Research Article |
Corresponding author: Cristian Aldea ( cristian.aldea@umag.cl ) Academic editor: Thierry Backeljau
© 2018 Jorge Holtheuer, Cristian Aldea, Dirk Schories, Carlos Gallardo.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Holtheuer J, Aldea C, Schories D, Gallardo CS (2018) The natural history of Calyptraea aurita (Reeve, 1859) from Southern Chile (Gastropoda, Calyptraeidae). ZooKeys 798: 1-22. https://doi.org/10.3897/zookeys.798.25736
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Hard bottom communities of the Reloncaví Estuary and adjacent areas, Region de los Lagos, Chile (42°S), were studied between 2008 and 2011. All hard substrates between the lower intertidal and 25 m depth were dominated by the calyptraeid gastropods, Crepipatella dilatata and C. fecunda. Epibenthic coverage of the hard bottoms markedly decreased further down with the exception of vertical cliffs. In a depth range between 26 to 48 m repeatedly dense patches of another calyptraeid species, Calyptraea aurita (Reeve, 1859), were observed. Densities reached up to 1475 individuals m-2 and covered up to 50 % of the rock surfaces. In shallower depths C. aurita was not present. However, despite its huge abundance, C. aurita has not been documented for more than 150 years in the southeastern Pacific, being described superficially by Reeve, through only shell characteristics. Here, we redescribe and compare it with other members of the family Calyptraeidae through characteristics of shell, radula, and soft parts, including also details of the egg mass and intracapsular development of their embryos. Males were mobile and females sessile. Shell size ranged from 6.6 to 12.4 mm for immature individuals, from 10.6 to 24.9 mm for males, 15.1 to 25.9 mm for intersex individuals, and from 21.0 to 39.6 mm for females. Up to three individuals stacked together were found, always presenting a female at the base with up to a maximum of two male individuals above. Laboratory studies demonstrated that C. aurita has an indirect larval development, liberating planktotrophic larvae with a bilobed ciliated velum into the water column. A transplantation experiment demonstrated that survival, growth, and reproduction of C. aurita is also possible in depths shallower than its normal distribution. The geographic distribution of C. aurita, was previously only known as being from Valparaíso (33°S) and is now extended down to the Reloncaví Sound (41°S).
Comunidades de fondos duros del estuario de Reloncaví y áreas adyacentes, Región de los Lagos, Chile (42 ° S), fueron estudiados entre el 2008–2011. Todos los fondos duros entre la profundidad intermareal inferior y 25 m fueron dominados por los gasterópodos caliptreidos, Crepipatella dilatata y C. fecunda. La cobertura epibentónica de los fondos duros disminuyó notablemente a mayor profundidad, con la excepción de los acantilados verticales. En un rango de profundidades entre 26 y 48 m fueron observados parches repetidamente densos de una tercera especie de Calyptraeidae, Calyptraea aurita (Reeve, 1859). La densidad alcanzó hasta 1475 ind. m-2 y una cobertura de hasta un 50 % de la superficie de las rocas. En profundidades menores C. aurita no estuvo presente. A pesar de su gran abundancia, C. aurita no se ha documentado desde hace más de 150 años en el Pacífico Suroriental, siendo descrita superficialmente por Reeve, solamente a través de las características de la concha. En este trabajo, nosotros redescribimos y comparamos esta especie con otros miembros de la familia Calyptraeidae a través de características de la concha, rádula y partes blandas, incluyendo algunos detalles de la masa de huevos y desarrollo intracapsular de sus embriones. Los machos fueron móviles y las hembras sésiles. El tamaño de la concha varía entre 6,6 y 12,4 mm para los individuos inmaduros, 10,6 a 24,9 mm para los machos, 15,1 a 25,9 mm para los individuos intersexo y desde 21,0 a 39,6 mm para las hembras. Fueron encontrados hasta tres individuos apilados juntos, presentando siempre una hembra en la base y hasta un máximo de dos individuos machos sobre ella. Los estudios de laboratorio demostraron que C. aurita tiene un desarrollo larval indirecto liberando una larva planctotrófica con un velo ciliado bilobulado en la columna de agua. Un experimento de trasplante demostró que la supervivencia, el crecimiento y la reproducción de C. aurita es posible en profundidades menores que su distribución normal. La distribución geográfica de C. aurita, anteriormente sólo se conocía desde Valparaíso (33°S) extendiéndose hasta el Seno de Reloncaví.
Calyptraeid gastropod, external morphology, growth, radula, reproduction, shell, transplantation
Crecimiento, concha, Gasterópodos caliptreidos, morfología externa, rádula, reproducción, trasplante
Gastropods with external shells belong to the most studied groups of all the marine fauna of Chile due to their economic importance (
Among the 18 known species of Calyptraeidae of the continental coast of Chile (
A major part of taxonomic studies of mollusks is still based on shell characteristics of type specimens (
The family Calyptraeidae counts approximately 139 living species (123 valid) in total (
In May 2008 we noticed for the first time the presence of Calyptraea aurita in depths below 30 m near Caleta Yerbas Buenas (41°40'20"S, 72°39'24"W), Reloncaví Sound, Chile (Figure
Three additional sites were chosen to study the possible presence of C. aurita in the vicinity of the first place: (1) Reloncaví Estuary: 41°42'33.13"S, 72°37'30.95"W, (2) Caleta Gutiérrez, 41°39'15.48"S, 72°40'1.20"W, and (3) Caleta Chaicas: 41°38'17.78"S, 72°40'10.94"W (Figure
The distribution and coverage of C. aurita were studied using transect photographs along a depth gradient and analyzed with the Windows–based software CPCe 3.6 (
In October 2009 a total of 190 individuals were sampled from four quadrants in order to estimate shell length distribution, sex ratio and the relationship between dry tissue biomass and shell length. The samples were fixed in 4% formalin–seawater after sampling. Shell sizes were measured with a digital caliper and sexual maturity status was registered for each individual. Afterwards, tissue biomass was separated from the shell, rinsed with freshwater and dried for 48 h at 60 °C.
Ten specimens were used for the species description. These specimens are deposited in the collections of mollusks, Laboratory of Malacology, Zoology of Invertebrates of the National Museum of Natural History (MNHNCL), Santiago de Chile, and the Instituto de Zoología, Universidad Austral de Chile (
Specimen | Total length | Width | Height | Sex |
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MNHNCL 7570 | 32.92 | 31.89 | 11.64 | female |
MNHNCL 7571 | 28.5 | 28.05 | 10.41 | female |
MNHNCL 7572 | 16.2 | 17.04 | 6.64 | male |
MNHNCL 7573 | 17.14 | 16.44 | 7.66 | male |
MNHNCL 7574 | 37.29 | 34.66 | 13.15 | female |
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21.51 | 21.48 | 9.25 | male |
|
20.88 | 19.69 | 7.83 | male |
|
29.59 | 26.36 | 12.65 | female |
|
25.78 | 25.41 | 11.45 | female |
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33.84 | 33.65 | 12.27 | female |
Scuba divers in the field collected a total of 38 females with egg capsules in their mantle cavity, removing them carefully from the rock. Females without egg capsules were reattached by the divers to the rock. Back at the beach, the collected individuals reattached quickly to acrylic plates stored in coolers with 80 L saltwater and were transferred to the laboratory. Up to ten individuals were allowed to fix on a single acrylic plate, 40 × 45 cm in size. In the laboratory the plates with the attached individuals were transferred to 250 L tanks with permanent water flow and exchange. We used unfiltered seawater for the experiment and did not supply additional food. Intracapsular development was observed every three days with inverted light microscopy.
The different embryonic stages up to the liberation of the larvae are described using the criteria of Wyatt (1960),
An experiment was conducted to determine whether growth and reproduction is possible in shallower depths than those found in the field. Specimens collected at 30 m depth at Yerbas Buenas were marked with numbers on the shore and allowed to reattach onto transparent acrylic plates (25 × 40 cm, 20 individuals per plate). Each animal was measured and the plates with the animals on them were placed vertically at 10 and 20 m depth (four plates in each depth). After 165 and 326 days each animal’s length was measured to monitor its growth. Growth percentage was estimated based on the initial size compared with the final size at the end of the experiment. A t–test was used to compare growth after 165 days in 10 m and 20 m depth. The heavy loss of individuals during the course of time did not allow for the data measured at the end of the experiment to be included in the statistics.
Calyptraea
striata
(non Say, 1826):
Crucibulum
auritum
Reeve, 1859: sp. 17, pl. 6, fig. 17a, b;
[Crucibulum auritum] is housed at
MNHNCL 7570 (female), MNHNCL 7571–7574 and MZUA–UACH 501–505, all specimens from Caleta Yerbas Buenas, 41°40'20"S, 72°39'24"W. All coll. Jorge Holtheuer and Dirk Schories.
Shell (Figures
Shell length in mm of Calyptrea aurita sampled randomly at Yerbas Buenas. N = number of individuals sampled; SD = Standard Deviation.
N | Min | Max | mean | SD | |
---|---|---|---|---|---|
immature | 9 | 6.6 | 12.5 | 9.1 | 1.7 |
Male | 82 | 10.6 | 24.9 | 17.6 | 3.7 |
intersex | 6 | 15.1 | 25.9 | 19.2 | 4.2 |
Female | 83 | 21.0 | 39.6 | 31.7 | 3.5 |
Radula (Figure
Head–foot (Figures
Mantle (Figures
Gill: typical to those of Calyptraea, occupying most of inner pallial space, inserts all along left and anterior pallial margins. Gill filaments also similar to those of Calyptraea, with very long (Figure
Male (Figure
Female (Figures
External morphology of Calyptraea aurita. a female, without shell and whole, dorsal view b same animal, whole, ventral view c male, foot removed, ventral view. Abbreviations: fd: dorsal surface of foot; ft: foot; gi: gill; ll: left lateral expansion (flan); mb: mantle border; ns: neck “sole”; pd: penis sperm groove; pe: penis; pg: pedal gland anterior furrow; pp: penis papilla; pr: propodium; rl: right lateral expansion (flan); sn: snout–proboscis; te: cephalic tentacle. Scale bar: 10 mm (a, b), 5 mm (c).
Calyptraea aurita (Reeve, 1859) is a protandric hermaphrodite producing a maximum of 16 egg capsules per female which contain an average of 119 eggs each (Figure
The females of Calyptraea aurita deposit their eggs in thin–walled brooded capsules directly attached to hard substrates. These capsules have a triangular, flattened morphology and are fixed with a fine stem to the substrate. The eggs are concentrated at the distal end of the sac embedded in an uncoloured liquid. All eggs are able to develop into planktonic veliger stages which are liberated into the water column. The veliger has a bilobed ciliated and pigmented velum and two small black–coloured eyes between the velar lobes, a circular mouth, and a transparent protoconch. The mean initial egg size is ca. 150 μm and the size of the veliger, when liberated into the water column is ca. 300 μm. The intracapsular development up to the larval release took ca. 42 days in the laboratory.
Size: A total of 180 individuals were collected in October 2010 in 30 m depth. Shell length, height, and width were measured. Shell length distribution was two peaked, the first peak corresponded to males and intersex individuals and the second peak to females (Figure
Four samples with 38 to 77 females were taken in October 2010 and were checked underwater for the presence of the pinnotherid decapod Calyptraeotheres politus (Smith, 1870). A total of 4.5 ± 1.3 % of females were infested by C. politus. None of the infested females deposited eggs.
Calyptraea aurita occurs at Valparaíso at depth of 82–110 m (
The experiment was realized for a total time span of 326 days. Several individuals got lost during transport from the experimental depth to the shore, died during course of time, or did not reattach once unintentionally detached from the acrylic plate. Nevertheless all remaining individuals grew several mm in both depths (Figure
Only two valid species of Calyptraea (s. s.) are considered along the coasts of the southeastern Pacific: C. aurita (Reeve, 1859), distributed in central and south Chile, and C. mamillaris Broderip, 1834, from Baja California to Peru. Calyptraea mamillaris differs externally from C. aurita in having only growth striations and external and internal white coloration and the apex located in the central part of the shell (see
Calyptraea aurita was reported by
According
On the other hand, the species Calyptraea intermedia d’Orbigny, 1839, was described from the coasts of Peru, and still awaits confirmation of validation. Until today it has not been re-recorded, except for the reports of
The geographical distribution of other calyptraeid species, Trochita pileus (Lamarck, 1822) and T. pileolus (d’Orbigny, 1841), overlaps with C. aurita (
Reproduction of Calyptraea aurita occurs during most of the year with the exception of the winter months. In June (austral winter) no brooding was observed, but data for July and August are lacking. In general, calyptraeid species are known to vary in brooding season, some species like Crepidula adunca brood throughout the year whereas others like C. lingulata brood only throughout the summer months (
4.5 ± 1.3 % of females were infested by the pinnotherid crab Calyptraeotheres politus, which inhabits the mantle cavity of the limpets. This obligatory symbiont to slipper snails (
The transplantation experiment demonstrated that Calyptraea aurita can survive, grow, and reproduce successfully in the shallow subtidal zone, although it was never found at that depth in the field. The vertical distribution of C. aurita is discrete and marked by its complete absence in depths of less than 25 m, whereas another calyptraeid species, Crepipatella peruviana (named as C. fecunda), dominates the sessile fauna (del Moral and Schories, pers. comm.). Although abundance of C. peruviana diminishes with increasing depth, the free space is not used immediately by C. aurita. Additional factors than competition for space must explain its absence in shallower water. C. aurita does not form continuous belts but shows a patchy distribution. This explains the huge differences in abundance and coverage between the four sample sites, because in the immediate vicinity of the transect lines dense patches of C. aurita were always found.
Dense aggregations of calyptraeid species covering up to 100% of the substrate are common.
Using traditional shell characteristics, Calyptraea aurita bears no resemblance to suggested synonyms among other species. Most probably the species has not been redescribed before due to its depth distribution, which is below the main diving activities in the region. Calyptraea aurita can be easily identified by the spiral channel present in the umbilicus at the inner surface of the shell and by the sculpture with numerous fine radial ribs. In addition the edges of the shell have a regular circular shape. However, we never found empty shells of this species on the beaches or in the intertidal zone, which might be explained by the pronounced depth gradient along the rocky coast of the eastern part of the Reloncaví Sound, also the material type of the species was dredged at 82–110 m. In contrast to the Atlantic coast of South America no detailed revision of the genus Calyptraea (s. s.) has been undertaken.
We gratefully acknowledge the diving assistance of Ignacio Garrido and Isabel del Moral during our field expeditions. We thank Andreia Salvador and Kevin Webb for provided syntype material (