A Pleistocene legacy structures variation in modern seagrass ecosystems.

Distribution of Earth's biomes is structured by the match between climate and plant traits, which in turn shape associated communities and ecosystem processes and services. However, that climate-trait match can be disrupted by historical events, with lasting ecosystem impacts. As Earth's environment changes faster than at any time in human history, critical questions are whether and how organismal traits and ecosystems can adjust to altered conditions. We quantified the relative importance of current environmental forcing versus evolutionary history in shaping the growth form (stature and biomass) and associated community of eelgrass (Zostera marina), a widespread foundation plant of marine ecosystems along Northern Hemisphere coastlines, which experienced major shifts in distribution and genetic composition during the Pleistocene. We found that eelgrass stature and biomass retain a legacy of the Pleistocene colonization of the Atlantic from the ancestral Pacific range and of more recent within-basin bottlenecks and genetic differentiation. This evolutionary legacy in turn influences the biomass of associated algae and invertebrates that fuel coastal food webs, with effects comparable to or stronger than effects of current environmental forcing. Such historical lags in phenotypic acclimatization may constrain ecosystem adjustments to rapid anthropogenic climate change, thus altering predictions about the future functioning of ecosystems.

The biogeography of community assembly: latitude and predation drive variation in community trait distribution in a guild of epifaunal crustaceans.

While considerable evidence exists of biogeographic patterns in the intensity of species interactions, the influence of these patterns on variation in community structure is less clear. Studying how the distributions of traits in communities vary along global gradients can inform how variation in interactions and other factors contribute to the process of community assembly. Using a model selection approach on measures of trait dispersion in crustaceans associated with eelgrass (Zostera marina) spanning 30° of latitude in two oceans, we found that dispersion strongly increased with increasing predation and decreasing latitude. Ocean and epiphyte load appeared as secondary predictors; Pacific communities were more overdispersed while Atlantic communities were more clustered, and increasing epiphytes were associated with increased clustering. By examining how species interactions and environmental filters influence community structure across biogeographic regions, we demonstrate how both latitudinal variation in species interactions and historical contingency shape these responses. Community trait distributions have implications for ecosystem stability and functioning, and integrating large-scale observations of environmental filters, species interactions and traits can help us predict how communities may respond to environmental change.

Diel vertical movements and feeding behaviour of blue humphead parrotfish Scarus ovifrons in a temperate reef of Japan.

The feeding ecology of scarinine parrotfishes on tropical coral reefs has received considerable attention in the past few decades; nonetheless, relatively few studies have been conducted in high-latitude reefs. Among the Indo-Pacific Scarus species, Scarus ovifrons is unique, being largely restricted to the warm temperate waters of Japan. Nonetheless, there is very little information available on the feeding ecology of this species. In this study, the authors used acoustic telemetry to detect the diel vertical movement patterns of S. ovifrons, video survey to detect its feeding depths and substrata and focal follow survey and genetic analysis to identify algae composition on the feeding scars at Kashiwajima Island, southwestern Japan (32° 46' N, 132° 38' E). Acoustic telemetry revealed that S. ovifrons spent most of its time in shallow water (<10 m) during the day and slept in deeper water (10-15 m) at night. Video and focal follow surveys revealed that most fishes of various sizes regularly took bites on epilithic algae and detrital materials on rocky substrata at depths of <10 m, but large fishes (>40 cm total length) sometimes took bites directly on live corals (Acropora solitaryensis) at the 5 m depth zone where live tabular corals dominated the benthos. Molecular phylogenetic analyses revealed that epilithic algae collected from feeding scars were mainly composed of Rhodophyta, and coralline algae were less often targeted. Overall, this study revealed that S. ovifrons feeds mostly at depths <10 m, and the feeding algae substrata of the species are similar to those of tropical coral reef parrotfishes.

How do microbiota associated with an invasive seaweed vary across scales?

Communities are shaped by scale dependent processes. To study the diversity and variation of microbial communities across scales, the invasive and widespread seaweed Agarophyton vermiculophyllum presents a unique opportunity. We characterized pro- and eukaryotic communities associated with this holobiont across its known distribution range, which stretches over the northern hemisphere. Our data reveal that community composition and diversity in the holobiont vary at local but also larger geographic scales. While processes acting at the local scale (i.e., within population) are the main structuring drivers of associated microbial communities, changes in community composition also depend on processes acting at larger geographic scales. Interestingly, the largest analysed scale (i.e., native and non-native ranges) explained variation in the prevalence of predicted functional groups, which could suggest a functional shift in microbiota occurred over the course of the invasion process. While high variability in microbiota at the local scale supports A. vermiculophyllum to be a generalist host, we also identified a number of core taxa. These geographically independent holobiont members imply that cointroduction of specific microbiota may have additionally promoted the invasion process.

Latitude, temperature, and habitat complexity predict predation pressure in eelgrass beds across the Northern Hemisphere.

Latitudinal gradients in species interactions are widely cited as potential causes or consequences of global patterns of biodiversity. However, mechanistic studies documenting changes in interactions across broad geographic ranges are limited. We surveyed predation intensity on common prey (live amphipods and gastropods) in communities of eelgrass (Zostera marina) at 48 sites across its Northern Hemisphere range, encompassing over 37° of latitude and four continental coastlines. Predation on amphipods declined with latitude on all coasts but declined more strongly along western ocean margins where temperature gradients are steeper. Whereas in situ water temperature at the time of the experiments was uncorrelated with predation, mean annual temperature strongly positively predicted predation, suggesting a more complex mechanism than simply increased metabolic activity at the time of predation. This large-scale biogeographic pattern was modified by local habitat characteristics; predation declined with higher shoot density both among and within sites. Predation rates on gastropods, by contrast, were uniformly low and varied little among sites. The high replication and geographic extent of our study not only provides additional evidence to support biogeographic variation in predation intensity, but also insight into the mechanisms that relate temperature and biogeographic gradients in species interactions.

Biodiversity mediates top-down control in eelgrass ecosystems: a global comparative-experimental approach.

Nutrient pollution and reduced grazing each can stimulate algal blooms as shown by numerous experiments. But because experiments rarely incorporate natural variation in environmental factors and biodiversity, conditions determining the relative strength of bottom-up and top-down forcing remain unresolved. We factorially added nutrients and reduced grazing at 15 sites across the range of the marine foundation species eelgrass (Zostera marina) to quantify how top-down and bottom-up control interact with natural gradients in biodiversity and environmental forcing. Experiments confirmed modest top-down control of algae, whereas fertilisation had no general effect. Unexpectedly, grazer and algal biomass were better predicted by cross-site variation in grazer and eelgrass diversity than by global environmental gradients. Moreover, these large-scale patterns corresponded strikingly with prior small-scale experiments. Our results link global and local evidence that biodiversity and top-down control strongly influence functioning of threatened seagrass ecosystems, and suggest that biodiversity is comparably important to global change stressors.

The Kuroshio current influences genetic diversity and population genetic structure of a tropical seagrass, Enhalus acoroides.

Information on genetic diversity and differentiation of seagrass populations is essential for the conservation of coastal ecosystems. However, little is known about the seagrasses in the Indo-West Pacific Ocean, where the world's highest diversity of seagrasses occurs. The influence of sea currents on these populations is also unknown. We estimated the genetic diversity and population genetic structure and identified reproductive features in Enhalus acoroides populations from the Yaeyama Islands, Hainan Island and the Philippines. The Philippines are situated at the centre of the E. acoroides range, Yaeyama and Hainan are peripheral populations, and the Yaeyama population is at the northern limit of the species range. The powerful Kuroshio Current flows from the Philippines to Yaeyama. Genetic analyses using nine microsatellite markers indicated that reproduction of E. acoroides is mostly sexual. Clonal diversity does not decrease in northern populations, although genetic diversity does. However, the genetic diversity of the Yaeyama populations is greater than that of the Hainan populations. Significant genetic differentiation among most populations was evident; however, the Yaeyama and north-east Philippines populations were genetically similar, despite being separated by ~1100 km. An assignment test suggested that recruitment occurs from the north-east Philippines to Yaeyama. The strong current in this region is probably responsible for the extant genetic diversity and recruitment patterns.

Effects of spatial structure of population size on the population dynamics of barnacles across their elevational range.

Explanations for why population dynamics vary across the range of a species reflect two contrasting hypotheses: (i) temporal variability of populations is larger in the centre of the range compared to the margins because overcompensatory density dependence destabilizes population dynamics and (ii) population variability is larger near the margins, where populations are more susceptible to environmental fluctuations. In both of these hypotheses, positions within the range are assumed to affect population variability. In contrast, the fact that population variability is often related to mean population size implies that the spatial structure of the population size within the range of a species may also be a useful predictor of the spatial variation in temporal variability of population size over the range of the species. To explore how population temporal variability varies spatially and the underlying processes responsible for the spatial variation, we focused on the intertidal barnacle Chthamalus dalli and examined differences in its population dynamics along the tidal levels it inhabits. Changes in coverage of barnacle populations were monitored for 10.5 years at 25 plots spanning the elevational range of this species. Data were analysed by fitting a population dynamics model to estimate the effects of density-dependent and density-independent processes on population growth. We also examined the temporal mean-variance relationship of population size with parameters estimated from the population dynamics model. We found that the relative variability of populations tended to increase from the centre of the elevational range towards the margins because of an increase in the magnitude of stochastic fluctuations of growth rates. Thus, our results supported hypothesis (2). We also found that spatial variations in temporal population variability were well characterized by Taylor's power law, the relative population variability being inversely related to the mean population size. Results suggest that understanding the population dynamics of a species over its range may be facilitated by taking the spatial structure of population size into account as well as by considering changes in population processes as a function of position within the range of the species.

Dietary exposure experiments on the migration of chemical pollutants from microplastics to bivalves.

Plastics can contain two types of organic contaminants; absorbed from ambient water, and already contained as additives. To investigate the bioaccumulation of these substances, we conducted two types of exposure experiments using mussels and polyethylene microplastics with absorbed PCBs and containing four types of additives (BDE209, DBDPE, UV327 and UV234). After dietary exposure for 15 days, significantly higher concentrations of total PCBs, UV327 and UV234 were detected in the gonad of exposed groups than in the control groups, respectively. However, no significant differences in BDE209 or DBDPE levels were observed between the control and exposure groups. Although a higher transfer ratio was shown for PCB congeners with octanol-water partition coefficients (logKow) below 7, the ratio was lower for higher-hydrophobic PCBs with logKow above 7. This suggests that higher hydrophobic compounds (not only highly chlorinated PCBs, but also BDE209 and DBDPE) tend not to desorb or leach from plastics.

Ocean current patterns drive the worldwide colonization of eelgrass (Zostera marina).

Currents are unique drivers of oceanic phylogeography and thus determine the distribution of marine coastal species, along with past glaciations and sea-level changes. Here we reconstruct the worldwide colonization history of eelgrass (Zostera marina L.), the most widely distributed marine flowering plant or seagrass from its origin in the Northwest Pacific, based on nuclear and chloroplast genomes. We identified two divergent Pacific clades with evidence for admixture along the East Pacific coast. Two west-to-east (trans-Pacific) colonization events support the key role of the North Pacific Current. Time-calibrated nuclear and chloroplast phylogenies yielded concordant estimates of the arrival of Z. marina in the Atlantic through the Canadian Arctic, suggesting that eelgrass-based ecosystems, hotspots of biodiversity and carbon sequestration, have only been present there for ~243 ky (thousand years). Mediterranean populations were founded ~44 kya, while extant distributions along western and eastern Atlantic shores were founded at the end of the Last Glacial Maximum (~19 kya), with at least one major refuge being the North Carolina region. The recent colonization and five- to sevenfold lower genomic diversity of the Atlantic compared to the Pacific populations raises concern and opportunity about how Atlantic eelgrass might respond to rapidly warming coastal oceans.

Species level mapping of a seagrass bed using an unmanned aerial vehicle and deep learning technique.

Background: Seagrass beds are essential habitats in coastal ecosystems, providing valuable ecosystem services, but are threatened by various climate change and human activities. Seagrass monitoring by remote sensing have been conducted over past decades using satellite and aerial images, which have low resolution to analyze changes in the composition of different seagrass species in the meadows. Recently, unmanned aerial vehicles (UAVs) have allowed us to obtain much higher resolution images, which is promising in observing fine-scale changes in seagrass species composition. Furthermore, image processing techniques based on deep learning can be applied to the discrimination of seagrass species that were difficult based only on color variation. In this study, we conducted mapping of a multispecific seagrass bed in Saroma-ko Lagoon, Hokkaido, Japan, and compared the accuracy of the three discrimination methods of seagrass bed areas and species composition, i.e., pixel-based classification, object-based classification, and the application of deep neural network. Methods: We set five benthic classes, two seagrass species (Zostera marina and Z. japonica), brown and green macroalgae, and no vegetation for creating a benthic cover map. High-resolution images by UAV photography enabled us to produce a map at fine scales (<1 cm resolution). Results: The application of a deep neural network successfully classified the two seagrass species. The accuracy of seagrass bed classification was the highest (82%) when the deep neural network was applied. Conclusion: Our results highlighted that a combination of UAV mapping and deep learning could help monitor the spatial extent of seagrass beds and classify their species composition at very fine scales.

Spatial variation in diatom abundance and composition in Biwase Bay and Hamanaka Bay (Eastern Hokkaido, Japan), with reference to environmental features.

This study aims to examine the spatial variation of diatom abundance and composition along the nearshore areas of Biwase Bay and Hamanaka Bay, eastern Hokkaido. Terrestrial input via Kiritappu Wetland is expected to affect variation and composition differently depending on the position of the two bays. We conducted an oceanographic survey in June 2014 to measure seawater temperature, salinity, colored dissolved organic matter (CDOM) absorption, nutrient concentrations, and total and size-fractionated chlorophyll (Chl) a concentration at 11 stations of the shallowest (<5 m) parts of the bays. These were grouped into four areas (Areas 1 and 2 in Biwase Bay, and Areas 3 and 4 in Hamanaka Bay) based on the distance of the location from the wetland outlet (nearest in Area 1 to the farthest in Area 4). Diatoms are the major primary producers in the water column. Therefore, we also determined genus level cell abundance and diversity of diatoms to compare similarity among areas. Sea surface temperature was the lowest at Area 4, whereas sea surface salinity was the lowest at Area 1. The contribution of CDOM absorption, an indicator of wetland-influenced river discharge, and silica concentration was highest at Area 1. Total amount of nitrite and nitrate concentrations was the highest at Area 4. Total amount of Chl a concentration was also lowest in Area 1. Our size-fractionated Chl a results revealed that while the size composition of phytoplankton varied among areas, micro-sized (>10 µm) phytoplankton were predominant in Area 4. Finally, diatom composition at the genus level differed greatly among areas. Pennate diatoms were predominant in Areas 1 and 2, but centric diatoms dominated in Areas 3 and 4. Our results suggested great spatial variability in oceanographic conditions among areas, with less influence of wetland and more influence of Coastal Oyashio Water based on distance from the wetland outlet. Diatom composition showed geographical division between Biwase and Hamanaka Bays.

The significance of trophic transfer of microplastics in the accumulation of plastic additives in fish: An experimental study using brominated flame retardants and UV stabilizers.

Marine organisms ingest microplastics directly from water and indirectly from food sources. Ingesting microplastics can lead to the accumulation of plastic-derived chemicals. However, the relative contributions of the two exposure routes to the accumulation of plastic-derived chemicals in organisms are unknown. Using microplastics containing two brominated flame retardants (BFRs; BDE209 and DBDPE) and three UV stabilizers (UVSs; UV-234, UV-327, and BP-12), we performed exposure experiments to compare chemical accumulation patterns in fish (Myoxocephalus brandti) between exposure from water and prey (Neomysis spp.). We found significantly higher concentrations of BFRs in fish fed microplastic-contaminated prey than fish exposed to microplastics in the water. However, we observed similar concentrations of UVSs in fish exposed to both sources. As BFRs are more hydrophobic than UVSs, the differences may reflect the hydrophobic nature of the additives. Our findings indicate that both exposure routes are crucial to understanding the accumulation of plastic additives in fish.

Plastic and natural inorganic microparticles do not differ in their effects on adult mussels (Mytilidae) from different geographic regions.

Microplastics are ubiquitous in the marine environment and studies on their effects on benthic filter feeders at least partly revealed a negative influence. However, it is still unclear whether the effects of microplastics differ from those of natural suspended microparticles, which constitute a common stressor in many coastal environments. We present a series of experiments that compared the effects of six-week exposures of marine mussels to two types of natural particles (red clay and diatom shells) to two types of plastic particles (Polymethyl Methacrylate and Polyvinyl Chloride). Mussels of the family Mytilidae from temperate regions (Japan, Chile, Tasmania) through subtropical (Israel) to tropical environments (Cabo Verde) were exposed to concentrations of 1.5 mg/L, 15 mg/L and 150 mg/L of the respective microparticles. At the end of this period, we found significant effects of suspended particles on respiration rate, byssus production and condition index of the animals. There was no significant effect on clearance rate and survival. Surprisingly, we observed only small differences between the effects of the different types of particles, which suggests that the mussels were generally equally robust towards exposure to variable concentrations of suspended solids regardless of whether they were natural or plastic. We conclude, that microplastics and suspended solids elicit similar effects on the tested response variables, and that both types of microparticles mainly cause acute responses rather than more persistent carry-over effects.

Trophic transfer of microplastics from mysids to fish greatly exceeds direct ingestion from the water column.

Predators ingest microplastics directly from the environment and indirectly via trophic transfer, yet studies have not investigated the contribution of each pathway to microplastic ingestion in fish. We assessed the relative importance of the two exposure routes using mysids (Neomysis spp.) and a benthic fish (Myoxocephalus brandti) as a model prey-predator system. We first exposed the mysids to fluorescent polyethylene beads (27-32 µm) at concentrations of 200 and 2000 µg/L. We then exposed the fish to water containing the same concentrations of polyethylene beads or to nine mysids pre-exposed to polyethylene beads. We quantified the size and overall mass of polyethylene beads in mysids and in fish to assess polyethylene beads fragmentation by the mysids. Mysids ingested 2-3 more polyethylene beads from water containing the higher concentration, and fish ingested 3-11 times more polyethylene beads via trophic transfer than from the water column. The percentage of fragmented particles was higher in mysids and in fish fed bead-exposed mysids, suggesting that the mysids can fragment polyethylene beads. Our experiments demonstrate that trophic transfer is a major route of microplastic ingestion by fish and that prey such as mysids can fragment microplastics. Small particles can translocate from the digestive system into tissues and exert adverse physiological effects. Trophic transfer of microplastics may therefore pose more serious threats to organisms at higher trophic levels.

The gut retention time of microplastics in barnacle naupliar larvae from different climatic zones and marine habitats.

Microplastic ingestion has been widely documented in marine zooplankton, but the retention time of microplastics in their digestive gut are still poorly studied, especially among species from different climatic zones and marine habitats. This study evaluated the ingestion and gut retention time of four sizes of fluorescent microplastic beads (1.3, 7.3, 10.6, and 19.0 µm) in stage II naupliar larvae of nine barnacle species from different habitats (epibiotic on turtles, mangroves, coral reefs, and rocky shores) and climatic zones (subtropical/tropical and temperate). Microbeads were not lethal to all species (climatic zones/habitats) tested from the four sizes of non-fluorescent virgin microbeads (1.7, 6.8, 10.4 and 19.0 µm, each at concentrations 1, 10, 100, and 1000 beads mL-1). Gut retention time of microplastic beads in barnacle naupliar larvae significantly increased with decreasing size. Microbeads resided in digestive tracts generally 3-4 times longer in rocky shore and coral reef barnacles than in muddy shore and epibiotic ones. However, species from different climatic zone did not differ in retention time. Our results suggested nauplius larvae from rocky shore and coral reef barnacles appear to be more susceptible to the impacts of longer retained microplastics (e.g., toxic chemicals present on the surface).

Quantifying the dynamics of rocky intertidal sessile communities along the Pacific coast of Japan: implications for ecological resilience.

Long-term patterns in trajectories of natural communities provide insights into ecological resilience, but their assessment requires long-term census data. We analyzed 16-year census data for intertidal communities from 30 rocky shores along Japan's Pacific coast to assign community change to four possible trajectories (stable, reversible, abrupt, or linear) representing different aspects of ecological resilience, and to estimate multiple metrics of temporal invariability (species richness, species composition, and community abundance). We examined (1) how the prevalence of the four trajectories differs among regions, (2) how the features (model coefficients) of each trajectory vary among regions, and (3) how the temporal invariabilities differ among trajectories and regions. We found that the stable trajectory was the most common. Its features differed among regions, with a faster recovery to steady-state equilibrium in low-latitude regions. Furthermore, trajectories and temporal invariabilities both varied among regions, seemingly in association with the strength of ocean current fluctuations. Thus, the relationship between community temporal invariability and trajectory may be weak or absent, at least at the regional scale.

The role of host promiscuity in the invasion process of a seaweed holobiont.

Invasive species are co-introduced with microbiota from their native range and also interact with microbiota found in the novel environment to which they are introduced. Host flexibility toward microbiota, or host promiscuity, is an important trait underlying terrestrial plant invasions. To test whether host promiscuity may be important in macroalgal invasions, we experimentally simulated an invasion in a common garden setting, using the widespread invasive macroalga Agarophyton vermiculophyllum as a model invasive seaweed holobiont. After disturbing the microbiota of individuals from native and non-native populations with antibiotics, we monitored the microbial succession trajectories in the presence of a new source of microbes. Microbial communities were strongly impacted by the treatment and changed compositionally and in terms of diversity but recovered functionally by the end of the experiment in most respects. Beta-diversity in disturbed holobionts strongly decreased, indicating that different populations configure more similar -or more common- microbial communities when exposed to the same conditions. This decline in beta-diversity occurred not only more rapidly, but was also more pronounced in non-native populations, while individuals from native populations retained communities more similar to those observed in the field. This study demonstrates that microbial communities of non-native A. vermiculophyllum are more flexibly adjusted to the environment and suggests that an intraspecific increase in host promiscuity has promoted the invasion process of A. vermiculophyllum. This phenomenon may be important among invasive macroalgal holobionts in general.

Joint effects of patch edges and habitat degradation on faunal predation risk in a widespread marine foundation species.

Human activities degrade and fragment coastal marine habitats, reducing their structural complexity and making habitat edges a prevalent seascape feature. Though habitat edges frequently are implicated in reduced faunal survival and biodiversity, results of experiments on edge effects have been inconsistent, calling for a mechanistic approach to the study of edges that explicitly includes indirect and interactive effects of habitat alteration at multiple scales across biogeographic gradients. We used an experimental network spanning 17 eelgrass (Zostera marina) sites across the Atlantic and Pacific oceans and the Mediterranean Sea to determine (1) if eelgrass edges consistently increase faunal predation risk, (2) whether edge effects on predation risk are altered by habitat degradation (shoot thinning), and (3) whether variation in the strength of edge effects among sites can be explained by biogeographical variability in covarying eelgrass habitat features. Contrary to expectations, at most sites, predation risk for tethered crustaceans (crabs or shrimps) was lower along patch edges than in patch interiors, regardless of the extent of habitat degradation. However, the extent to which edges reduced predation risk, compared to the patch interior, was correlated with the extent to which edges supported higher eelgrass structural complexity and prey biomass compared to patch interiors. This suggests an indirect component to edge effects in which the impact of edge proximity on predation risk is mediated by the effect of edges on other key biotic factors. Our results suggest that studies on edge effects should consider structural characteristics of patch edges, which may vary geographically, and multiple ways that humans degrade habitats.

Seasonality in the strength and spatial scale of processes determining intertidal barnacle population growth.

1. Population growth rate is determined by both density-dependent and density-independent processes. In the temperate zone, the strength and spatial scale of these processes are likely to differ seasonally, but such differences have rarely been quantitatively examined. 2. Coverage, the area occupied by organisms, is a measure of resource use in sessile marine populations. Population models used for density-based studies should be able to characterize effectively fluctuations in coverage, but few have tried to apply such models to sessile populations. 3. We observed coverage of the intertidal barnacle Chthamalus challengeri at 20 plots on four shores along the Pacific coast of Japan over 8 years. We then fitted a population model that incorporated both a density-dependent process (strength of density dependence) and density-independent processes (intrinsic growth rate and stochastic fluctuation at different spatial scales) to these data to analyse the seasonal variation of these processes and answer the following two questions: (i) How do the effects of density-dependent and density-independent processes on population growth vary seasonally? (ii) At what spatial scale, regional (tens of kilometres), shore (hundreds of metres), or rock (tens of centimetres), does density-independent stochastic fluctuation most strongly affect population size changes? 4. Barnacle population size tended to decrease in summer, when population dynamics were characterized by a relatively lower intrinsic growth rate, weaker density dependence and stronger stochastic fluctuation. In contrast, population size tended to increase in winter, reflecting a higher intrinsic growth rate, strong density dependence and weak stochastic fluctuation. 5. In summer, population growth rate was strongly affected by regional-scale stochastic fluctuation, whereas in winter it was affected more by rock-scale stochastic fluctuation, suggesting that populations were strongly affected by regional-scale processes in summer but not in winter. 6. These results indicate that seasonally variable density-dependent and density-independent processes determine the population dynamics of C. challengeri. Therefore, to understand fluctuation patterns of populations of this species, seasonality should be taken into account. Moreover, this study demonstrates that population models commonly used for density-based studies are also applicable to coverage-based population studies.