The Role of Alternate Life-History Stages of a Marine Macroalga: A Seed Bank Analogue?

Abstract

Many organisms occurring in temporally variable environments have evolved life-history traits that enable their populations to persist during unfavorable environmental conditions. Numerous terrestrial plants, insects, and marine invertebrates, for example, rely on resting stages that disperse their propagules in time. Although widely observed among many taxa, few examples exist for marine macroalgae, at least in part because of the methodology involved in studying them. Here, I determined that microscopic life stages of the annual marine macroalga Desmarestia ligulata overwinter during periods when the macroscopic thalli are absent, thereby allowing this species to persist in temporally variable environments. Examination of field-grown microscopic stages with fluorescence microscopy identified these stages as gametophytes. Holdfast tagging experiments determined that recruitment of the macroscopic stages was not enhanced by regrowth of perennial thalli as observed in other macroalgae, suggesting that overwintering gametophytes were the sole source of sporophyte recruitment. In contrast to true resting stages, Desmarestia gametophytes were not dormant, but rather were metabolically active, sensitive to small differences in environmental quality, and highly subject to physical damage. Gametophyte photosynthetic rates were greater under higher irradiance, and growth rates were greater under longer photoperiods and higher irradiance. Although their survival appeared to be reduced by grazing from large (Ͼ1 cm) invertebrates and sedimentation, gametophytes were able to survive in the field for at least 15 mo and thereby enhance sporophyte recruitment more than a year after settlement. I suggest that Desmarestia gametophytes be regarded as alternate life-history stages that simply maintain populations under a different set of environmental conditions than the macroscopic sporophytes do, rather than as ''dormant'' or ''resting'' stages.

Estimating scale-dependency in disturbance impacts: El Ni�os and giant kelp forests in the northeast Pacific

“…In contrast, recovery occurred within~6 months at all locations in southern and central California, presumably facilitated by the strong La Niña (Hayward et al 1999) and the presence of microscopic life stages (e.g. Dayton 1985;Edwards 2000). Then, nearly 2 years after the El Niño ended (June 2000), outbreaks of purple and red urchins (Strongylocentrotus purpuratus and S. fransiscanus) denuded the kelp at some sites within certain areas in southern California (e.g.…”

ARRESTED DEVELOPMENT OF GIANT KELP (MACROCYSTIS PYRIFERA, PHAEOPHYCEAE) EMBRYONIC SPOROPHYTES: A MECHANISM FOR DELAYED RECRUITMENT IN PERENNIAL KELPS?1

“…Laboratory culture studies (Anderson and North 1969, Lüning and Dring 1972, Lüning and Neushul 1978, Lüning 1980b, Dring and Lüning 1981, Lüning and tom Dieck 1989) and in situ field experiments (Deysher and Dean 1986a) have shown that many aspects of gametophyte growth, development, and reproduction are synchronized to periodically varying cues such as photoperiod, spectral quality of light, and temperature. Field studies have identified gametophytes as the microscopic stage responsible for delayed recruitment in at least one annual brown alga (Edwards 2000). However, the programmed responses that adapt gametophytes for response to predictable periodic variation in environmental quality may be costly when adult population dynamics are dominated by unpredictable disturbances and recruitment is limited by patchy episodic fluctuations in limiting resources.…”

“…Broad dispersal of propagules in space can enhance persistence when short‐lived sessile adults are faced with high spatial and temporal variability in recruitment success (Dayton 1973, Venable and Lawlor 1980, Levin et al 1984) but may result in recruitment failure when unfavorable conditions periodically extend over large regions. As an alternative, seaweeds may adopt limited propagule dispersal in space and avoid recruitment‐limiting factors in time by either restricting propagule production to predictable periods of high recruitment success or developing mechanisms by which settlers can delay recruitment to adult populations until locally unfavorable conditions have subsided (Hoffmann and Santelices 1991, Edwards 2000). When adult mortality or recruitment‐limiting factors vary predictably (e.g.…”

“…due to seasonal changes in light or nutrients), many seaweeds have evolved programmed responses to periodic exogenous cues (e.g. photoperiod or temperature) to synchronize propagule production or the emergence of settlers to the onset of favorable conditions (Lüning 1980a, Waaland et al 1987, Santelices 1990, Edwards 2000). Such rigid endogenous cycles, however, may not be advantageous when adult mortality or the onset of recruitment‐favorable conditions are episodic, for example, in the presence of stochastic fluctuations in benthic irradiance due to algal canopy disturbance (Reed and Foster 1984, Tegner and Dayton 1987, Seymour et al 1989) or nutrient supply due to variation in upwelling intensity (Dayton et al 1999).…”

Contrasting timing of life stages across latitudes – a case study of a marine forest-forming species

“…3). Nevertheless, many factors influence the development of the microscopic stages: shading is known to inhibit growth, which, in the field, is expected to be halted with sporophyte decay; natural light and water motion may result in faster development; and lower nutrient concentration, when compared with the enriched culture medium, may be limiting to growth (Edwards, 2000;Andersen, 2005;Pedersen et al, 2012;Carnell & Keough, 2014). As such, extrapolation of the results obtained in controlled conditions to the field should be made with caution.…”