The success of invasive species can be measured by invasiveness, which depicts intrinsic characteristics that enable them to thrive in new environments. In invasive seaweeds, for example, the persistence of multiple overlapping cohorts throughout the year plays a key role in increasing plant cover and exerting unrelenting pressure on invaded areas. The marine brown macroalgae Rugulopteryx okamurae has recently established abundant populations in the Mediterranean Sea and Atlantic Ocean, negatively affecting both biodiversity and socioeconomic factors by unprecedently aggressive invasive behaviour. The objective of the study is to understand the invasiveness of R. okamurae through its popu lation dynamics. For this, a year-round study was conducted in a protected habitat of Posidonia oceanica in southern Spain, revealing that R. okamurae uses alternating mechanisms for population maintenance. It achieves high density of young individuals in late summer and autumn, peaking at 3285 individuals per square metre. In spring and early summer, the population shifts towards fewer – but larger – individuals, with densities dropping to 888 individuals per square metre and biomass reaching a peak of 170 g dry weight (DW) per square metre. Six overlapping cohorts were identified by Gaussian curves. They persisted throughout the year, but they were not related to environmental factors, which indicates adaptive physiological mechanisms that sustain dense monospecific populations. Additionally, the association between cohorts and different morphotypes suggests that R. okamurae phenotypic plasticity enables its persistence in introduced areas. These findings provide valuable insights into the biological traits underpinning its invasiveness in P. oceanica meadows, revealing temporal windows of invasiveness driven by different mechanisms. This knowledge is crucial for developing effective conservation and management strategies aimed at mitigating the impact of this invasive species.

Demography, density, generation, macroalga, Posidonia oceanica, recruitment

Invasion success refers to an invasive species’ ability to progress through all stages of invasion, from introduction to dispersion, by overcoming ecological barriers and progressing through successive stages of establishment and expansion in a new environment (Gioria et al. 2023). Studies aiming to identify and understand the factors that contribute to the success of invasive species have led to the development of various invasive hypotheses (Lowry et al. 2013). Currently, there are more than thirty invasion hypotheses that try to explain the relationship between invasive species, invaded communities and their interactions (Enders et al. 2018). According to Gioria et al. (2023), invasion hypotheses can be grouped into three major categories, namely: (1) propagule pressure, which involves the introduction efforts by invasive species in a new area and is defined as the number and frequency of propagule release (Lockwood et al. 2005; Colautti et al. 2006), (2) invasibility, referring to the characteristics of the receiving ecosystem and its susceptibility to being invaded (Catford et al. 2012; Colautti et al. 2014) and (3) invasiveness, referring to intrinsic characteristics of the species, including functional traits that determine its invasive potential (Pyšek et al. 2014; Jehangir et al. 2024). In this context, identifying the traits that serve as good predictors of invasiveness involves several factors, including physical performance, growth rate, size, biomass allocation, physiology and phenotypic plasticity (Richardson and Pyšek 2006). The latter expands the range of responses to biological and abiotic factors encountered in introduced areas, allowing the species to adapt quickly to the new environment and facilitating their establishment and expansion (Richards et al. 2006). This trait has been used to evaluate invasiveness by comparing population abundances and survival rates with native populations (Ebeling et al. 2008; Colautti et al. 2014). Collecting censuses across all major life stages of invasive species and employing demographic models are essential tools for gaining deeper insights into the population dynamics of invasive species (Williams et al. 2010; Colautti et al. 2014).

The study of seaweeds’ invasiveness has predominantly focused on a limited number of species (Dalla Vecchia et al. 2020). The common traits that contribute to their invasiveness are morphology, physiologic plasticity, productivity and reproduction. These are the most studied characteristics (Mabey et al. 2023). Invasive seaweeds often show rapid growth rates and early maturation of reproductive structures, which allows them to quickly establish and spread in new environments (South et al. 2017; Zanolla et al. 2017). Other traits, including multiple overlapping cohorts maintained by both older individuals and new recruits, were described for Undaria pinnatifida (Harvey) Suringar (Schiel and Thompson 2012) and Asparagopsis taxiformis (Delile) Trevisan (Zanolla et al. 2019). This ability to persist year-round in introduced areas has been attributed to their morphological and physiological plasticity (Campbell 1999; Zanolla et al. 2015).

Rugulopteryx okamurae (E.Y. Dawson) I.K. Hwang, W.J. Lee & H.S. Kim (Dictyotaceae, Phaeophyceae), a flattened brown seaweed with dichotomous branching (Hwang et al. 2009), is native to the western Pacific Ocean (Verlaque et al. 2009). Starting as an unprecedented cryptic invasion in the western Mediterranean in 2015, it now forms abundant populations in Spain, including the Canary Islands and the Chafarinas Archipelago (Altamirano et al. 2016; REDEXOS 2022); France (Ruitton et al. 2021); Italy (Bellisimo et al. 2024); Morocco (El Aamri et al. 2018); and Portugal, including the Azores and Madeira (Faria et al. 2021; Bernal-Ibáñez et al. 2022; Liulea et al. 2023). Currently, R. okamurae continues its expansion both in the Mediterranean Sea and the Atlantic Ocean, being most recently recorded in northern Spain, which indicates a worrying upward trend in its spread (Díaz-Tapia et al. 2024). Predictive models suggest that the European and north African coasts are highly favourable habitats for this species, so it is likely that its expansion will continue in the coming years (Muñoz et al. 2019). Like other Dictyotaceae species, R. okamurae exhibits a digenetic isomorphic life cycle, alternating haploid gametophytes with diploid sporophytes. At a morphological level, it presents up to three different morphotypes throughout the year in both native and introduced areas (Sun et al. 2006; Salido and Altamirano 2020). The species can reproduce by propagules, asexually by mitotic monospores and sexually by gametes and meiotic tetraspores, but gametangia have only recently been observed in northern Spain (Díaz-Tapia et al. 2024).

Rugulopteryx okamurae can settle on both horizontal and vertical rocky surfaces within a bathymetric range from eulittoral zones to depths of more than 50 m (García-Gómez et al. 2018; Altamirano et al. 2019). In southern Spain, R. okamurae has seriously impacted native flora, including the seagrass Posidonia oceanica (Linnaeus) Delille (García-Gómez et al. 2018; Junta de Andalucía 2019). Posidonia oceanica is a native seagrass listed in the Spanish List of Wild Species under the Special Protection Regime (Listado Español de Especies Silvestres en Régimen de Protección Especial y Catálogo Español de Especies Amenazadas) (Real Decreto 139/2011). It is also considered to form a priority habitat by the Habitats Directive (Council Directive 92/43/EEC). Similar impacts on native flora have been observed in the Azores Islands (Faria et al. 2022), where R. okamurae is replacing dominant species and altering the structure of shallow-water benthic communities. The fast and abundant proliferation of R. okamurae biomass not only produces high environmental impacts, but also socioeconomic ones (Altamirano et al. 2016; MITECO 2022). In particular, the fishing industry has been suffering economic losses estimated in millions of euros because of a decrease in fish stocks (MITECO 2022). Moreover, the extensive efforts to remove castaway biomass accumulated from beaches in tourist areas is also affecting local administrations (MITECO 2022). All these impacts have led to its inclusion in the List of Invasive Alien Species of Union Concern, being the first seaweed to be added (Commission Implementing Regulation (EU) 2022/1203 of 12 July 2022 amending Implementing Regulation (EU) 2016/1141). However, despite numerous studies about the species’ potential biotechnological uses (e.g. Romero-Vargas et al. (2024)), only few studies focused on its basic biology, which is key to our understanding of the risks associated with its invasion and to lay the groundwork for implementing effective conservation and management strategies for affected marine ecosystems.

In this context, the objective of the present study is to understand the invasiveness of R. okamurae by analysing its population dynamics on an invaded P. oceanica meadow in southern Spain and exploring the relationship of several demographic descriptors with abiotic environmental factors throughout the year.

Population dynamics of R. okamurae on a P. oceanica meadow during the year explains its invasive behaviour, characterised by the constant presence of a high density of individuals. This is achieved through its ability to continuously produce recruits and the presence of year-round short-lived overlapping cohorts that are not affected by the environmental parameters of the area.

The seaweeds’ continuous presence is a characteristic of invasiveness shared amongst invasive seaweed species in invaded areas. Examples include the red seaweeds Womersleyella setacea (Hollenberg) R.E. Norris (Cebrian and Rodríguez-Prieto 2012), Asparagopsis armata Harvey (Aranda et al. 1984) and A. taxiformis (Zanolla et al. 2019), the brown seaweeds Sargassum muticum (Yendo) Fensholt (Thomsen et al. 2006) and U. pinnatifida (Schiel and Thompson 2012) and the green seaweed genus Caulerpa, specifically C. taxifolia (M. Vahl) C. Agardh (de Villèle and Verlaque 1995) and C. cylindracea Sonder (Ruitton et al. 2005). All these species showed the ability to maintain stable populations throughout the year, suggesting the existence of adaptive physiological mechanisms to the newly-invaded area and posing a continuous impact over native communities. Likewise, R. okamurae demonstrated a remarkable ability to establish dense monospecific populations, maintaining densities exceeding 3000 individuals per square metre and reaching biomass up to 170 g DW per square metre. These values greatly surpass other documented invasive seaweeds. For instance, A. taxiformis in the southern Iberian Peninsula, reached the highest biomass in the summer (Zanolla et al. 2017), but these values were 40% lower than those recorded for R. okamurae in this study. Another example was U. pinnatifida with a maximum density of about 100 individuals per square metre in affected areas in New Zealand (Schiel and Thompson 2012) or S. muticum with a maximum of 1000 individuals per square metre in Spain (Arenas and Fernández 2000). These are 97% and 67% lower than for R. okamurae, respectively, but this can be explained by species size differences. Density peaks of individuals were recorded in late summer and autumn, while biomass peaks were observed in late spring and summer. This pattern suggests a seasonal variation in the species’ invasiveness in P. oceanica meadows, with space occupation influenced either by the high influx of new recruits or the substantial biomass of larger adult individuals. A similar pattern in temporal fluctuation of invasive behaviour was observed in different invasive seaweeds, such as S. muticum, showing a population dynamic characterised by alternating periods dominated by either few large individuals or numerous small individuals (Arenas and Fernández 2000).

The lack of significant correlation between abiotic factors, density of individuals and biomass is useful for understanding the success and establishment of invasive species (Jehangir et al. 2024). This result suggests that R. okamurae can thrive under diverse physical-chemical conditions, tolerating a wide range of abiotic environmental factors, which enhances invasiveness (Alpert et al. 2000). A similar pattern was documented in A. taxiformis, which maintains a high productive succession of cohorts throughout the year, regardless of changing environmental conditions (Zanolla et al. 2019). During the study period, R. okamurae exhibited continuous recruitment, with peaks of young individuals observed in summer and autumn. Although the specific mechanisms involved were not detailed, the presence of propagules – diminute proliferous branches developed from cortical cells of the parent blade (Kajimura 1992) – was noticeable throughout the year, except in January (pers. obs.). This ability, coupled with its capacity for clonal multiplication through fragmentation (Rosas-Guerrero et al. 2020), facilitates ongoing recruitment regardless of abiotic factors. This mechanism not only adds to its continuous presence in the P. oceanica meadow, but also contributes to the release of new individuals into the water column. These unattached thalli can be detected at a depth of 1141 metres, where they remain photosynthetically active after light exposure (Mateo-Ramírez et al. 2023). This agrees with the propagule pressure invasion hypothesis, which emphasises the continuous input of new individuals into an invaded area (Simberloff 2009).

The identification of six successive cohorts throughout the year revealed the specific ecological strategies of R. okamurae for maintaining its population in the introduced area. The presence of different cohorts under varying environmental conditions suggests distinct environmental requirements for each cohort, a trait shared with other invasive species, such as A. taxiformis (Zanolla et al. 2019) and U. pinnatifida (Schiel and Thompson 2012). The population’s prevalence is driven by constant recruitment and continuous generational succession. Most cohorts had a brief duration of about two months, except cohort IV, which lasted for six months. This finding suggests that the species is unable to complete the typical haplodiplontic digenetic life cycle exhibited in its native area, which usually spans more than two years and involves an annual alternation between gametophytic and sporophytic phases (Agatsuma et al. 2005). Although reproductive characterisation is still being processed, the continuous presence of propagules and monospores (pers. obs.) may indicate that the population is sustained primarily through asexual reproduction and vegetative multiplication, with sporophytes playing a key role in population maintenance. Furthermore, overlapping cohorts observed in some months allows for a continuous succession of individuals and sustained occupation of space resulting in high coverage throughout the year. This pattern, like that observed for U. pinnatifida in New Zealand, enhances the invasion success of the species and increases propagule pressure in invaded areas (Schiel and Thompson 2012; South et al. 2017). This continuous occupation can have more impact on the structure and function of the ecosystem than intermittent periods of high and low coverage (Schiel and Thompson 2012) and is likely to disrupt native species and alter ecosystem dynamics, contributing to its invasive potential.

The identified cohorts might be linked to the occurrence of the species’ morphotypes described in both native and introduced areas, characterised by variations in thallus thickness and width and the number of dichotomies (Sun et al. 2006; Salido and Altamirano 2020). These morphotypes appear to follow a seasonal pattern. For example, in introduced areas, the thick morphotype arises in winter and the thinner one in summer, alternating with the intermediate morphotype (Salido and Altamirano 2020). Therefore, cohort IV could align with the thicker morphotype, cohorts II and VI with the thinner morphotype and cohorts I, III and V with the intermediate morphotype. This potential association between morphotypes and cohorts provides valuable insights into the adaptability of the different morphotypes of R. okamurae in response to changing environmental conditions, which contributes to understanding the species’ dynamics in marine ecosystems. Although this study did not explore the relationship between morphotypes and abiotic factors, identifying the environmental drivers behind morphotype development would be essential for understanding the species’ invasion success and its impact on ecosystems. Theoretical frameworks exploring the connection between phenotypic plasticity and invasion success propose that invasive species could maintain high fitness across diverse environmental conditions owing to their physiological plasticity and can even thrive under unfavourable conditions (Richards et al. 2006; Gioria et al. 2023), which may explain the observed patterns in R. okamurae. Understanding this behaviour could deepen knowledge about the species’ invasiveness and the factors influencing morphotype succession throughout the year.

Overall, R. okamurae exhibited a notable ability to persist in the P. oceanica meadow despite fluctuating environmental conditions. Its capacity to endure under a wide range of abiotic factors highlights its invasiveness, which is facilitated through population dynamics. This invasiveness observed in this specific habitat is further enhanced by continuous recruitment and a succession of distinct cohorts. This study also reveals temporal windows of invasiveness for R. okamurae, driven by an intense density of new small-sized individuals during summer and early autumn, while late spring and summer are characterised by high biomass accumulation of larger-sized individuals. These findings contribute to a deeper understanding of the invasiveness of R. okamurae in the P. oceanica meadows through population dynamics, underscoring its ability to dominate space and persist in a variety of environmental conditions. Identifying these patterns offers crucial insights into the success of R. okamurae and can guide effective management strategies.

The authors thank to Gianluca Nania and the other volunteers for their support in the measurements of thalli. We further thank comments provided by reviewers.