Abundance, Distribution, Diversity and Zoogeography of Epipelagic Copepods Oﬀ the Egyptian Coast (Mediterranean Sea)

Egyptian Journal of Aquatic Research (2016) xxx, xxx–xxx

HOSTED BY National Institute of Oceanography and Fisheries Egyptian Journal of Aquatic Research

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FULL LENGTH ARTICLE Abundance, distribution, diversity and zoogeography of epipelagic copepods oﬀ the Egyptian Coast (Mediterranean Sea)

Howaida Y. Zakaria a,*, Abdel-Kader M. Hassan b, Fekry M. Abo-Senna b, Hussein A. El-Naggar b a National Institute of Oceanography and Fisheries, Alexandria, Egypt b Department of Zoology, Faculty of Science, Al-Azhar University (Boy), Cairo, Egypt

Received 11 May 2016; revised 31 October 2016; accepted 1 November 2016

KEYWORDS Abstract The abundance, distribution and diversity of epipelagic copepods were studied along the Copepods; Egyptian Mediterranean Coast during April, August, 2008, February, 2009 and 2010. The geo- Alien; graphical distribution and ecological affinities of the recorded species are presented in order to fol- Migration; low up the migrant species that recently entered in the study area. Copepoda was the most Egypt; dominant zooplankton group, representing 74.14% of the total zooplankton counts. The annual Eastern Mediterranean averages of copepod abundance in the coastal, shelf and offshore zones were 699.3, 609.7 and 555.7 ind.m3, respectively. Spring was the most productive and diversified season. 118 copepod species were identified in the study area; among them twelve species are recorded in the Mediter- ranean Sea for the first time and 41 species are new records in the Egyptian Mediterranean waters. The community was dominated by Oithona nana, Calocalanus pavo, Nannocalanus minor, Clauso- calanus arcuicornis and Paracalanus parvus. The study area could be considered as a crossroad for migration process from Atlantic Ocean in the west and Indian Ocean via Red Sea and Suez Canal from the south. In addition, the maritime activities in the Mediterranean Sea may have contributed into the change of copepod diversity in the study area where some species could have come to the Egyptian Coast from other water systems via ballast water. Ó 2016 Hosting by Elsevier B.V. on behalf of National Institute of Oceanography and Fisheries. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Introduction

The Mediterranean Sea is one of the most oligotrophic semi- * Corresponding author. enclosed basins and its marine life is heavily threatened by E-mail addresses: [email protected] (H.Y. Zakaria), habitat degradation mostly due to human activities (Lancelot [email protected] (A.-K.M. Hassan), hu_gar2000@ et al., 2002). Por (1978) declared that the Suez Canal is consid- yahoo.com (H.A. El-Naggar). ered as a link and barrier in plankton migration between the Peer review under responsibility of National Institute of Oceanography Red Sea and the Mediterranean. The Suez Canal’s being a nar- and Fisheries. http://dx.doi.org/10.1016/j.ejar.2016.11.001 1687-4285 Ó 2016 Hosting by Elsevier B.V. on behalf of National Institute of Oceanography and Fisheries. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Figure 1 Area of investigation and the locations of the sampling stations.

Table 1 Ecological affinities and geographical distribution of the recorded copepod species. Kingdom: Animalia. Ecological affinities Geographical distribution Phylum: Arthropoda Subphylum: Crustacea Class: Maxillopoda Subclass: Copepoda AO. PO. IO. RS. MS. EsM. EM. PS. Order: Calanoida Family: Calanidae Calanus helgolandicus (Claus, 1863)* t+ +++ Canthocalanus pauper (Giesbrecht, 1888) T + + + + + + + Cosmocalanus darwinii (Lubbock, 1860)* T, S + + + + + + + Mesocalanus tenuicornis (Dana, 1849) t, T + + + + + + + + Nannocalanus minor (Claus, 1863) t, T + + + + + + + + Neocalanus gracilis (Dana, 1849) t, T + + + + + + + Neocalanus plumchrus (Marukawa, 1921)*#A + + + Neocalanus robustior (Giesbrecht, 1888) t + + + + + + + + Family: Eucalanidae Pareucalanus attenuatus (Dana, 1849) t, T + + + + + + + + Subeucalanus crassus (Giesbrecht, 1888) t + + + + + + + + Subeucalanus monachus (Giesbrecht, 1888) t + + + + + + + + Subeucalanus subcrassus (Giesbrecht, 1888)* T+++++++ Family: Paracalanidae Acrocalanus gibber Giesbrecht, 1888* t, S + + + + + + + Calocalanus contractus Farran, 1926 t + + + + + + + + Calocalanus pavo (Dana, 1852) T, t + + + + + + + + Calocalanus styliremis Giesbrecht, 1888 P, t + + + + + + + + Ischnocalanus plumulosus (Claus, 1863) T, t + + + + + + + + Mecynocera clausi Thompson I.C., 1888 P, t + + + + + + + + Paracalanus parvus (Claus, 1863) Co, t, + + + + + + + + Family: Clausocalanidae Clausocalanus arcuicornis (Dana, 1849) t, Co + + + + + + + + Clausocalanus furcatus (Brady, 1883) T, t + + + + + + + + Clausocalanus ingens Frost and Flemin., 1968*#t + + + + Clausocalanus pergens Farran, 1926 t + + + + + + + + Pseudocalanus elongatus (Boeck, 1865) C + + + + + + Family: Aetideidae Aetideus armatus (Boeck, 1872)* S+++++++ Aetideus bradyi Scott A., 1909*#S +++ + Aetideus giesbrechti Cleve, 1904 T, t + + + + + + + Family: Scolecitrichidae Scolecithrix bradyi (Giesbrecht, 1888) t, C + + + + + + + Family: Euchaetidae Euchaeta acuta Giesbrecht, 1892 t + + + + + + + Euchaeta marina (Prestandrea, 1833) T, t + + + + + + + + Euchaeta media Giesbrecht, 1888* t, T, S + + + + + + Family: Phaennidae Phaenna spinifera Claus, 1863 t, S + + + + + + + + Family: Centropagidae Centropages abdominalis Sato, 1913*#t + + Centropages aucklandicus Kramer, 1895 t, C + + + + + Centropages bradyi Wheeler, 1900* Co + + + + + + Centropages elongatus Giesbrecht, 1896* T, t + + + + + Centropages kroyeri Giesbrecht, 1893 t + + + + + + + + Centropages tenuiremis Thom. and Scot. 1903*#T + + + Centropages violaceus (Claus, 1863) t + + + + + + + + Isias clavipes Boeck, 1865 t + + + + + Family: Temoridae Temora discaudata Giesbrecht, 1889* T, t + + + + + + + Temora stylifera (Dana, 1849) t + + + + + + + + Temora turbinata (Dana, 1849)* #T,S,t+++++ Family: Lucicutiidae Lucicutia flavicornis (Claus, 1863) t + + + + + + + + Lucicutia longicornis (Giesbrecht, 1889)* t++++++ Lucicutia ovalis (Giesbrecht, 1889) T, t + + + + + + + + Family: Heterorhabdidae

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Table 1 (continued) Kingdom: Animalia. Ecological aﬃnities Geographical distribution Phylum: Arthropoda Subphylum: Crustacea Class: Maxillopoda Subclass: Copepoda AO. PO. IO. RS. MS. EsM. EM. PS. Heterorhabdus papilliger (Claus, 1863) t + + + + + + + + Family: Metridinidae Pleuromamma abdominalis (Lubbock, 1856) t + + + + + + + + Pleuromamma borealis Dahl F., 1893* t+++++ Pleuromamma gracilis Claus, 1863 t + + + + + + + + Pleuromamma piseki Farran, 1929* t++++++ Pleuromamma robusta (Dahl F., 1893) t + + + + ++ ++ Pleuromamma xiphias (Giesbrecht, 1889) t + + + + ++ ++ Family: Augaptilidae Haloptilus longicornis (Claus, 1863) t + + + + ++ ++ Family: Acartiidae Acartia (Acartiura) clausi Giesbrecht, 1889 t + + + + + + + Acartia (Acartia) danae Giesbrecht, 1889 T, t + + + + ++ ++ Acartia (Acartiura) longiremis (Lilljeb., 1853) t + + + + + + Acartia (Acartia) negligens Dana, 1849 T, t + + + + + + + + Family: Candaciidae Candacia bipinnata (Giesbrecht, 1888)* T, t + + + + + + Candacia bispinosa (Claus, 1863) t + + + + + + + + Candacia bradyi Scott A., 1902*#T,S,t++++ Candacia curta (Dana, 1849)* T, S + + + + + + Candacia longimana (Claus, 1863) T, S + + + + + + + + Candacia simplex (Giesbrecht, 1889) t + + + + + + + + Candacia truncata (Dana, 1849)* T, S + + + + + + Order: Cyclopoida Family: Oithonidae Dioithona rigida Giesbrecht, 1896* T++++ Oithona fallax Farran, 1913* T+++++++ Oithona linearis Giesbrecht, 1891 t + + + + + + + Oithona nana Giesbrecht, 1893 T, t + + + + + + + + Oithona plumifera Baird, 1843 T, t + + + + + + + + Oithona robusta Giesbrecht, 1891* T++++++ Oithona setigera Dana, 1852 T, t + + + + + + + + Oithona similis Claus, 1866 Co, t + + + + + + + + Oithona tenuis Rosendorn, 1917* T, t + + + + + + + Family: Lubbockiidae Lubbockia squillimana Claus, 1863 t + + + + + + + + Family: Oncaeidae Monothula subtilis (Giesbre., 1893 [‘‘1892”]) t + + + + + + + + Oncaea atlantica Shmeleva, 1967* t+++++++ Oncaea lacinia Heron, Engl. and Damk., 1984*#C + + + Oncaea media Giesbrecht, 1891 T + + + + + + + + Oncaea mediterranea (Claus, 1863) T + + + + + + + + Oncaea venusta Philippi, 1843 t + + + + + + + + Spinoncaea ivlevi (Shmeleva, 1966)* T, t + + + + + + + Triconia conifera (Giesbrecht, 1891) T, t + + + + + + + + Triconia minuta (Giesbrecht, 1893 [‘‘1892”]) t + + + + + + + + Triconia similis (Sars G.O., 1918) t + + + + + + + + Family: Sapphirinidae Copilia longistylis Mori, 1932*#t ++ + Copilia quadrata Dana, 1849 T, t + + + + + + + + Sapphirina auronitens Claus, 1863 T, t + + + + + + + Sapphirina gastrica Giesbrecht, 1891 t + + + + + + + + Sapphirina metallina Dana, 1849 T, t + + + + + + + + Sapphirina nigromaculata Claus, 1863 t + + + + + + + + Sapphirina opalina Dana, 1849 T, S + + + + + + + + Sapphirina stellata Giesbrecht, 1891* S++++++ Family: Corycaeidae Agetus ﬂaccus (Giesbrecht, 1891) T, t + + + + + + + + Agetus limbatus (Brady, 1883) T, t + + + + + + + +

Table 1 (continued) Kingdom: Animalia. Ecological affinities Geographical distribution Phylum: Arthropoda Subphylum: Crustacea Class: Maxillopoda Subclass: Copepoda AO. PO. IO. RS. MS. EsM. EM. PS. Agetus typicus Krøyer, 1849 t + + + + + + + Corycaeus crassiusculus Dana, 1849* t+++++++ Corycaeus lautus Dana, 1849* T++++++ Corycaeus speciosus Dana, 1849 T, t + + + + + + + + Ditrichocorycaeus affinis McMurrich, 1916*#+++++ Ditrichocorycaeus andrewsi (Farran, 1911)* T, S + + + + + Ditrichocorycaeus asiaticus (Dahl F., 1894) *#++++ Onychocorycaeus catus (Dahl F., 1894)* T, t + + + + + + Onychocorycaeus ovalis (Claus, 1863) T + + + + + + + + Urocorycaeus furcifer (Claus, 1863) T, t + + + + + + + + Farranula carinata (Giesbrecht, 1891) T + + + + + + + + Farranula concinna (Dana, 1849)*#+++ Farranula curta (Farran, 1911)* +++++ + Farranula gracilis (Dana, 1849)* T, t + + + + + + + Farranula rostrata (Claus, 1863) T, t + + + + + + + + Family: Cyclopoida incertae sedis Pachos punctatum (Claus, 1863) t + + + + + + + + Order: Harpacticoida Family: Euterpinidae Euterpina acutifrons (Dana, 1847) T, t + + + + + + + + Family: Peltidiidae Goniopsyllus rostratus Brady, 1883 T + + + + + + + + Family: Ectinosomatidae Microsetella norvegica (Boeck, 1865) Co. + + + + + + + + Microsetella rosea (Dana, 1847) t + + + + + + + + Family: Miraciidae Macrosetella gracilis (Dana, 1847) T, t + + + + + + + + Family: Ameiridae Nitokra lacustris (Shmankevich, 1875) F + + + + + Order: Siphonostomatoida Family: Rataniidae Ratania flava Giesbrecht, 1893* T+++++++ Total 105 114 109 91 106 96 77 118 (AO = Atlantic Ocean, PO = Pacific Ocean, IO = Indian Ocean, RS = Red Sea, MS. = Mediterranean Sea, EsM. = Eastern Mediterranean, EM = Egyptian Mediterranean waters, PS. = Present Study, A = Arctic, T = Tropical, S = Subtropical, t = temperate, C = Cold water, Co = Cosmopolitan, F = Fresh water species, * = New recorded species in EM and # = New recorded species in MS). *Some publications were used for this table preparation such as Dowidar and El-Maghraby (1970), Hussein (1977), Tremblay and Anderson (1984), Nour El-Din (1987), Bottger-Schnack (1995), Khalil and Abd El-Rahman (1997), Abd El-Rahman (1999), Dowidar (2003), El-Serehy and Abdel-Rahman (2004), Nishibe and Ikeda (2004), Daly-Yahia et al. (2004), Abd El-Rahman (2005), Abd El-Rahman and Aboul-Ezz (2005), Somoue et al. (2005), Isari et al. (2006), Mckinnona et al. (2008), Raybaud et al. (2008), Bo¨ ttger-Schnack and Schnack (2009), Felder and Camp (2009), Homma and Yamaguchi (2010), Nowaczyk et al. (2011), Selifonova (2011), Dorgham et al. (2012), Zaafa et al. (2012), Arbakke (2013), Mikusˇ et al. (2013), Yamaguchi et al. (2013) and Razouls et al. (2005–2015). and 5.32 ml.l1 in winter, between 4.83 ml.l1 and 5.71 ml.l1 using CTD ‘‘Sea Bird 19+”, varied between 16.3 °C and in summer (Hemaida et al., 2008). 17.9 °C during winter and between 22 °C and 27.8 °C in sum- Four cruises were carried out for the purposes of the mon- mer. Zooplankton samples were collected from near bottom to itoring program ‘‘Marine Environment Division” on board the surface by vertical hauls using standard plankton net with total R/V SALSABEEL during April, 2008 (spring), August, 2008 length 225 cm, mouth diameter 50 cm and mesh size of 55 lm. (summer) and February, 2009, 2010 (winter). Zooplankton All samples were preserved in 4% neutral formalin solution samples were collected along six longitudinal sections perpen- and their volumes were concentrated to 100 ml. Three repli- dicular to the coast: at Fouka (F), Alam El-Rom (A), Marsa cates of 3 ml were transferred into a counting cell and each Matrouh (M), El-Shalia (El), Sidi Barany (S) and El-Sallum copepod species was identified and counted under a binocular (E) (Fig. 1). Each section comprised 3 stations covering the fol- research microscope. For quantitative work, the filtration coef- lowing depth zones: Coastal zone (depth 6 50 m), Shelf zone ficient of the net was considered equal to unity, thus the vol- (depth between 50 and 100 m) and offshore zone ume of water filtered was equal to pr2d, where r is the net (depth P 200 m). The water temperature of the study area diameter and d is the depth of water sampled. The abundance was measured from the surface to the bottom at all stations of the total copepod community was calculated and expressed

Table 2 Abundance (ind.m3) of copepod population per stations, sectors and seasons in the study area during 2008–09. Sectors Stations Seasons Average Average of sectors Spring 2008 Summer 2008 Winter 2009 Elsallom E1 313 290 443 348.67 407.96 ± 51.98 E2 510.5 565.5 261 445.67 E3 635 556 97.7 429.56 Sidi Brani S1 610 548 498 552 594.98 ± 76.04 S2 593.5 652 405 550.17 S3 904.7 647 496.7 682.78 Elshalia EL1 970 739 505 738.00 679.69 ± 53.07 EL2 707.5 776.5 516.5 666.83 EL3 651.3 779 472.3 634.22 Marsa Matrouh M1 1100 984 437 840.33 596.19 ± 233.56 M2 767.5 670 282.5 573.33 M3 446.7 519.3 158.7 374.89 Allam Elroum A1 540 614 600 584.67 619.85 ± 35.50 A2 772 653 542 655.67 A3 821.3 633.3 403 619.22 Fouka F1 1648 1100 648 1132 830.66 ± 274.99 F2 795.5 903.5 601 766.67 F3 711.7 701 367.3 593.30 Average of Seasons 749.9 ± 293.45 685.1 ± 183.82 429.7 ± 149.91 621.55 ± 137.17

Table 3 Temporal variations of the most dominant copepod species (% = Relative abundance of the total adult copepod counts) at the different seasons and sectors in the study area during 2008–09. Stations Seasons Spring Summer Winter Common species % Common species % Common species % El-Sallom Paracalanus paravus 12 Calocalanus pavo 14 Clausocalanus arcicornis 9.9 Oithona nana 11 Nannocalanus minor 11 Oithona nana 9 Oithona similis 10 Clausocalanus arcicornis 5.9 Paracalanus paravus 8.4 Sidi Brani Oithona nana 11 Nannocalanus minor 14 Farranula rostrata 7.4 Calocalanus pavo 8.2 Oithona nana 10 Clausocalanus arcicornis 5.7 Oithona plumifera 6 Centropages kroyeri 5.3 Calocalanus pavo 5.4 Subeucalanus crassus 5.4 El-Shalia Calocalanus pavo 10 Clausocalanus arcicornis 13 Subeucalanus crassus 7.4 Oithona nana 9.2 Calocalanus pavo 10 Clausocalanus arcicornis 7.4 Oncaea mediterranea 5,8 Nannocalanus minor 7.8 Calocalanus pavo 6.5 Oithona nana 6.5 Marsa Matrouh Oithona nana Paracalanus paravus 16 Nannocalanus minor 11 Oithona nana 11 12 Centropages abdominalis 8.6 Oncea venusta 11 Oithona plumifera 7.3 Oithona nana 7.5 Farranula rostrata 10 Allam Elroum Oithona nana 16 Nannocalanus minor 6.8 Subeucalanus crassus 9.1 Oithona plumifera 11 Paracalanus paravus 6.5 Oithona nana 8.2 Clausocalanus arcicornis 9.6 Temora stylifera 6.5 Oncaea mediterranea 8.2 Fouka Oithona nana 13 Calocalanus pavo 12 Farranula rostrata 12 Microstella norvigica 8.8 Oithona nana 9.2 Oithona nana 7.8 Oithona plumifera 6.8 Clausocalanus arcicornis 6.5 Paracalanus paravus 6.9 Most common Oithona nana 13 Nannocalanus minor 9.1 Farranula rostrata 8 Oithona plumifera 6.6 Calocalanus pavo 8.1 Oithona nana 7.3 Calocalanus pavo 5.7 Oithona nana 7 Clausocalanus arcicornis 6.7

During summer, the average abundance of copepods over Nannocalanus minor (5.6%) and Clausocalanus arcuicornis all stations was lower than in spring; 685.1 ± 183.8 ind.m3 (4.7%). and 36.7% of the total counts (Table 2). However, at some stations abundance values were higher in summer than in spring Spatial distribution of copepods e.g. E2, S2, El2 and El3. Copepod nauplii and copepodites constituted about 37.2% and 39.7% of the total copepod Overall the eastern sectors revealed higher abundance values counts respectively. Considering mean values over all stations, than the western ones, except transect of El-Shalia which pre- 3 Nannocalanus minor was the dominant species (62.1 ind.m sented higher mean value than the transect of Marsa Matrouh, and 9.1% of the total adult copepod counts) followed by Calo- due to the increased values in the shelf and offshore stations of calanus pavo (8.1%) and Oithona nana (7%) (Table 3). Clauso- El-Shalia (Table 2). Comparing the annual mean values, cope- calanus arcuicornis was found in high numbers in the area of pod abundance was a maximum in Fouka (830.7 ± 275 ind. El-Shalia (dominant species) as well as in the areas of El- m3) and minimum in El-Sallum (408 ± 51 ind.m3). Annual Sallum and Fouka. average values decreased from the coastal zone (699.3 In winter 2009, copepods constituted about 23.1% of the ± 270.7 ind.m3) toward the shelf (609.7 ± 111.2 ind.m3) 3 total counts (with an average of 429.7 ± 149.9 ind.m ). and the offshore zone (555.7 ± 123.6 ind.m3). However this Copepod nauplii and copepodites constituted about 39.1% general decreasing pattern of abundance from coast to off- and 36.2% of the total copepod counts respectively. During shore waters was not observed in all seasons and transects. this period Farranula rostrata (7.8% of the total adult copepod An opposite pattern (increase toward the offshore zone) was counts), Oithona nana (7.3%) and Clausocalanus arcuicornis observed at El-Sallum, Sidi Barany and Alam El-Rom in (6.7%) were the most abundant species (Table 3). Subeu- spring and at El-Shalia during summer. In winter no clear pat- calanus crassus was the dominant species at the areas of El- tern was observed in Sidi Barany (Table 2). The abundance Shalia and Alam El-Rom. The average copepod abundance values of nauplii and copepodites decreased westward in the decreased in winter 2010 at all depth zones compared to winter coastal and shelf zones (Fig. 3). Nauplii and copepodites were 2009 (Fig. 2). Values declined from coastal zone to the shelf very abundant at the coastal stations of Fouka and Marsa 3 3 and offshore zones (424.3 ind.m , 343.8 ind.m and Matrouh whereas their numbers decreased from the coast 3 302.6 ind.m , respectively). The decrease of copepod numbers toward the offshore zone in Fouka, Marsa Matrouh and El- in winter 2010 compared to winter 2009 was attributed to the Shalia (Fig. 3). Considering the average values over all areas, decrease in copepod nauplii and copepodites numbers, while Oithona nana was the dominant species in the coastal, shelf the abundance values of adult copepods ﬂuctuated within nar- and offshore waters (Table 4). In the coastal zone; Clauso- row range (Fig. 2). In winter 2010, the most abundant species calanus arcuicornis was the second dominant species followed were Oithona nana (7.9% of the total adult copepod counts), by Calocalanus pavo. An inverse rank was observed in the shelf

Adult copepod Nauplii larvae Copepodite stages 600

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0 Winter 2009 Winter 2010 Winter 2009 Winter 2010 Winter 2009 Winter 2010

Coastal Shelf Offshore

Comparative Seasons

Figure 2 Abundance (ind.m3) of the copepod population (adult, nauplii and copepodite stages) at the different three depth zones; coastal, shelf and offshore during winter in successive two years (2009–2010). zone, while Nannocalanus minor was the second dominant spe- due to spatial and temporal distribution and interactions cies in the offshore zone followed by Calocalanus pavo between them (Table 5). (Table 4). Discussion Copepod diversity Copepoda was the most dominant zooplankton group in the The highest number of copepod species was found in spring study area, representing 74.14% of the total zooplankton (95 species) and the lowest in winter (70 species). Regarding counts. Comparison between the present results and the previ- the spatial distribution, the maximum number of species was ous studies in the Egyptian Mediterranean waters, using the recorded in Sidi Barany area (86 species), followed by El- same mesh size nets, indicated that, the relative abundance Shalia (81 species) and Fouka (79 species), while the minimum of copepods in the present study was higher than that previ- was recorded at Marsa Matrouh (60 species) (Fig. 4). On the ously found in the coastal waters (Dowidar et al., 1983; other hand, the species number increased from the coastal zone Aboul-Ezz, 1994; Abdel-Aziz, 2002; Zakaria, 2006a, 2007a; (73 species) toward the shelf zone (93 species) and the offshore Abou Zaid et al., 2014) and lower than that in the offshore (102 species). The highest value of species richness was esti- (Abdel Aziz and Aboul-Ezz, 2003). The number of recorded mated at Sidi Barany (10.41), while the lowest at Marsa species in the present study was lower than that previously Matrouh (7.8) (Fig. 5). Mean value over seasons and stations recorded in the coastal waters by Dowidar and El- of the Shannon-Wiener diversity index was a maximum at Sidi Maghraby, 1970 and Dowidar and El-Maghraby, 1973 and Barany (5.47) and minimum at Marsa Matrouh (5.11) (Fig. 5). higher than that recorded by Aboul-Ezz (1994) and Abou Similarly to the number of species, species richness increased Zaid et al. (2014). In the offshore waters, the number of cope- from the coastal (4.47–6.36) toward the shelf (6.78–8.84) and pod species was higher than that previously recorded by Abdel the offshore zone (8.27–11.65). The values of Shannon–Wiener Aziz and Aboul-Ezz (2003). The differences in the relative diversity index followed the same spatial pattern; 2.48–3.23 in abundance and the diversity of copepod population between the coastal zone, 2.75–3.51 in the shelf and 2.73–3.44 in the the present work and the previous studies may be attributed offshore. to the difference of study sites along the Egyptian Mediter- The results of ANOVA analysis showed that, the p-values ranean Coast, period of collection and climate variability of all variables are quite small (p < 0.050) suggesting that which have an effect on plankton migration process there are signiﬁcance of seasonal and spatial distributions of (Irogoien et al., 2004; Hays et al., 2005 and Zakaria, 2014). abundance, diversity and richness. This means that, there is Comparison between the present data and that previously no effect on the abundance, diversity and richness of copepod recorded in the Egyptian Mediterranean waters indicated that,

Adult copepod Nauplii larvae Copepodite stages 1200

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200

0 F3 F2 F1 El1 E1 E2 E3 M3 S1 M1 M2 S2 A3 A1 A2 El3 El2 S3 Coastal Shelf Offshore Sectors

Figure 3 Abundance (ind.m3) of the copepod population (adult, nauplii and copepodite stages) at the different three depth zones; coastal, shelf and offshore in the study area during 2008–09. forty-one copepod species are new records in the Egyptian and Ikeda, 2004) and may be transported to the study area Mediterranean waters. Most of these species occur in the entire via ballast water. Canthocalanus pauper is common in the East- Mediterranean Sea or in the western Mediterranean (Razouls ern Mediterranean and was in fact transferred to the Black Sea et al., 2005–2015) and their occurrence should be due to the by ballast waters (Selifonova et al., 2008 Selifonova, 2011). sampling effort of the present study (wide sampling area and The finding of the all above species in the Egyptian Mediter- four sampling seasons). Some of them e.g. Candacia truncata, ranean waters suggests a migration through the Suez Canal Centropages elongates, Dioithona rigida and Ditrichocorycaeus or their transport by ballast waters. On the other side, the andrewsi have probably migrated from the Red Sea via Suez Egyptian Mediterranean waters are characterized by the pres- Canal, since they are not recorded in the Atlantic Ocean ence of different water masses which converge and mix: the (Khalil and Abd El-Rahman, 1997; Abd El-Rahman, 1999, surface water mass of minimum salinity (38.6–38.8 ppt) and 2005; Dowidar, 2003; El-Serehy and Abdel-Rahman, 2004; maximum oxygen concentration (>5.2 ml/l) which is of Atlan- Abd El-Rahman and Aboul-Ezz, 2005; Mckinnona et al., tic origin and extends 50–150 m in depth; the intermediate 2008; Dorgham et al., 2012). Among the new record species water mass of maximum salinity (38.9–39.1 ppt) which extends during the present study, twelve copepod species are recorded below 150 m to about 300–400 m depth; and the deep waters in the Mediterranean Sea for the first time. The majority of which are of eastern Mediterranean origin (Said and Eid, these species originate from the Indian and Pacific oceans 1994). The water circulation along the Egyptian Mediter- and some from the Red Sea also, namely Neocalanus plum- ranean Coast is dominated by the Atlantic water inflow along chrus, Centropages abdominalis, Centropages tenuiremis, Can- the North African Coast and by the Mersa Matruh and El- dacia bradyi, Ditrichocorycaeus asiaticus, Copilia longistylis Arish gyres. The Mersa Matruh gyre exhibits a strong winter and Farranula concinna (Razouls et al., 2005–2015). Neo- to summer variability, reversing from anticyclonic to cyclonic calanus plumchrus epipelagic arctic species is common in the (Said and Rajkovic, 1996). Some of the recorded species dur- Pacific Ocean and new geographical record in the Red Sea ing the present study might come from the Atlantic Ocean (Abd El-Rahman, 1999). Centropages abdominalis was (weren’t previously recorded in the Suez Canal, the Red Sea recorded only in the Pacific Ocean (Homma and Yamaguchi, and the Indian Ocean) such as Calanus helgolandicus 2010; Yamaguchi et al., 2013; Razouls et al., 2005–2015) and (Beaugrand et al., 2001; Somoue et al., 2005; Zaafa et al., may be transported via ballast water (Perkovic et al., 2004; 2012; Arbakke, 2013), it was common in the neritic waters of David et al., 2007). Oncaea lacinia, had been reported to occur the Atlantic Ocean and frequent in the Mediterranean offshore in high-latitude seas of both hemispheres (Heron and waters, coming from the subsurface or deep waters by upwel- Bradford-Grieve, 1995; Heron and Frost, 2000), it was com- ling (Vives, 1976). It was previously recorded in Ligurian Sea mon in Oyashio region, western subarctic Pacific (Nishibe (Raybaud et al., 2008), Balearic Sea (Fernandez de Puelles

Table 4 Spatial variations of the most dominant copepod species (% = Relative abundance from total adult copepods) at the different zones and sectors in the study area during 2008–09. Stations Zones Coastal Shelf Oﬀshore Common species % Common species % Common species % El-Sallom Paracalanus paravus 10.7 Calocalanus pavo 11.4 Calocalanus pavo 11.3 Oithona similis 6.5 Nannocalanus minor 7.8 Oithona nana 10.4 Calocalanus pavo 6.3 Oithona nana 7.8 Nannocalanus minor 8.8 Oithona nana 6.3 Paracalanus paravus 7.8 Sidi Brani Oithona nanaNannocalanus minor 8 Oithona nana 11.1 Oithona nana 8.2 6.8 Calocalanus pavo 9.9 Nannocalanus minor 6.1 Microstella norvigica 6.4 Oithona plumifera 6.1 Oithona similis 5.1 Paracalanus paravus 6.4 El-Shalia Clausocalanus arcicornis 12.2 Calocalanus pavo 8.4 Calocalanus pavo 7.8 Calocalanus pavo 11 Oithona nana 7.3 Nannocalanus minor 6.9 Oithona nana 7.7 Nannocalanus minor 5.6 Oithona nana 6.5 Marsa Matrouh Oithona nana 13.7 Oithona nana 11.1 Oithona nana 12.2 Paracalanus paravus 10.5 Paracalanus paravus 6.9 Nannocalanus minor 10.1 Oithona plumifera 6.3 Oncea venusta 5 Paracalanus paravus 7.1 Allam Elroum Oithona nana 14.5 Oithona nana 11.4 Oithona nana 10.2 Oithona plumifera 11 Clausocalanus arcicornis 9.3 Clausocalanus arcicornis 6.2 Clausocalanus arcicornis 9 Oithona plumifera 6.3 oithona setiger 5.4 Fouka Oithona nana 12.4 Oithona nana 9.8 Oithona nana 10.1 Oithona plumifera 7.7 Clausocalanus arcicornis 8.5 Clausocalanus arcicornis 7.6 Microstella norvigica 6.8 Calocalanus pavo 6.1 Calocalanus pavo 7 Most common Oithona nana 10.6 Oithona nana 9.7 Oithona nana 9.2 Clausocalanus arcicornis 6.6 Calocalanus pavo 7.1 Nannocalanus minor 6.7 Calocalanus pavo 6.1 Clausocalanus arcicornis 6.2 Calocalanus pavo 6.3

Spring 2008 Summer 2008 Winter 2009 Total diversity 100

40 Diversity (No. of species)

0 El-Sallom Sidi Brani El-Shalia Marsa Allam Elroum Fouka Matrouh

Sections

Figure 4 Spatial distribution of copepod diversity (No. of species) at the different seasons in the study area during (2008–09). et al., 2008), Alboran Sea (Andersen et al., 2004) and in the chocorycaeus afﬁnis, Aetideus bradyi, Clausocalanus ingens Levantine Basin of the Eastern Mediterranean Koppelmann and Oncaea lacinia occur in the Atlantic, Indian and Paciﬁc et al., 2009). Other species, namely Temora turbinata, Ditri- oceans (Razouls et al., 2005–2015) and could have migrated

Species richness Shanon index 12 5.5

10 5.4

8 5.3

6 5.2

4 5.1 index Shannon Species rechness

2 5

0 4.9 El-Sallom Sidi Brani El-Shalia Marsa Allam Elroum Fouka Matrouh Sectors

Figure 5 Spatial distribution of the diversity indices (species richness and Shannon index) in the study area during 2008.

Table 5 Analysis of variance (ANOVA) partitioning the total variance of abundance/richness/diversity in copepods per season/ distance in the study area during 2008–09. Analysis of variance (ANOVA) Degrees of freedom Abundance Diversity Species richness FP-value FP-value FP-value Temporal distribution 2 24.45 0.000 9.91 0.000 5.76 0.007 Spatial distribution 17 4.75 0.000 8.09 0.000 9.66 0.000 Error 34 Total 53 either through the Gibraltar Strait or the Suez Canal. How- the Mediterranean flow toward the Red Sea (Wust, 1934; ever, many of the recorded species during the present study Morcos, 1960). In addition, climate change favored the arrival have wide geographical distribution and were previously and establishment of alien species in the Mediterranean Sea recorded in other Mediterranean coasts (Daly-Yahia et al., (Raitsos et al., 2010; Zakaria, 2014). The migration of plank- 2004; Isari et al., 2006; Raybaud et al., 2008; Bo¨ ttger- ton organisms from the Red Sea was further enhanced by Schnack and Schnack, 2009; Nowaczyk et al., 2011; Mikus the observed rise in temperature and salinity (Lakkis and et al., 2013). The magnitude of new record species in the pre- Zeidane, 2004). This may declare the increase in number of sent study may be due to the migration activity from other Indo-Pacific species recoded during the present study (Neo- water systems to the Mediterranean. It is known that, more calanus plumchrus, Centropages abdominalis, Centropages than 200 invertebrates and fish species had succeeded in cross- aucklandicus, Centropages elongatus, Centropages tenuiremis, ing the Suez Canal and established themselves in the Eastern Candacia bradyi, Candacia truncata, Dioithona rigida, Copilia Mediterranean where the salinity and temperature conditions longistylis, Ditrichocorycaeus andrewsi, Ditrichocorycaeus asi- were nearly the same as their original environment (Halim aticus, Farranula concinna). These species may have migrated et al., 1995). According to more recent estimation, approxi- to the Mediterranean from Indian and Pacific Oceans across mately 500 species have passed the Suez Canal and were intro- the Red Sea. On the other side, Zaafa et al. (2012) supposed duced in the Mediterranean Sea either unaided (Lessepsian an increase in zooplankton migration in the Mediterranean immigrants) or ship mediated (Zenetos et al., 2012). The infil- Sea from Atlantic Ocean due to the continuous replenishment tration of species successfully passing through the Suez Canal of plankton populations by the inflow of Atlantic water from the Red Sea into the Mediterranean Sea seems to con- through the Strait of Gibraltar. Dorgham et al. (2012) pre- tinue for most of the year, except for two or three months dur- sumed that copepod species considered as immigrants from ing the summer, when the process is reversed and the waters of the Red Sea, may in fact come from the Atlantic Ocean. This

Please cite this article in press as: Zakaria, H.Y. et al., Abundance, distribution, diversity and zoogeography of epipelagic copepods off the Egyptian Coast (Mediter- ranean Sea). Egyptian Journal of Aquatic Research (2016), http://dx.doi.org/10.1016/j.ejar.2016.11.001 12 H.Y. Zakaria et al. assumption is based on the fact that these organisms occur Zakaria, 2006a; Zakaria et al., 2007; Aboul Ezz et al., 2014), as both in the eastern and the western Mediterranean and inhabit well as in other Mediterranean coastal areas where sampling the Atlantic Ocean and the Gibraltar Strait but are absent was performed by small mesh size nets (Daly-Yahia et al., from the Suez Canal. It can be presumed that some zooplank- 2004; Vidjak et al., 2007). In the coastal and shelf zone of ton species widespread in the world ocean entered the Mediter- the present study Clausocalanus arcuicornis and Calocalanus ranean Sea through the Gibraltar Strait and the Suez Canal. pavo were found abundant accompanied by Nannocalanus They proved again that, the Red Sea species play an important minor and Paracalanus parvus. The latter species together with role in formation of the flora and fauna of the eastern Mediter- Euterpina acutifrons were reported as dominant species in the ranean, especially along the southeastern coast. However, it coastal waters (Aboul-Ezz, 1994; Abdel-Aziz, 2002; Zakaria, seems that, the copepod fauna in the eastern Mediterranean 2006a; Zakaria et al., 2007; Vidjak et al., 2007; Aboul Ezz is a mixture of the Red Sea tropical fauna and the western et al., 2014). Clausocalanus arcuicornis and Paracalanus parvus Mediterranean which has more Atlantic characteristics. The are among the most abundant copepods in the Mediterranean present results reveal that among the copepod species recorded coastal waters (Gaudy, 1985; Lakkis, 1990; Champalbert, in the Egyptian Mediterranean waters 89.8% of them occur in 1996; Daly-Yahia et al., 2004). The relative abundance of the Atlantic Ocean, 96.6% in the Pacific Ocean, 92.4% in the Oithona nana decreased toward the offshore waters, whereas Indian Ocean and 77.12% in the Red Sea. that of Calocalanus pavo and Nannocalanus minor increased. The temporal distribution of copepod abundance and Indeed, the latter two species seem to prefer deeper than shal- diversity at all depth zones in the study area indicated that, lower stations (Siokou-Frangou, 1996). spring was the highest productive and diversified season and The diversity index is used as a measure of ecological winter was the lowest. This seasonal pattern was also observed ‘‘health” or stability of the biotic communities. The present previously in the coastal zone of Egypt (Aboul Ezz et al., 2014) data of the diversity index reveals that, the study area is highly and in the offshore zone of the Eastern Mediterranean (Abdel diversified compared to other Mediterranean regions e.g., the Aziz and Aboul-Ezz, 2003; Vidjak et al., 2007). Daly-Yahia Bay of Tunis where Shannon–Wiener index ranged between et al., 2004 reported that, spring was the flourishing period 3.83 and 0.24 (Daly-Yahia et al., 2004). Bojanic et al., 2012 of copepods in the Bay of Tunis, attributing it to synchronous found that, zooplankton abundance and species dominance blooming of diatoms and/or dinoflagellates. Seasonal fluctua- increased proportionally with increased trophic state. They tions in copepod nauplii followed a unimodal cycle, providing concluded that, the species richness was positively related to evidence of the importance of egg production during spring, overall abundance temporally and was also affected by envi- whereas during winter abundance of nauplii significantly ronmental trophic state. The analysis of variance which per- decreased indicating low egg production during this season formed to assess the significant difference of copepod (Daly-Yahia et al., 2004). However, the environmental condi- abundance/diversity/richness in relation to temporal and spa- tions in the study area during spring seem to be optimum for tial distributions, indicated a significant difference between the growth and breeding of many invertebrates (Zakaria, all temporal distribution and copepod abundance/diversity/ 1992). In the study area, Oithona nana, Oithona plumifera richness (F = 24.45, 9.91 and 5.76 for copepod abundance, and Calocalanus pavo were the most dominant species during diversity and richness respectively; and P < 0.050 for all). spring, Nannocalanus minor, Calocalanus pavo and Oithona Also, there are significant differences between temporal distri- nana dominated during summer, Farranula rostrata, Oithona bution and copepod abundance/diversity/ richness (F = 4.75, nana and Clausocalanus arcuicornis dominated during winter. 8.09 and 9.66 for copepod abundance, diversity and richness The dominance of Oithona nana during spring and summer respectively; and P < 0.050 for all). in the study area is a common feature with the Bay of Tunis, where a 55 lm mesh size net was used (Daly-Yahia et al., Conclusion 2004). Calocalanus pavo dominant in the study area with maxima in summer showed a different seasonal pattern in the Bay The study area is considered as a middle station for migration of Tunis where high values were recorded in autumn–winter. process from Atlantic Ocean in the west and Indian Ocean via Similarly, the seasonal variability of Clausocalanus arcuicornis Red Sea and Suez Canal from the south. Recently, the widen- was different between the study area (maxima in winter) and ing and deepening of the Suez Canal have created conditions the Bay of Tunis (maxima in summer-autumn) (Daly-Yahia which are likely to accelerate the biological exchanges between et al., 2004). In the latter area apart Oithona nana, the copepod the Red Sea and the Mediterranean. On the other side, as a species; Oithona helgolandica and Acartia clausi, dominated consequence of the retention of Nile waters, the barrier of during spring, Centropages kroyeri and Euterpina acutifrons lower salinity disappeared and the Atlantic species transported in summer (Daly-Yahia et al., 2004). by surface Modified Atlantic Water current circulating along The spatial distribution of copepod abundance indicated the North African Coast could have established themselves that, the eastern sectors of the study area were more abundant in the study area. In addition, the maritime activities in the than the western ones. In contrast, species richness and diver- Mediterranean Sea may have contributed in the change of sity index values followed an opposite pattern, in accordance copepod diversity where some species may have arrived to with previous study (Abdel Aziz and Aboul-Ezz, 2003). 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