Introduction
Ontogenetic shifts in marine predators are major drivers in the
mechanisms underlying ecosystem structure and functioning (Rudolf and
Rasmussen, 2013; Nakazawa, 2015). They are also considered a determinant
of food web diversity and stability, community resilience, and responses
to disturbance (de Roos and Persson, 2013; Nakazawa, 2015; Nilsson et
al., 2018). Although the importance of these ubiquitous changes in
ecosystems is well established, community ecology has traditionally been
based on species, thereby erasing intraspecific differences.
During ontogeny, individuals must
make trade-offs between their dietary needs, conditions necessary for
reproduction, and predator avoidance (Sutherland, 1996; Kimirei et al.,
2013; Sánchez-Hernández et al., 2019). All of these needs and trade-offs
change over the lifetime of species, requiring them to find habitats
that meet their needs (Werner and Gilliam, 1984; McNamara and Houston,
1986; Werner and Hall, 1988; Ludwig and Rowe, 1990). Thus, shifts in
diet and habitat use during ontogeny can lead to segregation in the
niches occupied by individuals of a species and thus reduce
intraspecific competition within a population (Sánchez-Hernández and
Cobo, 2012; Wollrab et al., 2013). At the interspecific level, these
shifts also play an important role in competitive interactions and niche
partitioning (Woodward and Hildrew, 2002; Woodward et al., 2005; de Roos
and Persson, 2013).
Fish species often show a close relationship between body size, which is
generally related to the size of the mouth opening, and the size of the
prey they consume (Dunic and Baum, 2017). Therefore, ontogenetic shifts
in resource use are very common in fish (Werner and Gilliam, 1984). In
general, early-stage fish feed on phytoplankton, zooplankton, or small
invertebrates (Nunn et al., 2012). As their vision and swimming
performance improve, fish begin to feed on macroinvertebrates and fish
(Huss et al., 2013). These shifts in food types are often associated
with or caused by a shift in habitat uses (Werner and Gilliam, 1984;
Sánchez-Hernández et al., 2019). For instance, a change in diet may be
the consequence of a change in habitat to cope with new predation risks
during ontogeny, or it may be caused by the search for more nutritious
and/or more abundant prey (Sánchez-Hernández et al., 2019). An example
of the consequences of a change in diet dictated by a change in habitat
use is that of small individuals of the Gobiidae speciesPterogobius elapoides , feeding on abundant pelagic copepods in
the water column where predation is high. As the individuals grow
larger, they limit the risk of predation by feeding only on prey found
in the sediments of the sandy bottom (Choi and Suk, 2012).
Meso- and bathypelagic fish communities (i.e., inhabiting the
mesopelagic zone between 200-1000 m, and the bathypelagic zone below
1000 m depth) are believed to dominate the fish biomass worldwide
(Irigoien et al., 2014). The deep pelagic food web is supported solely
by phytoplankton primary production, resulting in the segregation of
deep pelagic fish trophic niches essentially along a continuum of
trophic levels (Stowasser et al., 2012; Valls et al., 2014; Chouvelon et
al., 2022; Richards et al., 2023). Three main food guilds are generally
described for midwater fishes: zooplanktivores (e.g., Myctophidae),
micronektivores (e.g., Stomiidae), and generalists (e.g.
Eurypharyngidae, in which a wide variety of prey even benthic, is found)
(Gartner Jr et al., 1997; Drazen and Sutton, 2017). In addition to these
guilds, two main foraging strategies are employed by deep pelagic
fishes. Part of the community performs diurnal vertical migrations (DVM)
at night from the mesopelagic to the epipelagic zone to feed (Clarke,
1963; Badcock and Merrett, 1976; Watanabe et al., 1999). This migratory
behaviour is very energy-consuming but is compensated by the high prey
density in the epipelagic zone and the reduction of visual predation at
night. The non-migratory part of the community remains at depth. The
non-migratory species thus live in an environment of low prey density
but have lower energy requirements and a low risk of predation
(Marshall, 1979; Herring, 2001).
Most deep pelagic species, particularly Myctophidae, spend their larval
stage in the productive epipelagic zone (Ahlstrom, 1959; Loeb, 1979;
Moser and Smith, 1993; Sassa et al., 2002, 2004; Bowlin, 2016). Within
species, individual size generally increases with depth, indicating
ontogenetic vertical migrations (Loeb, 1979; Kawaguchi and Mauchline,
1982; Badcock and Araujo, 1988; Sassa and Kawaguchi, 2006). This
ontogenetic shift along the vertical habitat is related to shifts in
morphology and pigmentation (i.e., individuals becoming darker, having
photophores, and well-developed musculature) (Moser, 1996). Similarly,
the adults of several species have a different depth distribution
according to size, with larger individuals at deeper depths (Badcock and
Merrett, 1976; Loeb, 1979; Willis and Pearcy, 1980; Auster et al., 1992;
Stefanescu and Cartes, 1992; Sassa et al., 2007; Fanelli et al., 2014).
These ontogenetic shifts in habitat use may be related to shifts in
diet, as in the case of Lampanyctus crocodilus , where senescent
adults stop migrating and adopt benthopelagic behavior by feeding on
epibenthic prey (Stefanescu and Cartes, 1992; Fanelli et al., 2014).
Intraspecific trophic changes can be monitored from stable isotope
signatures (Hammerschlag-Peyer et al., 2011; Layman et al., 2012). For
decades, stable isotope ratios of nitrogen (δ15N
values) have been widely used as an indicator of species’ trophic level
(Peterson and Fry, 1987; Zanden and Rasmussen, 2001; Drazen and Sutton,
2017). This is because nitrogen isotopes undergo a significant and
relatively predictable level of fractionation during trophic transfer
between a predator and its prey, leading to a difference in
δ15N values (~3-5‰) between two
theoretical trophic levels and allowing the relative trophic level of
species to be inferred from their δ15N values
(Peterson and Fry, 1987; Post, 2002; Hussey et al., 2014). Since the
pelagic ecosystem has a wide depth gradient, microbial degradation of
organic matter in suspended particles also influences
δ15N values, with increasing values with depth (Saino
and Hattori, 1980; Casciotti et al., 2008). An enrichment in15N is thus found in zooplankton at greater depths
(Koppelmann et al., 2009; Hannides et al., 2013) and in deep benthic
communities (Bergmann et al., 2009; Trueman et al., 2014).
Only a few studies examined the effect of species size and depth on
δ15N values of deep pelagic fish, such as in the
Iberian Peninsula (North-East Atlantic) and the Gulf of Mexico
(North-West, Atlantic) (Romero‐Romero et al., 2019; Richards et al.,
2023), but never at the intraspecific scale. Here, we aimed to quantify
the influence of ontogeny on nocturnal habitat use and trophic ecology
for 12 deep pelagic fish belonging to nine genera, including both
migratory and non-migratory species from the Bay of Biscay, NE Atlantic.
Changes in foraging habitats were studied through shifts in the use of
the water column at night inferred from trawling data, while trophic
shifts were studied using stable isotopes of nitrogen measured in fish
muscle tissues. The first objective was to investigate whether an
ontogenetic shift in the water column utilization (i.e., relationships
between individual size and sampling depth) is observed at both the
specific and community level. The second objective was to explore if a
shift in the trophic ecology (and possibly in the trophic level) is also
observed during ontogeny (from the measurement of δ15N
values). To this end, the influence of individual size and/or sampling
depth on δ15N values was quantified for each species.