# Parental Effects and Reproductive Potential of Fish and Marine Invertebrates: Cross-Generational Impact of Environmental Experiences

Rosario Domínguez-Petit, Cristina Garcia Fernandez, Ezequiel Leonarduzzi, Karina Rodrigues, Gustavo Javier Macchi

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Rosario Domínguez-Petit, Cristina Garcia Fernandez, Ezequiel Leonarduzzi, Karina Rodrigues, Gustavo Javier Macchi. Parental Effects and Reproductive Potential of Fish and Marine Invertebrates: Cross-Generational Impact of Environmental Experiences. Fishes, 2022, 7 (4), 188 (16p.). 10.3390/fishes7040188. [https://doi.org/10.3390/fishes7040188](https://doi.org/10.3390/fishes7040188)

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# Parental Effects and Reproductive Potential of Fish and Marine Invertebrates: Cross-Generational Impact of Environmental Experiences

Rosario Domínguez-Petit <fnref n="1" />,* , Cristina García-Fernández <fnref n="2" />, Ezequiel Leonarduzzi <fnref n="3" />, Karina Rodrigues <fnref n="3" />,<fnref n="4" />
and Gustavo Javier Macchi <fnref n="3" />,<fnref n="4" />

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**Citation:** Domínguez-Petit, R.; García-Fernández, C.; Leonarduzzi, E.; Rodrigues, K.; Macchi, G.J. Parental Effects and Reproductive Potential of Fish and Marine Invertebrates: Cross-Generational Impact of Environmental Experiences. *Fishes* **2022**, *7*, 188. https://doi.org/10.3390/fishes7040188

Academic Editor: Azadeh Hafef

Received: 31 May 2022

Accepted: 23 July 2022

Published: 27 July 2022

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**Copyright:** © 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

**Abstract:** The reproductive success of aquatic animals depends on a complex web of relationships between the environment, the attributes of the reproductive individuals and human-induced selection. All of them are manifested directly or indirectly through parental effects, which can also compensate for certain external impacts. Parental effects refer to the influence that the phenotype and environmental conditions in which individuals develop exert on the phenotype of their offspring, and they can even have transgenerational impact. This paper describes the different types of parental effects and reviews the published literature to analyze the causes of their variation and their impact on reproductive resilience and population dynamics.

**Keywords:** reproductive potential; reproductive success; population dynamics; maternal effects; paternal effects

## 1. Introduction

During the 20th century, studies of fish population dynamics were based on the erroneous assumption that all individuals in a population have the same productivity [1]. In 1999, the term reproductive potential was coined to define the ability of a population to produce viable offspring that become recruited to the fishery [2]. This capacity depends on the parental characteristics (length, age, condition, etc.); therefore, the reproductive potential of a stock (SRP) is not proportional to the spawning stock biomass. The parameters mostly used to measure the SRP are fecundity, number of spawning, size and quality of eggs and larvae, and the time and duration of the spawning season, among others [3]. Parental effects refer to the influence that the phenotype and environmental conditions in which individuals develop exert on the phenotype of their offspring. The phenotype of an individual would not only be determined by its own genotype (inherited from its parents) and the environment in which it develops, but also by the phenotype and environmental experience of its parents [4]. An example of a parental effect would be the influence of the condition of reproductive females on larval size, which would reflect how the environment experienced by the mother (food availability) affects offspring characteristics (larval length) [5].

To date, the study of parental effects in aquatic animals has been dominated by research on maternal effects (i.e., derived from females), considering that the role of males was limited to gene transmission; and therefore, any paternal influence on offspring would derive exclusively to genotypic aspects [6,7] or fertilization success [8]. However, an increasing number of studies demonstrate the existence of paternal effects in aquatic

<footnote n="1">1 Centro Oceanográfico de Vigo (IEO-CSIC), 36390 Vigo, Spain</footnote>

<footnote n="2">2 Ifremer, University Brest, CNRS, IRD, LEMAR, F-29280 Plouzané, France; cristina.garcia.fernandez@ifremer.fr</footnote>

<footnote n="3">3 Instituto Nacional de Investigación y Desarrollo Pesquero (INIDEP), Mar del Plata 7600, Argentina; eleonard@inidep.edu.ar (E.L.); krodrigues@inidep.edu.ar (K.R.); gmacchi@inidep.edu.ar (G.J.M.)</footnote>

<footnote n="4">4 Instituto de Investigaciones Marinas y Costeras (IIMyC-CONICET), Mar del Plata 7600, Argentina</footnote>

<footnote>* Correspondence: rosario.dominguez@ieo.csic.es</footnote>
organisms, ranging from the direct influence of paternal attributes on offspring quality [9,10] or from the influence of parental behavior [11] on offspring survival, to the impact of the environment on male reproductive success [12–14]. Recent evidence shows that epigenetic factors transferred in the sperm to offspring, such as non-coding RNAs, DNA methylation or chromatin structure, also affect gene expression in developing embryos [15].

However, parental effects can have much more complex dynamics, with interactions between maternal and paternal effects. In this sense, Siddique et al. [16] demonstrated that different family combinations have an important impact on fish embryonic development. Lymbery and colleagues [17] reported how egg chemical fluids interact with sperm to define fertilization rate and offspring variability in blue mussel (*Mytilus galloprovincialis*). Even more, life strategy can be an additional source of complexity (see Section 3). For example, in some syngnathid species, such as *Syngnathus fucus*, nutrient transfer from the father to the offspring during the period of offspring care has been demonstrated, and such transfer could compensate for nutritional deficiencies of the eggs derived from a reduced maternal energetic investment [18]. Furthermore, in aquatic animals, the weight of maternal over paternal effects on offspring phenotype may be related to environmental stability [19]. In summary, the phenotype of the offspring is the result, not only of the interaction of its own genotype with the surrounding environment, but also of a complex web of relationships between the environment, genotype and phenotype of both parents.

Parental effects are not necessarily positive or adaptive; examples of negative effects would be pollutant transmission during embryonic development [20] or inappropriate site [21] or timing [22] of spawning.

Parental effects can result from: (i) the genetic or phenotypic characteristics of the parents, for example when larger females produce larger offspring [23], which is known as *parental inheritance or indirect genetic effects*, (ii) the parental behavior, for example the impact of parental care on offspring survival [24], which is known as *parental selection*, or (iii) the environment experienced by the parents, as in the case of ingested pollutants that are transmitted to the embryos, affecting their development used as an example above, which is known as *indirect environmental effects* [1,2].

Depending on the offspring life stage at which the parental effect occurs, they can be classified as: (i) *prezygotic* (the effect is on the characteristics of gametes and, therefore, is prior to fertilization), (ii) *prenatal postzygotic* (the effect is on embryonic development, both in fetuses and eggs) or (iii) *postnatal postzygotic* (the effect is on larvae and juveniles).

The existence of parental effects has a great influence on population dynamics. There are studies reporting that parental effects propagate through several generations [19,25,26]. Furthermore, they can play an important role in the evolutionary dynamics of a population, since selection for certain traits would no longer be determined exclusively by the genotype and phenotype of individuals, but also by the phenotype of preceding generations, i.e., parental effects can have a substantial impact on the rate and direction of genetic change in response to selection [27]. This issue is of particular relevance in the context of global change, as intergenerational parental effects can enhance rapid transgenerational responses to changing environments [28]. Parental exposure to a particular environment or stress has been shown to modify the phenotype of offspring to adapt to that environment; if the conditions in which the parents lived and reproduced are different from those experienced by their offspring, the offspring would be unable to adapt to the new conditions [11,29].

There are several papers that review in depth the mechanisms and implications of parental effects in general [4,30]. Regarding paternal effects, Curley et al. [31] and Rando [32] provide a review of some of the molecular mechanisms underlying such effects in animals, while Crean and Bonduriansky [33] describe the different types of paternal effects and their interactions with maternal effects.

## 2. Parental Effects and Population Dynamics

Parental effects and reproductive potential are key elements in the stock recruit-ment process and, therefore, for its dynamics. In the early larval stages, there is a high
themselves [64]. Moreover, in some freshwater species, paternal effects on embryonic stages can outweigh maternal effects [16]. Although studies focusing on paternal effects on recruitment are scarce, research on male reproductive potential and its influence on offspring fitness indicates that the impact of paternal effects on population dynamics is greater than previously considered.

Another important aspect that impacts on larval survival and recruitment and is influenced by the demographic structure of the stock is the location of spawning areas [65,66]. The spawning area is also the larval habitat; thus, choosing spawning areas with optimal environmental conditions will favor larval survival and recruitment [67]. Spawning spatial patterns vary depending on the size and age of the spawners as well, with larger females being located in optimal zones [68,69]. The effect of age on breeding site location is clearly established in the *entrainment hypothesis* developed by Petitgas et al. [70] based on observations of migratory fish. According to this hypothesis, repeat (older) females are responsible for maintaining migratory routes to spawning grounds. In these species, individuals spawn in the area where they first spawned, and after, adult individuals mix with juveniles in the feeding grounds. In the following reproductive season, the multiparous adults "entrain" the primiparous individuals to the areas where they have already spawned successfully. Once these primiparous individuals have spawn in a particular location, they will always return to the same site. This behavior means that changes in age structure of the population or environmental conditions of the spawning area impact the reproductive success of the stock. In the case of North Sea flounder, overexploitation depleted the larger and more experienced individuals to such an extent that the reproductive migration routes changed because there were no individuals able to guide the rest to the traditional spawning grounds [70].

Quantifying the direct impact of parental effects on annual recruitment is difficult, as great uncertainty is associated with the larval stage, where mortality due to environmental causes is high. However, recruitment has been shown to be positively correlated with the proportion of old females in several species, both in marine and freshwater vertebrates [71,72], as well as invertebrates [73]. However, beyond recruitment, it is necessary to take into account that parental effects can propagate over several generations [74–76]. The issue is that in the case of a sparse offspring in poor conditions producing a second generation with reduced reproductive potential, parental effects would have a deeper and more prolonged impact on stock dynamics than expected a priori, based on the traditional stock-recruitment relationship.

### 3. Influence of Life Strategies on Parental Effects

The degree of impact that parental effects have on population dynamics is defined by how individuals experience and respond to different environmental factors. This response is mediated in part by specific physiological mechanisms, which in turn are intimately linked to their life (range of strategies between K and r), energetic (growth vs. reproduction, capital and income breeders, sexual dimorphism, etc.) and reproductive strategies (oviparity vs. viviparity, polyandry, etc.), as well as their behavior (reproductive migrations, mating system, courtship, offspring care, etc.). Therefore, the type of parental effects (*parental inheritance*, *parental selection* or *indirect environmental effects*) and the time at which they exert their influence (*prezygotic*, *prenatal*- or *postnatal-postzygotic*) are intimately related to the life strategy and tactic of each population.

According to the *Life History Theory* (LHT), K-strategists are defined as species that invest more in the care of offspring than in numbers, as opposed to r-strategists, with a continuum of intermediate strategies between the two extremes [77]. In general, it is assumed that species in fluctuating and unpredictable environments tend to an r-type strategy, and to the K-type when living in stable environments [78]. In this sense, it is expected that parental selection (resulting from the behavior of the parents) and *postnatal postzygotic effects* (influencing larvae and juveniles) be more common in K-type species, due to the special investment they make in the care of the offspring. Benefits of parental care on
offspring fitness and survival have been documented in several studies [79,80], although
no significant effects are relatively common at least in fish [24].

Conversely, in capital breeder species, i.e., those that accumulate reserves for repro-
duction in advance of the spawning season onset, the *indirect environmental effects* will be
delayed with respect to the time of spawning. By contrast, in income breeder species, the
influence of these effects will be simultaneous, since the energy acquired through feeding
is used in reproduction almost immediately [81].

In the case of species with internal fertilization, courtship systems or offspring care, mate selection undoubtedly has a profound impact on the characteristics of the offspring, and this selection can be influenced by the environment. A clear example of this type of interaction is the common goby (*Pomatoschistus microps*), a species in which the male uses the noises emitted by the swim bladder to attract the female (Ref. [13] and references therein). When males of this species form nests in areas of high noise pollution, their probability of successful mating decreases, as females evaluate the suitability of males based on the sounds they emit [13]. Thus, males with the same characteristics (size, vocal ability, etc.) will have lower reproductive success in noisy areas.

In aquatic ecosystems, polygynyandry (males and females have multiple mating partners along the breeding season) is the most extended reproductive strategy in species, especially in those with external fertilization, but not the only one. However, having multiple mating partners during a breeding season influences their descendants' fitness, as it increases the chances of mating with a compatible partner, promotes sperm competition, and enhances genetic diversity [82]. For example, high sire diversity increases larval growth rate of the gastropod *Crepidula fornicata* [83], and the fertilization and hatching rates in the polychaete *Galeolaria caespitosa* [84]. In that sense, it is expected that greater genetic diversity will lead not only to an increase in the survival of the offspring, but also to a greater adaptive capacity of the offspring to environmental changes (see Section 5). Interspecific regulation of parental effects have been documented as well in parasite–host systems. Parental effects of parasites are largely determined by the choice of host, and at the same time, the parasite itself modulates the host’s parental effects on its offspring. [30]. This could have profound implications for parasite–host co-evolution and sympatric speciation processes. Although no such studies have been found in aquatic animals, similar interactions should be expected. Similarly, predator stress can also modulate parental effects, altering the mating behavior of descendants [28].

With respect to reproductive strategy at the population level, those species that have a
synchronized spawning season over a relatively short period of time (the entire population
reproduces in one or two months), will be less resilient to external changes than those
that have a prolonged reproductive season or several annual spawning peaks, as the
offspring are usually adapted to the environmental conditions to which their parents are
exposed [11,29]. Therefore, their progeny will have a lower adaptive capacity, reducing the
survival rate if the environment changes.

In conclusion, not only does the specific life strategy modulates parental effects, but
the interspecific interactions do as well, adding complexity to the mechanisms that regulate
the reproductive success of aquatic organisms.

4. Temporal and Geographic Variability of Parental Effects and Reproductive Potential

As mentioned above, environmental factors and parental effects coexist and modulate
the early life stages of aquatic organisms and are key in terms of recruitment variabil-
ity [85,86]. Since environmental and parental attributes vary spatially and geographically,
parental effects and their degree of impact on population dynamics will also vary. Such
spatio-temporal variability is evident in *indirect environmental effects*. For example, marked
seasonal fluctuations in temperature and productivity, characteristic of high latitudes, influ-
ence food availability and quality for both adult and juvenile fish [87,88]. Consequently,
the accumulation of energy reserves and the physiological condition of spawning indi-
viduals may show temporal variations in relation to natural production cycles [89]; thus,
years with good conditions during the feeding season will allow adult fish to enter the spawning season with high energy reserves. Conversely, the amount of energy devoted to reproduction—for example, linked to reproductive migrations or physiological changes related to courtship—varies according to individual metabolic expenditure [90], which responds to temperature and oxygen availability [91]. This energy balance between basal metabolism, energetic reserves, growth and reproduction will determine fecundity, egg quality [92,93], fertilization rate [94] and larval survival [95], even leading to no annual spawning when the condition of breeding females is low [50]. Therefore, temporal or spatial variations in temperature and oxygen will affect the quantity and quality of available food and the metabolic tradeoffs of spawners, causing spatio-temporal changes in conditions and, therefore, in reproductive success.

An example of the intra-annual or seasonal variability of parental effects can be found in European hake (*Merluccius merluccius*) in the Atlantic waters of the Iberian Peninsula. This species in this area presents three annual spawning peaks (winter-spring, summer and autumn) [96]. When analyzing the variability of maternal effects on the development of eggs and larvae in the three spawning peaks, it was observed that more and better quality eggs (larger diameter and dry weight) were produced in winter-spring than in the other spawning peaks [97]. For larvae, growth rates were similar regardless of hatching date, although those hatched in summer had more developed anterior body parts than those in winter-spring at the same age, which could also be associated with greater predatory capacity and, consequently, higher survival rate [97]. These authors propose that temporal differences in larval fitness and, hence, annual recruitment, are influenced by a combination of maternal attributes and environmental conditions. This suggests that the intensity of the impact of any stressor on the population dynamics of European hake in this area depends on the time of year it occurs. Another example of seasonal variability of maternal effects has been documented for some clupeiformes in which egg size decreases as the reproductive season progresses, which is related not only to variations in maternal energy reserves, but also to changes in the age structure of the spawning stock and changes in temperature that affect ovogenesis [98].

Inter-annual differences in parental effects have their origin in both dense-dependent and dense-independent factors. Among the most studied dense-dependent factors in fish are those related to growth and condition, the greater the abundance of individuals, the greater the intraspecific competition (less resources available), which causes a lower growth rate and poorer condition of individuals, with consequent effects on length and age at maturity, growth and reproductive potential [99,100]. However, there are other dense-dependent mechanisms that regulate parental effects, although they have been less studied. In some species that form reproductive aggregations, such as sea urchins of the genus *Strongylocentotus*, the rate of egg fertilization decreases with increasing distance between individuals or when the abundance of breeders (especially males) falls, mainly due to sperm dilution in the aquatic environment [101,102]. In the case of species with social mechanisms of reproductive control, such as the damselfish (*Pomacentrus amboinensis*) which forms reproductive pairs, an increase in the number of females in the breeding area, even when they do not have access to the reproductive partner, induces aggressive behavior of the spawning females, which increases cortisol levels (the stress hormone), causing a reduction in the size of the larvae produced by these females [37]. In other words, in years when the abundance of reproductive females decreases, the reproductive potential could increase.

Dense-independent factors driving inter-annual variation of parental effects have been especially studied in short-lived pelagic fishes, where environmental influence is much more pronounced. For example, in the Humboldt upwelling system of Peru, the reproductive success of anchoveta (*Engraulis ringens*) is high in years considered normal or during cold events of La Niña [103]. In the case of *Engraulis anchoita*, reproductive success is related not only to sea surface temperature, but also to the abundance of copepods, which is the main food of adults during the spawning season [104]. These types of environmental
variations can be particularly pronounced in highly changing ecosystems, such as coastal lagoons, such as the Laguna de Rocha (Uruguay). During 2010–2011, as a consequence of La Niña, the lagoon showed a drastic increase in salinity that caused an interruption of *Brevortia aurea* spawning during autumn and late maturation in spring [105], which probably affected egg and larval survival.

The observed geographic differences in reproductive patterns are linked to variable environmental conditions, which is considered strong evidence of intraspecific life history evolution in fishes [106]. In keeping with *Bergmann's rule*, which indicates an increase in body size toward higher latitudes, ectothermic organisms inhabiting relatively lower temperatures (characteristic of high latitudes) typically mature later and at larger sizes compared to conspecifics inhabiting higher temperatures [107]. The magnitude and direction of this variation is predicted by the *temperature–size rule*, whereby lower temperatures result in a lower initial growth rate and delayed maturation with larger body size [107]. Fernandez-Torres et al. [108] concluded that fish clearly follow such a pattern, with the largest species in temperate and cold regions. Furthermore, they observed a differential response of body size to the environment related to temperature, salinity and human impact, which in turn would affect reproductive potential and the ability to adapt to changing environments.

Therefore, it is to be expected that low temperatures and short reproductive seasons at high latitudes would result in low annual production. However, within a theoretical framework of compensation, organisms inhabiting high latitudes may develop compensatory responses to these climatic effects, such as higher egg production rates [109]. The rate of egg production can be increased by consuming and/or assimilating more energy or by varying the way in which assimilated energy is distributed among growth, reproduction and metabolism [110]. In some brachyuran crabs, latitudinal differences in embryo size have been reported, being larger at higher latitudes, probably related to the greater amount of yolk deposited in the egg [111]. In marine invertebrates inhabiting low latitudes, with high temperatures and low dissolved oxygen concentration, females support high energetic cost associated with the active ventilation of eggs to provide sufficient oxygen to the embryos and to maintain them at an optimal temperature [112]. The higher metabolic cost derived from the care of the offspring leads to a decrease in the energy available for reproduction, which is reflected in a low number of eggs [113]. In addition, the high intensity of active ventilation also produces mechanical loss of embryos. Both mechanisms provoke variations in the reproductive potential of these species as a function of latitude [113]. Similarly, latitudinal environmental changes cause differences in the conditions of the parents [114,115], to such an extent that Lloret et al. [93] propose using the condition of individuals as an indicator of habitat quality to identify optimal environments and design marine protected areas.

**5. Human-Induced Variability of Parental Effects and Reproductive Potential**

In addition to natural variability, there are changes in maternal effects that can be human induced, through selection for certain traits or behaviors that can affect the diversity and, ultimately, the resilience of populations. Industrial effluents, agricultural activities, urban waste, increases in urbanization and accidental spills are sources of pollutant-driven physiological stress for aquatic animals. The effect of noise pollution in the mating selection of the common goby (*Pomatoschistus microps*) and how similar males would have lower reproductive success in noisy areas [13] has already been mentioned. However, there is extensive research on how pollution impacts the reproduction of aquatic organisms in both fresh [116] and marine waters [117]. For example, endocrine disruptors affect sexual maturation, gamete production and transport, sexual behavior, fertility, and gestation by altering the integrity of the reproductive system of aquatic animals [118,119]. Microplastics reduce reproductive potential of some aquatic animals [120], while heavy metals such as mercury directly affect the reproductive system but also indirectly influence parental effects by provoking dysfunction of coordination, loss of appetite, osmoregulation, orient-
tation or prey location [121]; some contaminants even alter the reproductive behavior of these animals [122].

Contaminants not only affect the physiological processes of the spawners, but also those of the offspring; that is, the effect may be cross-generational. For example, Yin et al. [123] observed that parental Benzo[a]pyrene (BaP) exposure induced circadian rhythm disorder in offspring. Being that the larvae of exposed parents were more sensitive to BaP, paternal exposure to BaP produced more severe damage on offspring DNA than maternal exposure.

Fishing is also a mechanism for human-induced selection of parental attributes, as in many cases, it tends to target certain fractions of the population (large individuals, juveniles, spawning migrants, males, etc.). For example, the removal of individuals of greater length and age in the population, generated by fishing activity, can lead to a negative effect on the reproductive potential of the stocks, by reducing the number and quality of spawned eggs, which would reduce larval survival rates [124]. In some commercial invertebrates such as spider crab (Lithodes santolla), the fishery is based on the selective exploitation of males greater than 110 mm carapace length, a management measure that aims to protect females that carry the fertilized eggs [125]. However, despite prohibiting the commercialization of ovigerous females, during the last few years, there has been a significant decrease in population fecundity [126]. The two hypotheses that explain this phenomenon are that: the elimination of larger males, which produce more and better sperm, has reduced fertilization rates in the population; conversely, the capture and subsequent return to the sea of ovigerous females causes a loss of eggs due to the stress generated during this process [127]. As mentioned above, if selectivity is intense, it may even result in genetic and evolutionary changes in populations [128], which are difficult to reverse, leading to regime shifts that directly affect the resilience of the population and ecosystem [129]. Beyond the selective effect of fishing, the stress generated by the fishing operation itself can have negative effects on offspring development derived from the physiological response of females [130]. The changes generated by overfishing in the different reproductive traits of populations, which affect their renewal potential, are much more marked in species particularly vulnerable to exploitation, such as hermaphrodites [131], elasmobranchs [132] or deep-sea species [133]. In the case of hermaphrodite species, the magnitude of this effect could depend on the type of factor, social or genetic, that prevails in the control of sex change [131]. While in elasmobranchs and deep sea species, it is their complex reproductive strategies, which include late maturation, slow growth and low fecundity, among other aspects, that are the main sources of reproductive vulnerability [133,134].

Aquaculture can also be a source of disturbance to the parental effects of wild popula-
tions. Transmission of parasites and diseases from cultured to wild fish can lead to a decline
in the health status and condition of wild populations [135]. The escape of captive fish
and hybridization with wild individuals can lead to a reduction in the genetic variability
of the wild populations, which can cause maladaptations, reducing the fitness and repro-
ductive success of wild individuals [56,136]. An example of these effects was observed in
sockeye salmon (Oncorhynchus nerka) of the Cedar River (USA). A captive rearing program
of sockeye salmon was initiated in the Cedar River for restocking wild populations in the
mid-1990s. These salmon were fed an enriched diet and tended to begin spawning earlier
than wild populations, before optimum water temperature was reached. Release of these
individuals to the wild resulted in a 1–3 week earlier spawning onset than observed in the
1990s. This early reproduction affects embryonic development that is strongly influenced
by temperature, as earlier spawning exposes embryos to warmer water, provoking a low
survival rate of juveniles and reducing the reproductive success of the population [22].
Finally, climate change, one of the most global anthropogenic disturbances facing aquatic
ecosystems, also causes reproductive alterations by affecting environmental conditions that
modulate the neuroendocrine axis [137]. In addition, environmental variations are capable
of changing the demography and attributes of a population, with important consequences
on resilience. However, parental effects can compensate for these impacts, and their role
is especially relevant in situations of environmental stress, such as that caused by climate
change. In this sense, different or even contradictory effects can be observed depending on
the species or population. For example, the increase in temperature has caused in *Gadus morhua*, an advance of spawning season, with low fertility [138], and in *Thymalusthy mallus*, a low egg survival [139], while in *Salvelinus alpinus*, it has resulted in delayed spawning and inhibition of ovulation [140], [141], and in *Anarhichas lupus* to low embryonic survival [142]. Even more, global warming may favor reproductive potential in some cases, as has been reported for some invasive species [143,144]. Temperature changes can also affect the sex ratio in fish by regulating the expression and activity of certain hormones and enzymes that control sex determination, such that an increase in sea temperature would produce a tendency toward masculinization in gonochoric species [145], a premature transition from female to male in protandric hermaphrodite species, or an inhibition of the transition to female in protandric hermaphrodite species, even in the presence of an appropriate social context [146].

In summary, reproductive success is modulated by environmental factors and parental attributes, as well as by human-induced effects. Under climate change scenarios, small environmental variations can result in major changes in reproductive and biological traits [147], as well as at the physiological level [148]. These effects will be more marked in species that are limited in their ability to shift geographic distribution or are already at their tolerance limits [146]. In the last decades, numerous papers have reported changes in the distribution of marine species associated with rising sea temperatures in both the northern [149,150] and southern hemispheres [151], as well as in freshwater species in both hemispheres [152,153], which will undoubtedly have an impact on their reproductive success, given the characteristics of the new habitats and communities of which they will become part, and which will determine, among other things, the availability of food, the type of interspecific relationships or the degree of stress, modulating parental effects. Furthermore, different mechanisms of resistance to reproductive stress have been documented in many vertebrates, although these mechanisms are also regulated by a complex framework of environmental interactions [154]. All these issues must be taken into account to properly managing aquatic ecosystems if their resilience is to be preserved.

**6. Studies on Parental Effects and Reproductive Potential: Future Perspectives**

As we have mentioned, numerous studies of reproductive potential and parental effects have been carried out on different marine and freshwater species. Many studies focus on maternal effects and species with high commercial or ecological value. However, there are few studies on reproductive potential and parental effects in crustaceans, cephalopods, elasmobranchs and inland water species, which are of great importance in terms of socio-economic impact or ecological relevance.

Most of the work on reproductive potential and parental effects of aquatic organisms
has focused on the maternal part, analyzing the influence of the length, age and condition
of females on egg production and egg quality, as well as on the selection of the spawning
area and the duration and frequency of reproductive events, including the phenomenon
of skipping spawning that has been observed in some species [50,70,155]. There are also
some papers on maternal effects on larvae [97,156], although they are scarce. In addition,
although much has been theorized about the impact that these maternal effects may have
on recruitment to the fishery based on the study of temporal and geographic variation
in maternal attributes or egg and larval characteristics, there are hardly any papers that
directly relate recruitment to these attributes [157]. Conversely, most papers refer to parental
heritage and *indirect environmental effects*, both *prezygotic* and *prenatal postzygotic*, as well as
a few studies on *postnatal postzygotic effects*, but parental selection effects associated with
parental behavior and experience have been poorly studied. Similarly, there are few studies
on the transgenerational impact of parental effects, even though such transgenerational
effects have already been reported in some fish species [25,26]. Likewise, studies on
paternal effects are scarce. In that sense, although it is true that the impact of females on
their offspring may be greater than that of males, it has been shown that males also play a relevant role in the development of offspring [10,158]. More and more studies highlight the importance of paternal effects and their interaction with maternal effects on early life stages survival, which may be particularly relevant in environments with changing conditions [58,80]. Conversely, it is expected that paternal effects are especially determinant in the case of species in which males are responsible for the care of the offspring, the selection of the breeding area and the construction of nest, and in marked social and territorial behavior [11,80].

In relation to the transgenerational concept of reproductive potential, it is essential to further analyze the reproductive resilience of exploited species, especially in the context of climate change. This involves analyzing the factors that ensure long-term reproductive success under different climate scenarios and exploitation regimes, studying several generations of reproductive fitness. Most of the studies analyzing the effects of climate change have focused on shifting species distributions, but less attention has been paid to changing life rates (such as growth and reproduction), which may also determine life history strategies and population resilience in a changing climate. Reproductive success occurs at the individual scale and results in both density- and fitness-dependent feedback loops that act to maintain the reproductive success of the population over time and determine the reproductive resilience of that population [159]. Therefore, any stressor that affects individual fitness will have consequences throughout the population that may also be transmitted generation after generation. However, despite all these studies, some authors conclude that transgenerational parental effects are not as relevant in the adaptation to stress as expected [160].

In summary, although much progress has been achieved in the study of reproductive ecology, reproductive potential and maternal effects in aquatic organisms, there is still a long way to go. First, more studies on reproductive potential of invertebrates (crustaceans and cephalopods), elasmobranchs and inland water species are needed. Second, and for all families (including teleosts), other aspects of parental effects that have not been thoroughly investigated to date, such as *postnatal postzygotic parental effects*, parental selection, paternal effects and the transgenerational impact of reproductive potential, need to be investigated. Finally, it is necessary to analyze the reproductive-recruit system in a broader context, incorporating spatial and temporal perspectives at different scales that are appropriate to the life cycle of the individual, the population and the species, as well as the influence of the environment and evolutionary pressure on the reproductive-recruit system. In this context, it will be necessary to develop new tools for monitoring populations and ecosystems in all their dimensions with a transdisciplinary approach. In parallel, the construction and implementation of integral models is necessary to understand the multiple processes that determine reproductive potential and parental effects and their complex interrelationships at different scales of ecological organization (from the individual to the ecosystem).

The last purpose of research on reproductive potential and parental effects should be to evaluate the reproductive resilience of populations of aquatic organisms through holistic models that predict their variations under different environmental scenarios. Only in this way can populations be adequately managed under the climate threat and ocean pollution we are facing for a sustainable development of the blue growth strategy.

**Author Contributions:** Conceptualization, R.D.-P.; investigation, R.D.-P., C.G.-F., E.L., K.R. and G.J.M.; writing—original draft preparation, R.D.-P., C.G.-F., E.L., K.R. and G.J.M.; writing—review and editing, R.D.-P., C.G.-F., E.L., K.R. and G.J.M.; visualization—R.D.-P., C.G.-F., E.L., K.R. and G.J.M.; infographics, R.D.-P. and K.R.; supervision, R.D.-P. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research received no external funding.

**Institutional Review Board Statement:** Not applicable.

**Data Availability Statement:** Not applicable.
**Acknowledgments:** We thank the INVIPESCA Network for editing the book "Ecología Reproduc-
tiva y Pesquerías en el contexto iberoamericano" which was the seed of this manuscript.

**Conflicts of Interest:** The authors declare no conflict of interest.

**References**

1. Venturelli, P.A.; Shuter, B.J.; Murphy, C.A. Evidence for harvest-induced maternal influences on the reproductive rates of fish populations. *Proc. R. Soc. B Boil. Sci.* **2008**, *276*, 919–924. [CrossRef]

2. Trippel, E.A. Estimation of Stock Reproductive Potential: History and Challenges for Canadian Atlantic Gadoid Stock Assessments. *J. Northwest Atl. Fish. Sci.* **1999**, *25*, 61–81. [CrossRef]

3. Kjesbu, O.S.; Murua, H.; Saborido-Rey, F.; Witthames, P.R. Method development and evaluation of stock reproductive potential of marine fish. *Fish. Res.* **2010**, *104*, 1–7. [CrossRef]

4. Bernardo, J. Maternal Effects in Animal Ecology. *Am. Zool.* **1996**, *36*, 83–105. [CrossRef]

5. Reznick, D.; Callahan, H.; Llauredo, R. Maternal Effects on Offspring Quality in Poeciliid Fishes. *Am. Zool.* **1996**, *36*, 147–156. [CrossRef]

6. Von Siebenthal, B.A.; Jacob, A.; Wedekind, C. Tolerance of whitefish embryos to *Pseudomonas fluorescens* linked to genetic and maternal effects, and reduced by previous exposure. *Fish Shellfish Immunol.* **2009**, *26*, 531–535. [CrossRef] [PubMed]

7. Shama, L.N.S.; Strobel, A.; Mark, F.C.; Wegner, K.M. Transgenerational plasticity in marine sticklebacks: Maternal effects mediate impacts of a warming ocean. *Funct. Ecol.* **2014**, *28*, 1482–1493. [CrossRef]

8. Dietrich, G.J.; Dietrich, M.; Kowalski, R.; Dobosz, S.; Karol, H.; Demianowicz, W.; Glogowski, J. Exposure of rainbow trout milt to mercury and cadmium alters sperm motility parameters and reproductive success. *Aquat. Toxicol.* **2010**, *97*, 277–284. [CrossRef] [PubMed]

9. Carver, A.M. Selective Fishing Pressure on Large Male Blue Crabs Negatively Affect Small Size, Sex Ratio, and Population Reproductive Potential in the Upper Chesapeake Bay. Master's Thesis, North Carolina State University, Raleigh, NC, USA, 2001.

10. Rideout, R.M.; Trippel, E.A.; Litvak, M.K. Paternal effects on haddock early life history traits. *J. Fish Biol.* **2004**, *64*, 695–701. [CrossRef]

11. Stein, L.R.; Bell, A.M. Paternal programming in sticklebacks. *Anim. Behav.* **2014**, *95*, 165–171. [CrossRef] [PubMed]

12. Beirão, J.; Soares, F.; Herráez, M.; Dinis, M.; Cabrita, E. Changes in *Solea senegalensis* sperm quality throughout the year. *Anim. Reprod. Sci.* **2011**, *126*, 122–129. [CrossRef] [PubMed]

13. Blom, E.-L.; Kvarnemo, C.; Dekhla, I.; Schöld, S.; Andersson, M.H.; Svensson, O.; Amorim, M.C.P. Continuous but not intermittent noise has a negative impact on mating success in a marine fish with paternal care. *Sci. Rep.* **2019**, *9*, 5494. [CrossRef]

14. López-Galindo, L.; Galindo-Sánchez, C.; Olivares, A.; Avila-Poveda, O.H.; Díaz, F.; Juárez, O.E.; Lafarga, F.; Pantoja-Pérez, J.; Caamal-Monsreal, C.; Rosas, C. Reproductive performance of *Octopus maya* males conditioned by thermal stress. *Ecol. Indic.* **2018**, *96*, 437–447. [CrossRef]

15. Macartney, E.L.; Crean, A.J.; Bonduriansky, R. Epigenetic paternal effects as costly, condition-dependent traits. *Heredity* **2018**, *121*, 248–256. [CrossRef] [PubMed]

16. Siddique, M.A.M.; Linhart, O.; Krejszeff, S.; Žarski, D.; Pitcher, T.E.; Politis, S.N.; Butts, I.A.E. Paternal identity impacts embryonic development for two species of freshwater fish. *Gen. Comp. Endocrinol.* **2017**, *245*, 30–35. [CrossRef] [PubMed]

17. Lymbery, R.A.; Berson, J.D.; Evans, J.P. Indirect parental effects on offspring viability by egg-derived fluids in an external fertilizer. *Proc. R. Soc. B Boil. Sci.* **2020**, *287*, 20202538. [CrossRef]

18. Ripley, J.L.; Foran, C.M. Direct evidence for embryonic uptake of paternally-derived nutrients in two pipefishes (Syngnathidae: *Syngnathus* spp.). *J. Comp. Physiol. B* **2008**, *179*, 325–333. [CrossRef]

19. Guillaume, A.S.; Monro, K.; Marshall, D. Transgenerational plasticity and environmental stress: Do paternal effects act as a conduit or a buffer? *Funct. Ecol.* **2015**, *30*, 1175–1184. [CrossRef]

20. Lyons, K.; Adams, D. Maternal offloading of organochlorine contaminants in the yolk-sac placental scalloped hammerhead shark (*Sphyrna lewini*). *Ecotoxicology* **2014**, *24*, 553–562. [CrossRef]

21. Jones, G. Spawning-site choice by female *Pseudolabrus celidotus* (Pisces: Labridae) and its influence on the mating system. *Behav. Ecol. Sociobiol.* **1981**, *8*, 129–142. [CrossRef]

22. Tillotson, M.D.; Barnett, H.K.; Bhuthimethee, M.; Koehler, M.E.; Quinn, T.P. Artificial selection on reproductive timing in hatchery salmon drives a phenological shift and potential maladaptation to climate change. *Evol. Appl.* **2018**, *12*, 1344–1359. [CrossRef] [PubMed]

23. Marteinsdottir, G.; Begg, G.A. Essential relationships incorporating the influence of age, size and condition on variables required for estimation of reproductive potential in Atlantic cod *Gadus morhua*. *Mar. Ecol. Prog. Ser.* **2002**, *235*, 235–256. [CrossRef]

24. Goldberg, R.L.; Downing, P.A.; Griffin, A.S.; Green, J.P. The costs and benefits of paternal care in fish: A meta-analysis. *Proc. R. Soc. B Boil. Sci.* **2020**, *287*, 20201759. [CrossRef] [PubMed]

25. Schade, F.M.; Clemmesen, C.; Wegner, K.M. Within- and transgenerational effects of ocean acidification on life history of marine three-spined stickleback (*Gasterosteus aculeatus*). *Mar. Biol.* **2014**, *161*, 1667–1676. [CrossRef]
26. Jasperse, L.; Levin, M.; Rogers, K.; Perkins, C.; Bosker, T.; Griffitt, R.J.; Sepúlveda, M.S.; De Guise, S. Transgenerational effects of polycyclic aromatic hydrocarbon exposure on sheepshead minnows (*Cyprinodon variegatus*). *Environ. Toxicol. Chem.* **2018**, *38*, 638–649. [CrossRef] [PubMed]

27. Räsänen, K.; Kruuk, L.E.B. Maternal effects and evolution at ecological time-scales. *Funct. Ecol.* **2007**, *21*, 408–421. [CrossRef]

28. Lehto, W.R.; Tinghitella, R.M. Predator-induced maternal and paternal effects independently alter sexual selection. *Evolution* **2019**, *74*, 404–418. [CrossRef]

29. Jensen, N.; Allen, R.M.; Marshall, D.J. Adaptive maternal and paternal effects: Gamete plasticity in response to parental stress. *Funct. Ecol.* **2013**, *28*, 724–733. [CrossRef]

30. Mousseau, T. The adaptive significance of maternal effects. *Trends Ecol. Evol.* **1998**, *13*, 403–407. [CrossRef]

31. Curley, J.P.; Mashoodh, R.; Champagne, F.A. Epigenetics and the origins of paternal effects. *Horm. Behav.* **2011**, *59*, 306–314. [CrossRef]

32. Rando, O.J. Daddy Issues: Paternal Effects on Phenotype. *Cell* **2012**, *151*, 702–708. [CrossRef] [PubMed]

33. Crean, A.J.; Bonduriansky, R. What is a paternal effect? *Trends Ecol. Evol.* **2014**, *29*, 554–559. [CrossRef] [PubMed]

34. Catalán, I.A.; Reglero, P.; Álvarez, I. Research on early life stages of fish: A lively field. *Mar. Ecol. Prog. Ser.* **2020**, *650*, 1–5. [CrossRef]

35. Chambers, R.C.; Trippel, E.A. *Early Life History and Recruitment in Fish Populations*; Chapman & Hall/CRC: London, UK, 1997.

36. Green, B.S. Chapter 1: Maternal Effects in Fish Populations. *Adv. Mar. Biol.* **2008**, *54*, 1–105. [CrossRef] [PubMed]

37. McCormick, M.I. Mothers Matter: Crowding Leads to Stressed Mothers and Smaller Offspring in Marine Fish. *Ecology* **2006**, *87*, 1104–1109. [CrossRef]

38. Leggett, W.; Deblois, E. Recruitment in marine fishes: Is it regulated by starvation and predation in the egg and larval stages? *Neth. J. Sea Res.* **1994**, *32*, 119–134. [CrossRef]

39. Andree, S.R.; Feiner, Z.S.; Bledsoe, J.W.; Cragun, A.M.; Höök, T.O. Ontogenetic variability of maternal effects in an iteroparous fish. *Ecol. Freshw. Fish* **2014**, *24*, 384–396. [CrossRef]

40. Calder, W. *Size, Function, and Life History*; Harvard University Press: Cambridge, MA, USA, 1984.

41. Valentinsson, D. Reproductive cycle and maternal effects on offspring size and number in the neogastropod *Buccinum undatum* (L.). *Mar. Biol.* **2002**, *140*, 1139–1147. [CrossRef]

42. Shlesinger, T.; Loya, Y. Depth-dependent parental effects create invisible barriers to coral dispersal. *Commun. Biol.* **2021**, *4*, 202. [CrossRef]

43. Pitman, R.W. Effects of Female Age and Egg Size on Growth and Mortality in Rainbow Trout. *Progress. Fish-Culturist* **1979**, *41*, 202–204. [CrossRef]

44. Blaxter, J.H.S.; Hempel, G. The Influence of Egg Size on Herring Larvae (*Clupea harengus* L.). *ICES J. Mar. Sci.* **1963**, *28*, 211–240. [CrossRef]

45. Marteinsdottir, G.; Steinarsson, A. Maternal influence on the size and viability of Iceland cod *Gadus morhua* eggs and larvae. *J. Fish Biol.* **1998**, *52*, 1241–1258. [CrossRef]

46. Searcy, S.P.; Sponaugle, S. Selective Mortality during the Larval-Juvenile Transition in Two Coral Reef Fishes. *Ecology* **2001**, *82*, 2452. [CrossRef]

47. Kjesbu, O.; Solemdal, P.; Bratland, P.; Fonn, M. Variation in annual egg production in individual captive Atlantic cod (*Gadus morhua*). *Can. J. Fish. Aquat. Sci.* **1996**, *53*, 610–620. [CrossRef]

48. Ma, Y.; Kjesbu, O.S.; Jørgensen, T. Effects of ration on the maturation and fecundity in captive Atlantic herring (*Clupea harengus*). *Can. J. Fish. Aquat. Sci.* **1998**, *55*, 900–908. [CrossRef]

49. Kjesbu, O.; Witthames, P.; Solemdal, P.; Walker, M.G. Temporal variations in the fecundity of Arcto-Norwegian cod (*Gadus morhua*) in response to natural changes in food and temperature. *J. Sea Res.* **1998**, *40*, 303–321. [CrossRef]

50. Rideout, R.M.; Rose, G.A.; Burton, M.P.M. Skipped spawning in female iteroparous fishes. *Fish Fish.* **2005**, *6*, 50–72. [CrossRef]

51. Solemdal, P.; Kjesbu, O.S.; Fonn, M. Egg Mortality in Recruit- and Repeat-Spawning Cod—An Experimental Study. In *ICES CM 1995/G35*; ICES: Copenhagen, Denmark, 1995; 10p, Available online: https://imr.brage.unit.no/imr-xmlui/bitstream/handle/11250/100329/G35_1995.pdf?sequence=4&isAllowed=y (accessed on 17 July 2022).

52. Wright, P.J.; Trippel, E.A. Fishery-induced demographic changes in the timing of spawning: Consequences for reproductive success. *Fish Fish.* **2009**, *10*, 283–304. [CrossRef]

53. Lowerre-Barbieri, S.K.; Ganias, K.; Saborido-Rey, F.; Murua, H.; Hunter, J.R. Reproductive Timing in Marine Fishes: Variability, Temporal Scales, and Methods. *Mar. Coast. Fish.* **2011**, *3*, 71–91. [CrossRef]

54. Mertz, G.; Myers, R.A. Match/mismatch predictions of spawning duration versus recruitment variability. *Fish. Oceanogr.* **1994**, *3*, 236–245. [CrossRef]

55. Humphries, P.; Richardson, A.; Wilson, G.; Ellison, T. River regulation and recruitment in a protracted-spawning riverine fish. *Ecol. Appl.* **2013**, *23*, 208–225. [CrossRef]

56. Bekkevold, D. Male size composition affects male reproductive variance in Atlantic cod *Gadus morhua* L. spawning aggregations. *J. Fish Biol.* **2006**, *69*, 945–950. [CrossRef]

57. Trippel, E.; Kraus, G.; Köster, F. Maternal and paternal influences on early life history traits and processes of Baltic cod *Gadus morhua*. *Mar. Ecol. Prog. Ser.* **2005**, *303*, 259–267. [CrossRef]
58. Green, B.S.; McCormick, M. Maternal and paternal effects determine size, growth and performance in larvae of a tropical reef fish. *Mar. Ecol. Prog. Ser.* **2005**, *289*, 263–272. [CrossRef]

59. Hosoya, S.; Mizuno, N.; Kikuchi, K.; Kurokura, H. Rearing Takifugu rubripes larvae in communal tanks: Paternal genetic contribution to survivability. *Fish. Sci.* **2014**, *80*, 1037–1043. [CrossRef]

60. Crean, A.J.; Dwyer, J.M.; Marshall, D.J. Adaptive paternal effects? Experimental evidence that the paternal environment affects offspring performance. *Ecology* **2013**, *94*, 2575–2582. [CrossRef]

61. Rivera, H.E.; Chen, C.Y.; Gibson, M.C.; Tarrant, A.M. Plasticity in parental effects confers rapid larval thermal tolerance in the estuarine anemone *Nematostella vectensis*. *J. Exp. Biol.* **2021**, *224*, jeb236745. [CrossRef]

62. Kaufmann, J.; Lenz, T.; Milinski, M.; Eizaguirre, C. Experimental parasite infection reveals costs and benefits of paternal effects. *Ecol. Lett.* **2014**, *17*, 1409–1417. [CrossRef]

63. Wirtz-Ocaña, S.; Schütz, D.; Pachler, G.; Taborsky, M. Paternal inheritance of growth in fish pursuing alternative reproductive tactics. *Ecol. Evol.* **2013**, *3*, 1614–1625. [CrossRef]

64. Reznick, D. Grandfather Effects: The Genetics of Interpopulation Differences in Offspring Size in the Mosquito Fish. *Evolution* **1981**, *35*, 941. [CrossRef]

65. Macchi, G.J.; Pájaro, M.; Madirolas, A. Can a change in the spawning pattern of Argentine hake (*Merluccius hubbsi*) affect its recruitment? *Fish. Bull.* **2005**, *103*, 445–452.

66. Lowerre-Barbieri, S.K.; Henderson, N.; Llopiz, J.; Walters, S.; Bickford, J.; Muller, R. Defining a spawning population (spotted seatrout *Cynoscion nebulosus*) over temporal, spatial, and demographic scales. *Mar. Ecol. Prog. Ser.* **2009**, *394*, 231–245. [CrossRef]

67. Blanchfield, P.J.; Ridgway, M.S. The relative influence of breeding competition and habitat quality on female reproductive success in lacustrine brook trout (*Salvelinus fontinalis*). *Can. J. Fish. Aquat. Sci.* **2005**, *62*, 2694–2705. [CrossRef]

68. Álvarez-Colombo, G.; Dato, C.; Macchi, G.; Palma, E.; Machinandiarena, L.; Christiansen, H.; Betti, P.; Derisio, C.; Martos, P.; Castro-Machado, F.; et al. Distribution and behavior of Argentine hake larvae: Evidence of a biophysical mechanism for self-recruitment in northern Patagonian shelf waters. *Cienc. Mar.* **2011**, *37*, 633–657. [CrossRef]

69. Marteinsdottir, G.; Gudmundsdottir, A.; Thorsteinsson, V.; Stefansson, G. Spatial variation in abundance, size composition and viable egg production of spawning cod (*Gadus morhua* L.) in Icelandic waters. *ICES J. Mar. Sci.* **2000**, *57*, 824–830. [CrossRef]

70. Petitgas, P.; Reid, D.; Planque, B.; Nogueira, E.; O'Hea, B.; Cotano, U. The Entrainment Hypothesis: An Explanation for the Persistence and Innovation in Spawning Migrations and Life Cycle Spatial Patterns. In *ICES CM2006/B:07; ICES: Copenhagen, Denmark*, 2006; 9p, Available online: https://www.ices.dk/sites/pub/CM%20Documents/2006/B/B0706.pdf (accessed on 17 July 2022).

71. Lambert, T.C. The effect of population structure on recruitment in herring. *ICES J. Mar. Sci.* **1990**, *47*, 249–255. [CrossRef]

72. Shaw, S.L.; Sass, G.G.; Vandehey, J.A. Maternal effects better predict walleye recruitment in Escanaba Lake, Wisconsin, 1957–2015: Implications for regulations. *Can. J. Fish. Aquat. Sci.* **2018**, *75*, 2320–2331. [CrossRef]

73. Bloor, I.S.; Attrill, M.J.; Jackson, E.L. A Review of the Factors Influencing Spawning, Early Life Stage Survival and Recruitment Variability in the Common Cuttlefish (*Sepia officinalis*). *Adv. Mar. Biol.* **2013**, *65*, 1–65. [CrossRef]

74. Marshall, D.J. Transgenerational plasticity in the sea: Context-dependent maternal effects across the life history. *Ecology* **2008**, *89*, 418–427. [CrossRef]

75. Schwindt, A.R.; Winkelman, D.L.; Keteles, K.; Murphy, M.; Vajda, A.M. An environmental oestrogen disrupts fish population dynamics through direct and transgenerational effects on survival and fecundity. *J. Appl. Ecol.* **2014**, *51*, 582–591. [CrossRef]

76. Po, B.H.; Chiu, J.M. Transgenerational impairments of reproduction and development of the marine invertebrate *Crepidula onyx* resulted from long-term dietary exposure of 2,2',4,4'-tetrabromodiphenyl ether (BDE-47). *Environ. Pollut.* **2018**, *235*, 730–738. [CrossRef]

77. Figueredo, A.J.; Vásquez, G.; Brumbach, B.H.; Schneider, S.M.; Sefcek, J.A.; Tal, I.R.; Hill, D.; Wenner, C.J.; Jacobs, W.J. Consilience and Life History Theory: From genes to brain to reproductive strategy. *Dev. Rev.* **2006**, *26*, 243–275. [CrossRef]

78. Pianka, E.R. On r- and K-Selection. *Am. Nat.* **1970**, *104*, 592–597. [CrossRef]

79. Mary, C.M.S.; Gordon, E.; Hale, R.E. Environmental effects on egg development and hatching success in *Jordanella floridae*, a species with parental care. *J. Fish Biol.* **2004**, *65*, 760–768. [CrossRef]

80. McGhee, K.E.; Bell, A.M.; Chaplin-Kramer, R.; Dombeck, E.; Gerber, J.; Knuth, K.A.; Mueller, N.D.; Mueller, M.; Ziv, G.; Klein, A.-M. Paternal care in a fish: Epigenetics and fitness enhancing effects on offspring anxiety. *Proc. R. Soc. B Boil. Sci.* **2014**, *281*, 20141146. [CrossRef] [PubMed]

81. McBride, R.S.; Somarakis, S.; Fitzhugh, G.R.; Albert, A.; Yaragina, N.A.; Wuenschel, M.J.; Alonso-Fernández, A.; Basilone, G. Energy acquisition and allocation to egg production in relation to fish reproductive strategies. *Fish Fish.* **2013**, *16*, 23–57. [CrossRef]

82. Szala, A.; Shackelford, T.K. Polygynandry. In *Encyclopedia of Animal Cognition and Behavior*; Vonk, J., Shackelford, T., Eds.; Springer: Cham, Switzerland, 2019. [CrossRef]

83. Le Cam, S.; Pechenik, J.A.; Cagnon, M.; Viard, F. Fast versus Slow Larval Growth in an Invasive Marine Mollusc: Does Paternity Matter? *J. Hered.* **2009**, *100*, 455–464. [CrossRef]

84. McLeod, L.; Marshall, D.J. Do Genetic Diversity Effects Drive the Benefits Associated with Multiple Mating? A Test in a Marine Invertebrate. *PLoS ONE* **2009**, *4*, e6347. [CrossRef] [PubMed]

85. Lasker, R. The role of a stable ocean in larval fish survival and subsequent recruitment. In *Marine Fish Larvae: Morphology, Ecology and Relation to Fisheries*; Lasker, R., Ed.; Washington Sea Grant Program: Seattle, WA, USA, 1981; pp. 79–87.
86. Cury, P.; Roy, C. Optimal Environmental Window and Pelagic Fish Recruitment Success in Upwelling Areas. *Can. J. Fish. Aquat. Sci.* **1989**, *46*, 670–680. [CrossRef]

87. Potts, G.; Wootton, R. *Fish Reproduction: Strategies and Tactics*, 3rd ed.; Academic Press Limited: London, UK, 1989.

88. Beamish, R.J. Marine fish production trends off the Pacific coast of Canada and the United States. In *Climate Change and Northern Fish Populations*; Beamish, R.J., Ed.; Canadian Special Publication of Fisheries and Aquatic Sciences; NRC Research Press: Ottawa, ON, Canada, 1995; Volume 121, pp. 585–591.

89. Dygert, P.H. Seasonal Changes in Energy Content and Proximate Composition Associated with Somatic Growth and Reproduction in a Representative Age-Class of Female English Sole. *Trans. Am. Fish. Soc.* **1990**, *119*, 791–801. [CrossRef]

90. Lawson, J.; Magalhães, A.; Miller, E. Important prey species of marine vertebrate predators in the northwest Atlantic: proximate composition and energy density. *Mar. Ecol. Prog. Ser.* **1998**, *164*, 13–20. [CrossRef]

91. Kooijman, B.; Kooijman, S.A.L.M. *Dynamic Energy Budget Theory*, 3rd ed.; Cambridge University Press: New York, NY, USA, 2000.

92. Lambert, Y.; Dutil, J.-D. Energetic consequences of reproduction in Atlantic cod (*Gadus morhua*) in relation to spawning level of somatic energy reserves. *Can. J. Fish. Aquat. Sci.* **2000**, *57*, 815–825. [CrossRef]

93. Lloret, J.; Shulman, G.; Love, R.M. *Condition and Health Indicators of Exploited Marine Fishes*; John Wiley & Sons: Oxford, MA, USA, 2013.

94. Trippel, E.A. Estimation of male reproductive success of marine fishes. *J. Northwest Atl. Fish. Sci.* **2003**, *33*, 81–113. [CrossRef]

95. Knutsen, G.M.; Tilseth, S. Growth, Development, and Feeding Success of Atlantic Cod Larvae *Gadus morhua* Related to Egg Size. *Trans. Am. Fish. Soc.* **1985**, *114*, 507–511. [CrossRef]

96. Domínguez-Petit, R. Study of Reproductive Potential of Merluccius Merluccius in the Galician Shelf. Ph.D. Thesis, University of Vigo, Vigo, Spain, 2007.

97. Fernández, C.G.; Domínguez-Petit, R.; Aldanondo, N.; Saborido-Rey, F. Seasonal variability of maternal effects in European hake *Merluccius merluccius*. *Mar. Ecol. Prog. Ser.* **2020**, *650*, 125–140. [CrossRef]

98. Blaxter, J.; Hunter, J. The Biology of the Clupeoid Fishes. *Adv. Mar. Biol.* **1982**, *20*, 1–223. [CrossRef]

99. Rose, K.A.; Cowan, J.H.; Winemiller, K.; Myers, R.A.; Hilborn, R. Compensatory density dependence in fish populations: Importance, controversy, understanding and prognosis. *Fish Fish.* **2001**, *2*, 293–327. [CrossRef]

100. Samhoury, J.F. Food supply influences offspring provisioning but not density-dependent fecundity in a marine fish. *Ecology* **2009**, *90*, 3478–3488. [CrossRef] [PubMed]

101. Pennington, J.T. The ecology of fertilization of echinoid eggs: The consequences of sperm dilution, adult aggregation, and synchronous spawning. *Biol. Bull.* **1985**, *169*, 417–430. [CrossRef]

102. Levitan, D.R. Predicting Optimal and Unique Egg Sizes in Free-Spawning Marine Invertebrates. *Am. Nat.* **1996**, *148*, 174–188. [CrossRef]

103. Marilú, B.C.; Julio, M.P.; Cecilia, P.T.; Pepe, E.; Larry, H.; Betsy, B.D.; Ángel, P.d.; Carlos, G.V.; Monique, M. Biología de la anchoveta peruana, Engraulis ringens Jenyns. *Boletín del Inst. del Mar del Perú* **2010**, *25*, 23–30.

104. Pájaro, M.; Leonarduzzi, E.; Hansen, J.; Macchi, G. Analysis of the reproductive potential of two stocks of *Engraulis anchoita* in the Argentine Sea. *Cienc. Mar.* **2011**, *37*, 603–618. [CrossRef]

105. Rodriguez, C.; Norbis, W.; Vizziano, D. Efectos de los cambios ambientales en la estrategia reproductiva de la lacha (Brevoortia aurea) en una laguna costera de Uruguay. In *IV Simposio Iberoamericano de Ecología Reproductiva, Reclutamiento y Pesquerías; Iquique, Chile, 2018*; p. 76. Available online: http://docplayer.es/122775306-Libro-de-resumenes-sibecorp-iv-iquique-chile.html (accessed on 17 July 2022).

106. Olney, J.E.; McBride, R.S. Intraspecific variation in batch fecundity of American shad: Revisiting the paradigm of reciprocal latitudinal trends in reproductive traits. *Am. Fish. Soc. Symp.* **2003**, *2003*, 185–192.

107. Atkinson, D. Temperature and Organism Size—A Biological Law for Ectotherms? *Adv. Ecol. Res.* **1994**, *25*, 1–58. [CrossRef]

108. Fernández-Torres, F.; Martínez, P.A.; Olalla-Tárraga, M. Shallow water ray-finned marine fishes follow Bergmann's rule. *Basic Appl. Ecol.* **2018**, *33*, 99–110. [CrossRef]

109. Kokita, T. Latitudinal compensation in female reproductive rate of a geographically widespread reef fish. *J. Appl. Phycol.* **2004**, *71*, 213–224. [CrossRef]

110. Billerbeck, J.M.; Schultz, E.T.; Conover, D.O. Adaptive variation in energy acquisition and allocation among latitudinal populations of the Atlantic silverside. *Oecologia* **2000**, *122*, 210–219. [CrossRef]

111. Wear, R.G. Incubation in British Decapod Crustacea, and the Effects of Temperature on the Rate and Success of Embryonic Development. *J. Mar. Biol. Assoc.* **1974**, *54*, 745–762. [CrossRef]

112. Pörtner, H. Climate variations and the physiological basis of temperature dependent biogeography: Systemic to molecular hierarchy of thermal tolerance in animals. *Comp. Biochem. Physiol. Part A Mol. Integr. Physiol.* **2002**, *132*, 739–761. [CrossRef]

113. Brante, A.; Fernández, M.; Eckerle, L.; Mark, F.; Pörtner, H.; Arntz, W. Reproductive investment in the crab *Cancer setosus* along a latitudinal cline: Egg production, embryo losses and embryo ventilation. *Mar. Ecol. Prog. Ser.* **2003**, *251*, 221–232. [CrossRef]

114. Rätz, H.-J.; Lloret, J. Variation in fish condition between Atlantic cod (*Gadus morhua*) stocks, the effect on their productivity and management implications. *Fish. Res.* **2003**, *60*, 369–380. [CrossRef]

115. Hidalgo, M.; Massutí, E.; Moranta, J.; Cartes, J.; Lloret, J.; Oliver, P.; Morales-Nin, B. Seasonal and short spatial patterns in European hake (*Merluccius merluccius* L.) recruitment process at the Balearic Islands (western Mediterranean): The role of environment on distribution and condition. *J. Mar. Syst.* **2008**, *71*, 367–384. [CrossRef]
116. Amoatey, P.; Baawain, M.S. Effects of pollution on freshwater aquatic organisms. *Water Environ. Res.* **2019**, *91*, 1272–1287.
[CrossRef] [PubMed]

117. Mearns, A.J.; Reish, D.J.; Oshida, P.S.; Morrison, A.M.; Rempel-Hester, M.A.; Arthur, C.; Rutherford, N.; Pryor, R. Effects of Pollution on Marine Organisms. *Water Environ. Res.* **2016**, *88*, 1693–1807. [CrossRef]

118. Arukwe, A. Cellular and Molecular Responses to Endocrine-Modulators and the Impact on Fish Reproduction. *Mar. Pollut. Bull.* **2001**, *42*, 643–655. [CrossRef]

119. Matthiessen, P. Endocrine disruption in marine fish. *Pure Appl. Chem.* **2003**, *75*, 2249–2261. [CrossRef]

120. Foley, C.J.; Feiner, Z.S.; Malinich, T.D.; Höök, T.O. A meta-analysis of the effects of exposure to microplastics on fish and aquatic invertebrates. *Sci. Total. Environ.* **2018**, *631–632*, 550–559. [CrossRef]

121. Jakimska, A.; Konieczka, P.; Skóra, K.; Namieśnik, J. Accumulation of Metals in Tissues and Organs of Marine Organisms The Effect of Metals on Marine Organisms. *Polish J. Environ. Stud.* **2011**, *20*, 1117–1125.

122. Jones, J.C.; Reynolds, J.D. Effects of pollution on reproductive behaviour of fishes. *Rev. Fish Biol. Fish.* **1997**, *7*, 463–491. [CrossRef]

123. Yin, X.-H.; Liu, Y.; Zeb, R.; Chen, F.-Y.; Chen, H.-Y.; Wang, K.-J. The intergenerational toxic effects on offspring of medaka fish *Oryzias melastigma* from parental benzo[a]pyrene exposure via interference of the circadian rhythm. *Environ. Pollut.* **2020**, *267*, 115437. [CrossRef] [PubMed]

124. Rodrigues, K.A.; Macchi, G.J.; Militelli, M.I. Comparative study of spawning pattern and reproductive potential of the Northern and Southern stocks of Argentine hake (*Merluccius hubbsi*). *J. Sea Res.* **2015**, *102*, 22–32. [CrossRef]

125. Firpo, C.; Wyngaard, J.; Mango, C.M.V. Análisis Preliminar de la Temporada de Pesca de Centolla (Lithodes santolla), 2015-2016; Informe Técnico Oficial; Instituto Nacional de Investigación y Desarrollo Pesquero: Mar del Plata, Argentina, 2016; p. 12. Available online: https://www.researchgate.net/publication/308173455_Análisis_preliminar_de_la_temporada_de_pesca_de_centolla_patononica_Lithodes_santolla_2015-16 (accessed on 17 July 2022).

126. Militelli, M.I.; Firpo, C.; Rodrigues, K.A.; Macchi, G.J. Egg production and validation of clutch fullness indices scale of southern king crab, *Lithodes santolla*, in the Central Patagonian Sector, Argentina (44°–48° S). *Fish. Res.* **2018**, *211*, 40–45. [CrossRef]

127. Di Salvatore, P.; Gowland-Sainz, M.; Florentin, O.; Lovrich, G.A. Effects of fishery practices on fecundity of two lithodid crab species of commercial interest in Southern South America. *Fish. Res.* **2018**, *211*, 275–281. [CrossRef]

128. Dieckmann, U.; Heino, M. Probabilistic maturation reaction norms: Their history, strengths, and limitations. *Mar. Ecol. Prog. Ser.* **2007**, *335*, 253–269. [CrossRef]

129. De Roos, A.M.; Boukal, D.S.; Persson, L. Evolutionary regime shifts in age and size at maturation of exploited fish stocks. *Proc. R. Soc. B Boil. Sci.* **2006**, *273*, 1873–1880. [CrossRef]

130. Morgan, M.; Colbourne, E. Variation in maturity-at-age and size in three populations of American plaice. *ICES J. Mar.* **1999**, *56*, 673–688. [CrossRef]

131. Lloret, J.; Muñoz, M.; Casadevall, M. Threats posed by artisanal fisheries to the reproduction of coastal fish species in a Mediterranean marine protected area. *Estuar. Coast. Shelf Sci.* **2012**, *113*, 133–140. [CrossRef]

132. Musick, J.A.; Burgess, G.; Cailliet, G.; Camhi, M.; Fordham, S. Management of Sharks and Their Relatives (Elasmobranchii); Management of Sharks and Their Relatives (Elasmobranchii). *Fisheries*. **2000**, *25*, 9–13. [CrossRef]

133. Koslow, J.A.; Boehlert, G.W.; Gordon, J.D.M.; Haedrich, R.L.; Lorance, P.; Parin, N. Continental slope and deep-sea fisheries: Implications for a fragile ecosystem. *ICES J. Mar. Sci.* **2000**, *57*, 548–557. [CrossRef]

134. Gallagher, A.J.; Kyne, P.; Hammerschlag, N. Ecological risk assessment and its application to elasmobranch conservation and management. *J. Fish Biol.* **2012**, *80*, 1727–1748. [CrossRef] [PubMed]

135. Peeler, E.J.; Murray, A.G. Disease interaction between farmed and wild fish populations. *J. Fish Biol.* **2004**, *65*, 321–322. [CrossRef]

136. Hindar, K.; Ryman, N.; Utter, F. Genetic Effects of Cultured Fish on Natural Fish Populations. *Can. J. Fish. Aquat. Sci.* **1991**, *48*, 945–957. [CrossRef]

137. Servili, A.; Canario, A.; Mouchel, O.; Muñoz-Cueto, J.A. Climate change impacts on fish reproduction are mediated at multiple levels of the brain-pituitary-gonad axis. *Gen. Comp. Endocrinol.* **2020**, *291*, 113439. [CrossRef] [PubMed]

138. Tveiten, H. Temperature influence on reproductive development and gamete quality in Atlantic cod (*Gadus morhua*). *Cybium* **2008**, *32* (Suppl. 2), 195. [CrossRef]

139. Lahnsteiner, F.; Kletzl, M. The effect of water temperature on gamete maturation and gamete quality in the European grayling (*Thymalus thymallus*) based on experimental data and on data from wild populations. *Fish Physiol. Biochem.* **2011**, *38*, 455–467. [CrossRef]

140. Gillet, C. Egg production in an Arctic charr (*Salvelinus alpinus* L.) brood stock: Effects of temperature on the timing of spawning and the quality of eggs. *Aquat. Living Resour.* **1991**, *4*, 109–116. [CrossRef]

141. Gillet, C.; Breton, B.; Mikolajczyk, T.; Bodinier, P.; Fostier, A. Disruption of the secretion and action of 17,20β-dihydroxy-4-pregnen-3-one in response to a rise in temperature in the Arctic charr, *Salvelinus alpinus*. Consequences on oocyte maturation and ovulation. *Gen. Comp. Endocrinol.* **2011**, *172*, 392–399. [CrossRef] [PubMed]

142. Tveiten, H.; Johnsen, H.K. Thermal influences on temporal changes in plasma testosterone and oestradiol-17beta concentrations during gonadal recrudescence in female common wolffish. *J. Fish Biol.* **2001**, *59*, 175–178. [CrossRef]

143. Záhorská, E. Climate warming and invasive fish species: Will they replace native fish species in waters of temperate zones? *Biologia* **2016**, *71*, 727–735. [CrossRef]
144. Dijkstra, J.A.; Westerman, E.L.; Harris, L.G. Elevated seasonal temperatures eliminate thermal barriers of reproduction of a dominant invasive species: A community state change for northern communities? *Divers. Distrib.* **2017**, *23*, 1182–1192. [CrossRef]

145. Guiguen, Y.; Fostier, A.; Piferrer, F.; Chang, C.-F. Ovarian aromatase and estrogens: A pivotal role for gonadal sex differentiation and sex change in fish. *Gen. Comp. Endocrinol.* **2010**, *165*, 352–366. [CrossRef] [PubMed]

146. Pankhurst, N.W.; Munday, P.L. Effects of climate change on fish reproduction and early life history stages. *Mar. Freshw. Res.* **2011**, *62*, 1015–1026. [CrossRef]

147. Canales, C.M.; Adasme, N.A.; Cubillos, L.; Cuevas, M.J.; Sánchez, N.E. Variaciones en rasgos reproductivos de pequeños pelágicos conducidos por variables ambientales: El caso de *E. ringens* en Chile. In *Actas del IV Simposio Iberoamericano de Ecología Reproductiva, Reclutamiento y Pesquerías*; Iquique, Chile, 2018; p. 76. Available online: https://www.researchgate.net/publication/360702639_Actas_del_IV_Simposio_Iberoamericano_de_Ecologia_Reproductiva-Reclutamiento_y_Pesquerias (accessed on 17 July 2022).

148. Miranda, L.A.; Chalde, T.; Elisio, M.; Strüssmann, C.A. Effects of global warming on fish reproductive endocrine axis, with special emphasis in pejerrey *Odontesthes bonariensis*. *Gen. Comp. Endocrinol.* **2013**, *192*, 45–54. [CrossRef] [PubMed]

149. Perry, A.L.; Low, P.J.; Ellis, J.R.; Reynolds, J.D. Climate Change and Distribution Shifts in Marine Fishes. *Science* **2005**, *308*, 1912–1915. [CrossRef] [PubMed]

150. Baudron, A.R.; Brunel, T.; Blanchet, M.; Hidalgo, M.; Chust, G.; Brown, E.J.; Kleisner, K.M.; Millar, C.; MacKenzie, B.R.; Nikolioudakis, N.; et al. Changing fish distributions challenge the effective management of European fisheries. *Ecography* **2020**, *43*, 494–505. [CrossRef]

151. Last, P.R.; White, W.T.; Gledhill, D.C.; Hobday, A.J.; Brown, R.; Edgar, G.J.; Pecl, G. Long-term shifts in abundance and distribution of a temperate fish fauna: A response to climate change and fishing practices. *Glob. Ecol. Biogeogr.* **2010**, *20*, 58–72. [CrossRef]

152. Bond, N.; Thomson, J.; Reich, P.; Stein, J. Using species distribution models to infer potential climate change-induced range shifts of freshwater fish in south-eastern Australia. *Mar. Freshw. Res.* **2011**, *62*, 1043–1061. [CrossRef]

153. Comte, L.; Grenouillet, G. Distribution shifts of freshwater fish under a variable climate: Comparing climatic, bioclimatic and biotic velocities. *Divers. Distrib.* **2015**, *21*, 1014–1026. [CrossRef]

154. Wingfield, J.C.; Sapolsky, R.M. Reproduction and Resistance to Stress: When and How. *J. Neuroendocr.* **2003**, *15*, 711–724. [CrossRef] [PubMed]

155. Trippel, E.A.; Kjesbu, O.S.; Solemdal, P. Effects of Adult Age and Size Structure on Reproductive Output in Marine Fishes. In *Early Life History and Recruitment in Fish Populations*; Chambers, R.C., Trippel, E.A., Eds.; Chapman & Hall Fish and Fisheries Series; Springer: Dordrecht, The Netherlands, 1997; Volume 21, pp. 31–62. [CrossRef]

156. Moresino, R.D.H.; Gonçalves, R.J.; Helbling, E.W. Direct and indirect acquisition of photoprotective compounds in crab larvae of coastal Patagonia (Argentina). *J. Plankton Res.* **2014**, *36*, 877–882. [CrossRef]

157. Rodrigues, K.A.; Leonarduzzi, E.; Macchi, G.J.; Militelli, M.I. Maternal condition, fecundity and oocyte quality of Argentine hake (*Merluccius hubbsi*) from the Northern stock. *Fish. Res.* **2018**, *197*, 105–112. [CrossRef]

158. Wang, S.Y.; Lau, K.; Lai, K.-P.; Zhang, J.; Tse, A.C.-K.; Li, J.-W.; Tong, Y.; Chan, T.; Wong, C.K.-C.; Chiu, J.M.-Y.; et al. Hypoxia causes transgenerational impairments in reproduction of fish. *Nat. Commun.* **2016**, *7*, 12114. [CrossRef]

159. Lowerre-Barbieri, S.; DeCelles, G.; Pepin, P.; Catalán, I.; Muhling, B.; Erisman, B.; Cadrin, S.X.; Alós, J.; Ospina-Alvarez, A.; Stachura, M.M.; et al. Reproductive resilience: A paradigm shift in understanding spawner-recruit systems in exploited marine fish. *Fish Fish.* **2016**, *18*, 285–312. [CrossRef]

160. Byrne, M.; Foo, S.A.; Ross, P.M.; Putnam, H.M. Limitations of cross- and multigenerational plasticity for marine invertebrates faced with global climate change. *Glob. Chang. Biol.* **2019**, *26*, 80–102. [CrossRef] [PubMed]