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This study contributes to the understanding of the population dynamics of S. woodiana and its native counterparts during the early stages of invasion. It documents a self-sustaining population of S. woodiana in an area with cold and long winters and extends the known limits of its thermal tolerance. Comparison of demographic profiles shows a more favourable population structure in S. woodiana than in the native mussels, indicating possible future dominance shifts. This study also shows that S. woodiana is a habitat generalist concerning bottom sediments, and points to intentional introductions of adult individuals as an important and underappreciated route of dispersal of this invasive species.Thermal tolerance of S. woodiana
The introduction of Sinanodonta woodiana in 2000 resulted in a long-term establishment of its reproducing population, as evidenced by a high proportion of females carrying glochidia (17 out of 21 in 2018) and the presence of juveniles (the smallest individual of 33 mm shell-length was collected in 2019). While the populations of native mussels might have been augmented with glochidia attached to the stocking fishes, this was less likely in S. woodiana. The species was not recorded in the vicinity before13, and given the distance of over 500 km over which the founding individuals were transported, their local availability was unlikely. In any case, as the stocking fishes originated only from local sources, which did not include heated-water hatcheries, any S. woodiana glochidia would have also been from locally-adapted populations.Winters in the study area are relatively cold and long. In 2000–2019, the mean temperature of the coldest month was − 3.7 °C, and the lowest mean monthly temperature was − 10.8 °C. The absolute minimum temperature was − 31.1 °C. Ice formed each year, on average for 73 days, with a maximum of 104 days. As far as we know, these are the most extreme climatic conditions in which an established population of this species was documented to date. Sinanodonta woodiana has been reported from Sweden, but no reproduction was observed there30. The populations in the Yenisei and Ob River basins inhabit heated water effluents9,31. The other population in northern Poland in a thermally-unpolluted water body is in a milder climate24. Thus, our study extends the known limits of cold tolerance of S. woodiana, indicating a shift in its realized niche32 or an ongoing in situ adaptation11.Furthermore, with the ongoing climate change, the abiotic conditions in the invaded range of S. woodiana increasingly match its physiological optimum33. In our study area during the time since mussel introduction, the mean annual temperature increased by 0.8 °C, the number of days with ice formation decreased by 21, and the number of days with temperatures over 15 °C (coinciding with the production of ripe glochidia by S. woodiana15) increased by nine. Sinanodonta woodiana survives at water temperatures up to 38 °C34 and has a higher tolerance to thermal stress than the native mussels21. In heated water bodies it reproduces throughout the year18 and occupies habitats with higher temperature ranges than the native unionids14, indicating that climate warming will increase its competitive advantage. Additionally, high mobility of S. woodiana and its tendency to burrow deeply into the sediments may help it better survive during drought episodes.As shown in our study, in suboptimal thermal conditions, S. woodiana can persist at low abundances for decades. Outbreaks of such sleeper populations (sensu35) are likely to be triggered by changes in the environment, e.g., rising temperatures.Population structure of S. woodiana in relation to native unionidsOver four study years, the relative frequency of S. woodiana increased from 2 to 9%. A comparison of shell-length distributions, approximating population age-structure, shows that smaller-sized mussels contributed a higher proportion of individuals in S. woodiana than in the native mussels in all study years, and this difference was increasing over time. This increase over time was possibly related to the removal of S. woodiana individuals, as hand-sampling tends to be biased towards larger individuals. On the other hand, the high mobility of this species and its striking burrowing behaviour, which lowers its detectability, might have counterbalanced this effect, as illustrated by the largest S. woodiana individual, with a shell length of 22.5 cm, found in the last study year. Nevertheless, it is possible that without the removal of individuals, the size structure would also shift towards larger sizes in S. woodiana, and its relative abundance at the study sites would increase even faster. Interestingly, a higher contribution of smaller-sized individuals in S. woodiana than in the native mussels was also observed in24, where no mussels were removed before the study. Thus, in both these studies, S. woodiana not only established viable populations but also showed higher potential for population growth than the native mussels. This is not surprising given that S. woodiana grows faster, matures earlier and produces more glochidia per female than the native unionids17,18,19,36. At increasing relative frequencies, its direct effects on the native unionids: competition for food, bottom space and host fish, filtering out sperm and larvae, and transmission of diseases6 will play an increasing role, and a dominance shift can be expected. This, in turn, is expected to affect ecosystem functioning, including changes in water transparency and nutrient availability25,37, benthic habitat modification38,39, and reduction in the condition of fish40. Additionally, S. woodiana invasion threatens the endangered European bitterling Rhodeus amarus16, and its massive die-offs negatively impact water quality and reverberate to terrestrial ecosystems41,42.The increasing prevalence of S. woodiana in invaded areas17,23,43,44 supports its predicted ability to effectively compete with native mussels. Our present study shows that demographic profiles of co-occurring mussel populations can indicate future dominance shifts already at initial invasion stages. However, as in many alien species45,46, the time-lag between the establishment of S. woodiana and the expression of its impacts can last decades, explaining why, despite its striking body-size (“a football-sized invasive mussel”47), the threats from its invasion are largely underestimated.Tolerance of S. woodiana for bottom sediment typeDespite a large number of studies documenting the spread of S. woodiana (for a recent summary, see, e.g.,11,48), not much is known on its preferences concerning bottom sediments. Sinanodonta woodiana is mainly reported from ponds and reservoirs, which suggests its preference for muddy sediments. However, its presence in these habitats is related to its mode of dispersal rather than habitat preferences. Basing on a study in a heated lakes system with various habitats, Kraszewski and Zdanowski14 suggested a preference of S. woodiana for sandy bottom substrates. The patchy distribution of sandy and muddy bottom substrates allowed us to test this hypothesis in the present study.According to expectations, based on the known preferences of the native species49, A. cygnea occurred predominantly at sites with a muddy bottom, U. pictorum at sites with a sandy bottom, and A. anatina occurred at similar densities on both bottom types. Contrary to expectations, however, S. woodiana did not show a preference for either bottom type. Although its overall density was higher at sites with a sandy than a muddy bottom, this difference was not significant. Sinanodonta woodiana can utilize a broad range of host-fish species15,16,17 and survive in a broad range of water-body types13. Our study indicates that it is also a habitat generalist concerning bottom sediments and adds to the suit of the known tolerances of this species.Intentional human-mediated dispersalThe global spread of S. woodiana is primarily due to the trade in freshwater fish7,9. Our study points to intentional introductions for water filtration as an additional route of dispersal of this species. Large individual sizes and arguably beautiful colouration of S. woodiana add to its perceived attractiveness, and some people are willing to undertake considerable efforts to obtain individuals of this species. Occasional long-distance translocations can cause the bridgehead effect46,50, in which the establishment of populations in new locations facilitates the further dispersal of the species and leads to a self-accelerating invasion process. The way humans interact with invasive species is one of the main determinants of their spread and establishment51,52. Our local interviews indicate that individuals from the study pond have already been transferred to nearby water bodies, and their filtering ability is highly appreciated. The propensity of people to acquire and translocate Sinanodonta mussels has been noted before13,17,24,53,54,55 and is probably more important than previously appreciated.Management implicationsEradication of established invasive bivalve populations is extremely difficult6. An apparently successful attempt to eradicate S. woodiana from invaded fish ponds involved lowering the water level and poisoning the fish and mussels10,47, but usually such measures cannot be applied. An alternative is the removal of individuals by hand harvesting. To be effective, however, it should cover the whole surface of the invaded water body and be repeated regularly. A related, commonly used practice in field research on invasive species is to remove the collected individuals from the study area. Our study shows that at least in S. woodiana, this is not likely to have any practical effect. We took out all individuals collected during four annual surveys from collection sites covering approximately 8% of the surface area of the pond. The relative frequency of S. woodiana increased while its densities and shell-length distributions remained unchanged. This was not unexpected, given a small proportion of the population sampled, combined with the high reproduction rates and mobility of this species. As sampling rarely includes more than 10% of the studied populations, alternatively to removing individuals from a study area, long-term studies involving marking and releasing them back might be considered. Knowledge of the biology of S. woodiana in the wild (e.g., growth rates, longevity, behavioural responses) is scarce, limiting our ability to manage and reduce its further spread.The priority, however, is to prevent introductions of S. woodiana to non-invaded water bodies. Fish trade remains its dominant dispersal route, so effective biosecurity measures are necessary. Well-coordinated monitoring programmes are needed for evidence-based management decisions56. Public participation is key to successful management of invasive species. Publicly accessible educational programmes explaining the problems of invasive species and increasing the appreciation of the native ones are required, especially when the invasive species elicit favourable reactions from people51, as is the case with S. woodiana.Sinanodonta woodiana does not yet have the status of a recognized pest. For example, it is not included in the list of invasive alien species of European Union concern57 and there are no regulations concerning this species in most countries. Our study documents the potential of S. woodiana to demographically outcompete native unionids. Combined with its recognized impacts and rates of spread, it highlights the need to urgently call the attention of policymakers and the public to the threats posed by S. woodiana to the integrity of freshwater ecosystems. More

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Ecology of Yellowfoot limpetIn the Tropical Pacific, sympatric limpets (Cellana melanostoma, Cellana exarata, Cellana sandwicensis, Cellana talcosa) inhabit the Hawaiian rocky intertidal ecosystem, where they graze on crustose coralline algae (CCA) and epibenthic microorganisms. Distribution ranges from the splash zone (upper-intertidal) to subtidal zone, and across the entire Hawaiian Archipelago26. They are dispersed across the majority of seamounts, atolls, and islands, however, not all species are present in every rocky intertidal locality, which reflects species-specific micro-habitat preferences.The reproduction cycles for each species appears to vary in time and space, and on-going long-term monitoring efforts are in progress to define this critical life-history trait. Previous studies on the yellowfoot limpet C. sandwicensis, reveal that reproduction is highly synchronized from December to March27,29. Gametogenesis also occurs from June to August, however, the level synchronicity and intensity of this second spawn period are inconsistent.These limpets are gonochoristic and considered to be sequential hermaphrodites44. The sex ratio is near 1:1(M:F) during spawning season, however, we have directly observed populations to maintain disproportionate sex ratios.Development of this broad-cast spawning limpet has been described from egg to post-larvae, where settlement occurs in less than 4 days post-fertilization29. This short larval duration ensures recruitment to the same localized intertidal environment, and reduces likelihood of hybridization between sympatric species with similar life-histories26.For wild limpets, growth rates shift through ontogeny—average monthly growth decreasing from 4–5 mm shell length (SL) as juveniles to 2–3 mm SL as adults27. Limpets also exhibit seasonal growth patterns—influenced by temperature and feeding28,37. Currently, growth rates of large individuals ( >50 mm SL) and species longevity are absent in the literature.Regional climate and coastal oceanographyKa’alawai is located on the south-facing shoreline of Oahu Island, Hawai’i (21°15’20.7“N 157°47’30.8“W). This area, defined as a rocky intertidal zone, is primarily comprised of basalt outcrops, boulders and benches, and supports a diverse community of epibenthic flora and fauna. The area is relatively easy to access by foot, and has been continuously exposed to various anthropogenic factors, which includes development, urban run-off, and subsistence fishing.The microclimate of the region is characterized by mild, wet winters (January to March) and dry, hot summers (July to September). The mean daily atmospheric temperature range and mean daily sea-surface temperature range are 18.44–31.38 °C and 22.67–30.18 °C, respectively. The annual precipitation is low relative to windward sides of the island, with maximum rainfall of 6.35 cm (data sources: US climate station USC00519397: Waikiki 717.2; PacIOOS Nearshore Sensor 04 (NS04): Waikiki Aquarium). Although freshwater input from precipitation along this coastline is considered to be marginal, the mixing of submarine groundwater discharge generates a unique geochemical profile for surface seawater at Ka’alawai. In particular, the mean surface salinity for this study site has been reported to be 25.4 ‰, which reflects this highly localized land-sea interaction45.The coastal oceanography of this region is predominantly influenced by wave, wind, and tidal forces. The south-shore region experiences a mixed tidal cycle—having both diurnal and semi-diurnal sinusoidal constituents per lunar day—with a tidal range of 58 cm and 91 cm during neap tide and spring tide, respectively; The trade winds from north-easterly direction (between 22.5°–67.5°) account for ~63% of the year with mean annual intensity around 5 m/s;46 and South swells with wave amplitudes of ~3 m are generated by storms in the Tasmanian Sea during Northern Hemisphere Summer47,48.Modern and historical specimensOn June 28th of 2018, live Yellowfoot limpet (Cellana sandwicensis) specimens CW1 and CW2 were collected from the rocky intertidal zone at Ka’alawai, Oahu, Hawai’i (Fig. 7). The animals were immediately sacrificed/dissected using scalpel blade, and measured for shell dimensions using a caliper. Limpets were weighed to determine gonadosomatic index, and gonads were preserved for histological examination. Shells were rinsed in an ultrasonic bath and air-dried.Fig. 7: Study site map.Hawaiian limpet specimens (Cellana sandwicensis) were collected along the rocky intertidal shoreline of Ka’alawai (Oahu, Hawaii). Instrumental sea-surface temperatures were measured in-situ by PacIOOS Nearshore Sensor 04 (NS04) at the Waikiki Aquarium.Full size imageA historical specimen BPBM (identification number 250851-200492) was loaned from the Bernice Pauahi Bishop Museum Malacology Department Collection. This specimen’s geographical and ecological origin is unknown, but was identified as C. sandwicensis by its characteristic shell morphology49. This specimen was selected for its large size to estimate life-expectancy of this limpet species, as well as to evaluate this method for paleoclimatology studies.Permission was not required to obtain specimens used in this study, and limpets were collected at a size exceeds the legal minimum shell length of 31.8 mm (Hawaii State Law is enforced by Department of Land and Natural Resources). Ethical approval was not required to conduct analysis.Characterization of shell microstructureShell microstructure was identified before isotopic analysis could be attempted. Each shell was cross-sectioned from anterior to posterior direction using a low speed saw (Isomet 1000, Buehler) equipped with a 0.5 mm diamond coated blade. Parallel cuts were made at the apex or maximal growth-axis to obtain two replicate 1.3 mm thick-sections per specimen. The first replicate thick-sections, prepared for micro-sampling, were further cut into More

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