Indian Journal of Geo-Marine Sciences Vol. 44(9), September 2015, pp. 1282-1293
Changes in mesozooplankton community structure during Trichodesmium erythraeum bloom in the coastal waters of southwestern Bay of Bengal Gouri Sahu1, A. K. Mohanty1*, M. Smita Achary1, S. K. Sarkar2& K. K. Satpathy1 1
Environmetal Safety Division, Indira Gandhi Center for Atomic Research, Kalpakkam-603 102, Tamil Nadu, India 2 Department of Marine Science, University of Calcutta, Calcutta- 700 019, India [E-mail:
[email protected] ] Received 18 September 2012; revised 03 July 2013
Present study addresses variability in mesozooplankton community structure (size ranges from 0.2-20 mm) during the appearance of diazotrophic marine cyanobacterium Trichodesmium erythraeum bloom in the coastal waters southeastern part of India. Zooplankton density (individuals per 10 m3) was the maximum during pre-bloom period (5.5 x 105) followed by bloom (4.9 x 105) and post-bloom period (4.3 x 105). Copepods contributed ~ 64 % of the zooplankton abundance during pre-bloom period in which calanoids were dominant (41%). Carnivore copepods (25%) (Cyclopoids and Poicilostomatoids) dominated over herbivore (23%) (Paracalanidae) during the peak bloom. Non-copepod holoplankters and meroplankters were dominant during pre-bloom period. The cladoceran, Evadne tergestina (35% of total non-copepod crustacean holoplankton) was found to be the most important species during bloom period. Among the meroplankters, cirripede nauplii (59% of the total meroplankton) were dominant form during bloom period. Co-occurrence of Trichodesmium bloom with high abundance of Penilia avirostris & Evadne tergestina and association of Acartia spinicauda and Oithona spp., in large numbers during bloom were the interesting features of this study. [Keywords: Mesozooplankton, community structure, Trichodesmium erythraeum, algal bloom, Bay of Bengal, Southeast coast of India]
Introduction Zooplankton is a critical component of marine aquatic food webs. Its distribution and dynamics in marine ecosystem are driven by an array of factors such as, physical, chemical and biological characteristics, meteorological conditions and synergistic effects of these factors1-3. Moreover, they are considered as the chief index of utilization of aquatic biotope at the secondary trophic level and as primary & secondary consumers, they account for about one tenth of the total marine biomass on which the whole class of fishery depends upon. Thus, their abundance is taken as one of the prime indices of the available fishery resources of water masses. Many zooplankton species are used as water quality indicators. Owing to such multi-dimensional economic and ecological utility, zooplankton constituted a core subject of research in all marine biological investigations. There has also been extensive research on the effect of various factors like temperature, salinity, trophic state (nutrient levels and productivity) etc on the spatio-temporal variability in zooplankton community structure4-5. Studies on zooplankton distribution in the Atlantic Ocean6-8 and Pacific Ocean9-10 were considerable. However, from the Indian Ocean, such studies have been undertaken mostly from the Arabian Sea and such studies were found scarce from the Bay of Bengal (BOB) 11-13. Scrutiny of
literature showed that reports on zooplankton from the southeast coast of India are scanty. With respect to the present study area, there has been a single account of zooplankton distribution in the coastal waters during a monsoon transition period14. Furthermore, research on dynamics of zooplankton populations in marine ecosystems subjected to algal blooms is very meager globally15-16 as well as in the Indian context17-18. The present investigation documents a comprehensive account of the changes in mesozooplankton community structure due to occurrence of a mono-specific marine cyanobacteria, Trichodesmium erythraeum, bloom, in relation to prevailing physico-chemical features in the coastal waters. Materials and Methods Kalpakkam (12o 33' N Lat. and 80o 11' E Long.) is situated about 70 km south of Chennai city (Figure 1). At present a nuclear power plant (Madras Atomic Power Station, MAPS) and a desalination plant (Nuclear Demonstration & Desalination Plant, NDDP) are located near the coast. MAPS uses seawater at the rate of 35 m3sec-1 for the purpose of cooling the condenser and other auxiliary systems. After extracting heat, the heated seawater (≤ 7 oC of ambient seawater temperature) is released into the sea. Two backwaters namely, the Edaiyur and the Sadras backwater systems
SAHU et al.: MESOZOOPLANKTON COMMUNITY STRUCTURE DURING TRICHODESMIUM BLOOM
constitute important features of this coast. During the period of Northeast (NE) monsoon and seldom
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during Southwest (SW) monsoon, these two backwaters get opened into the sea discharging
Figure 1: Study area showing the sampling location
considerable amount of freshwater into the coastal milieu. The mean tidal range at this location varied from 0.3 – 1.5 m. The coastal currents at Kalpakkam has seasonal character and during SW monsoon the current is northerly (February to October) with a magnitude of 0.2 – 1.8 km h-1 and during NE monsoon the current is southerly (October to February) with a magnitude of 0.1 – 1.3 km h-1. The wind speed varied from 10-40 km h-1. These monsoonal winds cause a) southerly (~ 0.5 million m3 y-1) and northerly (~ 1 million m3 y1 ) littoral drift. The seawater temperature has two maxima (April / May & August / September) and two minima (December / January & June / July). According to the climatology of this area, the whole year has been divided into three seasons viz: i. post-monsoon/summer (February - May), ii. premonsoon or SW monsoon (June- September) and iii. NE monsoon (October - January). As much as about 65% of total rainfall (annual rainfall ~1250 mm) occurs during NE monsoon period. Besides the monsoonal rain, the monsoon dependent
current reversal brings visible alteration in the physico-chemical and biological characteristics of coastal waters19. Surface water samples were collected twice daily (between 9 to 10 AM and 4 to 5 PM during the bloom period (19th to 23rd February, 2008), whereas, during pre- and post-bloom periods samples were collected weekly only in the morning hours. Samples were drawn by lowering a clean plastic bucket from the Jetty of Madras Atomic Power Station (MAPS) and analyzed for various physicochemical parameters. Winkler’s titrimetric method20 was followed for the estimation of DO. Salinity measurements were carried out by Knudsen’s method20. pH measurement was carried out by a pH meter (CyberScan PCD 5500) with an accuracy of ± 0.01. Dissolved nutrients such as, nitrate (nitrite + nitrate), ammonia, silicate and phosphate along with total nitrogen (TN) and total
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Table-1- Summary of the hydro-biological parameters associated with Trichodesmium bloom in the coastal waters of Kalpakkam, Southeast coast of India o
Temp. ( C) Salinity (psu) pH DO (mg l-1) NO2 (µ mol l-1) NO3(µ mol l-1) NH3(µ mol l-1) TN (µ mol l-1) SiO4 (µ mol l-1) PO4 (µ mol l-1) TP (µ mol l-1) Chl-a (mg m-3) Phaeophytin (mg m-3) Phytoplankton density (x 105 cells l-1) Trichodesmium density ( x 105 cells l-1)
Pre-bloom 28.1-29.6 32.24-32.85 8.0-8.1 6.28-6.78 0.31-0.46 1.35-5.85 0.72-1.21 2.47-12.035 8.24-13.8 0.09-0.14 0.23-0.69 0.97-1.21 0.86-1.15 1.286-1.879
Bloom 28.4-32.6 32.28-32.52 8.1-8.2 6.65-7.21 0.11-1.06 0.46-1.079 0.66-284.36 2.28-392.80 9.37-11.77 0.05-1.51 0.27-2.83 1.56-42.15 1.38-46.23 1.23-294.05
Post-loom 29.3-29.7 33.08-33.2 8.1-8.2 6.21-6.42 0.3-0.41 4.41-6.18 0.39-0.94 10.24-12.45 9.45-16.28 0.37-0.73 0.50-0.93 2.24-2.34 1.67-1.85 1.79-2.12
0-0.035
0.11-287.85
0-0.04
phosphorous (TP) were estimated following standard methods20-21, using the filtered (through 0.45 μ Millipore filter) samples. Chlorophyll-a and phaeophytin were measured spectrophotometrically21 using a double beam UV– Visible Spectrophotometer (Chemito Spectrascan UV 2600). Phytoplankton density was estimated using Utermohl’s sedimentation technique22 and counted using Sedgwick Rafter counting chamber with the aid of binocular research microscope (Nikon Eclipse-50i, Zeiss Axiovert 40CFL). The identification of phytoplankton was done by following standard taxonomic monographs for diatoms23, dinoflagellates24-25 and green and bluegreen algae (Cyanobacteria) 26 for. Zooplankton samples were collected using conical plankton net with mouth area 0.125 sq. m (mesh size-200 μ) fitted with a calibrated flow meter (Hydrobios). Samples were brought to the laboratory and preserved with 5% buffered formalin for further analysis. Zooplankton biomass was measured by volume displacement method. Biomass was expressed in terms of ml per 10 m3. The larger organisms of zooplankton community from both holo- and meroplankton were sorted out from the plankton mixture and counted separately. Residual mixture was then diluted to exactly 100 ml with folmaldehyde solution. One ml of this aliquot was transferred onto Sedgewick Rafter cell for identification and numerical density of zooplankton, by examining under a stereo binocular research microscope (Nikon Eclipse-50i, Zeiss Stemi 2000). The examining procedure was repeated 10 times for each sample. Numerical
density was expressed in terms of individuals per 10 m3. Standard literature27-28 was followed for identification of copepods and other zooplankton groups. In order to get a clear picture of the difference in zooplankton assemblages during pre-bloom, bloom and postbloom periods, agglomerative hierarchical clustering (AHC) was performed. Impact of environmental variables on the zooplankton community was assessed through the correlation matrix. XLSTAT software (Addinsoft) was used for the above statistical analyses. Results Values of hydrographical parameters are given in Table 1. pH did not show any significant variation and ranged from 8.0-8.2 during the study period. It did not show any correlation to bloom appearance as it remained almost stable during prebloom, bloom and post-bloom periods. The surface water temperature during the study period ranged from 28.1-32.6 0C. Moderately high temperature values were noticed during the bloom period. The observed salinity values ranged from 32.24-33.20 psu. A gradual increase in salinity was noticed from pre-bloom to post-bloom period during the present investigation. DO concentration ranged from 6.21 - 7.21 mg l-1. The lowest and the highest DO concentration was observed during the postbloom and bloom period respectively. Nitrate concentrations ranged from 0.46 – 6.18 µ mol l-1, the highest value being observed during the post-bloom period and the lowest during the bloom (Table 1). No clear trend in nitrite content
SAHU et al.: MESOZOOPLANKTON COMMUNITY STRUCTURE DURING TRICHODESMIUM BLOOM
was noticed during the study period. Ammonia values (0.39-284.36 µ mol l-1) were significantly high during the bloom, and its highest value coincided with that of the highest cell density, which resulted in observation of very high TN concentration (392.80 µ mol l-1) on the day of bloom. Phosphate levels ranged from 0.05 µ mol l-1 during pre-bloom to 1.51 µ mol l-1 during the bloom period. In the present study, an abrupt increase (the peak) in phosphate content was encountered on the day of highest cell density compared to other observations. TP values also showed a trend similar to phosphate and ranged from 0.23-2.83 µ mol l-1. Silicate value ranged from 8.24–16.28 µ mol l-1 with lowest and highest values being observed during bloom and postbloom periods respectively. Phytoplankton community showed a distinct variation in its quantitative as well as qualitative aspects during the bloom. In total 69 species of phytoplankton were identified which comprised of 62 diatoms, 5 dinoflagellates, one silicoflagellate and the cyanobacteria Trichodesmium erythraeum. The population density of phytoplankters ranged between 1.23 x 105 and 2.94 x 107 cells l-1 showing a two order increase during the peak bloom. Lowest cell density was observed during postbloom period. Surprisingly, Trichodesmium was exclusively found during the bloom period from 19.02.08-23.02.08 and was totally absent during the preand post-bloom observations. Contribution of Trichodesmium to the total cell count ranged from 7.79 % to 97.01 %. Perusal of published literature showed that the present observed density of Trichodesmium is the highest, reported to date from Indian waters, and surpassed by a factor of 1.75 times from that of earlier reported highest density (1.75 x 107 cells l-1) from Tuticorin Bay, south eastern part of India 29. Phytoplankton species such as Asterionellopsis glacialis, Nitzschia longissima, Thalassionema nitzschioides, Thalassiosira decipiens and Thalassiothrix longissima were present almost throughout the study period. Species such as Biddulphia heteroceros, Cocconeis distans and Leptocylindrus minimum were found only during the pre-bloom period and totally absent during bloom and post-bloom periods. On the contrary, two species of Biddulphia (B. aurita and B. rhombous) were found only during the post-bloom period. Chlorophyll-a concentration ranged from 0.97-42.15 mg m-3 during the study with the highest concentration coinciding with the observation of peak bloom. Similarly, the highest phaeophytin content (46.23 mg m-3) also coincided with the highest phytoplankton density.
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The zooplankton community comprised of 63 species (48 holoplanktoers and 15 meroplankters). Copepods emerged as the dominant component with 40 species. A sharp elevation in number of species of copepods (33) was observed during the bloom, which was about two fold higher than the pre-bloom (18 species) and post-bloom (20 species) periods. Copepod nauplii and copepodites of three sub-orders i.e. calanoida, cyclopoida and harpacticoida were observed throughout the study except cyclopoid copepodites, which were absent during the pos-bloom period. Ovigerous females of Pseudodiaptomous serricaudatus, Oithona rigida, Oithona brevicornis, Oithona similis, Euterpina acutifrons and Macrosetella gracilis were observed during the study. A conspicuous change in the zooplankton community structure was observed during the bloom period. During the bloom period an aggregation copepods namely, Canthocalanus sp., Parvocalanus crassirostris, Pseudodiaptomus sp., Temora turbinata, Labidocera acuta, L. pavo, Pontellopsis scotti, Pontella securifer, Acartia sp., Oithona hebes and Microsetella rosea were observed and they were neither present during prebloom nor during post-bloom period (Figure 2). Exclusive zooplankton assemblages were found during pre-bloom and post-bloom period also. Zooplankton assemblage of only pre-bloom period includes Eucalanus crassus, Acrocalanus sp., Labidocera minuta, Centropages tenuiremis and Oithona sp. Similarly, Pseudodiaptomous aurivilli, ovigerous Oithona brevicornis and Hapacticoid copepodites were observed only during post-bloom period (Figure 3). Among holoplankters Evadne tergestina showed its dominance during bloom and postbloom period and was totally absent during prebloom period. Another cladoceran Pennilia avirostris was found in relatively high density during the bloom. Density of Sagitta sp and Oikopleura sp were relatively high during the bloom followed by the post-bloom period. A unique grouping of various crustacean meroplankters (nauplius, protozoea, postzoea, mysis etc) together with bivalve veliger larvae, polychaete larvae, cirripede nauplii were encountered during the study period (Figure 3). Appearance of echinoderm larvae was observed exclusively during the blooming phase with low density whereas; Diphyes sp and Fish larva appeared only during post-bloom period. Numerical abundance showed a descending order from pre-bloom to post-bloom period with average values of 5.5 x 105, 4.9 x 105, 4.3 x 105 individuals per 10 m3 during pre-bloom, bloom and post-bloom periods respectively (Figure 4).
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density was found to be 3.5 x 105, 3.0 x 105 and 2.5 post-bloom x 105 during pre-bloom, bloom, bloom and post
Copepods contributed up to 64 % of the total population during pre-bloom bloom period. Their average
Dendrogram Pseudodiaptomous aurivilli Oithona brevicornis (O) Oithona rigida (O) Centropages tenuiremis Acrocalanus sp. Eucalanus crassus Labidocera minuta Oithona sp. Bestiolina similis Acrocalanus longicornis Canthocalanus pauper Centropages elongatus Centropages orsinii Centropages sp. Euterpina acutifrons Oithona similis Oithona similis (O) Paracalanus sp. PS Clytemnestra scutellata Acrocalanus gibber Oithona brevicornis Oithona rigida Paracalanus aculeatus Paracalanus parvus Corycaeus danae Macrosetella gracilis Corycaeus sp Macrosetella gracilis (O) Oncaea venusta Canthocalanus sp. Acartia sp. Euterpina acutifrons (O) Labidocera acuta Labidocera pavo Microsetella rosea Oithona hebes Parvocalanus crassirostris Pontella securifer Pontellopsis scotti Pseudodiaptomous sp. Temora turbinata Acartia erythraea Acartia centrura Acartia spinicauda PS (O) 0.85
0.65
0.45
0.25
0.05
-0.15
-0.35
-0.55
Similarity
Figure 2: Dendrogram showing the formation of clusters by various copepod species during different phases of the Trichodesmium bloom (PS- Pseudodiaptomus serricaudatus serricaudatus; (O)- Ovigerous). The boxes assigned with English alphabets represent group of species (belonging to respective boxes) present or absent during different periods of bloom. A- Present only during pre pre-bloom and bloom; B- Most of the species were absent during pre-bloom totally absent during bloom and post-bloom; bloom period and relatively high density observed during ng bloom and post-bloom post period; C- Highest density during bloom as compared to that of pre pre- and postbloom periods; D- Exclusively present during bloom and were absent during prepre and post-bloom bloom periods; E- These three species of the genus Acartia were totally ally absent during the post post-bloom bloom period with relatively high density during the bloom period as compared to that of the pre-bloom bloom period.
periods respectively (Figure ure 5). Calanoids dominated the copepod community followed by cyclopoids & poicilostomatoids and harpacticoids. Calanoids were found to be very dominant dominan during pre-bloom bloom period (41%) and Paracalanidae was the most dominant family among calanoids .5% and 17.5% of the total contributing 22.5%
zooplankton community during pre pre-bloom and bloom period respectively. Other families such as Acartiidae, Pseudodiaptomidae, Pontellidae, Calanidae, Temoridae were the associated calanoid families appeared along with Paracalanidae during the period of study. However, during bloom period, cyclopoids & poicilostomatoids (25%)
SAHU et al.: MESOZOOPLANKTON COMMUNITY STRUCTURE DURING TRICHODESMIUM BLOOM
were the dominant group (calanoid population, 23%) (Figure 6).
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Copepod nauplii (14%), copepodites (3%) and ovigerous copepods (7%) contributed the highest
Dendrogram Oikopleura sp Evadne tergestina PL-Spiophanes sp Copepodites- Harpacticoid Decapod Zoea Decapod Mysis
A
Fish larvae Sagitta sp Decapod Nauplius Bivalve larva Decapod Post-zoea Hydromedusae
B
Lucifer sp Copepod nauplius
Copepodites - Calanoid
C
Diphyes sp Cirripede nauplii Fish egg Decapod Protozoea Penilia avirostris Gastropod larva Cirripede cypris PL- Myriochele sp
D
Lucifer hanseni Sagitta bedoti
Copepodites – Cyclopoid
0.93
0.83
0.73
0.63
0.53
Similarity
0.43
0.33
0.23
0.13
0.03
Figure 3: Dendrogram showing the formation of clusters by various non-copepod holoplankters, meroplankters and copepodites during Trichodesmium bloom (PL- polychaete larvae). The boxes assigned with English alphabets represent group of zooplankters (belonging to respective boxes) present or absent during different periods of bloom. A- totally absent during pre-bloom with highest density during bloom as compared to post-bloom period; B- relatively high density observed during bloom and post-bloom period; C- Highest density during post-bloom as compared to that of pre-bloom and bloom periods; D- first 5 species from top of the box were having relatively high density during bloom as compared to pre- and post-bloom periods, whereas, the other 4 species were present only during pre-bloom and bloom and absent during post-bloom period.
during post-bloom compared to bloom (Copepod nauplii- 9%; copepodites-1% & ovigerous copepods-5%) and pre-bloom period (Copepod nauplii- 3%; copepodites-1% & ovigerous copepods-3%). The non-copepod holoplankters contributed 13%, 11% and 6% to the total zooplankton density during pre-bloom, bloom and post-bloom period respectively. Among these noncopepod holoplankters, major species were Oikopleura sp., Sagitta bedoti, Lucifer hanseni, Penilia avirostris and Evadne tergestina. Evadne tergestina (35 %) contributed the highest to the
total non-copepod holoplankton abundance during bloom period followed by Penilia (27 %), Oikopleura (16 %), Sagitta (13 %) and Lucifer (9 %) (Figure 7). Chaetognatha was represented by Sagitta bedoti and Sagitta sp which contributed the highest (60%) to the total non-copepod holoplankton community during pre-bloom period followed by post-bloom (26%) and bloom period (13%). Contribution of Lucifer was the maximum (45%) among all the non-copepod holoplankters during post-bloom period.
INDIAN J. MAR. SCI., VOL. 44, NO. 9 SEPTEMBER 2015
Pre-bloom
Total density Total biomass 6.0
10 9 8 7 6 5 4 3 2 1 0
5.0 4.0 3.0 2.0 1.0 0.0 Pre-bloom
Bloom
Bloom
Post-bloom
100%
Biomass (ml per 10 m3)
Numerical Density (x 105 individuals per 10 m3)
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80% 60% 40% 20% 0%
Post Post-bloom Figure 7: Relative abundance of dominant non non-copepod holoplankters during pre-bloom, bloom, bloom and post-bloom periods
Density (x 105 organisms per 10 m3)
Figure 4: Variations in zooplankton density and bloom, bloom and post-bloom biomass during pre-bloom, post periods Total density
Total Copepod
Other holoplankton
Total meroplankton
6.0 5.0 4.0 3.0 2.0 1.0 0.0 Pre-bloom
Bloom
Post-bloom
Figure 5: Density of different groups of zooplankton during the study period Pre-bloom
Bloom
Post Post-bloom
100% 80% 60% 40% 20% 0%
Figure 6: Relative abundance of different copepod groups, non-copepod copepod holoplankters, meroplankters, Ovigerous copepods and copepodites during the study period
Zooplankton biomass values ranged between 3.16 – 8.61 ml per 10 m3 (Figure 4). The lowest value was observed during post post-bloom and the highest was observed during pre pre-bloom period. During pre-bloom bloom period, the biomass was mainly contributed by the members of the family Paracalanidae. The present study coincided with the post-NE NE monsoon period during which nutrient enrichment takes place in this coastal water essentially due to land run off and ingress of nutrient enriched freshwater from the backwaters. Subsequently when conditions such as optimum salinity, adequate irradiance and temperature prevail, phytoplankton population proliferates leading to elevation in zooplankton population. Goswami and Padmavati30 also reported the post-monsoon abundance of phytoplankton during post months which also supported higher population of herbivores. Diversity indices Species diversity is a measure of relationship between number of individuals and number of species. It tends to be low in physically controlled ecosystem31. As expected, species diversity (3.2) and species richness (2.7) showed relatively high values during the bloom period due to the existence of certain copepods belonging to the family Paracalanidae, Pontellidae, Temoridae, Oithonidae and Oncaedae ((Figure 9). In contrast, species composition was found to be low during pre-bloom bloom period although zooplankton density and biomass were high. This resulted in low species diversity as well as richness during pre prebloom period (Species es diversity diversity-2.7; Species richness-1.7). 1.7). Similarly, although zooplankton biomass and density were relatively low during post-bloom bloom period as compared to bloom and pre prebloom, qualitatively the post post-bloom period was
SAHU et al.: MESOZOOPLANKTON COMMUNITY STRUCTURE DURING TRICHODESMIUM BLOOM
observed to be similar as that of pre-bloom pre period. Evenness showed a very steady trend throughout the study period. Pre-bloom
Bloom
Post Post-bloom
100% 80% 60% 40% 20% 0%
Figure 8: Relative abundance of dominant meroplankters during pre-bloom, bloom and post-bloom bloom periods
3.5
SD
SR
E
3.0 2.5 Values
2.0 1.5 1.0 0.5 0.0 Pre-bloom
Bloom
Post-bloom
Figure 9: Variations in zooplankton diversity indices during the study period
Discussion The species composition, growth, proliferation and abundance of zooplankton are collectively influenced by a variety of abiotic environmental variables especially temperature, salinity, nutrients, transparency etc13. However, Dominance of particular zooplankton groups during different phases of environmental change depends upon their response to one of the most important factors present instance, due i.e. food availability32. In the pre to the short-term nature of the investigation that focused mainly on the impact of bloom on zooplankton, no significant influence of the above observed. On the other abiotic parameters could be observed hand, it has been reported that coastal water wat enriched with nutrients during the post-monsoon post period at this region results in spring outburst of phytoplankton, which leads to subsequent
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alteration in zooplankton distribution30, post-monsoon period, . Generally, during post temperature and salinity remains at optimum level in this coastal water, which assists in phytoplankton growth. It is well known that, optimal growth of Trichodesmium occur in the temperature range of 25 25-35 oC and salinity >32 34-36 psu . A similar temperature and salinity condition as above was observed during the present study, which further corroborated with the earlier reports of Trichodesmium bloom29, 37-40. Phytoplankton bloom has long been known as a phenomenon that can change the aquatic 43 ecosystem drastically41-43 . Though for a short period of time, it has a significant impact on the water quality, plankton dynamics, fishery and benthic organisms44-47. Release of toxins and depletion of oxygen by the decaying biomass could have a deleterious effect whereas; boost in primary production could enhance the fishery potential of 48-52 the region temporarily48 . Primary consumers, mostly the zooplankters, act as the main link for the above negative as well as positive affects being propagated to the higher trophic level in the food chain. In the present study a significant increase in species diversity and richness of zooplankton observed during the bloom. Similarly, the number of copepod species observed during bloom was the pre-bloom and highest as compared to that of the pre post-bloom periods. eriods. It amply signifies that copepods along with other zooplankton species thrived well during the bloom period as Trichodesmium could have served as the food resource13, 35, 53. On the other hand, some workers have attributed the reduction of copepod ddensity during bloom and post-bloom bloom period either to the neurotoxic behavior of Trichodesmium or deoxygenation of water during bloom decay17, 54. During phytoplankton bloom, some groups of zooplankters rise in the water column to be within the food source32. A couple of such varieties of zooplankton are cyclopoid and poicilostomatoid copepods32. They are the most active feeders during initial period of the bloom (regarded as herbivores, carnivores and omnivores) 32, 55. most common Though calanoids alanoids are arguably the mo and abundant planktonic copepods anywhere in the world oceans56 at any given time, carnivorous nature of most of the cyclopoids & poicilostomatoids might be the plausible cause of the calanoid population reduction57-58 and boosting of cyclopoid & poicilostomatoid population during the bloom period in the present study. As expected, during bloom and post post-bloom period, the abundance of Oithona spp. was relatively high as the bloom acted as the food source for them.
33
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According to Atkinson and Shreeve32, Oithona spp. is a major feeder among the copepods having wide range of food habits55, feeding selectively on motile food. Moreover, Oithona is known to survive and reproduce under a broad range of conditions55, 59-60. Despite of a significant reduction in population of calanoids, species such as Paracalanus parvus, P. aculeatus, Acrocalanus gibber, Acrocalanus longicornis and Bestiolina similis (family-Paracalanidae) were abundant during the bloom and post-bloom periods (Figure 2). The representatives of family Acartiidae might be considered as the key element in food webs because they act as predator consuming ciliates and other copepods. Interestingly all the 3 species (Acartia spinicauda, A. erythraea and A. centrura) belonging to this family, omnivorous in nature, were completely absent during post-bloom period. This suggests that, their distribution was possibly affected due to predation. Interestingly, Oithona rigida abundantly co-occurred with Acartia spinicauda during the bloom period which has also been observed by others61-62. The other major group of copepods, harpacticoids (harpacticoida) represented by 4 species, thrived well during the bloom and postbloom periods. Reports indicate that toxins released by Trichodesmium deter grazers (calanoid and cyclopoid copepods- considered to be the major grazers in these systems) other than those specialized harpacticoids of the family Miraciidae63. Abundance of Macrosetella gracilis, Microsetella rosea and Euterpina acutifrons during bloom period showed that these harpacticoid species are well equipped for grazing of Trichodesmium. Microscopic analysis showed adult and larval Macrosetella gracilis attached to Trichodesmium filaments. These copepod larvae require substrate for creeping, which lead them for development, whereas, adults graze on Trichodesmium filaments. The above observation is supports by the findings of others63-65 wherein the authors have reported the survival of harpacticoids in presence of high Trichodesmium density. Abundance of cladocerans has been reported during spring phytoplankton blooms, particularly the Trichodesmium bloom15, 18. In the present study, Evadne tergestina and Penilia avirostris are the two species found abundantly during the bloom period. Generally, Evadne tergestina abounds in, when the temperature and salinity values are moderately high30 and similar conducive condition during the present study ameliorated its abundance during bloom and post-bloom period. As observed in the present instance, synchronization in the occurrence of Trichodesmium bloom and swarming
of Evadne tergestina has also been reported off Cochin66. Of all the cladocerans, Penilia avirostris has been described as the true filter feeder which inhabits near-shore waters of tropical and warm temperate areas67. Observation of relatively high Penilia avirostris density during bloom could be attributed to the fact that it has got good feeding adaptations to outcompete other components of marine zooplankton such as copepods68. Chaetognaths are considered as the primary as well as secondary carnivores in zooplankton community and thus, can survive adverse conditions. They mainly feed upon the abundant species of zooplankton that includes copepods, crustacean larvae, luciferidae, hydromedusae etc69. Their abundance during the bloom could be attributed to the fact that relatively high species diversity and richness of zooplankton observed during that period could have served as good food source. A direct relationship between the abundance of chaetognaths and population of copepods & total zooplankton was observed during the study period as has been reported earlier from other region70. Similar to that of the chaetognaths, the appendicularian Oikopleura sp was present in relatively high density during bloom and postbloom period. Variations in larval plankton population in terms of total density were minimal during the prebloom, bloom and post bloom periods. However, significant increase in population of copepod nauplii, copepodites and ovigerous copepods during post-bloom period could be ascribed to adequate food availability during bloom period, which has also been reported by others57, 71. Observation of cirripede nauplii in relatively high density during bloom and post-bloom period could be attributed to enough food supply and renewing of reserves in the adults during the bloom. Starr et al.72 and Barnes73 have reported coupling of naupliar release in barnacles with that of phytoplankton blooms and the same has also been observed in case of urchins and mussels. Presence of fish egg and larvae in good quantity during the bloom showed that the bloom biomass provided food and shelter to the fishes which corroborated the findings of Padmakumar et al.64. Conclusion The cyanobacterial bloom had a considerable impact on the zooplankton community of the coastal waters. A significant reduction in zooplankton density was observed from bloom to post-bloom periods. Calanoid copepods dominated the mesozooplankton community prior to bloom whereas; reduction in calanoid population and boosting of cyclopoid & poicilostomatoid population was observed during the bloom period.
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Increase in population density of copepod nauplii, copepodites and ovigerous copepods during postbloom period could be attributed to the adequate food availability during bloom. Relatively high density of Penilia avirostris & Evadne tergestina and Acartia spinicauda alongwith Oithona spp., during peak bloom were found to be the interesting features of this study. Reports indicate that some species of Trichodesmium produce a toxin that deters grazing by copepods (calanoid and cyclopoid copepods- considered to be the major grazers in these systems) other than those specialized harpacticoids of the family Miraciidae63. However, in the present instance, intraand inter-specific interactions of zooplankters during bloom could be the primary factor leading to change in their community structure.
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References 1.
Li M, Gargett A & Denman K, What determines seasonal and interannual variability of phytoplankton and zooplankton in strongly estuarine systems? Application to the semi-enclosed estuary of Strait of Georgia and Juan de Fuca strait. Estuar. Coastal Shelf Sci., 50 (2000) 467488. 2. Kibirige I & Perissinotto R, The zooplankton community of the Mpenjati estuary, a South African temporarily open/closed system. Estuar. Coastal Shelf Sci., 58 (2003) 1-15. 3. Telesh I V, Plankton of a Baltic estuarine ecosystem with emphasis on Neva estuary: a review of present knowledge and research perspectives. Mar. Pollut. Bull., 49 (2004) 206-219 4. Hall C J & Burns CW, Responses of crustacean zooplankton to seasonal and tidal salinity changes in the coastal Lake Waihola, New Zealand. New Zeal. J. Mar. Freshwater Res., 37 (2003) 45-52. 5. Lam-Hoai T, Guiral D & Rougier C, Seasonal Change of Community Structure and size spectra of zooplankton in the Kaw River estuary (French Guiana). Estuar. Coast. Shelf Sci., 68 (2003) 47-61. 6. Deevey G B & Brooks A L, Copepods of the Sargasso Sea off Bermuda: species composition, and vertical and seasonal distribution between the surface and 2000 m. Bull. Mar. Sci., 27 (1977) 256-291. 7. Madlin L P, Erich F H & Steinberg D K, Zooplankton at the Bermuda Atlantic time-series study (BATS) station: diel, seasonal and interannual variation in biomass, 19941998. Deep Sea Res. II, 48 (2001) 2063-2082. 8. Alcaraz M, Calbet A, Estrada M, Marrase C, Saiz E and Trepat I, Physical control of zooplankton communities in the Catalan Sea. Prog. Oceanogr., 74 (2007) 294–312. 9. Roman M R, Dam H G, Gauzens A L, Urban-Rich J, Foley D G & Dickey T D, Zooplankton variability on the equator at 140ºW during the JGOFS EqPac study. DeepSea Res. II, 42 (1995) 673- 693. 10. White J R, Zhang X, Welling L A, Roman M R & Dam H G, Latitudinal gradients in zooplankton biomass in the tropical Pacific at 140ºW during the JGOFS EqPac study: Effects of El Nino. Deep Sea Res. II, 42 (1995) 715-733. 11. Achuthankutty C T, Madhupratap M, Nair V R, Nair S R S & Rao T S S, Zooplankton biomass and composition in
19.
20.
21.
22.
23. 24.
25.
26. 27.
28.
29.
1291
the western Bay of Bengal during late southwest monsoon. Indian J. Mar. Sci., 9 (1980) 201-206 Nair S R, Nair V R, Achuthankutty C T & Madhupratap M, Zooplankton composition and diversity in western Bay of Bengal. J Plankton Res., 3 (1981) 493–508. Rakesh M, Raman A V & Sudarshan D, Discriminating zooplankton assemblages in neritic and oceanic waters: a case study for the Northeast coast of India, Bay of Bengal. Mar. Environ. Res., 61 (2006) 93-109. Saravanane N, Nandakumar K, Durairaj G and Nair K V K, Plankton as indicators of coastal water bodies during southwest to northeast monsoon transition at Kalpakkam. Curr. Sci., 78 (2000) 173-176. Turner J T & Tester P A, Toxic marine phytoplankton, zooplankton grazers, and pelagic food webs. Limnol. Oceanogr., 42 (1997) 1203-1214. Turner J T, Harmful algae interactions with marine planktonic grazers, in: Ecology of Harmful Algae, edited by E. Granéli & J T Turner (Springer, Netherlands) 2006. Devassy V P, Bhatrarhiri P M A & Qasim S Z, Succession of organisms following Trichodesmium phenomenon. Indian J. Mar. Sci., 8 (1979) 89-93. Nair V E, Devassy V P & Madhupratap M, Blooms of phytoplankton along the coast of India associated with nutrient enrichment and the response of zooplankton, in: Marine coastal eutrophication, edited by R.A. Vollenweiden, et al. (Science of the Total Environment, Elsevier) 1992, pp. 819-828. Satpathy K K, Mohanty A K, Sahu G, Natesan U, Venkatesan R & Prasad M V R, Physico-chemical alterations in the coastal waters of Kalpakkam, east coast of India during the southwest to north-east monsoon transition. Environ. Monit. Assess., 171, (2010) 411-424. Grasshoff K, Ehrhardt M & Kremling K, Methods of seawater analysis, (Wiley- VCH, New York) 1983, pp. 786 Parsons T R, Maita Y & Lalli C M, A manual of chemical and biological methods for Seawater analysis, (Pergamon Press, New York) 1984, pp. 173 Vollenweider, R. A. A manual on methods for measuring primary production in aquatic environments, (IBP hand book no 12, Blackwell scientific publication, London) 1974, pp. 225 Desikachary T V, Atlas of diatoms III & IV, (Madras Science Foundation, Madras) 1987, pp.239 Subramanian R, The Dinophycaes of Indian Seas Part-I. Genus Ceratium, (Marine Biological Association of India) 1968, pp. 129 Subramanian R, The Dinophycaes of Indian Seas Part-II. Peridiniaceae, (Marine Biological Association of India) 1971, pp. 134 Fristch F E, The Structure and Reproduction of Algae, Vol. II, (Cambridge Univ. Press, London) 1935, pp. 263 Kasturirangan L R, Saraswathy M & Gopalakrishnan T C, Distribution of copepoda in the Indian Ocean, in: Biology of the Indian Ocean, edited by B. Zeitzschel & S.A. Gerlach (Springer-Verlag, Berlin) 1973, pp. 331– 333. Conway D V P, White R G, Hugues-Dit-Ciles J, Gallienne C P & Robins D B, Guide to the coastal and surface zooplankton of the south-western Indian Ocean, (Occasional Publication No - 15, Marine Biological Association, UK) 2003, pp 354. Santhanam R, Srinivasan A, Ramadhas V & Devaraj M, Impact of Trichodesmium bloom on the plankton and productivity in the Tuticorin Bay, Southeast coast of India. Indian J. Mar. Sci., 23 (1994) 27-30.
1292
INDIAN J. MAR. SCI., VOL. 44, NO. 9 SEPTEMBER 2015
30. Goswami S C & Padmavati G, Zooplanktyon production, composition and diversity in the coastal waters of Goa. Indian J. Mar. Sci., 25 (1996) 91–97. 31. Odum E P, Fundamentals of ecology, (W B Saunders Comp., Philadelphia, London, Toronto) 1971. 32. Atkinson A & Shreeve R S, Response of the copepod community to a spring bloom in the Bellingshausen Sea. Deep Sea Res. II, 42 (1995) 1291-1311. 33. Satpathy K K & Nair K V K, Occurrence of phytoplankton bloom & its effect on coastal water quality. Indin J. Mar. Sci., 25 (1996) 145-147. 34. Marumo R & Nagasawa S, Seasonal variation of the standing crop of a pelagic blue-green alga, Trichodesmium in the Kuroshio water. Bull. Plankton Soc. Japan, 23 (1976) 19–25. 35. Carpenter E J, Physiology and ecology of the marine plankton Oscillatoria (Trichodesmium). Mar. Biol. Lett., 4 (1983) 69-85. 36. Krishnan A A, Krishnakumar P K & Rajagopalan M, Trichodesmium erythraeum (EHR) bloom along the southwest coast of India (Arabian Sea) and its impact on trace metal concentrations in seawater. Estuar. Coast. Shelf Sci., 71 (2007) 641-646. 37. Qasim S Z, Some characteristic of a Trichodesmium bloom in the Laccadives. Deep Sea Res., 17 (1970) 655660. 38. Ramamurthy V D, Selva Kumar A R & Bhargava R M S, Studies on the blooms of Trichodesmium erythraeum (EHR) in the waters of the central west coast of India. Curr. Sci., 41,(1972) 803-805. 39. Desa E, Suresh T, Matondakar S G P, Desa E, Goes J, Mascarenhas A, Parab S G, Shaikh N & Fernandes C E G, Detection of Trichodesmium bloom patches along the eastern Arabian Sea by IRS-P4/OCM ocean colour sensor and by in-situ measurements. Indian J. Mar. Sci., 34 (2005) 374-386. 40. Satpathy K K, Mohanty A K, Gouri sahu, Usha Natesan, Venkatesan R & Prasad M V R, On the occurrence of Trichodesminum erythraeum (Ehr.) bloom in the coastal waters of Kalpakkam, east coast of India. Indian J. Sci. Tech., 1 (2007) 1-11. 41. Shumway S, A review of the effects of algal blooms on shellfish and aquaculture. J World Aquacult. Soc., 21 (1990) 65–104. 42. Smayda T J, Primary production and the global epidemic of phytoplankton blooms in the sea: a linkage? In: Novel Phytoplankton Blooms, edited by E.M. Cosper, V.M. Bricelj & E.J. Carpenter (Coastal and Estuarine Studies, No. 35, Springer-Verlag, New York) 1989, pp 449–484. 43. Landsberg J H, The effects of harmful algal blooms on aquatic organisms. Rev. Fish. Sci., 10 (2002) 113–390. 44. Shimizu Y, Unexpected developments in red tide research. Maritimes, 4 (1983) 62-71. 45. Hallegraeff G M, A review of algal blooms and their apparent global increase. Phycologia, 32 (1993) 79-99. 46. Anderson, D.M. Toxic algal blooms and red tides: a global perspective. In Okaichi, T., Anderson, D.M. & Nomoto, T. (Eds.) Red Tides: Biology, Environmental Science and Toxicology (pp 11-16), Elsevier, New York. (1989). 47. Glibert P, Pitcher G, Global Ecology and Oceanography of Harmful Algal Blooms, (Science Plan. SCOR and IOC, Baltimore and Paris) 2001. 48. Eashwar M, Nallathambi T, Kuberaraj K & Govindarajan G, Noctiluca blooms in Port Blair Bay, Andaman. Curr. Sci., 81 (2001) 203-206. 49. Dharani G, Abdul Nazar A K, Kanagu L, Venkateshwaran P, Kumar T S, Ratnam K, Venkatesan R & Ravindran M, On the reoccurrence of Noctiluca
50.
51. 52.
53.
54.
55.
56.
57.
58.
59.
60.
61.
62.
63.
64.
65.
66.
scintillans bloom in Minnie Bay, Port Blair: Impact on water quality and bioactivity of extracts. Curr. Sci., 87 (2004) 990-994. Matondkar S G P, Bhat S R, Dwivedi R M & Nayak S R, Indian satellite IRS-P4 (OCEANSAT) monitoring algal blooms in the Arabian Sea. Harmful Algae News, 26 (2004) 4-5. Devanesan D W, A note on the food and feeding habit of Sardinella gibbosa. J. Madras Univ., 11 (1932) 142. Subrahmanyam, R. Studies on the phytoplankton of the west coast of India. Proc. Indian Acad. Sci., 50 (1959) 113-187. Bryceson I & Fay P, Nitrogen fixation and the autecology of Oscillatoria erythraea (Erhenberg) Kuetzing a planktonic cyanophyte from the coastal waters of Tanzania: a preliminary investigation, in: Proceedings of symposium on the coastal and marine environment of the Red Sea, Gulf of Aden and tropical Western Indian Ocean in Khartoum, Sudan, 1980, pp. 471-494. Qasim S Z, Some observations on Trichodesmium bloom, in: Taxonomy and Biology of Blue-green algae, edited by T.V. Desikachary, (University of Madras, India) 1972, pp. 433-438. González H E & Smetacek V, The possible role of the cyclopoid copepod Oithona in retarding vertical flux of zooplankton faecal material. Mar. Ecol. Prog. Ser., 113 (1994) 233–246. Madhupratap M, Free-living copepods of the Arabian Sea: Distributions and research perspectives. Indian J. Mar. Sci., 28 (1999) 146–149. Fransz H G, Vernal abundance, structure and development of epipelagic copepod populations of the eastern Weddell Sea (Antarctica). Polar Biol., 9 (1988) 107–114. Fernandes V & Ramaiah N, Mesozooplankton community in the Bay of Bengal (India): spatial variability during the summer monsoon. Aquat. Ecol., 43 (2009) 951-963. Gauld D T, The swimming and feeding of planktonic copepods, in: Some contemporary studies in marine science, edited by H. Barnes, (George Allen and Unwin Ltd, London) 1966, pp. 313-334. Turner J T, Zooplankton feebng ecology: contents of fecal pellets of the cyclopold copepods Oncaea venusta, Corycaeus amazonicus, Oithona plumifera and O. Slmplex from the northeastern Gulf of Mexico. P.S.Z.N.I. Mar. Ecol., 7 (1986) 289-302. Tan Y, Huang L, Chen Q, et al., Seasonal variation in zooplankton composition and grazing impact on phytoplankton standing stock in the Pearl River Estuary, China. Cont. Shelf Res., 24 (2004) 1949-1968. Omori M & Hamner W N, Patchy distribution of zooplankton: behavior, population assessment and sampling problems. Mar. Biol., 72 (1982) 193–200. O'Neil J M & Roman M R, Ingestion of the cyanobacterium Trichodesmium spp. by the pelagic harpacticoid copepods Macrosetella, Miracia, and Oculasetella, Hydrobiologia, 235 (1994) 92–293. Padmakumar K B, Smitha B R, Thomas L C et al., Blooms of Trichodesmium erythraeum in the South Eastern Arabian Sea during the onset of 2009 Summer Monsoon. Ocean Sci. J., 45 (2010) 151-157. Hawser S P, O’Neil T M, Roman M R & Codd G A, Toxicity of blooms of Trichodesmium to zooplankton. J. Appl. Phycol., 4 (1992) 79-86. Kasturirangan L R, A Key to the identification of the more common planktonic copepoda of India coastal waters, (Publication no-2, Indian national committee on
SAHU et al.: MESOZOOPLANKTON COMMUNITY STRUCTURE DURING TRICHODESMIUM BLOOM
67.
68.
69.
70.
oceanic research, Council of Scientific and Industrial Research, New Delhi) 1963, pp. 87. Marazzo A, & Valentin J L, Spatial and temporal variations of Penilia avirostris and Evadne tergestina (Crustacea, Branchiopoda) in a tropical bay, Brazil. Hydrobiologia, 445 (2001) 133-139. Atienza D, Saiz E, & Calbet A, Feeding ecology of marine cladoceran Penilia avirostris: natural diet, prey selectivity and daily ration. Mar. Ecol. Prog. Ser., 315 (2006) 211-220. Marazzo A, Machado C F & Nogueira C S R, Notes on feeding of chaetognatha in Guanabara Bay, Brazil. J. Plankton Res., 19 (1997) 819-828. Sarkar S K, Singh B N and Choudhury A, Composition and variations in the abundance of zooplankton in the
1293
Hooghly estuary, West Bengal, India. Proceedings: Animal sciences, 95 (1986) 125-134. 71. Hopkins T L, Lancraft T M, Torres J J & Donnelly J, Community structure and trophic ecology of zooplankton in the Scotia Sea marginal ice zone in winter. Deep Sea Res., 40 (1993) 81-105. 72. Starr M, Himmelman J H & Therriault J C, Coupling of nauplii release in barnacles with phytoplankton blooms: a parallel strategy to that of spawning in urchins and mussels. J. Plankton Res., 13 (1991) 561-571. 73. Barnes H, Note on variations in the release of nauplii of Semibalanus balanoides with special reference to the spring diatom outburst. Crustaceana, 4 (1962) 118-122.
