Potential Use of Biomarkers in Zooplankton as Early Warning Signals of Ecotoxicological Risk in the Marine Food Chain

Abstract. Zooplankton is an essential component of the marine and brackish food chains. The ecotoxicological risk of zooplanktonic communities, estimated by the modern methodological approach of biomarkers, can be used as an early warning signal of ecosystem health. The aim of this project is to estimate the potential use of several biomarkers (esterases, mixed function oxidases, porphyrins) in zooplanktonic organisms. Studies were carried out with different zooplanktonic crustaceans: the copepods Acartia margalefi and Acartia latisetosa collected in Ganzirri Lake (Messina); the mysid Siriella clausi collected in Faro Lake (Messina); the mysids Diamysis bahirensis, Siriella armata and Mysidopsis gibbosa collected in Stagnone di Marsala (Palermo); the Antarctic euphausiids Euphausia crystallorophias and Euphausia superba; the am-phipod Streetsia challengeri and the euphausiid Meganycthiphanes norvegica collected after a shore-stranding along Messina's Ionian coast. Moreover, experiments were carried out with the benthic decapods Eriphia verrucosa and Pachygrapsus marmoratus from a rocky shore of Messina's Ionian coast. Acetylcholinesterase activity (AChE) was determined in homogenates of whole organisms. The key result of this project concerns the different AChE activity basal values of different crustacean species. Particular attention should be paid to the difference in basal activity found between the Antarctic and the Mediterranean species.     

Multi-trial biomarker approach in Meganyctiphanes norvegica: a potential early indicator of health status of the Mediterranean "whale sanctuary."

The aim of this study was to propose a suite of biomarkers (BPMO activity, NADPH-cytocrome c reductase, NADH-ferricyanide reductase. esterases, porphyrins, vitellogenin and zona radiata proteins) and residue levels (organochlorines, PAHs and heavy metals) in the zooplanktonic euphausiid Meganyctiphanes norvegica as a potential multi-disciplinary diagnostic tool for assessment of the health status of the Mediterranean "whale sanctuary". Very little difference in BPMO was detected between sites, with values ranging from 0.75 to 2.68 U.A.F./mg prot/h. On the other hand larger differences between sites were found for reductase activities. Esterases (AChE), porphyrins (Copro-, Uro-, Proto-porphyrins) vitellogenin and zona radiata proteins were also detectable in this zooplanctonic species. Hg showed mean levels of 0.141 ppm d.w., Cd 0.119 ppm d.w. and Pb 0.496 ppm d.w. Total PAHs ranged from 860.7 to 5,037.9 ng/g d.w., carcinogenic PAHs from 40.3 to 141.7 ng/g d.w., HCB from 3.5 to 11.6 ng/g d.w., DDTs from 45.3 to 163.2 ng/g d.w. and the PCBs from 84.6 to 210.2 ng/g d.w.     

Successful colonization of the calanoid copepod Acartia tonsa in the oligo-mesohaline area of the Gironde estuary (SW France) – Natural or anthropogenic forcing?

The copepod Acartia tonsa appeared in Europe in the first half of the 20th century and colonized progressively European seas and estuaries, possibly transferred from North Atlantic Coast of America. It had been reported in the polyhaline area of the Gironde estuary for a long time but was first recorded in the oligo-mesohaline area in 1983. Its abundance has been increasing significantly. High abundances of A. tonsa were reported since 1999, supplanting the abundances of its autochthonous congeneric species, Acartia bifilosa. This colonization was characterized by analyzing the mean seasonal variability: (1) for three 5-year periods corresponding to three different steps of A. tonsa appearance (1978–1982, A. tonsa was absent; 1988–1992, low abundances of the species; and 1999–2003, high abundances of A. tonsa) in the oligo-mesohaline area and (2) for three stations distributed along the salinity gradient during the recent period. The aim of this work was to define if this colonization was due to natural or anthropogenic forcing and to evaluate its possible impact on autochthonous zooplanktonic community.Both natural and anthropogenic forcings seem to explain the colonization of Acartia tonsa in the oligo-mesohaline area of the Gironde estuary. First records (1983–1988) could be due to marine water inputs caused by high values of the North Atlantic Oscillation index. The global warming which caused the increase of the summer warm period, the marinisation of the system and the local decrease of the turbidity should have been the key factors favoring the establishment of the species. Anthropogenic forcings as the establishment of the nuclear power plant which locally causes warmer conditions are also important factors explaining the differences of seasonal cycle observed between oligo-mesohaline area and other stations: the seasonal pattern of A. tonsa in the oligo-mesohaline area was indeed characterized by an autumnal peak of abundances which has been observed in other stations and in many North European estuaries, and by a second spring peak that had only been observed in Southern estuaries.The introduction of Acartia tonsa in the Gironde estuary significantly changed the seasonal pattern of autochthonous copepods, by limiting their seasonal abundances without affecting their long-term population stability. Finally, the successful colonization of A. tonsa had led to the spread of the seasonal zooplanktonic production which could have had an impact on fish and shrimp productions.     

Biomarker responses to pollution in two invertebrate species: Scrobicularia plana and Nereis diversicolor from the Cádiz bay (SW Spain)

The clam Scrobicularia plana and the polychaete worm Nereis diversicolor were collected in several sites from a littoral enclosure in SW Spain. The aim of our study was to relate various biomarker responses in these species to a pollution gradient caused by untreated domestic discharges and to verify the adequacy of the selected species as sentinels in this habitat. The biomarkers selected were the antioxidant enzymes catalase (CAT), glutathione peroxidase (GPX) and DT-diaphorase (DT-D). In addition, the activities of cytochrome P450-dependent ethoxyresorufin O-deethylase (EROD) activity, the phase II detoxifying enzyme glutathione S-transferase (GST) and the neurotoxicity marker acetylcholinesterase (AChE) were measured. Metallothionein levels were selected as biomarkers of heavy metals exposure in both species. The results suggest a different response in the water filtering organism (clam) and the sediment eater (polychaete), probably as a consequent of different pollution exposure and that samples from the “Caño Sancti-Petri” were exposed to biologically active compounds that altered some of their biochemical responses. AChE was the most sensitive biomarker in both species and N. diversicolor proved to be a more robust sentinel in this ecosystem.     

In vitro and in vivo inhibition of acetylcholinesterase and carboxylesterase by metals in zebrafish (Danio rerio)

Metals are natural components in ecosystems; however, if these elements are in excess, they can have adverse effects on living organisms. This study analyzes the interference of copper, lead, iron and cadmium in acetylcholinesterase (AChE) and carboxylesterase (CbE) activities in zebrafish. AChE was significantly inhibited in vitro by copper, iron, lead and cadmium at higher concentrations (10 and 20 mmol/L), whereas CbE was inhibited only at a concentration of 20 mmol/L. In vivo, only lead and cadmium were able to cause AChE inhibition at higher concentrations, while iron didn't cause any changes, and copper promoted an increase in AChE activity at a concentration of 0.06 mg/L. CbE activity did not change at any of the times (two and seven days) and concentrations tested, except in the case of copper exposure, which resulted in a decrease in CbE activity. Indeed, iodoacetamide treatment didn't changed AChE neither CbE activities, results which indicate that the metal inhibiting effect is probably not due to its biding to thiol groups close the active site of the enzyme. This outcome reveals that metals are important esterase inhibitors in zebrafish, and should be considered in environmental monitoring studies that use esterase inhibition as exposure biomarkers of organophosphate and carbamate pesticides.     

Biomarker responses to pollution in two invertebrate species: Scrobicularia plana and Nereis diversicolor from the Cádiz bay (SW Spain)

The clam Scrobicularia plana and the polychaete worm Nereis diversicolor were collected in several sites from a littoral enclosure in SW Spain. The aim of our study was to relate various biomarker responses in these species to a pollution gradient caused by untreated domestic discharges and to verify the adequacy of the selected species as sentinels in this habitat. The biomarkers selected were the antioxidant enzymes catalase (CAT), glutathione peroxidase (GPX) and DT-diaphorase (DT-D). In addition, the activities of cytochrome P450-dependent ethoxyresorufin O-deethylase (EROD) activity, the phase II detoxifying enzyme glutathione S-transferase (GST) and the neurotoxicity marker acetylcholinesterase (AChE) were measured. Metallothionein levels were selected as biomarkers of heavy metals exposure in both species. The results suggest a different response in the water filtering organism (clam) and the sediment eater (polychaete), probably as a consequent of different pollution exposure and that samples from the "Ca?o Sancti-Petri" were exposed to biologically active compounds that altered some of their biochemical responses. AChE was the most sensitive biomarker in both species and N. diversicolor proved to be a more robust sentinel in this ecosystem.     

Response of Acartia populations to environmental variability and effects of invasive congenerics in the estuary of Bilbao, Bay of Biscay

The effect of environmental factors (river discharge, water temperature and dissolved oxygen saturation) on the abundance and distribution of Acartia populations and the interactions between their congenerics was evaluated by means of transfer function (TF) models in the estuary of Bilbao during the period 1998–2005. The recorded species were Acartia clausi, Acartia tonsa, Acartia margalefi and Acartia discaudata. Acartia clausi dominated in the entire euhaline region of this estuary until 2003 when it was displaced from the inner part by A. tonsa. This invasive species (A. tonsa) was found for the first time in 2001 and colonized successfully the inner (salinity 30) and intermediate (salinity 33) waters of this estuary since 2003. The TF models revealed an immediate and negative effect of A. tonsa on A. clausi in the intermediate salinity (33) waters, where these species showed the highest spatial overlap. The results indicate that environmental changes from 2003 influenced the abundance of Acartia species, being unfavourable for A. clausi. The decrease of A. clausi abundance in low salinity waters was related to a significant decrease of dissolved oxygen saturation levels, whereas the increase of temperature was linked to a significant increase of A. tonsa. Acartia margalefi and A. discaudata were scarce over the entire period, but they were found to be valuable indicators of hydrological changes, which were associated to climate factors. These two latter species increased in abundance and expanded their seasonal distribution, and in the case of A. margalefi also its spatial distribution, in 2002, coinciding with the period in the time-series when autumn–winter rainfall and summer temperatures were lowest, and dissolved oxygen saturation levels were highest.     

基于线粒体cox1片段序列的胶州湾浮游动物DNA条形码分析

采用cox1基因特异扩增测序的方法,分析了胶州湾45种常见海洋动物的DNA条形码序列82条,联合GenBank中28条cox1序列的分析结果表明：种内个体间遗传差异均值为0.013（0—0.11）;属内不同种间遗传差异均值为0.265（0.137—0.369）,是种内遗传差异的20多倍,条形码间隙明显。在分子系统树中,...     

Kinetic and toxicological characteristics of acetylcholinesterase from the gills of oysters (Crassostrea rhizophorae) and other aquatic species

The aim of this work was to characterize the cholinesterases from gills of Crassostrea rhizophorae in order to use them as biomarkers. Gills were homogenized and then centrifuged (9,000 x g, 4 degrees C, 30 min). S9 and Triton X-100 S9 treated (TX S9) fractions were employed as enzyme source. Km(ap) and Vmax were estimated, using acetylthiocholine iodide as substrate. Inhibition assays were performed with iso-OMPA and eserine. The Km(ap) for S9 and TX S9 fractions were 0.05 and 0.06 mM, whereas the Vmax were 1.92 and 5.84 nmol/min/mg protein. respectively. No inhibition was detected when the samples were incubated with iso-OMPA, suggesting the presence of acetylcholinesterases (AChE) in oyster gill homogenates. Sensitivity to eserine inhibition of AChE in the gills of oysters is intermediate when compared with other aquatic species.     

温度和饵料对双刺纺锤水蚤产卵率和孵化率的影响

Acartia bifilosa (Copepoda: Calanoida) is a common species in offing of global waters and it often becomes dominant species in some estuaries. This species develops different strategy according to variation of environment. Despite its ecological role, Acartia bifilosa also has been concerned as live feeds in aquaculture, but study on egg production rate of this species in saturated diet in different temperature and different diet is so far not available. In order to interpret the importance of temperature and diet on natural population variation and also on aquaculture as foods of larval fish, the functional response of reproductive success of Acartia bifilosa was quantified in the laboratory using different temperatures and diets. Acartia bifilosa was captured in Jiaozhou Bay and acclimated to corresponding temperature for 3~4 days. In order to reduce the effect of large extent temperature range on organism, we captured Acartia bifilosa from March to June and acclimated them to temperature which is adjacent to natural temperature. Daily egg production rate (EPR, eggs female-1day-1) was detected for 11~15 days at 5 different temperatures ranged from 8.0 to 23 °C and all the females was feed on saturated diet all through the experiments. EPR on first day was not calculated in the mean EPR to eliminate the effect of different diets. This result showed that Acartia bifilosa spawned continuously during the experiment days and no obvious regulation was found. EPR was positively correlated with temperature from 8.0 to 23 °C. The highest mean EPR was observed at 23 °C (7.3 eggs female-1day-1), and the lowest value was found at 8 °C (3.8 eggs female-1day-1). The effect of diets on EPR was evaluated at two different temperatures (8.0 °C and 12.5 °C). Same trends were found at the two temperatures: mean EPR fed on Chaetoceros sp. was higher than that fed on Skeletonema costatum, and during the 14-day experiments, EPR was higher for females fed on Skeletonema costatum than chaetoceros sp. in the first few days (3~5 days), but it changed reversely in the subsequent days until the end of the experiments. Hatched eggs were observed in the two experiments at temperature 8°C and 12.5 °C and no diapause eggs were found. The hatching success rate was low at 8°C but reached 93.2% at 12.5 °C. According to the results in this paper, we detected the comfortable temperature range for EPR, and evaluated the effect of Skeletonema costatum which often brings out red tide in natural waters. These results are beneficial to ecological research for explaining population variation and population recruitment of this species, These data also can be used in Acartia bifilosa aquaculture.     

北黄海獐子岛海域浮游动物群落年际变化

本文比较了海洋普查期间（1959年1-12月）和2009-2010年獐子岛海域附近站位的浮游动物的种类组成、优势种、丰度、生物多样性,结果显示,北黄海区域浮游动物群落物种组成未发生较大的变化,在獐子岛海域以及整个北黄海,中华哲水蚤和强壮箭虫的优势种地位没有发生变化,细足法虫戎也一直出现且为冬春季的优势种;太平洋磷虾在2009-2010年獐子岛海域虽然全年均有出现,但是全年均不是优势种,而在1959年的獐子岛海域,作为优势种出现在4月和11月;1959年与2009年相较,腹针胸刺水蚤在春夏季优势种的地位被沃氏纺锤水蚤所取代。2009年浮游动物丰度（131.26 ind/m3）比1959年（78.90 ind/m3）高;浮游动物多样性指数（H'）均在夏秋季高于冬春季节,且年平均多样性指数也有所提高。     

Evaluation of neutral red retention assay,micronucleus test,acetylcholinesterase activity and a signal transduction molecule (cAMP) in tissues of Mytilus galloprovincialis (L.), in pollution monitoring

The neutral red lysosomal retention assay (NRR) of the haemocytes, and the acetylcholinesterase activity (AChE) in the haemolymph, the digestive gland, the gills and the mantle/gonad complex have been evaluated on mussels Mytilus galloprovincialis collected from Thermaikos and Strymonikos gulfs (northern Greece) in June and October 2001. The validity of performing the above core biomarkers is supported, firstly by their ability to respond to different pollution levels and, secondly, by the significant linear correlation among them. The evaluation of the micronuclei frequency (MN) has been performed in gill tissue and haemocytes of the same mussels and, according to the results, it needs more research in order its use as stress indices to be validated. In addition, the first results on cAMP levels in the gills, the mantle/gonad complex and the digestive gland, whose concentrations correlated to both, NRR and AChE introduce this signal transduction molecule as a new, promising biomarker.     

胶州湾浮游动物生态学研究Ⅰ.种类组成

根据2004年1—12月用浅水Ⅰ型和浅水Ⅱ型浮游生物网在胶州湾进行的每月一次垂直拖网采集的浮游动物样品,分析了胶州湾浮游动物的种类组成。调查结果表明,在胶州湾出现的浮游动物共81个种,春、夏季的种类数多于秋、冬季,湾北部的种类数少且年内波动大,湾南部、湾口和湾外种类数多且年内波动小。胶州湾浮游动物优势种为双刺纺锤水蚤(Acartia bifilosa)、小拟哲水蚤(Paracalanus parvus)、太平洋纺锤水蚤(Acartia pacifica)、中华哲水蚤(Calanus sinicus)、拟长腹剑水蚤(Oithona similis)、短角长腹剑水蚤(O.brevicornis)、近缘大眼剑水蚤(Corycaeus affinis)、异体住囊虫(Oikopleura dioica)、强壮箭虫(Sagitta crassa)、八斑芮氏水母(Rathkea octopunctata)和小介穗水母(Podocoryne minima)等。从个体大小上来看,体长<1mm的浮游动物丰度最大。与历史资料的比较显示,2004年胶州湾水母类比90年代同期增加15种,八斑芮氏水母成为冬季优势种。海区比较显示,胶州湾浮游动物的种类组成与渤海相似,与黄海有所不同。     

Characterization of cholinesterases in marbled sole, Limanda yokohamae, and their inhibition in vitro by the fungicide iprobenfos

Cholinesterases (ChEs) have been characterized in marbled sole (Limanda yokohamae) for use as a possible biomarker of pollution exposure. In brain, ChEs existed almost exclusively (>95%) as acetylcholinesterase (AChE) whereas in muscle, about 20-30% of ChE activity was in the form of butyrylcholinesterase (BChE; pseudocholinesterase). Acetylthiocholine and butyrylthiocholine (identified in mammalian studies as diagnostic substrates for AChE and BChE respectively) were hydrolyzed mainly, but not exclusively, by these enzymes. The inhibitors BW284C51 and iso-OMPA (identified in mammalian studies as diagnostic inhibitors of AChE and BChE respectively) were not specific for these enzymes in marbled sole. Brain AChE and muscle AChE and BChE were characterized in terms of their kinetic properties (KM etc.) and optimal conditions (substrate concentration, protein concentration, pH etc.) were established to allow routine assays of ChE activity to proceed under pseudo-first order conditions. The sensitivity of ChEs to a locally significant pesticide, iprobenfos (IBP; kitazin) was established in terms of IC50 concentrations. Brain AChE was relatively insensitive to IBP, but muscle AChE and BChE were sensitive to IBP concentrations in the high nM range. However, ambient IBP concentrations in Korean coastal waters are usually not high enough to cause detectable ChE inhibition in this species.     

Distribution of sterol and fatty alcohol biomarkers in particulate matter from the frontal structure of the Alboran Sea (S.W. Mediterranean Sea)

Sterol and fatty alcohol biomarkers were analyzed in suspended and sinking particles from the water column (20–300 m) of the Almeria–Oran frontal zone to characterize the biogenic sources and biogeochemical processes. Diatom- and haptophyte-related sterols were predominant at all sites and vertical distributions of sterol, and fatty alcohol biomarkers in sinking particles were markedly different from suspended particles. In contrast to the relatively fresh sinking particles with elevated concentrations of phyto- and zooplanktonic sterols, suspended particles were extensively degraded with increasing depth and exhibited a more terrestrial and zooplanktonic signature with depth.Sterol and alcohol biomarkers distributions and δ¹³C values from the jet core and the associated gyre of Atlantic waters showed a decoupling between the sinking particles of 100- and 300-m depth, demonstrating the influence of lateral advection in the frontal zone. In contrast, vertical transport of the particulate organic matter in Mediterranean waters was interpreted from the similar isotopic and molecular composition at both depths. The high abundance of phytosterols and phytol below the euphotic zone at 100 m signified that downwelling of biomass occurred on the downstream side of the gyre. The high concentrations of phytosterols and POC, in combination with the high phytosterols/phytol ratio, indicated the accumulation of detrital plant material in the oligotrophic Mediterranean waters near the frontal zone.A higher contribution of phytol in the sinking particles collected during the night at the surface of the jet and at the upstream side of the gyre provided evidence of diel vertical zooplankton migration and important grazing by herbivorous zooplankton.Carbon isotope ratios of sterols confirmed that the 24-ethylcholest-5-en-3β-ol, commonly associated with terrestrial sources, was a substantial constituent of the phytoplankton in this area. However, the more δ¹³C depleted values obtained for this compound in suspended particles suggested that there was some terrestrial contribution that only becomes evident after degradation of the more labile marine organic matter.     

Congruence between euphausiid community and water region in the northwestern Pacific: particularly in the Oyashio–Kuroshio Mixed Water Region

The relationship between euphausiid community structure and water region was studied during a 2-year seasonal survey in the northwestern (NW) Pacific Ocean. The euphausiid community structure and its associated species were analyzed from 38 micronekton samples collected during eight cruises. The euphausiid community structure and its distribution patterns clearly corresponded to physical oceanographic features in the Oyashio region, Oyashio–Kuroshio Mixed Water Region (OKMWR), and Kuroshio region. In contrast, community structure was unrelated to seasonality. The 19 species out of 40 identified in this area were grouped and named after their habitats. The six cold-water species were grouped into three regional types: two coastal Oyashio species, three Oyashio–OKMWR species, and one Oyashio–Kuroshio species. The four species dominating in the OKMWR were categorized into each specific types: Nematoscelis difficilis as OKMWR–Oyashio species, Euphausia gibboides as OKMWR species, Euphausia similis as OKMWR–Oyashio & OKMWR–Kuroshio species, and Euphausia recurva as OKMWR–Kuroshio species. The seven warm-water species were categorized as Kuroshio–OKMWR species or Kuroshio species. The other two species were categorized as cosmopolitan species. In particular, regarding the result in the OKMWR, our study suggest that (1) the OKMWR has high species diversity, and (2) the dominant species, such as Euphausia pacifica, N. difficilis, E. similis, and E. gibboides, are considered to be key species in the food webs in this region.     

Chemical identification,antioxidant, cholinesterase inhibitory,and cytotoxic properties of fucoidan extracted from Persian Gulf Sargassum angustifolium

Marine macroalgal sulfated fucose-containing polysaccharides, like fucoidan, have drawn significant attention due to their biotechnological potentials, such as anti-cancer, antioxidant, and anti-cholinesterase activities. The fucoidan derived from brown macroalgae Sargassum angustifolium species (FSA) was investigated for its cytotoxic effects and alterations in cell proliferation, and cell cycle-related gene expression in the present study occurred on NB4 cell line. The results showed that FSA would induce p53, p21, pro-apoptotic genes and increase expression of the p15 gene as a cell arrest marker. Also, FSA inhibited the anti-apoptotic effect of the Bcl-2 gene and decreased dnmt-1 gene expression. FSA significantly exhibited potent 2, 2-diphenyl-1-picrylhydrazyl (DPPH) radical scavenging activity (p<0.05) with an IC₅₀ value of 0.157 mg/mL and showed moderate anti-acetylcholinesterase activity with an IC₅₀ value of 1.20 μg/mL. These results indicated the potential of FSA for the development of therapeutic or preventive agents of cancer and Alzheimer’s disease mainly through cytotoxic effect and AChE (acetylcholinesterase) inhibition as well as additional antioxidant capacities.     

春、夏季长江口邻近水域浮游动物优势种的生态特征

依据2000～2003年长江口邻近海域5月和8月8个航次的调查资料,对长江口浮游动物优势种的生态特征进行了研究。根据优势种出现的年份,平均丰度、优势度、聚集强度和对总丰度变化的回归贡献,确定本区优势种的重要性为真刺唇角水蚤（Labidocera euchaeta）〉中华哲水蚤（Calanus sinicus）〉背针胸刺水蚤（Centropage dorsispinatus）。太平洋纺锤水蚤（Acartia pacifica）,火腿许水蚤（Schmackeria poplesia）和虫肢歪水蚤（Tortanus vermiculus）为次要优势种。马蹄娩螺（Limacina trochiformis）是偶然出现的优势种。中华哲水蚤在春季对总丰度贡献最大。真刺唇角水蚤是8个航次唯一的优势种,种群年间变化不显著。太平洋纺锤水蚤,火腿许水蚤和虫肢歪水蚤分布范围相对狭小,火腿许水蚤和虫肢歪水蚤分布在沿岸偏淡水的水体,适合较低的温度。太平洋纺锤水蚤分布在近岸偏成水的水体,适合较高的温度。     

三角褐指藻和亚心形扁藻对太平洋纺锤水蚤繁殖与生化指标的影响

采用实验生态的方法,探讨三角褐指藻(Phaeodactylum tricornutum)、亚心形扁藻(Platymonassubcordiformis)对太平洋纺锤水蚤(Acartia pacifica)繁殖及其生化指标的影响.实验结果表明,三角褐指藻对太平洋纺锤水蚤产卵量和卵的孵化率均具有抑制作用,随着投喂时间的增加,太平洋纺锤水蚤的产卵量由15.02±3.15 ind/d下降到3.25±3.15 ind/d(p<0.05),其卵的孵化率由22.88%±2.49%下降到14.84%±1.20%(p<0.05).而投喂亚心形扁藻的太平洋纺锤水蚤其产卵量和卵的孵化率与对照组无显著差异(p>0.05).投喂三角褐指藻后,太平洋纺锤水蚤的超氧化物歧化酶(SOD)活力相对于投喂亚心形扁藻的增加了20.94±0.04μg/mg,其谷胱甘肽过氧化物酶(GPX)活力增加了15.812±1.240 U/mg.这表明相对于亚心形扁藻,三角褐指藻对太平洋纺锤水蚤的抗氧化性酶具有诱导作用.