Spatial and temporal habitat use by penaeid shrimp (Decapoda: Penaeidae) in a coastal lagoon of the southwestern Gulf of Mexico

Journal Pre-proof Spatial and temporal habitat use by penaeid shrimp (Decapoda: Penaeidae) in a coastal lagoon of the southwestern Gulf of Mexico Jony R. Torres V., Alberto J. Sánchez, Everardo Barba M.

PII: DOI: Reference:

S2352-4855(19)30146-X https://doi.org/10.1016/j.rsma.2020.101052 RSMA 101052

To appear in:

Regional Studies in Marine Science

Received date : 14 February 2019 Revised date : 26 December 2019 Accepted date : 3 January 2020 Please cite this article as: J. Torres, A.J. Sánchez and M.E. Barba, Spatial and temporal habitat use by penaeid shrimp (Decapoda: Penaeidae) in a coastal lagoon of the southwestern Gulf of Mexico. Regional Studies in Marine Science (2020), doi: https://doi.org/10.1016/j.rsma.2020.101052. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

© 2020 Published by Elsevier B.V.

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Spatial and temporal habitat use by penaeid shrimp (Decapoda: Penaeidae) in a coastal lagoon of the southwestern Gulf of Mexico

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*Jony R. Torres V.a, Alberto J. Sánchezc, Everardo Barba M.b a

Tecnológico Nacional de México/I.T. del Valle del Yaqui, Academy of Biology, Coastal Zone

Ecology Laboratory. Avenida Tecnológico Block 611, Bácum, Sonora. México. C.P. 85276 b

El Colegio de la Frontera Sur, Sustainable management of basin and coastal zones,

Sustainable Sciences Department. Carretera a Reforma, km 15.5 s/n Ra. Guineo 2da Sección, C.P. 86280 Villahermosa, Tabasco, México; [email protected] c

Universidad Juárez Autónoma de Tabasco, Tropical wetlands management laboratory.

DACBIOL, [email protected]

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*Corresponding author: [email protected] (J. Torres) ABSTRACT

Knowledge of the environmental factors that influence the spatial-temporal densities of penaeid shrimp in Mecoacán Lagoon is important for understanding their relationship with the presence (migration) and estuarine habitat preferences. In the present study, the relationships

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between the physical-chemical components of water and sediments and the population dynamics of penaeid shrimp in Mecoacán Lagoon were evaluated according to a spatialtemporal and multihabitat approach. In six monitoring sites (Boca, Cerros, Mojarrero, Aspoquero Arrastradero and Pajaral), the density and biomass of shrimp were determined from November 2014 to October 2015 based on monthly captures with two nets (seine and

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renfro) in three habitats: mangrove, soft substrates without vegetation, and submerged aquatic vegetation that corresponds to seagrasses (seagrasses was registered only in Boca and Cerros). The maximum salinity was found in Boca (23±2.6PSU), with pH values ranging from 7.9±0.1 to 8.3±0.2, and the maximum dissolved oxygen was found in Cerros (6.6±0.5mg/L). The average texture of sediments was 62±3.5% sand, 24±2.4% silt, and 14±1.2% clay. The highest organic matter (7.8±1.2%) and nitrogen (875mg/kg) contents were recorded in Pajaral. A total of 5,085 penaeid shrimp were captured (seine 77% and renfro 33%), including the species

Farfantepenaeus

aztecus

(Ives)

(1,774

ind.),

Farfantepenaeus

duorarum

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(Burkenroad) (1,559 ind.), and Litopenaeus setiferus (L.) (1,752 ind.), with a total wet weight of 2,419 g. The spatial segregation patterns of penaeid shrimp suggest that their temporal distribution and habitat preferences are important for reducing interspecific competition. Salinity, dissolved oxygen, organic matter content, and sediment type were the factors that most influenced the spatial-temporal differences in the density and biomass of the penaeid

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shrimp among sites. Knowledge of the habitat distribution and preferences of key estuarine species such as penaeid shrimp can be used as an informational baseline for evaluating future environmental scenarios and modeling species distribution along the estuarine gradient.

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Keywords: Shrimp Penaeid Density Biomass Habitat Season

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1. Introduction

Estuarine ecosystems are highly complex environments. This complexity is mainly due to the physiographic characteristics and the environmental gradients present in these ecosystems that promote high spatial and temporal heterogeneity (Thrush et al., 2013). Consequently, these ecosystems generally contain fishing resources of considerable magnitude because

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invertebrate organisms and fish use them as areas for refuge, growth, and feeding (Barba, 1999; Domínguez et al., 2003; Barba et al., 2005). The spatial organization of estuarine species is highly correlated with the type of substrate (Hamerlynck and Hostens, 1993), and the temporal structure is often the result of the seasonal migration of crustaceans, which move between the coast and adjacent estuaries (McLusky, 1989; Robertson and Duke, 1990). The

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life cycles of penaeid shrimp include offshore spawning, development of oceanic larvae, and migration to estuaries of post larval shrimp, which are transported to coastal zones by ocean currents (Pérez-Castañeda and Defeo, 2004; Rajendran and Kathiresan, 2004; Matthews, 2008). However, the degree of estuarine dependence is the main characteristic that differentiates these species, including species of the same genus, and is related with their tolerance to salinity and capacity to establish in different habitats (Gracia et al., 1991; Gracia and Hernández, 2005). For example, Litopenaeus setiferus (L.) is more abundant in areas of

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lower salinity compared to Farfantepenaeus aztecus (Ives) (Gunter, 1961). Overall, penaeid shrimp are well adapted to fluctuations in environmental conditions (Brito et al., 2000). The physical structure of seagrasses enables shrimp to reduce the probability of being detected and consumed by predators (Heck and Crowder, 1991). The abundance of crustaceans is substantially higher in habitats in which seagrass grow than in those comprising unvegetated sediments (Liao et al., 2015). In addition, mangroves have long been recognized 2

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as an important habitat for the feeding and refuge of shrimp (Sasekumar et al., 1992; Vance et al., 1996). Knowledge of the environmental factors (biotic and abiotic) that influence the spatial-temporal

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densities of penaeid shrimp in Mecoacán Lagoon is important for understanding the relationship between these factors and their presence in and preference for certain estuarine habitats. The objective of the present study was to evaluate the relationship between the environmental heterogeneity (physical-chemical components of water and sediments) of Mecoacán Lagoon and the population dynamics of penaeid shrimp according to spatialtemporal approach and multihabitat approach. In this context, the following hypotheses were proposed: (i) F. aztecus and Farfantepenaeus duorarum (Burkenroad) will colonize sites with higher salinity, whereas L. setiferus will be distributed in sites with lower salinity. (ii) These species will prefer different habitats: F. aztecus will show a preference for mangrove (MAN),

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F. duorarum for submerged aquatic vegetation (SAV), and L. setiferus for soft substrates without vegetation (SSWV) with a high clay content. 2. Materials and methods 2.1. Study area

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Mecoacán Lagoon has an extension of 96,454.39 ha (Barba et al., 2006) and is located in the southern Gulf of Mexico (18°16’–18°20’ N & 93°04’ –93°14’ W). The Escarbado and Cuxcuchapa Rivers discharge into the lagoon at the eastern and southeastern margins, respectively (Gómez, 1977) (Fig. 1). Mecoacán lagoon is located close to a petroleum refinery with latency of oil spills, as well as neighboring areas such as urban areas and agricultural

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fields involving agrochemical handling (Armenta-Arteaga and Elizalde-González, 2003). The salinity fluctuates between 0.5 and 29 PSU. Minimum salinity was previously recorded in the southeastern portion of the lagoon in the rainy season and maximum salinity in the northern and western portions during the dry season (Domínguez et al., 2003). The dominant vegetation of Mecoacán Lagoon is mangrove (MAN) composed of Rhizophora mangle L. (red mangrove), Laguncularia racemosa (L.) Gaertn (white mangrove), and Avicennia germinans (L.) Stearn (black mangrove) (Torres et al., 2017) and submerged aquatic vegetation (SAV) composed of Halodule wrigthii Asch., Ruppia marítima L., and macroalgae of the genera

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Hypnea and Gracilaria (Orozco and Dreckmann, 1995; Flores et al., 1996).

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Fig. 1. Mecoacán Lagoon sampling sites, southwestern Gulf of Mexico. Sites are shown with

2.2. Sampling design

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solid black dots. Meteorological tower is shown with * (CONAGUA-SMN-EMAS, 2015).

Six sites were selected in areas adjacent to conserved mangrove (Sites without registration of mangrove use activities) (Domínguez-Domínguez et al., 2011). In the northern portion of the lagoon, Boca is directly influenced by tidal streams, and Cerros is located in the mixing zone

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of the incoming and outgoing streams (Gómez, 1977). In the eastern portion, Pajaral and Arrastradero are influenced by the Cuxcuchapa and Escarbado Rivers (Torres et al., 2018; Hernández, 2007). In the southwestern and western portions, Aspoquero and Mojarrero, respectively, receive a lower amount of fresh water and are thus more saline (Domínguez et al., 2003; Infante-Mata et al., 2014) (Fig. 1). The study cycle was November 2014 to October 2015.

2.3. Physical-chemical variables in water and sediments

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In the surface water (first 20 cm) of the lagoon, the salinity, temperature, dissolved oxygen, and pH were measured monthly in each site with a Hanna HI9828 multiparameter (salinity was measured using the Practical Salinity Scale). One sediment sample was collected per site (72 samples) using a coring device (0.0033 m2). The texture of the sediments was determined according to the Bouyucos method (Klute, 1986), the pH by electrometry in a 1:2 4

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ratio with water, and the organic matter content according to Walkley and Black (1934). Total nitrogen (NT) and phosphorus (PT) were analyzed according to NOM-021-SEMARNAT-2000. 2.4. Collection of penaeid shrimp and determination of density and biomass

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The penaeid shrimp (F. aztecus, F. duorarum, and L. setiferus) were collected monthly in each sampling site (triplicate in each habitat type) during daylight hours in the morning (1,008 trawls of shrimp nets). Two net collection techniques were used: A renfro beam net was trawled over an area of 50 m2 (opening of 1.6 × 0.5 m, 1.5 m in length, and 1-mm mesh) (Renfro, 1962), and a seine net over an area of 62 m2 (13 m in length, 2.3 m in width, and 1-cm mesh). The organisms were fixed in 4% formalin and transported to the laboratory for separation and identification at the species level based on Pérez-Farfante (1969, 1970). Then, the organisms were counted and weighed on an analytical balance (0.001 g of precision) and conserved in 96% alcohol. The density was recorded in ind•m-2 and the biomass in g•m-2. The size

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classification of juveniles (1.7–4.7 cm in total length) and adults (>4.7 cm in total length) was based on taxonomic keys and Pérez-Farfante (1969, 1970). Finally, the organisms were deposited in the Southeastern Aquatic Organism Reference Collection: Macroinvertebrates and Fish of the Laboratory of Aquatic Resource Utilization of the Southern Frontier College

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(El Colegio de la Frontera Sur [ECOSUR]) in Villahermosa. 2.5. Distribution of penaeid shrimp in habitats

The collection techniques were carried out in triplicate in each habitat type: MAN, SAV and SSWV (Heck and Crowder, 1991; Minello and Zimmerman, 1991; Barba, 1999; Rozas and Minello, 2006). All sites presented SSWV and MAN habitats, but only two sites (Boca and

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Cerros) presented SAV. The use of different collection techniques creates bias that may influence the resulting data (Gillanders et al., 2003), seine is for organisms of the water column and renfro is more oriented for benthos sampling. However, the distinct physical structures of the different habitats made sampling by distinct methods necessary (Blaber et al., 1989; Blanco-Martínez et al., 2017). Accordingly, the analysis of the data was performed per collection technique (renfro or seine net). The distribution of the density and biomass of penaeid shrimp was analyzed per the representative climatic seasons of the region: the northerly winds (November to February), the dry season (March to June), and the rainy season

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(July to October).

2.6. Data analyses

The data were first explored using a Kolmogorov-Smirnov normality test, and the homogeneity of variance was analyzed using Levene’s test. The level of significance was set at 5%. A oneway ANOVA was applied in addition to the Kruskal-Wallis (kw) non-parametric multiple 5

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comparison test when the assumption of normality was not fulfilled (Steel and Torrie, 1996). All analyses were performed in the IBM SPSS Statistics 20 software. The correlations of the environmental conditions, including the water variables (salinity, temperature, dissolved oxygen, and pH) and the sediment variables (texture, pH, organic matter, nitrogen, and

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phosphorus), with the density and biomass of the penaeid shrimp (F. aztecus, F. duorarum, and L. setiferus) were examined according to the Pearson coefficients (r). Finally, a canonical correspondence analysis (CCA) was carried out in the PAST 2.17c software to analyze the density and biomass of penaeid shrimp among sites considering the physical-chemical water and sediment variables (Hammer et al., 2001). 3. RESULTS

3.1. Physical-chemical variables in water and sediments

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Among sites, the average salinity of surface water differed significantly. The maximum salinity was recorded in Boca (23±2.6) and the minimum in Pajaral (5.9±1). The average temperature ranged from 26.4±0.6 °C in Boca to 29.4±1.1 °C in Mojarrero. The pH of the water presented low variation, ranging from 7.9±0.1 to 8.3±0.2 (Fig. 2). Temporally (monthly), the salinity ranged from 7.6±2.7 to 17.1 during the study period without presenting significant differences

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(F=1.4 p=0.2 N=72). The temperature (F=18.2 p<0.05 N=72) was lower in the months of November, December, and January (23.1±0.4, 24.3±0.2, and 23.9±0.1 °C, respectively) compared to the highest temperature recorded in May of 31.8±0.6 °C. Finally, the level of dissolved oxygen (DO) was lowest in Arrastradero and Pajaral (4.3±0.5 and 4.7±0.5 mg/L, respectively), and temporal significant differences (F=18.3 p<0.05 N=72) were found between

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the lowest level in November (2.8±0.6 mg/L) and the highest in May (8.8±0.6 mg/L).

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Fig. 2. Physicochemical variables of surface water at monitoring sites of the Mecoacán lagoon.: (A) Salinity, (B) Temperature, (C) Dissolved oxygen and (D) pH. Letters show

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significant similarities among sites (Tukey p<0.05) (±SE).

Overall, the highest densities of F. aztecus were found at Cerros, Aspoquero, and Pajaral, which ranged in salinity from 1.3 to 19.7, of F. duorarum in Boca, Cerros, and Aspoquero, which ranged in salinity from 2.2 to 33.5, and of L. setiferus in Pajaral, which ranged in salinity

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from 2.4 to 9.8.

In addition, the average texture of the sediments was 62±3.5% sand, 24±2.4% silt, and 14±1.2% clay. Significant spatial differences were found among sites. All sediments had a higher percentage of sand; the highest sand content was found in Arrastradero (84±2.3%). Meanwhile, the highest silt content was found in Boca (35±2.5%) and the highest clay content in Pajaral (26±2.9%) (Table 1). The lowest pH was recorded in Mojarrero (5.5±0.2) and organic matter in Arrastradero (4±0.9%). Table 1

Texture %

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Physical chemical of sediment in monitoring sites, Mecoacán Lagoon

Sand

Boca 49±3.3 a

Cerros 58±2.5 ab

Mojarrero 65±3.4 b

Sitio Aspoquero 68±4.7 b

Arrastradero 84±2.3 c

Pajaral 44±4.8 a

F 14

p <0.05

16 21

<0.05

Silt

35±2.5 a

31±2.8 a

25±2.8 ab

21±4.1 b

6±1.1 c

30±0.9 ab

Clay

16±0.7 a

11±0.9 a

11±1.2 a

11±0.5 a

10±1.1 a

26±2.9 b

<0.05

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pH %OM

5.8±0.1 5.3±0.8

6±0.1 4.2±0.9

5.5±0.2 4.3±0.9

6±0.2 4.4±0.9

5.8±0.1 4±0.9

6.1±0.1 7.8±1.2

2 2.5

0.08 0.07

Letters show significant similarities among sites (Tukey p<0.05, N=72) (±SE). (OM) Organic matter.

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The highest nitrogen content was recorded in Pajaral (0.09±0.008%; 875 mg/kg) and the lowest in Arrastradero (0.03±0.005%; 275 mg/kg). Temporally, the nitrogen content of sediments ranged from a low of 283 mg/kg (0.03±0.007%) in August and to a high of 733 mg/kg (0.07±0.002%) in April (Fig. 3). Meanwhile, the highest phosphorus content was recorded in Cerros (0.2%±0.04%; 2,042 mg/kg) and the lowest in Pajaral (0.03%±0.003%; 289 mg/kg). Temporally, the phosphorus content ranged from a low of 209 mg/kg

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(0.02%±0.005%) in September to a high of 1,548 mg/kg (0.15%±0.04%) in December (Fig. 3).

Fig. 3. Total content of nitrogen (TN) and phosphorus (TP) of the sediment in monitoring sites of the Mecoacán lagoon: (A) sites, (B) months. Letters indicate significant differences (Tukey p<0.05) (±SE). 8

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A highly negative correlation was found between the sandy texture and the silt, clay, nitrogen, phosphorus, and organic matter contents of sediments. Also, a positive correlation was found between the nitrogen content and the organic matter, silt, and clay contents of sediments. The density and biomass of L. setiferus (Table 4). 3.2. Density and biomass of penaeid shrimp

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DO was positively correlated with clay, pH, and salinity and negatively correlated with the

A total of 5,085 penaeid shrimp were captured (77% with a seine net and 33% with a renfro net), corresponding with the species F. aztecus (1,774 ind.), F. duorarum (1,559 ind), and L. setiferus (1,752 ind) and a total wet weight of 2,419 g. Most collected shrimp were juvenile (86%), and the remaining were sub-adult (14%). The size distribution of juvenile shrimp differed among sites (F=16.1 p<0.05 N=4,451), with the lowest average size in Cerros

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(2.7±0.02 cm) and the highest in Mojarrero (3.2±0.04 cm). The size of the captured juveniles did not significantly differ with respect to the collection techniques (seine and renfro nets) (F=38 p=0.6 N=4,451). Meanwhile, the size distribution of sub-adult shrimp also differed (F=5.8 p<0.05 N=4,378), with the highest average size in Pajaral (6.1±0.06 cm). The size of sub-adults did not differ with respect to collection technique (F=0.7 p=0.4 N=707). However,

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differences were found with respect to the total sample (juveniles+subadults) (F=26.1 p<0.05 N=5,085): The largest sizes were associated with the seine net (3.42±0.02 cm) compared to the renfro net (3.1±0.03 cm), and 89% of sub-adults were captured by the seine net. The penaeid shrimp with a total length of 25 to 30 mm (1,187 shrimp) were most abundant followed

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by those 20 of 25 mm in length (1,105 shrimp) (Fig. 4).

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Fig. 4. Total abundance distribution of penaeid shrimp by size (total length): A) sites and B) habitats. Spatially, F. aztecus presented the highest density in Pajaral for both collection techniques

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(seine 0.71±0.2 and renfro 0.67±0.1 ind•m-2) and the lowest density in Arrastradero (seine 0.06±0.04 and renfro 0.06±0.02 ind•m-2). Its highest biomass in the seine net was recorded in Boca (0.48±0.15 g•m-2) and in the renfro net in Pajaral (0.28±0.05 g•m-2), and its lowest biomass was recorded in Arrastradero (0.04±0.02 and 0.01±0.01 g•m-2, respectively) (Table 2). Farfantepenaeus duorarum presented the highest density in the seine net in Aspoquero (1.05±0.32 ind•m-2) and in the renfro net in Cerros (0.54±0.11 ind•m-2); however, this species was absent in the seine net at Mojarrero, Arrastradero, and Pajaral. Its highest biomass was found in Boca in both the seine and renfro nets (0.32±0.07 and 0.26±0.05 g•m-2, respectively). Notably, L. setiferus was absent in Boca but showed its highest density in Pajaral (seine

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1.41±0.23 and renfro 0.83±0.14 ind•m-2). Its highest biomass in the seine net was recorded in Mojarrero (0.54±0.16 g•m-2) and in the renfro net in Pajaral (0.28±0.04 g•m-2) (Table 2). Table 2

Density and biomass of penaeid shrimp by monitoring sites in Mecoacán Lagoon

Biomass (g-1 m-2)

Density (ind-1 m-2)

Biomass (g-1 m-2)

P. aztecus

0.55±0.2 ab

P. duorarum

0.65±0.13 ad

L. setíferus

0±0 a

P. aztecus

0.48±0.15 a

P. duorarum

0.32±0.07 a

L. setíferus

0±0 a

Cerros

Mojarrero

Aspoquero

Arrastradero

Pajaral

0.27±0.08 b

0.08±0.02 c

0.69±0.27 a

0.06±0.04 c

0.71±0.2 a

0.21±0.06 b

0±0 c

1.05±0.32 d

0.05±0.03 c

0.37±0.12 ab

0.16±0.08 b

0.65±0.23 c

0.43±0.19 bc

0.81±0.23 cd

1.41±0.23 d

F

p

kw

5.9 <0.05 0.06 0.9 7.3 <0.05

0.15±0.05 b

0.05±0.02 bd

0.21±0.12 c

0.04±0.02 d

0.31±0.12 abd

0.1±0.04 b

0±0 c

0.28±0.06 a

0.02±0.01 c

0.16±0.05 ab

0.06

0.07±0.04 a

0.54±0.16 bc

0.24±0.11 b

0.32±0.11 b

0.8±0.15 c

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Density (ind-1 m-2)

Boca

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Seine net

Specie

Renfro beam net

P. aztecus

0.21±0.07 ac

0.63±0.11 b

0.11±0.03 ad

0.29±0.1 c

0.06±0.02 d

0.67±0.1 b

3.2

0.01

P. duorarum

0.38±0.08 a

0.54±0.11 a

0±0 b

0.29±0.11 a

0±0 b

0±0 b

1.7

0.03

L. setíferus

0±0 a

0.06±0.03 b

0.12±0.06 b

0.14±0.08 b

0.12±0.05 b

0.83±0.14 c

0.4

0.04

P. aztecus

0.13±0.04 ab

0.25±0.05 bd

0.07±0.02 a

0.1±0.04 a

0.01±0.01 c

0.28±0.05 d

2

0.01

P. duorarum

0.26±0.05 a

0.18±0.05 a

0±0 c

0.07±0.03 b

0±0 c

0±0 c

L. setíferus

0±0 a

0.01±0.01 ab

0.06±0.02 c

0.07±0.03 c

0.04±0.02 bc

0.28±0.04 c

7.8 <0.05 0.17

Letters indicate significant similarities among sites (Tukey Test and Kruskal Wallis

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nonparametric multiple comparison p<0.05) (±SE).

F. aztecus presented its highest density in October (seine 1.54±0.3 and renfro 1.21±0.19 ind•m-2) and its highest biomass in the seine net in March (0.73±0.19 g•m-2) and in the renfro net in October (0.29±0.5 g•m-2). The lowest density and biomass of F. aztecus in both the seine and renfro nets occurred in December (Table 3). Farfantepenaeus duorarum presented

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its highest density and biomass in the seine net in August (1.69±0.25 ind•m-2 and 0.42±0.07 g•m-2, respectively) and in the renfro net in September (0.86±0.11 ind•m-2 and 0.25±0.05 g•m2

, respectively). The lowest density and biomass of F. duorarum in both the seine and renfro

nets occurred in December (Table 3). Notably, L. setiferus was absent in the sampling sites

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from October to February. Its highest density in the seine net occurred in August (1.81±0.39 ind•m-2) and in the renfro net in July (0.75±0.16 ind•m-2), and its highest biomass in both the seine and renfro nets was recorded in June (1.52±0.24 and 0.41±0.07 g•m-2, respectively. The density and biomass of F. aztecus in the seine and renfro nets were negatively correlated with the sand content of sediments and positively correlated with the silt, clay, pH, nitrogen, and organic matter contents. The density and biomass of F. duorarum in the renfro net were positively correlated with the silt content of sediments and the pH, DO, and salinity of water

Table 3

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(Table 4).

Density and biomass of penaeid shrimp in months of monitoring in Mecoacán Lagoon   

Especie 

N 

D 

J 

F 

M 

Seine net  A 

M 

J 

J 

A 

S 

O 

F 

p 

kw 

0.37±0.2  0.04±0.04  0.28±0.14  0.23±0.15  0.74±0.24  0.7±0.25  0.42±0.15 0.09±0.03 0.09±0.05  0.1±0.04  0.12±0.06  1.54±0.3  1.8  0.04  acd  b  ac  ac  d  d  cd  ab  ab  ab  ab  c     Density  0.09±0.03  0.03±0.02  0.19±0.12  0.04±0.02  0.35±0.18  0.14±0.07  0.91±0.3  0.28±0.14  0.27±0.1  1.69±0.25  0.32±0.14  0.4±0.21  1.7  0.04  (ind/m2) F. duorarum  a  a  ab  a  b  ab  c  b  b  d  b  cb     L. setíferus 

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F. aztecus 

0±0  0±0  0±0  0±0  0.88±0.32 0.32±0.12 0.88±0.34  1.78±0.4  0.81±0.37 1.81±0.39  0.49±0.2  0±0  1.8  0.04     0.3±0.1  0.02±0.02  0.09±0.04  0.11±0.05  0.73±0.19 0.27±0.07 0.14±0.03 0.09±0.04 0.04±0.02 0.04±0.02 0.09±0.04 0.54±0.13  1.6 <0.05  bc  a  a  a  d  b  a  a  a  a  a  cd     Biomass  0.06±0.02  0.01±0.01  0.11±0.04 0.02±0.003 0.18±0.05 0.04±0.02 0.41±0.06  0.1±0.04  0.12±0.03 0.42±0.07 0.17±0.05 0.17±0.05  F. duorarum  1.1  0.04  (ind/m2)  ab  a  bc  a  c  a  d  c  c  d  c  c     0.47±0.18 0.09±0.05 0.43±0.18 1.52±0.24 0.51±0.14 0.55±0.21  0.36±0.1  L. setíferus  0±0  0±0  0±0  0±0  0±0  1.2  0.03  b  a  b  c  b  b  b     F. aztecus 

Renfro beam net  0.09±0.05  0.05±0.02  0.16±0.07  0.24±0.11  0.31±0.11  0.5±0.11  0.53±0.1  0.21±0.09 0.13±0.06  0.14±0.1  0.24±0.11 1.21±0.19  1.3  0.02     a  a  a  ab  b  b  ab  a  ab  b  c  b  0.07±0.04  0.01±0.01  0.15±0.04  0.1±0.05  0.09±0.04 0.16±0.04 0.32±0.06 0.14±0.04 0.11±0.04  0.2±0.07  0.86±0.11  0.29±0.1  Density  F. duorarum        0.32  b  a  b  b  b  bc  dc  b  b  bcd  c  c  (ind/m2)  0.1±0.03  0.12±0.04 0.42±0.11 0.74±0.15 0.75±0.16 0.21±0.06 0.22±0.06  L. setíferus  0±0  0±0  0±0  0±0  0±0        0.7  a  ab  b  c  c  b  b  0.13±0.04  0.02±0.01  0.11±0.03  0.14±0.03  0.17±0.05 0.27±0.06  0.2±0.05  0.21±0.04 0.04±0.02 0.03±0.02  0.1±0.02  0.29±0.5  F. aztecus  1.6 <0.05     bc  a  b  bc  bc  c  cd  cd  a  a  b  d  0.04±0.02 0.002±0.001 0.09±0.03  0.1±0.03  0.02±0.01 0.04±0.02 0.09±0.03 0.05±0.02 0.04±0.02 0.04±0.02 0.25±0.05 0.24±0.04  Biomass  F. duorarum        0.6  bs  a  c  c  c  b  c  bc  bc  bc  d  d  (ind/m2)  0.02±0.01 0.07±0.02 0.07±0.03 0.41±0.07 0.17±0.05 0.08±0.03 0.12±0.04  L. setíferus  0±0  0±0  0±0  0±0  0±0        0.06  a  b  b  d  c  bc  bc 

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F. aztecus 

Letters indicate significant similarities among months (Tukey Test or Kruskal Wallis

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Nonparametric Multiple Comparison, p<0.05). (±SE).

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Table 4 Density and biomass (Spatial) of penaeid correlation with physical chemical of water and sediment variables in Mecoacán Lagoon Seine net

Sediment

Sand

Dn Du

Dn St

-0.6

Silt

0.66

Clay

0.63

pH

0.72

TN

0.74

Bm Az

Refro beam net Bm Du

Bm St

-0.77

0.6

0.61

0.64

0.63

0.63

Water

pH 0.49

T(°C)

-0.48

-0.77

Bm Du

Bm St

-0.82

0.6

0.75

0.63

0.69

0.76

0.77

0.61

0.67

0.6

0.8

0.62

0.73

0.65

0.72

0.91

0.66

0.65

0.65

0.6

-0.92

-0.8

Sal

Bm Az

0.86

-0.88

DO

Dn St

0.6

TP OM

Dn Du

-0.67

0.71 0.65

Dn Az

pro of

Dn Az

-0.61 0.74

0.71

-0.83

-0.61

-0.65

0.83

0.9

0.77

-0.65

0.94

-0.7

0.73

-0.6

0.71

-0.64

0.5

-0.6

0.79

-0.6

-0.42

-0.73

Dn=Density; Bm=Biomass; Az=F. aztecus; Du=F. duorarum; St=L. setiferus; TN=Total T(°C)=Temperature, (p<0.05).

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nitrogen; TP=Total phosphorus; OM=organic matter; DO=Dissolved oxygen; Sal=Salinity and

The density and biomass of L. setiferus in the seine and renfro nets were positively correlated with the organic matter and clay contents of sediments and also negatively correlated with the

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pH, DO, and salinity of water. In addition, the density and biomass of this latter species in the renfro net were positively correlated with the pH and nitrogen content of sediments. Furthermore, a positive correlation was identified between the density of the species F. aztecus and F. duorarum in the seine and renfro nets and a negative correlation between the density of L. setiferus and F. duorarum in the renfro net (Table 4). The CCA grouped the

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density and biomass of F. aztecus and F. duorarum in the renfro net with the DO and pH of water in Cerros and in the seine net with the salinity in Boca and Aspoquero. In addition, the analysis correlated the density and biomass of L. setiferus in Pajaral with the organic matter,

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nitrogen, and clay contents of the sediments (Fig. 5).

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Fig. 5. Analysis of canonical correspondence (ACC) between sites for the density and biomass of penaeid shrimp and physical chemical variables of sediment and surface water. Explanation of the

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cumulative variation of 86.2%, axis 1 explains 69.2% and axis 2 explains 17% of the variation. Bm: biomass, D: density, Se: seine net, Rb: renfro beam net, Az: F. aztecus, Du: F. duorarum, St: L. setíferus, TN: total nitrogen, OM: organic matter, Cl: clay, Sn: sand, Sl: silt, DO: dissolved oxygen, Temp: temperature, Sal: salinity.

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3.3. Distribution of penaeid shrimp in habitats

The highest density of F. aztecus was recorded in the seine net in Aspoquero, where this species showed preference for MAN (0.65±0.1 ind•m-2), followed by Pajaral, where it showed preference for MAN and SSWV (0.42±0.1 and 0.28±0.08 ind•m-2, respectively). This species was absent in the renfro net in Arrastradero but showed its highest density in the renfro net in

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Pajaral and a preference for MAN (0.34±0.05 ind•m-2) (Fig. 6). The highest density of F. duorarum was recorded in the seine net in Aspoquero (MAN: 0.56±0.15 ind•m-2; SSWV: 0.49±0.12 ind•m-2), yet no individuals were recorded in the renfro net in Mojarrero, Arrastradero, and Pajaral. In Cerros and Aspoquero, this latter species showed preference for MAN (0.26±0.07 and 0.24±0.05 ind•m-2, respectively). Finally, L. setiferus was absent in the SAV of Boca and Cerros, but its highest density was recorded in Pajaral where it showed a preference for SSWV according to both collection techniques (seine: 1.24±0.3 ind•m-2; renfro: 0.83±0.1 ind•m-2) (Fig. 6).

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The highest biomass of F. aztecus in the seine net was recorded in Boca in the MAN and SSWV habitats (0.21±0.06 and 0.17±0.07 g•m-2, respectively) and in the renfro net in Pajaral (0.13±0.04 and 0.15±0.03 g•m-2, respectively) (Fig. 6). The highest biomass of F. duorarum was found in MAN at Aspoquero in the seine net (0.18±0.03 g•m-2) and also in MAN at Boca in the renfro net (0.09±0.02 g•m-2). The highest biomass of L. setiferus was recorded in MAN 13

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at Pajaral in the seine net (0.84±0.1 g•m-2) and in SSWV in the renfro net (0.29±0.05 g•m-2)

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(Fig. 6).

Fig. 6 Density and biomass of penaeid shrimp by habitat in Mecoacán Lagoon sites. (±SE). Mangrove.

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(SSWV) soft substrates without vegetation, (SAV) submerged aquatic vegetation, (MAN)

3.4. Distribution of penaeid shrimp per season

In the seine net, the average density of penaeid shrimp in Mecoacán Lagoon was 0.31 ind1

-2

•m

during the northerly winds, 1.87 ind-1•m-2 during the dry season, and 1.91 ind-1•m-2 during

1

-2

•m

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the rainy season and, in the renfro net, was 0.21 ind-1•m-2 during the northerly winds, 0.9 indduring the dry season, and 1.12 ind-1•m-2 during the rainy season. The highest biomass

in both the seine and renfro nets was presented in the dry season (1.11 and 0.4 g-1•m-2, respectively). The density and biomass of F. aztecus differed significantly among seasons in the renfro net (F=5 p=0.006 N=72 and F=4.6 p=0.01 N=72, respectively) but presented its highest density and biomass in the seine net during the dry season (0.49 ind-1•m-2 and 0.3 g1

-2

•m

, respectively) (Fig. 7). The density and biomass of F. duorarum also differed significantly

among seasons in the seine net (F=5.4 p<0.05 N=72 and F=3.1 p=0.04 N=72, respectively).

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The highest density and biomass of this latter species were recorded in the seine and renfro nets in the rainy season. Finally, L. setiferus was not present during the northerly winds (October to January) but presented its highest density and biomass in the seine and renfro nets during the dry season (Fig. 7).

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Fig. 7. Density and biomass of penaeid shrimp by seasons in Mecoacán Lagoon. Letters indicate significant similarities among seasons (Tukey Test p <0.05) (±SE).

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4. DISCUSSION

The Mecoacán Lagoon receives terrigenous sediments from the Escarbado and Cuxcuchapa Rivers to the east and southeast, respectively (Fig. 1), that consist of fine silt and clay (Kennish, 2015). These sediments are carried by the counter clockwise currents that move toward Boca located near the mouth of the lagoon (Gómez, 1977), resulting in higher silt, clay,

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and organic matter at Pajaral and Boca. However, coastal lagoons generally contain low levels of organic matter (<10%) (Howe et al., 1999), and only a small fraction is available as food for shrimp (Rulifson, 1981). In Mecoacán Lagoon, the content of organic matter ranged from 2.3% to 9.3%. The species F. aztecus and L. setiferus showed preference for sites with higher levels of organic matter. Therefore, the organic matter content was positively correlated with the density and biomass of these latter two species. Salinity is one of the most important environmental factors for penaeid shrimp because it

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influences the distribution of these organisms in estuarine systems (Day et al., 1982; Gracia, 1991). The first hypothesis that (i) F. aztecus and F. duorarum would prefer sites with higher salinity and L. setiferus sites with lower salinity was rejected because the distribution of F. aztecus was not correlated with salinity. However, the hypothesis was fulfilled for L. setiferus, which had higher densities at sites with lower salinity (Pajaral and Arrastradero). Accordingly, 15

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the density and biomass of this latter specie was strongly and negatively correlated with salinity. Nevertheless, the high variation in salinity throughout the distribution of F. aztecus in Mecoacán Lagoon suggests that salinity is only one of several variables that influences the distribution of this specie in estuaries (May-Kú et al., 2014; Doerr et al., 2015; Mace and

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Rozas, 2017).

The maximum abundances of juvenile L. setiferus were reported in estuarine water with a salinity between 0 and 10 in Texas (Gunter et al., 1964) and South Carolina (Wenner and Beatty, 1993); similar values were recorded in the present study at Pajaral (2.4 to 9.8) and Arrastradero (1.3 to 11.8). Additionally, similar results were reported for L. setiferus by Flores et al. (1996), who found that density increased when salinity decreased in the rainy season. Howe et al. (1999) did not find significant correlations between the three species of penaeid

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shrimp and temperature or salinity. In Mecoacán Lagoon, only a negative spatial correlation was identified between the density and biomass of L. setiferus captured using both collection techniques (seine and renfro nets) and the salinity of water. Notably, F. duorarum was not collected in the renfro net. Its minimum density was recorded in the seine net in Arrastradero, which may reflect the low levels of DO and salinity at this site and the positive correlation of

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these latter parameters with the density and biomass of this species. Accordingly, the lower level of salinity at Arrastradero contributed to the movement of F. duorarum toward zones of greater salinity (Brito et al., 2000). Meanwhile, the absence of F. duorarum in Mojarrero may be attributed to its highly negative correlation with temperature, as the highest temperature was presented at this site (up to 33.5 °C). Although few correlations with temperature and

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salinity were found, other studies have identified such relationships (Zimmerman and Minello, 1984; Zein-Eldin and Renaud, 1986; Wenner and Beatty, 1993). The second hypothesis that (ii) F. aztecus would prefer the MAN habitat, F. duorarum the SAV habitat, and L. setiferus the SSWV habitat with clay substrates is accepted given that F. aztecus and F. duorarum presented high densities in MAN and L. setiferus in SSWV with a high percentage of clay (Pajaral). Additionally, F. duorarum had a high density in SAV in the renfro net (Gillanders et al., 2003; Macia, 2004; Brito et al., 2016). Thus, habitat preferences

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apparently vary per species (Coles et al., 1987; Dall et al., 1981; Macia, 2004). In Mecoacán Lagoon, L. setiferus was not found in SAV, as this species does not demonstrate selectivity for substrates covered with vegetation (Costello and Allen, 1970; Zimmerman and Minello, 1984). Only two sites (Boca and Cerros) contained SAV with high values of pH, DO, and salinity, which decrease the density and biomass of L. setiferus which can be attributed to the preference of this species at low values of these parameters in the water. On the other hand, 16

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the high density of L. setiferus in SSWV with clay substrates and high organic matter content (Pajaral) is due to the omnivorous habits of this species (Minello and Zimmerman, 1991; Sánchez, 1997; Domínguez et al., 2003).

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The species F. duorarum presented higher biomass in Boca and Cerros that can be attributed to the movement of sub-adults toward the open sea. Overall, 84% of sub-adult shrimp were captured in these sites by seine beam net, similar to that recorded by Broadhurst et al. (2016) with the largest sizes in the water column. Flores et al. (1996) also highlighted the preference of F. duorarum for SAV, coinciding with the findings of other studies, for example in Florida (Gore et al., 1981; Sheridan, 1992) and Laguna de Términos (Mier-Reyes et al., 1994). The selectivity of F. duorarum for SAV was experimentally evaluated by Sánchez (1997) and appears to result from the high availability of prey and low risk of mortality due to predation in this habitat (Sánchez and Soto, 1993; Sánchez, 1997). The highly positive correlation of the

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density and biomass of F. aztecus with that of F. duorarum indicates that these species can generally be found at the same sites. However, these species do not necessarily share seasonality nor habitat preferences, as large differences in density were found on a monthly basis, and F. aztecus shows a preference for MAN and F. duorarum for SAV.

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The osmotic capacity of shrimp is a useful indicator of the stress that shrimp experience in face of diverse environmental factors, including low DO (Charmantier et al., 1988; Rosas et al., 1999) and high salinity (Dall and Smith, 1981; Day et al., 1982; Brito et al., 2000). In Mecoacán Lagoon, the highest density of L. setiferus was recorded in sites with lower DO and salinity (Pajaral and Arrastradero) and of F. duorarum in sites with higher DO and salinity. On

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the other hand, F. aztecus presented better growth within a salinity range of 8.5–17‰ (Venkataramiah et al., 1974). This explains the wide distribution of F. aztecus across the lagoon (Boca, Cerros, Aspoquero, and Pajaral) and evidences its apparent tolerance to a wide range of DO values (2.9 to 8.1 mg/L).

The marked presence of L. setiferus in Mecoacán Lagoon during the dry and rainy seasons (March to September) can be highlighted, whereas F. aztecus and F. duorarum are present throughout the year. In the dry season, Domínguez et al. (2003) similarly observed the high

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density and biomass of L. setiferus in the southern portion of Mecoacán Lagoon (Manatí Lagoon), with 90% of the density and biomass of penaeid shrimp corresponding with this species. Pérez-Castañeda and Defeo (2001) identified greater differences over time (one to four months) in the population parameters of penaeid shrimp in Celestun Lagoon and suggested a clear link between the life cycle stages and the time of residence of three to four months in the estuary. In Mecoacán Lagoon, this tendency was also observed for the species 17

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F. aztecus and L. setiferus; however, F. duorarum presented high density during eight months of the study cycle (March to October). The seasons presented differences in the physical-chemical variables of water, which can

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influence the assemblage and distribution of shrimp (Hajisamae and Yeesin, 2014). In penaeid shrimp, the temporal distribution of species is an important mechanism for reducing interspecific competition (Pérez-Castañeda and Defeo, 2001; Lüchmann et al., 2008; May-Kú et al., 2014). In Mecoacán Lagoon, different temporal patterns in density were presented: F. aztecus was present during the months of March to May but peaked in density during October, whereas F. duorarum showed its maximum density from March to October. Litopenaeus setiferus showed high density from May to August. Notably, this latter species was distributed in sites with low salinity and DO in contrast with F. duorarum. Wakida-Kusunoki et al. (2008) also identified temporal patterns of use in the lagoon zone of Madre Lagoon: The highest

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abundance values of each species occurred during different periods of the year. In the present study area, complementary studies analyzing the temporal variation in the distribution of the different class sizes of each species of penaeid shrimp per habitat and site could enable a more complete understanding of the population dynamics of these species (Baker and Minello,

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2010; May-Kú et al., 2014).

Flores et al. (1996) reported in 1990 that the maximum density of penaeid shrimp in Mecoacán Lagoon occurred during the months of June (1.2 ind•m2), August (1.4 ind•m2), and October (2.2 ind•m2). In the present study, differences in the total maximum density of penaeid shrimp varied according to collection technique. In the seine net, the maximum densities were

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encountered during the months of May, June, and August (2.2, 2.16, and 3.6 ind•m2, respectively), whereas in the renfro net, these were encountered during the months of May, September, and October (1.3, 1.4, and 1.5 ind•m2, respectively). These differences in the number of collected shrimp per collection technique can be explained by two factors: 1) the selectivity (per size) of the collection nets (seine and renfro) (Broadhurst et al., 2016) and 2) the combined effects of the collection techniques and the segregation in the spatial habitat use of the species. The variation in density might also be explained by ontogenetic changes

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in behavior (Lorenagan et al., 1994; Kenyon et al., 1995). 5. Conclusions

The spatial patterns in the segregation of penaeid shrimp in Mecoacán Lagoon suggest that the distinct temporal distributions and habitat preferences of these species are important for reducing interspecific competition. Salinity, DO, organic matter content, and sediment type were the factors that most influenced the spatial-temporal differences in the density and 18

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biomass of penaeid shrimp among sites. Further studies of the movement of penaeid shrimp among habitats and its relationship to the development (ontogeny) of organisms are recommended. In addition, it is important to characterize the structure of seagrasses and the border of mangroves (habitat complexity), as these are critical habitats and elements that

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influence the colonization patterns and preferences of crustacean species. Finally, the monitoring of the recruitment parameters and habitat preferences of shrimp species of commercial importance is important, as this information can be used as a baseline for modeling subsequent scenarios such as the effects of climate change or restoration on estuarine recruitment. Acknowledgments

This work was supported by Network of Natural Protected Areas (CONACYT 269540) and

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Network for the Knowledge of Coastal Resources in Southeastern Mexico (RECORECOS 293923). Jony R. Torres was a recipient of a PhD fellowship from Consejo Nacional de Ciencia y Tecnología, Mexico (377996). References

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Author statement

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Dr. Jony Ramiro Torres Velázquez Conceptualization Methodology

Formal analysis Writing - Review & Editing Dr. Everardo Barba Macías Conceptualization Methodology Resources Supervision

Funding acquisition

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Dr. Alberto de Jesús Sánchez Martínez Methodology

Supervision

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Writing - Review & Editing

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Declaration of interests ☒ The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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☒The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: