Asian Journal of Biology

4(4): 1-16, 2017; Article no.AJOB.37671 ISSN: 2456-7124

First Report on Zooplankton Abundance and Composition in Hadhramout Coast, Gulf of Aden

Ali Attaala Mukhaysin 1* , Salem Rubaea Bazar 1 and Moteah Sheikh Aideed 2

1Faculty of Environmental Sciences and Marine Biology, Hadhramout University, Mukalla, Yemen. 2Freelance Marine Biology, Mukalla, Yemen.

Authors’ contributions

This work was carried out in collaboration between all authors. Author AAM designed the study, wrote the protocol, and wrote the draft of the manuscript. Author SRB managed the analyses of the study, managed the literature searches. Author MSA performed the statistical analysis. All authors read and approved the final manuscript.

Article Information

DOI: 10.9734/AJOB/2017/37671 Editor(s): (1) Behrouz behrouzi-Rad, Associate Professor, Department of Environment, Ahvaz Branch, Islamic Azad University, Tehran, Iran. Reviewers: (1) Fábio Henrique Portella Corrêa de Oliveira, Universidade Federal Rural de Pernambuco, Brazil. (2) Hanife Özbay, University of Nevsehir, Turkey. (3) Jorge Castro Mejia, Universidad Autonoma Metropolitana Xochimilco, Mexico. Complete Peer review History: http://www.sciencedomain.org/review-history/22463

Received 24 th October 2017 Accepted 22 nd December 2017 Original Research Article Published 27 th December 2017

ABSTRACT

Five stations were investigated to represent the Hadhramout coast in the Gulf of Aden. This area, totally or partially, is under the influence of the western Indian Ocean seasonal monsoons. Zooplankton was collected monthly during daytime in 2009 – 2010 with vertical towing of 200 µm mesh plankton nets. The zooplankton community was characterized by its high variability and diversity. 226 taxa of zooplankton were identified in the coast through the different seasons. Zooplankton community was dominated by during the four seasons, followed by Euphausiids and Chaetognatha. The peak of zooplankton abundance was in northeast monsoon. The present results showed that the composition and distribution of zooplankton differed between the monsoon seasons, but little between the stations.

Keywords: Zooplankton; Gulf of Aden; copepods; hadhramout coast; coastal upwelling.

______

*Corresponding author: E-mail: [email protected];

Mukhaysin et al.; AJOB, 4(4): 1-16, 2017; Article no.AJOB.37671

1. INTRODUCTION corridors of Socotra Archipelago which are rich in phytoplankton [9]. This coastal upwelling brings Zooplankton plays a significant role as a key link nutrients to the surface, where the light, creating in any local food chain, nutritional levels, and a fuel to photosynthesis and phytoplankton transporting energy from bacteria and growth feed to zooplankton and consequently to phytoplankton to macroinvertebrates and fish. fishes. The structure of plankton communities in any body of coastal waters is also important to It is not new talking about the environmental commercial fisheries. importance of zooplankton in the marine water bodies, particularly the most abundant Hadhramout coast is well known by a multi component, the Copepods, in pelagic food webs species fishery. Its fishing and oceanic properties of Global Ocean. These organisms are often represents a system of the Upwelling considered distinctive component of the phenomenon in the Gulf of Aden, which occur zooplankton community in a lot of marine along most of its regions including a Hadhramout conditions and play a key role in converting coast during the months of summer monsoon nutrients and energy through the trophic levels from May to September. The productivity that [10,11]. Quantitative studies of the dynamics of a follows this phenomenon sustains the catches of nearshore zooplankton community along the considerable number of fishes, and coast of Gulf of Aden are still fragmentary mollusks of commercial interest. Hadhramout [12,13,14]. In contrast, the taxonomy and coast characterized by riches of primary seasonal standing stock of the phytoplankton productivity of 685 mg C / m 2 / day, secondary community in the coastal waters of the Gulf of productivity ranging between 14 - 68 mg C / m 2 / Aden and Hadhramout area has been day [1,2], and contributes by an enormous share investigated but occasionally [15,16,17]. of the quantities of fish landing in the whole Yemen - 29% (for 2012). This coast is There is a big scarcity of knowledge about the characterized by abundance of Indian oil spatial and temporal dynamics of zooplankton in sardines Sardinella longiceps , Indian mackerel the northern coast of the Gulf of Aden, in Rastrelliger kanagurta and yellowfin tuna particular the coast of Hadhramout. In addition Thunnus albacares . Latter supports coastal there is no information on the zooplankton surface and pelagic catches of the Gulf of Aden productivity and diversity on the coast of for more than 30000 tons of fish [3,4]. Hadhramout. Thus, the main objective of our study is to evaluate the possibility of securing zooplankton is the main organisms in biological productivity to support the aquatic ecosystems, as they represent an sustainability and development of the coastal important link in marine food webs. They fisheries. transport materials and energy from primary phytoplankton production to a higher level of 2. MATERIALS AND METHODS many species of fish and other marine . A detailed description of the study area and East of the Gulf of Aden includes the stations sampling for some physical indicators Hadhramout coast considered one of the most (temperature and salinity) and chemical global ocean parts by productivity; its average (dissolved oxygen, nutrients: phosphorus, productivity for more than a hundred kilometers nitrates, silicate, and chlorophyll a) are presented from the beach is more than the productivity of in Ali and Bazar [17]. Analysis of biomarkers other Upwelling areas, like Peru Coast and West samples were taken from all water columns Africa [5,6], higher productivity have been according to the total depth, which ranges observed in this region (more than 1000 mg / m 3) between 100 - 90 meters and surface of water. around August, at the end of the south-western monsoon; while less productivity (about 400 mg / Zooplankton samples were carried out in the five m3) in January through the northeastern stations representing the coast of Hadhramout monsoon [7,8]. monthly during the 2010 (Fig. 1). We used for this purpose zooplankton open nets with mouth The Gulf of Aden and its Hadhramout coast are diameter of 50 and 80 cm (0.25 and 0.4 m 2) with located directly under the influence of the sub 200 microns mesh. Sample were taken by Somali sea current approaches, in summer vertically open nets from near the bottom - 5 (upwelling phenomenon), mainly through meters above the bottom and up to the surface,

2

Mukhaysin et al.; AJOB, 4(4): 1-16, 2017; Article no.AJOB.37671

with filtered water volume calculated through the hours until reaching to the lab. In the laboratory it net, which represents the multiplication the net has been separated into several homogeneous opening area by distance, which was to contain parts according to the test program for (the depth of station). In our study, we chose a measuring the mass, a part re-saved in 10% depth of 90 meters per station because fading of phosphate buffered formalin in sea water for the thermocline in the coastal area in most months of microscopic study for identifying a taxonomic the year typically can be found at depths greater belonging. To determining the dry weight, the than 100 meters [18,19]. secondary sample of specified volume was filtered through filter paper (Whatman GF/C Dry weight analyses were performed on filters, diameter 5.5 cm) to a specified weight preserved zooplankton samples to examine before burning, and wash with the sample with temporal variability in biomass. The procedure, distilled water and then dried under 60 Celsius involved dividing the samples into halves using a for 36-48 hours (till constancy weight) then be modified sand splitter [20]. Large scyphozoan calculated weight, and therefore the dry mass of medusae and juvenile fishes were not the Zooplankton was weighted. considered in dry weight measurements. 3 The Mass (mg Dry wt / m ) is calculated as Each sample was divided into two parts and after follows: rinsing the splitting apparatus, one half was Biomass (mg/ l) = [zoopl. dry weight (gm) / returned to the original sample jar, preserved in 3 100% formalin, and stored in the Faculty volume of filtered water (m )] × 1000, concerned laboratory. The remaining half-sample Where the filtered volume of water entering the was flushed in running tap water for five minutes, plankton net, it was calculated as follow: drained, and poured into a tared, aluminum foil tray. Samples were dried to constant weight at V= ð r 2 d 56°C for 18 to 24 hours [21]. Newly removed samples were cooled in desiccators for 10 In the formula, V is the volume of water filtered minutes and then weighed to the nearest by net, r is the radius of the hoop of the net and d milligram on the Mettler 3 F16GN balance. is the length of the water column transverse by the net [22]. Monthly samples of zooplankton were collected early in the morning at 6 – 8 hours; it has been The samples were examined to study the preserved by adding formalin 4%, the samples abundance and belonging zooplankton by taking have been saved in an icebox for about 2 to 3 several secondary samples by 5 ml of the

Fig. 1. Study area and sample sites in coast of Hadhramout, geographical locations are as follows: Balhaf (BirAli) (N13° 55 ′, E48 °26 ′), Broom (N 14°22 ′, E49°00 ′), Mukalla (N14°48 ′, E50°00 ′), Sheher (N14 °43 ′, E49 °40 ′), Sharma (N14 °48 ′, E50 °00 ′)

3

Mukhaysin et al.; AJOB, 4(4): 1-16, 2017; Article no.AJOB.37671

sample which well mixed by using a stempel characterized by abundance of species of genus pipette (piston pipette) and Bogarov chamber Oncaea. Table 1 shows a picture of the [23] to examine the samples to count and numerical abundance in Hadhramout coast. As it diagnosis by anatomical microscope under is shown in the table, the 171 species of the magnification ranged between 40 and 200 times. copepods are belonging to 20 genera and Counting has been for each slide cells (Bogarov several families. This kind of numerical chamber); a diagnosis of zooplankton to species abundance of the was recorded in or genus despite the difficulty of diagnosis. The many studies to some areas of the Indian Ocean abundance of some groups and for the [31,32,13,33]. zooplankton are calculated by re-calculation to cubic meter, depending on the volume of water From the results, it is seen that the most drawn by used planktonic net. For an accurate widespread and abundant in Hadhramout coast assessment of the population density we adhere represent a group of Copepods, which accounted to necessity to do multiple repetitions in the as average of more than 83%, followed by calculation of the organisms in a sub-sample. groups Euphausiids that formed 9%; Chaetognath, Decapods and Tunicate formed by It has been emphasis in analysis of zooplankton 2% each (Fig. 2). samples, at four-time periods envisaged the inclusion of monsoonal seasons: summer and The Cyclopods were represented by Oithona winter and the in between periods: the months spp. genus. Decapod zoaeas were observed at November 2010 represents the period between winter monsoon intraseason (March-April) as the summer and winter monsoons, January 2010 much as 11% represented, principally, by the represented the winter monsoon and May families Portunidae, and Xanthidae. The represents a post-winter monsoon and Prior Chaetognatha group was found throughout the Summer monsoon and August 2010 as year, mainly represented by the genus Sagitta representative of the top of Summer monsoon. spp. through the end of winter monsoon and the Intermonsoon season beyond. Fish eggs and In all stages of the quantitative and qualitative larvae found during the spring and summer methods of samples collection and analysis of months and autumn with higher density during zooplankton, we follow and guided with what the spring and early summer monsoon. stated in the relevant references, each according to the depth of analysis [24,25]. The taxonomic The abundance of zooplankton was show in identification has relied on a lot of special and Table 1 and Fig. 3. Copepods group was the general keys and guides for zooplankton of the most abundant, principally in Bir Ali and Sheher Indian and the Atlantic Oceans, and the Indo- stations. Zoaea and megalops of the true craps Pacific region [26,27,28]. Despite the lack of (Brachyura ) were also spread out with distinction studies and references for larval stages of fish at Sheher and Sharma stations, while the larvae and crustaceans in the Gulf of Aden, but it of mollusks have prevailed in the stations of Bir possible to adopt some of which belong to other Ali and Sheher compared to other stations. All areas of the Indian Ocean and the Indian Pacific coastal stations are equal by relative abundance region, including: [29,30]. of the fish larvae. However, Sheher and Sharma stations were distinguished in terms of the larvae The species richness, Shannon-Weaver Index H ′ of family Scombridae and Carangidae during and evenness J ′ as well as the Bray-Curtis August and September. Similarity Index were computed using the multivariate ecological software packages The Copepod group prevailed during the four PRIMER program v.6. seasons achieving an average: 82.6% (3125 individuals / m 3 during the winter northeastern 3. RESULTS AND DISCUSSION monsoon, 2660 individuals / m 3 during southwest monsoon, 1643 individuals / m 3 during post In this study it was possible to diagnose and southwest monsoon, and 1071 individuals/m 3 in counted 226 species of zooplankton which the post northeastern monsoon (Table 2, Fig. 4). distributed mainly within a basic eight groups; the Abundance of Copepod clearly increased during most common among them were a Copepods, in the winter monsoon, as compared with other which prevailed the species belonging to order seasons. There are distinct spatial differences , particularly species of Acartia, during the summer monsoon, the post monsoon, and Eucalanus genders. The and northeastern monsoon, that appears from second order is Poecilostomatoida, which the analyzing of both Tables 1 and 2 and Fig. 3.

4

Mukhaysin et al.; AJOB, 4(4): 1-16, 2017 ; Article no. AJOB.37671

Ostracod Pteropod Chaitogn. Decapod 1% 0.5% 2% 2% Tunicate Cladocera 2% 1% Euphausid 9%

Copepod 83%

Fig. 2. Relative abundance (%) of different zooplankton grougroupsps in Hadhramout coast

4000 3800 3600 3400 3200 Tunicate 3000 2800 Decapod

3 2600 2400 Chaitogn. 2200 2000 Pteropod 1800 Inds/ m Inds/ 1600 Ostracod 1400 1200 Cladocera 1000 Euphausid 800 600 Copepod 400 200 0 Bir Ali Broom Mukalla Shehir Sharma

Fig. 3. Zooplankton density and the contribution of the Copepods related to the other groups, in the Hadhramout coast stations.

Even though, the predominance of the copepod (p>0.05). Here we notice that south Hadhramout group in all stations is observed, the coeff icient of coast (i.e. Sheher and Sharma) exhibited higher zooplankton diversity in these stations has a zooplankton diversity than west coast. Mean H marked tendency to vary - from 0.42 in Bir Ali ranged from 0.42 to 1.27 in south coast while it station to 1.33 in Sharma, the same trend was ranged between 0.42 and 0.99 in west c oast - Bir Evenness index (Figs. 4 and 5); but there were Ali and Mukalla. Species diversity varied no significant differences between density and significantly between seasons ( p < 0.05). Mean Shannon’s ind ex temporally and spatially zooplankton diversity was higher in May (H =

5

Mukhaysin et al.; AJOB, 4(4): 1-16, 2017; Article no.AJOB.37671

0.9) and Aug. (H = 0.8) than in Jan (H = 0.54) Euphausiids, such as Pseudeuphausia latifrons , (Fig. 6). Euphausia distinguenda , and E. diomediae , which also prevail in the Hadhramout coast partly It is obvious that Calanoides carinatus is the in the southwestern monsoon, and decreases in most abundant in the community of the Copepod the northeastern monsoon. Although it known for group during the upwelling season in the group of Euphausiids their coexistence at Hadhramout coast; this is in agreement with the higher depths, especially in daylight time, but the nature of its abundance in the Somali and Omani fact that the plankton samples taken mostly at Upwelling areas [34], as well the findings reveal the early morning, so the presence in the that this species in great abundance at the samples was distinct in terms of quality and stations Bir Ali , Broom and Al Mukalla during the quantity, sometimes E. diomedeae has been summer season (southwest monsoon), this present more in Bear Ali and Broom and was not means that this species is predominant in the found of them just a few individuals in the Upwelling seasons; and its life cycle here seems Sharma station. These Euphausiids also present to be depend largely on the physical conditions in Red Sea, thought Ponomareva [36] discusses of the coastal Upwelling [35]. This is also that 10 species of this group known from Red reflected on the species of the group of Sea being immigrants from Gulf of Aden.

Fig. 4. Relative abundance of zooplankton groups and diversity profile according to seasons in Hadhramout coast

1.4 1.2 1 Shannon_H 0.8 Evenness 0.6

Indices 0.4 0.2 0 Bir Ali Broom Mukalla Shehir Sharma Stations

Fig. 5. Variations of different species diversity indices (Shannon-Weaver diversity and evenness) of zooplankton present in the Hadhramout coast stations

6

Mukhaysin et al.; AJOB, 4(4): 1-16, 2017; Article no.AJOB.37671

Table 1. Zooplankton species found according to stations: (+++ Abundant (more than 500 cells / m 3), ++ Frequent (more than 150) and + Present (less than 50), - absent

Groups, genus and the species BirAli Broom Mukalla Sheher Sharma Copepods:2800 ind/ m 3 171 taxa Order Calanoida Acartia danae ++ + ++ + + A. (Acanthacartia) dweepi + + + + + A. (Acanthacartia) tropica ++ ++ + + ++ A. (Acanthacartia) fossae + + + + + A. (Acartia) negligens ++ ++ +++ +++ ++ A. (Acartiura) clausi + + + + + A. (Acartiura) longiremis + + + + + A. (Odontacartia) centrura + - - - - A. (Odontacartia) erythraea ++ ++ +++ + +++ A. eremeevi + + + + + A. spinicuda Mukalla + beer +++ ++ +++ + + Acrocalanus gracilis ++ +++ + + +++ Acrocalanus longicornis +++ +++ ++ + ++ Bestiolina arabica +++ ++ + + + Bestiolina similis +++ ++ + + + Calanus finmarchicus +++ +++ +++ + ++ Calanoides carinatus + + ++ +++ +++ Calanoides carinatus dominant +++ +++ +++ +++ +++ Calanopia minor ++ +++ ++ ++ +++ Calanopia elliptica + + + + ++ Calanopia media ++ ++ ++ ++ ++ Candacia pachydactyla + + ++ ++ ++ Candacia bispinosa + + ++ + + Candacia longimana ++ ++ ++ ++ ++ C. curta +++ +++ ++ + ++ C. tenuimana very rare (Sharm) + + + + - C. bipinnata very rare ( Sharm) + + + + - C. cheirura + + + + + C. discaudata + + + + + C. tuberculata + + - - - C. armata + ++ ++ ++ ++ C. samassae very in Bir +++ ++ + + + C. bradyi ++ ++ ++ ++ ++ C. catula ++ ++ ++ ++ ++ C. truncata ++ ++ ++ ++ ++ Calocalanus contractus ++ +++ ++ ++ +++ Calocalanus elegans +++ +++ ++ ++ ++ Calocalanus indicus +++ +++ ++ ++ ++ Calocalanus kristalli + + ++ ++ ++ Calocalanus latus +++ +++ ++ ++ ++ Calocalanus lomonosovi ++ ++ ++ +++ +++ Calocalanus longifurca + + ++ +++ +++ Calocalanus neptunus + + + + + Calocalanus styliremis + + + + + Calocalanus minor + + + - - Calocalanus minutus - - - + + Calocalanus namibiensis + - - - - Calocalanus nanus + + - - - Calocalanus pavo ++ ++ + +++ ++ Calocalanus pavoninus + + + - - Calocalanus plumulosus + + + - -

7

Mukhaysin et al.; AJOB, 4(4): 1-16, 2017; Article no.AJOB.37671

Clausocalanus minor ++ +++ ++ +++ +++ Clausocalanus arcuicornis ++ ++ ++ ++ ++ Clausocalanus furcatus +++ +++ ++ ++ ++ Canthocalanus pauper + + ++ ++ ++ Cosmocalanus darwini + + + + + Cosmocalanus indica ++ +++ ++ ++ ++ Centropages calaninus +++ +++ ++ ++ +++ Centropages dorsispinatus ++ +++ + + ++ Centropages elongatus +++ +++ + + + Centropages furcatus + + + + ++ Centropages kroeyeri + + + + + Centropages gracilis ++ +++ +++ ++ + Centropages orsinii + + - - - Centropages violaceus - - + + - Cymbasoma tropicum + + + + + Cymbasoma spp + + + - - Eucalanus crassus ++ +++ +++ +++ ++ Eucalanus subtenuis ++ + + + ++ Eucalanus attenuatus + + + + + Eucalanus elongatus +++ ++ ++ ++ ++ Euchaeta marina ++ + ++ +++ +++ Euchaeta rimana + + + - - Gaussia swelli + + + + + Heterostylites longicornis + + + + + Labidocera minuta + + + + + Labidocera acuta + + + + + Lucicutia grandis + + + + + Lucicutia parva + + + + + Macrosetella gracilis ++ +++ ++ + ++ Microsetella rosea +++ +++ ++ ++ + Mesocalanus tenuicornis + ++ + + + Nannocalanus minor 1078/L ++ +++ +++ ++ ++ Neocalanus grasilis 10 -20cold water ++ + + ++ +++ Paracandacia simplex +++ +++ ++ + + Paracandacia truncata ++ + + +++ ++ Paracandacia sp. + + + + + Paracalanus aculeatus ++ ++ + ++ +++ Paracalanus aculeatus minor + + ++ +++ +++ Paracalanus arabiensis +++ ++ + + +++ Paracalanus denudatus + ++ + ++ ++ Paracalanus indicus +++ +++ ++ ++ +++ Paracalanus nanus + ++ + + + Paracalanus parvus +++ +++ ++ ++ ++ Paracalanus tropicus ++ + + + ++ Paracalanus sp. ++ + + ++ ++ Paracartia latisetosa + + + + + Paracartia dubia ++ ++ - - + Parvocalanus dubia + + + ++ ++ Phaenna spinifera + + + + + Pleuromamma abdominalis + + + + + Pleuromamma indica + + ++ ++ ++ Pontella fera - - - + + Pontella investigatoris ++ ++ ++ + + Pontella securifer + + + + + Pontella karachiensis + + + + + Rhincalanus nasutus ++ ++ ++ + +++ Rhincalanus cornutus - + + + +

8

Mukhaysin et al.; AJOB, 4(4): 1-16, 2017; Article no.AJOB.37671

Sapphirina gastrica + - - - - Sapphirina maculosa + - - - - Sapphirina scarlata + + - - - Sapphirina vorax + - - - - Scolecithrix bradyi ++ + - - - Scolecithrix longipes ++ + + + + Scolecithricella tropica + + + + + Scolecithricella orientalis + + + ++ ++ Scolecithricella minor + + - - + Subeucalanus crassus ++ + - - - Subeucalanus pileatus + + + - - Subeucalanus subcrassus + + - - - Subeucalanus subtenuis + + - - - Undinula vulgaris ++ + + ++ +++ Xanthocalanus gigas + + + + + Ord. Cyclopoida Acanthocyclops vernalis ++ ++ ++ ++ ++ Oithona attenuata - - + + + Oithona brevicornis ++ ++ + + + Oithona decipiens ++ + + + + Oithona fallax + + + + + Oithona nana + + + + + Oithona pacifica ++ ++ + + + Oithona plumifera + + + + + Oithona pulla + + + + + Oithona robusta ++ + + + + Oithona setigera + + + + + Oithona simplex + - - + + Oithona tenuis + + + - - Oithona vivida - - - + + Oithona spinirostris + + + + + Triconia conifera + + - - - Triconia rufa - - - - + Triconia umerus - - + + + Triconia parasimilis - - + + + Ord. Poecilostomatoida Amallothrix indica + + + ++ ++ Corycaeus (Agetus) limbatus + + + + + Corycaeus typicus ++ +++ + + + Corycaeus speciosus ++ ++ ++ + ++ Corycaeus asiaticus + + + + + Corycaeus erythraeus + + + ++ ++ Corycaeus agilis +++ +++ + ++ ++ Corycaeus latus + + + + + Corycaeus ovalis + + - - - Corycaeus pacificus + - - - - Corycaeus pumilus + + ++ ++ ++ Corycaeus sp. + + + - - Copilia quadrata - - - + + Copilia lata - - - - + Copilia spp. + + + + + Oncaea venella ++ +++ ++ ++ ++ Oncaea mediterranea ++ ++ ++ + + Oncaea paraclevei + + + + + Oncaea ivlevi + + ++ ++ ++ Oncaea vodjanitskii + + + + + Oncaea venusta + + + - -

9

Mukhaysin et al.; AJOB, 4(4): 1-16, 2017; Article no.AJOB.37671

Oncaea media ++ +++ ++ + + Oncaea longipes ++ ++ ++ + + Oncaea ovalis ++ ++ + + + Oncaea cristata + + + + + Oncaea clevei + + + + + Oncaea brodskii + + + ++ ++ Oncaea similis ++ ++ ++ ++ ++ Oncaea subtilis + + + + + Oncaea tenella + + - - - Oncaea zernovi + + + ++ ++ Oncaea bispinosa + + + + + Spinoncaea ivlevi - - - + + Temora stylifera + + + + + Ord. Siphonostomatoida Caligus diaphanus ++ ++ +++ + + Lernaeocera branchialis + + + + + Lernaeenicus hemirhamphi + + ++ +++ ++ Ord. Harpacticoida Clytemnestra scutellata + + + + + Macrosetella gracilis + + + +++ ++ Copepod nauplius +++ +++ ++ ++ ++ Copepodids stage ++ ++ ++ ++ ++ Ord. Euphausiacea: 14 taxa Bentheuphausia amblyops + + + + + Euphausia brevis + + + + + E. sibogae + + + + + E. sibogae Calyptopis C2 + + + + + E. sibogae Furcilia 2 E. sanzoi + + + + + Euphausia diomedia SW abundant ++ ++ ++ + ++ Euphausia distingüenda?? 96/m3 SW abundant + + + + + E. paragibba + + + + + E. pseudogibba + + + + + E. mutica Calyptopis/ Furcilia F1 + + + + + Nematoscelis tenella Larva F2 Pseudeuphausia latifrons 12/m3 SW abundant + + + + ++ Stylocheiron abbreviatum Furcilia ++ + + + + Stylocheiron armatum + + + + + S. carinatum + + + + + Ord. Cladocera: 42 ind/ m3 4 taxa Evadna nordmanni + + + +++ +++ E. tergestina + + + ++ ++ Penilia avirostris + + + + ++ Podon intermedius + - - + + Ord. Ostracoda : 25 ind/ m3 3 taxa Conchoecia sp. + + + + + Cypridina sp. + + + + + Euconchoecia spp. + + + + + Ord. Pteropods: 14 ind/ m3 Creseis acicula + + + + + Cavolinia globulosa - - - + + Limacina inflata + + + + + Ord. Chaitognatha: 20 taxa Eukrohnia sp. +++ +++ ++ ++ ++ Krohnitta pacifica ++ ++ + + + Krohnitta balagopali + + + + + Sagitta adenensis ++ ++ ++ + ++

10

Mukhaysin et al.; AJOB, 4(4): 1-16, 2017; Article no.AJOB.37671

Sagitta bipunctata + + + + + Sagitta erythraea + + ++ ++ ++ Sagitta enflata + + + + + Sagitta ferox + + + + + Sagitta hexaptera ++ ++ ++ + + Sagitta lucida + + + + + Sagitta madhupratapi + + + ++ ++ Sagitta nagae + + + + + Sagitta neglecta ++ ++ ++ + + Sagitta regularis ++ ++ + + + Sagitta robusta + + + + + Sagitta serratodentata ++ +++ + + + Sagitta sibogae ++ ++ +++ +++ +++ Sagitta setosa ++ ++ ++ ++ ++ Pterosagitta draco + + + + + Pterokrohnia arabica ++ ++ ++ ++ ++ Ord. Decapoda: 3 ind/m 3 1 taxa Lucifer spp. ++ ++ ++ +++ ++ larvae of sergestids ++ ++ ++ ++ ++ Penaed nauplius +++ +++ + + ++ Megalopa of crab +++ ++ +++ +++ +++ Decapod zoea +++ +++ +++ +++ +++ Ord. Tunicate: 125 ind/m 3 10 taxa Cyclosalpa affinis + + + + ++ Fritllaria borealis f. sargassi - - - + + Fritllaria formica f. digitata - - - + + Fritllaria tenella - - - + + Oikopleura albicans + + + - - Oikopleura parva + + - - - Oikopleura rufescens + + - - - Stegosoma magnum - - + + ++ Salpa fusiformis + + + + + Thalia democratica 386/m 3 upwelling time + +++ ++ + + dominant Bivalve viliger +++ +++ ++ ++ ++ Gastropod veliger +++ +++ + + ++ Auricularia - larva of a sea cucumber +++ +++ + + ++ TOTAL spp. 226

Table 2. The numerical abundance and dry weight of the main groups of zooplankton in Hadhramout coast according to the seasons

Groups January 2010 May 2010 August 2010 Nov. 2010 Ind/m 3 mg/m 3 Ind/m 3 mg/m 3 Ind/m 3 mg/m 3 Ind/m 3 mg/m 3 Copepods 3125 128.5 1071 39.7 2660 83.8 1643 52.4 Euphausiids 248 24 185 17.5 429 29.2 170 13.8 Cladocera 19 12.3 11 8.6 29 16.4 12 13.5 Ostracoda 25 17 9 13.3 16 11.6 9 10.2 Pteropods 12 6.6 10 3.7 9 8.5 5 2.8 Chaitognatha 57 23.6 56 19.2 65 16 60 25 Decapoda 1 1.8 3 2.6 3 2.2 1 3.6 Tunicate 51 0.7 60 09 177 2.8 56 1.5 Total 3538 214.5 1405 113.6 3388 170.5 1957 122.8

11

Mukhaysin et al.; AJOB, 4(4): 1-16, 2017; Article no.AJOB.37671

1 0.913 0.8 0.8051 0.6915 0.6 0.5444 Shannon_H 0.4 Evenness_e^H/S Indices

0.2

0 Jan May Aug Nov

Fig. 6. Seasonal variations of different species diversity indices (Shannon-Weaver diversity and evenness) of zooplankton present in the Hadhramout coast

The species C. carinatus is significant in station in May and 113.6 mg / m 3 for station of biological configuration of water mass as all, Broom, which characterized by low zooplankton being a subject in a relatively short life to climate indicators during all months). As for spatial impacts which controls the seasonal cycle of distribution of the abundance zooplankton mass upwelling. Angel [37] was found that it can build has shown heterogeneity clearly between a large gathering where there are stable hydro stations (Table 2), the highest value for dry mass cyclones systems in open offshore upwelling reached 222.6 mg / m3 registered in Sharma zone. Smith [38] found such qualities for these station, while the minimum value was in Sheher groups in such deep eddy in the east of the Gulf station, reaching 38.5 mg / m3 (Fig. 7). As of a of Aden and the coast of Oman at the end of statistical standpoint, the mass of zooplankton is upwelling seasons. subject to significant variation between different stations ( p< 0.05). Although the marine Cladocera have limited diversity and abundance in most seas [39,40], It is obvious that these preliminary results of but being unique by ways of asexual community of zooplankton of Hadhramout coast reproduction and what resulting from, prosperity not differ significantly from the situation observed of their groupings in the marine coasts during in most of the northern Arabian Sea regions certain seasons of the year, being an adequate [41,42]; but it much more than what recorded in and typical prey for fishes that feeding on the Indian Ocean mission during southwestern plankton their early stages. Cladocera presence monsoon [43]. Also, a result of this study in zooplankton samples of Hadhramout coast characterized by a diagnosis of species was little in terms of diversity and quantities that combination of Copepods, the traditional coastal varied at the sites as they are in the seasons; as and oceanic surface illuminated areas of appears from the Tables 1 and 2, the presence northwest and east of the Indian Ocean. What of species of this group of mezozooplankton was was found of them a total of 171 elements here is a little more in the eastern stations of the coast in much more than recorded in the inner continental most of the seasons; at the same time their shelf of western India [44] and for the Bay of abundance is noticeable at the end of the Bengal [45]; but it less than what is found in the southwest monsoon period and beyond - August Somali eastern coast, the traditional Upwelling and September. area [32]. Although, this difference is illustrate distinction of Hadhramout coast by relative bio The study reveals that the biomass of richness, however, it might due to the differences zooplankton in the whole Hadhramout coast in zooplankton net meshes that used in the characterized by high-value, which ranged on different studies. It was found by Bathafari [18] in average between 113.6 and 214.5 mg / m 3 dry a previous study that there are more than 13 weight with an average of 128.28 mg / m 3 taxonomic units of zooplankton in the waters of (ranging between 214.5 mg / m 3 of Sharma the northern Gulf of Aden, from which the richest

12

Mukhaysin et al.; AJOB, 4(4): 1-16, 2017; Article no.AJOB.37671

representatives of the copepod represented then through studying food and primary production by only about 163 species consisting until 69% of relationships of Somali current, where Copepods zooplankton mass in period of winter northeast group dominated within the zooplankton, monsoon (January). During the summer especially in the Upwelling center and the monsoon (July), the role of the Copepods was regions, which fueled by this current. largest and has reached more than 79% of the total mass. In the transitional period from Fertility of zooplankton apparently follows, in summer monsoon to winter northeast monsoon Hadhramout coast, the quarterly monsoonal (Sept.) for the same period, the role of copepods cycle of the wind and the nutrient-rich, an in composition of zooplankton has not declined essential element regulator temporal variation in but dropped relatively little bit to 58% in the total zooplankton (often Copepods) in coastal mass of zooplankton. conditions [49]. Although the phytoplankton is a source of nutrition of herbivorous copepod, but There is no appropriate information or data for we did not find a clear correlation between the this coast regarding the zooplankton, as they are concentration of chlorophyll and the abundance for other indicators, nevertheless, the present of copepod, but there was found a time lag results showed that the coast of Hadhramout is between the phytoplankton bloom and the rich by zooplankton and includes at least main increase of zooplankton abundance (Fig. 8). groups with large food important for most marine organisms as mollusks, crustaceans and fish. The zooplankton plays, along with phytoplankton, Despite the lack of the studies, but that carried of in the Arabian coast of the Gulf of Aden, a them for the Gulf of Aden found that the significant role in feeding and food for small zooplankton mass during the autumn intern pelagic fish, for example, the elements of period (October to January) was the highest in Euphausidia, Decapoda and Stomatoids the Hadhramout coast, particularly the east of (Squilids) occupies about 50% of stomach Mukalla, and during August in the west of content of chub mackerel Scomber japonicus Mukalla - Ras El Kalb (Mayfa'a Hajar) [46,47]. [18]. Phyto and zooplankton are considered having a special valuable in the food of Scombrid Through the role of this species by its optional and Carangids fishes [50]. feeding on large diatoms and Dinoflagellates, and because these species, as we noted, prevail We believe that the high density of zooplankton in mass and quality of phytoplankton of in the waters of the coast due to the favorable Hadhramout coast and Gulf of Aden at all [17], environmental conditions during the year, such the observer simply can see the extent of as salinity and temperature that ideal for good securing and ensuring the food resources and productivity of the phytoplankton, existing and feeding base in primary and secondary prevailing in the region [17]. production. This is what mentioned by Smith [48]

Fig. 7. The quarterly mean variation of zooplankton groups’ abundance in Hadhramout coast

13

Mukhaysin et al.; AJOB, 4(4): 1-16, 2017 ; Article no. AJOB.37671

3500 3000 Avr. Phyto 2500 Avr. Zoo 2000 1500 1000 500 Mg./ m3 Mg./ 0

Seasons

Fig. 8. Time lag between the phytoplankton bloom and the increase of zooplankton abundance

In this study it had been getting larvae of differentdifferent 2. Savidge G, Gilpin L. Seasonal influences crustaceans and fish that formed between 2 and on size fractionated chlorophyll a 12% of the zooplankton mass during the study concentrations and primary production in period, even though it not included in the the northwest Indian Ocean. Deep Sea accounts of the quantity of zooplankton, and was Research II. 1999;46:701-723. isolated according to traditional methods to study 3. IFAD. Fisheries investment project, them independently of the zooplankton. Republic of Yemen. Project final design report, 92pp (Main report and Annexes); 4. CONCLUSION 2010. Available: http://www.ifad.org/operations/pr This study is the first report on distribution of ojects/design/ 101/yemen.pdf ; [accessed zooplankton from the coastal waters of Gulf of October 2016] Aden, Yemen. In the present study, a total of 226 4. Ministry of Fisheries Wealth (MFW). species belonging to eight taxa such as copepod, Information on Fisheries management in medusae, ctenophores, Chaetognaths, the Republic of Yemen; Report; 2002. Appendicularians, Tunica te, Siphonophores and 5. Krey J, Babenerd B. Phytoplankton developmental stages of different taxa was production atlas of the international Indian identified. A variation in species composition Ocean expedition. Intergovernmental between stations was recorded. This study Oceanographic Commission, Paris. indicates that Bir Ali and Broom stations had a 1976;70. higher abundance of zooplankton than that of 6. Wooster WS, Schaefer MB, Robinson MK. other sta tions, and their abundance and Atlas of the Arabian Sea for fishery successful diversity is governed by geographical oceanography. University of California, features of locality. It is obvious that Calanoides Institute of Marine Resources, La JoUa carinatus is the most abundant in the community California. 1967;22. of the Copepod during the upwelling season in 7. Nair VR. Organic carbon content of tropical Hadhramout coast. The study r eveals that the zooplankton. Indian J ournal of Marine biomass of zooplankton in the whole Science. 1980;9(2):114-116. Hadhramout coast characterized by relatively 8. Madhupratap M, Nair SRS, Achuthankutty high-value. CT, Nair VR. Major crustacean groups and

total zooplankton diversity around COMPETING INTERESTS Andaman-Nicobar islands. Indian Journal

Authors have declared that no competing of Marine Science. 1981;10: 266 -269. interests exist. 9. Fratantoni DM , AS Bower , Johns WE , Peters H. Somali current rings in the REFERENCES eastern Gulf of Aden. Journal of Geophysics Research. 2006;111. C09039, 1. Khimitsa VA. Hydrological structure of the DOI :10.1029/2005JC003338 waters of Gulf of Aden, Okeanology. 10. Poulet SA, Williams R. Characteristics and 1968;8:379-402. properties of copepods affecting the

14

Mukhaysin et al.; AJOB, 4(4): 1-16, 2017; Article no.AJOB.37671

recruitment of fish larvae. Bulletin of Studies in Marine Science. George Allen Plankton Society of Japan. 1991;7:271- and Unwin. 1966;429–467. London. 290. 22. Goswami SC. Zooplankton methodology, 11. Marcus N. An overview of the impacts of collection and Identification- a field eutrophication and chemical pollutants on manual. National Institute of copepods of the coastal zone. Zoological Oceanography. 2004;16. Studies. 2004;43(2):211–217. 23. Omori M, Ikeda T. Methods in marine 12. Vinogradov ME, Voronina NM. Influence of zooplankton ecology. John Wiley and the oxygen deficit on the distribution of Sons, NY. 1984;332. plankton in the Arabian Sea. Deep-Sea 24. Madhupratap M. Zooplankton standing Research. 1962;9:523–530. stock and diversity along an oceanic track 13. Schneider G, Lenz J, Rolke M. in the western Indian Ocean. Mahasagar- Zooplankton standing biomass and Bulletin of the National Institute of community size structure within the Oceanography. 1983;16(4):463-467. epipelagic zone: A comparison between 25. Goswami SC, Padmavathi G. Zooplankton the central Red Sea and the Gulf of Aden. production, composition and diversity in Marine Biology. 1994;119:191–198. the coastal waters of Goa. Marine Science. DOI: 10.1007/BF00349556 1996;25:91-97. 14. Wiebinga CJ, Veldhuis MJW, Baar HJWD. 26. Silas EG, Srinivasan M. Chaetognaths of Abundance and productivity of the Indian Ocean with a key for their bacterioplankton in relation to seasonal identification. Proceedings of the Indian upwelling in the northwest Indian Ocean. Academy of Sciences- Section B. Deep Sea Research Part I. Oceanographic 1970;71(5):177-192. Research Papers. 1997;44(3):451-476. 27. Bradford JM. Review of the taxonomy of DOI: 10.1016/S0967-0637(96)00115-X the Calanidae (Copepoda) and the limits to the genus Calanus . Hydrobiologia. 15. Savich MS. Phytoplankton of Aden Gulf 1988;167/168:73–81. (PhD. Thesis). University of Odessa, DOI:10.1007/BF00026295. Odessa, USSR; 1979. 28. Conway DVP, White RG, Hugues-Dit-Ciles 16. Alkawri Abdulsalam and Gamoyo J, Gallienne CP, Robins DB. Guide to the Majambo. Remote sensing of coastal and surface zooplankton of the phytoplankton distribution in the Red Sea South-Western Indian Ocean. Plymouth, and Gulf of Aden. Acta Oceanologica UK: Occasional Publication of the Marine Sinica. 2014;33(9):93–99. Biological Association of the United DOI: 10.1007/s13131-014-0527-1. Kingdom. 2003;15:1-354. 17. Ali Attaala M, Bazar SR. First observations 29. Leis JM, Carson-Ewart BM. Orientation of on phytoplankton and chlorophyll ecology pelagic larvae of coral reef fishes in the in the coast of Hadhramout, Gulf of Aden. ocean. Marine Ecology Progress Series. International Journal of Fisheries and 2003;252:239–253. Aquatic Studies. 2016;4(2):191-202. 30. Leis JM, Trnski T. The larvae of Indo- 18. Bathafari AF. Ecological and biological Pacific shorefishes. New South Wales characteristics of little tuna ( Euthynnus University Press, Sydney and University of affinis ) from Aden Gulf (Ph.D Thesis). Hawaii Press, Honolulu. 1989;371. Astrakhan State Technical University, 31. Gowsami SC. Zooplankton standing stock Astrakhan, Russia; 2003. and composition in coastal waters of Goa, 19. Al-Saafani MA. Physical oceanography of West coast of India. Indian Journal of the Gulf of Aden (PhD Thesis). Goa Marine Science. 1985;14:177-180. University, Goa, India; 2008. 32. Van Couwelaar M. Zooplankton and 20. Cooney RT. Zooplankton and micronekton micronekton biomass off Somalia and in associated with a diffuse sound scattering the southern Red Sea during the SW layer in Puget Sound, (PhD Thesis); monsoon of 1992 and the NE monsoon of University of Washington, Seattle, 1993, Deep Sea Research II. 1997;44(6- Washington; 1971. 7):1213–1234. 21. Lovegrove T. The determination of the dry 33. Piontkovski SA, Al-Maawali A, Al-Mantheri weight of plankton and the effect of various W, Al-Hashmi K, Popova E. Zooplankton factors on the values obtained. In H. of Oman coastal waters. Agricultural and Barnes, (ed.), Some Contemporary Marine Sciences. 2013;18:37–50.

15

Mukhaysin et al.; AJOB, 4(4): 1-16, 2017; Article no.AJOB.37671

34. Stephen R, Saraladevi K, Journal of Union Arab Biologists. 1999;12: Meenakshikunjamma PP, Gopalakrishnan 113-125. TC, Saraswathy M. In Desai, B. N. (Ed.), 43. GLOBEC. GLOBEC workshop on Oceanography of the Indian Ocean (pp. biotechnology applications to field studies 143-156). Oxford & IBH Publ. Co., New of zooplankton (Report No. 3). Joint Delhi; 1992. Oceanographic Institutions, Inc.; WDC. 35. Madhupratap M, Haridas P, Ramaiah N, 1991;29. Achuthankutty CT. Zooplankton of the 44. Goswami SC, Krishna Kumari L, Yashoshri southwest coast of India: abundance, Shrivastava. Diel variations in zooplankton composition, temporal and spatial and their biochemical composition from variability in 1987. In Desai, B. N. (Ed.), Vengurla to Ratnagiri, west coast of India. Oceanography of the Indian Ocean (pp. Indian Journal of Marine Science. 2000;29: 99-112), Oxford & IBH Publ. Co., New 277-280. Delhi; 1992. 45. Rakhesh M, Roman AV, Sudarsan D. 36. Ponomareva LA. Euphausiids of the Indian Discriminating zooplankton assemblages Ocean and Red Sea. Div. of Oceanology, in neritic and oceanic waters: A case for Atmospheric Physics and Geography. the northeast coast of India, Bay of Moscow. Publishing house "NAUKA", 83 Bengal. Marine Environmental Research. pp. 1975. (Russian). 2006;61(1):93-109. 37. Angel MV. Detrital organic fluxes through DOI: 10.1016/ j.marenvres.2005.06.002. pelagic ecosystems. In: M.J.R. Fasham 46. Khan J, Hempel G. Relation of fish larvae (ed.), Flows of Energy and Materials in and zooplankton biomass in the Gulf of Marine Ecosystems (pp. 475-516), Plenum Aden. Marine Biology. 1974;28:311–319. Press, New York; 1984. 47. Druzhinin A. Fishery resources of the Gulf 38. Smith SL. The northwestern Indian Ocean of Aden and some adjacent areas – FAO / during the monsoons of 1979: distribution, UN Report for the fishery development in abundance and feeding of zooplankton. the Gulf of Aden. DP9/12 PDY 64/ 501 / 7: Deep Sea Research. 1982;29:1331-1353. 1973;229. 39. Onbe T. The biology of marine 48. Smith SL. Biological indications of active cladocerans in warm temperate water, (pp. upwelling in the Northwestern Indian 383-393). In: Proceedings of a Symposium Ocean in 1964 and 1979, and a on Warm Water Zooplankton. Special comparison with Peru and Northwest publication, UNESCO/ National Institute of Africa. Deep Sea Research II. 1984;31: Oceanography, Goa; 1977. 951–967. 40. Tang K, Chen QC, Wong CK. Distribution 49. Garcia JR, Lopez JM. Seasonal patterns of and biology of marine cladocerans in the phytoplankton productivity, zooplankton coastal waters of southern China. abundance and hydrological conditions in Hydrobiologia. 1995;307:99–107. Laguna Joyuda, Puerto Rico (pp. 625- 41. Jayalakshmy KV. Spatial zonation of 631). In Ros J. D. (Ed.). Topics in Marine zooplankton in the Northwestern Arabian Biology, Scientia Marina. 1989;53(2-3). Sea: a multivariate approach. International 50. Morote E, Olivar MP, Villate F, Uriare I. Journal of Ecology and Environmental Diet of round sardinella Sardinella aurita , Sciences . 2000;26:253-268. larvae in relation to plankton availability in 42. El-Serehy HA. Species composition and the NW Mediterranean. Journal of community structure of zooplankton in the Plankton Research. 2008;30(7):807-816. Emirates coastal water on the RSA. ______© 2017 Mukhaysin et al.; This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0 ), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Peer-review history: The peer review history for this paper can be accessed here: http://sciencedomain.org/review-history/22463

16