowledgments
We thank Sergi Perez-Jorge, Miriam Romagosa and all the
interns and volunteers who over the years helped with fieldwork
and data collection. We are also grateful to our skippers, Bruno
Castro and Renato Bettencourt, and to the whale watching
companies and lookouts from Faial and Pico islands for all the
support at sea.
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.
The reviewer JG declared a past co-authorship with the author
JS to the handling editor.
The author(s) declared that they were an editorial board
member of Frontiers, at the time of submission. This had no
impact on the peer review process and the final decision.
Publisher’s note
All claims expressed in this article are solely those of the authors
and do not necessarily represent those of their affiliated organizations,
or those of the publisher, the editors and the reviewers. Any product
that may be evaluated in this article, or claim that may be made by its
manufacturer, is not guaranteed or endorsed by the publisher.
Supplementary material
The Supplementary Material for this article can be found online
at: https://www.frontiersin.org/articles/10.3389/fmars.2024.
1283357/full#supplementary-material
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