Fieldwork

For the present study, from to 2010 at 2012, technical personnel from ICMyL, UNAM, sampled Penaeus setiferus and P. duorarum postlarvae in the Puerto Real Inlet (18°46′46.40″N, 91°30′1.55″W) located in Términos Lagoon, México (Fig. 1). For catching post-larvae, a special device was used, and it incorporated three CALCOFI trapeze-type nets placed on the surface (1 m), at mid-water (4 m), and the bottom (9 m). Each net has a 50 cm mouth diameter, 1.5 m total length, and a 505 μm mesh size (^{Flores-Coto & Zavala-García, 1994}). The device was placed with ballast at the bottom of the lagoon and secured to one of the Puerto Real bridge columns via parallel cables. In the field, collected postlarvae were preserved in 4% formalin (neutralized with sodium borate).

Figure 1 The geographical location of Términos Lagoon. Campeche Bank sector (grey area), a) Palizada, b) Chumpam and c) Candelaria rivers. Single sampling station (black point). 

Reproductive seasons

In the laboratory, postlarvae were transferred to bottles with 70% alcohol. According to ^{Ringo & Zamora (1968)} and ^{Subrahmanyam (1971)}, postlarvae were separated and identified as P. setiferus or P. duorarum. For the three depth levels, postlarvae density was estimated × 100 m³ of filtered water (Table 1). This information was used to establish the total postlarvae density that entered monthly into Términos Lagoon. Based on this information, the two-time series was composed, and named P. setiferus postlarvae density (Ps) and P. duorarum postlarvae density (Pd), respectively.

The mentioned time series were analyzed via the CENSUS method in order to estimate the harmonic pattern variation (HPV) (referred to as the seasonal factor in Statistica 7.0 software) (^{Cervantes-Hernández et al., 2016}). HPV is a mathematical application used to detect, from Ps and Pd time series, monthly cyclical anomalies of equal magnitudes (cycle height) and amplitudes (cycle width). These monthly cyclical anomalies can be positive or negative, with the zero value as the midpoint of change. Positive cyclical anomalies represented the increases in postlarvae entrance into Términos Lagoon, and negative cyclical anomalies represented the decreases. The positive cyclical anomalies were explicitly used to describe when postlarvae started to arrive, reached their maximum density, and finished entering Términos Lagoon. In this study, HPV were named as follows: HPV-Ps for P. setiferus postlarvae density and HPV-Pd for P. duorarum postlarvae density.

Hydrologic information

During the postlarvae sampling in Puerto Real Inlet, monthly salinity and lagoon water temperatures were recorded at the three depth levels. Additionally, we used fluvial discharge records from the Candelaria, Chumpan, and Palizada rivers (in m³ s^-1) provided by the Government Agency CONAGUA in Campeche State.

The salinity and the lagoon water temperature were averaged monthly, considering the three depth levels. With that information and the monthly accumulate fluvial discharge, three-time series were composed. Each time series was analyzed via the Census method to estimate their corresponding HPV. The increases in salinity, lagoon water temperature and accumulate fluvial discharge were represented by positive cyclical anomalies. Additionally, the respective decreases were represented by negative cyclical anomalies. The positive cyclical anomalies were specifically used to describe internal lagoon conditions during the entrance of shrimp postlarvae.

In this study, the aforementioned HPV were named as the following: HPV-salinity, HPV-lagoon water temperature, and HPV-accumulate fluvial discharge, respectively.

Multiple correlations

Once HPV-Ps and HPV-Pd were estimated, a complete postlarvae entrance cycle was identified and taken as reference to explain the other found cycles in the study period. The cycle of reference was divided into two sections. The first section was established from initial to maximum postlarvae entrance the first postlarvae entrance episode, and the second section was established from after maximum until the end of the postlarvae entrance the second postlarvae entrance episode. Finally, for each postlarvae entrance episode, the following HPV time series were statistically correlated: Ps, Pd, salinity, lagoon water temperature and accumulate fluvial discharge. The Statistica 7.0 software performed the correlation process.

Reproductive seasons and postlarvae entrance

In average, the positive cyclical anomalies of the HPVPs and HPV-Pd showed that Penaeus setiferus and P. duorarum postlarvae entered Términos Lagoon annually from June to September, with the highest density of postlarvae entrance occurring in August (Fig. 2). The corresponding negative cyclical anomalies showed that each year postlarvae entrance decreased from October to May, and the lowest density of postlarvae entrance was recorded during March (Fig. 2).

Figure 2 Harmonic pattern variations (HPV) of Penaeus setiferus postlarvae density (HPV-Ps, discontinuous line) and P. duorarum postlarvae density (HPV-Pd, black line). The estimated range for positive cyclical anomalies was from 1 to 440, and in the case of negative cyclical anomalies, it was between −1 and −110: the first postlarvae entrance episode (a) and the second postlarvae entrance episode (b). 

For both shrimp species, the first postlarvae entrance cycle was used as reference, and this was divided into two sections from June to August (the first postlarvae entrance episode), and the complete month of September (the first postlarvae entrance episode) (Fig. 2). The aforementioned was equally taken into account for other found years.

An analysis more detail on the positive cyclical anomalies of the HPV-Ps and HPV-Pd signals suggests that both species of shrimp postlarvae did not enter lagoon environment at the same time. In the case of P. setiferus, its postlarvae entered from early June to late September. In the case of P. duorarum, its postlarvae entered from middle June to middle September. So, it was detected that there is a difference of 15 days between the postlarvae entrance of both shrimp species (Fig. 2).

Hydrologic information

Estimated hydrologic HPV time series are shown in Figure 3.

Figure 3 Harmonic pattern variations (HPV) for salinity (continuous gray line), lagoon water temperature (discontinuous gray line) and accumulate fluvial discharge (black line). The estimated range for positive cyclical anomalies was from 1 to 9, and in the case of negative cyclical anomalies, it was between −1 and −9. 

A highest postlarvae density on entrance into Términos Lagoon during was recorded during the first episodes (Table 1, Fig. 2). In this case, prevalent hydrologic lagoon conditions were high salinity (34), a warm lagoon temperature (30°C), and low accumulate fluvial discharge (2,828 m³ s^-1) (Table 1, Fig. 3).

A lowest postlarvae density on entrance into Términos Lagoon was recorded during the second episode (Table 1, Fig. 2). In this case, prevalent hydrologic lagoon conditions were low salinity (28), a moderately warm lagoon temperature (29°C), and high accumulate fluvial discharge (3,934 m³ s^-1) (Table 1, Fig. 3).

Muliple correlations between the HPV time series

In the first postlarvae entrance episode, Ps and Pd showed direct correlations with salinity (r = 0.46 and r = 0.86, respectively), lagoon water temperature (r = 0.90 and r = 0.99, respectively) and accumulate fluvial discharge (r = 0.38 and r = 0.82, respectively). All correlation cases resulted statistical not significance (P > 0.05). Additionally, Ps and Pd showed direct correlation (r = 0.84, P > 0.05).

In the second postlarvae entrance episode, Ps and Pd showed inverse correlations with salinity (r = −0.99 (P < 0.05) and r = −0.76 (P > 0.05), respectively), lagoon water temperature (r = −0.99 and r = −0.77, respectively, P > 0.05), and accumulate fluvial discharge (r = −0.72 (P > 0.05) and r = −0.99 (P < 0.05), respectively). Additionally, Ps and Pd showed direct correlation (r = 0.71, P > 0.05).

The first postlarvae entrance episode

In complementary studies conducted in Términos Lagoon, ^{Flores-Coto et al. (2018)} and ^{Gómez-Ponce et al. (2018)}, again documented the first postlarvae entrance episode mentioned by ^{Gracia & Soto (1990)}. These authors implemented nine months of sampling (between March and November 2010 and 2013, respectively), and they documented maximum P. setiferus and P. duorarum postlarvae entrance in June and in September 2013. Between those particular studies, the most significant differences were found for P. setiferus and P. duorarum postlarvae entrance dates, and these differences were partially explained concerning changes lagoon water temperature. ^{Flores-Coto et al. (2018)} and ^{Gómez-Ponce et al. (2018)} concluded that most postlarvae entrance occurs from June to September (during the rainy season) when the lagoon water temperature is warm. Also, these authors mentioned that during the rest of the year, postlarvae entrance is reduced (from October to May).

In the present study, problems identifying entrance dates for the maximum entry influx of P. setiferus and P. duorarum postlarvae were solved via HPV-Ps and HPV-Pd signals. Results showed that the entrance of P. setiferus and P. duorarum postlarvae into Términos Lagoon occurs from June to September (during the rainy season), with maximum postlarvae entrance occurring in August (Fig. 2). Additionally, postlarvae entrance decreased from October to May, and the lowest signal was recorded during March (Fig. 2). It was concluded that the annual cycleof postlarvae entrance is similar for both shrimp species, but itis important to recognize that a difference of 15 days was recorded in their arrival dates (Fig. 2).

When a complete postlarvae entrance cycle was divided into two sections, it was found that postlarvae entrance kept increasing while prevalent hydrological conditions were high salinity (34), a warm lagoon temperature (30°C), and low accumulate fluvial discharge inside Términos Lagoon (2,828 m³ s^-1) because the rainy season is just beginning (Table 1, Fig. 3). After September, postlarvae entrance decreased when prevalent hydrological conditions were low salinity (28), a moderately warm lagoon temperature (29°C) and high accumulate fluvial discharge (3,934 m³ s^-1) because the rainy season ends, but the river discharge from the rivers continues due to runoff (Table 1, Fig. 3).

In contrast to our study, in the available literature, divisions of a complete postlarvae entrance cycle were not taken into account. For this reason, there was confusion in documenting correlations between postlarvae entrance, salinity and lagoon water temperature. Regarding salinity, ^{Flores-Coto et al. (2018)} and ^{Gómez-Ponce et al. (2018)} did not establish conclusions. Finally, adverse to our results, they mentioned that postlarvae entrance should increase during seasonal periods of low salinity. ^{Gracia & Soto (1990)} indicated that most postlarvae entrance occurs between salinities of 22 and 34. Regarding lagoon water temperature, ^{Gómez-Ponce et al. (2018)} indicated that most postlarvae entrance occurs between 28.3 and 28.7°C, while ^{Flores-Coto et al. (2018)} documented it from 29.7 to 30.8°C. ^{Gracia & Soto (1990)} reported lagoon water temperature results similar to those obtained in this study.

It should be taken into account that in Términos Lagoon, the second postlarvae entrance episode spawned in prevalent hydrological conditions: low salinity, a warm lagoon temperature and high accumulate fluvial discharge (Fig. 3). These hydro-logical conditions did not favor shrimp postlarvae entrance into lagoon systems (Figs. 2–3). According to the available bibliography (^{Cervantes-Hernández, 1999}, ²⁰¹⁵; ^{Ramírez-Rodríguez et al., 2006}; ^{Cervantes-Hernández et al., 2012}, ²⁰¹⁷), these hydrological conditions are better at stimulating “lagoon recruitment” or the natural movement of shrimp postlarvae from the marine environment towards lagoon systems. For this reason, it should not be confused in which hydrological conditions lagoon recruitment occurs, and in which hydrological conditions immense postlarvae entrance occurs. Finally, in Términos Lagoon, the first postlarvae entrance episodes spawned in prevalent hydrological conditions: high salinity, warm lagoon temperature (^{Gracia & Soto, 1990}; ^{Flores-Coto et al., 2018}) and low accumulate fluvial discharge (Fig. 3).

Marine spawner abundance changes

As established, ^{Gracia & Soto (1990)} reported a higher abundance of P. setiferus spawners in the Campeche Bank sector from October to February. Before 1993 it was similarly reported for P. duorarum (^{Cervantes-Hernández & Gracia, 2011}) and P. aztecus in the Madre Lagoon, Tamaulipas-Veracruz sector, México (^{Cervantes-Hernández, 2015}) (Fig. 4). In this last sector, studies on postlarvae entrance are not documented. For Campeche Bank sector reports on the winter presence of P. setiferus and P. duorarum, postlarvae cohorts were not found. In this study, we did not detect a cycle winter cycle.

In conclusion, it was demonstrated that postlarvae abundance did not occur in the season of maximum reproduction (winter months of December 2011 and January-February 2012) for both shrimp species. These were the fishing seasons. To explain this, we took into account the available literature and suggested the following explanation. Since 1993, after implementation of closure seasons throughout the Gulf of México, fishing seasons have been mainly implemented from November/October to May (SAGARPAINP, 2012) (Fig. 4) and during this time fishing efforts quickly reduce shrimp spawner abundance in marine environments. Then as an immediate result, shrimp postlarvae abundance abruptly declines. So, the indicating signal of reproductive activity that we associate with postlarvae entrance became a weak undetectable signal inside Términos Lagoon. As was established in this study, the opposite occurs during closure seasons (from May to August with modifications until September/October), as fishing does not then affect shrimp spawner abundance, and as a result, shrimp postlarvae abundance does not collapse. So, then the indicating signal of reproductive activity can be detected inside Términos Lagoon.

Figure 4 shows the variation in the approximate number of winter shrimp spawners for P. setiferus (^{Gracia & Soto, 1990}) and P. duorarum (^{Cervantes-Hernández & Gracia, 2011}) from October to February. Also, a complete P. aztecus reproductive season spawned from November to June, with the highest spawner abundance signal during February (^{Cervantes-Hernández, 2015}). Complementary studies conducted in the Araya Peninsula, Venezuela (^{Marval-Rodríguez et al., 2015}), and the Gulf of Ana María, Cuba (^{Giménez-Hurtado et al., 2012}), show that Farfantepenaeus notialis and P. duorarum generate winter cohorts.

Additionally, throughout the closure seasons from 1998-2002, ^{SAGARPA-INP (2012)} described the average presence of mature shrimp females in the Campeche Bank as between 10 and 33 per km². This report suggests a lower presence of mature shrimp females during closure seasons than during the fishing seasons (Fig. 4), which is consistent with the following: in the Mexican Pacific, ^{Cervantes-Hernández (2008)} reported a higher percentage of egg-laying by F. californiensis mature females in phase IV from October to January. Also, the lowest percentage of egg-laying by F. californiensis mature females in phase IV was observed from July to September. Phase IV in shrimp of the genus Penaeus is characterized by dark-colored mature ovaries and an empty gonadal mass (^{Sandoval-Quintero & Gracia, 1998}).

In conclusion, it was demonstrated that the postlarvae abundance encountered in this study was not generated during the maximum reproductive seasons of both shrimp species, which should have occurred during winter when fishing seasons were implemented (Fig. 4).

Additional information on the reproductive activity of P. aztecus in the Tamaulipas and Veracruz sector indicates that annual reproductive seasons occur in winter oceanographic conditions of high Chl-a levels (>1.0 mg m^-3) and a colder sea surface temperature (SST 21-24°C) (^{Cervantes-Hernández, 2015}). The author mentioned that the Chl-a presence is relevant because the trophic chain is activated from it, and larval stages of shrimp can feed directly on phytoplankton and zooplankton biomass. So, for P. aztecus, a high Chl-a level means a greater degree of shrimp postlarvae survival due to the greater availability of its food. The aforementioned is evident from the immense shrimp postlarvae entrance inside Madre (Tamaulipas) and Tamiahua (Veracruz) lagoons.

Similar oceanographic conditions to those in the Tamaulipas and Veracruz sectors were documented during winter in the Campeche Bank sector. ^{Salmerón-García et al. (2011)} documented high Chl-a levels (>1.0 mg m^-3) between November and January, and low Chl-a levels (<1.0 mg m^-3) between April and November (1998-2008 period). The high Chl-a level is associated with offshore transport caused by stronger wind during winter (like that which occurs in the Gulf of Tehuantepec), from December to January, while there is minimum wind impact in summer, from May and June (^{Romero-Centeno et al., 2003}). Also, in the Gulf of Tehuantepec during winter upwelling seasons, oceanographic conditions of high Chl-a levels (>1.0 mg m^-3) and colder SST (~25-27°C) were recorded. There, during winter upwelling seasons, the highest abundance of F. californiensis spawners was reported (^{Cervantes-Hernández et al., 2008}). So, it should be taken into account that winter oceanographic conditions are better to stimulate spawning and increase shrimp postlarvae entrance into different lagoons. For this reason, we considered changes to closure season implementation.

We know that closure seasons are not entirely functional because ^{Cervantes-Hernández & Gracia (2011)} reported the following monthly mortality balance: natural mortality M = 0.21, fishing mortality F = 0.25, and total mortality Z = 0.46. The final balance was F > M, and based on this result, it was concluded that the population of P. duorarum was overfished from 1974-1989. Additionally, ^{Cervantes-Hernández (2015)} reported the following monthly mortality balance: M = 0.20, F = 0.54, Z = 0.74. The final balance was F > M, and based on this result, it was concluded that the population of F. aztecus was overfished from 1974 to 1995.

Taking into account documented postlarvae abundance, we did not find evidence to demonstrate that closure seasons function effectively. When the study of ^{Gracia & Soto (1990)} was conducted, fishing seasons were not delimited, and fishing efforts often affected the postlarvae abundance signal. For this reason, the authors reported lower shrimp postlarvae abundance with P. setiferus postlarvae dominant in all obtained samples (4,743 × 100 m^-3), while P. duorarum postlarvae were estimated at 817 × 100 m^-3. After the implementation of closure seasons, shrimp postlarvae abundance increased, maintaining the same abundance tendencies (41,284 P. setiferus postlarvae × 100 m^-3 and 37,558 P. duorarum postlarvae × 100 m^-3) (^{Flores-Coto et al., 2018}). Similarly, low results were obtained in this study, considering the two postlarvae entrance episodes. On the other hand, in a study conducted in the Carmen and Machona lagoons, Tabasco, México, ^{Flores-Coto et al. (2010)} documented more P. setiferus postlarvae entrance (13,332 for 100 m^-3) than F. duorarum postlarvae entrance (2,198 for 100 m^-3).

In conclusion, the populations of P. setiferus and P. duorarum in the Campeche Bank sector have two recruitment and reproductive seasons throughout the whole year. The first occurs between the early and mid-rainy season (from June to September). The second occurs from early fall and during winter (from October to February).