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Introduction
Reproductive strategies aim to optimize the production of reproductively capable offspring in relation to the energy available in the environment to ensure the species’ survival over time (Roff 1992, Muchlisin 2014). These strategies are therefore crucial because they determine the ability of newborn individuals to enter the future population (Stearns 1976, Wootton 1984, Roff 1992, Pianka 2000).
Batoids are a group of cartilaginous fish that are characterized by 2 main reproductive modes (based on gestation site): oviparity and viviparity (Wourms and Demski 1993). Viviparity has been considered the most evolved and advantageous reproductive mode (Wourms and Lombardi 1992) because it increases the probability of neonate survival through nutrition provided by the mother and, with decreased fecundity, it allows for larger sizes at birth (Shine 1989, Clutton-Brock 1991, Roff 1992). This reproductive mode is present in the 4 batoid orders, and only the Rajidae family is oviparous (Musick and Ellis 2005). In viviparous batoids there are only 2 reproductive modes based on fetal nutrition (Wourms 1981), viviparous with yolk sac and definitive lipid histotrophy (Musick and Ellis 2005).
The energy distribution patterns during reproduction are related to the life history strategy of the species (Frisk and Miller 2009). Considering that viviparity is selectively more advantageous, it could be inferred that this reproductive mode requires more energy investment into the offspring, thus ensuring their survival. Acuña et al. (2001) proposed several indicators to evaluate reproductive effort, which is defined as the portion of total energy that an organism invests in reproductive processes to ensure fertile offspring (Thompson 1984). According to Acuña et al. (2001), 2 main parameters have to be evaluated: fecundity, which accounts for the contribution of new individuals to the next generation (Charlesworth 1994), and offspring mass, which allows for the comparison of energy investment by cohorts. The potential rate of population increase (rʹ), which uses survival and reproduction data such as age at maturity and fecundity, is likewise an effective measure to evaluate the productivity of fish populations. The rate of population increase is also useful for comparing how fish populations respond to exploitation (Jennings et al. 1998, Frisk et al. 2001).
The giant electric ray,Narcine entemedor(Torpediniformes), and the Pacific cownose ray,Rhinoptera steindachneri(Myliobatiformes), are 2 sympatric batoid species distributed in La Paz Bay (Baja California Sur, Mexico), southern Gulf of California, on the Pacific coast of Mexico. Both species are frequently captured by fisheries in the Mexican northwest region. In the Gulf of California, the number ofN. entemedorcatches declined in the period from 1997 to 2014 (Saldaña-Ruiz 2016). In addition, recently, the International Union for Conservation of Nature (IUCN) classified the species as Vulnerable (Pollom et al. 2020a). On the other hand,R. steindachneriis one of 5 species comprising more than 80% of the current catches in the Gulf of California and is listed as Near Threatened by the IUCN (Pollom et al. 2020b).
Despite the data available on the fishing effort to whichN. entemedorandR. steindachneriare subjected and the IUCN’s recent update on their conservation statuses, information on their reproductive characteristics, life history, fishing dynamics, and conservation is limited (Villavicencio-Garayzar 2000, Márquez-Farías 2002, Bizzarro et al. 2007, Burgos-Vázquez et al. 2017, Burgos-Vázquez et al. 2018, Jiménez-García 2020, Carrillo-Colin 2021). Consequently, their vulnerability to commercial fishing is unknown. Some data on the species’ age, growth, reproductive characteristics, and demographics are available (Villavicencio-Garayzar 2000, Márquez-Farías 2002, Bizzarro et al. 2007, Burgos-Vázquez et al. 2017, Burgos-Vázquez et al. 2018, Carrillo-Colin et al. 2021), allowing researchers to make inferences about the species’ susceptibility to overexploitation. Therefore, this study aims to evaluate the reproductive potential andrʹ, as well as contrasting the reproductive strategy, to infer, with limited data, how susceptible these 2 batoid species are to fishing exploitation.
Materials and methods
Indicators of reproductive potential
The information for this research was derived from project SEP-CONACYT 180894, which included monthly collections made from 2013 to 2018 by artisanal fishermen from La Paz Bay, Baja California Sur, Pacific coast of Mexico (Fig. 1).
Figure 1. Studyarea (Gulf of California and La Paz Bay) where the samples ofNarcine entemedorandRhinoptera steindachneriwere collected from 2013 to 2018.
To evaluate the reproductive potential ofN. entemedorandR. steindachneri, a total of 21 indicators were estimated using the method first proposed by Vooren (1992) and later modified by Acuña et al. (2001). These indicators were divided into 2 groups according to the data’s origin: those dependent on fecundity and those dependent on mass (as indicated in Table 1). The maximum age (indicator A2) ofN. entemedorwas taken from Mora-Zamacona et al. (2022), while the A2 ofR. steindachneriwas taken from Pabón-Aldana (2016).
Table 1. Comparison of reproductive potential indicators based on
fecundity and mass amongNarcine
entemedor(
),Rhinoptera steindachneri(
), and the
optimal indicator (OI) qualitative rating for each indicator
according to the life-history traits that make a population less
vulnerable to fishing exploitation conditions, as proposed by Holden (1974), Walker and Hislop (1998), Musick (1999), Dulvy et al. (2000), Stevens et al. (2000), and
Cailliet (2015).
| Indicator | Definition/estimation | Narcine entemedor | Rhinoptera steindachneri | OI | Species closest to the OI |
| Fecundity | |||||
| A1: age at first maturity (years) | Age of the youngest mature organism | 2.8 | 1.7 | Low |
|
| A2: maximum age (years) | Maximum age recorded | 14.0 | 9.8 | Low |
|
| W1: average mass (eviscerated, g) | Average mass of all eviscerated females | 2,709.0 | 3,737.1 | Low |
|
| W2: maximum eviscerated mass (g) | Maximum eviscerated mass recorded | 5,200.0 | 12,900.0 | Low |
|
| R1: duration of the reproductive cycle (years) | Beginning of follicular development until birth | 1.0 | 1.0 | Short |
|
| R2: duration of the reproductive life (years) | A2 - A1 | 11.2 | 8.1 | Short |
|
| An1: average number of embryos (embryos per litter per year) | Average fecundity | 8.0 | 1.0 | High |
|
| Ap2: annual production of offspring (embryos per litter per year) | A1/R1 | 8.7 | 1.1 | High |
|
| No3: number of offspring accumulated during the period of reproductive activity (annual production of offspring in the reproductive life cycle) | R2 × Ap2 | 104.4 | 8.8 | High |
|
| Mass | |||||
| W3: mass at first maturity (g) | Mass of the smallest mature organism | 1,710.0 | 3,900.0 | Low |
|
| W4: average mass of embryos to term (g) | Average mass of embryos in the “late” stage | 36.5 | 841.0 | Low |
|
| W5: average litter mass (g) | W4 × Ap1 | 291.0 | 841.0 | Low |
|
| W6: annual mass of juvenile production (g) | W4 × Ap2 | 317.5 | 917.5 | High |
|
| W7: growth during the life phase of reproductive activity (g) | W2 - W3 | 3,490.0 | 9,000.0 | High |
|
| W8: accumulated mass of the progeny (g·y-1) | R2 × W6 | 3,809.6 | 7,422.2 | Low |
|
| Rwlitter: relative production of litter biomass per cycle (g·y-1) | W5/W6 | 0.9 | 0.9 | Low |
|
| Rwyear: relative annual biomass production (g·y-1) | W6/W1 | 0.1 | 0.2 | High |
|
| Rwbirth: relative body mass at birth (g) | W4/W1 | 0.0 | 0.2 | Low |
|
| RB1: relative production of biomass during the reproductive phase of life (g·y-1) | (W7 + W8)/W3 | 4.3 | 4.2 | Low |
|
| RB2: relative production of body mass during the reproductive phase of life (g·y-1) | W7/W3 | 2.0 | 2.3 | High |
|
| RB3: relative production of the litter mass during the reproductive phase of life (g·y-1) | W8/W3 | 2.2 | 1.9 | Low |
|
To evaluate the indicators based on embryonic information, we used only embryos in the “late” stage. The late-stage embryos ofN. entemedorwere defined using Burgos-Vázquez et al.’s (2017) criteria, and the late-stage embryos ofR. steindachneriwere defined using the Burgos-Vázquez et al.’s (2018) criteria. The average embryo mass to term (late-stage embryos, indicator W4), age at first maturity (A1), the median age at maturity (A50), and the median age at pregnancy (AP50) were estimated with the biological data derived from Project SEP-CONACYT 180894. Indicator W4 was estimated using the average mass of 77 embryos ofN. entemedor(mass: 21.3-47.7 g) and 37 embryos ofR. steindachneri(mass: 723.0- 912.0 g).
For the A1 and A50estimations, a total of 230N. entemedorfemales were used, and they were distinguished as mature or immature following that proposed by Burgos-Vázquez et al. (2017). In the case ofR. steindachneri, 150 females were evaluated, differentiating maturity according to that proposed by Burgos-Vázquez et al. (2018). The estimate of A1 was made on the basis of the age of the youngest recorded female. For the AP50estimation, 64 females ofN. entemedorand 15 females ofR. steindachneriin the pregnancy stage were evaluated. A50and AP50were calculated using a binomial logistic model (0: immature individuals/females without eggs or embryos in the uterus; 1: mature individuals/females with eggs or embryos in the uterus) in MATLAB r2015a.
The indicators based on fecundity and mass were average mass (W1), maximum eviscerated mass (W2), duration of the reproductive cycle (R1), duration of the reproductive life (R2), average number of embryos (An1), annual production of offspring (Ap2), number of offspring accumulated during the period of reproductive activity (No3), mass at first maturity (W3), average litter mass (W5), annual mass of juvenile production (W6), growth during the life phase of reproductive activity (W7), accumulated mass of the progeny (W8), relative production of litter biomass per cycle (Rwlitter), relative annual biomass production (Rwyear), relative body mass at birth (Rwbirth), relative production of biomass during the reproductive phase of life (RB1), relative production of body mass during the reproductive phase of life (RB2), and relative production of the litter mass during the reproductive phase of life (RB3). They were estimated using the information proposed by Burgos-Vázquez et al. (2017) forN. entemedorand by Burgos-Vázquez et al. (2018) forR. steindachneri.
Comparisons between reproductive traits
To compare the reproductive potential betweenN. entemedorandR. steindachneri, a qualitative rating, called optimal indicator (OI), was assigned as low, high, or short. OIs were assigned on the basis of the life history traits that make a species either more or less vulnerable to overexploitation by fishing, considering that proposed by Holden (1974), Walker and Hislop (1998), Musick (1999), Dulvy et al. (2000), Stevens et al. (2000), and Cailliet (2015) (Table 1). Since large bodies, late maturity, high longevity, long reproductive cycles, high energy demand for reproduction, and low fecundities are traits that make organisms more sensitive to fishing mortality, each evaluated trait was designated as OI when it presented values or characteristics that were different from those of these traits sensitive to overfishing, for example low A1, high fecundity, or short reproductive cycle.
The proportion of A1, A50, and AP50, with respect to the A2 of each species, was evaluated.
Potential rate of population increase
As part of the evaluation and comparison of the reproductive potential ofN. entemedorandR. steindachneri, we used therʹ proposed by Jennings et al. (1998). According to Jennings et al. (1998),rʹ can be used as a measure of the ability of a population to compensate for exploitation. Comparisons between both species were carried out with the assumption that lowrʹ values were associated with a decrease in abundance caused by fishing (Frisk et al. 2001).
Results
In total, 21 indicators of the reproductive potential ofN. entemedorandR. steindachneriwere evaluated.Narcine entemedorpresented 11 OIs (W1, W2, An1, Ap2, No3, W3, W4, W5, W8, Rwbirth, and RB3), andR. steindachneripresented 8 (A1, A2, R2, W6, W7, Rwyear, RB1, and RB2). The rest of the indicators (R1 and Rwlitter) were tied for both species. Regarding fecundity and mass, of the 2 species,N. entemedorpresented more indicators close to the OI related to fecundity (N. entemedor: 5;R. steindachneri: 3; both: 1) and mass (N. entemedor: 6;R. steindachneri: 5; both: 1) (Table 1).
A1 was lower inR. steindachneri, and A2 was higher inN. entemedor. W1 and W2 were higher forR. steindachneri. R1 for both species was approximately 1.0 y; however, R2 forN. entemedorwas 4.0 y longer, at approximately 12.0 y, while R2 forR. steindachneriwas approximately 8.1 y. This difference is due to the divergence in the A2 of both species (Table 1).
Narcine entemedorshowed a higher An1 (8 embryos/female) compared toR. steindachneri(1 embryo/female). Consequently, Ap2 and No3 were higher inN. entemedor. On the other hand, W3, W4, W5, W6, W7, and W8 were higher inR. steindachneri.
Rwlitterwas the same for both species (average fecundity: 0.9), but Rwyearand Rwbirthwere higher inR. steindachneri. RB1, RB2, and RB3 were similar between the 2 species (Table 1).
Females of both species showed a similar A1 relative to A2 (Fig. 2). The A50inN. entemedorfemales was estimated at 5.1 y (95% CI: 3.5-6.7, Fig. 3a), whereas the A50inR. steindachnerifemales was estimated at 3.8 y (95% CI: 1.6-5.9, Fig. 3a). The AP50values forN. entemedorandR. steindachneriwere estimated at 6.8 y (5.3-8.3 and 5.0-8.6, respectively; Fig. 3b, Table 1). The proportions of A50relative to A2 for both species were similar, while AP50was higher inR. steindachneri(Fig. 2).Therʹ value was higher inN. entemedor(0.48) than inR. steindachneri(-0.18).
Figure 2. Proportion of maximum age (A2), age at first maturity (A1), median age at maturity (A50), and median age at pregnancy (AP50) forNarcine entemedorandRhinoptera steindachneri.
Discussion
This is the first study evaluating the reproductive potential ofN. entemedorandR. steindachneri, which is useful for comparing the energetic cost for each species in terms of reproduction (Vooren 1992). Our analysis represents an approximate inference about the vulnerability of these 2 batoid species, which are frequently captured in the southern Gulf of California and for whom there is insufficient information on their population parameters. Because of this insufficient information, we cannot develop complex fishing models to predict population trends.
The reproductive potential regarding fecundity inN. entemedorhad more indicators close to the OI (55.6%) compared toR. steindachneri. Therefore, it is likely thatN. entemedorinvests more energy in reproduction in terms of increasing offspring size. Still,N. entemedoroffspring are smaller thanR. steindachnerioffspring. It can be observed, for example, that Ap2 was 8 times higher forN. entemedorthan forR. steindachneri, and No3 was 96 times higher. Because both indicators use the duration of the reproductive cycle and the percentage of litters for that time, our analyses confirm that high fecundity and embryonic diapause (Burgos-Vázquez et al. 2017) are advantages that improve the reproductive effort inN. entemedor. Because of the small size at birth ofN. entemedor, this species is likely to present a trade-off between fecundity and size at birth, investing a large portion of its energy in increasing the litter number but not body size.
In terms of the reproductive potential regarding mass,R. steindachnerishowed 50% of the total indicators closest to the OI, andN. entemedorshowed about 58.3% of the total indicators closest to the OI. According to Roff (1992) and Haag (2013), the method for evaluating reproductive effort using body mass is an adequate proxy for estimating the energy invested in reproduction; however, it can be biased, mainly because it considers the energy destined to produce body mass, gonadic mass, and embryonic mass.Rhinoptera steindachnericompensates low fecundity with energy investment in embryonic development. Thus, reproductive effort is likely higher inR. steindachnericompared toN. entemedorbecause of the reproductive mode (embryonic nutrition: definitive lipid histotrophy). Therefore, a trade-off between energy investment in embryonic development and fecundity is likely to occur in this species. However, the high energy demand for reproduction could affect the maintenance of the population in the event of overfishing (Cortés 2000, Dulvy et al. 2014).
The main reproductive difference betweenN. entemedorandR. steindachneriis the mode in which the mother nourishes the embryos. WhereasN. entemedorshows limited histotrophy (Burgos-Vázquez et al. 2017) with low nutritional input (mucoproteins) from the mother to the embryo (Hamlett et al. 2005, Musick and Ellis 2005),R. steindachneripresents matrotrophy with definitive lipidic histotrophy (Hamlett et al. 2005, Musick and Ellis 2005), where the embryos are nourished mostly with the nutrients produced and secreted by the mother, at least by the “mid” stage of embryonic development (Burgos-Vázquez et al. 2018).Rhinoptera steindachneriinvests more energy in embryonic nutrition by producing the vitelline reserve, along with the production and secretion of uterine milk (Wallace 1978, Wallace and Selman 1981, Wourms 1981, Wourms and Lombardi 1992). Thus,N. entemedorcould have the advantage of requiring less energy for embryonic development, but matrotrophy allowsR. steindachnerito produce larger and more developed offspring that have higher probability of survival (Wourms 1981, Qualls and Shine 1995, Goodwin et al. 2002).
According to Frisk et al. (2001) and Frisk (2010), the difference between age at maturity and maximum age represents the portion of time that the organism will invest in reproduction. Both species invest the relatively same amount of time in their reproductive activities (the A1 to A2 ratio equals 0.36 forN. entemedorand 0.39 forR. steindachneri), and it appears that they have relatively early ages at maturity.Rhinoptera steindachnerihad a higher proportion (0.7) of age at pregnancy compared toN. entemedor(0.5), which may be related to the reproductive mode, whereR. steindachneriprobably needs more time to develop a larger abdominal cavity to carry a single large embryo.
Frisk et al. (2001) usedrʹ to evaluate the response of some elasmobranch species to exploitation and compared it with the values obtained by Jennings et al. (1998). Both studies associated the lowrʹ values with populations that were declining due to fishing exploitation. In the present study,N. entemedorshowed a highrʹ value (0.48), whileR. steindachneripresented a very low value (-0.18). Compared to other elasmobranch species,N. entemedorshows one of the highestrʹ values, only after the bonnethead shark,Sphyrna tiburo(rʹ = 0.60), which has an earlier maturity age, and the skateLeucoraja erinacea(rʹ = 0.68), which shows a fecundity of 30 capsules/year (6 embryos more per year thanN. entemedor) (Frisk et al. 2001). Furthermore, therʹ value forAmblyraja radiata(rʹ = 0.43) is similar to the one found inN. entemedor, given the similarity in age at maturity and fecundity (Frisk et al. 2001).
The negativerʹ value forR. steindachnericould be affected by fecundity, which is one of the lowest among the elasmobranchs (1 embryo/female; Frisk et al. 2001, Burgos-Vázquez et al. 2018). In their study, Frisk et al. (2001) did not include species with fecundity values of 1 embryo/female; the species with the lowest fecundity wasCarcharias taurus(2 embryos/female), which had an age at maturity of 7 y andrʹ < 0.001. Due to its low fecundity and relative early A1,R. steindachneri, is less productive thanN. entemedor, and it probably has lower capacity to recover from overexploitation by fishing. Lowrʹ values have also been associated with species that have large body sizes, late maturity, and low growth rates. Moreover, these species appear to be more susceptible to population decline due to overexploitation by fishing (Frisk et al. 2001, Frisk and Miller 2009).
According to the reproductive indicators, characteristics, andrʹ value evaluated in the current study, when compared to other elasmobranchs,N. entemedorcan be deemed a species with a relatively early A1, high reproductive effort dependent on fecundity, and high capacity to compensate for overexploitation by fishing. On the other hand, when compared to other elasmobranchs,R. steindachneriis a species with early A1, high reproductive effort dependent on embryonic mass, and low ability to compensate for overexploitation by fishing. The low fecundity value forR. steindachneriis related to the lowrʹ values, indicating thatR. steindachneriwould be more vulnerable to overexploitation by fishing (Jennings et al. 1998, Frisk et al. 2001). Both species have relatively high reproductive potential (i.e.,N. entemedorthrough fecundity andR. steindachnerithrough embryonic mass). However,N. entemedorshowed the highestrʹ values; therefore, it could be deemed more resilient to environmental disturbances and fishing susceptibility.
In Mexico, the main problem in analyzing the fishery dynamics of a batoid species is that fishing records do not include the scientific names of species or species are poorly identified, which could lead to erroneous information for management. For this reason, it is very difficult to carry out robust analyses of population trends and establish adequate management plans. A susceptibility characteristic ofN. entemedoris that it is marketed as a shark species and there is therefore no specific information about its fishery. In the case ofR. steindachneri, it is a species that forms schools (Bizzarro et al. 2007), which makes it more susceptible to being trapped in large numbers. Additionally, it has low fecundity. Our main recommendation is to use this methodology for species with nil information on catch series, abundances, or demographic data to create a purely precautionary management plan.
