Did global warming really cause range contraction and genetic erosion of brown seaweed Fucus vesiculosus? A close look at sampling, biological process, and anthropogenic impact
Zi-Min Hu, Institute of Oceanology, Chinese Academy of Sciences
16 April 2014
Zi-Min Hu1, Lopez-Bautista Juan2 and De-Lin Duan1
1Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China.
2Department of Biological Sciences, The University of Alabama, Tuscaloosa, AL35487, USA.
Background
Linking the distribution shift of species to recent global warming may shed light on future geographical range of species under climate change and offer pivotal conservation insights for sustainable biodiversity. The recent BMC Biology article by Nicastro et al. [1] combined temporal changes of distribution range of canopy-forming seaweed Fucus vesiculosus with historical sea surface temperature (SST) during 1982 – 2011 and genetic data (five microsatellites and 12 populations), to unravel the influence of climate warming on the distribution pattern along Iberian and Atlantic North African coastlines and associated evolutionary consequence. Their main result states that ‘a remarkable climate-induced species range reduction is driving a cryptic genetic clade (southern clade) to extinction’. We generally agree with the point that global warming is responsible for the contraction of F. vesiculosus in its geographic range. However, to the extent of our knowledge, several interactive environmental variables can contribute to species distribution in the context of increasing anthropogenic impact on coastal ecosystem. In particular, this article provides no direct physiological evidence regarding the sub-lethal performance of F. vesiculosus in response to long-term or abrupt thermal stress. We will discuss potential bias of incomplete sampling and highlight some overlooked factors contributing to range shift of F. vesiculosus reported by Nicastro et al. [1] in view of recent relevant findings.
Sampling coverage and a vanishing genetic lineage
F. vesiculosus is characterized by different depth distributions and ecological niches varying from tidal marshes to exposed rocky intertidal and shallow subtidal shores. The current field survey of eighty-four moderately wave-exposed and estuarine locations from Hondarribia to Dakhla [1] may be good sampling cover but geographically irregular and scattered (e.g. habitat coverage in elevation), and thus may bias the subsequential genetic investigation at population level.
First, Nicastro et al. [1] reported that population LX from Morocco was extinct in 2009, such a conclusion is questionable because recent field investigation indicated that F. vesiculosus still can be collected from the same geographic site [2]. This discrepancy may stem from the species’ variable and cryptic living habitats at the southern edge. For instance, from Northern Portugal southwards towards Morocco F. vesiculosus disappears from the open coast, whereas occurs only inside estuaries and coast lagoons where no other Fucus species is present (allopatric range) [3]. In addition, some “relict” Fucus populations which reflect the permanence of species left behind the retreating margin during warming periods [4], can just occur in some cryptic sites outside its “normal” range including isolated and wave-sheltered estuaries [5], which has been confirmed recently in San Vicente de la Barquera or Tapia Port, North Spain [6]. Thus Nicastro et al. [1] probably missed some important geographic samplings. Increased sampling from these areas may concrete the observed conclusion that population biomass of F. vesiculosus has reduced mostly in the southern areas.
Second, F. vesiculosus can dominate the subtidal hard-bottom areas down to 4.0 – 9.0 m depth [7,8], and Nicastro et al. [1] sampled only two sites from 500 m to 1 km apart for each locality; thus this sampling approach did not take into account depth gradient and thus may lead to a rough generalization. To minimize the bias of sampling, we therefore advocate that more deliberate sampling methods should be designed and conducted at both transection (width) and longitudinal-section (depth) scales, such as covering a 1-km2 grid cell in the intertidal zone [9] or choosing an intertidal fringe in a linear direction from five to ten meters deep into the subtidal zone at each location.
Last, the historical distribution edge of F. vesiculosus extends farthest south to the Canary Islands (20 oC winter isotherm) [10-15]. The lack of F. vesiculosus specimen from this area presented by Nicastro et al. [1] prompts us to question the associated genetic findings: Is the southern clade really in danger of extinction? Due to a long-term persistence, the southern-edge populations of F. vesiculosus in the Canary Islands are generally centers of genetic diversity with unique alleles [16,17], suggesting that this area potentially harbor the same genetic lineage that was also identified by Nicastro et al. [1] in North Africa and southern Iberia. Most importantly, F. vesiculosus populations showed significant genetic differentiation at different spatial scales, from stands only 10 m apart to several hundred kilometers distance [18]. Therefore, the so-called ‘vanishing southern lineage’ probably can be shared with the Canary Islands and adjacent areas, thus merely representing a minor part of the detected southern genetic clade in F. vesiculosus.
Range shift: southward expansion or trailing edge contraction?
Although northward expansion in response to global climate warming has been well documented for many intertidal cold-temperate seaweeds [6,19,20], there is less evidence that they are retreating at their southern trailing edge [21]. In reality, recent comparative data showed that F. vesiculosus has expanded 154 km (average rate of 3 km/year) southwards along the Portuguese coast during 1950 and 2000 [20]. Such an observation is in accordance with the most recent modeling species and habitat distribution projections by Jueterbock et al. [22]; they found that the projected southern limit of F. vesiculosus extends to 27oN, which is 5.5o latitude (ca. 780 km) further south than the southernmost record of this species on the Canary Islands. This species may lose most habitats along the Atlantic coast of Africa, Spain and Portugal in 2200. More significantly, a meta-analysis based on distribution shift of 139 seaweed species from Portuguese coastline showed that the detected number of species shifted north or south was precisely the same, indicating that cold-water seaweeds did not show any particular range shifting trend probably driven by chance fluctuations, because the proportion of seaweeds shifting northwards, southwards, or not shifting did not differ from chance (χ2 = 1.93, df = 2, P>0.05) [20]. Likewise, the distributional edge for F. vesiculosus set by salinity in the northern Baltic Sea is expected to shift southwards in the course of ongoing climate change [23]. These researches are entirely contrary to the reported viewpoint of edge contraction by Nicastro et al. [1].
Another point to be raised in this context is SST isotherms, which are undoubtedly important delimiters for biogeographic range shifts of marine macroalgae. However, for F. vesiculosus the climate-induced (0.214 oC/decade) northward latitudinal shift of 1250 km in three decades [1] far surpassed the recorded shift rates available for marine invertebrates and seaweeds. Recent studies suggested that SST isotherms shifted 30-100 km/decade northwards from 1975 to 2005 [24], which is comparable to the latest detected mean range-shift rate at either trailing-edge (15.4 ± 8.7 km/decade) or leading-edge (72 ± 13.5 km/decade) of 857 marine species worldwide [25]. The mentioned geographic contraction of approximately 1250 km [1] is, as far as we are concerned, more likely to be driven by abrupt temperature extreme rather than long-term warming (see discussion below).
Non-climate factors: eutrophication and organic sedimentation
Nicastro et al. [1] reported that the warming trend (0.214 oC/decade) caused a northward latitudinal shift of 1250 km in North Africa and Basque [1]. Interestingly, SST analysis during the similar period indicates that the coastlines of Portugal and North Spain (including Galician, Asturian, Cantabrian and Basque zones) have been warming at an average rate of 0.3-0.4 oC/decade [26], and the English Channel and North Sea have even been warming at a greater rate of 0.5 oC/decade [27]. However, F. vesiculosus populations in these northern adjacent areas did not show mass range contraction. It is therefore not tenable for the viewpoint that the reported disequilibrium of biogeographic change in F. vesiculosus is due to the vulnerable feature of edge populations.
In a marine intertidal zone, the response of species distribution to environmental conditions may be complex and vary geographically, because non-climate variables are also relevant to range shift. Biogeographic studies revealed that the distribution of F. vesiculosus expanded southward along Portugal shores whereas contracted in the Cantabrian sea (Southern Bay of Biscay) under a warming scenario [4,20], suggesting that this species’ distribution range is associated with various environmental factors [9,23]. Therefore, it is quite necessary to evaluate the impact of non-climate factors on geographic shift of F. vesiculosus because recent habitat distribution models suggested that the distribution of two-thirds of intertidal seaweed species (including F. vesiculosus) in Northwestern Iberian Peninsula is correlated with non-climatic factors [9].
Eutrophication effects are not a dispensable biological process contributing to the decline in depth limit of F. vesiculosus over the 20th century [8]. It can both reduce the survival of adult individuals [28] and prevent the establishment F. vesiculosus juveniles [29] by means of decreasing light permeability in deeper littoral zone [7], increasing sedimentation and light with opportunistic filamentous algae [30,31]. High concentrations of nitrate can directly reduce osmotic tolerance of gametes [32], inhibit spore settlement and initial development [33], decrease germination success and delay cell division of zygotes [33], and hinder photosynthetic performance of adults [34]. Eutrophication has already proved to be an important determinant causing the decrease in distribution and abundance or even disappearances of F. vesiculosus from locally polluted areas in the Baltic Sea through affecting the performance of a particular life-history stage [23], including the inner Stockholm Archipelago [35], the Tallinn Bay [36], the Gulf of Gdansk [37], the Helsinki Archipelago and the Gulf of Riga [38].
From an ecological point of view, fucoid plants have short-lived eggs and sperm, and the fertilized eggs disperse poorly before settlement [39]. Numerous data showed that the germlings of F. vesiculosus in early post-settlement stages suffer considerable stress and mortality from sediment and deposited matter [40]. Organic sedimentation in marine intertidal can cover the available substrate and thereby reduce the settlement of F. vesiculosus [41], and this effect has increased substantially due to large-scale eutrophication [42]. Likewise, field and laboratory bioassays showed that sedimentation regimes can strongly influence the distribution patterns of F. vesiculosus at both regional and local scales partly through modifying the recruitment opportunities of propagules [43,44]. In addition, anthropogenic induced contamination reinforced the unbalanced competition for space between fucoids and green algal species [45]. Recent studies demonstrated that the massive occurrence of filamentous algae (e.g. Cladophora glomerata and Pilayella littoralis) which benefit from more eutrophicated enrichment locally have negative effects on the early life-cycle stage of F. vesiculosus, thus leading to declining populations or reduced capability of recruitment [43,46]. In reality, coastal eutrophication in northwest Iberia (e.g. Mondego and Mira estuaries, Portugal) has also been documented [47], but the negative response of F. vesiculosus in this area was less severe than in the southern lineage. In view of long-term ecological disturbance imposed by anthropogenic and natural eutrophication on the Western coasts of the Iberian Peninsula (e.g. Mondego estuary [45]) since 1990s, the conclusion ‘climate-induced species range reduction’ is rushed and arbitrary under the condition that other non-climate factors not directly related to global warming also act as important drivers for range shift of seaweeds [48].
Non-climate factors: coastal habitat erosion
Sea-level rise during the 21st Century is considered as one of the major threats to coastal ecosystems [49]. Historical tide gauge records in Basque, North Spain revealed a consistent sea-level rise of 2-3 mm yr-1 from 1940s to 2000s, and particularly identified sea-level rise of 104 mm at Santander area [50,51]. In comparison with natural erosive processes and the driving forces of global warming during 1954 and 2004, the local anthropogenic activity played a dominant negative role to Basque coastal (southeastern Bay of Biscay) and estuarine habitats in North Spain [51,52]. During the 1954-2004 period among the 18.7 hectares of coast area (2.8% of the intertidal zone) driven by sea-level rise for all of Gipuzkoa, 13.39 hectares of estuaries has been lost, which represents 72% of the overall intertidal zone affected [51]. These results imply that the combination of human-induced physical disturbance and sea-level rise may result in the loss of the southern lineage despite no evidence presented to date. In our opinion, we should take into account the scenario seriously that the degradation and fragmentation of suitable coastal habitat niches can consequently lead F. vesiculosus populations to be fragile and susceptible, and consequently to its disappearance. Similarly, it also reported that coastal urbanization may induce a remarkable Phaeophyceaen species loss and a substantial increase of green algae across a wide latitudinal gradient along the SW Atlantic [53]. Therefore, coastal habitat can not be dismissed as a negligible environmental factor in shaping distribution change of marine intertidal organisms.
Long-term warming vs. abrupt heat-wave
Biogeographic change of intertidal organisms in response to climate is a ratchet-like process, with gradual long-term change punctuated by advances and retreats caused by extreme events [54]. In the northeastern Atlantic, sub-lethal effects of water temperature seems to play a dominant role in setting the distributional limits of most warm and cold-water seaweed species through reduced reproduction and growth [34,40], including F. vesiculosus [55]. Thus, loosely or arbitrarily linking the parallel occurred long-term warming and range contraction of individual seaweed species can be problematic if we are short of relevant mechanistic knowledge of sub-lethal stresses [56]. In particular, the most recent studies demonstrated that the marine heat wave of 2011 along the warm temperate western coast of Australia (a warming anomaly ≥ 2.0 oC) led to a significant reduction in the abundance of benthic seaweeds (e.g. canopy-former Scytothalia dorycarpa) and sessile invertebrates, resulting in a subsequent shift in species distribution and ecosystem structure [57,58]. We then may ask if temperature extremes also played an analogous role in contribution to the range shift of F. vesiculosus.
As expected, numerous climatic indices revealed statistically significant increments of extreme heat events for spring and summer over Portugal in the period of 1976-2006 [59]. Specifically, two prominent temperature extremes occurred in the Iberian Peninsula and the Atlantic North Africa since 2000. The first heat wave was 2003, which yielded large positive anomalies (> 2.0 oC) along the Atlantic North Africa coastlines [60], and affected several thousand kilometers of coastline, leading to extensive mass mortality of at least 25 rocky benthic macro-invertebrate species in the entire Northwestern Mediterranean region [61]. The second unusually occurred in a row (warm summer followed by cold winter in 2009-2010), leading to largest biogeographic consequences for F. vesiculosus because it suffers regional adult population reduction below their thresholds for persistence or range extension by recruitment [62,63]. The extreme temperatures far exceed the lethal threshold of individuals within marginal populations, as a key physiological process could not be maintained under prolonged heat wave conditions [58].
Taken all together, the distributional range of F. vesiculosus in the Eastern Atlantic is in a process of reorganization as a consequence of species introductions and stress in relation to long-term climate warming and abrupt temperature extremes, eutrophication, and anthropogenic-mediated impacts. The accumulation of climatic and non-climatic effects acting in a non-linear manner could suddenly move forwards a tipping point and major regime shift on its biogeographic distribution [64,65]. A continuous study should characterize the underlying linear and/or nonlinear relationships between seaweed performance and enough temperatures across a wide biogeographic range [56]. It is also essential to gather and keep up to date accurate records of a large number of sympatric species distributions in order to empirically identify the coastal structure change under global warming scenarios.
Acknowledgements
This work was supported by National Natural Science Foundation of China (31000103 and 31370264).
Authors’ contributions
Z. M. Hu, L. B. Juan and D. L. Duan contributed to the conception and coordination of this commentary. Z. M. Hu conducted literature search and drafted the first text version. L. B. Juan and D. L. Duan made corrections. All authors read and approved the final version of this manuscript.
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Competing interests
The authors declare that they have no competing interests.
Did global warming really cause range contraction and genetic erosion of brown seaweed Fucus vesiculosus? A close look at sampling, biological process, and anthropogenic impact
16 April 2014
Zi-Min Hu1, Lopez-Bautista Juan2 and De-Lin Duan1
1Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China.
2Department of Biological Sciences, The University of Alabama, Tuscaloosa, AL35487, USA.
Background
Linking the distribution shift of species to recent global warming may shed light on future geographical range of species under climate change and offer pivotal conservation insights for sustainable biodiversity. The recent BMC Biology article by Nicastro et al. [1] combined temporal changes of distribution range of canopy-forming seaweed Fucus vesiculosus with historical sea surface temperature (SST) during 1982 – 2011 and genetic data (five microsatellites and 12 populations), to unravel the influence of climate warming on the distribution pattern along Iberian and Atlantic North African coastlines and associated evolutionary consequence. Their main result states that ‘a remarkable climate-induced species range reduction is driving a cryptic genetic clade (southern clade) to extinction’. We generally agree with the point that global warming is responsible for the contraction of F. vesiculosus in its geographic range. However, to the extent of our knowledge, several interactive environmental variables can contribute to species distribution in the context of increasing anthropogenic impact on coastal ecosystem. In particular, this article provides no direct physiological evidence regarding the sub-lethal performance of F. vesiculosus in response to long-term or abrupt thermal stress. We will discuss potential bias of incomplete sampling and highlight some overlooked factors contributing to range shift of F. vesiculosus reported by Nicastro et al. [1] in view of recent relevant findings.
Sampling coverage and a vanishing genetic lineage
F. vesiculosus is characterized by different depth distributions and ecological niches varying from tidal marshes to exposed rocky intertidal and shallow subtidal shores. The current field survey of eighty-four moderately wave-exposed and estuarine locations from Hondarribia to Dakhla [1] may be good sampling cover but geographically irregular and scattered (e.g. habitat coverage in elevation), and thus may bias the subsequential genetic investigation at population level.
First, Nicastro et al. [1] reported that population LX from Morocco was extinct in 2009, such a conclusion is questionable because recent field investigation indicated that F. vesiculosus still can be collected from the same geographic site [2]. This discrepancy may stem from the species’ variable and cryptic living habitats at the southern edge. For instance, from Northern Portugal southwards towards Morocco F. vesiculosus disappears from the open coast, whereas occurs only inside estuaries and coast lagoons where no other Fucus species is present (allopatric range) [3]. In addition, some “relict” Fucus populations which reflect the permanence of species left behind the retreating margin during warming periods [4], can just occur in some cryptic sites outside its “normal” range including isolated and wave-sheltered estuaries [5], which has been confirmed recently in San Vicente de la Barquera or Tapia Port, North Spain [6]. Thus Nicastro et al. [1] probably missed some important geographic samplings. Increased sampling from these areas may concrete the observed conclusion that population biomass of F. vesiculosus has reduced mostly in the southern areas.
Second, F. vesiculosus can dominate the subtidal hard-bottom areas down to 4.0 – 9.0 m depth [7,8], and Nicastro et al. [1] sampled only two sites from 500 m to 1 km apart for each locality; thus this sampling approach did not take into account depth gradient and thus may lead to a rough generalization. To minimize the bias of sampling, we therefore advocate that more deliberate sampling methods should be designed and conducted at both transection (width) and longitudinal-section (depth) scales, such as covering a 1-km2 grid cell in the intertidal zone [9] or choosing an intertidal fringe in a linear direction from five to ten meters deep into the subtidal zone at each location.
Last, the historical distribution edge of F. vesiculosus extends farthest south to the Canary Islands (20 oC winter isotherm) [10-15]. The lack of F. vesiculosus specimen from this area presented by Nicastro et al. [1] prompts us to question the associated genetic findings: Is the southern clade really in danger of extinction? Due to a long-term persistence, the southern-edge populations of F. vesiculosus in the Canary Islands are generally centers of genetic diversity with unique alleles [16,17], suggesting that this area potentially harbor the same genetic lineage that was also identified by Nicastro et al. [1] in North Africa and southern Iberia. Most importantly, F. vesiculosus populations showed significant genetic differentiation at different spatial scales, from stands only 10 m apart to several hundred kilometers distance [18]. Therefore, the so-called ‘vanishing southern lineage’ probably can be shared with the Canary Islands and adjacent areas, thus merely representing a minor part of the detected southern genetic clade in F. vesiculosus.
Range shift: southward expansion or trailing edge contraction?
Although northward expansion in response to global climate warming has been well documented for many intertidal cold-temperate seaweeds [6,19,20], there is less evidence that they are retreating at their southern trailing edge [21]. In reality, recent comparative data showed that F. vesiculosus has expanded 154 km (average rate of 3 km/year) southwards along the Portuguese coast during 1950 and 2000 [20]. Such an observation is in accordance with the most recent modeling species and habitat distribution projections by Jueterbock et al. [22]; they found that the projected southern limit of F. vesiculosus extends to 27oN, which is 5.5o latitude (ca. 780 km) further south than the southernmost record of this species on the Canary Islands. This species may lose most habitats along the Atlantic coast of Africa, Spain and Portugal in 2200. More significantly, a meta-analysis based on distribution shift of 139 seaweed species from Portuguese coastline showed that the detected number of species shifted north or south was precisely the same, indicating that cold-water seaweeds did not show any particular range shifting trend probably driven by chance fluctuations, because the proportion of seaweeds shifting northwards, southwards, or not shifting did not differ from chance (χ2 = 1.93, df = 2, P>0.05) [20]. Likewise, the distributional edge for F. vesiculosus set by salinity in the northern Baltic Sea is expected to shift southwards in the course of ongoing climate change [23]. These researches are entirely contrary to the reported viewpoint of edge contraction by Nicastro et al. [1].
Another point to be raised in this context is SST isotherms, which are undoubtedly important delimiters for biogeographic range shifts of marine macroalgae. However, for F. vesiculosus the climate-induced (0.214 oC/decade) northward latitudinal shift of 1250 km in three decades [1] far surpassed the recorded shift rates available for marine invertebrates and seaweeds. Recent studies suggested that SST isotherms shifted 30-100 km/decade northwards from 1975 to 2005 [24], which is comparable to the latest detected mean range-shift rate at either trailing-edge (15.4 ± 8.7 km/decade) or leading-edge (72 ± 13.5 km/decade) of 857 marine species worldwide [25]. The mentioned geographic contraction of approximately 1250 km [1] is, as far as we are concerned, more likely to be driven by abrupt temperature extreme rather than long-term warming (see discussion below).
Non-climate factors: eutrophication and organic sedimentation
Nicastro et al. [1] reported that the warming trend (0.214 oC/decade) caused a northward latitudinal shift of 1250 km in North Africa and Basque [1]. Interestingly, SST analysis during the similar period indicates that the coastlines of Portugal and North Spain (including Galician, Asturian, Cantabrian and Basque zones) have been warming at an average rate of 0.3-0.4 oC/decade [26], and the English Channel and North Sea have even been warming at a greater rate of 0.5 oC/decade [27]. However, F. vesiculosus populations in these northern adjacent areas did not show mass range contraction. It is therefore not tenable for the viewpoint that the reported disequilibrium of biogeographic change in F. vesiculosus is due to the vulnerable feature of edge populations.
In a marine intertidal zone, the response of species distribution to environmental conditions may be complex and vary geographically, because non-climate variables are also relevant to range shift. Biogeographic studies revealed that the distribution of F. vesiculosus expanded southward along Portugal shores whereas contracted in the Cantabrian sea (Southern Bay of Biscay) under a warming scenario [4,20], suggesting that this species’ distribution range is associated with various environmental factors [9,23]. Therefore, it is quite necessary to evaluate the impact of non-climate factors on geographic shift of F. vesiculosus because recent habitat distribution models suggested that the distribution of two-thirds of intertidal seaweed species (including F. vesiculosus) in Northwestern Iberian Peninsula is correlated with non-climatic factors [9].
Eutrophication effects are not a dispensable biological process contributing to the decline in depth limit of F. vesiculosus over the 20th century [8]. It can both reduce the survival of adult individuals [28] and prevent the establishment F. vesiculosus juveniles [29] by means of decreasing light permeability in deeper littoral zone [7], increasing sedimentation and light with opportunistic filamentous algae [30,31]. High concentrations of nitrate can directly reduce osmotic tolerance of gametes [32], inhibit spore settlement and initial development [33], decrease germination success and delay cell division of zygotes [33], and hinder photosynthetic performance of adults [34]. Eutrophication has already proved to be an important determinant causing the decrease in distribution and abundance or even disappearances of F. vesiculosus from locally polluted areas in the Baltic Sea through affecting the performance of a particular life-history stage [23], including the inner Stockholm Archipelago [35], the Tallinn Bay [36], the Gulf of Gdansk [37], the Helsinki Archipelago and the Gulf of Riga [38].
From an ecological point of view, fucoid plants have short-lived eggs and sperm, and the fertilized eggs disperse poorly before settlement [39]. Numerous data showed that the germlings of F. vesiculosus in early post-settlement stages suffer considerable stress and mortality from sediment and deposited matter [40]. Organic sedimentation in marine intertidal can cover the available substrate and thereby reduce the settlement of F. vesiculosus [41], and this effect has increased substantially due to large-scale eutrophication [42]. Likewise, field and laboratory bioassays showed that sedimentation regimes can strongly influence the distribution patterns of F. vesiculosus at both regional and local scales partly through modifying the recruitment opportunities of propagules [43,44]. In addition, anthropogenic induced contamination reinforced the unbalanced competition for space between fucoids and green algal species [45]. Recent studies demonstrated that the massive occurrence of filamentous algae (e.g. Cladophora glomerata and Pilayella littoralis) which benefit from more eutrophicated enrichment locally have negative effects on the early life-cycle stage of F. vesiculosus, thus leading to declining populations or reduced capability of recruitment [43,46]. In reality, coastal eutrophication in northwest Iberia (e.g. Mondego and Mira estuaries, Portugal) has also been documented [47], but the negative response of F. vesiculosus in this area was less severe than in the southern lineage. In view of long-term ecological disturbance imposed by anthropogenic and natural eutrophication on the Western coasts of the Iberian Peninsula (e.g. Mondego estuary [45]) since 1990s, the conclusion ‘climate-induced species range reduction’ is rushed and arbitrary under the condition that other non-climate factors not directly related to global warming also act as important drivers for range shift of seaweeds [48].
Non-climate factors: coastal habitat erosion
Sea-level rise during the 21st Century is considered as one of the major threats to coastal ecosystems [49]. Historical tide gauge records in Basque, North Spain revealed a consistent sea-level rise of 2-3 mm yr-1 from 1940s to 2000s, and particularly identified sea-level rise of 104 mm at Santander area [50,51]. In comparison with natural erosive processes and the driving forces of global warming during 1954 and 2004, the local anthropogenic activity played a dominant negative role to Basque coastal (southeastern Bay of Biscay) and estuarine habitats in North Spain [51,52]. During the 1954-2004 period among the 18.7 hectares of coast area (2.8% of the intertidal zone) driven by sea-level rise for all of Gipuzkoa, 13.39 hectares of estuaries has been lost, which represents 72% of the overall intertidal zone affected [51]. These results imply that the combination of human-induced physical disturbance and sea-level rise may result in the loss of the southern lineage despite no evidence presented to date. In our opinion, we should take into account the scenario seriously that the degradation and fragmentation of suitable coastal habitat niches can consequently lead F. vesiculosus populations to be fragile and susceptible, and consequently to its disappearance. Similarly, it also reported that coastal urbanization may induce a remarkable Phaeophyceaen species loss and a substantial increase of green algae across a wide latitudinal gradient along the SW Atlantic [53]. Therefore, coastal habitat can not be dismissed as a negligible environmental factor in shaping distribution change of marine intertidal organisms.
Long-term warming vs. abrupt heat-wave
Biogeographic change of intertidal organisms in response to climate is a ratchet-like process, with gradual long-term change punctuated by advances and retreats caused by extreme events [54]. In the northeastern Atlantic, sub-lethal effects of water temperature seems to play a dominant role in setting the distributional limits of most warm and cold-water seaweed species through reduced reproduction and growth [34,40], including F. vesiculosus [55]. Thus, loosely or arbitrarily linking the parallel occurred long-term warming and range contraction of individual seaweed species can be problematic if we are short of relevant mechanistic knowledge of sub-lethal stresses [56]. In particular, the most recent studies demonstrated that the marine heat wave of 2011 along the warm temperate western coast of Australia (a warming anomaly ≥ 2.0 oC) led to a significant reduction in the abundance of benthic seaweeds (e.g. canopy-former Scytothalia dorycarpa) and sessile invertebrates, resulting in a subsequent shift in species distribution and ecosystem structure [57,58]. We then may ask if temperature extremes also played an analogous role in contribution to the range shift of F. vesiculosus.
As expected, numerous climatic indices revealed statistically significant increments of extreme heat events for spring and summer over Portugal in the period of 1976-2006 [59]. Specifically, two prominent temperature extremes occurred in the Iberian Peninsula and the Atlantic North Africa since 2000. The first heat wave was 2003, which yielded large positive anomalies (> 2.0 oC) along the Atlantic North Africa coastlines [60], and affected several thousand kilometers of coastline, leading to extensive mass mortality of at least 25 rocky benthic macro-invertebrate species in the entire Northwestern Mediterranean region [61]. The second unusually occurred in a row (warm summer followed by cold winter in 2009-2010), leading to largest biogeographic consequences for F. vesiculosus because it suffers regional adult population reduction below their thresholds for persistence or range extension by recruitment [62,63]. The extreme temperatures far exceed the lethal threshold of individuals within marginal populations, as a key physiological process could not be maintained under prolonged heat wave conditions [58].
Taken all together, the distributional range of F. vesiculosus in the Eastern Atlantic is in a process of reorganization as a consequence of species introductions and stress in relation to long-term climate warming and abrupt temperature extremes, eutrophication, and anthropogenic-mediated impacts. The accumulation of climatic and non-climatic effects acting in a non-linear manner could suddenly move forwards a tipping point and major regime shift on its biogeographic distribution [64,65]. A continuous study should characterize the underlying linear and/or nonlinear relationships between seaweed performance and enough temperatures across a wide biogeographic range [56]. It is also essential to gather and keep up to date accurate records of a large number of sympatric species distributions in order to empirically identify the coastal structure change under global warming scenarios.
Acknowledgements
This work was supported by National Natural Science Foundation of China (31000103 and 31370264).
Authors’ contributions
Z. M. Hu, L. B. Juan and D. L. Duan contributed to the conception and coordination of this commentary. Z. M. Hu conducted literature search and drafted the first text version. L. B. Juan and D. L. Duan made corrections. All authors read and approved the final version of this manuscript.
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Competing interests
The authors declare that they have no competing interests.