Introduction
Life is not a beach for those animals that survive in the rough ecological conditions found in marine sandy beaches. Early beach ecologists categorized beaches amongst the harshest aquatic ecosystems on Earth (McLachlan et al., 1993), and even dubbed beaches asmarine deserts of sand and salt water (McLachlan, 1983). Beaches, as ecotones between the ocean and the land, indeed represent steep environmental gradients largely defined by exposure to tides and waves (Brown & McLachlan, 1990; Brazeiro, 2001). Temporally dynamic changes of waves and level of exposure on the one hand, and beach morphology on the other hand, affect each other, driving the morphodynamic evolution of a beach over cycles that might extend for long temporal scales, ultimately influenced by changes in regional climate, sea level, tidal regime, and long-term geological processes (McLachlan & Defeo, 2018). Beach morphodynamic stages range from dissipative—waves break far from the coast, favouring progressive profiles and flatter slopes—to reflective—waves directly reach the beach front producing short and steep slopes (Short and Wright, 1983; Short, 1996). Because energy is released progressively on dissipative beaches, environmental conditions are more benign in them, and become harsher as the reflective condition increases (McLachlan et al., 1993, 1995). As a result, the number of species, as well as density, abundance and biomass of fauna, increases from reflective beaches to dissipative beaches (McLachlan & Defeo, 2018). In addition, within each beach, the number of species is known to be lower in the wave-incidence zone (McLachlan et al., 1981, 1993, 1996, McLachlan 1990, Jaramillo et al., 1995), with a pattern that seems to be robust at global scale for large, macrofauna species (McLachlan & Dorvlo, 2005; Defeo & McLachlan, 2005). Such a pattern is considered to arise from the congruent but independent responses of different species living on the beach to the harsh physical environmental conditions of the wave-incidence zone of beaches (Noy-Meir, 1979; McLachlan, 1990).
Yet, sandy beaches might look deserted at the first glance because most of their biodiversity is represented by small meiobenthic organisms, which take advantage of the habitat available in the small spaces amongst the sand grains (McLachlan and Defeo, 2017). Meiofauna, defined as a heterogeneous group of small animals passing through a sieve of 0.5mm mesh (Giere, 2009), is a crucial component of beach ecosystems, not only in terms of number of species and abundances, but also because of its role in carbon cycling, sediment transportation, and interstitial water circulation (Schratzberger and Ingels, 2018). Therefore, in contrast to their minute size, the importance of meiofaunal organisms is larger than their size would suggest as meiofauna is involved in many processes directly linked to the ecosystem services that beaches provide to human societies (Harris and Defeo, 2022), mostly by shaping biogeochemical processes (Bonaglia et al. 2014, 2020; Bonaglia & Nascimento, 2023). Understanding the responses of meiofauna to different environmental stressors is then crucial not only from a theoretical perspective, but also to design strategies to preserve those services upon local and global anthropogenic perturbations (Defeo et al., 2021). And here things get interesting, because in contrast to macrofauna, meiofaunal organisms exhibit a wider range of responses to beach environmental parameters (Moens et al., 2013; Venekey et al. 2014; Maria et al. 2018), with some species even preferring areas of strong hydrodynamic disturbance. Counterintuitively, meiofauna, in contrast to macrofauna, is generally more diverse and abundant in reflective than in dissipative beaches (Gheskiere et al. 2005, McLachlan et al., 2018). In reflective beaches, there are even species that prefer the hydrodynamic turmoil of the reflective wave-incidence zone than deeper and far less agitated subtidal areas (Di Domenico et al., 2009; 2013). Problematically, incongruent species-specific responses across many meiofaunal groups may hamper any attempt to identify changes in taxonomic diversity patterns across beaches or beach levels, thereby masking the overall effect of stressors on beach meiofaunal communities, even if, for example, hydrodynamical gradients might exert ecological filtering on meiofauna similarly to what is known to occur on macrofaunal species (e.g. Albuquerque et al., 2007; Moreno et al., 2006; Sevastou et al., 2011). These difficulties in understanding meiofaunal responses to stress are increased by the lack of trained taxonomist as well as the large number of undescribed species and the conserved morphology that many meiofaunal lineages exhibit (Jörger & Schrödl, 2013; Fontaneto et al., 2015). Altogether, the role of environmental stressors on beach communities might be better characterized using functional metrics, which attempt to identify and quantify the traits that explain each species differential response across levels, in addition to and/or regardless of the species identity (Martínez, García-Gómez et al., 2021).
A quick browse over the pictures and drawings in any specialized identification guide (Schmidt-Rhaesa, 2022) immediately highlights that taxonomical diversity metrics might only capture a small part of the diversity of meiofauna. Meiofaunal species, far from representing a bunch of small worm-like creatures, exhibit a remarkable diversity of shapes, sensory structures, reproductive organs, and swimming capabilities, even within a single family or genus. Descriptions of different species-specific adaptations to interstitial life style in meiofauna populate the specialized zoological literature (Martínez et al., 2013; 2015, Polte & Schmidt-Rhaesa 2011, Herranz et al., 2019, 2021, Jörger et al., 2009); sometimes experimentally proved in model species (Armonies 1988, Boaden, 1963, 1968). What remains to be quantified is how the frequency of different traits might affect the ecological response of meiofaunal communities across beach hydrodynamic gradients. This is challenging, not only because very different structures might perform the same function across meiofaunal phyla, but also because many meiofaunal groups need to be studied alive, making any multi-taxon study across a large geographical area very complicated (Leasi et al., 2018, Martínez, Eckert et al., 2020). These problems can be alleviated by targeting a model group of organisms with enough taxonomic and functional diversity, focusing on a habitat that maximize hydrodynamic gradient but reduces other confounding environmental factors.
Our goal here is to quantify the response of meiofauna to beach hydrodynamic gradients, using communities of proseriate flatworms in 116 Western Mediterranean reflective beaches. Proseriate flatworms exhibit a remarkable diversity in beaches in terms of number of species as well as morphological and behavioural characters, some of which have been proposed as functionally important to cope with turbulence and hydrological stress (Reise, 1988). Even before the first studies on beach morphodynamics (Wright and Short, 1982), the upper, swash level of reflective beaches was known as “Otoplanen -zone”, due to the abundance of proseriates, and particularly Otoplana species, which dominates the swash level of Atlantic-Mediterranean beaches (Gerlach, 1953; Ax, 1956). We here focused on reflective beaches, so we can establish a comparable zonation across all sampled beaches, avoiding the confounding factors introduced by different hydrodynamic stages due to reefs, barriers, or progressive slopes. By selecting the Western Mediterranean Sea, we not only delineate a common pool of species for the study, but we also avoid the confounding effect introduced by ample tidal fluctuations of beaches on open oceans. Our overall hypothesis is that species responses to hydrodynamics depend on the presence of certain traits, with the main rationale included in the four alternative scenarios, depending on whether the environmental condition of the swash zone affects species richness or not; whereas it selects for specific combination of species traits (Figure 1). In order to select amongst these four scenarios, we first investigate the drivers for species richness, specifically testing whether the number of species differs across beach levels. Then, we explore the drivers for species composition, focusing on whether species composition across beach levels depends on species traits. Third, we compare the properties of the functional space of each beach level, under the assumption that the swash zone exhibits a lower functional richness and higher species functional contributions than the shoaling and subtidal levels. Finally, we aim to explain these overall differences by the presence of a higher frequency of traits related to hydrodynamics in the species in the swash level.