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Article

Predicted Changes in the Biogeographical Range of Gracilaria vermiculophylla under Present and Future Climate Scenarios

by
Clara Mendoza-Segura
1,
Emilio Fernández
2 and
Pedro Beca-Carretero
1,*
1
Department of Oceanography, Institute of Marine Research (IIM-CSIC), 36208 Vigo, Spain
2
Centro de Investigación Marina, Facultad de Ciencias del Mar, Universidad de Vigo, 36310 Vigo, Spain
*
Author to whom correspondence should be addressed.
J. Mar. Sci. Eng. 2023, 11(2), 367; https://doi.org/10.3390/jmse11020367
Submission received: 15 December 2022 / Revised: 18 January 2023 / Accepted: 30 January 2023 / Published: 7 February 2023
(This article belongs to the Special Issue Marine Macrophyte Restoration and Restocking)
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Abstract

:
Global change effects have favoured the introduction of new species in marine ecosystems in recent years. Gracilaria vermiculophylla, a red seaweed native from the north-eastern Pacific, has successfully colonised large regions in the Northern Hemisphere. In this research, we implemented species distribution models (SDMs) to (i) examine which were the most important environmental factors defining the presence of G. vermiculophylla at a global scale, and (ii) determine the potential current and future distribution of G. vermiculophylla based on two climate scenarios (representative concentration pathways (RCP 2.6 and RCP 8.5)). Our results suggest that temperature and salinity were the most important variables explaining the distribution of the target species. Additionally, the SDMs for present climate settings showed a potential wider distribution than is recorded to date. In addition, a subtle habitat expansion of 2.9° into higher latitudes was reported under the RCP 2.6 scenario by the end of this century. The high-carbon-emission scenario (RCP 8.5) delivered a potential large habitat expansion (6.0°), even reaching arctic latitudes, and a remarkable habitat loss of 11° in its southern distribution range. SMDs also forecasted suitable areas for this species in the Southern Hemisphere, pointing toward a potential global expansion in the coming decades.

1. Introduction

Climate change and the introduction and spreading of non-native species represent a real threat to marine ecosystems generating changes in native biodiversity, creating novel biological interactions, and altering the provision of ecological services [1,2,3]. Global warming is expected to affect marine species distribution ranges, creating novel habitats potentially available to be colonized by non-native species [3,4,5]. Marine traffic and aquaculture have been identified as two of the main vectors of invasion in marine systems, favouring long-distance transportation of sessile organisms such as seaweeds [1,6,7,8]. As a result, macroalgae invasions have been recorded in most parts of the globe; however, seaweed species distribution responses to climate change and their ecological impacts remain largely unknown, e.g., [7,8,9,10].
To date, approximately 7400 species of red algae have been described [11] and it is estimated that over 80% of the orders in the Rhodophyta have been reported out of their native areas [6]. The red alga Gracilaria vermiculophylla ((Ohmi) Papenfuss 1967), also known as Agarophyton vermiculophyllum (Gurgel, Norris & Fredericq, 2018), is native to the north-western Pacific coast of Japan, China and Korea, e.g., [12,13,14]. In these temperate regions, G. vermiculophylla is a perennial and foundation species that creates highly productive habitats and nursery grounds for fish and invertebrates, providing other ecological functions including CO2 uptake and sequestration, organic carbon production and nutrient recycling [15,16,17,18,19]. Temperature, irradiance and salinity have been identified as the most important environmental variables controlling its physiological, growth and reproductive responses [16,20,21]. Sea surface temperature (SST) is, aside from irradiation, one of the key factors that controls the germination and growth of macroalgae [22]. Gracilaria vermiculophylla is characterised by a clear seasonal growth pattern with peaks of maximum biomass production observed in summer and minimum in winter under coldest temperatures [23,24]. Both life stages of G. vermiculophylla—gametophyte and tetrasporophyte—have been proven to be eurythermal, tolerating a wide range of thermal conditions with an optimal growth occurring between 15 to 30 °C [15,17,25]. Salinity also plays a major role in Gracilaria species, varying not only growth responses, but also photosynthesis performance [25,26,27]. Gracilaria vermiculophylla is a euryhaline species exposed to broad salinity changes in its natural intertidal estuarine areas [28,29]. Unlike other algae species, a low irradiance level (maximum growth occurring at 80–100 µmol m−2 s−1) at natural conditions is not a limiting factor determining its survival, as this species can persist for several months in darkness by reducing metabolic costs and growth rates until environmental conditions are more favourable [15,16,20,25,28]. To a lesser extent, nutrient availability and pH also influence physiological and growth responses of the target species; however, their effects are often temperature-dependent [5,22,30,31]. It is noteworthy that previous experimental studies indicated that its growth is not constrained by nutrient limitations in the environment due to its high capacity to store nutrients in its tissues, which are then remobilised and utilised during starvation months [5,22,30,32,33]. However, P-limitation was suggested to limit blooms of this species during the growing season in non-native regions [30,34].
Gracilaria vermiculophylla has become one of the most widespread invasive macroalgae in the Northern Hemisphere [7,35,36]. This species was first recorded in non-native regions over both coasts of the Atlantic Ocean, the Mediterranean Sea and the eastern Pacific coasts in the early 2000s [28,37,38]. Its introduction in new regions has been linked to oyster culture followed by an expansion to other sites due to secondary vectors such as fouled gear, birds, boats and other vessels [7,16,39]. In native areas, this species is usually found as gametophytes and tetrasporophytes in wave-exposed habitats attached to hard substrata such as rocks or calcareous organisms, while in non-native regions, it is mainly distributed in soft sediments in sheltered bays, estuarine or mudflats areas as unattached tetrasporophytes [16,17,40]. Thus, due to the different reproduction strategies, native populations have shown strong genetic structure (heterogeneity), whereas in non-native areas, only a few haplotypes have been described [35,36,40]. Gracilaria vermiculophylla is characterised by great morphological plasticity, fast propagation, and the capacity to synthesise chemical defences against grazers [5,20,41,42,43]. These capabilities make G. vermiculophylla a great competitor for resources and habitat, allowing this species to colonize a wide variety of environments such as shallow bays, semi-exposed habitats or intertidal regions in coastal lagoons or estuaries [7,44,45]. However, despite the growing ecological impact of G. vermiculophylla in non-native areas and its recent use in industry [17,46], there are no reports to date assessing how present and future climate conditions will affect its potential habitat distribution outside its native range [47,48].
Species distribution models (SDM) are valuable tools that generate robust explicit spatial data, allowing the prediction of potential shifts in habitat distribution, thus contributing to the management of native and non-native species [49,50]. They have been widely implemented to predict the potential suitable habitat distribution of marine species, including primary producers, in response to environmental factors, e.g., [51,52].
In this study, by applying SDMs and spatial analyses, we aimed to (i) examine which are the most important variables explaining the distribution of G. vermiculophylla at a global scale at present conditions; (ii) compare the SDM predictions for current habitat suitability of G. vermiculophylla based on multiple environmental variables versus the predictions only using sea surface temperature and salinity; and (iii) investigate the potential changes in the biogeographical range of G. vermiculophylla under future climate scenarios by implementing SDMs based on sea surface temperature and salinity. Our first hypothesis states that SST and salinity are the main environmental variables that determine the current distribution of G. vermiculophylla based on previous in situ and experimental studies. We also hypothesize that this species will continue expanding its biogeographical range towards higher latitudes and will potentially colonize novel habitats as climate change progresses.

2. Methodology

2.1. Gracilaria vermiculophylla Occurrences

Data of presence and distribution of G. vermiculophylla were compiled from diverse sources such as published articles and databases (e.g., the Global Biodiversity Information Facility (GBIF) [53] (Table S1). The total records of the distribution of the target species were 743. In addition, we added a new location from our study site in the northwest of Spain, Galicia (latitude: 42.30956, longitude: −8.62582), where this species is usually found coexisting with Zostera marina (Linnaeus, 1753) and Z. noltei (Hornemann, 1832) in intertidal and upper subtidal areas. In this location, we are currently conducting research studies assessing the ecological impacts of G. vermiculophylla in seagrass ecosystems and in shell fishing grounds, as shown in Figure S1.

2.2. MAXENT Model

In this study, we implemented the MAXENT model, based on a maximum-entropy algorithm, characterised by robustly performing using only occurrence datasets; thus, this approach is capable of creating background data [54,55]. Previous studies successfully implemented this modelling approach to evaluate species’ geographic extent for different purposes, such as biological invasions or species management and conservation [56,57,58].
MAXENT generated a continuous raster file with a pixel value ranging from 0 to 1, with 0 representing the absence of the target species, and 1 representing the highest probability for potential habitat suitability. The predicted probabilities derived from the SDMs were transformed into binary maps with two categories: suitable or unsuitable habitats for the presence of the species. To assume the potential habitat suitability of Gracilaria vermiculophylla, the logistic threshold “equal training sensitivity and specificity” was set as 0.215 for the SDM built with several environmental descriptors and 0.156 for the model built after SST and salinity values (see Tables S2 and S4).
SDMs were calibrated using a random sample of 70% (520 records) of the presence of the target species at a global scale, and later validated by selecting a random 30% (223 records) of the distribution data of the species. The calibration was conducted 25 times using different random distributions of the target species. To evaluate the model, we used four different approaches. The first approach was based on “sensitivity”, which is the proportion of the presence of the species adequately forecasted by the model [59]. The second evaluation approach was based on the threshold-independent metric “area under the curve” (AUC) and “receiver operating characteristic (ROC)”; ROC values ranging from 0.5 to 0.7 indicated a poor prediction by the SDM; outcomes between 0.7 and 0.9 have a moderate discriminatory ability; and SDM outcomes with values higher than 0.9 were considered able to predict with high robustness [60]. The significance of the AUC was assessed by implementing a cross-validation procedure covering 100 interactions. Additionally, to assess the model performance, we analysed the true skill statistic (TSS) and kappa [59]. The final distribution maps of the target species, were obtained based on the average of the 25 independent predictions.

2.3. Environmental Variables

To conduct the SDMs and spatial analyses of the target species, we used the environmental variables available in the BIO-ORACLE database [61]. The variables used in all SDMs had a spatial resolution of 30 arc-seconds.
In this study, we developed two models for present climate conditions, one including mean values of SST, salinity, photosynthetic active radiation (PAR), nitrate, phosphate, dissolved molecular oxygen and pH, and a second model only including SST and salinity. In the latter, we included mean, maximum and minimum SST values, as well as maximum and minimum surface salinity. Variables with a positive significant correlation with r >0.85 were excluded from the spatial analyses. Specifically, mean salinity was excluded due to its high collinearity with minimum and maximum salinity.
To perform future predictions, we only used SST and salinity as environmental descriptors due to the limited availability of marine environmental variables under future climate scenarios [62]. Thus, we run the models based on future climate scenarios with a final set of five environmental descriptors: mean, maximum and minimum SST values, along with maximum and minimum surface salinity. For future climate scenarios, we used two contrasting greenhouse gas concentration scenarios: RCP 2.6 (representative concentration pathway; low-carbon-emission scenario) and RCP 8.5 (high-carbon-emission scenario) [62,63].

2.4. Species Distribution Models (SDMs) and Spatial Analyses

To test which were the most important variables explaining the distribution of Gracilaria vermiculophylla and to compare predictions for current habitat suitability, we applied two SDMs: one including mean values of SST, salinity, PAR, nitrate, phosphate, dissolved molecular oxygen and pH, and a second model only including SST and salinity.
SDMs were also executed to investigate the potential variation in the biogeographical range of G. vermiculophylla during the 21st century based on SST and salinity. These models were built taking into consideration that the presence of G. vermiculophylla, in the locations where it has been identified from the literature review depicted in Figure 1 and has remained constant since its first record.
Lastly, we implemented density curve analyses to investigate latitudinal changes in the frequency distribution of the target species based on all the models built in this study for present and future climate scenarios (RCP 2.6 and 8.5) in the Northern Hemisphere [64]. Density analyses were conducted using the ggplot2 package with R software.
Jmse 11 00367 g001 550
Figure 1. Map of the current distribution of Gracilaria vermiculophylla showing native (green points) and non-native populations (purple points). References noted in the map [16,28,37,38,65,66,67,68,69] represent the first records of G. vermiculophylla that were made outside its native area.
Figure 1. Map of the current distribution of Gracilaria vermiculophylla showing native (green points) and non-native populations (purple points). References noted in the map [16,28,37,38,65,66,67,68,69] represent the first records of G. vermiculophylla that were made outside its native area.
Jmse 11 00367 g001

3. Results

This study includes an updated review of the distribution of Gracilaria vermiculophylla at a global scale, as shown in Figure 1. In addition, data of the locations displayed on the map are available for query in Table S1.
Based on the conducted literature review, G. vermiculophylla is currently distributed in its native region (Northwest Pacific Ocean) from 21.5 to 45.3° N, covering a latitudinal distribution of ~23.8°, exposed to annual SST ranging of 8.6–19.6 °C. In non-native regions, its distribution covers a latitudinal ranging from 22.6 to 58.9° N, and it is exposed to SST ranging from 7.5 to 26.9 °C; see Table 1. Particularly, this species is currently living at a maximum SST of 26.9 ± 0.1 °C and 26.6 ± 2.2 °C in the Mediterranean Sea and the Northeast Atlantic Ocean, respectively, and a minimum SST of 3.0 ± 4.6 °C and 5.8 ± 4.7 °C in the Northwest Pacific Ocean and the Northeast Pacific Ocean, respectively. This species inhabits coastal waters with maximum salinities of 32.8 ± 1.2‰ and a minimum of 26.9 ± 3.0‰.

3.1. Comparison of SDMs for the Current Climate Scenario

The predictions of the model built for present climate conditions using SST, salinity, PAR, nitrate, phosphate, dissolved molecular oxygen and pH as environmental descriptors showed a high robustness and discriminatory performance with values of AUC = 0.98; sensitivity = 0.95; TSS = 0.92; and kappa = 0.79 (Table S2). Results of the relative contribution of the environmental descriptors indicated that salinity was the most relevant variable explaining the current distribution of G. vermiculophylla with a relative contribution of 25.8%, followed by temperature (19.8%) and nitrate (17.9%) (Table S3). In contrast, irradiance (measured here as PAR) and oxygen contributed less than 5%.
The evaluation of the model using SST and salinity as environmental descriptors reported a high robustness and discriminatory performance with values of AUC = 0.97; sensitivity = 0.93; TSS = 0.88; and kappa = 0.63 (Table S4). The scores of the relative contribution of the environmental descriptors indicated that the most relevant factors explaining the distribution of G. vermiculophylla were minimum salinity (36.2%) and minimum temperature (29.1%), followed by mean temperature (26.2%) and finally, with minor importance, maximum temperature (7.4%) and mean salinity (1.1%), as shown in Table S5.
Figure 2a shows that the SDM based on SST, salinity, PAR, nitrate, phosphate, dissolved molecular oxygen and pH predicted a slightly wider distribution of G. vermiculophylla than did the model based on SST and salinity under present conditions. Particularly, the SDM including all the variables forecasted the area of suitability of the target species in novel areas such as the coast of Alaska, scattered areas of Africa’s coastline, nearly the whole coastal area of the Sea of Okhotsk, the White Sea and the Baltic Sea. Additionally, density curve analyses reported differences in the maximum abundance of G. vermiculophylla between both models under present conditions. The SDM built with SST and salinity as environmental descriptors showed a maximum abundance at ~48° N, whereas the model using all the variables pointed out the maximum at 44° N (Figure 2c). However, as shown in Figure 2b, there were no significant differences between the potential habitat suitability of G. vermiculophylla predicted with the SDM based on SST and salinity, and the model based on SST, salinity, PAR, nitrate, phosphate, dissolved molecular oxygen and pH.

3.2. SDMs for the Future Climate Scenario

The SDM built for G. vermiculophylla for present climate settings based on temperature and salinity showed a potentially wider distribution (12.1 to 65.1° N) than recorded to date (21.5 to 45.3° N), as shown in Figure 3.
Overall, future projections predicted a northward latitudinal expansion and a habitat regression in its southern latitudinal distribution range as climate change progresses during this century; however, these trends differed in the two tested climate scenarios. The simulation performed under the RCP 2.6 scenario, shown in Figure 3a, predicted a northward expansion of the habitat suitability of 2.0° by 2040–2050, and 3.0° under the high-carbon-emission scenario (RCP 8.5). By 2100, a northward expansion reaching latitudes of 68.1° N was projected under RCP 2.6, and subarctic latitudes (71.1° N) under the RCP 8.5 climate scenario. SDMs predicted a southern habitat regression by 2100 of 1.0° under the RCP 2.6 scenario, whereas 11.0° was predicted under the RCP 8.5 scenario, as reported in Figure 3a,b and Figure 4a. In addition, density analyses forecasted a northward latitudinal displacement of the potential maximum abundance of G. vermiculophylla of ~1.6° under RCP 2.6 from present conditions to 2050 and 2100 (see Figure 4b). On the contrary, a northward latitudinal displacement of the potential maximum abundance of the target species of ~2.0° and 14.1° was observed under RCP 8.5 from present conditions to 2050 and 2100, respectively (see Figure 4c). Lastly, the SDM built for G. vermiculophylla also forecasted suitable habitats based on temperature and salinity drivers in the Southern Hemisphere in north Australia and South American coasts at latitudes ranging from 28° to 38° S.

4. Discussion

The spread and colonisation of marine macroalgae in non-native regions over recent decades is a phenomenon that has been linked to human activity and global warming, and is expected to intensify during this century as climate change progresses [1,3,6]. Some of the most notorious and successful settlements of non-native macroalgae species have been reported in the Mediterranean Sea by Caulerpa racemosa ((Forsskål) J.Agardh, 1873) or in the North Atlantic Sea by Sargassum muticum ((Yendo) Fensholt, 1955) and Rugulopterix okamurae ((E.Y. Dawson) I.K. Hwang, W.J. Lee & H.S. Kim, 2009), e.g., [1,8,43]. In this study, we observed that the habitat suitability of Gracilaria vermiculophylla can be larger than is currently reported, indicating a potential expansion in non-native regions. Additionally, our predictions showed that future climate scenarios will favour the expansion of the species’ habitat to higher latitudes during this century, as suggested by [48], for the distribution of this species in its native region.
For present conditions, our SDMs identified temperature, salinity and nitrate as the main variables explaining the distribution of G. vermiculophylla at a global scale. Previous investigations under natural and laboratory conditions have studied the effects of multiple abiotic factors on the life history of the target species, demonstrating the key roles of temperature and salinity in regulating fundamental physiological and biological functions [15,17,20,25,29]. In this matter, our SDMs that only included SST and salinity as environmental variables showed that the most important environmental variables explaining the distribution of G. vermiculophylla were minimum salinity and minimum temperature (data displayed in Table S5). This is probably because temperatures below 3 °C and salinities below 21.5 psu may represent a physiological threshold for the growth and survival of this species in natural environments, hence limiting its presence in higher latitudes, e.g., [17]. Additionally, other researchers have reported that its metabolism remains stable from 20–60 psu, whereas optimal conditions for growth have been observed between 26 and 35 psu [20,26]. Mean SST was also relatively important in determining the spatial distribution of G. vermiculophylla, probably due to the presence of this species in temperate regions characterized by the absence of extreme thermal ranges. Former experimental studies with non-native specimens of G. vermiculophylla reported a high tolerance to temperatures ranging from 5 to 34 °C and salinity conditions ranging from 2 to 60‰, e.g., [15,20,41]. Notoriously, as shown in Table S1, in invaded areas, G. vermiculophylla is exposed to both lower and higher SST than in its native area. This suggests that the species has been able to increase its thermal niche in comparison with specimens from its native habitat, an observation also reported by [47], who observed higher tolerance for thermal stress in non-native species than in native species. This phenomenon was also found in non-Mediterranean specimens of the invasive seagrass Halophila stipulacea ((Forsskål) Ascherson, 1867), which were able to better acclimate to colder conditions than those from native regions in the Red Sea, also suggesting a shift in its thermal niche [58,70]. Lastly, as noted in Table S3, nitrate was also identified as an important factor determining the presence of G. vermiculophylla in the model built with SST, salinity, PAR, nitrate, phosphate, dissolved molecular oxygen and pH. Previous studies indicated that growth performance of this species was not limited by nutrient availability. Indeed, this species was characterised by a high efficiency for nitrate uptake under a wide range of N concentrations, which is considered to provide a competitive advantage under nitrogen-depleted conditions with respect to other species, such as the seagrass Z. noltei, which has higher nutrient requirements [31,33]. Moreover, the effects of nutrients in this species seems to be temperature-dependent, as nitrate limitation can decrease the growth performance of G. vermiculophylla under rising temperature conditions [33,48,71]. This scenario may be particularly relevant in the present ocean-warming context in regions with no nutrient limitation and should be especially considered in northern regions, which are notably sensitive to the invasive species, i.e., [72].
Gracilaria vermiculophylla is a recent but well-establish species in non-native regions such as in the Northeast Pacific Ocean, covering a latitudinal distribution of ~23.8° [28,37,38,66]. The results from the SDM built for the present scenario pointed out that this species may potentially be found in a wider latitudinal distribution in non-native regions (Figure 2b). Interestingly, the two predictions for the present climate scenario, either using a set of seven variables or only SST and salinity, reported no significant differences in the distribution of the target species at a global scale. For instance, as seen in Figure 2c, both models situated the potential maximum abundance of G. vermiculophylla at ~45° N. This is consistent with previous studies that reported slight differences in spatial predictions between models using different numbers of environmental variables, concluding that the selection of adequate environmental predictors is critical in obtaining optimal predictions when implementing SDMs [73,74].
Despite the potential wider habitat suitability modelled for Gracilaria vermiculophylla, some factors including the absence of transport vectors, such as ships or boats, or the lack of human activities such as aquaculture, may constrain its dispersal and colonization in further areas. Additionally, diverse local factors including biological interactions or the absence of adequate substrates can limit the settlement of G. vermiculophylla in novel habitats [16,17,20,40,47]. The lack of monitoring programmes for the early detection of the presence of this species, or the difficulty of differentiating it from other native species such as Gracilaria asiatica (Zhang & B.M.Xia, 1985) or Gracilaria verrucosa ((Hudson) Papenfuss, 1950), may also explain its underestimation in non-native regions [5,12,14,21]. We suggest performing field assessments to check the presence of the target species in those areas where our SDMs forecasted its presence, but where it has not been recorded to date. For example, in the Southern Hemisphere, the presence of G. vermiculophylla might go unnoticed due to the occurrence of other species of this genus (e.g., Gracilaria chilensis (C.J. Bird, McLachlan & E.C. Oliveira, 1986)) [14].
Our study reports two contrasting scenarios of potential habitat expansion of the biogeographical range of Gracilaria vermiculophylla based on temperature and salinity as climate change progresses during this century. Under the low-carbon-emission scenario (RCP 2.6), the distribution habitat remained rather stable, and little habitat regression was found. However, under the high-carbon-emission scenario (RCP 8.5), a great potential expansion of its biogeographical range was forecasted, being able to colonize large regions of the Northern Hemisphere, and even reaching arctic latitudes (~71° N). The arrival of exotic seaweed species into new habitats has generated diverse negative ecological impacts such as the displacement of native species, changes in the trophic chain and biogeochemical alterations [9,75]. The formation of high-density matts of G. vermiculophylla drastically reduced oxygen fluxes by increasing sediment deposition, promoting anoxia and sulphides in the sediments that were linked to mortality events of associated fauna and difficulties in the recruitment of indigenous species [76,77]. Nevertheless, the successful colonization and settlement of G. vermiculophylla in non-native regions also generated positive ecological services (see Table 2). For instance, this species provided shelter and refugee for multiples species in their juvenile stages, increased the biodiversity and ecological complexity of coastal ecosystems, created novel and positive biological interactions with native species, and even restored ecosystem functionalities that were degraded as a result of the loss of native species, e.g., [43,78].
Our SDMSs pointed out that the non-native areas currently occupied by G. vermiculophylla will remain suitable during this century; however, some species-specific characteristics may have negative effects on their long-term persistence. One of the main differences between native and non-native populations of G. vermiculophylla is the low-genetic diversity found in the latter one as a result of the dominance of asexual reproduction [35]. This characteristic could compromise the resistance, and ultimately the survival, of specimens against environmental disturbances or pathogens [81,82]. Drastic collapses of invasive species have been previously reported in other successful invasive macroalgae such as Caulerpa taxifolia ((M.Vahl) C.Agardh, 1817) [40,83]. In accordance with the outcomes reported by [48] the predicted distribution loss in native areas of this engineering species under the higher-carbon-emission scenario (RCP 8.5) could negatively affect the native community and ecological functionality and trigger drastic ecosystem changes, as has been previously observed in marine coastal habitats [84]. In addition, the predicted increase in the frequency and duration of extreme climate events such as storms and hurricanes could generate the emergence and dispersal of new fragments of marine macroalgae invasive species, fostering its arrival and spread in novel habitats [1,16].
This study provides the first projections of the potential variation in the biogeographical range of G. vermiculophylla under current and future climate scenarios in non-native regions. Our outcomes are of interest due to the ecological implications and the potential commercial interest associated with this species. Particularly, G. vermiculophylla is used in a diversity of industrial applications, such as seaweed aquaculture in Japan and the Adriatic Sea in Italy, to produce agar-agar or bio-filters for aquaculture, e.g., [17,46]. However, our outcomes should be interpreted with caution. Our SDMs do not include factors operating at a local scale such as current velocity, nutrients, sediment type or biotic interactions, which, ultimately, may alter the habitat suitability predicted by the models. In particular, as observed in SDMs under current climate conditions, the inclusion of a wider number of environmental descriptors can affect the forecasted habitat suitability of the species. Therefore, it could be expected that the future availability of additional variables may slightly modify the reported predictions, i.e., [57,85]. It is noteworthy that, in native and non-native regions, this species is usually found in bays or estuaries exposed to a wide range of environmental conditions, such as pH, wave action or desiccation. Therefore, projections at a global or regional scale are not able to explain processes at a local scale. Lastly, our species distribution maps may be useful to develop management tools to anticipate the potential colonization patterns of G. vermiculophylla, thus contributing to the design and implementation of contingency plans to mitigate its impact in novel habitats.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/jmse11020367/s1, Figure S1: Gracilaria vermiculophylla in interaction with Zostara marina and Z. noltei beds in intertidal and upper subtidal areas in our study site in the northwest of Spain, Galicia, at the beach of Cesantes; Table S1: Databased of all the sites where Gracilaria vermiculophylla has been recorded until date (n = 743). For more information please check [86,87,88,89,90,91,92,93,94,95,96,97,98,99,100]; Table S2: Characteristics of the MAXENT model built for G. vermiculophyllum based on salinity, temperature, nitrate, pH, phosphate, PAR and oxygen, including the evaluation approaches, the area under the receiver operating characteristic curve (AUC), sensitivity, Kappa and true skill statistics (TSS). Model outputs are derived from the average of 25 simulations; Table S3: Results of the relative contributions (%) of the environmental descriptors of the SDMs built for G. vermiculophyllum based on salinity, temperature, nitrate, pH, phosphate, PAR and oxigen. Results are derived from the average of 25 simulations; Table S4: Characteristics of the MAXENT model built for G. vermiculophyllum based on temperature and salinity including the evaluation approaches, the area under the receiver operating characteristic curve (AUC), sensitivity, Kappa and true skill statistics (TSS). Model outputs are derived from the average of 25 simulations; Table S5: Results of the relative contributions (%) of the environmental descriptors of the SDMs built for G. vermiculophyllum based on temperature and salinity. Results are derived from the average of 25 simulations.

Author Contributions

Conceptualization, P.B.-C., C.M.-S. and E.F.; methodology, P.B.-C. and C.M.-S.; software, P.B.-C. and C M-S.; validation, P.B.-C., C.M.-S. and E.F.; formal analysis, P.B.-C. and C.M.-S.; investigation, P B-C. and C M-S; resources, P B-C., C.M.-S. and E.F.; data curation, P.B.-C. and C.M.-S.; writing—original draft preparation, P.B.-C., C.M.-S. and E.F; writing—review and editing, P.B.-C., C M-S and E.F; visualization, P.B.-C., C.M.-S. and E.F; supervision, P.B.-C., C.M.-S. and E.F; project administration, P.B.-C.; funding acquisition, P.B.-C. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

The study did not require ethical approval.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data supporting reported results can be found in the supplementary materials section.

Acknowledgments

We thank Sara Varela for helping us in the development of the SDMs and L. Saige Alloway for helping in the edition of the article. This project was supported by a “JAE intro” Scholarship to Clara Mendoza-Segura and “Juan de la Cierva Formación” grant to Pedro Beca-Carretero of the Spanish Ministry of Science and Innovation.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 2. Panel (a): Map of the current distribution of Gracilaria vermiculophylla where habitat suitability is delimited by a set of environmental descriptors (red areas) and by sea surface temperature (SST) and salinity on their own (green areas). Panel (b,c): Representation of the dispersion (box plot graph) and present abundance layout (probability density curves) of the target species in the Northern Hemisphere in the two tested situations. Variations in distribution are expressed in latitudinal degrees (°).
Figure 2. Panel (a): Map of the current distribution of Gracilaria vermiculophylla where habitat suitability is delimited by a set of environmental descriptors (red areas) and by sea surface temperature (SST) and salinity on their own (green areas). Panel (b,c): Representation of the dispersion (box plot graph) and present abundance layout (probability density curves) of the target species in the Northern Hemisphere in the two tested situations. Variations in distribution are expressed in latitudinal degrees (°).
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Figure 3. Maps of the potential habitat distribution based on temperature and salinity descriptor build for G. vermiculophylla under present conditions of temperature and salinity and under predicted future climate change scenarios (RCP 2.6 (Panel a) and RCP 8.5 (Panel b)) by 2050 and 2100. Results were derived from the average of 25 simulations.
Figure 3. Maps of the potential habitat distribution based on temperature and salinity descriptor build for G. vermiculophylla under present conditions of temperature and salinity and under predicted future climate change scenarios (RCP 2.6 (Panel a) and RCP 8.5 (Panel b)) by 2050 and 2100. Results were derived from the average of 25 simulations.
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Figure 4. Panel (a): Current distribution (green bar), and variations in habitat suitability of Gracilaria vermiculophylla in the Northern Hemisphere under present conditions and under future climate change framework predicted for two carbon emission scenarios (RCP 2.6 and RCP 8.5) by 2050 and 2100. Variations in distribution are expressed in latitudinal degrees (°). Blue colour represents the stable distribution, yellow represents the gain distribution, and red represents the loss habitat distribution. Panel B and C: Probability density curves show more favourable latitudinal (°) regions for habitat colonization of the target species based on sea surface temperature (SST) and surface salinity under both RCP (2.6 (Panel b) and 8.5 (Panel c)) climate scenarios by 2050 and 2100. Latitudinal changes in the frequency distribution of G. vermiculophylla are shown above each curve for present, future carbon emission scenarios.
Figure 4. Panel (a): Current distribution (green bar), and variations in habitat suitability of Gracilaria vermiculophylla in the Northern Hemisphere under present conditions and under future climate change framework predicted for two carbon emission scenarios (RCP 2.6 and RCP 8.5) by 2050 and 2100. Variations in distribution are expressed in latitudinal degrees (°). Blue colour represents the stable distribution, yellow represents the gain distribution, and red represents the loss habitat distribution. Panel B and C: Probability density curves show more favourable latitudinal (°) regions for habitat colonization of the target species based on sea surface temperature (SST) and surface salinity under both RCP (2.6 (Panel b) and 8.5 (Panel c)) climate scenarios by 2050 and 2100. Latitudinal changes in the frequency distribution of G. vermiculophylla are shown above each curve for present, future carbon emission scenarios.
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Table
Table 1. Summary of the environmental descriptors including minimum, maximum and mean temperature (°C), and maximum and minimum salinity (‰), of the biogeographical regions of Gracilaria vermiculophylla.
Table 1. Summary of the environmental descriptors including minimum, maximum and mean temperature (°C), and maximum and minimum salinity (‰), of the biogeographical regions of Gracilaria vermiculophylla.
Mean Temp.Max. Temp.Min. Temp.Max. SalinityMin. Salinity
Northwest Pacific Ocean11.6 ± 2.119.3 ± 1.13.0 ± 4.630.4 ± 5.321.3 ± 10.7
Northeast Pacific Ocean16.3 ± 3.925.6 ± 2.95.8 ± 4.733.0 ± 2.428.5 ± 4.8
Northwest Atlantic Ocean15.0 ± 5.620.2 ± 5.910.8 ± 4.632.9 ± 1.627.3 ± 5.0
Northeast Atlantic Ocean17.4 ± 3.526.6 ± 2.29.3 ± 5.133.7 ± 1.530.2 ± 2.8
Mediterranean Sea17.6 ± 0.326.9 ± 0.17.4 ± 1.133.8 ± 1.027.2 ± 2.4
Average values15.6 ± 2.223.7 ± 3.37.2 ± 2.732.8 ± 1.226.9 ± 3.0
Table
Table 2. Application and effects recorded for Gracilaria vermiculophylla present in non-native areas. Ecological effects are strongly linked to its ecosystem engineer performance, and environmental risks are associated with high-biomass episodes of this seaweed.
Table 2. Application and effects recorded for Gracilaria vermiculophylla present in non-native areas. Ecological effects are strongly linked to its ecosystem engineer performance, and environmental risks are associated with high-biomass episodes of this seaweed.
LevelTypeDescriptionReferences
EconomicIndustry
  • Production of agar;
  • Soil conditioner;
  • Potential source of nutrients;
  • Sustainable fish packaging;
  • Compounds with industrial and medical applications;
  • Bio-filter for nitrogen forms in eutrophic systems or aquaculture farms.
[17,31,46,79]
EcologicalEcosystem services
  • Nursery habitats;
  • Substratum for epiphytes and invertebrates;
  • Reduce wave erosion;
  • Enhanced biodiversity and habitats niches;
  • Source of detritus;
  • Refuge from predators;
  • Stabilization of sediments.
[5,17,19,43,45,77,78,80]
Interactions with organisms
  • Association with the polychaete Diopatra cuprea (Bosc, 1802);
  • Facilitation in the formation of vegetative fragments by Littorina littorea (Linnaeus, 1758) and Diopatra cuprea;
  • Competition with native seagrass and macroalgae;
  • Potential positive interaction with Zostera marina (based on our personal observations).
[5,17,45,77]
Environmental Risks
  • Limit oxygen flow in sediment causing anoxia and sulphidic poisoning of native species;
  • Increase mortality of native organisms;
  • Sediment accumulation;
  • Reduce heterogeneity in the long term, affecting specialized organisms.
[5,45,77,78]
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Mendoza-Segura, C.; Fernández, E.; Beca-Carretero, P. Predicted Changes in the Biogeographical Range of Gracilaria vermiculophylla under Present and Future Climate Scenarios. J. Mar. Sci. Eng. 2023, 11, 367. https://doi.org/10.3390/jmse11020367

AMA Style

Mendoza-Segura C, Fernández E, Beca-Carretero P. Predicted Changes in the Biogeographical Range of Gracilaria vermiculophylla under Present and Future Climate Scenarios. Journal of Marine Science and Engineering. 2023; 11(2):367. https://doi.org/10.3390/jmse11020367

Chicago/Turabian Style

Mendoza-Segura, Clara, Emilio Fernández, and Pedro Beca-Carretero. 2023. "Predicted Changes in the Biogeographical Range of Gracilaria vermiculophylla under Present and Future Climate Scenarios" Journal of Marine Science and Engineering 11, no. 2: 367. https://doi.org/10.3390/jmse11020367

APA Style

Mendoza-Segura, C., Fernández, E., & Beca-Carretero, P. (2023). Predicted Changes in the Biogeographical Range of Gracilaria vermiculophylla under Present and Future Climate Scenarios. Journal of Marine Science and Engineering, 11(2), 367. https://doi.org/10.3390/jmse11020367

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