Next Article in Journal
Environmental Drivers and Aquatic Ecosystem Assessment of Periphytic Algae at Inflow Rivers in Six Lakes over the Yangtze River Basin
Previous Article in Journal
A Study on the Online Attention of Emergency Events of Torrential Rain in Shanxi and Henan
Previous Article in Special Issue
Epiphyton in Agricultural Streams: Structural Control and Comparison to Epilithon
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Communication

Gone and Back—The Anthropogenic History of Coccotylus brodiei (Turner) Kützing and Furcellaria lumbricalis (Hudson) J.V. Lamouroux in the Gulf of Gdańsk (Southern Baltic Sea)

Faculty of Oceanography and Geography, Institute of Oceanography, University of Gdańsk, Al. Piłsudskiego 46, 81-378 Gdynia, Poland
*
Author to whom correspondence should be addressed.
Water 2022, 14(14), 2181; https://doi.org/10.3390/w14142181
Submission received: 13 June 2022 / Revised: 29 June 2022 / Accepted: 8 July 2022 / Published: 10 July 2022
(This article belongs to the Special Issue Phytoplankton and Phytobenthos: From Freshwater to Marine Ecosystems)

Abstract

:
The Gulf of Gdańsk environment has supported the development and growth of the local community for centuries but has been significantly degraded as a result of the progressive eutrophication process that started in 1960, the extensive exploitation of marketable species (plants and fish) and pollution limiting the growth of marine organisms. Multistressors of the Anthropocene era have left their mark on all aspects of the ecosystem, but despite this, the gulf region has been considered to have exceptional environmental value and high biodiversity in comparison with adjacent regions. In 2004, a Natura 2000 site was created in the eastern part known as Puck Bay, and actions were taken to protect endangered habitats and species. Between 2019 and 2020, intensive field studies were conducted in Puck Bay on flora to assess biodiversity and habitat resources. The material was collected for qualitative and quantitative analysis. This allowed observation of species that have not been reported since the 1970s, i.e., Coccotylus brodiei (Turner) Kützing and Furcellaria lumbricalis (Hudson) J.V. Lamouroux. Both species co-occurred as in the period before the 1960s in the form of free-floating thalli. The rediscovery of these taxa suggests that despite very unfavourable conditions for their development due to anthropogenic pressures, they were able to survive, and their occurrence throughout Puck Bay indicates improvement in environmental quality due to declining human impact. Our results indicate that benthic algal communities have high regeneration potential, but in the case of severe environmental degradation caused by synergistic pressures of high intensity, plant recovery without measures to support remediation takes at least 30 years.

1. Introduction

The Gulf of Gdańsk has been significantly degraded as a result of extensive exploitation of marketable species (plants and fish) from late 1950 to 1970 combined with strong eutrophication and pollution limiting the growth of organisms [1,2,3,4,5]. Multifaceted pressures contributed to the disappearance of economically valuable species, e.g., in Puck Bay (shallow-water basin of the Gulf of Gdańsk), Fucus vesiculosus Linnaeus, was last observed in 1977 and Furcellaria lumbricalis in 1979, and a reduction in the total phytobenthos biomass by 15.6% between 1979 and 1987. Impoverished communities were dominated by Pylaiella littoralis (Linnaeus) Kjellman and Ectocarpus siliculosus (Dillwyn) Lyngbye (Ectocarpaceae) as well as Zannichellia palustris L. (Spermatophyta) [5]. Despite this, the Gulf of Gdańsk, especially the eastern part of Puck Bay, is still considered a region of exceptional environmental conditions (low mean depth of 2 m, stable low salinity of approximately 7 PSU and relatively low waves and weak currents) and high biodiversity in comparison with adjacent regions [6]. Therefore, to protect endangered habitats and species, the lagoon has been designated as a Special Protection Area (PLB 220005) and Special Area of Conservation (PLH 220032) as described in the EU-wide network of nature protection areas Natura 2000, and actions were taken to protect the environment and endangered habitats and species, e.g., construction of sewage treatment plants and restitution programs of fish and Zostera marina (Spermatophyta). The regeneration of some ecosystem elements and a general increase in water quality in the region have been confirmed by scientific research [7,8] and the reports of the National Monitoring Programme [9], but some fish stocks are in strong decline due to overfishing and bacterial infections [9,10,11].
In this paper, we present the results of new observations of two Rhodophyta species considered absent from the Puck Bay region, i.e., Coccotylus brodiei and Furcellaria lumbricalis, for approximately 40 years. In addition to the morphological description of the currently observed representatives of both species, we present the history of observations and possible reasons for the disappearance of both species.

2. Materials and Methods

Intensive field studies were conducted in Puck Bay (western shallow-water part of the Gulf of Gdańsk) on benthic flora to assess biodiversity and habitat resources. The material for qualitative and quantitative analysis was collected at 62 sites (Figure 1) between 20 August 2019 and 20 September 2020. All samples were taken using diving techniques with the assistance of the RIB (Rigid Inflatable Boat). At all stations, at least 4 subsamples were collected for quantitative analysis using the aluminum frame with sides 20 cm × 20 cm, and reconnaissance was performed within a radius of approximately 50 m from the place where the samples were collected for qualitative analysis to learn about species richness and to make photographic documentation. All subsamples were put in plastic bags and transported to the laboratory in a cool box. The plant material was identified and sorted in the laboratory within 2 days. The fieldwork and laboratory work methods were carried out according to the recommendations of the Polish National Monitoring Programme [12]. The collection of samples and storage of specimens was carried out with the permission of the Regional Director for Environmental Protection in Gdańsk (RDOŚ-Gd-WZG.6400.228.2018.AB.2). Additional underwater observations by a free-diver with experience in the identification of benthic flora took place in September 2021.
The morphological identification of macroalgae was based mostly on local key floras [13,14,15] and widely recognized literature [16,17]. Morphological analysis to properly identify a representative Phyllophoraceae (between Coccotylus brodiei and C. truncatus (Pallas) M.J.Wynne & J.N.Heine 1992) was based on the Lundsteen and Nielsen paper [18]. Formal identification of the plant material used in this study was undertaken by A. Zgrundo and I. Złoch. A voucher specimen of this material has been deposited and is available in the Herbarium Division of Marine Biology and Ecology, University of Gdańsk (contact person: [email protected]).
Maps included in the manuscript were made in QuantumGis ver 3.16, (QGIS.org, 2022. QGIS Geographic Information System. QGIS Association).

3. Results

During field studies, two representatives of Rhodophytes, i.e., Coccotylus brodiei (Figure 2) and Furcellaria lumbricalis (Figure 3) (both belonging to separate families within the order Gigartinales) were observed that have not been reported in Puck Bay since 1979. Both species were observed in the form of free-floating thalli (Figure 4) in areas where flora covered 80–100% of the bottom.
Coccotylus brodiei (Turner) Kützing 1843 is the name currently accepted taxonomically [19]. The taxon was described as Fucus brodiei by Turner in 1809. A recent taxonomic revision placed this taxon as a form of Coccotylus truncatus f. brodiei (Turner) M.J.Wynne & Heine 1992. However, modern taxonomy of Coccotylus genus distinguishes C. briodiei and C. truncatus as separate species, as they were previously considered single. It has been proven by DNA barcode analyses and different kinds of growth [20]. Some papers also report forms of loose growing individuals [21,22]; however, when we think about the smallest taxonomic category, some minor variations still require clarification. Cryptic diversity within the genera Coccotylus has been partially revealed [20]; however, generic boundaries in the Phyllophoraceae still remain a challenge for modern molecular methods.
The name of C. truncatus is based on Fucus truncatus Pall. but it was Zinova (1955) [23] who attributed F. truncatus to Phyllophora, and a new combination of Phyllophora truncata was presented. The name Coccotylus brodiei was resurrected based on molecular analysis (Turner) Kützing [20] previously recognized as Phyllophora truncata (Pallas) comb. nov. forma brodiaei (Turner) [24].
It was emphasized that C. brodiei and C. truncatus can be difficult to distinguish from one another due to their variation [20]. Features more usual for or typical of C. brodiei may be found in C. truncatus and the other way around [20]. However, compared to the variation in multiple leaf shapes of C. brodiei, the relative uniformity in C. truncatus is noticeable. Intergrading forms between C. brodiei and C. truncatus cannot also be excluded, as such forms have been previously found in Canada [24]. In the present investigation, C. truncatus individuals were not found.
Typical morphological features of C. brodiei collected in the Gulf of Gdańsk include the repeatedly branched leafy bushes up to 15 cm high, red-brown and lightly coloured in new parts and darker in older parts. Branches in the form of stipitate leaves spring from all parts of the plants, and the blades are typically dichotomously divided into two lobes attenuated to a pointed apex. The loose growing forms of C. brodiei (Figure 2) morphologically are consistent with the C. brodiei f. ligulata (C. Agardh) Sjöstedt description [18].
Furcellaria lumbricalis (Hudson) J.V. Lamouroux 1813 is the name of an entity that is currently accepted taxonomically, but it was described as Fucus lumbricalis by Hudson in 1762. Since then, 15 synonyms of the taxon have appeared [19]. One of the most popular was Furcellaria fastigiata (Turner) J.V. Lamouroux 1813 widely used in the 20th century.
The genus Furcellaria is less diverse than genus Coccotylus. It consists of one species Furcellaria lumbricalis (Hudson) J.V. Lamouroux 1813, previously also known as Furcellaria fastigiata or Furcellaria fastigiata f. aegagropila (special unattached form in the Baltic Sea, in this paper both names are used interchangeable for the unattached form). Other variations or forms have not been reported in the Baltic, and currently the taxonomic position of Furcellaria is not a subject of any change.
Although Furcellaria lumbricalis, like C. brodiei, is also subject to phenotypic variation, thalli examined in this study reflected the general taxonomic description, i.e., consisted of clumps of firm, cylindrical, dichotomously branched fronds arising from a holdfast of intertwined rhizoidal strands (stolons) (Figure 3). Their colour was dark red to brown, sometimes with greenish-purple or greenish-brown tips. Free-living F. lumbricalis is generally referred to as asf. aegagropila. It differs morphologically from the typical attached form in several respects: its globose thallus of radiating fronds, its smaller stature and frond diameter, its general lack of haptera, its denser and more irregular branching, and its ability to produce adventitious lateral proliferations. In the present study, F. lumbricalis individuals who were loosely lying or drifting matched morphologically to the free-living form F. lumbricalis (=f. aegagropila).
The observations and analysis of the representatives of Coccotylus brodiei and Furcellaria lumbricalis carried out in the summer of 2019 and 2021 in Puck Bay showed that both taxa were present in limited areas outside the previous maximum population range at depths between 2 and 3 m, and the plants themselves remained in good condition. The number of individuals and their total biomass was low. We estimated C. brodiei dry weight at 0.09 g·m2 (near Rewa) and 0.03 g·m2 (near Swarzewo) and F. lumbricalis at 3.17 g·m2 (near Rewa), but during underwater observations in 2021, both taxa were identified in the next three sites at depths between 1.7 and 3.7 m. Moreover, in the vicinity of Puck, we found a habitat where representatives of both species together with another species considered extinct, i.e., Fucus vesiculosus, occurred in larger numbers. This habitat is under archaeological protection and is avoided by fishermen and sailors because of its shallow depth and the bottom riddled with the remains of a medieval harbour. In all probability, this is the refugium we have been looking for, but to confirm this information with certainty, a focused field survey should be conducted.

4. Discussion

4.1. The State of Populations in the 20th Century

The occurrence of Furcellaria lumbricalis form aegagropila (formerly named Furcellaria fastigiata (Turner) J.V. Lamouroux) together with Coccotylus brodiei was estimated in 1957 and 1968 to be approximately half of the Puck Bay region (Figure 5). According to estimates from 1957, the fresh weight of Furcellaria lumbricalis was 148 g·m2–728 g·m2 (in the region planned for exploitation on average 467 g·m2) and that of Coccotylus brodiei was 1–14 g·m2 [25].
After publication showing that Furcellaria’s total resources amount to 11,500 t and can generate a profit of PLN 280 million [25] (currently approximately PLN 889 million (€ 192 million) [26]), interest in obtaining Furcellaria lumbricalis for industrial purposes significantly increased, and a programme for processing seaweed and obtaining agar and alginic acid was developed. It was established that without disturbing the biological balance of long-term exploitation, approximately 3000 tons of seaweed could be caught annually. Exploitation of Furcellaria lumbricalis started in 1963, and by the end of 1969, only 3388 tons of seaweed had been extracted [27], i.e., 35% of the established limit quantity from 11,500 tons of total resources estimated by other authors [25]. The exploitation ended in 1972 after the production of agar–agar was stopped due to an increase in the heavy metal content in thalli exceeding the contemporary limit values and drastically decreasing the biomass of seaweeds, which was explained by plant dwarfing as the effect of pollutants.
In summer 1977, Furcellaria lumbricalis was found only at a few stations (Figure 5) with fresh weights of 1.41 g·m2–713.46 g·m2 (0.10 g·m2–128.25 g·m2 dry weight). For comparison, in some Baltic subareas (reported by different unpublished sources and personal communications until 2000 after [28]), the average biomass of F. lumbricalis ranges from 90 g·m2 to 691 g·m2 and is reported to be clearly overestimated due to sampling from the maximum cover. Similarly, Coccotylus brodiei had a much smaller fresh weight than earlier −0.06 g·m2–167.85 g·m2 (=0.01 g·m2–36.21 g·m2 dry weight) [4]. A drastic decrease in the quantity of Furcellaria lumbricalis in 1979 and its absence in 1987 and 1988 was recorded [5]. The situation in Estonia had a different dynamic. F. lumbricalis and C. truncatus biomass described in the early 1960s was estimated to be 150,000 t wet weight [29] and in the 1970s 140,000 t ww [30]. During the 1980s and 1990s, a remarkably lower total biomass was observed, which was probably caused by an overgrowth of the opportunistic filamentous brown alga Pylaiella littoralis. This was followed by a recovery of the total biomass, and since 2011, F. lumbricalis stocks in Estonia have remained stable and were estimated to be 179,000 t ww in 2017. On average, Furcellaria lumbricalis accounts for 60–73% and Coccotylus truncatus accounts for 13–25% of the total community biomass [28].
The reasons for the disappearance of some plant species in Puck Bay, including Coccotylus brodiei, Fucus vesiculosus, and Furcellaria lumbricalis, and for limiting the range of others, e.g., Zostera marina, were given in most cases as pollution and strong eutrophication in the 1980s. These factors led to changes in trophic conditions, reduced water transparency, and the disappearance of sensitive plant species followed by the mass appearance of Ectocarpacae (Pylaiella littoralis) in their place [3,4,5,27,31].
In the study prepared on data from 2007 [6] (p. 122), soft bottoms devoid of vegetation were mainly observed in the area of primary occurrence of Furcellaria lumbricalis (compare with Figure 5).
Thus, we hypothesize that the primary cause of the disappearance of species was overexploitation and simultaneous destruction of their habitats on which the effects of eutrophication and pollution overlapped, particularly evident in the 1980s and 1990s [7]. The tool for exploiting macroalgae resources was an industrial dredge towed behind a fishing vessel [2]. This type of exploitation is considered to be very harmful to the vegetation on soft bottoms as not only free-floating forms are removed, as C. brodiei and F. lumbricalis in our case, but also the surface layer of sediment with rooted plants which are often key species for such habitats [32,33,34]. The disturbed rooted vegetation recovery rates depend on exploitation density and can take on average 11 years to match pre-exploitation standards as in the case of Zostera marina beds in Maine [35]. The recolonization of degraded habitats is regarded to be dependent on the quality of habitat which remained following a dredging episode, but what must be emphasized in the case of total removal of rooted plants is that recolonization will not occur [32,34].
Currently, it is difficult to reach out to witnesses of seaweed harvesting in Puck Bay, but few reports confirm that the seabed was overexploited. One of the divers described traces of the industrial dredge used for harvesting in his memoirs as follows: “What we saw underwater looked like a trace of a combine harvester picking grain and planting potatoes simultaneously. We did not think about the environmental impact of this overharvesting of the seabed as it was used at the time. Our task was to determine where the largest concentrations of this seaweed were located so that their subsequent exploitation could be as easy as possible” (Anonymous 2009). Taking into account the reported condition of the bottom of Puck Bay and literature data on damage caused by dredging of soft bottoms covered with vegetation [32,33,34,35], we may assume that the natural habitats of C. brodiei and F. lumbricalis were severely damaged.
Data from experiments [1] suggested that F. lumbricalis showed the highest biomass growth rate of approximately 15–16% in early summer (June–July) and between 7–13% in the remaining months. The geometric mean of the monthly biomass increase calculated by us based on those data [1] was 11%. This means that if industrial harvesting was carried out for a period of five months from May to October [2], the possibility of population biomass recovery was violated if at least in one month more than 11% of the biomass estimated at 11,500 t, i.e., more than 1610 t from the annual limit of 3000 t, was caught. With a minimum biomass increment of 7%, 9% of the stock, i.e., 1035 t, could be harvested without disturbing its regeneration capacity. The slow growth of F. lumbricalis in comparison to other red algae was also stated by other authors [36]. The low recovery rate was further affected by the lack of ability of F. lumbricalis present in the Puck Bay basin to develop generative organs [1]. The free-floating form Furcellaria lumbricalis form. aegagropila reproduces only vegetatively through fragmentation, regeneration, and proliferation [37]. Proliferation, where propagules develop on the parent plant and then detach, is probably the most important mechanism. Recruitment usually occurs on a much more local scale, typically within 10 m of the parent plant. Hence, it is expected that Furcellaria lumbricalis would normally only be recruited from local populations. The recovery would be even more protracted in isolated areas. Given the slow growth of the attached F. lumbricalis, time to maturity (4–6 years), and limited dispersal, recoverability of the epilithic form of Furcellaria lumbricalis is assessed as moderate [37]. The growth rate of free-floating F. lumbricalis is reported to be slower than that of the attached form; therefore, it may be outcompeted by the attached form in shallower habitats with better light conditions. However, in deeper waters, the free-floating form performs better [38]. Furthermore, because of its sterility and reproduction by fragmentation, the regeneration capacity of the free-floating form is regarded as low [39]. Recently, it was demonstrated that the growth of red algae is highly density-dependent; thus, the biomass pattern of the drifting F. lumbricalis is likely determined by the share of C. truncatus in the community [40].
Some authors suggest that intensive harvesting in the past decimated the drifting Furcellaria stocks in central Kattegat [28]. The presence of C. brodiei and F. lumbricalis was recently confirmed in other exploited sites on the Swedish coast in both the Kattegat and the Skagerrak [41] and on the German coast [42]. Currently, in the Baltic Sea, the only stable free-floating populations of taxa in question enabling harvesting are restricted to Estonia [28].
Despite the intensive studies carried out in the 1970s and 1980s, no Coccotylus brodiei or Furcellaria lumbricalis form. aegagropila were found in the Puck Bay area. Over the years, it was believed that seaweeds together with another exploited taxon, Fucus vesiculosus, were completely extinct in the Polish zone of the Baltic Sea. Only in the 1990s, during amateur explorations, did divers find epilitic forms of Furcellaria lumbricalis in remote sites on the boulders of the Slupsk Bank and near Gdynia Orłowo [27]. Since the publication presenting data from the 1980s [5], no free-floating form in the Polish Baltic Sea zone has been observed, and some authors assumed that natural recovery of Furcellaria lumbricalis form. aegagropila in Puck Bay, even if environmental conditions are improved, is highly improbable [43].

4.2. The State of Populations in the 21st Century

Both species, Coccotylus brodiei and Furcellaria lumbricalis, are subject to phenotypic variation and pose several morphological ecotypes. The comparisons with a collection material stored in the herbarium at the University of Gdańsk suggest that thalli examined in our study show the same features as specimens collected in the 1970s before the collapse of populations. In addition, observations in the environment are in agreement with historical reports—typical free-floating form of growth and co-existence of populations [3,44]. In the present investigation, C. truncatus individuals were not found. A probable reason for the reduced development of C. truncatus in the Gulf of Gdańsk could be the relatively high temperatures compared to its predominately northern distribution [20] and possibly the reduced salinities [45].
The observations in the 1940s recorded the presence of both taxa at depths of 2.5 m–4 m [44], and in the 1950s, they were found at depths of 4 m and below [25]. Currently, taxa were observed at depths ranging from 1.7 to 3.7 m, but it should be emphasized that in our case deeper stations are under-represented.
Although at present both species are rarely observed underwater and their biomass in our estimates is 100 to 1000 times lower than before their exploitation began in the 1960s, [25] there are further signs documenting the beginnings of populations recovery, e.g., thalli of both taxa have been regularly observed on the beach in section Rewa-Beka over the last three years. Additionally, thalli of another species considered to be extinct, i.e., Fucus vesiculosus, is observed in this section, and in the section Swarzewo-Gnieżdżewo together with Coccotylus brodiei, but its sites on the bay seabed have not yet been found. Citizen science-based research conducted in 2021 showed that thalli of C. brodiei, F. lumbricalis and F. vesiculosus are present on the southern and western shores of Puck Bay in the beach [46]. Furthermore, the presence of Furcellaria lumbricalis in the adjacent area in the outer part of Puck Bay was recorded in 2015 [47].
Finding species considered extinct in an area intensively explored by scientists after 40 years seems surprising. Some of the individuals in the populations described have likely survived in places not customarily explored by marine biologists for scientific purposes, as archaeological sites which we only visited by chance in 2021, and the ability to identify these species among the local population disappeared. In addition, in the last 10 years, vegetation studies were carried out randomly in the case of studies of other ecosystem elements [48,49]. In turn, the national monitoring of macroalgae and flowering plants in Puck Bay has been conducted since 2010 on a short transect (approximately 400 m) located in the Zostera meadow at the northeastern end of the bay near Kuźnica [43]. The low intensity of the research conducted on vegetation may probably be the reason for the lack of previous observations of representatives of both species, i.e., Coccotylus brodiei and Furcellaria lumbricalis, even if they started to appear in higher numbers long before 2019. On the other hand, it can be assumed that the effects of pressure from human activity factors from the period of intensive degradation were relatively extended over time, as the information on the improvement of the Puck Bay water quality and some biological elements is relatively new [9]. Hence, “old sins” could effectively inhibit the regeneration of populations and their habitats. In particular, the duration of generation time, for example, Furcellaria lumbricalis, is estimated to be 5–10 years [37].
The observations of the representatives of Furcellaria lumbricalis and Coccotylus brodiei carried out between 2019 and 2021 confirm the reports on the regeneration of the macrophytobenthic communities and the increase in water quality in the region [9,50,51]. These observations testify to the incredible resistance of natural systems and their regenerative potential. On the other hand, there is a possibility that the observed thalluses are descendants of algae from other parts of the Baltic Sea, such as Furcellaria lumbricalis with free-flowing thalli from Estonia. Without a genetic test of the historical reference material, it is not possible to unequivocally answer the question about the history of both species in the Puck Bay region. Unfortunately, despite our search, it was not possible to reach reference materials in local and European collections, a necessary condition for such an analysis.
After a period of strong degradation of the bottom of Puck Bay and adjacent waters associated with intensive human activity, eutrophication, and pollution, the vegetation communities gradually rebuilt [47,50,52]. However, vegetation recovery has lasted in our opinion for at least 30 years, which is far too long in comparison with rocky shores or bottoms in other marine locations [53,54,55]. This fact suggests that the process of secondary succession does not occur at the same speed in all aquatic ecosystems. This phenomenon is greatly influenced by the very nature of the bottom (sand versus rock) in addition to the type of human pressures on the ecosystem under consideration and their timing and local organism characteristics (propagule availability, life span, etc. [54,55]). The recovery of perennial macroalgae communities following the shift back to a less eutrophic state of Baltic waters in areas such as Sweden and Estonia was reported recently [28]. However, Germany and Poland were given as examples, where due to the discharge of excessive amounts of waste nutrients from agriculture into coastal waters, microphytobenthos recovery was lacking [28]. Here, we confirm that the start of the recovery process is also observed in Polish coastal waters. The observed recovery is a challenge for environmental managers to develop fit-to-purpose sustainable management in the region. On the other hand, it provides an opportunity to accelerate the recovery of other elements of the environment, for instance, fish of high economic value.
Concerns about the future fate of the species in question or in general the recovery of macrophytobenthic communities may be raised by climate change, which in the southern Baltic region is associated with, among other things, the increase in water temperature and the lack of ice in winter [56]. The literature indicates that for some species, climate change causes precipitous declines in population size by reducing fecundity and survival across multiple life stages [57,58]; however, in algae, early sporophytes seem to be more tolerant to temperature changes than gametophytes [59]. On the other hand, there are examples from marine environments where after a short period of regression, species started to regenerate and successfully develop [28,54,55,60]. Other observations show that under warming conditions and enhanced pCO2, neither an increment nor mitigation in macroalgae phenology shift or growth rates is observed [61,62]. All the above findings indicate that only the use of a complex and multifaceted approach could indicate the direction of changes occurring during the regeneration of macrophytobenthic communities.

5. Conclusions

After a period of strong degradation of the bottom habitats of Puck Bay associated with intensive unsustainable human activity (dragging of the bottom and uncontrolled discharge of domestic, agricultural, and industrial pollution), the vegetation communities gradually rebuilt as shown in a number of reports and papers. The new observations of Coccotylus brodiei and Furcellaria lumbricalis are further evidence of this phenomenon. The habitat recovery has, in our opinion, been ongoing for at least 30 years and still the most affected species as C. brodiei and F. lumbricalis are rare. The long history of the recovery process is probably due to the combination of a variety of stressors and their high level of severity. However, the damage caused to habitats and plant communities appeared to be reversible although no specific remediation measures were taken, only measures to eliminate or reduce human impact.
Undoubtedly, a great surprise is the return of species Coccotylus brodiei and Furcellaria lumbricalis not observed for 40 years, which are known to prefer clean water and to be sensitive to mixtures of oils and dispersants [37]. This fact speaks for their relatively high recoverability potential. Our study shows that the observations indicate improvement in the environmental quality due to declining human pressure but are also the result of extensive studies in search of taxa in question.

Author Contributions

A.Z.: Conceptualization, resources, investigation, writing—original draft; I.Z.: resources, investigation, writing—review and editing. All authors have read and agreed to the published version of the manuscript.

Funding

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data that support the findings of this study are available on request from the corresponding author, Z.I.

Acknowledgments

We would like to express our very great appreciation to Jerzy Bolałek for inspiration and Agnieszka Wochna for valuable and constructive suggestions during the planning and development of this research work. We would also like to extend our thanks to University of Gdańsk employees: Patryk Pezacki and Jakub Zdroik for assistance with research equipment and a number of students: Armin Halicki, Jakub Targoński, Anita Lipska, Marcelina Makuch, Wiktoria Kwiatkowska, Adam Jurkiewicz, Mikołaj Halicki, Marta Kucharska, Emilia Zygarłowska, and volunteers: Paulina Brzeska-Roszczyk, Maciej Koniuszy who helped in the laboratory work and material collection in the field.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Kentzer, T.; Borowczak, E.; Szczepkowska, E. Investigations on the growth intensity and its modification due to impurities in certain baltic algae. Biol. Morza 3 Studia I Mater. Oceanogr. 1976, 15, 169–186. (In Polish) [Google Scholar]
  2. Ślesińska, B. The species composition of plants taken when collecting furcellaria from the Puck Bay. Zesz. Nauk. Wydziału Biol. I Nauk. O Ziemii Uniw. Gdańskiego Oceanogr. 1976, 3, 139–148. (In Polish) [Google Scholar]
  3. Klekot, L. Quantitative analysis of the underwater meadows of the Puck Bay. Oceanologia 1980, 12, 125–140. (In Polish) [Google Scholar]
  4. Pliński, M. The distribution and biomass of phytobenthos in the internal part of Puck Bay. Studia I Mater. Oceanol. 1982, 39, 195–217. [Google Scholar]
  5. Kruk-Dowgiałło, L. Long-term changes in the structure of underwater meadows of the Puck Lagoon. Acta Ichthyologica. Et Piscatoria. Suppl. 1991, 21, 78–84. [Google Scholar] [CrossRef] [Green Version]
  6. Gic-Grusza, G.; Kryla-Straszewska, L.; Urbański, J.; Warzocha, J.; Węsławski, J.M. Atlas of Polish Marine Area Bottom Habitats: Environmental Valorization of Marine Habitats; Węsławski, J.M., Ed.; Broker-Innowacji: Gdynia, Poland, 2009. [Google Scholar]
  7. Pastuszak, M.; Stålnacke, P.; Pawlikowski, K.; Witek, Z. Response of Polish rivers (Vistula, Oder) to reduced pressure from point sources and agriculture during the transition period (1988–2008). J. Mar. Syst. 2012, 94, 157–173. [Google Scholar] [CrossRef]
  8. Savchuk, O.P. Large-scale nutrient dynamics in the Baltic Sea, 1970–2016. Front. Mar. Sci. 2018, 5, 95. [Google Scholar] [CrossRef]
  9. Zalewska, T.; Kraśniewski, W. Assessment of the State of the Environment of the Polish Maritime Areas of the Baltic on the Basis of Monitoring Data from 2018 against the Background of the Decade 2008–2017; Inspekcja Ochrony Środowiska—Biblioteka Monitoringu Środowiska: Warszawa, Poland, 2019. (In Polish) [Google Scholar]
  10. Grawiński, E.; Kozińska, A.; Paździor, E. Studies on the pathology of South Baltic Sea fish—A review. Życie Weter. 2013, 88, 851–860. [Google Scholar]
  11. Lang, T.; Kotwicki, L.; Czub, M.; Grzelak, K.; Weirup, L.; Straumer, K. The health status of fish and benthos communities in chemical munitions dumpsites in the baltic sea. In Towards the Monitoring of Dumped Munitions Threat (MODUM); Beldowski, J., Been, R., Turmus, E.K., Eds.; Springer: Dordrecht, The Netherlands, 2017. [Google Scholar]
  12. Kruk-Dowgiałło, L.; Brzeska, P.; Opioła, R.; Kukliński, M. Macroalgae and Angiosperms. Przewodniki Metodyczne do Badań Terenowych i Analiz Laboratoryjnych Elementów Biologicznych Wód Przejściowych i Przybrzeżnych; Kruk-Dowigiałło, L., Ed.; Biblioteka Monitoringu Środowiska: Warszawa, Poland, 2010; ISBN 978-83-61227-36-6. (In Polish) [Google Scholar]
  13. Pliński, M.; Hindak, F. Chlorophyta (green algae). Filamentous green algae (Ulotrichophycae, Conjugatophycae and Charophyceae). In Flora Zatoki Gdańskiej i Wód Przyległych (Bałtyk Południowy); Pliński, M., Ed.; Wydawnictwo Uniwersytetu Gdańskiego: Gdańsk, Poland, 2012; Volume 7/2. (In Polish) [Google Scholar]
  14. Pliński, M.; Surosz, W. Red algae and brown algae. In Flora Zatoki Gdańskiej i wód Przyległych (Bałtyk Południowy); Pliński, M., Ed.; Wydawnictwo Uniwersytetu Gdańskiego: Gdańsk, Poland, 2013; Volume 6. (In Polish) [Google Scholar]
  15. Pliński, M.; Szmeja, J. Seed Plants—Spermatophyta (Magnoliopsida & Liliopsida). In Flora Zatoki Gdańskiej i Wód Przyległych (Bałtyk Południowy); Pliński, M., Ed.; Wydawnictwo Uniwersytetu Gdańskiego: Gdańsk, Poland, 2013; Volume 8. (In Polish) [Google Scholar]
  16. Braune, W.; Guiry, M.D. Seaweeds. A Colour Guide to Common Benthic Green, Brown and Red Algae of the World’s Oceans; A.r.g. Gantner Verlag: Ruggell, Liechtenstein, 2011; ISBN 9780995567337. [Google Scholar]
  17. Bunker, F.; Brodie, J.A.; Maggs, C.A.; Bunker, A.R. Seaweeds of Britain and Ireland, 2nd ed.; Marine Conservation Society: Edinburgh, UK, 2017; ISBN 9780995567337. [Google Scholar]
  18. Lundsteen, S.; Nielsen, R. Coccotylus brodiei, C. truncatus and other Phyllophoraceae (Rhodophyta) in Danish waters. Forum om Marin Bundfauna og –Flora 2015, 2–120. Available online: http://bios.au.dk/fileadmin/bioscience/Forskning/Roskilde/2015-12-08_forum_bundfauna_Coccotylus.pdf (accessed on 25 September 2021).
  19. Guiry, M.D.; Guiry, G.M. AlgaeBase; National University of Ireland: Galway, Ireland, 2021; Available online: https://www.algaebase.org (accessed on 3 January 2021).
  20. le Gall, L.; Saunders, G.W. Dna Barcoding Is a Powerful Tool to Uncover Algal Diversity: A Case Study of the Phyllophoraceae (Gigartinales, Rhodophyta) in the Canadian Flora. J. Phycol. 2010, 46, 374–389. [Google Scholar] [CrossRef]
  21. Rosenvinge, L.K. The Marine Algae of Denmark. Contributions to Their Natural History. Part IV. Rhodophyceae IV. (Gigatinales, Rhodymeniales, Nemastomatales). Det K. Dan. Vidensk. Selsk. Skr. 7 Række 1931, 7, 491–626. [Google Scholar]
  22. Kylin, H. Die Rhodophyceen Der Schwedischen Westküste. Acta Univ. Lund. N.F. 1944, 40, 1–104. [Google Scholar]
  23. Zinova, A.D. Etermination Book of the Red Algae of the Northern Seas of the U.S.S.R.; Izdatelstvo Akademii Nauk SSSR: Leningrad, Moscow, 1955. [Google Scholar]
  24. Newroth, P.R.; Taylor, A.R.A. The nomenclature of the north atlantic species of Phyllophora Greville. Phycologia 1971, 10, 93–97. [Google Scholar] [CrossRef]
  25. Ciszewski, P.; Demel, K.; Ringer, Z.; Szatybelko, M. Zasoby widlika w Zatoce Puckiej oszacowane metoda nurkowania. Prace Mor. Inst. Ryb. Gdyni II Czesc A, Oceanogr.-Ichtiol. 1962, II, 9–36. [Google Scholar]
  26. Reprywatyzacja. Available online: http://www.reprywatyzacja.info.pl/b_wsk_fin_od_1939.htm (accessed on 18 December 2021).
  27. Trokowicz, D.; Andrulewicz, E. Wydobycie i przetwórstwo wodorostów z Zatoki Puckiej. Wiad. Ryb. Pismo Mor. Inst. Ryb. Państw. Inst. Badaw. 2019, 11–12, 20–22. [Google Scholar]
  28. Weinberger, F.; Paalme, T.; Wikström, S.A. Seaweed resources of the Baltic Sea, Kattegat and German and Danish North Sea coasts. Bot. Mar. 2020, 63, 61–72. [Google Scholar] [CrossRef] [Green Version]
  29. Kireeva, M.S. Commercial resources of algae in the coastal seas of Soviet Union. Okeanologiya 1965, 5, 14–21. (In Russian) [Google Scholar]
  30. Trei, T. The physiognomy and structure of the sublittoralmacrophyte communities in Kassari Bay (an area between the isles of Hiiumaa and Saaremaa). Kiel. Meeresforsch-Ungen Sonderh. 1978, 4, 117–121. [Google Scholar]
  31. Kruk-Dowgiałło, L.; Szaniawska, A. Gulf of Gdańsk and Puck Bay. In Ecology of Baltic Coastal Waters; Schiewer, U., Ed.; Springer: Berlin/Heidelberg, Germany, 2008; pp. 139–165. ISBN 978-3-540-73524-3. [Google Scholar]
  32. Fonseca, M.S.; Thayer, G.W.; Chester, A.J.; Foltz, C. Impact of scallop harvesting on eelgrass (Zostera marina) meadows: Implications for management. N. Am. J. Fish. Manag. 1984, 4, 286–293. [Google Scholar] [CrossRef]
  33. Creed, J.C.; Amado, G.M.; Filhô, F. Disturbance and recovery of the macroflora of a seagrass (Halodule Wrightii Ascherson) meadow in the Abrolhos Marine National Park, Brazil: An experimental evaluation of anchor damage. J. Exp. Mar. Biol. Ecol. 1999, 235, 285–306. [Google Scholar] [CrossRef]
  34. d’Avack, E.A.S.; Tillin, H.; Jackson, E.A.S.; Tyler-Walters, H. Assessing the Sensitivity of Seagrass Bed Biotopes to Pressures Associated with Marine Activities; JNCC: Peterborough, UK, 2014.
  35. Neckles, H.A.; Short, F.T.; Barker, S.; Kopp, B.S. Disturbance of eelgrass Zostera marina by commercial mussel Mytilus edulis harvesting in Maine: Dragging impacts and habitat recovery. Mar. Ecol. Prog. Ser. 2005, 285, 57–73. [Google Scholar] [CrossRef] [Green Version]
  36. Bird, N.L.; Chen, L.C.-M.; McLachlan, J. Effects of temperature, light and salinity on growth in culture of Chondrus crispus, Furcellaria lumbricalis, Gracilaria tikvahiae (Gigartinales, Rhodophyta), and Fucus serratus (Fucales, Phaeophyta). Bot. Mar. 1979, 22, 521–528. [Google Scholar] [CrossRef]
  37. Rayment, W.J. Furcellaria lumbricalis a red seaweed. In Marine Life Information Network: Biology and Sensitivity Key Information Reviews; Tyler-Walters, H., Hiscock, K., Eds.; Marine Biological Association of the United Kingdom: Plymouth, UK, 2008; Available online: https://www.marlin.ac.uk/species/detail/1616 (accessed on 13 June 2020).
  38. Martin, G.; Paalme, T.; Torn, K. Growth and production rates of loose-lying and attached forms of the red algae Furcellaria lumbricalis and Coccotylus truncatus in Kassari Bay, the West Estonian Archipelago Sea. Hydrobiologia 2006, 554, 107–115. [Google Scholar] [CrossRef]
  39. Bird, C.J.; Saunders, G.W.; McLachlan, J. Biology of Furcellaria lumbricalis (Hudson) Lamouroux (Rhodophyta: Gigartinales), a commercial carrageenophyte. J. Appl. Phycol. 1991, 3, 61–82. [Google Scholar] [CrossRef]
  40. Kersen, P.; Orav-Kotta, H.; Kotta, J.; Kukk, H. Effect of abiotic environment on the distribution of the attached and drifting red algae Furcellaria Lumbricalis in the Estonian Coastal Sea. Estonian J. Ecol. 2009, 58, 245. [Google Scholar] [CrossRef] [Green Version]
  41. Pedersen, M.; Snoeijs, P. Patterns of macroalgal diversity, community composition and long-term changes along the Swedish west coast. Hydrobiologia 2004, 459, 83–102. [Google Scholar] [CrossRef]
  42. Schories, D.; Selig, U.; Schubert, H. Species and synonym list of the german marine macroalgae based on historical and recent records (Arten- und Synomliste der Makroalgen in den Deutschen Küstengewässern—Auswertung von historischen und rezenten Befunden. Rostock. Meeresbiol. Beitr. 2009, 21, 7–135. [Google Scholar]
  43. Osowiecki, A.; Łysiak-Pastuszak, E.; Kruk-Dowgiałło, L.; Błeńska, M.; Brzeska, P.; Kraśniewski, W.; Lewandowski, Ł.; Krzymiński, W. Development of tools for ecological quality assessment in the Polish marine areas according to the Water Framework Directive. Part IV—Preliminary assessment. Oceanol. Hydrobiol. Stud. 2012, 41, 1–10. [Google Scholar] [CrossRef]
  44. Kornaś, J.; Medwecka-Kornaś, A. Associations Végétales Sous-Marines Dans Le Golfe de Gdańsk (Baltique Polonaise). Vegetatio 1950, 2, 120–127. [Google Scholar] [CrossRef]
  45. Sparre, A. The Climate of Denmark, Summaries of Observations from Light Vessels (IV), Salinity, Means, Extremes and Frequency; Danish Meteorological Institute: Copenhagen, Denmark, 1984; Volume 11. [Google Scholar]
  46. Jodziewicz, B. Citizen Science as a Tool for the Study of Rare Algae Species (Nauka Obywatelska Jako Narzędzie do Studiowania Rzadkich Gatunków Glonów). Bachelor’s Thesis, University of Gdańsk, Gdańsk, Poland, 2021. [Google Scholar]
  47. Brzeska-Roszczyk, P.; Kruk-Dowgiałło, L. Preliminary results of monitoring studies on macrophytes in the area of brine discharge from the creation of gas storage caverns (Puck Bay, Baltic). Biul. Inst. Mor. 2017, 32, 50–65. [Google Scholar] [CrossRef]
  48. Bełdowska, M.; Jędruch, A.; Zgrundo, A.; Ziółkowska, M.; Graca, B.; Gębka, K. The influence of cold season warming on the mercury pool in coastal benthic organisms. Estuar. Coast. Shelf Sci. 2016, 171, 99–105. [Google Scholar] [CrossRef]
  49. Sokołowski, A.; Ziółkowska, M.; Zgrundo, A. Habitat-related patterns of soft-bottom macrofaunal assemblages in a brackish, low-diversity system (Southern Baltic Sea). J. Sea Res. 2015, 103, 93–102. [Google Scholar] [CrossRef]
  50. Zgrundo, A. EN Ruppia maritima, L. Rupia morska. In Czerwona Księga Roślin Naczyniowych Pomorza Gdańskiego TOM 1 Zagrożone Gatunki Nadmorskich Plaż, Wydm i Solnisk oraz wód Słonawych Strefy Przymorskiej; Lazarus, M., Afranowicz-Cieślak, R., Eds.; Wydawnictwo Uniwersytetu Gdańskiego: Gdańsk, Poland, 2020; pp. 180–183. ISBN 978-83-8206-047-8. (In Polish) [Google Scholar]
  51. Zgrundo, A.; Złoch, I.; Kobos, J. Macroflora of the Puck Bay. In The Puck Bay Vol. 3; Bolałek, J., Burska, D., Eds.; Wydawnictwo Uniwersytetu Gdańskiego: Gdańsk, Poland. (In Polish)
  52. Zgrundo, A.; Lazarus, M. VU Zannichellia palustris L. Zamętnica błotna. In Czerwona Księga Roślin Naczyniowych Pomorza Gdańskiego TOM 1 Zagrożone Gatunki Nadmorskich Plaż, Wydm i Solnisk oraz wód Słonawych Strefy Przymorskiej; Lazarus, M., Afranowicz-Cieślak, R., Eds.; Wydawnictwo Uniwersytetu Gdańskiego: Gdańsk, Poland, 2020; pp. 183–187. ISBN 978-83-8206-047-8. (In Polish) [Google Scholar]
  53. Sousa, W.P. Intertidal mosaics: Patch size, propagule availability, and spatially variable patterns of succession. Ecology 1984, 65, 1918–1935. [Google Scholar] [CrossRef]
  54. Díez, I.; Santolaria, A.; Secilla, A.; Gorostiaga, J.M. Recovery stages over long-term monitoring of the intertidal vegetation in the ‘abra de bilbao’ area and on the adjacent coast (N. Spain). Eur. J. Phycol. 2009, 44, 1–14. [Google Scholar] [CrossRef] [Green Version]
  55. Kim, H.H.; Ko, Y.W.; Yang, K.M.; Sung, G.; Kim, J.H. Effects of disturbance timing on community recovery in an intertidal habitat of a Korean rocky shore. Algae 2017, 32, 325–336. [Google Scholar] [CrossRef] [Green Version]
  56. Sztobryn, M.; Wójcik, R.; Mietus, M. Występowanie zlodzenia na Bałtyku—Stan obecny i spodziewane zmiany w przyszłości. In Warunki Klimatyczne i Oceanograficzne w Polsce i na Bałtyku Południowym. Spodziewane Zmiany i Wytyczne do Opracowania Strategii Adaptacyjnych w Gospodarce Krajowej, Seria Monografie; Wibig, J., Jakusik, E., Eds.; IMGW-PIB: Warszawa, Poland, 2012; pp. 189–215. [Google Scholar]
  57. Panetta, A.M.; Stanton, M.L.; Harte, J. Climate warming drives local extinction: Evidence from observation and experimentation. Sci. Adv. 2018, 4, eaaq1819. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  58. Martins, G.; Harley, C.; Faria, J.; Vale, M.; Hawkins, S.; Neto, A.; Arenas, F. Direct and indirect effects of climate change squeeze the local distribution of a habitat-forming seaweed. Mar. Ecol. Prog. 2019, 626, 43–52. [Google Scholar] [CrossRef]
  59. Coelho, S.M.; Rijstenbil, J.W.; Brown, M.T. Impacts of anthropogenic stresses on the early development stages of seaweeds. J. Aquat. Ecosyst. Stress Recover. 2000, 7, 317–333. [Google Scholar] [CrossRef]
  60. Schiel, D.R.; Lilley, S.A. Impacts and negative feedbacks in community recovery over eight years following removal of habitat-forming macroalgae. J. Exp. Mar. Biol. Ecol. 2011, 407, 108–115. [Google Scholar] [CrossRef]
  61. Graiff, A.; Bartsch, I.; Ruth, W.; Wahl, M.; Karsten, U. Season exerts differential effects of ocean acidification and warming on growth and carbon metabolism of the seaweed Fucus vesiculosus in the Western Baltic Sea. Front. Mar. Sci. 2015, 2, 112. [Google Scholar] [CrossRef] [Green Version]
  62. Kang, E.J.; Kim, K.Y. Effects of future climate conditions on photosynthesis and biochemical component of Ulva pertusa (Chlorophyta). Algae 2016, 31, 49–59. [Google Scholar] [CrossRef]
Figure 1. Location of sampling sites (red-coloured spots indicate Coccotylus brodiei and Furcellaria lumbricalis collection sites). The inset shows the location of Puck Bay.
Figure 1. Location of sampling sites (red-coloured spots indicate Coccotylus brodiei and Furcellaria lumbricalis collection sites). The inset shows the location of Puck Bay.
Water 14 02181 g001
Figure 2. Coccotylus brodiei collected in Puck Bay in 2019. The line represents a distance of 5 cm.
Figure 2. Coccotylus brodiei collected in Puck Bay in 2019. The line represents a distance of 5 cm.
Water 14 02181 g002
Figure 3. Furcellaria lumbricalis collected in Puck Bay in 2019. The line represents a distance of 10 cm.
Figure 3. Furcellaria lumbricalis collected in Puck Bay in 2019. The line represents a distance of 10 cm.
Water 14 02181 g003
Figure 4. Free-floating thalli of Rhodophyta in Puck Bay in 2019.
Figure 4. Free-floating thalli of Rhodophyta in Puck Bay in 2019.
Water 14 02181 g004
Figure 5. Changes in the distribution of Furcellaria lumbricalis and Coccotylus brodiei in Puck Bay between 1957 and 1988 (based on data available in [1,3,4,25]).
Figure 5. Changes in the distribution of Furcellaria lumbricalis and Coccotylus brodiei in Puck Bay between 1957 and 1988 (based on data available in [1,3,4,25]).
Water 14 02181 g005
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Zgrundo, A.; Złoch, I. Gone and Back—The Anthropogenic History of Coccotylus brodiei (Turner) Kützing and Furcellaria lumbricalis (Hudson) J.V. Lamouroux in the Gulf of Gdańsk (Southern Baltic Sea). Water 2022, 14, 2181. https://doi.org/10.3390/w14142181

AMA Style

Zgrundo A, Złoch I. Gone and Back—The Anthropogenic History of Coccotylus brodiei (Turner) Kützing and Furcellaria lumbricalis (Hudson) J.V. Lamouroux in the Gulf of Gdańsk (Southern Baltic Sea). Water. 2022; 14(14):2181. https://doi.org/10.3390/w14142181

Chicago/Turabian Style

Zgrundo, Aleksandra, and Ilona Złoch. 2022. "Gone and Back—The Anthropogenic History of Coccotylus brodiei (Turner) Kützing and Furcellaria lumbricalis (Hudson) J.V. Lamouroux in the Gulf of Gdańsk (Southern Baltic Sea)" Water 14, no. 14: 2181. https://doi.org/10.3390/w14142181

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop