Trait-based ecology (TBE) has proven useful in the terrestrial realm and beyond for collapsing ecological complexity into traits that can be compared and generalized across species and scales. However, TBE for marine macroalgae is still in its infancy, motivating research to build the foundation of macroalgal TBE by leveraging lessons learned from other systems.

Our objectives were to evaluate the utility of mean trait values (MTVs) across species, to explore the potential for intraspecific trait variability, and to identify macroalgal ecological strategies by clustering species with similar traits and testing for bivariate relationships between traits. To accomplish this, we measured thallus toughness, a trait associated with resistance to herbivory, and tensile strength, a trait associated with resistance to physical disturbance, in eight tropical macroalgal species across up to seven sites where they were found around Moorea, French Polynesia.

We found interspecific trait variation generally exceeded intraspecific variation across species. Further, MTV within species varied across sites, suggesting future research should focus on whether these traits are influenced by site-specific differences in biotic and abiotic drivers. Species grouped into three clusters representing different ecological strategies: species that were defended against herbivores but not strong, species that were strong but not defended, and species that were neither. Intraspecific Standardized Major Axis regressions revealed five species exhibited significant or marginally significant positive relationships between these two traits, suggesting trait syndromes within species. Only one species exhibited a significant intraspecific tradeoff, as indicated by a negative regression slope.

Synthesis: Our results point to three key takeaways that should provide a foundation to rapidly advance development of TBE for macroalgae in the future. First, our evidence supports the use of MTVs for macroalgae. Second, we identified significant spatial variability in macroalgal traits may indicate an ability to respond to shifting environmental drivers. Third, measuring even a few traits can be a powerful tool to identify different ecological strategies to resist disturbances such as herbivory and removal by wave action.  We hope these novel findings motivate future research into a wider suite of macroalgal traits, functions, and strategies to further develop trait-based approaches for marine macroalgae.

Approaches

Our overall approach was to measure MTV and the associated variance of two functional traits for eight common species of coral reef macroalgae across seven fringing reef sites in Moorea, French Polynesia. To maximize our probability of capturing a wide range of interspecific variation, we chose a diverse set of commonly occurring algal species while to maximize our probability of capturing a wide range of intraspecific variability, we collected these algae at a diverse set of fringing reefs. We aimed to determine if MTV differs between species as well as within species across sites. Next, we identified ecological strategies used by clusters of species that could be used to resistant either herbivory or physical disturbance. Finally, we assessed the nature of bivariate trait relationships for individuals within each species.

Study system

 We conducted our study on fringing reefs of Moorea, a high volcanic island in the Society Islands archipelago of French Polynesia in the South Pacific. Moorea is approximately 18 kilometers northwest of Tahiti. We targeted fringing reefs for our study because, while variable, macroalgae are generally abundant on these reef types around Moorea.

We chose seven fringing reef sites with abundant and diverse macroalgae. From easternmost to westernmost, sites included Temae (TE), Maharepa (MA), Gump (GU), Green Marker (GM), Hilton (HI), Sailing School East (SSE), and Sailing School West (SSW). While all sites were fringing reefs, they varied in their continuity (continuous vs. patch reef) and exposure to wind and waves (within a bay with anthropogenic influences or along the more exposed open shore), which we reasoned maximized our likelihood of capturing each algal species’ potential for intraspecific trait variation. Temae, Maharepa, and Hilton likely experience the highest water movement as they are on the more exposed northern or eastern shore. In addition, a portion of Temae’s backreef was filled to create the airport, resulting in substantial wave driven current (pers. obs.). In contrast, Gump, Sailing School East, and Sailing School West are located within bays and are likely more enriched with nutrients due to greater proximity and exposure to local agricultural land (Clausing et al., 2016; De’ath & Fabricius 2010). Finally, herbivory pressure is generally higher at Maharepa and Hilton compared to sites within the bays (Bergman et al., 2016). Temae is an MPA and appears to have abundant herbivorous fish communities (pers. obs.); however, we could not find any formal surveys.

Algal collection

We collected eight macroalgal species from each of our seven sites where they were available and noted the life cycle type. If possible, we also noted the generation ID of the thallus collected as ploidy has been shown to influence algal responses to environmental drivers in some cases (see Krueger-Hadfield 2020; Table 1) and therefore may influence trait distributions four brown algae (class Phaeophyceae) Dictyota bartayresiana (Dictyotales), Padina boryana (Dictyotales; lightly calcified), Sargassum pacificum (Fucales), and Turbinaria ornata (Fucales), three red algae (division Rhodophyta) Acanthophora spicifera (Ceramiales), Amansia rhodantha (Ceramiales), and Galaxaura divaricata (Nemaliales; heavily calcified), and one green alga (division Chlorophyta) Halimeda opuntia (Bryopsidales; heavily calcified). D. bartayresiana, P. boryana, and A. spicifera tend to occur in more sheltered habitats (Guiry & Guiry 2022) and can be found in many fringing reef habitats in Moorea (pers. obs.). A. rhodantha, G. divaricata, H. opuntia, T. ornata, and S. pacificum can occur in sheltered areas to more high-energy, exposed areas of the reef, with T. ornata and S. pacificum the only species able to persist on the high-energy reef crest. H. opuntia, A. spicifera, T. ornata, S. pacificum are able to reproduce asexually via fragmentation (Kilar & McLachlan 1986; Walters et al., 2002), and some studies suggest species in the Dictyota genus are capable of reproduction via fragmentation as well (Herren et al., 2006).

From each site, approximately 15 whole, macroscopic thalli that appeared healthy (no decay visible) for each species were haphazardly collected via snorkel at approximately 1- to 2-m depth. Although our target was n=10, extra thalli were collected in case trait measurements needed to be repeated (see below). Macroalgae were collected and tested the same day between April 21 and May 15, 2019, usually completing approximately one site per day. All collected algal thalli were immediately transported back to the UC Berkeley Gump South Pacific Research Station and placed in an outdoor flow-through water table. Using ambient seawater, thalli were cleaned of sediment and associated organisms and processed within approximately six hours of collection.

Thallus toughness

 To measure thallus toughness (“weight to penetrate”) for each species from each site, we attempted to collected similar-sized individuals for each species and sampled blades or tissue from the middle of each thallus (where applicable, see below), as all of the collected algal species exhibit apical growth. Using this location across all species maximized our ability to achieve a representative average for thallus toughness as it limited sampling tissue that may differ in toughness due to differences in age. For example, for more simple growth forms that were primarily blade-like (D. bartayresiana and P. boryana) or mainly composed of branches without distinct stipes (A. spicifera, G. divaricata, and H. opuntia), we sampled tissue from the blade or branch in the middle of each thallus. For more complex growth forms with distinct stipes and blades (S. pacificum, T. ornata) or a midrib (A. rhodantha), we sampled individual blades from the middle of each thallus and tested the middle of each blade (avoiding the midrib for A. rhodantha). Despite our best attempts to minimize variation in trait values due to algal age/size, it is possible that sites could differ in age of the algal communities (i.e., sites with new algal growth vs. no new growth), which would contribute to inter-site trait variation.

To measure thallus toughness for each species, we secured each algal subsample below a penetrometer so the needle of the penetrometer gently rested on the surface of the thallus (adapted from Duffy & Hay 1991; Bittick et al., 2016; Ryznar et al., 2021). Then, we sequentially added weight to the penetrometer until the needle just pierced the thallus surface. This was repeated for 10 different replicate thalli for each species at each site.

Thallus tensile strength

 To measure thallus tensile strength (“weight to break”), we used 10 whole replicate thalli (apex through holdfast) of similar sizes for each species from each site. The basal end at the holdfast (where one was apparent) of each thallus was secured to a spring scale while the apical end was pulled until the thallus broke. The force (weight) required to break the thallus was used as a measure of tensile strength. Data were discarded if the thallus broke where it was secured at the base or where it was being pulled near the apical end.