1. Introduction
Sea urchins are benthic marine echinoderms with high dispersal life history, high fecundity and external fertilization, with a key role in nutrient recycling in intertidal areas, seagrass and coral ecosystems [
1]. The ecological importance of sea urchins has been well documented [
2,
3,
4,
5]. These herbivore species can exert great pressure on the structure of biological assemblages through the removal of algae or the prevention of their establishment [
6,
7]. They can also act indirectly by creating cleared areas, allowing for the settlement of other organisms [
8].
The non-edible black sea urchin
Arbacia lixula (Linnaeus, 1758) (Echinodermata: Echinoidea) and the co-occurring edible species
Paracentrotus lividus (Lamarck, 1816) are the most widely distributed echinoids in the Mediterranean sublittoral zone [
9,
10], with the potential to influence, to a great extent, benthic communities with their intense grazing activity [
5,
11]. Despite their coexistence,
P. lividus is generally more abundant on horizontal or gently sloping surfaces, whereas
A. lixula is more common on vertical substrata [
11]. Both are opportunistic generalist species with the ability to exploit numerous food sources. Despite
A. lixula having a strong preference for encrusting corallines [
12], it can feed on a variety of food items [
13]. In general,
A. lixula is distributed in areas without the presence of macroalgal species, and consumes crusts and newly settled organisms [
12,
14,
15]. Sea urchins exert considerable pressure on their surrounding communities, the extent of which depends on the size of their assemblage.
P. lividus is the species mainly responsible for macroalgae clearance and the subsequent shift from macroalgal stands to barren areas.
A. lixula grazes on encrusting algae and is able to maintain the barren state even if the
P. lividus population eventually declines [
15].
Sea urchins exhibit three main feeding behaviors: (1) absorption by dermal skeleton of organic matter captured by sulcated spines and aboral tube feet, (2) consumption of macroalgae and invertebrates from the substratum with the use of Aristotle’s lantern and (3) the use of the ambulacral tube feet and spines to capture drift algae in the water column [
16,
17].
Since sea urchins are considered the main culprit in the reduction of macroalgal species and are often responsible for the creation of barren areas, their feeding ecology has been largely described in the literature [
18]. There have been numerous peaks in the population density of
A. lixula populations in the past [
19], resulting in attention focusing on its potential impact on benthic communities in the Mediterranean, especially in the context of global warming [
20,
21].
The present study aims to assess population characteristics of A. lixula, namely variations in space and time of its biometric characteristics, allometric relationships, numerical abundance, reproduction, growth, age composition and spatial point pattern distribution, between sites with varying degrees of anthropogenic impact. We aimed to address a present knowledge gap on the population characteristics of A. lixula by assessing its population structure and characteristics in the supralittoral fringe of the Pagasitikos Gulf. Physio-chemical measurements were recorded during the study to identify the prevalent environmental conditions and allow for future reference and comparison.
4. Discussion
Sea urchins often determine the extent of abundance and distribution of multicellular photosynthetic organisms in the sublittoral coastal zone, and have a substantial effect on their surrounding ecosystem [
5]. They affect dynamics, structure and assemblages of coastal marine habitats, including seagrass meadows [
41].
The proximity of the population collected from Site 1 (Agios Stefanos) to the treated sewage effluents discharge is probably the main reason why at this site, sea urchins are significantly larger in size and weight due to higher food availability. Areas with high food availability create ideal conditions for increased development [
42], resulting in an improved physiological condition of the sea urchins. Black sea urchin, despite its high dispersal capacity, has exhibited phenotypic variability even within restricted geographical areas [
43].
The co-occurring sea urchin
P. lividus density similarly increased progressively towards the sewage outlet of Cortiou cove (Morocco), with higher densities observed in the vicinity of the discharge point [
44]. It has been demonstrated that
P. lividus is not adversely affected by organic pollution, and in fact displays increased growth in the presence of organic pollution [
9]. Environmental factors that include food quantity ingested, amount of food absorbed and the quantity of dry matter absorbed may also affect growth, resulting in morphological differences [
45]. Phenotypic variation of organisms at different spatial scales could be the result of interaction among several factors, including interspecific competition, availability of resources and climatic conditions [
43]. It has been demonstrated that there is a positive relationship between food availability and test thickness (and thus urchin weight) [
45].
Variation in weight and test diameter of the gracious sea urchin
Tripneustes gratilla was linked to diet, season and population density [
46]. Increased size could also contribute to specific feeding habits.
A. lixula has been shown to change its feeding habit depending on food availability [
13,
47]. Hence, black sea urchin morphology could be affected by food type available at each site. An increase in test weight could also contribute to improved stability when exposed to hydrodynamic forces [
45]. Furthermore, a heavier test (greater mass) could contribute to a higher chance of survival [
48,
49]. It has been noted that increased test thickness helps the
P. lividus individuals escape fish predation and thus increase their longevity [
45].
Spatial point pattern analysis of the spatial distribution of
A. lixula indicated the highest population density during summer (4.0 ± 5.96 ind. m
−2) and lowest during autumn (0.8 ± 1.69 ind. m
−2) for both sampling sites, with slightly higher values mainly in Site 2 (Kato Gatzea). Similarly, around Ustica Island (Italy), the density of
A. lixula was more abundant in summer (3.1 ± 0.5 ind. m
−2) and less abundant in autumn (0.7 ± 0.2 ind. m
−2) [
50]. Along the Ligurian coast (Italy),
A. lixula density ranged between 0.2 ± 0.9 ind. m
−2 and 6.1 ± 1.1 ind. m
−2 [
51] and on the north coast of Sicily, its density was 3.10 ± 0.72 ind. m
−2 [
17].
The advantages of living in patches (clustered distribution) include the protection from predators and waves [
52,
53]. High densities are the result of both a highly successful recruitment [
54] and the anti-predatory benefits of dense aggregations [
1]. Variations in
P. lividus density can be misleading, mainly due to variable daily and seasonal behavior and the adopted census method used [
9].
P. lividus populations can be relatively stable for several years; however, rapid changes in density of large individuals are often observed, with annual changes in density occurring very frequently [
9,
55].
Fish predation has been considered the most important factor controlling sea urchin populations [
4]. However, it has been demonstrated that factors other than fish predation actually control sea urchin densities [
56]. Poor recruitment, losses during larval life, migrations, variations in abundance of sea urchin predators, overfishing of predators (especially crabs and fish), pollution, high rainfall, diseases and increased fishing efforts are potentially contributing factors for observed short- and long-term fluctuations [
2,
57,
58,
59]. A direct result of high fishing pressure is that sea urchins can lack natural direct control, with a tendency to increase in population densities [
5]. It has been reported that at the density of about 7–9 ind. m
−2,
P. lividus can affect benthic assemblage composition and biodiversity, and reduce total algal cover, resulting in bare areas of coralline encrusting algae [
60].
Several techniques, each with its own limitations, have been employed for the study of growth and population structure in echinoids, namely the study of size–frequency distributions, the analysis of growth rings in the test, mark–recapture techniques (usually with tetracycline and calcein labeling) [
61,
62] and monitoring of animals in enclosures [
63]. Size distribution analysis generally works well with short-lived animals that show clearly defined modes; however, these modes are difficult to discern and interpret in longer-lived animals that grow more slowly with age, as has been shown in sea urchins [
64,
65]. This is mainly due to the variation in growth of smaller individuals and results in size classes of mixed ages for the smaller as well as for the larger size classes [
61]. The present study used data on size–frequency distributions through time to assess growth and dynamics of the study populations. An initially similar size class of juvenile
P. lividus could result in a variable size distribution, with individuals growing at a different rate as a result of intraspecific competition [
9]. Observed growth inhibition in the natural environment could contribute to the stabilization of field aggregative populations by maintaining a protected pool of small individuals with high growth potential but inhibited by the density of larger ones. A decrease in the density of large individuals would remove the inhibition of small sea urchin growth [
66].
For
P. lividus, 2 cm individuals are generally considered 2 years old, on average, and 4 cm individuals are considered 4–5 years old. Growth curves cannot account for the largest individuals that are 7 cm in diameter [
9]. It is possible that these large individuals are several decades old, as suggested by [
61] for
Strongylocentrotus droebachiensis.
Strongylocentrotus purpuratus at Cape Arago, Oregon, USA, of 15 to 20 mm test diameter are about 1 year old, animals of 25–30 mm test diameter are about 2 years old, and animals of 35–37 mm test diameter are about 3 years old [
67]. Work on
Strongylocentrotus purpuratus at Cape Arago [
68,
69] indicated that age estimations from the size above 40 mm test diameter are inaccurate due to the strong influence of habitat on size. The estimated age and size of
S. purpuratus during the first three years of life generally agree with the determined age–size estimates of [
70] for the related species,
Strongylocentrotus intermedius, from Hokkaido, Japan.
Sea urchins follow a unique form of skeletal growth among organisms, where the skeleton (test) is composed of single calcite plates that follow a pentaradial symmetry [
71]. There are many different functions for modeling growth, but the von Bertalanffy model is the most commonly used because it satisfactorily describes the growth pattern of many species [
33]. The inflection point in the von Bertalanffy growth curve (4.45 years) coincides approximately with the size of sexual maturity of the species, reflecting the high energy investment towards reproduction of adults at the expense of somatic growth [
33]. However, unfavorable conditions and limiting food supply can decrease the size at which reproduction begins [
55]. Food quantity and quality can affect sea urchin reproductive maturation and growth [
72,
73]. Growth can be affected by environmental and demographic conditions [
33]. In the Mediterranean, maximum growth of
P. lividus occurs between 12 and 18 degrees in spring, sometimes in autumn, and is minimal in winter [
74]. Variations in food abundance, preference, assimilation and nutritive value directly affect metabolism and seasonal patterns in feeding and somatic growth of echinoids [
75]. In the present study, the maximum approximate age of the total
A. lixula population was estimated at 15.27 years. The maximum age of
P lividus using the von Bertalanffy model was estimated in Croatia [
76] at 15 years.
The reproductive cycle undergoes a seasonal cycle with a peak in May and low in August, in agreement with [
77]. In the south-western Mediterranean (Algeria) [
35], massive emission of
A. lixila gametes begins and coincides with the rise in temperature (20 °C), with maximum gonad volume in May and minimum at the end of summer to the beginning of autumn [
35]. In the Ligurian Sea (Italy),
A. lixula was reported to exhibit high fecundity and a long planktonic larval stage with abundant pluteus observed in the plankton during October and November, with a secondary peak in June and July [
78]. An experimental investigation [
77] indicated that larval survival and size of
A. lixula significantly increase with temperature.
In the Mediterranean, two spawning periods have been reported to occur for
P. lividus, one in early summer and a second in autumn [
59], that appear to be influenced by the increase in temperature to a critical point in June, and then a decrease past this critical temperature again in August. It appears that the increase in sea temperature serves as a cue for spawning induction, as suggested for
A. lixula [
35] and
P. lividus populations [
59]. Additional factors apart from temperature increase appear to play a role in spawning, namely, illumination, pheromones or gametes in the water [
79]. Sea urchin gonads act as the main organ of nutrient storage [
80] with the amount of nutrient intake and subsequent gonad growth depending on food quantity/quality and consumption, digestion and absorption rate [
81,
82].
The gonadosomatic index in males was significantly higher compared to the females. The opposite was indicated for
P. lividus, where the index was found to be significantly higher in females compared to males, suggesting that females might have better efficiency in converting nutrients into gonad tissue compared to males [
83]. All three factors (sex, site, season) posed a significant effect on the GSI, in contrast with [
35], which indicated no significant differences between sexes and sites. The gonad index is directly correlated with food availability [
84], which influences the condition of the nutritive phagocytes.
The overwhelming majority of the coastal areas are globally influenced by pollution, affecting commercial coastal and marine resources. Sewage comprises the largest source of contamination, by volume, of the marine and coastal environment [
85], with coastal sewage discharges exhibiting an increasing trend over the past 30 years. The control of aquatic pollution is therefore imperative as an immediate need for sustained management and conservation of existing fisheries and aquatic resources. Numerous pollution indicator organisms have been extensively used as bioindicators since pollutant concentrations in their tissues relate to the surrounding marine environment. Echinoids are valuable biological indicators of heavy metal contamination [
86], with
A. lixula identified as an indicator species with the advantage to occupy polluted and unpolluted areas alike [
87,
88]. Patterns of fluctuating asymmetry have been shown to occur in
A. lixula [
89], since a degree of pollutant bioaccumulation occurs when
A. lixula develops in polluted sediment [
87,
90].
Complex interactions and human impacts could have adverse effects on the whole coastal biota, with wider socioeconomic implications [
51]. Anthropogenic activities in the marine coastal environment could potentially affect the natural system, causing degradation and fragmentation of habitats [
91]. Assessing, interpreting and predicting these direct and indirect changes are essential to fine-tune conservation activities and environmental management [
3]. Subtidal rocky substrates of the Mediterranean Sea are highly disturbed by anthropogenic activities, ranging from seafood collection to diving tourism [
92], that can affect marine food webs by altering dynamics among trophic levels [
93,
94].