Some aspects of the reproductive biology of two populations of Musculium argentinum (d'Orbigny, 1835) (bivalvia: sphaeriidae) from Southern Chile.
Bivalvia (Environmental aspects)
Population biology (Research)
von Brand, Elisabeth
|Publication:||Name: Journal of Shellfish Research Publisher: National Shellfisheries Association, Inc. Audience: Academic Format: Magazine/Journal Subject: Biological sciences; Zoology and wildlife conservation Copyright: COPYRIGHT 2011 National Shellfisheries Association, Inc. ISSN: 0730-8000|
|Issue:||Date: August, 2011 Source Volume: 30 Source Issue: 2|
|Topic:||Event Code: 310 Science & research|
|Geographic:||Geographic Scope: Chile Geographic Code: 3CHIL Chile|
ABSTRACT Sphaerids have adopted a variety of life strategies that
have allowed them to show a cosmopolitan distribution. Among these
strategies, those related to reproduction, such as sexuality
(hermaphroditism), offspring incubation, fertility, number of
generations per year, times an individual reproduces during its
lifespan, among others, have been decisive with regard to its permanence
in time and space, and to colonize and maintain populations in permanent
or temporary freshwater bodies. The aim of the current study is to
compare reproductive traits of 2 Musculium argentinum populations
inhabiting different environments (stream and lake) to determine the
potential influence of the environment on reproduction of these
populations. During 1 y (October 2006 to 2007) monthly samples were
taken at 2 study sites: Lautaro stream (38032' S,
72[degrees]27' W) and La Poza, Villarrica Lake
(39[degrees]16'27" S, 71[degrees]58'54" W). Sixty
specimens were collected monthly from each population. Valve length of
each specimen of the sample was registered to determine the size
structure of each population. Fifty animals of known valve length were
dissected to determine presence and number of brooding sacs in the inner
hemibranches, number of embryos in each sac, and number of newly hatched
clams. Ten specimens were processed for optical microscopy with routine
histological techniques to characterize the gonad activity pattern.
Results indicate that M. argentinum is hermaphroditic in both
populations; with gonadal activity throughout the year, iteroparous, and
with embryos in brooding sacs and newly hatched clams present
year-round. These results indicate that differences in the environment
did not produce major changes in reproductive strategies in both M.
argentinum populations studied.
KEY WORDS: Sphaeriidae, clams, Musculium argentinum, reproduction, Chile
The variety of life strategies adopted by sphaerid clams have allowed them to achieve a cosmopolitan distribution found in different freshwater streams and lacustrine environments in a temporary or permanent state. A review of literature on sphaerid reproduction features showed that populations of Musculium sp. inhabiting different habitats, displayed different life strategies. Among these strategies, those related to reproduction, such as hermaphroditism, ovoviviparity, brooding (synchronous or asynchronous), number of generations per year, bradyticyctic or tachytictic pattern, among others, have played a key role in its permanence in time and space, and its ability to colonize and maintain populations in temporary freshwater bodies (Hornbach et al. 1980, Hornbach et al. 1982, Morton 1985, Hornbach & Childers 1986, Way 1988, Hornbach et al. 1991).
In Chile, sphaerids are represented by 3 genera and 11 species: Pisidium with 7 species, Sphaerium with 2 species, and Musculium with 2 species (Parada & Peredo 2002). The first record of Musculium argentinum (D'Orbigny 1835) in Chile was reported by Sobarzo et al. (2002) for the basin of the Cautin River; Parada et al. (2009) have reported that M. argentinum is found discontinuously in Chile between the parallels 38[degrees] S and 41[degrees] S, and between the meridians 71[degrees] W and 72[degrees] W inhabiting streams and lacustrine environments. Sphaerids from the northern hemisphere have been extensively studied, particularly in North America (the United States and Canada). On the contrary, studies on sphaerids from the southern hemisphere--and in Chile, in particula--are scarce. Because of the impossibility of extrapolating results from studies on Sphaeriidae populations from the northern hemisphere to the southern hemisphere as a result of the different environmental conditions in which these populations occur, among other factors, it is important to carry out studies on Sphaeriidae in the southern hemisphere, and from Chile in particular. Conservation or management initiatives of species require an accurate knowledge of the population dynamics of species, and reproductive traits are of particular importance. In addition, studies of freshwater bivalves have reported a decrease in their populations as a result of an anthropogenic influence (Peredo et al. 2005). Moreover, sphaerids are filter feeders and often play an important role in the dynamics of nutrient and energy cycling in freshwater bodies such as streams, ponds, and lakes (Wallace et al. 1977).
On the basis of the aforementioned factors, the aim of the current study was to determine whether M. argentinum populations inhabiting different environmental conditions show differences in reproductive traits as reported in previous studies carried out in the northern hemisphere in populations occurring at different environmental conditions and latitudes (Mackie et al. 1976, Morton 1985, Hornbach et al. 1991, O'Toole & Wilson 2001, Mouthon 2004). The hypothesis established in this study is that M. argentinum populations living in lentic and lotic environments exhibit major changes in their reproductive strategies.
MATERIALS AND METHODS
The current study was carried out in two areas with different environmental conditions. The first area, the Lautaro Channel, corresponds to the evacuation channel of Lautaro Fish Farm located in the central valley of south--central Chile at a latitude of 38[degrees]32' S, 72[degrees]27' W, and an altitude of 190 masl. It runs through the interior of a recreational park with abundant tree vegetation represented by Pinus radiata (D. Don), Acacia melanoxylon (R. Br.), Eucalyptus globulus (Labill), and Rubus ulmifolius (Schott), and riverside vegetation with a predominance of Leontodon taraxacoides (Vill) Merat, Plantago lanceolata (L.), Taraxacum officinalis (Weber), and Blechnum hastatum (Kaulf). The Lautaro Channel has an approximate length of 2 km and a mean width of 2 m, until it flows into the basin of the Cautin River.
The second area, Lake Villarrica, is located at 39[degrees]16' 27" S, 71[degrees]58'54" W in the foothills of the Andes mountain range at an altitude of 250 masl. It is of glacial origin and has been characterized by Campos et al. (1983) as an oligotrophic lake, monomictic, with winter circulation and summer stagnation. The mean temperature in winter reaches 9.5[degrees]C, with small variations between the surface and the bottom. The maximum temperatures registered in spring and summer reach 22[degrees]C in the epilimnium and 9.5[degrees]C in the hypolimnium. The chemical and physical parameters of the water, as well as the phytoplankton and zooplankton, present a marked seasonal variation. M. argentinum inhabits the coastal area of the La Poza Bay in the northeastern extreme of the lake in a protected coastal area, with scarce vegetation represented by Juncus procerus (E. Meyer) and Salix viminalis (L.), with a high anthropic influence in the coastal area during the summer.
From October 2006 to October 2007, monthly samples were taken in both study areas to collect biological material. Sixty specimens per month were transferred to the laboratory to determine the valve length (VL) of each specimen using a digital caliper. From the sample, 50 specimens of known VL were selected at random to be processed under a stereomicroscope with the aim of determining the presence and number of brooding sacs in the inner hemibranches, the number of embryos in each sac and the number of newly hatched clams. Size structure was determined at the population level, as well as the age of the first individual and population brooding.
Soft tissues from 10 individuals from the largest size class from the sample were processed monthly via optical microscopy with routine histological techniques. The sections were examined using an a digital camera (Olympus model U-CMAD) to characterize gonad activity as well as features of marsupial sacs in the inner hemibranches. For climatic reasons, it was not possible to carry out the sampling during the month of July at La Poza station. Water temperature was recorded when samplings were carried out in both populations.
The size structure of both populations is presented in Figure 1. Both populations show a similar monthly size structure. In the La Poza M. argentinum population, the smallest individual was recorded in September with a VL of 1.7 mm; the largest was recorded in October 2007 with a VL of 7.8 mm. At Lautaro, of 840 individuals collected in the study, the smallest individual (VL, 1.8 mm) was found in September and the largest (VL, 8.0 ram) was found in October 2007.
In the Lautaro M. argentinum population, the higher amplitude of classes appeared in October; in La Poza, it occurred in December. The presence of juveniles (1-1.9 mm) appeared during different seasons--in the Lautaro channel in June and September, and in La Poza in December, April, and September (both coincided in September).
The gonad organization observed coincides with that reported by Peredo et al. (2010). Throughout the study period, gonads of M. argentinum specimens from both populations were observed to be active, containing germinal cells at different stages of gametogenesis.
Throughout the study period, specimens examined from both populations (Lautaro and La Poza) contained embryos and larvae at different stages of development in brooding sacs within inner hemibranches (Fig. 2).
Reproductive Population Dynamics
Of 840 individuals from each population, the monthly variation of gravid individuals showed the same tendency in both populations during the spring and summer months--that is, a progressive increase to reach the highest number of brooding adults in January (summer), decreasing afterward in both populations and reaching the lowest number of gravid individuals in March (the beginning of fall in Chile). During the fall and winter months, the behavior appears to be different; hence, the La Poza station tends to recover the mean percentage showing in May, June, August, and September over 50% of gravid individuals. Lautaro population during Fall months showed adult brooding percentage lower than 40%, registering an increase in July (winter), decreasing again in September (Fig. 3). Conversely, the population at Lautaro, during the fall months, showed a percentage of brooding adults less than 40%, registering an increase in July (winter) and decreasing again in September (Fig. 3).
The monthly variations of the total number of embryos or larvae within sacs and of newly hatched individuals (in the mantle cavity) in adult specimens of the Lautaro and La Poza populations are shown in Figures 4 and 5. In both populations, individuals with embryos or larvae were registered monthly; newly hatched specimens were not registered in November and August in Lautaro. There are no records for newly hatched individuals in January, February, and July for La Poza. The monthly count for the highest number of brooding sacs per gill recorded in individuals of both populations show that, in the Lautaro population, individuals with as many as 3 sacs per hemibranch during December and October were found. Meanwhile, for individuals in La Poza, the highest number registered was only 2 sacs per gill (Fig. 6).
The mean annual productivity values of embryos or larvae in brooding sacs and newly hatched produced by adult specimens was 96.2 [+ or -] 39 in the Lautaro population and 78 [+ or -] 25 for the La Poza population. Monthly variations in both populations are shown in Figure 7. Both populations showed similar tendencies throughout the study year. The Lautaro population curve is always above the La Poza population, except in May and June, when the number of embryos or larvae in the hemibranches in Lautaro decreased. At an individual level, the monthly variations of maximum fertility (measured as the number of embryos or larvae in brooding sacs of an individual) in each population are shown in Figure 8. Lautaro shows the highest values, with 26 embryos or larvae obtained in April and October for specimens of 4.5 mm and 6.2 mm in VL, respectively. In the La Poza population, the highest value of fertility was obtained in January in a specimen with a VL of 4.7 mm.
[FIGURE 1 OMITTED]
[FIGURE 2 OMITTED]
The smallest gravid individual (size of first specimen reproduction) in the Lautaro population was 2.3 mm, and, in La Poza population, was 2.8 mm. Both specimens were collected in May (Table 1).
Regarding the size of the first population reproduction (the smallest size class in which at least 50% of the specimens are brooding) corresponded to the 3.0-3.9 size class for both populations, was recorded in July and August for the Lautaro populations and in February and May for the La Poza population respectively (Table 1).
[FIGURE 3 OMITTED]
The physical and chemical parameters of substratum in both locations show differences related with the percentage of organic matter and granulometry. The substratum of the Lautaro stream station presented a percentage considerably higher in organic matter (11%) than the lacustrine La Poza station, with only 1.5%. Both stations also presented different granulometry according to the textural triangle of the U.S. Department of Agriculture (1975). The substratum of Lautaro is composed of lime and clay, with 0.91% sand, 54% lime, and 45.1% clay. La Poza, instead, presents a clayey substratum, with 7.3% sand, 12.2% lime, and 81.8% clay.
The physical and chemical parameters of the water inhabited by both populations are shown in Table 2. The water quality of both environments is very similar, with small differences in some chemical parameters, such as chloride and nitrite. This difference is more evident at La Poza. Calcium is only present in Lautaro. The differences appear only in the physical parameters, especially the depth fluctuations, which, in the coastal areas of Lake Villarrica, reach a minimum of 30 cm in the summer and 2.5 m in the winter; and the flow velocity, which is absence at La Poza and 55 m/sec at Lautaro. The size structure of both populations is presented in Figure 1. Both populations do not show significant variations throughout the year. The monthly variations in water temperature in both populations show the same tendency throughout the year, with the stream population of Lautaro showing lower water temperatures (Fig. 9).
[FIGURE 4 OMITTED]
[FIGURE 5 OMITTED]
The results of the current comparative study of the reproductive traits of stream and lacustrine populations of M. argentinum show a similar pattern previously reported for Sphaeriidae specimens. Gonad sections reveal the hermaphroditic condition of individuals. However, gonad follicles have gametes only from one sex.
Regarding gonad activity, sections showed the presence of gametes throughout the entire study period, with continuous activity, as described for other freshwater bivalves (Heard 1965, Heard 1970, Ghosh & Ghose 1972, Zumoff 1973, Nagabhushanam & Lohgaonker 1978, Peredo & Parada 1986).
The presence of embryos or larvae within the inner hemibranches demonstrates the ovoviviparous condition of M. argentinum (Fig. 2AC), which is in agreement with Mackie's definition of ovoviviparity (Mackie 1978). Examination of inner hemibranch sections could not determine the presence of functional nutritive cells located in the wall of the brood sacs or any other cell or structure that could provide parental nutrients to the embryos. Thus, M. argentinum is not viviparous, which is in contrast to reports by Korniushin and Glaubrecht (2003) and Hetzel (1993) for other sphaerids.
According to the results observed in the current study, both populations of M. argentinum did not present a specific spawning period during the study period. A percentage of brooding specimens were observed, although this percentage varied through the months (Fig. 3). The highest percentages of brooding specimens in the Lautaro population were registered in January (summer) and in October (spring), coinciding with the La Poza population. Both populations showed a similar tendency in the percentage of brooding specimen fluctuation during the spring/summer period (October to February). In March (fall), the percentage of brooding specimens in both the Lautaro and La Poza populations decreased abruptly, then showed a more marked and stable increase in the La Poza population than in that of Lautaro. This higher percentage of brooding specimens showed by the La Poza population could be attributed to the higher temperatures registered at La Poza (Villarrica Lake) than at Lautaro (Fig. 9).
[FIGURE 6 OMITTED]
[FIGURE 7 OMITTED]
As a result of the presence of brooding specimens throughout the year, in the M. argentinum populations studied, adults and juveniles were present throughout the study period, in contrast to results reported by Mackie et al. (1976) in a Musculium securis population, by Morton (1985) for Musculium lacustre, by Hornbach et al. (1991) for Musculium partumeium and O'Toole and Wilson (2001) for M. lacustre. Therefore, M. argentinum would originate several generations in a year, being November, February and April the months with the highest number of newly hatched individuals in Lautaro specimens population, and November and March the months with the highest number of newly hatched present in La Poza specimen population (Figs. 4 and 5). In this aspect, M. argentinum resetfibtes Sphaerium striatinum which was reported as a sequential brooder and producing offspring throughout the year (Beekey & Hornbach 2004), whereas S. lacustre was characterized by a single annual reproduction (Gong et al. 2004). Newly hatched individuals present in M. argentinum populations were almost similar or of the same size than juveniles found in the substrate. Marsupial embryos or larvae and newly hatched clams were more abundant in Lautaro than in La Poza.
[FIGURE 8 OMITTED]
In addition, individuals in the Lautaro population registered a higher reproductive productivity monthly (potential recruitment) than the individuals at La Poza (Fig. 7). Lautaro also showed higher individual fertility (specimens with the greatest number of sac embryos and newly hatched clams; Fig. 8).
The presence of adult M. argentinum in both populations that produce offspring year-round could be indicative of iteroparity instead of semelparity, as reported for other species of Musculium inhabiting various environments (Morton 1985, O'Toole & Wilson 2001, Mouthon 2004). Iteroparity reported in M. argentinum populations in the current study could be indicative of a reproductive strategy to favor reproductive success, as indicated by numerous models (Wilbur & Rudolf 2006). Mackie et al. (1976) related embryo growth rates with iteroparity or semelparity. Thus, species with slow larval (embryonic) growth rates are usually semelparous and univoltine, but can be iteroparous by precocious birth of larvae (embryos), and multivoltine by accelerated growth of semelparous individuals. Species with rapid larval growth rates are usually iteroparous because larvae grow faster than parents, or there is precocious birth (hatching) of larvae.
Beekey et al. (2000) point out that retention of competent offspring within brood pouches represents a form of extended parental care. The presence of newly hatched animals with similar size to juveniles in M. argentinum specimens in both studied populations also represents a form of extended parental care, because the newly hatched clams, although not within the brooding sacs, were in the mantle chamber.
Beekey & Karlson (2003) concluded that physical constraints are more important in determining overall brood size than energetic constraints in S. striatinum. Variations observed in reproductive traits in the M. argentinum populations studied can be attributed to conditions present in lotic (channel) and lentic (lake) environments.
Another difference registered is related to the number of sacs produced in each hemibranch. Only the individuals at Lautaro produced up to three brooding sacs per gill (Fig. 4); the maximum number of sacs produced by hemibranches in La Poza is just two (Fig. 5). There is no correlation in M. argentinum between the numbers of sacs produced versus VL of the individuals in both populations--a fact already mentioned by Peredo et al. (2007). Beekey and Hornbach (2004) state that, in S. striatinum, the size of the brood is limited by the number of the marsupial sacs and the retention of offspring. A fact worth noting is that the individuals at Lautaro showed a higher convexity index or roundness (sensu Ituarte (1996)) than the La Poza population (65.4 for Lautaro and 59.1 for La Poza) (Parada et al. 2009). This means that, at higher altitudes, the Lautaro individuals are more globular than those of La Poza. This morphometric characteristic could be directly related to the possibility of producing more offspring, as shown by the fertility results and number of sacs formed in the individuals at Lautaro, and it would help to shelter or to produce a larger brood.
[FIGURE 9 OMITTED]
Another difference is related to the size of the first individual brooding. Both populations register the gravid individuals of smallest size in May. However, at Lautaro, the smallest gravid individual is 2.3 mm; in La Poza, the smallest is 2.8 mm. This indicates that M. argentinum individuals at Lautaro mature before those at La Poza.
Mackie et al. (1976) show that inter- and intrapopulation variations in the fertility of M. securis could be explained by differential embryonic mortality during the incubation period. In this respect, it is worth noting that in the case of M. argentinum, all dissociated embryonic sacs carried out monthly in both populations, no case showed dead embryos with or without shell in the inner sacs, and no residual body that would lead to think of a situation of that kind. The interpopulation differences registered in M. argentinum could be explained by the environmental characteristics where the populations live. The higher fertility registered in the stream population could be a strategy to (or compensation) due to the loss of juveniles swept away by the current. It is also possible that the difference in the food supply, determined by the quantity of organic matter of the sediment used as food by the specimens, is significantly higher in at Lautaro (11%) that at La Poza (1.5%).
Another difference between Lautaro and La Poza is the population density. The value registered for Lautaro is almost double (325 individuals/[m.sup.2]) that registered at La Poza (187.5 individuals/[m.sup.2]), a parameter that could also be related to the greater food supply at Lautaro. In this context, the environmental parameters represent relevant factors in the dynamics, reproductive biology, and permanence of the populations in time. For both populations of M. argentinum, the water temperature had an average of 23[degrees]C and a minimum of 8[degrees]C (Fig. 9), and the water itself had low values of total dissolved solids, low conductivity, was highly oxygenated, with low values of ammonium, nitrite, nitrate chloride, sulfate, inorganic phosphorus, and calcium (Table 1). These values are much lower than those registered in the Saone River in France for M. lacustre (Mouthon 2004).
With respect to the substratum, both populations inhabit a clayey (La Poza) or clay-muddy substratum (Lautaro), and with concentrations of organic matter ranging from 11.03% at Lautaro and 1.52% at La Poza. The importance of the organic matter in the sediment has also been documented for M. lacustre (Morton 1985, Mouthon 2004) and for M. securis by Mackie et al. (1976)
Several authors, empirically as well as theoretically, have tried to establish life history patterns of species, relating certain parameters of the individuals: age at first reproduction, fertility, number of reproductions during a lifetime, growth rate, and generational time, among others, with the habitat where they are found. Morton (1991) points out that, although intraspecific variations in life history tactics and sexual strategies equip all species for a variable environment, permutations of the dioecious condition, mediated through variations in the sex ratio, either overall or with age, broadly equip Bivalvia for the total range of aquatic habitats.
The results of the current study allow us to conclude that both M. argentinum populations studied are oviparous, iteroparous, and sequential incubators, producing offspring throughout the year. The pattern developed by the Lautaro stream population, unlike the lacustrine population, is characterized by presenting a reproductive seasonal variation with emphasis in spring and summer, higher individual fertility and population productivity, higher production of brooding sacs per gill favored by a higher globularity of the shells of adults, and a higher availability of food in the environment than individuals in the lacustrine population at La Poza. The differences observed indicate that dissimilarities in the environment did not bring out major changes in reproductive strategies in both M. argentinum populations studied, in contrast to the results reported in earlier studies on sphaerids from the northern hemisphere (Heard 1965, Hornbach & Childers 1986, Hornbach et al. 1980, Hornbach et al. 1991). Results obtained show that the hypothesis established is not correct because major changes in reproductive strategies between both populations were not registered. On the other hand, results obtained in the current study, in regard to conservation or management initiatives show the feasibility to relocate threatened populations of M. argentinum in lotic or lentic environments, independent of their original habitat.
The distribution of M. argentinum is discontinuous in the southern cone of America, from southern Brazil (Mansur et al. 1991, Ituarte 1996), Uruguay (Figueiras 1965), and Argentina in the eastern and western sides (Ituarte 1996), and Chile (Parada et al. 2009). This species occupies different biotops and climates thus constituting an attractive species for the analysis of the variety of ecological and historical circumstances that influence in the historical and modeled life histories to different environmental characteristics.
This work was supported with funds from the Direcci6n General de Investigacion, Universidad Cato1ica de Temuco, Chile (project 2005-4-03). We thank Matias Peredo and Angel Contreras for their technical assistance with figures and microphotographs.
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PEDRO JARA-SEGUEL, (1) * SANTIAGO PEREDO, (1) ELISABETH VON BRAND (2) AND ESPERANZA PARADA (1)
(1) Escuela de Ciencias Ambientales, Facultad de Recursos Naturales, Universidad Catolica de Temuco, Casilla 15-D, Temuco, Chile; (2) Departamento de Biologia Marina, Facultad de Ciencias del Mar, Universidad Catolica del Norte, Casilla 117, Coquimbo , Chile
* Corresponding author. E-mail: email@example.com
TABLE 1. Individual and population first reproduction at Lautaro and La Poza Bay M. argentinum populations during the study period. Population Lautaro Individual First Population First Reproduction Reproduction Valve Length Size Class Month (mm) (mm) October 4.4 5-5.9 November 3.6 4-4.9 December 3.4 4-4.9 January 3.8 4-4.9 February 4.2 5-5.9 March 4.1 5-5.9 April 3.5 3-3.9 May 2.3 Undetermined June 3.2 3-3.9 July 3.7 4-4,9 August 4.3 5-5.9 September 4.7 Undetermined October 4.5 5-5.9 Population La Poza Individual First Population First Reproduction Reproduction Valve Length Size Class Month (mm) (mm) October 4.9 5-5.9 November 4.3 5-5.9 December 3.9 4-4.9 January 3.2 4-4.9 February 3.3 3-3.9 March 3.6 Undetermined April 3.3 4-4.9 May 2.8 3.3-9 June 4.4 Undetermined July Undetermined Undetermined August 3.1 Undetermined September 3.6 4-4.9 October 3.8 4-4.9 TABLE 2. Water physical-chemical parameters at Lautaro and La Poza Bay stations during the study period. Parameters Lautaro La Poza Total suspended solids (mg/L) 1.5 1.6 Conductivity ([micro]S/cm) 62.1 57.9 Dissolved oxygen (mg/L) 11.54 10.13 pH 7.71 7.79 Alkalinity (mg/L) 26.5 28.35 Calcium (mg/L) 5.73 0 Total ammonium (mg/L) 0.024 0.007 Nitrite (mg/L) 0.003 0.05 Nitrate (mg/L) 0.06 0.06 Chloride (mg/L) 0.7 1.3 Phosphorus (mg/L) 0.03 0.01 Sulfate (mg/L) 0 6 Temperature ([degrees]C) 10 13 Depth (cm) 15.7 30 Water flow (m/sec) 55 0
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