Can the collection of "Tyrian purple" from Plicopurpura pansa (Gould, 1853) (Prosobranchia, Muricidae) be blamed for its declining population?

ABSTRACT Marked, sized and sex determined purple snails Plicopurpura pansa, (Gould, 1853) were distributed randomly among other snails in crevices of an intertidal rocky island splashed during high tides by high impact waves. After 89 days 18%, after 117 days 12%, after 145 days 8% and after 183 days only 3% of the marked snails could be recovered. There was no statistically significant difference between size and sex and the recovery rate. In the laboratory we determined the time needed for reattachment to the surface under different situations. Snails placed with the aperture down on a wet surface or in water reanached themselves after about 20 min, snails placed in water on their backs; in about 40 min, and snails left on a wet surface on their backs after 2 hours. After 4 hours only 50% of the snails placed on their backs in a wet surface were found to be reanached. Great differences were noticed in the period needed for reattachment among individual snails. The time needed for the snails to overcome the stress of being detached from the surface and to reattach themselves again can be blamed for the loss of animals during the increasing incoming tides combined with the high impact wave actions. The prohibition of "milking" P. pansa to obtain "Tyrian Purple" and to collect the snails as a bait for fishery or as a special food for foreigners should be enforced and should be extended to the removal the snails from the crevices of intertidal rocks.

KEY WORDS: purple snail, Plicopurpura pansa, muricidae

INTRODUCTION

In antiquity, the "Tyrian purple" from the Mediterranean muricids, Murex trunculus, M. brandaris and Purpura haemastoma was used extensively to dye materials for the nobility. Because of the enormous number of snails to be killed for the extraction of a minute amount of the chromogens produced by the hypobranchial gland, the scarcity of the snails, and the technical difficulties to obtain the final dye explains why "Tyrian Purple" was at that time a most expensive luxury article. A remarkable exception amongst the muricids is Plicopurpura pansa (Gould, 1853) from the Pacific coast of Central America and Mexico, because this mollusc ejects its dye-producing liquid in such a quantity that there is no need to kill the animal to obtain the purple. Furthermore, the dye-producing hypobranchial gland is so active that the snails can be "milked" periodically without harming them (Rios-Jara et al. 1994, Naegel 2005). It is possible that "Tyrian Purple" from P. pansa was used on the Pacific coast of Central America and Mexico before Columbus, however our current knowledge about this is very limited. During the Spanish rule, the peninsula of Nicoya in Costa Rica was center for the production of "hilo morado," which played an important commercial role for the church to charge for their services in "hilo morado," and for the "gold-hungry" Spanish magistrates to obtain an income from exports to Central and South America. The high demand for "hilo morado" resulted in a decreased population of P. pansa, even leading in 1760 to an uprising of the indigenous people in Nicoya against the Spanish administration (Fernandez-Guardia 1938, Jinesta 1940). From written reports it is seen that at the end of the 19th century indigenous people from Mexico (Martens, v. 1874) and Nicaragua (Schunck 1880) dyed textiles with "Tyrian Purple" obtained from P. pansa. Von Martens mentioned that the high value of purple dyed skirts is explained by the high number of snails needed, which are not numerous at Tehuantepec (Oaxaca) (Martens, v. 1898). In 1909, the ethnologist Zelia Nuttall visited Tehuantepec, and she also reported that the population of the purple snails seemed to be over-exploited and became scare, in spite of the careful treatment of the snails during the "ink" collection (Nuttall 1909). In recent years, with the increasing interest in natural colors, the commercial exploitation of the purple snail for dyeing kimonos with natural "Tyrian purple" had reached in Mexico, in the States of Oaxaca, Nayarit, Guerrero and Michoacan, such levels as to threaten the survival of the species (Castillo-Rodriguez & Amezcua-Linares 1992, Acevedo-Garcia 1995). In 1988 P. pansa had to be declared a species under special protection by the Mexican government (Anonymous 1988, Anonymous 1994).

Like following a golden thread in the history of the exploitation of P. pansa for the production of "Tyrian Purple" it can be observed that it resulted in a decrease of the snail population, in spite of careful treatment of the snails during the "ink" collection and replacement afterwards on the rocks where they have been previously removed. Naegel (2005) has shown that removing the snails from the surface, and Rios-Jara et al. (1994) and Naegel (2005) have demonstrated that periodically collecting the secretion of the hypobranchial gland does not harm the animals. What are the reasons for the declining snail population after "milking"? In a previous study Ramirez-Rodriguez and Naegel (2003) suggested that the snails are just washed away by high impact waves from the rocks after "milking" before being able to attach themselves. In this study this suggestion will be followed up under natural conditions with marked and recaptured snails of different sizes and sexes. Snails reared in the laboratory were used for the determination of the time needed to reattach themselves to the surface after being removed. The results will serve as a prerequisite for the planning, site selection and management of the potential exploitation of P. pansa for its "Tyrian purple."

MATERIALS AND METHODS

In the laboratory at CICIMAR (La Paz, Baja California Sur, Mexico) from 431 P. pansa snails the size and sex were determined and afterwards they were tagged with colored and numbered marks as used in bee-keeping. On November 11, 2005 the snails (266 males with an average total shell length of 27.9 mm; range 17.5-44.4 mm and 165 females with an average total shell length of 30.36 mm; range 18.2-47.4) (Table 1) were transferred to Playa Cerritos (23[degrees]19'49"N, 110[degrees]10'45"W) (Fig. 1) about 120 km southwest of La Paz, Baja California Sur, Mexico and placed randomly amongst other P. pansa snails in crevices on an intertidal rocky island. At low tide the basalt rock covers an area of about 800 [m.sup.2], from which, even at low tides, are accessible only about 400 [m.sup.2] because of the high impact waves striking the rock. The island has several elevated points, the highest with 3.04 m above the mean tide water level, with many crevices located opposite the impact of the waves. We determined in a rough estimate that only about l/8th of the total rock area is suited as a habitat for P. pansa.

[FIGURE 1 OMITTED]

The island was revisited during extreme low tides after 89, 117, 145 and 183 days, the marked animals recaptured, and afterwards placed carefully amongst other snails in crevices. The number and size of the recaptured marked snails was examined to determine possible effects of size and sex on the rate of recovery, and [chi square] test applied to determine significant differences. A level of significance of P < 0.05 was applied.

In the laboratory we determined the time needed for snails of different sizes (n: 382, average size: 32.2 mm, size range: 19-46.1 mm, SD [+ or -] 4 mm) and sex (males: n = 96, average size: 32.2 mm, size range: 24.3-44 mm, SD [+ or -] 3.8 mm; females: n = 96, average size 33.5 mm, size range; 23.1-46.1 mm, SD [+ or -] 4.6 mm) to reattach. For each position of the snails we repeated the experiments four times. We used a transparent plastic tray with a 5-cm wall height to observe the attachment of the foot of the snails to the surface. In the experiments with snails lying on their backs on the wet surface and after 4 hours remaining unattached to the surface we had to sprinkle a few drops of seawater on the operculum to prevent dehydration of the animals. To determine whether possible differences exist between laboratory and field snails in the time for reattachment required, we performed two additional experiments at Playa Cerritos with snails (n = 48; average size: 28.7 mm; size range: 22-36.9 mm; SD [+ or -] 3.8 mm).

The differences in the time needed for reattachment to the surface in the field and in the laboratory among the different size classes and sex were determined by 1-way ANOVA. The Tukey test was further used to determine significant differences and P < 0.05 was used as the significance level.

RESULTS

On November 11, 2004, during an extreme low tide (tidal difference between low and high tide: 1.89 m), 431 marked snails were placed randomly amongst other P. pansa snails in crevices of the intertidal rocky island.

After 89 days (difference between low and high tide of more than 2 m) 77 marked snails were recovered (57 males and 20 females), after 117 days 52 animals (19 females, 33 males), after 145 days 36 snails (12 females and 24 males) and after 183 days (difference between low and high tide: 1.30 m) 13 animals (no females and 13 males). To determine if the size of the animals had an impact on the likelihood of recovery, the recovered snails were divided into three size classes. Table 2 shows in three size classes the number of recovered females and males during the experimental period. After 89 days from the size class 17.5-26.4 mm 27% of the animals were covered. From the size class 26.5-35.4 mm 14% of the snails were recovered. From the larger size class (35.5-47.4 mm), after 117 days, not one male and after 145 days only one female was recovered. After 183 days of the experiment not one female was recovered from all three size classes, and from the male snails 7% from the smallest and only 3% from the medium size group. No statistical differences were found among the three size classes.

In the laboratory we determined the time needed for reattachment of the snails to the surface. Great differences were observed between individual snails and the time needed for their reattachment. These individual differences could not be statistically related to the size or sex of the animals (P > 0.05). For animals placed on their backs on a wet surface, it took an average of more than 2 hours for reattachment (Fig. 2). Seventy percent of the snails placed with the aperture down on the wet surface, or in water, reattached themselves on the surface only after 20 min, and 90% of the snails were reattached after 1 h (Fig. 3). There was no statistic difference (P > 0.05) in the time needed for reattachment between snails placed on the aperture in water and on a wet surface. Animals placed on their backs on the wet surface and in water behaved differently. A statistical difference (P < 0.05) was found among animals placed their backs on the wet surface and the other three groups. After 2 hours, 80% of the snails on their backs in water tuned over on their aperture and attached themselves to the surface, and after 6 hours 86% were attaching. From the 96 snails placed on their backs on the wet surface, only 50% were attached after 4 hours. After 4 hours the remaining 48 snails received a few drops of seawater on the operculum and the animals revived, and after 6 hours 86% of the snails were found attached to the surface (Fig. 3). This result shows the danger, for snails lying for longer periods in the dry on their backs, of being desiccated (Fig. 3).

[FIGURES 2-3 OMITTED]

We determined at Playa Cerritos the time needed for reattachment of snails placed with the aperture down and in water. The average time for reattachment took 11.7 min (SD [+ or -] 13.5 min). A result, which is statistically not different (P < 0.05) to the findings from the laboratory tests described before.

DISCUSSION

The recapture rate of snails placed carefully into crevices was astonishingly low. After 89 days of the 431 snails only 18% were recovered, mainly (27%) from the smallest size class. It is more likely for large and not yet attached animals to be swept away by strong waves. After 183 days of the experiment only 3% of the animals (13) were recovered. Wave-swept shores, like the intertidal rocks at Playa Cerritos, are physically harsh environments, and only crevices give the snails protection from not being washed away by high impact waves during high tides. P. pansa is a most spatially restricted species and over 75% is found primarily in crevices (Garrity, 1984). This microhabitat is important in reducing temperature and water loss. P. pansa is extremely sensitive to heat and desiccation on open surfaces. Animals removed from the crevices during daytime low tides reach higher tissue temperatures, lose more mass and suffer higher mortalities than control animals (Garrity 1984). Removing the snails carefully from the surface and replacing them afterwards in water does not cause mortalities (Naegel 2005). This finding is in contrast to the report by Castillo-Rodriguez and Amezcua-Linares (1992) who blamed the mortalities on the brusque removal of snails from the crevices, and the bending of the operculum and the muscular foot for the extraction of the dye precursors. Acevedo-Garcia (1995) mentioned differences in the way commercial "ink-collectors" and traditional indigenous people remove the snails from the crevices in the rocks: not to harm the animals the indigenous people use a wooden stick in the form of a spatula, the "ink-collectors," however, use a hook made out of wire, which sometimes breaks the shell. Acevedo-Garcia (1995) also mentioned the different methods used by indigenous people and commercial "ink-collectors" to obtain the dye secretion. To stimulate the expulsion of the "ink" the indigenous people spit and/or blow on the operculum, in contrast to the commercial "ink-collectors" who press the operculum with the thumb, which causes a weakening of the fixation of the animals to the rocks, from where they can easily be washed away by the strong waves. Some "ink collectors" place the snails after "milking" together with their "milk" in a small pot. The narcotizing compounds in the "milk" reduce the capability of the snails, after their release, to attach themselves fast enough, and consequently are in danger of being washed away.

During our field experiments we didn't use a spatula or a hook to remove the snails from the crevices so as not to hurt them. We replaced carefully the snails again in crevices. Despite all this care the recovery rate was very low.

The removal and the "milking" of the purple snails cannot alone be blamed for its declining population. The main reason is the time needed for reattachment to the surface, especially when the snails are placed on their backs and in dry locations. The attachment of the snails after replacing them on the surface takes too long and does not prevent them being washed away by the incoming tides. The period from "milking" until the attachment is a very critical phase for these animals. In the laboratory tests it took 2 hours for reattachment for 50%, and six for 80% of the animals placed on the back and on a wet surface. As soon as the animals are attached by their large foot muscle to the surface they are relatively safe from being displaced. Additionally the strong shell gives P. pansa protection against destruction by the waves. The removal of the purple snail from rocks causes a never-before-experienced situation and stress to the snails. Individuals respond in different ways by needing different periods for reattachment to the surface. The careful replacement of the snails after their removal from the rocks with the aperture down, on a moist surface or even in water, helps them to recover from the stress, and to reattach themselves. However, even under the most careful conditions of replacement some snails need long periods before reattachment and are in danger of being washed away during the approaching high tides with their high impact waves.

Today's commercial "ink-collectors" work under piecework conditions: the larger number of skeins dyed with the secretion of the snails in less time results in higher profits, but also inevitably in a larger number of snails "milked" and less care for their reattachment and conservation (Acevedo-Garcia 1995). In the past a similar situation existed in Costa Rica where the indigenous people had to fulfill the demands for "hilo morado" by the Spanish administrators and priests. This rush of work often results in the snails not being removed carefully from the rocks, not "milked" with care and at the end are left exposed to the strong wave actions of the sea or to the sun thus causing the death of the animals. Additionally, because female snails reach larger sizes than males and because of their larger size expel more secretion, they are preferred by "ink" collectors. Furthermore, the collection, especially of larger-sized purple snails as a special food for foreigners, is a recent development, which causes a reduction in recruitment and a decrease in the snail's population. However, not only the activities of collectors of the purple snail but also the increased effects in recent years of water contamination can be blamed for the decrease in snail populations (Castillo-Rodriguez & Amescua-Linares 1992).

A strict enforcement of the prohibition of collecting P. pansa is needed for the conservation of the purple snail, yes, even the prohibition to remove snails from the crevices of wave swept rocks. Additionally intensive research is required for the controlled reproduction to restock over-exploited areas.

ACKNOWLEDGMENTS

The authors thank Irma Castanon-Estrada and Anabel Rosales-Maldonado (U.A. Nayarit) for their help in determining the sex of the snails. Special thanks to Chris Cooksey for making suggestions to improve earlier versions of the manuscript and to the anonymous reviewers for their comments and corrections. This work was supported by grants from CGPI, COFAA and EDI (Instituto Politecnico Nacional, Mexico).

LITERATURE CITED

Acevedo-Garcia, J. 1995. Aprovechamiento del tinte de Purpura pansa en el Pacifico Mexicano. Secretaria de Medio Ambiente Recursos Naturales y Pesca; Instituto Nacional de la Pesca; Centro Regional de Investigacion Pesquera-Patzcuaro, Mexico. 22 pp.

Anonymous. 1988. Acuerdo intersecretarial que regula el desarrollo, conservacion y aprovechamiento de la especie denominada caracol Purpura pansa, en beneficio de los nucleos de poblacion que tradicionalmente lo ban explotado y dispone las medidas necesarias para la preservacion de las costumbres y tradiciones derivadas del aprovechamiento del molusco. Diario Oficial de la Federacion. Secretaria de Pesca, Mexico. March 30,1988. pp 10-12.

Anonymous. 1994. Norma Oficial Mexicana NOM-ECOL-059-1994, que determina las especies y subespecies de flora y fauna silvestres y acuaticas en peligro de extincion, amenazadas, raras y las sujetas a proteccion especial y que establece especificaciones para su proteccion. Diario Oficial de la Federacion, Mexico, May 16, 1994. pp. 2-56.

Castillo-Rodriguez, Z. G. & F. Amezcua-Linares. 1992. Biologia y aprovechamiento del caracol morado Plicopurpura pansa (Gould, 1853) (Gastropoda: Neogastropoda) en la costa de Oaxaca, Mexico. An. Inst. Cienc. del Mar y Limnol. Univ. Nal. Auton. Mexico 19(2):223-234.

Fernandez-Guardia, R. 1938. La sublevaciondes indios de Nicoya en 1760. Revista de los Archivos Nacionales (San Jose, Costa Rica) 2(7-8): 362-366.

Garrity, S. D. 1984. Some adaptations of gastropods to physical stress on a tropical rocky shore. Ecology 65(2):559-574.

Jinesta, R. 1940. Las industrias del anil y de caracol de purpura. Revista de los Archivos Nacionales (San Jose, Costa Rica) 4(5-6): 302-304.

Martens, V. E. 1874. Purpur und Perlen. Sammlung gemeinverstandlicher Vortrage (Berlin) 9(214): 845-905.

Martens, V. E. 1898. Purpur-Farberei in Central-America. Z. Ethnol. 30: 482-486.

Naegel, L. C. A. 2005. The effect of periodically "milking" to obtain Tyrian Purple from Plicopurpura pansa (Gould, 1853) on the frequency of expulsion and mortality. J. Shellfish Res. 24(1):85-90.

Nuttall, Z. 1909. A curious survival in Mexico of the use of the purpura shell-fish for dyeing. In: Putnam Anniversary Volume. Cedar Rapids, Iowa: The Torch Press. pp. 366-384.

Ramirez-Rodriguez, M. & L. C. A. Naegel. 2003. Growth of the purple snail Plicopurpura pansa in Baja California Sur, Mexico. Ciencias Marinas 29(3):283-290.

Rios-Jara, E., H. G. Leon-Alvarez, L. Lizarraga-Chavez & J. E. Michel-Morfin. 1994. Produccion y tiempo de recuperacion del tinte de Plicopurpura patula pansa (Neogastropoda: Muricidae) en Jalisco, Mexico. Rev. Biol. Trop. 42(3):537-545.

Schunck, E. 1880. LII. Notes on the purple of the ancients (continuation). 3. Purple dying in modern times. J. Chem. Soc. 37:613-617. (London)

LUDWIG C. A. NAEGEL * AND JORGE A. LOPEZ-ROCHA Centro Interdisciplinario de Ciencias Marinas, Instituto Politecnico Nacional (CICIMAR-IPN) Apdo. Postal 592 LA PAZ, B.C.S. 23000, Mexico

* Corresponding author. E-mail: [e-mail]

TABLE 1.
Size ranges of marked male and female of P. pansa snails
distributed on November 11, 2004 at Playa Cerritos,
Baja California Sur, Mexico.

                 Males             Females

Size (mm)     N        SD       n        SD

17.5-26.4     90      1.78      40      1.99
26.5-35.4    165      2.46      88      2.32
35.5-47.4     11      2.77      37      2.61
Total        266      4.04     165      5.54

SD = Standard deviation

TABLE 2.
Size classes of P. pansa snails recaptured at Playa Cerritos,
Baja California Sur, Mexico, after 89, 117, 145 and 183 days.

              89 Days       117 Days

Size (mm)   Number    %    Number    %

17.5-26.4     35     27%     15     12%
26.5-35.4     36     14%     34     13%
35.5-44.4      6     13%      3      6%
Total         77     18%     52     12%

              145 Days       183 Days

Size (mm)   Number    %    Number    %

17.5-26.4     10      8%      7     5%
26.5-35.4     25     10%      6     2%
35.5-44.4      1      2%      0     0%
Total         36      8%     13     3%