Course:CONS200/2023/Sustainable Management of Mediterranean Sea Urchin Populations in Greece

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Sea urchin management in Greece

Introduction

Sea urchins are marine animals that belong to the phylum Echinodermata[1] With over 900 species found around the globe, sea urchins are known for their unique appearance, with a spherical body covered in spines and tube feet that allow them to move along the ocean floor.[1] Sea urchins are an important and valuable species globally, known for their ecological, ornamental, nutritional, and economic significance [1]. They have high nutritional value and are considered a luxury delicacy in many cultures.[1][2][3] Additionally, sea urchins play a significant role in marine ecosystems acting as a keystone species[4]. They serve as indicators for ecosystem health by being sensitive to pollutants, as well as shaping ecosystems through their feeding habits, nutrient cycling, and acting as both predator and prey[1][4][5].

There are two main species of sea urchin found in Greece, Paracentrotus lividus and Arbacia lixula.

Purple sea urchin Paracentrotus lividus in the Mediterranean

Paracentrotus lividus

Paracentrotus lividus is an echinoderm sea urchin species native to the Mediterranean sea and eastern Atlantic ocean, commonly referred to as the purple sea urchin [6]. P. lividus is found in tide pools and other horizontal or gently sloping surfaces at depths of up to 30 m below sea level along rocky shores, however they may also be found deeper. To avoid agitation and desiccation from changing sea levels, the urchin uses its teeth and spines to create a burrow in soft rock, which increase in size as the urchin grows [7]. P. lividus is a generalist browser, eating a range of red, green and brown algae in addition to seagrass [8]. This species also serves as a bioindicator for pollutants due to their wide distribution, easy access, low mobility, and susceptibility to environmental pollutants [9]. It is this species of sea urchin that is harvested for its edible roe, which is a delicacy in many parts of the world [3].

A black sea urchin (Arbacia lixula) in the Mediterranean



Arbacia lixula

The black sea urchin, Arbacia lixula, is an echinoderm species native to the Mediterranean Sea, but can also be found along the Atlantic coast of western Africa and off the Brazilian coast [5]. A. lixula is abundant on vertical rocky surfaces of subtidal coasts to a depth of 30m and prefers environments which are exposed to a high degree of hydrodynamic forces [5].It is typically distributed in areas lacking macroalgal species and instead feeds on crusts and newly settled organisms [5]. A. lixula is able to change its feeding habit depending on food availability; when food availability is high, A. lixula can adapt its feeding habits, resulting in improved physiological conditions and increased development [5]. As a result, areas with high food availability provide ideal conditions for the species to thrive[5].




Impacts

Ecological Significance

Sea urchins serve as an important indicator species and general maintainer of the marine environment’s health. Through their eating habits, they regulate algae levels and clear areas where other marine life settle [10]. Specifically, P. lividus has a preference for macroalgae, and A. lixula prefers encrusting corallines, however both are opportunistic feeders [5]. Consequently, sea urchins affect the structure of habitats and engage in nutrient cycling in intertidal areas, seagrass, and coral ecosystems. This is particularly important as P. lividus has been shown to reap benefits from consuming organic pollution, and thus can be important for environmental stability and recovery [5].  

This map shows the location of the Aegean Sea between Greece and Turkey where the urchin species and barrens are found.

Negative Ecological Effects

Urchin Barrens

A common negative ecological effect attributed to sea urchins is a phenomenon known as an “urchin barren”. Urchin barrens are characterized by large areas of benthic communities on rocky subtidal reefs that have been dominated by urchins and coralline algae and are devoid of seaweed [11]. The cause of such urchin barrens is the overgrazing of herbivorous species, such as sea urchins, which moves the system from one stable state to another [11]. Urchin barrens result in low primary productivity and low food-web complexity relative to healthy kelp communities [11].

Barrens in the Mediterranean

Urchin barrens are a phenomena that have been observed in the Mediterranean sea, with documentation of large expanses of rocky subtidal habitats being completely degraded to the barren state due to the high grazing pressure exerted by sea urchins [10] [12]. Due to human-caused climate change, oceanic warming is predicted to drive A. lixula ranges northwards in the northern hemisphere and southwards in the southern hemisphere, which could have the potential to increase the range of urchin barrens in the Mediterranean Sea [2].

In the Cyclades (a Greek archipelago in the central Aegean sea), it was observed that sea urchin biomass was positively correlated with the presence of barrens [10]. It has been noted that the Cyclades display much lower fish biomass than similar areas elsewhere in the Mediterranean[10]. It has therefore been suggested by researchers that a possible explanation for the presence of barrens in this region is the reduction in predatory fish abundance caused by historical unsustainable fishing practices [10]. Indeed, It has been suggested that the historical overfishing in the region represents the most likely explanation for the depletion of the shallow sublittoral communities in the Cyclades Archipelago[10]. If the low abundance of predatory fish is indeed causing the increase in urchin abundance this would be through a process known as a trophic cascade.

Trophic Cascades

Trophic cascades are indirect species interactions that originate with predators and spread downward through food webs [13]. A trophic cascade refers to the indirect effects that can be observed within a food chain or food web when a change in one level of the system affects the other levels. Specifically, it occurs when the increase or decrease of a predator's population causes a ripple effect in the population of its prey, which in turn affects the population of the prey's prey and so on [13]. This cascade of effects can propagate through multiple trophic levels, leading to changes in ecosystem structure and function [13].

The depletion of populations of sea urchin predators caused by overfishing has been cited as the main driver of kelp bed collapse in different regions of the world [12]. In the Cyclades, historical overfishing of species that prey on such urchins, such as Diplodus spp., has led to a trophic cascade[10]. Through the reduction of these predators, sea urchin populations have been able to to grow unchecked, and consequentially increased the amount of urchin barrens[10]. It has been recorded that apex predators were only recorded in 44/181 sites, indicating a depleted ecosystem[10]

Invasive Diadema setosum (Feb 2014)

Threats

Other Marine Life

Invasive Sea Urchin Species: Diadema setosum

Diadema setosum, commonly referred to as the black longspine urchin, is a species of long-spined sea urchin that is becoming an increasing threat to populations of P. lividus and A. lixula on several Greek islands [14]. They are characterized by extremely long, hollow spines, which are mildly venomous[14]. D. setosum is a widely distributed species; its range stretches throughout the Indo-Pacific basin and can be found as far north as Japan and as far south as the southern tip of the African east coast [14]. They live in shallow depths of the sublittoral zone, often residing 20 m below the surface. While they prefer rocky habitats and biogenic reefs, they will also inhabit the sandy ocean floor or meadows of seagrass [14]. D setosum is a prolific grazer, feeding on many species of algae [14].D setosum is divided into two molecularly distinct clades, respectively occupying the Indo-West Pacific and the Arabian Peninsula [14]. Both these environments are considered tropical, characterized by high annual temperatures and the recent increase in temperature of the Mediterranean Sea seems to accelerate its spread. The first reports of D. setosum in the Mediterranean date back to 2006; these individuals were removed, however, established populations of this species have since established in the Aegean Sea. It is likely that these organisms were transported unintentionally by ships or migrated through the Suez Canal. [15]

Major predators: Diplodus sargus and D. vulgaris

Successful predation is often size dependent, with predator size increasing as prey size goes up. This means that most predation attempts on sea urchins, especially considering their (sometimes venomous) spines, fail. However, through scuba-diving expeditions in sea urchin hotspots, scientist and research Sala was able to identify the tactics used by Grecian sea urchins' major predators, Diplodus sargus and Diplodus vulgaris [16][10]. This genus of fish consumes both juvenile and adult sea urchins by swallowing them whole or breaking them with a strong bite, sometimes breaking the spines and turning the urchin upside down first if the urchin is too large to bite efficiently[16].

Diplodus Vulgaris (2012)
Diplodus sargus. (2020)

Local Human Activities

Consumption and Fishing

In most of its geographical range, the gonads of Paracentrotus lividus are appreciated as seafood and have been intensely harvested. Presently, its consumption is mainly limited to France, and to a lesser extent to Italy, Spain and Greece [6]. Due to their gonads, or "roe" being constituted a highly appreciated gastronomic delicacy, sea urchins are among the most intensively harvested invertebrates[1]. This especially damaging, as they are harvested during the period when nutritive material is stored in the gonads before being converted into gametes[14].

Overfishing has been identified as the most likely cause for species residing in shallow sublittoral zone depleted population levels [10]. Technological advances for vessels, gear, and devices such as radar has allowed humans to fish sea urchins in much larger quantities at accelerated speed [10]. Coupled with a lack of enforcement and non-compliance to fishery regulations by both authorised fishermen and poachers, this efficiency causes a detrimental over-depletion of wild sea urchin stocks [3][10][17]

This overexploitation and premature harvesting has a significant impact on the species' reproductive output, which is further exacerbated by the negative effects of global warming on natural stocks of the species [1].

Microplastics

In recent years, concern about the presence of microplastics in food has grown due to their ubiquity in the environment and the potential adverse effects they pose on human health [9]. Paracentrotus lividus grazes on available resources found on the surfaces they inhabit, which unfortunately include microplastics. Microplastics have been shown to impair the sea urchin’s health at embryonal, larval and adult stages, this may be of particular concern due to the recent dramatic decline of P. lividus in some parts of the Mediterranean Sea [9]. Microplastics were found in every individual studied and concentrations were positively correlated to microplastic concentrations within sediment samples from their habitat in Greece’s Aegean sea [9]. The presence of microplastics in the Aegean sea pose a threat to human health as well as the health of P. lividus organisms and populations [9].

Climate Change

Ocean Acidification

Ocean acidification is caused by the ocean sequestering excess CO2 emissions, resulting in the decrease of both surface seawater pH level and the saturation state of calcium [18]. Many marine organisms, including sea urchins, form their skeletons or shells out of calcium carbonates and thus are put at risk by calcium’s dissolution threshold being lowered [11]. Specifically, sea urchins’ endoskeleton is composed of a high Mg-calcite, meaning that many of the Ca2+ ions found in regular calcite have been replaced by Mg2+ ions [11]. This is especially detrimental as the Mg2+ ions significantly decrease the mineral’s stability, making it 30 times more soluble than regular calcite [11][10]. Consequently, because sea urchins are so susceptible to corrosive water, pH level decrease caused by ocean acidification requires sea urchins to direct more effort into skeletal organization, and harms their metabolism and reproduction [10]. Furthermore, warming ocean temperatures causes an increase in Mg content within calcite, further exacerbating their skeletons’ solubility [11].

Climate change and the increase in ocean temperatures

For thousands of years, the temperature in the Mediterranean sea remained at a stable 19°C[19], this warm stable temperature has allowed the tropical A. lixula to settle and populate the Mediterranean Sea [20]. However, in conflict with this ecosystem's stability is the threat of increasing oceanic temperatures caused by anthropogenic climate change. A study based on 14 different climate models developed by the Intergovernmental Panel on Climate Change (IPCC) suggests that there will be a temperature increase of 3–5°C in the Aegean Sea by 2100[21].

Due to the already increasing water temperatures of the Mediterranean Sea, the thermophilic sea urchin species Arbacia lixula has increased in abundance by over 12 times in a span of nine years [2]. This increase has facilitated the expansion of the species' distribution range, as well as the formation of barren grounds in some areas[2]. In contrast, the co-occurring Paracentrotus lividus has undergone a large-scale decline in abundance in many areas of the Mediterranean Sea [2].

It has been observed that the increasing water temperature associated with climate warming can inhibit and/or interrupt P. lividus gametogenesis leading to decreased fecundity. [2]. Conversely, A. lixula exhibits an opposite trend[2]. There has been observed a positive correlation between increased surface sea temperature and GSI (gonadal somatic index; the index of gonad mass relative to whole organism size) of A. lixula[2].

This change in environmental conditions may result in the environmental conditions favouring A. lixula over P. lividus, leading to the former becoming the dominant species in Mediterranean rocky reefs[2]. This shift could have serious consequences for the diversity and functioning of the Mediterranean sub-littoral ecosystem, as A. lixula is less prone to predation than P. lividus and thus may establish a positive feedback loop that stabilizes and maintains barren grounds in rocky littoral ecosystems[2].

Management

Current Techniques Around the Globe

Culling of Urchins as a Management Strategy

In several areas of the world, the removal of sea urchins has been found to have a positive effect on the recovery of overexploited subtidal rocky habitats [12]. Findings have suggested sea urchin culling as a promising practice for aiding in the recovery from urchin barrens macroalgae habitats [12]. Considering the limited cost of the intervention, culling also represents an attractive option economically [12]. In a study conducted in the Mediterranean in 2015, the large-scale culling of urchins was found to be successful in assisting the recovery of the assemblage in barren grounds with clear signs of recovery after 1 year after the intervention [12]. Even at the end of the experiment, 3 years post intervention, sea urchins at culling sites were approximately 75% less abundant than at the beginning [12]. 36 months after sea urchin removal, significant changes had occurred in the structure of benthic assemblages [12]. A progressive contraction of barren extent was observed, with a reduction in bare substrate of 50% [12]. It is important to recognize however that no difference was detected in the diversity and in the overall assemblage composition between culling and control sites,  Differences were due, rather, to the increased relative abundance of macroalgal taxa, which were originally present in sparse, small, and isolated patches [12]. As well, during the experiment, the condition reached 1 year after the initial treatment did not evolve further [12]. This supports concerns about the pervasive trend of the alternative state characterized by the dominance of turfs persisting once established, thus preventing the recovery of highly structured macroalgal forests, specifically recruitment of habitat-forming species (i.e., Cystoseria and Sargassum species) [12].

Effort to prohibit spearfishing and other types of fishing on North-West Mediterranean protected and non protected areas

Researchers Sala and Zavala both agree that the most important and stabilizing predator of sea urchins in the northwestern territories of the Mediterranean is Diplodus sargus. The prohibiting of certain methods of fishing (spearfishing and angling), they posit, represents a good effort and direct solution to prevent the decrease of the mean size of predators. Most major predators depend on size in order to kill sea urchin not only in juvenile stages but also in adulthood[16]. Sala suggests then the extension of a more broad prohibition of fishing techniques in order to let species recover and increase predation of sea urchins around these areas [16] . Fish predators, they suggest, are not the only threat to sea urchins populations but are arguably the most important one[22].

Conclusion

Due to the ecological and economic importance of Paracentrotus lividus and Arbacia lixula in Greece, sustainable and efficient management of both the urchins, and their co-existing species is crucial. As of 2010, the management techniques in Greece included: maximum mesh sizes, licensing for fishermen, prohibiting trawlers within 1.5 nauticals miles from the coast or waters shallower than 50m, and prohibiting purse-seining within 300m from the coast or in in water shallow than 30m [10]. However, despite their preventative measures, the negative threats to and from sea urchins are still overwhelming.

To assist in the sustainable management of urchin species in the Mediterranean the authors of this wiki firstly recommend the halt to the activities that are leading to the overexploitation of the predators of the urchins living in the Mediterranean. We recommend the creation of stricter licensing rules and regulations, as well as the creation of well-monitored protected areas as that has been shown to increase fish biomass in areas near the Greek Cyclades, including predatory species.[10].

We also recommend the interim use of urchin culling as an effective intervention mechanism that can assist in minimizing the destruction that overpopulated communities of sea urchins can inflict on macroalgae habitats[12].

The authors of this wiki finally, strongly advocate for the halting of activities that are contributing to anthropogenic climate change. By addressing climate change, slowing its rate, and eventually reversing its effects, we can help to ensure that the Mediterranean marine ecosystem remains healthy and productive into the future[4][2][18][21][19].

References

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  2. 2.00 2.01 2.02 2.03 2.04 2.05 2.06 2.07 2.08 2.09 2.10 Gianguzza, Paola; Agnetta, Davide (2010). "The rise of thermophilic sea urchins and the expansion of barren grounds in the Mediterranean Sea". Chemistry and Ecology. 27: 129–134 – via Taylor & Francis Online.
  3. 3.0 3.1 3.2 Matsiori, Steriani (January 2012). "Economic value of conservation. The case of the edible sea urchin Paracentrotus lividus". Journal of Environmental Protection and Ecology. 13: 269–274 – via ResearchGate.
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  5. 5.0 5.1 5.2 5.3 5.4 5.5 5.6 5.7 Klaoudatos, Dimitris (March 2022). "Population characteristics of the upper infralittoral sea urchin Arbacia lixula (Linnaeus, 1758) in Eastern Mediterranean (Central Greece): An indicator species for coastal water quality". Journal of Marine Science and Engineering. 10: 395 – via MDPI.
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  9. 9.0 9.1 9.2 9.3 9.4 Hennicke, A (2021). "Assessment of microplastic accumulation in wild paracentrotus lividus, a commercially important sea urchin species, in the eastern Aegean Sea, Greece". Regional Studies in Marine Science. 45.
  10. 10.00 10.01 10.02 10.03 10.04 10.05 10.06 10.07 10.08 10.09 10.10 10.11 10.12 10.13 10.14 10.15 10.16 Giakoumi, Sylvaine (August 2012). "Relationships between fish, sea urchins, and macroalgae: The structure of shallow rocky sublittoral communities in the Cyclades, Eastern Mediterranean". Estuarine, Coastal and Shelf Science. 109: 1–10 – via ScienceDirect.
  11. 11.0 11.1 11.2 11.3 11.4 11.5 11.6 Filbee-Dexter, K (2014). "Sea urchin barrens as alternative stable states of collapsed kelp ecosystems". Marine Ecology Progress Series.
  12. 12.00 12.01 12.02 12.03 12.04 12.05 12.06 12.07 12.08 12.09 12.10 12.11 12.12 Guarnieri, G (2020). "Large-scale sea urchin culling drives the reduction of subtidal Barren Grounds in the Mediterranean Sea". Frontiers in Marine Science.
  13. 13.0 13.1 13.2 Ripple, W (2016). "What is a trophic cascade?". Trends in Ecology and Evolution.
  14. 14.0 14.1 14.2 14.3 14.4 14.5 14.6 Vafidis, D (2021). "Abundance and population characteristics of the invasive sea urchin Diadema setosum (Leske, 1778) in the South Aegean Sea (Eastern Mediterranean)". Journal of Biological Research-Thessaloniki.
  15. Voulgaris, K (2021). "Mechanical defensive adaptations of three Mediterranean Sea urchin species". Ecology and Evolution.
  16. 16.0 16.1 16.2 16.3 Sala, E. (1997). "Fish predators and scavengers of the sea urchin Paracentrotus lividus in protected areas of the north-west Mediterranean Sea". Springer link. 129: 531–539.
  17. Pantazis, P. (2017, June). Echinoculture in Greece: Present status and perspectives. World Aquaculture 2017. https://www.researchgate.net/publication/321797164_Echinoculture_in_Greece_present_status_and_perspectives
  18. 18.0 18.1 McClintock, J (2011). [457-466, https://doi.org/10.1086/660890 "The Mg-calcite composition of Antartic echinoderms: Important implications for predicting the impacts of ocean acidficiation"] Check |url= value (help). The Journal of Geology.
  19. 19.0 19.1 Bardají, T (2008). "Sea level and climate changes during OIS 5e in the Western Mediterranean". Science Direct. 104: 22–37.
  20. Wangensteen, Owen S. (2012). "Natural or Naturalized? Phylogeography Suggests That the Abundant Sea Urchin Arbacia lixula Is a Recent Colonizer of the Mediterranean". Pub Med Central.
  21. 21.0 21.1 Patel, Samir H. (2016). "Climate Impacts on Sea Turtle Breeding Phenology in Greece and Associated Foraging Habitats in the Wider Mediterranean Region". Pub Med Central.
  22. Savy, s (1987). "Les preÂdateurs de Paracentrotus lividus (Echinodermata). In: Boudouresque CF (ed) Colloque International sur Paracentrotus lividus et les oursins comestibles". GIS Posidonie, Marseille: 413–423. line feed character in |title= at position 110 (help)