Multiscale stability of an intertidal kelp (Postelsia palmaeformis) near its northern range edge through a period of prolonged heatwaves.

BACKGROUND AND AIMS: Climate change, including gradual changes and extreme weather events, is driving widespread species losses and range shifts. These climatic changes are felt acutely in intertidal ecosystems, where many organisms live close to their thermal limits and experience the extremes of both marine and terrestrial environments. A recent series of multiyear heatwaves in the northeast Pacific Ocean might have impacted species even towards their cooler, northern range edges. Among them, the high intertidal kelp Postelsia palmaeformis has traits that could make it particularly vulnerable to climate change, but it is critically understudied. METHODS: In 2021 and 2022, we replicated in situ and aerial P. palmaeformis surveys that were conducted originally in 2006 and 2007, in order to assess the state of northern populations following recent heatwaves. Changes in P. palmaeformis distribution, extent, density and morphometrics were assessed between these two time points over three spatial scales, ranging from 250 m grid cells across the entire 167 km study region, to within grid cells and the individual patch. KEY RESULTS: We found evidence consistent with population stability at all three scales: P. palmaeformis remained present in all 250 m grid cells in the study region where it was previously found, and neither the extent within cells nor the patch density changed significantly between time points. However, there was evidence of slight distributional expansion, increased blade lengths and a shift to earlier reproductive timing. CONCLUSIONS: We suggest that apparent long-term stability of P. palmaeformis might be attributable to thermal buffering near its northern range edge and from the wave-exposed coastlines it inhabits, which may have decreased the impacts of heatwaves. Our results highlight the importance of multiscale assessments when examining changes within species and populations, in addition to the importance of dispersal capability and local conditions in regulating the responses of species to climate change.

Microclimate predicts kelp forest extinction in the face of direct and indirect marine heatwave effects.

Marine heatwaves threaten the persistence of kelp forests globally. However, the observed responses of kelp forests to these events have been highly variable on local scales. Here, we synthesize distribution data from an environmentally diverse region to examine spatial patterns of canopy kelp persistence through an unprecedented marine heatwave. We show that, although often overlooked, temperature variation occurring at fine spatial scales (i.e., a few kilometers or less) can be a critical driver of kelp forest persistence during these events. Specifically, though kelp forests nearly all persisted toward the cool outer coast, inshore areas were >3°C warmer at the surface and experienced extensive kelp loss. Although temperatures remained cool at depths below the thermocline, kelp persistence in these thermal refugia was strongly constrained by biotic interactions, specifically urchin populations that increased during the heatwave and drove transitions to urchin barrens in deeper rocky habitat. Urchins were, however, largely absent from mixed sand and cobble benthos, leading to an unexpected association between bottom substrate and kelp forest persistence at inshore sites with warm surface waters. Our findings demonstrate both that warm microclimates increase the risk of habitat loss during marine heatwaves and that biotic interactions modified by these events will modulate the capacity of cool microclimates to serve as thermal refugia.

Something Darwin didn't know about barnacles: spermcast mating in a common stalked species.

Most free-living barnacles are hermaphroditic, and eggs are presumed to be fertilized either by pseudo-copulation or self-fertilization. Although the common northeast Pacific intertidal gooseneck barnacle, Pollicipes polymerus, is believed only to cross-fertilize, some isolated individuals well outside penis range nonetheless bear fertilized eggs. They must therefore either self-fertilize or-contrary to all prior expectations about barnacle mating-obtain sperm from the water. To test these alternative hypotheses, we collected isolated individuals bearing egg masses, as well as isolated pairs where at least one parent carried egg masses. Using 16 single nucleotide polymorphism markers, we confirmed that a high percentage of eggs were fertilized with sperm captured from the water. Sperm capture occurred in 100 per cent of isolated individuals and, remarkably, even in 24 per cent of individuals that had an adjacent partner. Replicate subsamples of individual egg masses confirmed that eggs fertilized by captured sperm occurred throughout the egg mass. Sperm capture may therefore be a common supplement to pseudo-copulation in this species. These observations (i) overturn over a century of beliefs about what barnacles can (or cannot) do in terms of sperm transfer, (ii) raise doubts about prior claims of self-fertilization in barnacles, (iii) raise interesting questions about the capacity for sperm capture in other species (particularly those with short penises), and (iv) show, we believe for the first time, that spermcast mating can occur in an aquatic arthropod.

Modular phenotypic plasticity: divergent responses of barnacle penis and feeding leg form to variation in density and wave-exposure.

Traits can evolve both in response to direct selection and in response to indirect selection on other linked traits. Although the evolutionary significance of coupled traits (e.g., through shared components of developmental pathways, or through competition for shared developmental resources) is now well accepted, we know comparatively little about how developmental coupling may restrict the independent responses of two or more phenotypically plastic traits in response to conflicting environmental cues. Such studies are important because coupled development, if present, could act as an important limit to the evolution of functionally independent plasticity in multiple traits. I tested whether developmental coupling can restrict the direction of plastic responses by studying how penis form and leg form--both highly plastic traits of barnacles--varied in response to differences in conspecific density and water velocity. Penis length and leg length in Balanus glandula varied in parallel with variation in wave-exposure but varied in opposite directions with variation in conspecific density. This study represents one of the rare tests of developmental coupling between multiple (demonstrably adaptive) plastic traits: Barnacle legs and penises appear to exhibit modular development that can respond concurrently--yet in independent directions--to conflicting environmental cues.

Environmental heterogeneity mediates scale-dependent declines in kelp diversity on intertidal rocky shores.

Biodiversity loss is driven by interacting factors operating at different spatial scales. Yet, there remains uncertainty as to how fine-scale environmental conditions mediate biological responses to broad-scale stressors. We surveyed intertidal rocky shore kelp beds situated across a local gradient of wave action and evaluated changes in kelp diversity and abundance after more than two decades of broad scale stressors, most notably the 2013-2016 heat wave. Across all sites, species were less abundant on average in 2017 and 2018 than during 1993-1995 but changes in kelp diversity were dependent on wave exposure, with wave exposed habitats remaining stable and wave sheltered habitats experiencing near complete losses of kelp diversity. In this way, wave exposed sites have acted as refugia, maintaining regional kelp diversity despite widespread local declines. Fucoids, seagrasses and two stress-tolerant kelp species (Saccharina sessilis, Egregia menziesii) did not decline as observed in other kelps, and the invasive species Sargassum muticum increased significantly at wave sheltered sites. Long-term monitoring data from a centrally-located moderate site suggest that kelp communities were negatively impacted by the recent heatwave which may have driven observed losses throughout the region. Wave-sheltered shores, which saw the largest declines, are a very common habitat type in the Northeast Pacific and may be especially sensitive to losses in kelp diversity and abundance, with potential consequences for coastal productivity. Our findings highlight the importance of fine-scale environmental heterogeneity in mediating biological responses and demonstrate how incorporating differences between habitat patches can be essential to capturing scale-dependent biodiversity loss across the landscape.

Precisely proportioned: intertidal barnacles alter penis form to suit coastal wave action.

For their size, barnacles possess the longest penis of any animal (up to eight times their body length). However, as one of few sessile animals to copulate, they face a trade-off between reaching more mates and controlling ever-longer penises in turbulent flow. We observed that penises of an intertidal barnacle (Balanus glandula) from wave-exposed shores were shorter than, stouter than, and more than twice as massive for their length as, those from nearby protected bays. In addition, penis shape variation was tightly correlated with maximum velocity of breaking waves, and, on all shores, larger barnacles had disproportionately stouter penises. Finally, field experiments confirmed that most of this variation was due to phenotypic plasticity: barnacles transplanted to a wave-exposed outer coast produced dramatically shorter and wider penises than counterparts moved to a protected harbour. Owing to the probable trade-off between penis length and ability to function in flow, and owing to the ever-changing wave conditions on rocky shores, intertidal barnacles appear to have acquired the capacity to change the size and shape of their penises to suit local hydrodynamic conditions. This dramatic plasticity in genital form is a valuable reminder that factors other than the usual drivers of genital diversification--female choice, sexual conflict and male-male competition--can influence genital form.

Ecology and Evolution of Phenotypic Plasticity in the Penis and Cirri of Barnacles.

Most barnacles are sessile, simultaneous hermaphrodites that reproduce by copulation. This is achieved through the extension of a muscular penis, famous for being the proportionally largest in the animal kingdom. The penis is a long cylindrical or conical organ, composed of a series of folded rings, allowing it to stretch to great lengths. The penises are covered with chemosensory setae allowing them to seek out receptive neighbors. For many species, the condition of the penis changes seasonally. In the most extreme circumstances, it degenerates and is shed during the first post-mating molt and is re-grown for the next mating season. Barnacle penises have been shown to exhibit phenotypic plasticity in response to many different challenges. When exposed to heavy waves, diameter is increased by thickening both the cuticle and muscles. When mates are far, length increases by adding ringed annulations. Experiments have shown that these plastic traits are modular, capable of changing independently from each other and that they improve mating ability. Alternate strategies to increase reproductive ability by barnacles include the production of dwarf and complemental males, sperm casting and sperm leakage, and aerial copulation. All of these mating strategies may have important implications for the study of reproductive biology, life history, and sex allocation theory.

Interpopulational variation in the cold tolerance of a broadly distributed marine copepod.

Latitudinal trends in cold tolerance have been observed in many terrestrial ectotherms, but few studies have investigated interpopulational variation in the cold physiology of marine invertebrates. Here, the intertidal copepod Tigriopus californicus was used as a model system to study how local adaptation influences the cold tolerance of a broadly distributed marine crustacean. Among five populations spanning 18° in latitude, the following three metrics were used to compare cold tolerance: the temperature of chill-coma onset, the chill-coma recovery time and post-freezing recovery. In comparison to copepods from warmer southern latitudes, animals from northern populations exhibited lower chill-coma onset temperatures, shorter chill-coma recovery times and faster post-freezing recovery rates. Importantly, all three metrics showed a consistent latitudinal trend, suggesting that any single metric could be used equivalently in future studies investigating latitudinal variation in cold tolerance. Our results agree with previous studies showing that populations within a single species can display strong local adaptation to spatially varying climatic conditions. Thus, accounting for local adaptation in bioclimate models will be useful for understanding how broadly distributed species like T. californicus will respond to anthropogenic climate change.

Experimental evidence for latent developmental plasticity: intertidal whelks respond to a native but not an introduced predator.

Animals with highly inducible traits may show no inducible response when exposed to a related but wholly novel cue. This appears to be true for the intertidal whelk Nucella lamellosa faced with a voracious introduced predator. In the laboratory, we exposed whelks to effluent from two species of predatory crab, the native red rock crab Cancer productus and the invasive European green crab Carcinus maenas. Nucella and Cancer have a long shared history in the northeast Pacific, whereas potential interaction with Carcinus began here less than 10 years ago. Although Nucella responded adaptively to Cancer effluent by increasing shell thickness and decreasing somatic growth, there was no such response to Carcinus. Furthermore, thicker shelled Nucella were less likely to be eaten by Carcinus. Because Nucella produces thicker shells when exposed to Cancer cues, its ability to respond similarly to Carcinus depends only on the coupling of the Carcinus cue to the existing developmental pathways for adaptive changes in shell form. Such coupling of latent plasticity to a novel cue -- via genetic changes or associative learning -- could explain many cases of rapid phenotypic change following a sudden shift in the environment.