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Membranipora membranacea. (A) Heavily encrusted thallus of Laminaria digitata with M. membranacea completely covering the meristem and greatly eroded blades. (B) Residual stipes of Saccharina longicruris after complete loss of blades following a major bryozoan outbreak. Photographs by R. E. Scheibling
Source publication
We used underwater videography to examine seasonal and interannual patterns in the cover (on kelp) of the encrusting epiphytic bryo- zoan Membranipora membranacea, and associated changes in the structure and abundance of native kelp (Saccharina longicruris) populations, at 2 sites on the Atlantic coast of Nova Scotia and over 4 to 11 yr since initi...
Similar publications
Despite the significance of marine habitat-forming organisms, little is known about their large-scale distribution and abundance in deeper waters, where they are difficult to access. Such information is necessary to develop sound conservation and management strategies. Kelps are main habitat-formers in temperate reefs worldwide; however, these habi...
Citations
... When kelp gametophytes experience unusually warm conditions, their sporophyte offspring-generally recruiting in the winter and early spring-are less abundant, grow more slowly, harbor fewer nutrients, and display higher sensitivities to heat stress (Gauci et al., 2022;Liesner et al., 2020). Finally, warming can also facilitate the introduction of novel species that increase adult kelp mortality (Scheibling & Gagnon, 2009) and/or inhibit recruitment (Wernberg et al., 2016); ourselves and others (Dijkstra et al., 2017) have identified the proliferation of filamentous red "turf algae" across the southwest (Figure 9). It is possible that F I G U R E 8 Percent cover of each kelp species (subregional mean ± 95% CI) in 2004 versus 2018. ...
Ecological theory predicts that kelp forests structured by trophic cascades should experience recovery and persistence of their foundation species when herbivores become rare. Yet, climate change may be altering the outcomes of top‐down forcing in kelp forests, especially those located in regions that have rapidly warmed in recent decades, such as the Gulf of Maine. Here, using data collected annually from 30+ sites spanning >350 km of coastline, we explored the dynamics of Maine's kelp forests in the ~20 years after a fishery‐induced elimination of sea urchin herbivores. Although forests (Saccharina latissima and Laminaria digitata) had broadly returned to Maine in the late 20th century, we found that forests in northeast Maine have since experienced slow but significant declines in kelp, and forest persistence in the northeast was juxtaposed by a rapid, widespread collapse in the southwest. Forests collapsed in the southwest apparently because ocean warming has—directly and indirectly—made this area inhospitable to kelp. Indeed, when modeling drivers of change using causal techniques from econometrics, we discovered that unusually high summer seawater temperatures the year prior, unusually high spring seawater temperatures, and high sea urchin densities each negatively impacted kelp abundance. Furthermore, the relative power and absolute impact of these drivers varied geographically. Our findings reveal that ocean warming is redefining the outcomes of top‐down forcing in this system, whereby herbivore removal no longer predictably leads to a sustained dominance of foundational kelps but instead has led to a waning dominance (northeast) or the rise of a novel phase state defined by “turf” algae (southwest). Such findings indicate that limiting climate change and managing for low herbivore abundances will be essential for preventing further loss of the vast forests that still exist in northeast Maine. They also more broadly highlight that climate change is “rewriting the rules” of nature, and thus that ecological theory and practice must be revised to account for shifting species and processes.
... pyrifera (Yoshioka, 1982b;Arkema and Samhourri, 2019) and on the Atlantic coast as an invader that damages kelps (Scheibling and Gagnon, 2009;Caines and Gagnon, 2012;Filbee-Dexter et al., 2016;Pratt et al., 2022). Recruitment to the benthic population depends on the supply of metamorphically competent larvae (Yoshioka, 1982b;. ...
... Disease outbreaks in sea urchin populations increased in frequency and intensity during the early 2000s, leading to concurrent mass mortalities over multiple subsequent years and ultimately a decline in sea urchin populations in shallow water (Feehan and Scheibling, 2014). Since the decline of sea urchins, spatial and temporal variability in kelp abundances have largely been attributed to interactions between ocean warming and invasive species (Scheibling and Gagnon, 2009;Watanabe et al., 2010;Filbee-Dexter et al., 2016). Surveys conducted by Watanabe et al. (2010) showed that kelp was common in high abundances coast-wide in 2007, and that recovery of kelps had occurred between 2000 and 2007 following invasion-mediated declines in the early 2000s and a loss of sea urchins (Watanabe et al., 2010). ...
Background and Aims
Changes in kelp abundances on regional scales have been highly variable over the past half-century owing to strong effects of local and regional drivers. Here, we assess patterns and dominant environmental variables causing spatial and interspecific variability in kelp persistence and resilience to change in Nova Scotia over the past 40 years.
Methods
We conduct a survey of macrophyte abundance at 251 sites spanning the Atlantic coast of Nova Scotia from 2019-2022. We use this dataset to describe spatial variability in kelp species abundances, compare species occurrences to surveys conducted in 1982, and assess changes in kelp abundance over the past 22 years. We then relate spatial and temporal patterns in abundance and resilience to environmental metrics.
Key Results
Our results show losses of sea urchins and the cold-tolerant kelp species Alaria esculenta, Saccorhiza dermatodea, and Agarum clathratum in Nova Scotia since 1982 in favor of the more warm-tolerant kelps Saccharina latissima and Laminaria digitata. Kelp abundances have increased slightly since 2000, and S. latissima and L. digitata are widely abundant in the region at the present time. The highest kelp cover occurs on wave exposed shores and at sites where temperatures have remained below thresholds for growth (21°C) and mortality (23°C). Moreover, kelp has recovered from turf dominance following losses at some sites during a warm period from 2010-2012.
Conclusions
Our results indicate that dramatic changes in kelp community composition and a loss of sea urchin herbivory as a dominant driver of change in the system have occurred in Nova Scotia over the past 40 years. However, a broad-scale shift to turf-dominance has not occurred, as predicted, and our results suggest that resilience and persistence are still a feature of kelp forests in the region despite rapid warming over the past several decades.
... Higher temperatures experienced during summer are, however, also associated with increased grazer abundances and consumption rates that can further exacerbate tissue damage Krumhansl & Scheibling, 2011;Toth & Pavia, 2002). Increased cover of epiphytes also generally occurs through summer when temperatures are high, is often indicative of senescing kelp tissue, and can increase breakage and detritus production (Scheibling & Gagnon, 2009). While it is not possible to disentangle the relative importance of these factors in the current study, particularly when variability is high, it is likely they influenced detrital production rates and may to some extent explain the observed variability between survey years. ...
Coastal habitats are increasingly recognized as fundamentally important components of global carbon cycles, but the rates of carbon flow associated with marine macrophytes are not well resolved for many species in many regions. We quantified density, rates of primary productivity, and detritus production of intertidal stands of two common intertidal kelp species-Laminaria digitata (oarweed) and Saccharina latissima (sugar kelp)-on four NE Atlantic rocky shores over 22 months. The density of L. digitata was greater at exposed compared to moderately exposed shores but remained consistently low for S. latissima throughout the survey period. Individual productivity and erosion rates of L. digitata did not differ between exposed and moderately exposed shores but differed across exposure levels throughout the year at moderately exposed sites only. Productivity and erosion of S. latissima remained low on moderately exposed shores and showed no clear seasonal pattern. Patterns of productivity and total detrital production (erosion and dislodgement) per m2 of both L. digitata and S. latissima followed closely that of densities per m2, peaking in May during both survey years. Temperature and light were key factors affecting the productivity rates of L. digitata and S. latissima. Erosion rates of L. digitata were affected by wave exposure, temperature, light, grazing, and epiphyte cover, but only temperature-affected erosion of S. latissima. Production of biomass and detritus was greater in L. digitata than in S. latissima and exceeded previous estimates for subtidal and warmer-water affinity kelp populations (e.g., Laminaria ochroleuca). These biogenic habitats are clearly important contributors to the coastal carbon cycle that have been overlooked previously and should be included in future ecosystem models. Further work is required to determine the areal extent of kelp stands in intertidal and shallow subtidal habitats, which is needed to scale up local production estimates to entire coastlines.
... These highly productive systems provide many ecosystem functions, including habitat provision (Teagle et al. 2017), detrital food supply (Krumhansl & Scheibling 2012), and nutrient cycling (Pfister et al. 2019). Since the early 1990s the integrity of these kelp beds has been compromised, in part, by a successful invasive species, the epiphytic bryozoan Membranipora mem branacea (Saunders & Metaxas 2008, Scheibling & Gagnon 2009, Caines & Gagnon 2012. Outbreaks of M. membranacea can lead to substantial defoliation of kelps (Saunders & Metaxas 2008, Scheibling & Gagnon 2009, as encrustation by the bryozoan decreases the strength of the kelp tissue, increasing the probability of breakage and dislodgement in periods of intense wave action such as storm events (Krumhansl & Scheib ling 2011, Filbee-Dexter & Scheibling 2012, O'Brien et al. 2015. ...
... Since the early 1990s the integrity of these kelp beds has been compromised, in part, by a successful invasive species, the epiphytic bryozoan Membranipora mem branacea (Saunders & Metaxas 2008, Scheibling & Gagnon 2009, Caines & Gagnon 2012. Outbreaks of M. membranacea can lead to substantial defoliation of kelps (Saunders & Metaxas 2008, Scheibling & Gagnon 2009, as encrustation by the bryozoan decreases the strength of the kelp tissue, increasing the probability of breakage and dislodgement in periods of intense wave action such as storm events (Krumhansl & Scheib ling 2011, Filbee-Dexter & Scheibling 2012, O'Brien et al. 2015. Temperature is known to re gu late outbreaks of M. membranacea in the invaded range (Saunders & Metaxas 2009a, Scheibling & Gagnon 2009, with higher temperatures leading to increased and earlier settlement (Saunders & Metaxas 2007) as well as enhanced colony (Saunders & Metaxas 2009b) and population growth (Denley et al. 2019a). ...
... Outbreaks of M. membranacea can lead to substantial defoliation of kelps (Saunders & Metaxas 2008, Scheibling & Gagnon 2009, as encrustation by the bryozoan decreases the strength of the kelp tissue, increasing the probability of breakage and dislodgement in periods of intense wave action such as storm events (Krumhansl & Scheib ling 2011, Filbee-Dexter & Scheibling 2012, O'Brien et al. 2015. Temperature is known to re gu late outbreaks of M. membranacea in the invaded range (Saunders & Metaxas 2009a, Scheibling & Gagnon 2009, with higher temperatures leading to increased and earlier settlement (Saunders & Metaxas 2007) as well as enhanced colony (Saunders & Metaxas 2009b) and population growth (Denley et al. 2019a). ...
In certain regions of the northwest Atlantic, rocky subtidal habitats have transitioned from luxuriant kelp beds to turf dominated ecosystems. Encrustation by the invasive epiphytic bryozoan Membranipora membranacea has accelerated the defoliation of macroalgal stands, particularly on the southwestern shore (SWS) of Nova Scotia. In contrast, at the Eastern Shore Islands (ESI) in Nova Scotia, a temperate island archipelago with relatively high wave exposure, kelp beds persist. We investigated how spatial and temporal dynamics of the dominant kelps (Saccharina latissima and Laminaria digitata) and M. membranacea relate to wave exposure. We examined canopy cover and density of kelps using video transects and quadrat sampling at 6 sites of different wave exposures at ESI and a highly wave exposed site on the SWS (Shag Rock), where kelp also persists, in summer and autumn 2018-2020. We measured percent cover of adult colonies of M. membranacea on kelps from autumn 2018 to autumn 2020, and density of settlers in 2019. Colony cover of M. membranacea was comparable across the range of wave exposures at ESI, whereas settler density peaked at intermediate wave exposure. Despite annual outbreaks of the bryozoan, kelp beds at ESI persisted over multiple years, in contrast to a declining trend at Shag Rock. Overwinter recovery of kelps at ESI following bryozoan-induced seasonal declines the preceding autumn indicate that, in contrast to sites on the SWS, these colder more wave exposed kelp beds may be resilient to defoliation.
... In addition, there are known cases of competition for food (Wahl, 1989), limitation of growth of the basibiont (Reaka, 1978;Denisenko and Savinov, 1984;Denisenko et al., 2013) and even its death, for example, in case of heavy encrusting of a species of Antarctic brachiopods by bryozoans, blocking the slit between the valves (Barnes and Clarke, 1995). In macrophytes, such interactions often lead to a decrease in growth intensity due to reduction of a general area of photosynthesis (Oswald et al., 1984), as well as a breakdown of the thalli under the weight of a crust made of epibionts, in particular bryozoans (Scheibling and Gagnon, 2009). The development of such a crust also negatively affects the reproduction of algae (Saier and Chapman, 2004). ...
The life of sedentary organisms faces strong competition for space against neighboring epibionts, and the impact of predators. The emergence of various adaptations to cope these problems includes establishing various interactions with other members of benthic communities. Various symbiotic (commensal, mutualistic, and even parasitic) relationships presented in multiple variations allow not only to succeed in the competition for free space, but also provide other equally important advantages for survival. Being one of the most abundant groups of colonial invertebrates in marine benthic ecosystems, bryozoans are not an exception. This group demonstrates both common and unique symbiotic associations. This article provides an overview of all known forms of symbiosis in Bryozoa, fossil and modern, and discusses the consequences of such relationships.
... Membranipora membranacea is an invasive epiphytic bryozoan in the northwest Atlantic Ocean (NWA) responsible for severe defoliation of kelp beds (Scheibling & Gagnon 2009, Filbee-Dexter et al. 2016, which support diverse communities and provide valuable ecosystem services (Wernberg et al. 2019). The extent of kelp defoliation in a given area is related to the percentage of kelp blade surface area covered by colonies of M. membranacea (percent cover) and, specifically, peak percent cover of the bryozoan during its annual life cycle (Scheibling & Gagnon 2009). ...
... Membranipora membranacea is an invasive epiphytic bryozoan in the northwest Atlantic Ocean (NWA) responsible for severe defoliation of kelp beds (Scheibling & Gagnon 2009, Filbee-Dexter et al. 2016, which support diverse communities and provide valuable ecosystem services (Wernberg et al. 2019). The extent of kelp defoliation in a given area is related to the percentage of kelp blade surface area covered by colonies of M. membranacea (percent cover) and, specifically, peak percent cover of the bryozoan during its annual life cycle (Scheibling & Gagnon 2009). Temperature is the primary driver of peak percent cover of M. membranacea (Scheibling & Gagnon 2009). ...
... The extent of kelp defoliation in a given area is related to the percentage of kelp blade surface area covered by colonies of M. membranacea (percent cover) and, specifically, peak percent cover of the bryozoan during its annual life cycle (Scheibling & Gagnon 2009). Temperature is the primary driver of peak percent cover of M. membranacea (Scheibling & Gagnon 2009). Consequently, with ocean warming, it is expected that the negative impact of the bryozoan on kelp beds in its invaded range will increase (Saunders et al. 2010, Denley et al. 2019a) and that its range may expand into the Arctic (Goldsmit et al. 2018, Denley et al. 2019b. ...
Climate change is expected to create more favourable climatic conditions for many invasive species, increasing their abundance and range. One such invasive species is Membranipora membranacea , an epiphytic bryozoan causing defoliation of kelp beds in the northwest Atlantic Ocean (NWA). The impact of M. membranacea is directly linked to its abundance, which is anticipated to increase due to climate change. Additionally, further range expansion may threaten Arctic kelp beds in the future. We constructed a species distribution model (SDM) to predict the abundance of M. membranacea in the NWA under present and future climate scenarios. We also assessed the effect of a possible additional invasion of M. membranacea from populations in Norway. The projected future abundance distribution of M. membranacea in the NWA differed substantially depending on the future climate scenario employed, but the bryozoan was predicted to occur in the Arctic at low abundances regardless of the scenario. However, we also found that populations of M. membranacea in Norway achieve much higher abundances at lower temperatures than NWA populations and could pose a dire threat to kelp beds in the NWA and southern Canadian Arctic if introduced in these regions. Although the SDMs performed well under internal validation, estimating the impact of M. membranacea is complicated by the context-dependent response of kelp communities to coverage by the bryozoan. Nonetheless, this study provides valuable predictions of the response of an ecologically significant invasive species to climate change with findings of broader relevance to the study of other invasive organisms.
... In addition, the available substrate plays a relevant role, where more ancient ports (i. e. Funchal), with less available space/niches, have more NIS but lesser total diversity as detected in the present study evidencing more homogeneous assemblages (Scheibling and Gagnon, 2009). ...
Anthropogenic pressures such as the introduction of non-indigenous species (NIS) have impacted global biodiversity and ecosystems. Most marine species spreading outside their natural biogeographical limits are promoted and facilitated by maritime traffic through ballast water and hull biofouling. Propagule pressure plays a primary role in invasion success mixed with environmental conditions of the arrival port. Moreover, with the current ocean sprawl, new substrates are offered for potential NIS recruits. Here, differences in the fouling assemblages thriving inside three different ports/marinas facilities in Madeira Island were assessed for comparison. The locations showed significant differences concerning assemblage structure. Most NIS were detected in plastic floating pontoons. Funchal harbour receives most of the marine traffic in Madeira, acting as the main hub for primary NIS introductions, being recreational boating involved in NIS secondary transfers. Our results highlight the need for future management actions in island ecosystems, particularly monitoring and sampling of recreational boating.
... There are many reports that epibionts increase the defoliation or dislodgement of host macrophytes, especially during winter storms (e.g. Dixon et al., 1981;Lambert et al., 1992;Scheibling et al., 1999;Levin et al., 2002;Saier and Chapman, 2004;Saunders and Metaxas, 2008;Scheibling and Gagnon, 2009;Watanabe et al., 2010;da Gama et al., 2014), leading to loss of biomass from macrophyte communities and seaweed farms and to an increase in the supply of detritus for benthic communities (Fletcher, 1995;. It has been suggested that epibionts cause this macrophyte loss by increasing the hydrodynamic forces the hosts must bear in flowing water (Dixon et al., 1981;Wahl, 1989;Wahl, 2008;Harder, 2009). ...
Macroalgae provide surfaces where other organisms live. Unlike organisms on rigid substrata, epibionts on host macroalgae sit on flexible surfaces that bend, stretch, and move in turbulent water currents and waves. We used blade-like red algae, Mazzaella splendens, and encrusting bryozoans, Membranipora membranacea, to investigate the biomechanical and hydrodynamic effects of encrusting epibionts on macroalgae, and of flexible hosts on epibiotic bryozoans. Passive flapping by algae in wave-driven ambient flow enhanced renewal of water near hosts and epibionts. Wave exposure and the presence of a surrounding canopy of flexible algae altered the locations along algal blades where bryozoans encountered the highest time-averaged boundary shear velocities. Hydrodynamic forces on flexible algae moving back-and-forth with the water were lower in waves than in unidirectional flow. Bryozoan epibionts increased hydrodynamic forces on host algae by affecting their reconfiguration in moving water. Encrusting bryozoans increased the flexural stiffness of algal blades, but the elastic modulus, extensibility, and strength of blade tissue was unaffected by bryozoan epibionts. Algal blades were more extensible and stronger than bryozoans, so bryozoans fractured or popped off stretched algae. Algae in rapid-flow habitats had few epibionts, and encrusted algae transplanted from a protected to a wave-exposed habitat lost their epibionts.
... Membranipora membranacea is a native species in Europe, but is documented causing weakness in blades in places where it is non-native (i.e. North America, see Scheibling and Gagnon, 2009). There is a lack of information on the effect M. membranacea has on detrital production in North-East Atlantic kelp forests, but the species is often seen on detritus towards the end of summer months (Figure 2.2.2 c). ...
The ecological and biological importance as well as economic, and cultural value of macroalgae is becoming more prominent. Introduction of the term ‘blue carbon’ (BC) has drawn attention to natural coastal ecosystems, the habitats they provide, and their capacity to fix CO2. The overall aim of this thesis was to place the importance of carbon sequestration within the already essential services that macroalgae provide to the biosphere. This thesis focused on: 1) Quantifying the amount of detritus produced by species in Scottish macroalgae habitats and providing annual figures of total carbon leaving kelp forests in fluxes, 2) understanding the processes of degradation of detritus from three dominant kelp species and estimating the pathways of carbon loss of the detritus, and 3) identifying the sources of sediment carbon using biomarkers and environmental DNA primers specific to the class Phaeophyceae.
Macroalgae in the North-East Atlantic: 1) fix significant amounts of CO2 through photosynthesis thus removing it from the atmosphere, 2) release the carbon fixed through photosynthesis as detritus which accumulates and is buried, broken down by bacteria, and contributes to food webs, and 3) contributes carbon to sediment stores in Scotland and the wider North-East Atlantic shelf. These three criteria are fundamental blue carbon habitat characteristics. It is thereby recommended that macroalgae are henceforth included in blue carbon frameworks and directives, particularly in Scotland, where the contribution to long-term carbon stores in fjord and shelf systems is potentially greater than any other BC habitat in the region. It is estimated that 0.2 Mt C yr-1 is transferred to sediments from macroalgae in Scotland, the equivalent of 0.04 g C m-2 of kelp forest.
