Effects of Rock Type and Food Availability on Bioerosion by the Purple Sea Urchin, Strongylocentrotus purpuratus.

Purple sea urchins (Strongylocentrotus purpuratus) profoundly impact nearshore rocky coasts through their feeding habits. Their intense grazing sculpts substrates through bioerosion using their teeth and spines and controls the alternative stable state dynamic between kelp bed and urchin barrens. These states have contrasting food availability for sea urchins, with abundant food in kelp beds and scarce food in barren grounds. However, the relationship between food availability and bioerosion is unknown. We predicted that when kelp is available, it would ameliorate the action of teeth on the substrate. Our 11-weeks long, 2 × 2 factorial experiment, crossed community state (kelp present vs absent) and rock type (sandstone vs mudstone). We also quantified the contribution of spine abrasion to bioerosion on the two rock types. The bioerosion rates did not differ between treatments with and without kelp. Although there was no significant difference in net bioerosion between the rock types, there was a large difference between the proportion of bioerosion from teeth vs spine abrasion. Approximately a third of the sandstone bioerosion was from spines whereas less than 2% of mudstone bioerosion could be attributed to spines. As anticipated, growth of sea urchins fed kelp ad-libitum was higher than food-limited sea urchins. Surprisingly, sea urchins on mudstone (which has a higher organic component) grew faster than sea urchins on sandstone. Although bioerosion rates may not differ on a per-urchin basis between community states, the sea urchin population densities between kelp beds and urchin barrens likely causes a difference in net bioerosion between these communities. Our results point to the importance of lithology on the mechanics of sea urchin bioerosion. Differences in texture, grain size, and hardness of rock substrates undoubtedly contribute to bioerosion rates and dynamics.

Repeated Hyposalinity Pulses Immediately And Persistently Impair The Sea Urchin Adhesive System.

Climate change will increase the frequency and intensity of extreme climatic events (e.g., storms) that result in repeated pulses of hyposalinity in nearshore ecosystems. Sea urchins inhabit these ecosystems and are stenohaline (restricted to salinity levels ∼ 32 ‰), thus are particularly susceptible to hyposalinity events. As key benthic omnivores, sea urchins use hydrostatic adhesive tube feet for numerous functions, including attachment to and locomotion on the substratum as they graze for food. Hyposalinity severely impacts sea urchin locomotor and adhesive performance but several ecologically-relevant and climate change-related questions remain. First, does sea urchin locomotion and adhesion acclimate to repeated pulses of hyposalinity? Second, how do tube feet respond to tensile forces during single and repeated hyposalinity events? Third, do the negative effects of hyposalinity exposure persist following return to normal salinity levels? To answer these questions, we repeatedly exposed green sea urchins (Strongylocentrotus droebachiensis) to pulses of three different salinities (control: 32 ‰, moderate hyposalinity: 22 ‰, severe hyposalinity: 16 ‰) over the course of two months and measured locomotor performance, adhesive performance, and tube foot tensile behavior. We also measured these parameters 20 hours after sea urchins returned to normal salinity levels. We found no evidence that tube feet performance and properties acclimate to repeated pulses of hyposalinity, at least over the timescale examined in this study. In contrast, hyposalinity has severe consequences on locomotion, adhesion, and tube foot tensile behavior and these impacts are not limited to the hyposalinity exposure. Our results suggest both moderate and severe hyposalinity events have the potential to increase sea urchin dislodgment and reduce movement, which may impact sea urchin distribution and their role in marine communities.

Hyposalinity reduces coordination and adhesion of sea urchin tube feet.

Climate change will increase the frequency and intensity of low-salinity (hyposalinity) events in coastal marine habitats. Sea urchins are dominant herbivores in these habitats and are generally intolerant of salinity fluctuations. Their adhesive tube feet are essential for survival, effecting secure attachment and locomotion in high wave energy habitats, yet little is known about how hyposalinity impacts their function. We exposed green sea urchins (Strongylocentrotus droebachiensis) to salinities ranging from ambient (32‰) to severe (14‰) and assessed tube feet coordination (righting response, locomotion) and adhesion [disc tenacity (force per unit area)]. Righting response, locomotion and disc tenacity decreased in response to hyposalinity. Severe reductions in coordinated tube foot activities occurred at higher salinities than those that affected adhesion. The results of this study suggest moderate hyposalinities (24-28‰) have little effect on S. droebachiensis dislodgement risk and survival post-dislodgment, while severe hyposalinity (below 24‰) likely reduces movement and prevents recovery from dislodgment.

Plasticity in fluctuating hydrodynamic conditions: tube foot regeneration in sea urchins.

Regenerating structures critical for survival provide excellent model systems for the study of phenotypic plasticity. These body components must regenerate their morphology and functionality quickly while subjected to different environmental stressors. Sea urchins live in high-energy environments where hydrodynamic conditions pose significant challenges. Adhesive tube feet provide secure attachment to the substratum but can be amputated by predation and hydrodynamic forces. Tube feet display functional and morphological plasticity in response to environmental conditions, but regeneration to their pre-amputation status has not been achieved under quiescent laboratory settings. In this study, we assessed the effect of turbulent water movement, periodic emersion and quiescent conditions on the regeneration process of tube foot morphology (length, disc area) and functionality (maximum disc tenacity, stem breaking force). Disc area showed significant plasticity in response to the treatments; when exposed to emersion and turbulent water movement, disc area was larger than that of tube feet regenerated in quiescent conditions. However, no treatment stimulated regeneration to pre-amputation sizes. Tube foot length was unaffected by treatments and remained shorter than non-amputated tube feet. Stem breaking force for amputated and non-amputated treatments increased in all cases when compared with pre-amputation values. Maximum tenacity (force per unit area) was similar among tube feet subjected to simulated field conditions and amputation treatments. Our results suggest a role of active plasticity of tube foot functional morphology in response to field-like conditions and demonstrate the plastic response of invertebrates to laboratory conditions.

Homogenization and miniaturization of habitat structure in temperate marine forests.

Humans are rapidly transforming the structural configuration of the planet's ecosystems, but these changes and their ecological consequences remain poorly quantified in underwater habitats. Here, we show that the loss of forest-forming seaweeds and the rise of ground-covering 'turfs' across four continents consistently resulted in the miniaturization of underwater habitat structure, with seascapes converging towards flattened habitats with smaller habitable spaces. Globally, turf seascapes occupied a smaller architectural trait space and were structurally more similar across regions than marine forests, evidencing habitat homogenization. Surprisingly, such habitat convergence occurred despite turf seascapes consisting of vastly different species richness and with different taxa providing habitat architecture, as well as across disparate drivers of marine forest decline. Turf seascapes contained high sediment loads, with the miniaturization of habitat across 100s of km in mid-Western Australia resulting in reefs retaining an additional ~242 million tons of sediment (four orders of magnitude more than the sediments delivered fluvially annually). Together, this work demonstrates that the replacement of marine forests by turfs is a generalizable phenomenon that has profound consequences for the ecology of temperate reefs.

The effect of variable temperature, humidity, and substrate wettability on Gecko (Gekko gecko) locomotor performance and behavior.

Adhesive and locomotor performances of geckos are inherently linked by specialized morphological and biomechanical features. As such, we predict that conditions that lead to poor adhesive performance (i.e., low resistance to applied force while clinging) also lead to poor locomotor performance and behavior (i.e., slowed running speed, increased frequency and duration of stops, more failed or incomplete runs). In this study, we test the prediction that running speed changes as a function of adhesive performance in variable temperature (12 and 32°C), humidity (30, 55, 70, 80% relative humidity), and substrate wettability (hydrophilic glass, intermediately wetting plexiglass). We also expect other locomotor performance traits and behaviors, such as stopping and avoiding treatment conditions, to change as a function of adhesive performance. The results of this study do not fully support our prediction: gecko locomotor performance does not change as a function of humidity or substrate wettability, unlike adhesive performance. As an anticipated result of ectothermy, geckos run significantly slower and stop more frequently and longer at 12°C than 32°C. At high temperature, geckos required significantly more running attempts on hydrophilic glass than plexiglass to complete the experimental procedure, suggesting that this treatment condition is unfavorable. The results of this study highlight the robust locomotive response of geckos to variation in adhesive performance and environmental conditions, and have significant implications for predictions about habitat use and behavior in their natural environment.

Adhesive plasticity among populations of purple sea urchin (Strongylocentrotus purpuratus).

Sea urchins native to the nearshore open coast experience periods of high, repeated wave forces that can result in dislodgement. To remain attached while clinging and locomoting across rocky substrates, sea urchins use adhesive tube feet. Purple sea urchins (Strongylocentrotus purpuratus) adhere to a variety of rock substrates (e.g. sandstone, mudstone, granite), and display morphological plasticity (skeletal morphology) to native substrate. We tested the hypothesis that their adhesive system is also plastic and varies as a function of native population and substrate. The results of our study support our hypothesis. Sea urchins from sandstone adhere less strongly to most substrates than those native to mudstone and granite rock. Sandstone produced the lowest whole animal adhesive force values across all populations, suggesting that this rock type is particularly challenging for sea urchins to adhere to. The number of adhesive tube feet that failed during experimental trials and the area used by sea urchins to attach, matches closely with whole animal adhesive force values: higher forces resulted in more tube foot failure and larger attachment area. On artificial substrates (glass and Plexiglass), differences in adhesion among populations was consistent with differences in adhesion on rock substrates except on glass, where sea urchins native to sandstone adhered more strongly to glass than any other substrate tested. To our knowledge, this study is the first to describe population-level plasticity in a biological adhesive system related to native substrate, and has significant implications for sea urchin ecology, behavior and functional morphology.

Ecological feedbacks stabilize a turf-dominated ecosystem at the southern extent of kelp forests in the Northwest Atlantic.

Temperate marine ecosystems globally are undergoing regime shifts from dominance by habitat-forming kelps to dominance by opportunistic algal turfs. While the environmental drivers of shifts to turf are generally well-documented, the feedback mechanisms that stabilize novel turf-dominated ecosystems remain poorly resolved. Here, we document a decline of kelp Saccharina latissima between 1980 and 2018 at sites at the southernmost extent of kelp forests in the Northwest Atlantic and their replacement by algal turf. We examined the drivers of a shift to turf and feedback mechanisms that stabilize turf reefs. Kelp replacement by turf was linked to a significant multi-decadal increase in sea temperature above an upper thermal threshold for kelp survival. In the turf-dominated ecosystem, 45% of S. latissima were attached to algal turf rather than rocky substrate due to preemption of space. Turf-attached kelp required significantly (2 to 4 times) less force to detach from the substrate, with an attendant pattern of lower survival following 2 major wave events as compared to rock-attached kelp. Turf-attached kelp allocated a significantly greater percentage of their biomass to the anchoring structure (holdfast), with a consequent energetic trade-off of slower growth. The results indicate a shift in community dominance from kelp to turf driven by thermal stress and stabilized by ecological feedbacks of lower survival and slower growth of kelp recruited to turf.