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Rol de la temperatura en el ciclo reproductivo de Thais chocolata (Gastropoda, Muricidae) en Chanavaya, Tarapaca, Chile.

Role of temperature in the reproductive cycle of Thais chocolata (Gastropoda, Muricidae) in Chanavaya, Tarapaca, Chile


Thais chocolata (Duelos, 1932) is a mollusk found between Paita, Peru, and the Valparaiso region in Chile (Osorio, 2002). Historically it has been an important benthie resouree for artisanal fishing economy in northern Chile. However, given the high exploitation levels since 1978, and after reaching the maximum catch level in 1986 with 8,244 ton (Avendano et al., 1998), the vulnerable fraction of the shallow area strongly decreased. Extraction of T. chocolata is currently restricted to the Arica and Parinacota, Tarapaca, and Antofagasta regions, where in 2010 only 160 ton (SERNAPESCA, 2010) were extracted, corresponding to the lowest catch level since the beginning of the resource's exploitation.

This snail is distributed in depths between 5 and 40 m, over rocky and shell substrates and over thick sand (Andrade et al., 1997; Avendano et al., 1997, 1998). It is a gonochoric species, with internal fertilization and without external evidence of sexual dimorphism (Rojas et al., 1986). During the reproduction season, adults concentrate forming aggregations (Retamales & Gonzalez, 1982; Avendano et al., 1997, 1998), as occurs with other species of this genus (Bertness, 1977; Palmer, 1983). This strategy, in which adult specimens group together during reproductive seasons, has serious consequences for their survival, given that fishers resort mainly to these aggregations for extraction (Andrade et al., 1997; Avendano et al., 1997, 1998). In Chile, closed seasons have been established with fixed extraction periods to protect the reproductive activity. However, the few studies concerning the reproductive cycle (Andrade et al., 1997; Avendano et al., 1997, 1998), and which currently sustain this closed season, showed that the species does not present a specific reproduction season, with mature specimen being present the entire year, and showing certain increases in presence during some months. Clutches can also be observed during most of the year, invalidating the establishment of fixed extraction periods. These studies have also shown that sexually immature females are frequently found in deeper areas, while mature specimens tend to be found in more shallow waters (Retamales & Gonzalez, 1982; Rojas et al., 1986; Andrade et al., 1997; Avendano et al., 1997, 1998).

There is little information concerning exogenous factors acting on the reproduction processes of this species, considering that temperature and feeding have been proven to be the most influential factors on the reproductive cycles of mollusks (Pena, 1987; Roman et al., 2001; Michel-Morfin et al., 2002; Ponce-Diaz et al., 2003). With the objective of showing whether the reproductive process of this species responds to environmental temperature variations, in the present study we have monitored the reproductive cycle of this gastropod, its distribution between 5 to 20 m depth, and the temperature of the deep section of an exposed area in the Tarapaca region, Chile.


The study area is located in Chanavaya (20[degrees]53'S, 70[degrees]08'W), Tarapaca region, Chile. In this area T. chocolata is distributed over a rocky substrate, associated in the shallow areas with banks of the mytilidae Chorumytilus chorus (Molina, 1782), and the brown algae Lessonia trabeculata (Villouta & Santelices, 1986), and in the deep area, with banks of the mytilidae Aulacomya ater (Molina, 1782) which extends over 30 m depth. This area is located in a subtropical transition zone, with predominance of the Subantarctic Water mass (SAAW), which dominates the upper 200 m of the northern branch of the cold Humboldt Current System. These waters (SAAW), mix with a lower proportion of Subtropical waters with greater salinity and temperature, and also periodically mixed with colder Equatorial Subsurface waters from greater depths, which rise to the coast given upwelling processes induced by south and southwest winds that predominate in the area (Avendano & Cantillanez, 2008).

A data loggers (model Tid Bit, onset), programmed to register temperature measurements every hour, starting February 2009 through January 2010, was installed in the study area at 16 m depth, with the objective of evaluating the potential role of temperature in the reproductive process of T. chocolata.

Between early February 2009 and January 2010, random monthly samplings between 5 and 20 m depth were carried out by diving, to determine the distribution of T. chocolata through density (20 m is the authorized limit for compressor diving, used by mollusk divers in the extraction of benthic resources in Chile (Armada de Chile, 2006)). For this purpose, three sampling transects were marked using a GPS map 76CSx Garmin. These transects were separated by 100 m from each other and covered both isobaths. In each one of these transects, the specimen density was determined randomly, dropping a 1 [m.sup.2] quadrant and replicating it 10 times along said transect. On each sampling point, the depth was registered using a Beuchat CX 2000 comex submarine computer.

The resource distribution model was characterized using the Morisita Dispersion Index (1962), reinforced using the Standardized Index (Smith-Gill, 1975), which acts independently of studied population density and sample size (Myers, 1978). The Standardized Index turns the values of the original index into an absolute scale varying between -1 and +1, with a confidence interval between +0.5 and -0.5 at [alpha] = 0.05. For this index, random patterns mark 0, values above 0 represent aggregated distributions and values below 0 correspond to a uniform distribution pattern.

A submarine route was followed to detect the presence of T. chocolata reproductive aggregations, covering a distance of 300 m parallel to the coastline between 5 to 17 m depth. The reproductive cycle of T. chocolata was studied from a monthly sample of 40 specimens over 30 mm of maximum length, extracted from the three sampled transects. An additional sample of 25 specimens was added every time reproductive aggregations were found. The extracted specimens were transported to the laboratory where they were dissected and sections of the middle area of the gonad-hepatic gland complex of 100% of the females (considering that they better represent the reproductive processes (Cantillanez et al., 2011)), were fixed in Bouin and included in paraffin. Cuts 6 um thick were colored with hematoxylin and eosin (Gabe, 1968), and were then microscopically analyzed to classify their maturity state, according to the scale proposed by Cantillanez et al. (2011).


During the period of study, the average daily temperature, registered at 16 m depth, varied between 13.6 and 16.8[degrees]C (Fig. 1a). During May, June, July, and December 2009 and January 2010 the average monthly temperature rose above 15[degrees]C, while a strong decrease was registered during April 2009, the coldest month, with an average of 13.8[degrees]C (Fig.1b).

The density of T. chocolata in the sampled strata varied between 0 and 27 ind [m.sup.-2], presenting an aggregate distribution according to the Morisita Index (Table 1). Considering this aggregated distribution, the average monthly abundance was determined from the quadrants with a registered presence of specimens, within the stratus in which reproductive aggregations were found (5 to 17 m depth). The results obtained using this criteria showed important specimen abundance increases during June-August, with averages between 10.1 and 8.4 ind [m.sup.-2], and during December-January, with averages of 9.0 and 14.0 ind m-2, respectively (Fig. 2).

The reproductive stages of female T. chocolata in the samples showed that maturity was present during the entire year, in proportions varying between 45.7 and 83.9%, with the highest levels registered in May 2010 (Fig. 3). Specimens with evacuated gonads (fluctuating between 3.0 and 42.9% of the sample), were registered during the entire study period except in April and May (Fig. 3). The integration of both reproductive stages (mature and evacuated), showed that the highest percentages occurred during July-August with 85.2 and 88.6% of the population, respectively, and in December-January with 85.7 and 100% respectively.

The studies carried out searching for reproductive aggregations of T. chocolata with specimens in copulation and clutch laying in capsules, showed their presence in 4 and 16 m depth isobaths, from early February to late August 2009, and reappearing in January 2010. The aggregations detected between early February and April were small, with no more than 100 specimens (Fig. 4a), and were located between 7 and 16 m depth. In May, only one aggregation with over 100 specimens was found at 4 m depth, while in early June new aggregations began to form at 12 m depth. In July the magnitude of these aggregations grew significantly, reaching the 14 m depth isobaths and containing several thousands of specimens (Fig. 4b). These were however extracted by the local fishers, who reported a catch of around 12 ton. In August, large extensions of clutches were observed in different maturity stages with the isolated presence of breeders. During October only capsules with eggs and without breeders are observed at 15 m depth. However, in January 2010, new important aggregations were registered at 5, 8, and 15 m depth, again extracted by the local fishermen.

The extractions affecting the July aggregations left clutches with unprotected eggs (Fig. 8c) causing a strong predation (Fig. 8d) by other gastropods such as Priene spp., Mitrella unifasciata (Sowerby, 1832), and Mitra orientalis (Griffith & Pidgeon, 1838); equinoderms such as Stichaster striatus (Muller & Troschel, 1880), and fishes such as Chromis crusma (Valenciennes, 1833) and Cheilodactylus variegatus (Valenciennes, 1833).


Results obtained from the histological analysis, showed that the gonad development of T. chocolata is not a synchronic process, with the presence of specimens in different phases of gametogenesis development, and with predominance of mature females during the entire year. The presence of mature specimens of this resource during different months has also been mentioned in other studies (Rojas et al., 1986; Andrade et al., 1997; Avendano et al., 1997), as well as with other species of the same family, reported by Rojas et al. (1986), such as Morula marginalba (Blainville, 1832), Thais emarginata (Deshayes, 1839) and Thais canaliculata (Gray, 1839). An asynchronic reproductive process with significant maturity periods during some months has also been found for the Muricidae Concholepas concholepas (Bruguiere, 1789) by Aviles & Lozada (1975) and Ramorino (1975).

The permanent existence of mature and evacuated females in variable proportions and the presence of reproductive aggregations in shallow waters, in which mainly adult specimens concentrate in high densities for copulation and clutch laying, allow us to determine that the reproductive process of T. chocolata, in the shallow stratus, occurs with greater or lesser intensity during the entire year. However, the increase in aggregated specimens during June-July and January, as well as the high percentage of evacuated specimens during those months, allow establishing those periods as the ones with highest reproductive activity. Intense clutch laying periods occurring during JuneSeptember and February-March have also been found for other populations in Peninsula Serrano Tarapaca (Retamales & Gonzalez, 1982), while in La Rinconada (Antofagasta, Chile), large aggregations have been registered in June (Avendano et al., 1997), and in the last years, also during December-January (Cantillanez et al., 2011), showing variability in the more important events. Rojas et al. (1986), also pointed out this variability for populations in the Pisco area in Peru, with the occurrence of intense reproduction periods in October 1978 and in August 1975. These variations in T. chocolata reproductive events in the northern Chile populations could be a response strategy to the temperature variability presented by the environment. In several gastropods such as Haliotis discus hannai (Reeve, 1886), H. tuberculata (Linnaeus, 1758), H. midae (Linnaeus, 1758), C. concholepas, and Strombus luhuanus (Linnaeus, 1758), temperature variations have been mentioned as one of the main factors that influence gonad maturation (Pena, 1987). One of the characteristics of the studied zone is the temperature variations which alter the seasonal cycle as a response to irregular cold water upwelling processes present during most of the year, with intense periods during summer and winter (Escribano et al., 1995, 2002; Blanco et al., 2001). The variability of this annual cycle could explain the interannual temporal variations presented by the reproductive aggregations, which along with demonstrating the ineffectiveness of proposing fixed extraction periods could induce new studies to contrast said hypothesis.

The results obtained show that the most important reproductive aggregations (June-July and January), coincide with periods presenting temperatures above 15[degrees]C, and that the decrease in reproductive activity observed during early April is associated with a decrease in temperature maintained until early May. This relation also allowed observing that periods of abrupt temperature variations in short periods of time (decrease from 16.5 to 18.5[degrees]C between May 25 and 31; and decrease from 16.1 to 18.8[degrees]C between December 29 and 31, 2009) preceding the formation of aggregations could act as a precursor mechanism for mature specimens to begin aggregating. In the gastropod (Muricidae) Plicopurpura pansa (Gould, 1853) reproduction begins following a temperature drop (Michel-Morfin et al., 2002).

Although the results show an aggregate distribution of T. chocolata during the entire year, the abundance of specimens found within the stratum containing reproductive aggregations (5 to 17 m) increased before, during and following the formation of these aggregations. This shows a change in the degree of spatial aggregation in these periods, as has been observed in the La Rinconada population (Avendano et al., 2010). This increase in population density in the shallow levels, independent of the formation of aggregations, could be used as an indicator of the reproductive activity of T. chocolata for monitoring future aggregation and clutch laying processes.

The specimen's strategy of aggregating in shallow waters to reproduce could guarantee the dispersion of the larvae, considering that T. chocolata presents planktotrophic teleplanic larvae, which after remaining approximately one month in the capsules and four months in plankton reaches competition (Romero et al., 2008). Long larval life periods extending over several months in larvae capable of responding positively to light and establishing close to the surface, as occurs with the larvae of several gastropods, reflects their capacity of overcoming major biogeographic barriers for colonization after being dispersed by wind and surface currents (Scheltema, 1989; Gasca et al., 1998; Stoner & Smith, 1998; Oliva-Rivera & De Jesus-Navarrete, 2000). The in situ observations carried out show that the aggregations in shallow waters also provide protection to the clutch capsules until the hatching and dispersal of the larvae, with the adult breeders avoiding predation with their bodies. This has also been indicated for the gastropods Fusitriton oregonesis (Redfield, 1886), Thais lamellosa (Gmelin, 1791), and Purpura pansa (Gould, 1853) (Stickle & Mrozek, 1973; Acevedo & Hernandez, 1988).

The combined effect generated by the extraction of aggregated specimens, the predation on the clutches following this extraction and the long larval life cycle greatly increase vulnerability levels and would be the main causes for uncertainty concerning the extraction process which has unbalanced the ecosystem dynamics where the species develops. This calls for a greater protection of the resource during the reproductive aggregation process, which has been shown to vary in time making the establishment of closed seasons an ineffective means to manage this objective.

DOI: 103856/vol41-issue5-fulltext-6


The present study was carried out through the project FIP 2008-27.


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Received: 16 January 2013; Accepted: 28 August 2013

Marcela Cantillanez (1) & Miguel Avendano (1)

(1) Departamento de Ciencias Acuaticas y Ambientales, Universidad de Antofagasta Av. Angamos 601, Antofagasta, Chile

Corresponding author: Miguel Avendano (

Table 1. Morisita Index (Id) and Standardized Morisita
Index (Ip) obtained for T. chocolata between 5 to 20 m
depth, February 2009 and January 2010 in the Chanavaya

Date          Ip          Id       Decision

Feb-2009   0.5038752   1.8621889   Aggregate
Mar-2009   -0.828808   1.2561576    Uniform
Apr-2009   0.5101076   1.5158371   Aggregate
May-2009   0.5098268   1.3852818   Aggregate
Jun-2009   0.5158982   1.5623762   Aggregate
Jul-2009   0.5061920   1.2888615   Aggregate
Aug-2009   0.5122887   1.8727668   Aggregate
Sep-2009   0.5125252   1.5918367   Aggregate
Oct-2009   0.5138572   1.5852716   Aggregate
Nov-2009   0.5220768   1.7910888   Aggregate
Dec-2009   0.5182662   1.6578078   Aggregate
Jan-2010   0.5286332   1.7819088   Aggregate
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Title Annotation:articulo en ingles
Author:Cantillanez, Marcela; Avendano, Miguel
Publication:Latin American Journal of Aquatic Research
Date:Nov 1, 2013
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