Mussel attachment strength
There is apparent contradiction in the outcomes of global and local comparisons of mussel attachment strength across rock types. Mussels showed stronger attachment in orthoquartzite than loess when measurements are globally averaged across sites (see Fig. 2a). However, mussel attachment strength did not differ across rock types at sites where orthoquartzite and loess co-occur (i.e., local comparisons; see Fig. 3). Here we argue that local comparisons provide a reliable test of rock type effects on mussel attachment, as they were conducted within a restricted spatial extent at each site (10 m radius; see “Methods” section) which allowed keeping to a minimum any variation in factors other than rock type. Therefore, we conclude that variations in mussel attachment strength across our entire study range (see Fig. 2b) are unrelated to rock type. Meanwhile, the observed interaction between site and sampling date (see Table 3) suggests that temporal variation in attachment strength is not spatially synchronized, possibly due to site-specific variations in environmental factors and/or mussel physiological status—e.g., asynchrony in mussel reproductive condition, which may affect the allocation of energy to byssus production [8].
Since mussel attachment strength does not vary with rock type at the local scale (i.e., where variations in factors other than rock type is likely minimum), global variations in mussel attachment strength with rock type across natural platforms should be attributed to confounding influences of co-varying factors. Wave exposure is perhaps the most obvious, potentially confounding variable in this study system. Indeed, mussels attach more strongly at sites with stronger wave action [32, 38], meanwhile wave exposure also positively co-varies with the hardness of natural rocky substrates [4]. While we did not quantify wave exposure in this study, orthoquartzite sites are distributed along headlands (see Fig. 1), show relatively steep slopes (Table 1) and, thus, are expected to receive more wave energy—e.g., through wave refraction and convergence [39]—than straight and gently sloping loess shorelines (this is also apparent from our casual observations of relative wave splash across the study sites). Increased wave exposure could account for stronger mussel attachment in natural orthoquartzite sites, mostly if we consider that mussels can adjust their attachment strength to increased wave action by increasing byssus production [3, 8, 16, 17]. Other potentially confounding factors leading to increased attachment strength in orthoquartzite sites include reduced desiccation stress (orthoquartzite sites are more likely to remain splashed-out by waves during low tide; pers. obs.) and higher food quality (suspended particles may include a larger proportion of sediments at loess sites due to soft cliff erosion) [39], both of which might allow allocating a larger amount of energy to byssus production.
Byssal thread counts and failure locations
Similar attachment strength to loess and orthoquartzite at the local scale might either be due to (a) dislodgement primarily occurring via byssus failure (in which case rock type would be irrelevant for dislodgment) or, (b) mussels showing compensatory mechanisms to reduce their probability of dislodgement from friable substrates. Our data do not support the first alternative. Here we observed that the dislodgement of individual mussels from either rock type results from a combination of byssus and substrate failures. Since byssal thread failure comprises just ca. 30% of all failures per individual in either rock type (see Fig. 4c), it is insufficient to explain lack of variation in mussel attachment strength among rock types.
Our results rather suggest that mussels increase byssus production to compensate for increased potential of substrate failure when attaching to soft, friable rock. In agreement, mussels from loess showed more byssal threads, but a similar attachment strength than those from orthoquartzite (see Fig. 4a, b). Again, mussels from each rock type were sampled here from the same site and within a restricted radius (< 10 m; see “Methods” section), which suggests that differences in byssal thread numbers are unlikely driven by factors other than rock type. In conjunction, these findings are in line with early predictions made by Bell and Gosline [3], who argued that by producing more byssal threads, mussels would increase the area of substrate that is sampled by the byssus and, thus, the probability of encountering stable pieces of substrate in friable rock. Although similar considerations may apply to byssal thread thickness (i.e., more area sampled by thicker threads; see [3]), mussels from friable and hard rock here did not differ in this regard.
The larger proportion (and number) of rock failures observed in mussels from loess than orthoquartzite suggests that, in the absence of increased thread production, the potential for substrate failure and dislodgement should be higher for mussels attaching to soft, friable loess. This gives additional support to early claims from Bell and Gosline [3] on the ability of mussels to increase thread production to counteract substrate failure and reduce their risk of dislodgement from friable rock.
Ecomechanical considerations
While the above findings suggest that rock type does not affect the potential for mussel dislodgement, it still remains to be evaluated if the observed values of mussel attachment strength can indeed be conducive to dislodgement. This can be explored by comparing mussel attachment strength against the forces acting on mussels at realistic flow velocities. Mussels occurring in beds are typically shielded by their neighbors from the drag and accelerational forces acting in the direction of water flow [3, 40]. Thus, they can be assumed to be dislodged only by the lift force (Flift). Lift acts perpendicular to the flow and results from differences in pressure due to a higher flow velocity above the mussel bed than in its interstices [40]. Lift is related to the square of flow velocity (U) and animal planform area (A) as follows:
$$ F_{\text{lift}} = \left(\rho U^{2} AC_{l}\right )/2 $$
where ρ is the density of sea water (1024 kg m−3) and Cl is the dimensionless coefficient of lift. (Cl = 0.88 for bed mussels, which are generally oriented with its long axis perpendicular to the substrate; see [3, 40]).
Figure 5 shows the theoretical lift forces acting on mussels 15–20 mm length (the range of mussel sizes in this study) at selected flow velocities (3, 6, 9, 12 m s−1; see Additional file 4 for details on lift calculations). Here, critical flow velocities for mussel dislodgement are those leading to a lift force equivalent to mussel attachment strength (i.e., flow will dislodge mussels when imposing on them a lift force that exceeds their attachment strength). Thus, from the lift necessary to dislodge mussels at the sites where they showed weakest and strongest attachment (i.e., Copacabana and Punta Iglesia respectively, May 2015; see Fig. 2b) we can predict that critical flow velocities are in the range of 3–12 m s−1 across our study area (i.e., compare expected lift curves against attachment strength data shown as white and gray diamonds in Fig. 5). These critical flow velocities are either comparable or lower than those occurring at wave-swept rocky shores (i.e., up to 25 m s−1, typically less than 12 m s−1; see [41,42,43,44]) as well as to maximum flow velocities registered at one of these sites (Copacabana) using spring dynamometers (up to 12.65 m s−1 between April 25 and May 26, 2018; authors’ unpublished data, see [42] for methods).
From the overlap in the range of critical and observed flow velocities, we can conclude that the values of mussel attachment strength registered here do not warrant resistance to dislodgement. Yet, the rates of mussel dislodgement at our study sites are certainly less than these numbers suggest. Indeed, from the above estimates alone it could be inferred that flow velocities equal or larger than 6 m s−1, which regularly occur in our study area and wave-swept rocky shores in general, would virtually extirpate mussels from sites where the mussel attachment strength is relatively weak (< 3 N; see Fig. 5). Clearly, this is not the case here as we have observed persistent mussel cover over the past several years across all our study sites, including those where mussel mussel attachment was weaker (e.g., Copacabana, Las Brusquitas, Frente Mar, Atlántida; see Fig. 2b). Rates of mussel dislodgement lower than the expected based on lift and critical flow estimates have also been reported in a previous study [40]. Here we postulate that this mismatch could be due to the afore-mentioned ability of mussels to adjust their attachment strength to increased hydrodynamic forcing via enhanced byssal thread production [3, 8, 16, 17]. As these responses to flow can be immediate [see 16, 40, 45], then measurements conducted during low tide and weather conditions benign enough for field work may underestimate the strength of mussel attachment at the time when wave action becomes more stringent.
Implications for habitat stability and function
Brachidontes rodriguezii [see 19,20,21] and bed-forming mussels in general [see 46,47,48 for reviews] are widely recognized as ecosystem engineers that generate physical habitat to a variety of other organisms. From the fact that B. rodriguezii attaches to a similar strength in hard and friable substrates within a given locale, we can conclude that substrate hardness and friability per se will not influence the structure and dynamics of the habitat that this species generates. Since mussel-associated organisms are largely influenced by the dynamics of mussel patch formation and decay [49, 50], we can also predict that local dynamics in our mussel bed communities would be independent of the nature and friability of the basal substrate. Yet, this does not mean that human-introduced orthoquartzite blocks and natural loess outcrops would have similar habitat function. Clearly, the attachment of sessile organisms outside from mussel patches may still be affected by rock type. Moreover, it is also well known that orthoquartzite hardness prevents the establishment of the various endolithic invertebrates that inhabit loess platforms [51].
Lastly, it becomes clear from our local comparisons that the softness and friability of loess relative to orthoquartzite does not limit B. rodriguezii attachment and colonization. Again, this is also evident from the ability of mussels to form persistent beds both in orthoquartzite and loess [19,20,21]. Relatively stable and continuous mussel cover may armor loess against mechanical impacts while potentially insulating it from extreme heat flows. This implies that mussels could reduce the impact of wave forces and abrasion on intertidal loess, while also playing indirect “bioprotective” roles [52] via influences on microclimate that limit weathering—e.g., reduced fluctuations in rock temperature and moisture [53]. If this is the case, the ability of mussels to attach and form relatively stable cover on otherwise erodible rock might have important large-scale implications for coastal geomorphology and evolution, and for the persistence of intertidal loess habitats as a whole.