Diversity, distribution and abundance of elasmobranchs and the main influent factors along the coast of Lebanon (eastern Mediterranean)

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The Mediterranean Sea: Biodiversity, threats and fisheries

Geographical overview

The Mediterranean is the largest and deepest enclosed sea on Earth. It has narrow continental shelves and a large area of open water. It covers approximately 2,500,000 km2 (excluding the Black Sea), representing around 0.2% of oceans volume, with an average depth of 1460 m and a maximum of 5267 m (Cuttelod et al., 2008) (Figure 1). It connects the three continents: Africa, Europe, and Asia. It is connected to the Atlantic Ocean in the west through the Strait of Gibraltar and to the Sea of Marmara and the Black Sea in the east through the Dardanelles. The Mediterranean has been artificially connected to the Red Sea and Indo-Pacific region through the building of the Suez Canal in 1869.
Figure 1: Map of the Mediterranean Sea and surrounding countries (Cuttelod et al., 2008).
The climate in the region is characterized by hot, dry summers and cool, humid winters. The annual mean sea surface temperature shows a high seasonality and important gradients from west to east and north to south (Hopkins, 1985). The strong environmental gradients in the basin makes the eastern part more oligotrophic than the western one (Azov, 1991). The increase in temperature and salinity from north to south and from west to east causes the decrease in biological production in a likewise direction (Danovaro et al., 2008).

Biodiversity

The recent marine biota in the Mediterranean Sea is primarily derived from the Atlantic Ocean, but the wide range of climate and hydrology has contributed to the co-occurrence and survival of both temperate and subtropical organisms (Bianchi and Morri, 2000). It is known for the diversity and high endemism of marine species (crabs and crayfish, mammals, and cartilaginous fish) (Cuttelod et al., 2008). Up to 18% of the world‘s macroscopic marine species (out of which 25 to 30% are endemic) are found in the Mediterranean basin although it makes less than 1% of the global ocean surface, confirming an incredibly rich biodiversity for such a small area (Bianchi and Morri, 2000). Currently, the Mediterranean Sea holds 17,000 (7%) of all known marine species (Coll et al., 2010). The level of endemism is especially high on the islands of the Mediterranean, where species have evolved to survive in very specific habitats (Blondel and Aronson, 1999). Around 23 of the world‘s cetacean species are found in the Mediterranean, consisting of 9 known year-round residents (Reeves and Notarbartolo di Sciara G., 2006). This sea is also home to the most endangered pinniped: the Mediterranean Monk Seal Monachus monachus and it holds around 80 cartilaginous fish species, 40% of which are threatened (Cavanagh and Gibson, 2007; Cuttelod et al., 2008; Bradai et al., 2012). However, Mediterranean biodiversity has been and will be continuously altered and shaped by natural and anthropogenic factors in the past and the coming future (Coll et al., 2010).

Threats

The effects of human activities are relatively stronger in the Mediterranean than in any other sea of the world (Blondel and Aronson, 2005). Its coasts are highly inhabited and the region strictly participates in the global economy and trade welcoming approximately 200 million tourists yearly (Bradai et al., 2012). Its coastal ecosystems have been particularly affected by the past and recent human activities and economic development (Cuttelod et al., 2008; Papadopoulou et al., 2011). The knowledge about processes, ecological species distribution, the condition of its ecosystems and the drivers for biodiversity loss is still vague, even more than most of the basin is unmanaged and exposed to threats (Notarbartolo di Sciara and Agardy, 2009). Many of the ecological characteristics in the Mediterranean Sea are under threat with areas of potential high cumulative threats overcoming the western and eastern basins and fewer in the southeastern region (Coll et al., 2012). The most important causes of current and future threats for the Mediterranean species are habitat loss and degradation, pollution, overexploitation (unsustainable aquaculture and fishing), eutrophication, maritime traffic, invasive alien species, human disturbance, climate change and bycatch (Cuttelod et al., 2008; Coll et al., 2010) (Figure 2). Moreover, temporal patterns indicate that overexploitation and habitat loss are the main human drivers of historical changes (Lotze et al., 2011). The marine ecosystems and species in the Mediterranean Sea are affected by several of these threats. For instance, some cetaceans are severely affected by noise pollution (due to marine traffic) that impairs their ability to find prey, while others are affected by chemical pollutants such as polychlorinated biphenyls (PCBs) which affect the immune system, increasing sensitivity to illness, and causing increased mortality and reduced reproduction (Cuttelod et al., 2008).
Furthermore, the southeastern region of the Mediterranean is also influenced by the introduction of Lessepsian (Indo-Pacific) species (Coll et al., 2010). In total, the number of Lessepsian species has reached more than 790 in the Mediterranean Sea, with some of the invaders through the Suez Canal having been very successful colonizers of Mediterranean marine ecosystems (Galil and Zenetos, 2002; Zenetos et al., 2005; Golani et al., 2007; Golani, 2010; Oral, 2010). One example is the silver-cheeked toadfish, Lagocephalus sceleratus which is causing several problems in the surrounding ecosystem and fisheries sector (Zenetos et al., 2005; Peristeraki et al., 2006; Streftaris and Zenetos, 2006). A study done in Lebanon concerned the population structure and the sexual maturity of this fish in the Lebanese and Syrian waters in order to shed light on the severity of this problem (Khalaf et al., 2014) (ANNEX I). In addition, the Mediterranean is also influenced by species introduced from the Atlantic Sea through the Strait of Gibraltar and have reached the Adriatic Sea and even the eastern basin. Some of these Atlantic species are invasive and showed continuous distribution, such as, Parablennius pilicornis (Pastor and Francour, 2010), Pomadasys incisus (Bodilis et al., 2013), and Lampris guttatus (Francour et al., 2010); others showed patchy distributions, such as, Kyphosus sectatrix (Francour and Mouine, 2008) and Pisodonophis semicinctus (Bodilis et al., 2012). Regarding both distributions, the number of individuals of all Atlantic species has increased during the last decade. Their increasing numbers have an impact on native populations and may lead to a reduction in the abundance of endemic species (Otero et al., 2013).
The creation of a new Suez canal parallel to the current channel (inaugurated on August 6, 2015) is expected to double the capacity of the Canal. This expansion is sure to quickly affect the Levantine Basin unfolding a diverse range of effects, at local and regional scales, on both the biological diversity and the ecosystems (Galil et al., 2014) that will subsequently spread to the rest of the Mediterranean.
Moreover, overexploitation (especially fishing) and bycatch are serious problems for Mediterranean species affecting many threatened marine species, such as, bony and cartilaginous fish, dolphins and marine turtles (Cuttelod et al., 2008). In addition, the overexploitation of large predators, with change in biomass and composition, could possibly have a greater impact on the stability of an ecosystem, especially the marine one, than removing species farther down the food chain (Larkin, 1979; Watson and Pauly, 2001). Bycatch, as well, can lead to the loss of biological resources along with its biological and ecological impact (Hall et al., 2000).

Fisheries

The Mediterranean is one of the oldest and most intensively exploited marine system. Its fisheries target different resources mostly pelagic stocks (Abella et al., 2002). More than one percent of world landings come from Mediterranean fisheries (Coll et al., 2010). This fishery is typically characterized by small fishing vessels and multispecies landings. important industrial fisheries mainly target small pelagics (mainly sardines and anchovies) which are principally caught using purse seines and pelagic trawls. Artisanal, as well as industrial fleets, exploit a large number of benthic and demersal species distributed over the generally narrow continental shelves characterizing the Mediterranean Sea. These stocks usually remain within national waters, except in some areas characterized by a wider continental shelf (Caddy, 1993). Catch assessments are difficult in the Mediterranean because of the multi-specific and multi-gear characteristics of most of its fisheries, the dispersed landing sites and the small fraction of the catch that generally passes through organized fish markets. Sometimes the same stocks are exploited by diverse fleets as their geographical distribution often exceeds the national waters of a single country (Abella et al., 2002). Furthermore, juveniles and commercially important species or untargeted species constitute the unknown quantity of bycatch, with some species often discarded dead at sea. Invertebrates constitute a minor fishery sector for most countries in the concerned area, partly due to cultural purposes (Bariche, 2012).
The Mediterranean Sea and Black Sea make up together FAO Fishing Area 37 (FAO, 2004). It is divided into four subareas, each of which has its own divisions: Western Mediterranean (Subarea 37.1), Central Mediterranean (Subarea 37.2), Eastern Mediterranean (Subarea 37.3), and Black Sea (Subarea 37.4) (Table 1) (Figure 3).
The Food and Agriculture Organization (FAO) has three main goals: the eradication of hunger, food insecurity and malnutrition; the elimination of poverty and the driving forward of economic and social progress for all; and, the sustainable management and utilization of natural resources, including land, water, air, climate and genetic resources for the benefit of present and future generations (FAO, 2015a).
FAO Fisheries and Aquaculture is one department of FAO. It contributes significantly to improving the well-being of poor and disadvantaged communities in developing countries and to achievement of several of the Millennium Development Goals, especially those related to poverty reduction and food and nutrition security, environmental protection and biodiversity. Its main mission is to strengthen global governance and the managerial and technical capacities of members and to lead consensus-building towards improved conservation and utilization of aquatic resources. In this context, the fisheries divisions of this department are employed in this study (FAO, 2015b).

Chondrichthyans: Status, fisheries and threats

Worldwide overview

Chondrichthyans make up one of the oldest and most ecologically diverse vertebrate families: sharks and their relatives, the batoids (including skates, rays, guitarfishes and sawfishes) and chimaeras are all chondrichthyans, or cartilaginous fishes (Fowler, 2005). Their classification according to Nelson (2006) comprises 14 orders and 54 families (ANNEX II). The class constitutes a conservative evolutionary group of around 1200 species which arose more than 400 million years ago and rapidly became top predators in aquatic food webs (Compagno, 1990; Kriwet et al., 2008). Most chondrichthyans are marine creatures, although many utilize estuaries, particularly as nurseries. Some even enter or are endemic to fresh water. Chondrichthyans can be present in immediate subtidal zone offshore to coastal, bathyal (200–2000m) and even abyssal habitats (>2000m). Most of them are predators, although some species may specialize on small benthic infaunal animals, such as polychaetes or amphipods. Other species, particularly the myliobatids, may consume hard-shelled bivalve molluscs. Most sharks consume fish and crustaceans, although white sharks prefer marine mammals, and basking sharks and whale sharks filter zooplankton from the sea (Fowler, 2005).
Cartilaginous fish are characterized by their conservative life-history traits. They have the latest maturity and the slowest reproduction of all vertebrates; they display long gestation periods and some of the highest levels of maternal investments in the animal kingdom (Cortés, 2000). These life history traits have been leading to low population growth rates and less compensation in juvenile survival, making them intensively vulnerable to elevated fishing exploitation and mortality (Musick, 1999b; Cortés, 2002; García et al., 2008; Dulvy and Forrest, 2010).
Elasmobranchs are essential to the balance of marine ecosystems. They have a key role, since they clean oceans of injured or sick prey, and thus contribute to maintain healthy populations. Furthermore, these top-predators regulate certain populations of carnivorous fish. The consequence of an over-exploitation of elasmobranchs would be an increase of forage fish, which would ultimately lead to algal and jellyfish blooms in oceans. Therefore, their decrease can lead to fishing down the food web and can disrupt ecosystem. For humains, it would mean an increase of the importance of organisms with less commercial significance and eating fish, shellfish and seafood would become scarcer.
The center of greatest chondrichthyan biodiversity lies in the Indo-West Pacific Region (Fowler, 2005) (Figure 4). Dulvy et al. (2014) identified three main hotspots where the biodiversity of sharks and rays was particularly seriously threatened – the Indo-Pacific Biodiversity Triangle, Red Sea, and the Mediterranean Sea – and claim that national and international action is required to protect them from overfishing.
Figure 4: The worldwide representation of the Elasmobranchii species richness (AquaMaps, 2013).
Chondrichthyans are often caught incidentally; however, they are mainly regarded as valuable bycatch of fisheries that focus on more productive teleost fish species, such as tunas or groundfishes (Stevens et al., 2005). They are mainly exploited for their meat, fins, livers and gill rakers carry high value; therefore, fishing pressure on chondrichthyans is increasing (Fowler et al., 2002; Clarke et al., 2006b; Clarke et al., 2007; Lack and Sant, 2009). The globalized trade to meet Asian demand for shark fin soup (traditional and expensive Chinese dish) is the main cause for shark fishing. This profitable trade also affects shark-like rays such as wedgefishes and sawfishes. It is mainly unregulated across the 86 countries and territories that exported large amounts of fins to Hong Kong (a major fin trade hub) in 2010 (Dulvy et al., 2014) (Figure 5). However, bans on ‗finning‘ (the removal of a shark‘s fins and discarding the carcass at sea is currently one of the regional and international management measures for sharks and rays through most Regional Fisheries Management Organizations (RFMOs) (Fowler and Séret, 2010).
Figure 5: The main shark and ray fishing nations are gray-shaded according to their percent share of the total average annual chondrichthyan landings reported to FAO from 1999 to 2009. The relative share of shark and ray fin trade exports to Hong Kong in 2010 are represented by fin size (Dulvy et al., 2014).
According to the Food and Agricultural Organization of the United Nations (FAO, 2011), elasmobranch landings have increased progressively to peak in 2003 and then showed a decline since then (Figure 6a); and rays have shown to dominate the landings in the past four decades (Figure 6b). Elasmobranch fisheries worldwide have expanded due to growing demand (particularly for highly valuable parts such as shark fins), the availability of new areas (i.e. open ocean, deep-sea bottom), and the use of highly technically equipped fishing vessels (Casey and Myers, 1998; Clarke et al., 2007; Worm et al., 2013). Moreover, most chondrichthyan catches are unregulated and often misidentified, unrecorded, aggregated, or discarded at sea, resulting in a lack of species-specific landings information, and the true catch is estimated 3 or 4 times greater than that reported (Barker and Schluessel, 2005; Clarke et al., 2006b; Ferretti et al., 2008; Iglésias et al., 2010; Bornatowski et al., 2013; Worm et al., 2013).
Figure 6: The temporal pattern of chondrichthyan fisheries catch landings. (A) The landed catch of chondrichthyans reported to the Food and Agriculture Organization of the United Nations from 1950 to 2009 up to the peak in 2003 (black) and subsequent decline (red). (B) The rising contribution of rays to the taxonomically-differentiated global reported landed catch: shark landings (light gray), ray landings (black), log ratio [rays/sharks], (red) (FAO, 2011; Dulvy et al., 2014).

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Mediterranean chondrichthyans

The Mediterranean Sea is identified as one of the three main hotspots where the diversity of sharks and rays is particularly seriously threatened (Dulvy et al., 2014). It holds 80 chondrichthyan species comprising 45 shark species from 17 families and 34 batoid species from 9 families and one chimaera species (almost 7% of total living chondrichthyans in the world) (Compagno, 2001; Compagno et al., 2005; Serena, 2005a; Cavanagh and Gibson, 2007). Out of these, 71 were assessed by the International Union for the Conservation of Nature (IUCN), where 42.25 percent are Vulnerable and Endangered to Critically Endangered, 18.31 percent are Near Threatened and 25.35 percent are Data Deficient (Cavanagh and Gibson, 2007) (Table 2).
Table 2: The number of chondrichthyan species in each IUCN Red List category (Cavanagh and Gibson, 2007).

Table of contents :

Chapter I: General Introduction
1. Overview
2. The Mediterranean Sea: Biodiversity, threats and fisheries
2.1. Geographical overview
2.2. Biodiversity
2.3. Threats
2.4. Fisheries
3. Chondrichthyans: Status, fisheries and threats
3.1. Worldwide overview
3.2. Chondrichthyan life history traits
3.3. Mediterranean chondrichthyans
3.4. Mediterranean chondrichthyan fisheries and threats
3.5. Various management tools for coastal ecosystems
3.6. Eastern Mediterranean chondrichthyans
4. Objectives of the study
Chapter II: Material and Methods
1. Characteristics of the study area
1.1. Overview of the region
1.2. The Lebanese coast
1.3. Currents and bathymetry
1.4. The fishery sector
2. Data collection
2.1. CIHEAM PESCA-Libano
2.2. Fishermen
Table of contents
2.3. Fisheries
3. Morphometric measurements
4. Biological indices and sexual maturity
4.1. Hepato-somatic index
4.2. Gonado-somatic index
4.3. Condition factor
4.4. Sexual maturity
5. Stomach contents analysis
5.1. Diet composition
5.2. Feeding strategy
6. Other data collected
7. Catch per unit effort
8. Biodiversity indices
8.1. The Shannon Index
8.2. Simpson‘s Index
8.3. Taxonomic diversity
9. Statistical analyses and regressions
9.1. Statistics
9.2. Linear regressions
9.3. Nonlinear regressions
9.3.1. Gonad weight and total length
9.3.2. Length-weight relationship
9.4. Logistic regressions
9.5. Maps and interpolation
Chapter III: The cartilaginous fishes of the Eastern Mediterranean: A literature review on the biology, ecology and geographic range of these species
1. Introduction
2. The cartilaginous fishes of the Levantine Basin and Aegean Sea
3. Cartilaginous fish observations and first records in the Eastern Mediterranean
4. Cartilaginous fishing in the Eastern Mediterranean
5. Age and growth
6. Length-weight relationships
7. Reproductive aspects and biological indices
7.1. Sharks
7.2. Batoids
8. Nutrition and feeding habits
9. Other studies
General conclusion
Chapter IV I- Diversity, distribution and abundance of elasmobranchs and the main influent factors along the coast of Lebanon (eastern Mediterranean)
1. Introduction
2. Materials and Methods
2.1. Description of the scientific survey: CIHEAM PESCA-Libano
2.2. Description of the fishery and fishermen data collection
2.3. Measures and biological parameters recorded after collection
2.4. Computation of the abundance index, statistical analyses and cartography
2.4.1. Computation of the abundance index
2.4.2. Factors impacting the abundance index of elasmobranch species
2.5. Biodiversity indices
3. Results
3.1. Scientific survey and fishery/fisherman data analysis
3.1.1. The scientific survey CPUE analysis: Depth, seasonal and spatial distribution
3.1.2. Fishery and fishermen data analyses: Seasonal and depth variation
3.2. Statistical analyses of the main factors impacting the abundance index
3.2.1. PERMANOVA of the survey and fishery and fishermen data
3.2.2. CCA of the survey and fishery and fishermen data
3.3. Spatial and seasonal diversity
4. Discussion
4.1. Variation of abundance index
4.2. Factors influencing spatial and seasonal diversity
II- The length-weight relationships of three sharks and five batoids in the Lebanese marine waters, eastern Mediterranean
1. Introduction
2. Materials and Methods
3. Results and Discussion
2.1. Sampling and study area
2.2. Biological measures
2.3. Stomach content analysis
2.4. Regressions and statistical analyses
3. Results
3.1. Sex ratio and length frequency distribution
3.2. Length-weight relationship
3.3. Sexual maturity and biological indices
3.4. Stomach content analysis
4. Discussion
1. Introduction
2. Materials and Methods
2.1. Sampling and study area
2.2. Morphometric and biological measurements
2.3. Catch per unit effort
2.4. Regressions and statistical analyses
3. Results
3.1. Morphometric measurements and depth distribution
3.2. Spatial distribution and gear
3.3. Sex ratio, length-frequency distribution and length-weight relationship
3.4. Sexual maturity and biological indices
Table of contents
3.5. Two-way Unbalanced ANOVA and Principal Component Analysis (PCA)
4. Discussion
4.1. Spatial and seasonal distribution, habitat and life cycle
4.2. Size and growth
4.3. Reproduction and biological indices
Chapter VII: General discussion, conclusion and perspectives
1. Elasmobranchs: Presence, diversity and fisheries in Lebanon
1.1. Presence and diversity
1.1.1. Abundance index
1.1.2. Spatio-temporal variations
1.1.3. Marine Protected Areas
1.1.4. Species identification
1.1.5. Lack of fishing logbooks
1.1.6. Fisheries
1.2. Length-weight relationships
2. Life history aspects and overexploitation
3. General situation and recommendations
4. Conclusion and perspectives
4.1. Perspectives about life history traits and fisheries
4.2. New study tools

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