An Individual-Based Model of the Red Alga Agarophyton chilense Unravels the Complex Demography of Its Intertidal Stands

Abstract

Algal demographic models have been developed mainly to study their life cycle evolution or optimize their commercial exploitation. Most commonly, structured-aggregated population models simulate the main life cycle stages considering their fertility, growth and survival. Their coarse resolution results in weak predictive abilities since neglected details may still impact the whole. In our case, we need a model of Agarophyton chilense natural intertidal populations that unravels the complex demography of isomorphic biphasic life cycles and be further used for: (i) introduction of genetics, aimed at studying the evolutionary stability of life cycles, (ii) optimizing commercial exploitation, and (iii) adaptation for other species. Long-term monitoring yield 6,066 individual observations and 40 population observations. For a holistic perspective, we developed an Individual-Based Model (IBM) considering ploidy stage, sex stage, holdfast age and survival, frond size, growth and breakage, fecundity, spore survival, stand biomass, location and season. The IBM was calibrated and validated comparing observed and estimated sizes and abundances of gametophyte males, gametophyte females and tetrasporophytes, stand biomass, haploid:dipoid ratio (known as H:D or G:T), fecundity and recruitment. The IBM replicated well the respective individual and population properties, and processes such as winter competition for light, self-thinning, summer stress from desiccation, frond breakage and re-growth, and different niche occupation by haploids and diploids. Its success depended on simulating with precision details such as the holdfasts’ dynamics. Because “details” often occur for a reduced number of individuals, inferring about them required going beyond statistically significant evidences and integrating these with parameter calibration aimed at maximized model fit. On average, the population was haploid-dominated (H:D > 1). In locations stressed by desiccation, the population was slightly biased toward the diploids and younger individuals due to the superior germination and survival of the diploid sporelings. In permanently submerged rock pools the population was biased toward the haploids and older individuals due to the superior growth and survival of the haploid adults. The IBM application demonstrated that conditional differentiation among ploidy stages was responsible for their differential niche occupation, which, in its turn, has been argued as the driver of the evolutionary stability of isomorphic biphasic life cycles.

Tetrasporophytic bias coupled with heterozygote deficiency in Antarctic Plocamium sp. (Florideophyceae, Rhodophyta)

“…In the red macroalgae Chondrus crispus (reviewed in Collén et al, 2014) and C. verrucosus (Bellgrove & Aoki, 2008), many intertidal populations are gametophyte biased. In contrast, ploidy dominance varies among species but sporophytes are often observed at greater frequencies in many populations in the Gracilariales (reviewed in Kain & Destombe, 1995, but also see Vieira et al, 2022), the Ceramiales (Cecere et al, 2000), some species of the Gigartinales (e.g., Hypnea musciformis ; Caires et al, 2013), as well as in other red macroalgae, such as Pterocladiella capillacea (Patarra et al, 2020) and green macroalgae, such as two Ulva spp. (Du et al, 2019).…”

“…Kamiya and Kawai (2002) showed evidence that maternal care provides germlings with additional nutrients leading to increased growth rates as compared to carpospores released from cystocarps which had been excised from the female gametophyte shortly after fertilization. Based on the extensive investigation of each life cycle stage in G. chilensis , Vieira et al (2022) observed that varying environmental factors throughout the year favored different stages. Whether similar mechanisms maintain both life cycle stages in Antarctic Plocamium sp.…”

“…Diploid stages have been hypothesized to be favored when nutrients are not limiting (Lewis, 1985), though this hypothesis was based on unicellular taxa, which raised questions as to whether it would apply for multicellular species (Bell, 1994). Vieira et al (2021) demonstrated that resource limitation more broadly may have differential effects on haploid and diploid stages of unicellular and multicellular taxa. Krueger-Hadfield and Ryan (2020) observed an increase in growth rates of adult Gracilaria vermiculophylla thalli under nutrient-enriched conditions but no differences among life cycle stages.…”

“…Antarctic seas are nutrient rich (Ducklow et al, 2007); hence, nutrients would only rarely, if ever, be expected to be limiting for macroalgal growth along the western Antarctic Peninsula (Wiencke & Amsler, 2012). Vieira et al (2021) expanded the nutrient limitation hypothesis to include resources in general and showed that G. chilensis haploids would perform better under resource limiting conditions. As such, nutrient availability in the Antarctic environment may contribute to the relative dominance of tetrasporophytes over gametophytes in Plocamium sp., which remains to be empirically tested.…”

“…Juvenile G. gracilis (Destombe et al, 1989) and adult G. vermiculophylla (Krueger-Hadfield & Ryan, 2020) gametophytes have higher mortality compared to tetrasporophytes. In G. chilensis, female gametophytes had higher survival (Vieira et and growth rates (Vieira et al, 2021), but terasporophytic germlings outperformed gametophytic germlings at very low and very high densities of adult fronds (Vieira et al, 2018b). In contrast, carpospore survival in G. chilensis was higher compared to tetraspores (Vieira et al, 2018b).…”