Sex-specific reproductive trade-offs in the gregarious fucoid macroalga Ascophyllum nodosum

Abstract

The existence of sex-specific reproductive trade-offs is well established in plants. They usually occur because females invest more resources into reproduction than males, and have to compensate by sacrificing growth or defence. Investigations into by-sex differences in resource allocation by seaweeds are comparatively scarce. A small number of authors report differences between the sexes in some red algae, but known by-sex differences in brown algae are largely confined to the reproductive structures. In this study, sex-specific reproductive trade-offs are investigated in the common temperate brown alga Ascophyllum nodosum from three distinct populations. Quantified investments into growth, defence, and reproduction of a large number of individuals (n = 720) selected across a full annual cycle are presented in parallel with feeding trials using a common gastropod herbivore and a comprehensive assessment of the biotic and abiotic stressors impacting on A. nodosum at three sites. These reveal that sex-specific reproductive trade-offs occur in two of the three populations, as females invest more into reproduction than males and are subsequently less chemically defended for the months post gamete release. Feeding trials confirm that this leaves females more vulnerable to grazing pressure during these months, although mortality and competitive ability appear unaffected in the field. Possible causes of the trade-offs made by females are discussed, and new avenues of investigation are identified which could reveal interesting parallels between seaweeds and higher plants.

Drivers of Sex-specific Trade-offs in the Macroalga <i>Ascophyllum nodosum</i>

“…In accordance with results on many higher-plant species, sex-specific-trade-offs positively correlate with stress in Ascophyllum nodosum, with females investing more into reproduction and therefore being lesser-defended than males at sites of high wave-action and herbivory [5]. Because eggs are limited compared to sperm in fucoids [6], and female reproductive tissue is both more valuable and often more expensive to produce, there are two non-mutually exclusive hypotheses that explain the pattern of reproductive trade-offs in this species.…”

“…Limited data exists on sex-specific disparities in seaweeds, but by-sex differences in mortality [1], production of metabolites [2], threshold size for reproduction [3], and susceptibility to herbivory [4][5] have been reported. In accordance with many terrestrial plants, the females of some seaweeds put more energy into reproduction [6], although sex-specific differences in reproductive effort are not always present [3,5]. Sexual dimorphism and other sex-specific trade-offs (e.g.…”

“…higher reproductive effort at the expense of anti-herbivore defence) arise in plants and algae because stressors act on males and females differently, owing to sexspecific costs associated with reproduction [7]. Stress therefore increases trade-offs in many plants [8], although only one investigation has so far examined the manifestation of sex-specific trade-offs with stress in a marine alga [5].…”

“…Therefore, females may be selected for which prioritise reproduction since increasing fecundity at the local scale most likely requires more eggs but not more sperm, because the latter outnumber the former by orders of magnitude in fucoid seaweeds [6]. Expenditure in reproduction comes at the cost of defence, and so sex-specific trade-offs manifest in these highly stressed populations [5]. Secondly, wave action and herbivory cause substantial frond damage, often resulting in the loss of the upper half of the frond [13,14].…”

The chemical defences of the invasive alga Sargassum muticum (Yendo) Fensholt correlate to mesoherbivore diversity, but not to time-since-invasion

“…Phlorotannin abundances in the fronds of Sargassum muticum were positively dependent on the diversity of grazers in its stand. Although phlorotannins are found in many fucoids, the abundances observed in S. muticum were particularly high; comparable to those found in the highly grazer-resistant Ascophyllum nodosum Kurr & Davies, 2017b). Pronounced invasion success has been attributed to chemical defences in other species of algae (Forslund et al, 2010;Enge et al, 2012;Nylund et al, 2012;Svensson et al, 2013) and plants (Van Kleunen & Schmid, 2003;Leger & Forister, 2005;Huang et al, 2010;Lind & Parker, 2010), and may also explain the success of S. muticum outside of its native range (Engelen et al, 2015).…”