Genetic relations between the bivalves Cardium (Cerastoderma) edule,Cardium lamarcki and Cardium glaucum,studied by means of crossed immunoelectrophoresis

Rabbit antisera were raised against Cardium edule (L.) from the Waddensea locality, Skallingen, against Cardium lamarcki (Reeve) from the Danish locality, Dybsø Fjord, and against Cardium glaucum (Bruguière) from the French Mediterranean coast at Ile des Embiez. Allopatric and sympatric populations of C. lamarcki and C. edule from Swedish and Danish localities, and allopatric populations of C. glaucum from the Mediterranean Sea, Red Sea and Black Sea were studied by means of the described method and by starch gel electrophoresis of malate dehydrogenase (MDH). By means of crossed immuno-electrophoresis, using intermediary gels containing antibodies against one of the Cardium types and receiver gels containing antibodies against one of the others, type-specific and type-non-specific reactions were recorded. The results are compared with a similar investigation of Mytilus edulis, M. galloprovincialis and M. californianus. Based on immunological properties, it is shown that C. edule is a valid species different from the C. lamarcki/C. glaucum complex. It is further suggested that C. lamarcki and C. glaucum should still be referred to by these two names as significant genetic differences between them is revealed by this immunological study.     

Studies on the reproductive cycles of Cardium edule and C. glaucum

Two allopatric populations of Cardium edule and two of C. glaucum were sampled over a period of 16 months and their gonad maturity cycles compared by histological methods. The onset of both spermatogenesis and oogenesis in C. edule took place between September and October; in C. glaucum it was slightly later, between October and November. Development of the gonads continued slowly throughout the winter, C. glaucum developing marginally faster than C. edule. Maturation accelerated in April and May, with the gonads of both species becoming fully ripe in late May and early June. Spawning of the two species approximately coincided at all the localities investigated. Spawning in C. edule was better coordinated than in C. glaucum. Transplanting cockles of one species to the typical habitat of the other did not appreciably alter the spawning period. The separation of spawning periods in sympatric associations of the two cockles is discussed.     

Evolution of Cardium (Cerastoderma) edule,C. lamarcki and C. glaucum: studies of DNA-variation

Genetic relations between populations of Cardium (Cerastoderma) edule (L.) and C. lamarcki (Reeve) from Danish waters and C. glaucum (Bruguiére) from the Mediterranean Sea were studied using DNA analysis. Repetitive sequences of nuclear DNA were compared by Southern blotting of enzyme digested DNA fragments, separated on agarose gel by electrophoresis. Fragments were visualized by autoradiography using ³²P labelled probes. These were nick translated, randomly sheared fragments of the whole chromosomal genomes of two species of distant taxa — Mytilus edulis and Mya arenaria, respectively. The number of detected DNA bands was 18 for C. edule, 32 for C. lamarcki, and 24 for C. glaucum. Measurements of genetic distances, based on comparisons of these repetitive sequences using a simple dissimilarity coefficients, show the greatest distance, i.e., 0.84 between C. edule and C. lamarcki, 0.69 between C. edule and C. glaucum, and the smallest, 0.52 between C. lamarcki and C. glaucum. Comparisons of the three Cardium types, using gene spliced and cloned C. edule nuclear DNA (nDNA) fragments as probes, accorded with these findings. Also, analysis of mitochondrial DNA (mtDNA) from eggs and hepatopancreas, although not in itself conclusive, accorded with the results of the analyses of nDNA. MtDNA was measured by electron micrograph to 15 000 base pairs (bp), and sizes of restriction enzyme digested fragments were compared by gel electrophoresis. The results of the comparisons based on repetitive sequences supported by the two other studies suggest that C. edule resembles the ancestral form more than the two others, and that C. lamarcki is the most different and recently evolved form. This hypothesis is discussed in relation to the geographical distribution of the species complex.     

Enzymatic and morphological criteria for distinguishing between Cardium edule and C. glaucum of the Portuguese coast

Cardium edule L. and C. glaucum Bruguière are two sibling species of cockles commonly found in littoral systems along the Portuguese coast, where they sometimes occur as mixed populations. The problem of morphological separation of these two cockle species has not been completely solved. Indeed, the distinctive morphological criterion proposed by Brock after identifying the specimens by means of electrophoretic patterns of hepatopancreatic malate dehydrogenase was not effective when applied to Portuguese Cardium spp. The object of the present study was to establish morphological discrimination criteria for distinguishing Portuguese C. edule and C. glaucum on the basis of initial identification of individuals through the enzymatic criterion established by Brock. Cockles were collected from 1988 to 1991 at 16 estuarine and lagoonal systems along the Portuguese coast. Hepatopancreatic extracts were submitted to horizontal starch gel electrophoresis following Brock's procedure. The malate dehydrogenase patterns obtained were identical to those found by Brock. Clear interspecific differences in the leucine aminopeptidase and esterase isozyme systems were also detected. The morphological study of the shells involved 7 morphometric and 9 qualitative and semiquantitative characters. Canonical variate analysis of the morphometric characters showed that these could not be used for identification purposes. However, a clear separation between the two species was obtained by a principal-component analysis of qualitative and semiquantitative characters. The characters mainly useful for distinguishing between the two species were valve profile, shape of ventral valve junction, type of calcareous scales and shell colour.     

Biological studies on Cardium glaucum,based on some Baltic and Mediterranean populations

The recent separation of Cardium glaucum Bruguière from C. edule L. and the scarcity of reports of populations containing both species has necessitated further ecological study to demonstrate differences in habitat preferences. Some mixed and unispecific populations of the cockles Cardium edule and C. glaucum, situated in fjords around the Kattegat and Baltic coasts of Denmark were studied; it was demonstrated that some degree of tidal influece was essential for the survival of C. edule, and that C. glaucum was being restricted by the exposure of the site. A study of the cockle populations of some étangs on the Mediterranean coast of France demonstrated that, despite earlier reports of its presence, C. edule was not present in that area. A brief survey of the Bassin d'Arcachon (France) showed that it contained a mixed cockle population. It was concluded that C. edule was unable to occupy localities having a tidal amplitude of less than 0.2 m, and that high temperatures also restricted occupation of semitidal habitats; similarly, the exposure of the site restricted colonisation by C. glaucum.     

Short-term shell growth in bivalves: Individual,regional, and age-related variations in the rhythym of deposition ofCerastoderma (=Cardium) edule

The influence of potential sources of variations (age, site, region) on the production of shell microgrowth increments was studied in the cockleCerastoderma edule (L.) from the shores of Denmark, Jersey Island and South Wales between 1978 and 1986. Microgrowth increments in the shell of the cockle were counted between annual growth marks corresponding to the second, third, and fourth yearly growth period of the cockle. The number of microgrowth increments per year showed a decrease with increasing age. Increments formed after deposition of the last annual mark in cockles sampled at different dates indicate that the rate of increment formation differed between age classes and populations. Furthermore, we observed pronounced intrapopulation differences in the number of increments for specimens of the same age, and differences in both number and clarity of increments in subtidal and intertidal populations. Our results do not support the hypothesis of a general endogenous rhythm of microgrowth that closely corresponds to tidal rhythms inCerastoderma edule. Instead, they emphasize the plasticity of deposition according to the origin and age of the experimental specimens.     

Divergence in female calling song discrimination between sympatric and allopatric populations of the southern wood cricket Gryllus fultoni (Orthoptera: Gryllidae)

Two species of closely related wood cricket, Gryllus fultoni (Orthoptera: Gryllidae) and Gryllus vernalis, occur together in some parts of the eastern United States and have a similar calling song structure, consisting of three-pulse chirps. A previous study revealed that chirp rate in G. fultoni was highest (greatest difference vis-à-vis chirp rate in G. vernalis) in sympatric populations, intermediate in near allopatric populations that were located close to the sympatric zone, and lowest in allopatric populations. A similar trend was observed in pulse rate, but the mean values of this trait showed much more convergence than chirp rate at the low end of the range of calling temperatures. In this study, we investigated the song discrimination of females from sympatric and allopatric populations of G. fultoni at about 23°C, which is near the middle of the normal range of calling temperatures. We used both single-stimulus and two-stimulus playback experiments to learn if geographical differences in song preferences paralleled those in calling songs. Stimuli presented were representative of calling songs in three classes of G. fultoni populations (sympatric, near allopatric, and far allopatric), a calling song of G. vernalis, and three calling songs with parameter values that were intermediate with respect to those of the songs of far allopatric G. fultoni and G. vernalis. In the single-stimulus playbacks, females of all G. fultoni populations responded poorly if at all to the heterospecific stimulus. Females of sympatric and near allopatric populations responded poorly to all intermediate stimuli, but females of far allopatric populations frequently responded to these sounds. In the two-stimulus playbacks, females of sympatric and near allopatric populations generally discriminated against intermediate and heterospecific stimuli. However, females of far allopatric populations often did not discriminate against intermediate stimuli, whose characteristics resembled the calling songs of G. vernalis. The divergent pattern of female phonotactic discrimination between sympatric and far allopatric populations was thus generally congruent with the pattern of divergence in chirp and pulse rates and would be expected to significantly reduce heterospecific mating in sympatry. These geographical patterns of female song discrimination and male calling songs conform to a commonly used definition of reproductive character displacement.     

Seasonal changes in the physiology,reproductive condition and carbohydrate content of the cockle Cardium (=Cerastoderma) edule (Bivalvia: Cardiidae)

Pronounced seasonal cycles in the rates of oxygen consumption and feeding were found for Cardium (=Cerastoderma) edule L. measured in the field under ambient conditions. The cockles had a maximum rate of oxygen consumption (0.89 ml O₂ g^-1 h^-1) in April which declined to a minimum of 0.35 ml O₂ g^-1 h^-1 in March. Their feeding rate was variable but had a maximum value (3.91 l g^-1 h^-1) in April and a minimum value (0.73 l g^-1 h^-1) in October. There was no apparent seasonal variation in absorption efficiency, with a mean value of 67.6%. Gametogenesis was initiated in January and the population reached a peak in reproductive condition in April/May, followed by a 3 month spawning period. Carbohydrate reserves were synthesised during spawning, and were then utilised during the winter and early spring. An adaptive function for a reduction in time spent feeding is postulated, and correlations between the rates of certain physiological processes and some exogenous and endogenous variables are discussed.     

Genetic evidence for cryptic speciation in allopatric populations of two cosmopolitan species of the calcareous sponge genusClathrina

Many sponge species are considered to be cosmopolitan. However, the systematics of marine sponges are very difficult because of the paucity of taxonomically useful characters, and hence the apparently cosmopolitan nature of many species may be simply a consequence of this. In this paper, geographically distant populations of two pairs of cosmopolitan calcareous sponges of the genusClathrina were compared genetically.C. clathrus andC. cerebrum were collected by SCUBA diving between January and March 1989 from two localities: the Mediterranean Sea at La Vesse, near Marseille, Frances, at 9 to 12 m depth, and from the South West Atlantic at Arraial do Cabo, about 200 km east of Rio de Janeiro, at 2 to 10 m depth. Very high levels of gene divergence were found between the allegedly conspecific populations. The levels of genetic identity,I, observed are so low (I=0.128 and 0.287) that the populations clearly cannot be considered conspecific. New species names ofC. aurea sp. nov. andC. brasiliensis sp. nov. are therefore assigned to the southwest Atlantic counterparts ofC. clathrus andC. cerebrum, respectively. It is concluded that, at least for the species studied, and probably for many other species in taxonomically difficult groups, the actual distributions of single species may be far more geographically restricted than is generally assumed.     

Comparative study of sympatric populations of two hyperiid amphipods,Primno johnsoni and P. evansi,from the eastern North Atlantic Ocean

Hyperiid amphipods are common components of oceanic plankton communities, and yet information is lacking on the ecology and biology of the majority of species. This study compares sympatric populations of two phrosinids, Primno johnsoni Bowman and P. evansi Sheader, using material collected on R.R.S. Discovery Cruises 121 and 140 in the eastern North Atlantic Ocean. The two species were essentially very similar in terms of their vertical distribution and diurnal migration, and in the timing and sequence of reproductive events (onset of maturity, ovary/oocyte development, marsupial development). Mature female and male size ranges were comparable for the two species, males maturing at a small body size, with little subsequent growth, and females producing a succession of 5 (P. evansi) or 6 (P. johnsoni) broods maximum. The species differed significantly in egg size and in total egg output. These dissimilarities were accentuated by differences in the patterns of female mortality in the two species, such that actual egg output per female was 1.8 times greater (2.4 times in terms of total egg volume) in P. johnsoni than in P. evansi. These differences were reflected in the relative size of populations in the field. Although both species are capable of consuming a wide range of planktonic prey, it is assumed that gelatinous species are important, especially as hosts for the parasitoid juvenile stages, and it is suggested that host-specificity might act to separate the niches.     

The breeding biology of two sympatric species of tropical intertidal hermit crabs,Clibanarius chapini and C. senegalensis

A one-year study of breeding in the two intertidal hermit crabs Clibanarius chapini Schmitt and C. senegalensis Chevreux and Bouvier showed that both species maintain a high reproductive activity throughout the year. Brief low reproductive activities, found in both species, occurred in different months: C. chapini in November, C. senegalensis in May. While these drops cannot be attributed to any recognisable environmental factor, it is suggested that such pattern may result from competition between the two species. Sex-ratio studies indicated slightly more females than males in both species. The maximal size attained by males of both species is considerably greater than that of the females; in C. senegalensis this is very marked. It is suggested that it may be selectively advantageous for a female to attain a smaller maximal size since her brood must also be accomodated within the shell. As expected for continuously breeding species, recruitment of young into the population is also continuous.     

Asymmetric mate choice,hybridization, and hybrid fitness in two sympatric grasshopper species

Hybridization between animal species has long been regarded as unusual, but is meanwhile accepted as a widespread phenomenon. Typically, sexual interactions among species are studied in secondary contact zones of closely related species (hybrid zones) or between invasive and native species, whereas hybridization between sympatric congeners has received little attention. Here, we present a study on the hybridization potential of two grasshopper species, Chorthippus parallelus and Chorthippus montanus, which occur sympatric in large parts of Eurasia. We performed a mate choice experiment with specimens from an area of local parapatry in northwestern Germany. Most copulations were conspecific, but males of both species and females of C. parallelus were indiscriminate in their mate choice, while females of C. montanus clearly preferred conspecific males. Although these results suggest asymmetric introgression, a no-choice hybridization experiment revealed that hybridization is possible in both directions. The hatching success of the hybrids was intermediate between the parental species. Female hybrids showed no clear mate preferences, indicating that back crossing in both directions is possible in principle, but the fertility of the hybrids and the fitness of the F2 generation remain unknown. Our study suggests that hybridization between sympatric species might occur more often than assumed. It might affect the ecology and local distribution of animals in a similar way as competition does.     

A case of parasite-mediated competition? Phenotypic differentiation among hookworms Uncinaria sp. (Nematoda: Ancylostomatidae) in sympatric and allopatric populations of South American sea lions Otaria byronia,and fur seals Arctocephalus australis (Carnivora: Otariidae)

Hookworms in otariids are considered to meet the conditions and to fulfill the predictions set forth in the theoretical literature to define a likely case of host coexistence mediation by a shared pathogen. The intensity of infections, the prevalence of skin lesions and the morphometry of hookworms Uncinaria spp. were examined in South American sea lions and fur seals sampled along the Chilean and the Uruguayan coasts in spring and summer 1981 to 1991. In sympatric host populations from Uruguay, there were clear differences in intensity of infections, prevalence of skin lesions, and body size of the hookworms from the two host species. Sea lions from Chile, allopatric to fur seal populations, are less intensively infected and hookworms found in these sea lions have the smallest body size reported in otariids, while those from South American fur seals are the largest. Hookworms found in sea lion pups from populations sympatric to fur seals revealed intermediate values in intensity and in body size, and the sea lion pups had the highest prevalence of skin lesions. Other reports of hookworms in otariids show intermediate morphometry, following a general linear trend of differentiation in size. Consequently, they are considered to belong to the same, widely distributed species Uncinaria lucasi Stiles, 1901.     

Does displacement of spawning time occur in the sibling species Cerastoderma edule and C. lamarcki?

The spawning cycles of the sibling species Cerastoderma edule (L.) and C. lamarcki (Reeve) were studied in allopatric and sympatric Danish populations from 1978–1980. The results do not support earlier findings of reproductive character displacement in sympatric populations of the two species. New records of hybrid formation and intermediate forms are presented and discussed.     

Reproduction of sympatric populations of Patiriella gunnii,P. calcar and P. exigua in New South Wales,asterinid seastars with direct development

Three asterinid seastars, Patiriella gunnii (Gray), P. calcar (Lamarck) and P. exigua (Lamarck) are sympatric in southeast Australia and form part of a series of Patiriella species endemic to Australian shores. Reproduction of co-occurring populations of P. gunnii, P. calcar and P. exigua was investigated in New South Wales from December 1988 to February 1991. Their reproductive cycles were documented by the gonad index (GI) method and by histological examination of the gonads. The annual cycle of the pyloric caecae was also documented and the relationship between the two indices was examined. Oogenesis and spermatogenesis are described in histological detail. The three species produce large yolky eggs and have direct development. Vitellogenesis and weight-gain by the ovaries results from accumulation of periodic acid Schiff (PAS +) material by the oocytes. P. gunnii and P. calcar are gonochoric and have well-defined reproductive cycles, spawning in spring and summer. There was a sharp decline in the GI of P. gunnii in December due to potentially synchronous spawning. Histological examination revealed that initiation of gamete release occurred in August. Gamete release by P. calcar also started in August, with episodic spawning through December. P. gunnii and P. calcar have coincident 3 to 4 mo breeding seasons. In general, P. exigua is protandrous with a broad size range over which sex change occurs. Some P. exigua, however are simultaneous hermaphrodites at the outset of gonad formation and become increasingly female with growth. This species has continuous gametogenesis and oviposits its eggs on the undersides of intertidal boulders, with enhanced oviposition during winter and spring. Newly metamorphosed P. exigua occupy intertidal microhabitats and were located in the field from August to October. It is suggested that increasing sea temperature during spring may serve to cue gamete release by P. gunnii and P. calcar and that enhanced oviposition of P. exigua in winter may be in response to conditions optimal for development of the egg masses at this time. The GI of male and female P. gunnii and P. calcar did not differ, while male P. exigua had a significantly lower GI than the females. Small males are characteristic of this latter species, and it is suggested that the decreased male investment in P. exigua is associated with its non-planktonic development. The gonad and pyloric caeca (PCI) indices of P. gunnii exhibited a reciprocal relationship, indicating that the transfer of nutrients from the caeca to the gonads supports gametogenesis. These indices were partly reciprocal in P. calcar. It is suggested that gonadal growth in P. calcar may be less dependent on caecal reserves than that in P. gunnii. The PCI of P. exigua maintained a similar level throughout the year and was higher than the GI. Although the Patiriella species have coincident breeding periods, temporal differences in the intensity of spawning appears to reproductively isolate them in the field.     

Defense mechanisms and antipredator behavior in two sympatric species of spiny lobsters, Panulirus argus and P. guttatus

The congeneric spiny lobsters Panulirus argus and P. guttatus co-occur throughout the Caribbean Sea, where they may share the coral reef habitat. Despite their phylogenetic closeness, both species have many different life-history traits that may partially explain their coexistence. However, even though both species may face the same predators, their defense mechanisms and antipredator strategies had not been compared. We compared the performance between species in 18 morphological and behavioral defense mechanisms commonly expressed by most spiny lobsters, including predator-avoidance mechanisms (activity schedule, sheltering behavior, delay to disturbance, and effect of conspecific damage-released scents on shelter choice) as well as antipredator mechanisms (body size, several parameters of the escape response and limb autospasy, clinging strength, antennal strength, and cooperative defense). As hypothesized, both species expressed all these defense mechanisms (except cooperative defense, shown only by P. argus), reflecting their phylogenetic closeness, but performed significantly differently in most, in accordance with their particular ontogenetic traits. Their comparative performance in individual defense mechanisms as well as the antipredator strategies displayed by groups of lobsters of each species in the presence of a common predator (the triggerfish Balistes vetula) showed that, in general, the defensive behavioral type of P. argus is more bold and that of P. guttatus more shy. Therefore, their distinct defensive behaviors contribute to their niche differentiation.     

Lights and shadows: growth patterns in three sympatric and congeneric sponges (Ircinia spp.) with contrasting abundances of photosymbionts

The life-history traits of long-lived benthic littoral invertebrates remain poorly understood. In this study, we analysed patterns of growth in three abundant sublittoral sponges from the western Mediterranean Sea, chosen for their close phylogenetic relatedness, sympatric distribution, and contrasting amounts of photosymbionts: high in Ircinia fasciculata, lower in I. variabilis, and absent in I. oros. Sponge area, perimeter, number of oscula, and epibiont abundance were quantified from in situ digital images taken monthly for 1.5 years and volumetric growth rates were calculated from empirical area–volume relationships. Volumetric growth rates were different among species and coherent with the photosymbiont abundance: high in I. fasciculata (40.03 ± 4.81 % year^?1, mean ± SE), low in I. variabilis (5.65 ± 6.11 % year^?1), and almost nil in I. oros (?0.04 ± 3.02 % year^?1). Furthermore, a marked seasonality was observed in the first two species, with greater growth during the warm season. The high growth rates of I. fasciculata were likely fuelled by symbiont-derived photosynthates and required to compete in the well-lit, algal-dominated habitats this species prefers. In contrast, I. variabilis and I. oros tended to dwell in shaded habitats, where competition from slow-growing invertebrates is intense, and featured lower growth rates. The flattened morphology and lower circularity of I. variabilis indicates a capacity for adaptation to any space that is freed, while I. oros had less oscula and was more massive and circular, suggesting a strategy of passive occupation and minimisation of biological interactions. The results show that even congeneric species living sympatrically can achieve important biomass using different growth and substrate occupation strategies.     

Population structure and reproductive biology of two sympatric hydrothermal vent polychaetes,Paralvinella pandorae and P. palmiformis

The alvinellid polychaetes Paralvinella pandorae Desbruyères and Laubier and P. palmiformis Desbruyères and Laubier occur at deep-sea hydrothermal vents along the Juan de Fuca and Explorer Ridges in the northeast Pacific Ocean. The population structure and reproductive biology of both species were studied in samples taken from three vent sites during six cruises in 1983 and 1984. Size-frequency analyses of two P. pandorae populations produced unimodal histograms, suggesting continuous or semi-continuous juvenile recruitment; in a third population two possible size classes were evident. Histograms of P. palmiformis displayed size-class peaks, which most likely reflected periodic recruitment of juveniles. Both species are gonochoric and gametes develop free in the coelom. Due to the simultaneous presence of a full range of gametogenic stages in P. pandorae populations, including spermatozoa in males, and to the continuous or semi-continuous recruitment pattern suggested by the size-frequency histograms, continuous reproduction is proposed for this species. In P. palmiformis a discrete, possibly synchronized, breeding cycle is thought to occur. Although maximum fecundity of P. pandorae is very low, continual reproduction over a long period of time could enhance its reproductive potential. The estimate of maximum fecundity for P. palmiformis is comparable to estimates for other polychaetes that undergo non-planktotrophic larval development. Maximum observed oocyte size was 215 and 260 m in P. pandorae and P. palmiformis, respectively. It is proposed that P. pandorae broods its young, while P. palmiformis probably undergoes demersal lecithotrophic larval development. The continual production of brooded young by P. pandorae could maintain a vent population, but severely limit dispersal to other vents. Demersal lecithotrophic larvae of P. palmiformis could repopulate vents, and potentially be carried by bottom currents to other vent sites.     

Reproduction of sympatric populations ofHeliocidaris erythrogramma andH. tuberculata (Echinoidea) in New South Wales

Reproduction ofHeliocidaris erythrogramma (Valenciennes) andH. tuberculata (Lamarck) was compared through examination of oogenesis, spermatogenesis and monthly measurement of the gonad index. These species occur sympatrically in the Sydney region. Their reproduction was examined at two sites near Botany Bay, New South Wales, Australia, from February 1989 through January 1990.H. erythrogramma produces buoyant, 450µm-diam eggs and the sperm have a head region 10µm in length. By contrast,H. tuberculata produces negatively-buoyant, 95µm-diam eggs and the sperm have a head region 4µm in length. Histochemical examination of the gonads revealed that periodic acid Schiff-positive (PAS +) material stored in the nutritive phagocytes appears to support vitellogenesis in both species. InH. tuberculata this material is utilized in the formation of PAS + yolk oligolecithal eggs, whereas inH. erythrogramma the PAS + material appears to be converted to lipid yolk in macrolecithal eggs.H. erythrogramma had a seasonal reproductive pattern with a 3 mo summer spawning period, whereas both populations ofH. tuberculata had a 9 mo breeding period characterized by the continual presence of nutrient reserves and vitellogenic oocytes which rapidly replaced spawned ova. Spawning ceased only for 3 mo over the summer. Due to the 9 mo spawning ofH. tuberculata it is not clear what factors serve to cue reproduction in this species.