The timing of gamete release by fucoid algae, although known to be restricted to calm days is not clearly understood within a circadian time scale. The need for externally fertilizing species to avoid gamete dilution suggests that in wave-exposed areas spawning may occur during particular tidal phases. However, this may differ between mating systems, as selfing species may be less affected by gamete dilution. In this study, two different approaches were used to determine when egg release occurs during the tidal cycle in two sister species with different mating systems. First, egg settlement of Fucus vesiculosus (dioecious) and Fucus spiralis (selfing hermaphrodite) was quantified on removable substrates (egg settlement disks) every day for 2 months and settlement patterns were used to statistically estimate the radius of a circle that would encompass 99% of each patch of settled eggs (the egg dispersal radius). Also, egg release was quantified every 2 h during the tidal cycle. A significantly larger egg dispersal radius (P < 0.02) was found for F. spiralis than F. vesiculosus, and this difference was somewhat site dependent with a greater difference between species in exposed sites. The egg dispersal radius was negatively correlated with significant wave height and positively correlated with sea surface temperature for both the species (P < 0.05), with a greater effect of both the factors for F. spiralis than for F. vesiculosus. Egg release during the tidal cycle was variable between species and experiments, with F. vesiculosus releasing more eggs, later in the day, and at a lower tide, than F. spiralis, which released fewer eggs, throughout the day and at all tides. The dioecious species, F. vesiculosus, may have developed a specific adaptation for timing the egg release to periods when emersed in exposed habitats to avoid rapid dilution of gametes that require outcrossing for fertilization. On the other hand, egg release for F. spiralis, which can self-fertilize, occurred both when emersed and immersed, suggesting this species has developed less synchrony with specific environmental factors. Site dependence also suggests local wave conditions can modulate timing of release. The data are consistent with the relaxation of the selective constraints of water motion on fertilization success in a selfing hermaphrodite, relative to an obligate outcrossing species. Results support the idea that species with different mating systems evolve different sensitivities to environmental cues for gamete release with specific implications for inbreeding and successful external fertilization in the ocean.
The authors are very thankful to the marine laboratory of Universidade de Évora for hosting us in Sines (especially to Teresa and João Cruz), and to Rafael Bermudez for technical help. We thank anonymous referees for their helpful suggestions. This study was funded by the Portuguese Science Foundation (FCT), including programs POCTI, POCI with FEDER and ESF. Funding to LBL was provided by CONACYT and UC MEXUS. Funding to FF was provided by NSF and CA Sea Grant.
Belorustseva SA, Marfenin NN (2002) Affect of variable phases of tide cycle on reproduction of Laomedea flexuosa (Hydroidea, Thecaphora). Zh Obshch Biol 63(1):50–61PubMedGoogle Scholar
Berndt ML, Callow JA, Brawley SH (2002) Gamete concentrations and timing and success of fertilization in a rocky shore seaweed. Mar Ecol Prog Ser 226:273–285. doi:10.3354/meps226273CrossRefGoogle Scholar
Billard E, Serrão EA, Pearson GA, Engel CR, Destombe C, Valero M (2005) Analysis of sexual phenotype and prezygotic fertility in natural populations of Fucus spiralis, F. vesiculosus (Fucaceae, Phaeophyceae) and their putative hybrids. Eur J Phycol 40:397–407CrossRefGoogle Scholar
Brawley SH (1992) Fertilization in natural populations of the dioecious brown alga Fucus ceranoides and the importance of the polyspermy block. Mar Biol (Berl) 113:145–157. doi:10.1007/BF00367648CrossRefGoogle Scholar
Brawley SH, Johnson LE, Pearson GA, Speransky V, Li R, Serrão E (1999) Gamete release at low tide in fucoid algae: maladaptive or advantageous? Am Zool 39(2):218–229Google Scholar
Coleman MA, Brawley SH (2005a) Are life history characteristics good predictors of genetic diversity and structure? A case study of the intertidal alga Fucus spiralis (Heterokontophyta; Phaeophyceae). J Phycol 41(4):753–762. doi:10.1111/j.0022-3646.2005.04136.xCrossRefGoogle Scholar
Coleman MA, Brawley SH (2005b) Spatial and temporal variability in dispersal and population genetic structure of a rockpool alga. Mar Ecol Prog Ser 300:63–77. doi:10.3354/meps300063CrossRefGoogle Scholar
Ladah LB, Bermudez R, Pearson GA, Serrão EA (2003) Fertilization success and recruitment of dioecious and hermaphroditic fucoid seaweeds with contrasting distributions near their southern limit. Mar Ecol Prog Ser 262:173–183. doi:10.3354/meps262173CrossRefGoogle Scholar
Levitan DR, Sewell MA, Chia FS (1992) How distribution and abundance influence fertilization success in the sea urchin Strongylocentrotus franciscanus. Ecology 73:248–254. doi:10.2307/1938736CrossRefGoogle Scholar
Marshall DJ, Semmens D, Cook C (2004) Consequences of spawning at low tide: limited gamete dispersal for a rockpool anemone. Mar Ecol Prog Ser 266:135–142. doi:10.3354/meps266135CrossRefGoogle Scholar
Pearson GA, Brawley SH (1996) Reproductive ecology of Fucus distichus (Phaeophyceae): an intertidal alga with successful external fertilization. Mar Ecol Prog Ser 143:211–223. doi:10.3354/meps143211CrossRefGoogle Scholar
Pennington JT (1985) The ecology of fertilization of echinoid eggs: the consequences of sperm dilution, adult aggregation, and synchronous spawning. Biol Bull 169:417–430. doi:10.2307/1541492CrossRefGoogle Scholar
Perrin C, Daguin C, Van de Vliet M, Engel C, Pearson GA, Serrão EA (2007) Implications of mating system for genetic diversity of sister algal species: Fucus spiralis and Fucus vesiculosus (Heterokontophyta, Phaeophyceae). Eur J Phycol 42:219–230. doi:10.1080/09670260701336554CrossRefGoogle Scholar