Download Evolutionary and ecological constraints of fish spawning habitats

ICES Journal of
Marine Science
ICES Journal of Marine Science (2015), 72(2), 285– 296. doi:10.1093/icesjms/fsu145
Review
Evolutionary and ecological constraints of fish spawning habitats
Lorenzo Ciannelli 1 *, Kevin Bailey 2, and Esben Moland Olsen 3,4
1
College of Earth, Ocean, and Atmospheric Sciences, Oregon State University, Corvallis, OR 97331, USA
Man & Sea Institute, LLC, 10335 46th Avenue NE, Seattle, WA 98125, USA
3
Institute of Marine Research, Flødevigen, 4817 His, Norway
4
Department of Natural Sciences, University of Agder, PO Box 422, 4604 Kristiansand, Norway
2
*Corresponding author: tel: +1 541 737 3142; fax: +1 541 737 2064; e-mail: [email protected]
Ciannelli, L., Bailey, K., and Olsen, E. M. Evolutionary and ecological constraints of fish spawning habitats. – ICES Journal of Marine
Science, 72: 285 – 296.
Received 25 March 2014; revised 31 July 2014; accepted 4 August 2014; advance access publication 4 September 2014.
For marine fish, the choice of the spawning location may be the only means to fulfil the dual needs of surviving from the egg to juvenile stage and
dispersing across different habitats while minimizing predation and maximizing food intake. In this article, we review the factors that affect the
choice of fish spawning habitats and propose a framework to distinguish between ecological and evolutionary constraints. We define the
former as the boundaries for phenotypically plastic responses to environmental change, in this case the ability of specific genotypes to change
their spawning habitat. Processes such as predation, starvation, or aberrant dispersal typically limit the amount of variability in spawning
habitat that fish may undergo from 1 year to the next, and thus regulate the intensity of ecological constraints. Evolutionary constraints, on
the other hand, refer to aspects of the genetic make-up that limit the rate and direction of adaptive genetic changes in a population across generations; that is, the potential for micro-evolutionary change. Thus, their intensity is inversely related to the level of genetic diversity associated with
traits that regulate spawning and developmental phases. We argue that fisheries oceanographers are well aware of, and more deeply focused on, the
former set of constraints, while evolutionary biologists are more deeply focused on the latter set of constraints. Our proposed framework merges
these two viewpoints and provides new insight to study fish habitat selection and adaptability to environmental changes.
Keywords: ecological constraint, evolutionary constraint, spawning habitat.
Introduction
Most marine bony fish species have external fertilization, and
to breed they gather year after year, often in large aggregations
within a concentrated area—the spawning ground. Yet, marine
fish find themselves caught between competing needs when it
comes to choosing a spawning location. On one side, like many
marine invertebrates, most fish have to complete pelagic embryonic
and/or postembryonic development while drifting with the prevailing currents. On the other side, and unlike many marine invertebrates, fish have to spatially close their life cycle, in ways that allow
ontogenetic connections among distant habitats and that increase
opportunities for feeding and escaping predation. In this context,
the location of the spawning habitat may be the only means that
fish have to fulfil various needs including that of surviving from
the egg to juvenile stage and dispersing across different habitats
while minimizing predation and maximizing food intake.
# International
The spawning location of marine fish typically has been viewed as
an adaptive choice to increase opportunity for larval feeding (Slotte
and Fiksen, 2000; Agostini and Bakun, 2002; Bakun, 2006), reduce
larval, egg and adult predation (Bakun, 2013), or stabilize transport
toward suitable nursery locations (Symonds and Rogers, 1995;
Bailey et al., 2005; Karnaukas et al., 2011). While these factors
certainly pose constraints on the choice of spawning habitats, they
are likely not the only ones at work. If feeding, predation, and dispersal
constraints were the main factors affecting the selection of a spawning
habitat, there would be an evolutionary pressure toward reducing
the extent of highly vulnerable life-history stages (i.e. the pelagic
larval duration) by restricting the dispersal phase and the time to
settlement—spawning habitats would ultimately be located near
the juvenile settlement areas and larval development would be considerably shortened. Several fish species seem to follow this strategy
(e.g. tropical or coastal fish species with short pelagic larval duration),
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L. Ciannelli et al.
but many others do not. Temperate and Subarctic fish species, for
example, are sometimes characterized by long pelagic larval duration
and extensive larval drift (Bradbury et al., 2008). Some fish populations, like coastal populations of Atlantic cod (Gadus morhua),
have long pelagic larval duration but are locally and coastally retained
(Ciannelli et al., 2010)—a strategy that hardly seems motivated by the
need of dispersing to the co-located nursery locations. It is likely that
the choice of a spawning habitat also depends on other constraints
acting on different life-history stages including the developing
embryo, larvae, juveniles, and adults. Thus, factors that contribute
to the selection of a spawning location are many and complex, and
depend on constraints that affect fish throughout their entire life
cycle, not only the larval stage (Claydon, 2004; McNamara and
Houston, 2008). It is therefore anticipated that the choice of a
suitable spawning location is subject to multiple trade-offs operating
at different spatiotemporal scales, the balance of which is linked to the
life history of the species (Jørgensen et al., 2008).
The goal of this article is to review the factors that affect the choice
of fish spawning habitats. Here the term “choice” is used metaphorically to indicate an evolutionary compromise among multiple
constraints. We consider fish species with pelagic embryonic or
postembryonic development and dispersing early life-history
stages from temperate and Subarctic systems in the Atlantic and
Pacific Oceans, for which we have greater knowledge and access to
data. We propose to expand similar concepts to fish species with a
variety of reproductive strategies and from diverse habitats. Our
eco-evolutionary framework to study fish spawning distribution
serves two purposes. First, it promotes new lines of inquiries to
study fish habitat selection. Second, it provides new insight to
study species adaptability to future environmental changes.
Type of constraints on fish spawning habitats
Ecological and evolutionary constraints
In our review, we refer to ecological and evolutionary constraints
affecting species’ spawning strategies (Table 1). We define the
former as those driven by the present and local environment.
Ecological constraints limit the ability of a population to change
Table 1. Description of ecological and evolutionary constraints
to changes of fish spawning habitats.
Ecological
Source of the
Present and local
constraint
environment
Demographic level Population
of the
constraint
Factors affecting
Predation, starvation,
the strength
competition, and
dispersal
Persistence
Traits affected by
the constraint
Consequences
Evolutionary
Species evolutionary
history
Species
Completing
development, social
structure, and
reproductive and larval
physiology
Low
High
Mostly behavioural
Egg buoyancy, larval
traits, directing fish to
behaviour, and pelagic
their spawning and
larval duration
nursery grounds
Constraints on
Constraints genetic
phenotypic plasticity
adaptations of
of spawning strategies
spawning strategies
its spawning habitat without incurring genetic adaptation, that is,
the boundaries for phenotypically plastic responses to environmental change. Processes such as predation, starvation, or aberrant dispersal typically limit the amount of variability in spawning habitat
that fish may undergo from 1 year to the next, and thus regulate
the intensity of ecological constraints. Evolutionary constraints,
on the other hand, refer to aspects of the genetic make-up that
limit the rate and direction of adaptive genetic changes in a population across generations; that is, the potential for micro-evolutionary
change (Olsen et al., 2009; Futuyma, 2010). Thus, their intensity is
inversely related to the level of genetic diversity associated with
traits that regulate spawning and developmental phases in the
entire species. For instance, some developmental traits may
become fixed at higher taxonomic levels (i.e. lineage-specific
effects) and offer no genetic variation for selection to act on.
These traits then become reference points for selection on other
traits in the organism (Stearns, 1992).
Spawning habitats are not ephemeral
Fish spawning in specific locales have been observed to repeat
spawning there. Fish can navigate thousands of kilometres to
reach the exact same site in which they were born (natal homing,
Cury, 1994; Thorrold et al., 2001) or had previously spawned
(repeated homing, Corten, 2002; Skjæraasen et al., 2011). High
site fidelity during spawning allows fish to place their offspring in
the same location or set of environmental conditions of the parental
or sibling generations, therefore, has fitness consequences. Yet, this
remarkable attachment to a specific site is only expressed at the time
of spawning, while there seems to be more plasticity and opportunistic behaviour when it comes to the choice of other important habitats, such as feeding grounds and, for some species, the juvenile
nursery habitat (Petitgas et al., 2012). This is demonstrated by examining the distribution range and spatial consistency of walleye
pollock (Gadus chalcogrammus, formerly Theragra chalcogramma)
throughout its life-history cycle in the eastern Bering Sea. Here,
we pragmatically quantify the spatial consistency of a population
life-history stage as directly proportional to the percentage of variance explained (i.e. R 2) by a statistical model (in this case generalized
additive model) that only contains geographic location and time of
the year as covariates, and is fit to multiple years. For the walleye
pollock case study, egg distribution, indicative of spawning habitats,
is spatially constrained compared to other stages, and over time is
consistently located in the southeast region of the surveyed grid.
In contrast, the spatial range of older pollock stages increases and
spatial consistency decreases (Figure 1).
The locations where fish spawn are either fixed in geographical or
in environmental coordinates. Fish use these geographic clues or environmental cues as a guiding compass to reach spawning locations
year after year, but they may also learn spawning routes through
social facilitation (Cury, 1994; Corten, 2002). Regardless of how
they reach their ultimate reproductive locale, the set of environmental and topographical conditions that fulfil the constraints on
spawning cannot be present in 1 year and absent in the following
year; it must on average always be present for fish to successfully
aggregate and reproduce. Thus, fish spawning habitats are not
ephemeral. This characteristic has important consequences on the
adaptability of fish to environmental changes—a topic reviewed
in the section Plasticity and adaptations.
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Fish spawning habitats
Figure 1. Spatial distribution of walleye pollock throughout various life-history stages in the southeastern Bering Sea. Image colour and red contour
lines indicates predicted abundance from a generalized additive model (GAM) in which spatial coordinates (latitude and longitude), time of the
year and year of survey where included as covariate. Abundance increases going from blue to yellow. Bubbles are the raw data and are proportional
to local abundance. Zero catches were not included in the analysis. The top left panels show egg distribution while other panels show the spatial
distribution of progressively larger life-history stages. Each panel contains the respective size range and the percentage of variance explained (R 2) by
the GAM model. Eggs data are from the Alaska Fisheries Science Center (AFSC) ichthyoplankton surveys from 1979, 1986, 1988, 1991 –2006
(Bacheler et al., 2012). Data for older pollock stages are from the AFSC groundfish survey during 1982 – 2011 (Lauth, 2011).
Processes affecting the intensity of constraints
on fish spawning habitats
In Table 1, we have identified a number of processes that modulate
the intensity of an evolutionary and ecological constraint. Here we
describe in greater detail these processes and provide evidence of
their influence on fish spawning distributions, starting from the
evolutionary ones.
Evolutionary processes
Completing development
Fish with external fertilization and a planktonic larval development
disperse with the currents. Thus, the question of what constrains the
choice of a spawning locale cannot be separated from question of
what constrains the early life development. The “migration hypothesis” states that the planktonic larvae of many marine invertebrates
perform a migration into the plankton for feeding and safety
(Strathmann, 1985). The hypothesis was first developed for
marine invertebrates but it bears an appealing analogy to fish life histories as well (Strathmann et al., 2002). A corollary of this hypothesis
is that while ocean conditions are permissive of pelagic and dispersing larval stages, dispersal itself is not the primary cause for why fish
have a planktonic early life-history stage. Confronted with the
choice of a pelagic or benthic development, the former may be a
valid alternative, because it provides safety from predation, access
to greater variety of food supplies and better oxygenation for the
developing embryo and larvae (Strathmann, 1985). This perspective
does not imply that larval dispersal in fish is not under adaptive
selection. Fish can change their dispersal strategy by changing the
location where they spawn, larval behavioural traits, egg buoyancy,
etc. All of these adaptations are tuned to the environment, but fish
survival will still depend on the spawning location that allows a
successful completion of their entire pelagic embryonic and
postembryonic development.
Adult and larval physiology
Fish may be constrained in the location of spawning sites by their
physiology, especially during early life-history stages and adult maturing stages. For example, the Thunnini tribe (all tunas) includes
five genera and 15 species with a clear gradient of morphological
adaptations. The most primitive genera (e.g. Auxis, Katsuwonus)
are confined to tropical waters while the most evolved genus
(Thunnus) can occupy temperate environments (Collette et al.,
2001). However, to spawn, all tuna species return to tropical or subtropical locations, which are typically oligotrophic and warm (Sund
et al., 1981; Reglero et al., 2014). Schaefer (2001) hypothesized that
tuna spawning is constrained by the larval development, which is
very short compared with temperate species. This hypothesis adds
an evolutionary perspective to the choice of spawning location
because it implies that in tuna the choice of spawning habitat is
not unbounded, but constrained by the need to quickly move
across developmental phases. Two such spawning locations for
the North Atlantic bluefin tuna (Thunnus thynnus) are in the
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Mediterranean Sea and in the Gulf of Mexico (Muhling et al., 2013).
In the Pacific Ocean, bluefin tuna (Thunnus orientalis) only spawn in
the western boundary region, which is warmer than the eastern
boundary (Sund et al., 1981). It is interesting that all members of
the Scombridae family have an exceptionally fast development of
the digestive and visual sensory systems (Tanaka et al., 1996;
Morote et al., 2008), developmental traits that allow them a fast
track toward piscivory. To complete their fast development
bluefin tuna larvae may therefore be constrained to the warm
waters of the Mediterranean and Gulf of Mexico.
In addition to larval development and physiology, fish species
may be constrained in the location of their spawning grounds by
the development of adult gonads. For example, Atlantic bluefin
tuna has very high fecundity (90 oocytes per gram) and asynchronous ovarian development, whereby all different stages of
oocyte maturation are found at any given time in the ovary
(Medina et al., 2002). Coupled to this gonad development strategy,
bluefin tuna are multiple batch spawners, with each batch separated
on average by 1.2 days. Once they enter the spawning grounds of
the western Mediterranean, bluefin tuna have undeveloped ovaries,
but within a few weeks the ovary increases fourfold in mass
(Medina et al., 2002; Abascal and Medina, 2005). Such prodigiously
fast ovarian development and oocyte maturation may be constrained
by the presence of warm water, which poses an evolutionary constraint on the spawning locale of the adult tunas. Subarctic species
may be equally constrained by adult physiology, for example by
being more dependent on seasonal warming events and light conditions, leading to a shortened spawning season.
Population social structure
To successfully breed, individuals of the opposite sex must first encounter each other. This need is probably most acute in nonschooling, rare or low abundance fish species. A classic example of a
reproductive strategy developed as a result of constraints on mate
encounters is that of the deep-sea anglerfish (family Ceratidae).
Here, the male has exceptionally developed olfactory systems that
enable him to sense the female in complete darkness from long distances. Once encountered, the male permanently attaches itself to
the female, and effectually becomes a traveling gonad, providing
gametes to the mate, in turn receiving nourishment from her—a
strategy known as sexual parasitism (Pietsch, 2005). The deep-sea
anglerfish example illustrates two effective strategies to facilitate
mate encounter, namely permanent proximity to the mate and
highly capable sensory systems. Fish that adopt either or both of
these strategies may not necessarily be constrained to a specific
geographic location to mate, but would still depend on a suite of
favourable environmental conditions.
School formation in pelagic fish is typically considered an antipredation (Pitcher, 1986) or a navigational (Couzin et al., 2005)
strategy, but it also has the clear advantage of favouring mate
encounters. Thus fish that travel in schools may not be limited by
converging all in one place at the same time during the breeding
season (Rose, 1993). At the opposite extreme, fish that have a
simpler social structure and travel solitarily have to either develop
a strong sensory system allowing for distant mate recognition (e.g.
eels, Huertas et al., 2008) and/or have strong spawning-site fidelity
to facilitate mate encounters. In this last instance, one would hypothesize that cuing the spawning time and location only to environmental features, may not be a winning strategy, as different fish
may have different perceptions of the labile environmental cue.
For these fish, the better option may be to converge in very
L. Ciannelli et al.
well-established geographic regions and within a brief temporal
window. Fish species that conform to this strategy (e.g. anadromous
salmonids) are expected to have strong navigational abilities
(Putman et al., 2014), innate homing behaviour, and their spawning
areas are likely to be less sensitive to environmental variation.
Ecological processes
Ecological constraints are linked to the present and local environment and affect the population ability to adapt their spawning
habitats to interannual environmental variations without changing
their genotype (i.e. phenotypic plasticity, Table 1). Here we describe
in greater detail the ecological processes that modulate the strengths
of these constraints and provide evidence, from the published
literature, on how they affect population’s spawning distribution.
Spatial closure of life cycle
Unlike many benthic invertebrates, fish have to spatially connect
among potentially distant habitats during ontogeny. Because most
fish have spawning-site fidelity (natal or repeated homing), strategies for life-cycle closures must be robust against interannual variations of egg and larval dispersal. Robust strategies for life cycle
closure can be grouped in three categories: (i) local retention
and self-recruitment in the parental habitat and population;
(ii) passive dispersal toward distant settlement locations, with
countranatant adult migrations to return to the natal site; and
(iii) a combination of the previous two, involving passive dispersal
from and back to the natal site at the settlement stage.
The first spawning strategy is common among tropical and
subtropical fish (Jones et al., 2005; Cowen et al., 2006; Almany
et al., 2007; Planes et al., 2009) but with increasing evidence also in
species residing in temperate and Subarctic systems (Miller and
Shanks, 2004; Ciannelli et al., 2010). Fish species that conform to
this strategy typically place their eggs in geographically fixed locations,
such as banks, fjords, and coastal lagoons, which are associated with
strong potential for water retention (Iles and Sinclair, 1982). This was
in fact the premise of the “member-vagrant” hypothesis, proposed by
Sinclair (1998), which links recruitment variability with advective
losses during the dispersal phase. Atlantic herring was the poster
child of this hypothesis. On both sides of the Atlantic, their spawning
sites co-occur with retention areas, such as those originated by tidally
driven fronts (Iles and Sinclair, 1982). However, several more recent
studies have shown that Atlantic herring has a diverse genetic structure (Bekkevold et al., 2005; Gaggiotti et al., 2009) and array of
life-history strategies (Haegele and Schweigert, 1985; Geffen, 2009),
some of which include long-distance dispersal between nursery and
spawning grounds (Hamre, 1990; Huse et al., 2010).
Fish that are adapted to long and geographically extensive early
drift pathways—the second strategy for life cycle closure—take advantage of spatially and temporally consistent circulation patterns
through which eggs and larvae reach distant settlement areas.
Common circulation patterns targeted by spawning adults are
coastal currents (e.g. walleye pollock in the Gulf of Alaska, Kendall
et al., 1996), slope currents (e.g. slope-spawning flatfish, Bailey
et al., 2008; Sohn et al., 2010), surface branches of subtropical
gyres (e.g. eels, Schabetsberger et al., 2013), or undercurrents (e.g.
Pacific hake, Bailey and Francis, 1985). It is expected that the
homing strategy in these fish include a combination of geographical
clues, allowing adult fish to reach specific regions, and environmental signals to narrow down on the circulation feature. For example,
adult individuals of the Barents Sea cod stock migrate to the
Vestfjorden near the Lofoten Islands along the west coast of
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Fish spawning habitats
Norway to spawn (Sundby and Nakken, 2008), but once there, they
select their spawning site based on local temperature and salinity
cues, that orient them within the Norwegian Coastal Current
(Ellersten et al., 1989).
The third strategy for closing the life cycle involves long-distance
bidirectional dispersal of eggs and larvae, first away then back into
the natal habitat and parental population. This strategy is frequent
in eastern boundary systems, in which advective loss of eggs and
larvae during their dispersal phase can be a strong selection pressure.
For example, in the California Current system (northeast Pacific), fish
spawning strategies appear well tuned with variations of circulation
patterns along an inshore–offshore gradient (Parish et al., 1981;
Shanks and Eckert, 2005). In offshore habitats, which are characterized by seasonally varying alongshore currents, fish species are
mostly live-bearing (e.g. Sebastes spp.) and pelagic broadcast spawners (e.g. slope-dwelling flatfish species), with a relatively long
pelagic larval duration, spanning over at least two contrasting oceanographic seasons. These species typically release their larvae or eggs
during winter, after which eggs are transported northward through
the inshore countercurrent (Shanks and Eckert, 2005) and inshore
by downwelling-favourable winds (Parish et al., 1981). At the onset
of spring and summer upwelling-favourable winds, larvae are transported southward through the California Current and, by residing
deeper in the water column, can reduce offshore transport. The
long-pelagic larval duration and bidirectional drift allow late-stage
larvae to settle in the proximity of their natal or adult habitat, even
after extensive pelagic dispersal (Strathmann et al., 2002).
Houde, 1989) and consequently constrains the spatial extent
and distribution of fish spawning habitats. However, feeding and
predation are hard to disentangle because these two mechanisms
are typically directly linked: good feeding areas have also greater
risk of predation. For bluefin tuna in the North Atlantic, tuna
spawning is limited to the Gulf of Mexico and Mediterranean Sea
(Muhling et al., 2013). Bakun (2013) suggests that these areas are
selected because of lower predation risk, rather than good feeding
grounds for developing larvae. On the other hand, faster growth
as a function of a more productive environment is related to less exposure to predation by shortening the duration of vulnerable stages
(Houde, 2008). There are competing ideas whether the decreased
mortality is related to a physiological advantage due to a process
of size-selective predation, whereby smaller fish are more vulnerable
to predation (Leggett and Deblois, 1994).
Settlement
Reaching favourable settlement grounds can constrain fish spawning habitats, particularly in species that have highly specialized
habitat requirements during the postsettlement phase. Flatfish are
Predation/starvation
Much has already been written about the importance of larval fish
feeding on their survival (see Houde, 2008 for a general review),
and on the biophysical processes that affect larval feeding (e.g.
MacKenzie et al., 1994; MacKenzie and Kjorboe, 2000).
Surprisingly however, there is less research devoted to understanding whether larval feeding can pose selective pressure on the choice
of spawning habitat. A notable exception is that of Bakun (2009) for
the “ocean triads” hypothesis. Namely, good reproductive areas
require enrichment, concentration, and retention processes.
Enrichment, for example via upwelling, fuels primary and secondary production, in turn providing food biomass for developing
larvae. Concentration mechanisms densely package food particles
(i.e. patches or layers) so that the within-patch prey density is
high enough to satisfy the larval feeding requirements. In the
ocean, concentration mechanisms are common around mesoscale
fronts, eddies and upwelling jets (Bakun, 2006), persistent thin
layers (Cowles et al., 1998), or following periods of relatively calm
conditions (Lasker, 1975). Finally, retention within (or drift
toward) appropriate nursery habitats is necessary to deliver latestage larvae to their next phase of life. The spatial co-occurrence
of these three processes considerably constrains the availability of
spawning habitats. In the California Current system for example,
many of the coastal fish species spawn in the California Bight or
Baja California regions, both of which provide the required enrichment (via upwelling), concentration (via relaxation events), and retention features of the triads hypothesis (Bakun and Parish, 1982).
Similar mechanisms have been proposed also for the spawning of
European anchovy in the Mediterranean (Agostini and Bakun,
2002) and in the Bay of Biscay (Bellier et al., 2007; Planque et al.,
2007).
Predation on adult stages (Claydon, 2004) and on fish eggs and
larvae can also affect their survival and recruitment (Bailey and
Figure 2. Plasticity and adaptability of spawning sites. Within a range
of environmental variability (realized niche) phenotypic plasticity is the
mechanism through which a fish population can change its spawning
distribution (occupied habitat) without genetic adaptation. This is
depicted by the population reaction norm (grey line)—a
population-level characteristic with the vertical range measuring the
total plasticity in spawning-site selection. The grey arrows depict
ecological constraints on the reaction norm. To achieve greater changes
of spawning distribution (potential habitat) or to respond to stronger
environmental signals (potential niche) species have to adapt.
Evolutionary constraints, inherent of the species evolutionary history,
limit the degree of such adaptations. The spawning envelope around
each reaction norm is a species-level characteristic emerging from
population-level reaction norms and depicts the adaptability of
spawning sites. The black arrows depict the evolutionary constraint on
the species’ spawning envelope. The placement and direction of the
black and grey arrows are not intended to imply the direction of the
constraint (vertical vs. horizontal) but rather the type of constraint
(ecological vs. evolutionary). See also Table 1 for a definition of
ecological and evolutionary constraints and factors that modulate their
intensity.
290
a good example in that regard (Duffy-Anderson et al., 2014). They
typically have extensive dispersal phase, during which the larvae
undergo radical morphological (e.g. asymmetry, eye migration,
cranial bones, and pigmentation) and behavioural (e.g. swimming
posture) changes (Schreiber, 2013). Such changes facilitate ecological transitions and allow individuals to inhabit a variety of habitats during their ontogeny (McMenamin and Parichy, 2013), but
they also constrain their distribution and the timing of arrival to
these habitats. The recruitment level of these flatfish is often
limited by the amount of available habitat (Rijnsdorp et al., 1992).
Plasticity and adaptations
Many fish populations are known to change their spawning distribution from 1 year to another in relation to environmental
changes (e.g. Bailey and Francis, 1985), a process that we refer to
as spawning plasticity. However, as we discuss in our review, there
is an ecological limit to such plasticity imposed by predation risk,
aberrant dispersal, or poor feeding conditions. To overcome these
limits, fish have to evolve and therefore change their genotypic distributions, a process that we refer to as spawning adaptability. In this
L. Ciannelli et al.
section, we review plasticity and adaptability of fish spawning habitats and propose a conceptual model to quantify both.
We apply the concept of reaction norms for understanding how
ecological and evolutionary constraints act on fish spawning habitat
selection (Figure 2). Reaction norms represent a way of visualizing
phenotypic plasticity, that is, what phenotype is expressed by a genotype over a range of environmental conditions. In general, plastic
changes are expected to shift the phenotype along the reaction
norm while evolutionary changes will shift the shape or position of
the underlying reaction norm itself (Hutchings, 2011). Dobzhansky
(1937) was one of the first to point out that what is inherited is not
specific traits, but rather a norm of reaction to environmental conditions. Since then, reaction norms have become a valuable tool in evolutionary ecology because they potentially allow for distinguishing
between phenotypic plasticity and evolution (Hutchings, 2011).
In this framework, ecological and evolutionary constraints
would define the boundary conditions of the reaction norm.
Specifically, ecological constraints set the outer limits for plastic
changes, while evolutionary constraints limit the shape and position of the reaction norm, that is, how it may potentially evolve
(Figure 2). We see the reaction norm as a population-level
Figure 3. Constraints acting on spawning-site selection in fish. Four scenarios are hypothesized: (a) low ecological constraint and low evolutionary
constraint, typical of small pelagics; (b) low ecological constraint and high evolutionary constraint, typical of large pelagics, such as bluefin tuna;
(c) high ecological constraint and low evolutionary constraint, typical of gadids and herring; and (d) high ecological constraint and high
evolutionary constraint, typical of slope-spawning species such as rockfish and large-bodied flatfish. The colour of the arrows indicates the nature of
the constraint (grey for ecological and black for evolutionary) while the thickness indicates the intensity of the constraint.
Fish spawning habitats
characteristic. Its vertical range is a measure of total plasticity in
spawning-site selection. The variability around each reaction
norm defines the spawning envelope. This is a species-level characteristic emerging from population-level reaction norms.
The proposed framework allows us to group marine fish species in
four categories with respect to spawning-site selection: (A) low ecological constraint and low evolutionary constraint, (B) low ecological
constraint and high evolutionary constraint, (C) high ecological constraint and low evolutionary constraint, and (D) high ecological
291
constraint and high evolutionary constraint (Figure 3). Fish with
high spawning plasticity (Groups A and B) are not geographically
constrained to a spawning area or to a nursery habitat. Rather they
select reproductive locations based on environmental cues and thus
have the potential to follow environmental gradients. For example,
Pacific sardine (Sardinops sagax) in the southern California current
system shows a high degree of spawning flexibility, which is related
to variations from the El Niño to La Niña conditions and water temperature (Figure 4; Weber and McClatchie, 2010; Song et al., 2012).
Figure 4. Variations of the annual centre of distribution for Pacific sardine eggs in the southern California region, in relation to water temperature
(upper panels) and December– January Multivariate ENSO Index (MEI, http://www.esrl.noaa.gov/psd/enso/mei/), lower panels. Solid and open
circles indicate values above and below the median, for temperature, or zero for MEI. Sardine egg data are from California Cooperative Oceanic
Fisheries Investigations (CalCOFI) and include only oblique tows from February to April. The polygon on the map shows the data range. Temporal
coverage goes from 1951 to 2011, however, years with uneven sampling coverage within the examined region and time frame were excluded from
the analysis. Temperature records are from CalCOFI hydrographic collections for the same years and months included in the egg data. Only
temperature records from 0 to 20 m are considered. There is a significant relationship between the latitude of the spawning centre and water
temperature (linear regression, p ¼ 0.008, R 2 ¼ 0.265) and MEI (linear regression, p ¼ 0.003, R 2 ¼ 0.331).
292
Several other small pelagic species in the eastern Bay of Biscay (Bellier
et al., 2007; Planque et al., 2007) and in the Benguella system (Kreiner
et al., 2011) display similar degrees of environmental flexibility in
their reproductive locale. In contrast, fish species that spawn in geographically constrained areas (e.g. canyons, fjords, and submerged
banks) and whose survival during early life-history stages depends
on long dispersal pathways to advect eggs and larvae to suitable juvenile nursery areas are expected to have a limited degree of spawning
plasticity (Groups C and D in Figure 3). Large-bodied, slopespawning flatfish, for example, fall into this latter group of fish,
having long larval drift pathways and geographically constrained
spawning and nursery habitats (Bailey et al., 2008; Sohn et al., 2010).
The spawning envelope, linked to the level of among-population
variation in spawning-site selection could serve as an indicator of
the level of evolutionary constraints, assuming that some of this variation has a genetic basis (i.e. representing local adaptations). For
example, single populations of Atlantic herring have limited plasticity
because they have demersal eggs and are dependent on landscape
and vegetation for the survival of the eggs (Figure 5, Petitgas et al.,
2012). At a species level, however, herring exhibit a large variety of
life-history strategies (Figure 5, Geffen, 2009). There is in fact an
L. Ciannelli et al.
Atlantic herring population spawning in every month of the year,
and over a wide range of salinity (Gaggiotti et al., 2009) and temperature (Oeberst et al., 2009). Similarly, walleye pollock in the Shelikof
Strait region of the Gulf of Alaska has very limited interannual spawning flexibility, regardless of transport or other environmental conditions within the region (Figure 6, Ciannelli et al., 2007; Bacheler et al.,
2009). As a species however, walleye pollock spawn in environmentally contrasting habitats, spanning from the Puget Sound in the
northeastern Pacific to Japan in the northwestern Pacific (Bailey
et al., 1999). Both of these examples conform to the third strategy
(Figure 3c), having high scope for genetic adaptability but limited
scope for phenotypic plasticity. Atlantic cod also fits in this category,
having a high scope for local adaptations (Knutsen et al., 2003; Olsen
et al., 2008, 2009). Bluefin tuna on the other hand has high plasticity
of spawning site, which is environmentally selected (Reglero et al.,
2012), but limited scope for adaptations at a taxon level. As a
species, Atlantic bluefin tuna spawning only occurs in two basins,
the Mediterranean and the Gulf of Mexico. Within each basin, tuna
can have finer genetic and population structure (Carlsson et al.,
2004; Riccioni et al., 2010) but across basins there is a striking
similarity of the environmental requirements for spawning
Figure 5. Variations of the annual centre of distribution for Atlantic herring small larvae (,9 mm SL) in the Western North Sea region, in relation
to water temperature. Solid and open symbols are above and below the median temperature value, respectively. Herring larval data are from ICES
ichthyoplankton collections (http://www.ices.dk/marine-data/data-portals/Pages/Eggs-and-larvae.aspx) from 1976 to 1990, during which the
sampling areas were most consistently covered, and from August to November—the period of intense spawning activity. Solid horizontal lines
separate the four spawning groups, from the North: Shetland (squares), Buchan (circles), and Banks, further divided between North (triangles) and
South (diamonds). Temperature values are from ICES hydrographic collections (http://www.ices.dk/marine-data/data-portals/Pages/ocean
.aspx), including data records shallower than 10 m, and for the same years, months, and spatial extent covered by the egg data. There is not a
significant relationship between the latitude and longitude of the spawning centre and water temperature.
Fish spawning habitats
293
Figure 6. Variations of the annual centre of distribution for walleye pollock eggs in the Western Gulf of Alaska, in relation to water temperature.
Solid and open circles are above and below the median temperature, respectively. Pollock egg data are from NOAA Fisheries Oceanographic
Coordinated Investigations and include only oblique tows from March to May—the period of intense spawning activity. The polygon on the map
shows the data range. Temporal coverage goes from 1981 to 2010, however, years with uneven sampling coverage within the examined region and
time frame were excluded from the analysis. Temperature values are surface records collected during the NOAA Midwater Assessment and
Conservation Engineering surveys for the same years, spatial extent, and months included in the egg data. There is not a significant relationship
between the latitude and longitude of the spawning centre and water temperature.
(Muhling et al., 2013), indicating an overall reduced diversity of
species spawning strategies and high evolutionary constraint to the
choice of spawning habitats (Figure 3b).
Conclusions
Fisheries oceanographers are well aware of the ecological constraints
on fish spawning habitats. Several studies have in fact demonstrated
that fish spawning distribution is tightly linked to the local and contemporary environment at relatively small scales (e.g. Bailey et al.,
2005; Bakun, 2006; Ciannelli et al., 2010). However, the notion
that evolutionary constraints can also affect distribution is less pervasive in studies that focus on fish spawning, although evolutionary
constraints are well accepted within other ecological disciplines
(Arnold, 1992; Schwenk, 1995; Futuyma, 2010). Much research
has been recently aimed at understanding how fish will adapt to incumbent changes in the Earth’s physical and biological systems
(Planque et al., 2011). Results from modelling projections have
also fuelled debate in the scientific community, centred mostly on
accuracy and precisions of such forecast (e.g. Brander et al., 2013;
Cheung et al., 2013). Here we refer to uncertainty of species’ projections based on the evolutionary constraints of spawning habitats,
and provide means to quantify it through the use of reaction
norms and spawning envelopes. Spawning location is the anchor
of a fish’s spatial distribution, and will therefore affect the degree
to which species can respond to environmental variability by changing their habitats. Projections of species’ distributions based on
retrospective analysis of habitat features (Cheung et al., 2010;
Pinsky et al., 2013) capture the effect of ecological constraints on
294
fish habitat selection but fail to include evolutionary processes. Our
conceptual review illustrates that there is an upper limit to the degree
to which fish can adjust and adapt to these changes, particularly for
species that have high ecological and evolutionary constraints.
Knowledge about these boundary responses is therefore valuable
for predicting the impact of future environmental change, such as
ocean warming.
Acknowledgements
We are grateful to Sam McClatchie and Norbert Rohlf for providing
data and insight for the analysis of the CalCOFI sardine egg data, and
the North Sea herring larval data, respectively. We are grateful to
Chris Wilson, Neal Williamson, and Annette Dogherty for providing the temperature data from the western Gulf of Alaska region.
Two anonymous reviewers and the editor provided valuable feedback. We acknowledge support from the NSF SEES Research
Coordination Network, Grant 1140207 “Sustainability of Marine
Renewable Resources in Subarctic Systems Under Incumbent
Environmental Variability and Human Exploitation.”
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Handling editor: Mikko Heino