Spermcasting of spermatozeugmata by the bivalvesNutricola confusaandN. tantilla

Abstract

The dynamics and consequences of the varied reproductive modes of marine invertebrates is a rich and vibrant field of inquiry for ecological and evolutionary studies. One mode of reproduction that is not as well-studied as others is "spermcasting" or "spermcast mating," when males broadcast sperm and females retain eggs and brood developing embryonic stages. This type of reproduction occurs in two small (maximum adult shell length~5-6 mm) venerid bivalves, Nutricola confusa and N. tantilla, that live in protected bays of the temperate eastern Pacific. Females of these species brood developing embryos in chambers formed by the inner demibranchs, and release fully formed juveniles. We discovered that upon exposing clams to fluvoxamine, a selective serotonin reuptake inhibitor, males release spermatozeugmata, clusters of sperm cells attached by their heads to a central core. Spermatozoa of Nutricola have unusually long, needle-shaped heads that are approximately one quarter of the total length of the cell. These heads are curled and "packaged" into the hemispherical-shaped cores of spermatozeugmata. The cores are about one-third as long as the heads, and the tails protrude out of the opposite side of the cap of the core. The spermatozeugmata display two different swimming patterns, one where the tails beat in synchrony, and the other where they do not. The size of the cores is not significantly different in the two species, but spermatozeugmata of N. tantilla have significantly longer and wider tails than those of N. confusa. Advantages to spermcasting spermatozeugmata instead of individual spermatozoa may include enhanced dispersal and increased probabilities of fertilization. One consequence of spermatozeugmata (rather than individual spermatozoa) entering female brood chambers might be lowering of the effective population size. For species like these, which lack pelagic larvae, spermatozeugmata could increase dispersal and gene flow.

Egg fertilisation in a freshwater mussel: effects of distance, flow and male density

“…Note that the left and middle columns (distance from males and male density) exclude ponds with no upstream females (model 1), and the right column (upstream females) includes results only from 25 m distance treatments (model 2). Fertilisation success in relation to male density is not shown for model 2, but these results were similar to those from model 1 and are reported on Table 2. the low flows in our experiments (0.03-0.04 m s À1 ), viable sperm could be transported about 5 km in 48 h and nearly 8 km in 72 h, corresponding to the range of extended sperm longevity provided by spermatozeugmata (see Ishibashi et al, 2000;Falese et al, 2011). The directional movement exhibited by spermatozeugmata could further extend dispersal distance and may be especially important in lentic environments without flow.…”

“…Release of sperm in spermatozeugmata is also likely to be important in facilitating efficient fertilisation. Even at the low flows in our experiments (0.03–0.04 m s −1 ), viable sperm could be transported about 5 km in 48 h and nearly 8 km in 72 h, corresponding to the range of extended sperm longevity provided by spermatozeugmata (see Ishibashi et al ., ; Falese et al ., ). The directional movement exhibited by spermatozeugmata could further extend dispersal distance and may be especially important in lentic environments without flow.…”

“…In spermcasters, males release gametes into the water, but females retain eggs in a brood chamber where eggs are fertilised by sperm obtained from the water (Bishop & Pemberton, 2006). Spermcasting typically is accompanied by release of sperm in aggregations called spermatozeugmata, which enhance sperm motility and longevity and allow fertilisation of numerous eggs simultaneously (Yund, 2000;Pemberton et al, 2003;Falese, Russell & Dollahon, 2011). Gradual acquisition and concentration of sperm by females over long time periods through suspension feeding can also increase the efficiency of spermcasting.…”

“…Like other spermcasters, male mussels release sperm into the water, and sperm are captured by females during filter feeding after which eggs are fertilised within the suprabranchial chamber (McMahon & Bogan, 2001). Mussel spermatozeugmata contain about 3000-9000 sperm, and they appear to contain a favourable osmotic environment, and potentially lipid reserves, that extend the longevity of sperm to 48-72 h (Ishibashi, Komaru & Kondo, 2000;Falese et al, 2011). Spermatozeugmata also exhibit directional movement, and it is proposed that they exhibit taxis towards chemical signals produced by ovigerous females (Barnhart & Roberts, 1997;Ishibashi et al, 2000;Falese et al, 2011).…”

“…Mussel spermatozeugmata contain about 3000-9000 sperm, and they appear to contain a favourable osmotic environment, and potentially lipid reserves, that extend the longevity of sperm to 48-72 h (Ishibashi, Komaru & Kondo, 2000;Falese et al, 2011). Spermatozeugmata also exhibit directional movement, and it is proposed that they exhibit taxis towards chemical signals produced by ovigerous females (Barnhart & Roberts, 1997;Ishibashi et al, 2000;Falese et al, 2011). Spermatozeugmata are reported for all five North American tribes within the family Unionidae, in the Margaritiferidae, and in two European and six Asian species, suggesting that they are a general feature of freshwater mussels worldwide (Haag, 2012 and sources therein).…”