Regulation of life history in the brackish cladoceran ...

Regulation of life history in the brackishcladoceran, Daphniopsis australis (Sergeevand Williams, 1985) by temperature andsalinity

HASNUN N. ISMAIL 1,2, JIAN G. QIN 1* AND LAURENT SEURONT 1,3,4

1SCHOOL OF BIOLOGICAL SCIENCES, FLINDERS UNIVERSITY, GPO BOX 2100, ADELAIDE SA 5001, AUSTRALIA, 2

BAHAGIAN HAL EHWAL AKADEMIK, UNIVERSITI

TEKNOLOGI MARA PERLIS, ARAU, PERLIS 02600 MALAYSIA, 3SOUTH AUSTRALIAN AND DEVELOPMENT INSTITUTE, AQUATIC SCIENCES, WEST BEACH SA 5022,

AUSTRALIA AND4

CENTRE NATIONAL DE LA RECHERCHE SCIENTIFIQUE, FRANCE

*CORRESPONDING AUTHOR: [email protected]

Received June 22, 2010; accepted in principle September 27, 2010; accepted for publication October 5, 2010

Corresponding editor: Beatrix E. Beisner

Temperature and salinity variations affect aquatic biodiversity by altering the lifehistory of poikilotherms and regulating their population dynamics. This studyaimed to reveal the response of the brackish cladoceran, Daphniopsis australis

exposed to three temperatures (16, 20 and 258C) cross-classified with three sali-nities (17, 22 and 27). Our results show a significant interactive effect of tempera-ture and salinity on most life history variables. The individual parametersincluding longevity, total egg clutch, egg development time, offspring productionand total moulting were negatively related to the elevations of temperature andsalinity. High salinity dampened the positive relationship between age at firstreproduction and increasing temperatures. Population parameters including age-specific survivorship, age-specific fecundity, net reproductive rate and generationtime were negatively affected by the increasing temperature and salinity. Theintrinsic growth rate showed a unimodal distribution with peak population growthoccurred at 208C and 22 salinity, indicating the optimal condition for populationgrowth. The poor performance of growth, reproduction and developmentoccurred at 258C and 27 salinity. Considering the dual effects of thermal andsaline fluctuation, the life history of D. australis is more greatly impacted by temp-erature rather than salinity, which can contribute to the explanation of seasonaldynamics of brackish water cladocera in salt lakes.

KEYWORDS: temperature; salinity; population growth; reproduction; brackishcladoceran

I N T RO D U C T I O N

Temperature is an important factor triggering thechange of the life history of aquatic poikilothermsbecause its fluctuation can induce a range of physiologi-cal responses in small aquatic animals such as

cladocerans (Smith 1990). Above the optimal range,warm temperature increases an animal’s metabolismand activities, resulting in faster development, growthand reproduction (Vijverberg, 2006). Likewise, whentemperature falls below the optimal range, cool

doi:10.1093/plankt/fbq145, available online at www.plankt.oxfordjournals.org. Advance Access publication November 9, 2010

# The Author 2010. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected]

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temperature decreases metabolism and slows activity.Under sub-optimum thermal conditions, aquaticanimals may develop alternative life strategies to offsetthe difference in physiological and behavioural changes.

In nature, the difference in temperature between tro-pical and temperate regions contributes to geographicdifferences in life strategy of cladoceran species (Sarmaet al., 2005). The life strategies of tropical species exhibitfast maturation leading to rapid growth and prolifer-ation (Murugan, 2006). The body size of tropical clado-cerans is usually smaller than that of the similar speciesin temperate zones because more energy is allocated toreproduction than to somatic growth in early maturedanimals (Taylor and Gabriel, 1992). Warm temperaturealso accelerates egg development and shortens theparthenogenetic reproductive cycle (Goss and Bunting,1983). Consequently, species at high temperatures mayreach senescence earlier than those at low temperatures(Sarma et al., 2005). Thus, at a population level, tropicalpopulations usually have shorter generation timesand higher reproduction than temperate populations(Angilletta et al., 2004).

In a brackish water ecosystem, salinity is anotherfactor influencing the life history of cladocerans alongwith temperature (Waterkeyn et al., 2010). Raised salinityusually results from high evaporation at warm tempera-ture. The direct impact of salinity on cladocerans is lessthan that of temperature (Gordo et al., 1994), butextreme salinity can alter osmoregulation (Aladin andPotts, 1996), feeding activity (Achuthankutty et al., 2000)and hormonal secretion (Bœuf and Payan, 2001). Thesephysiological changes require animals to spend extraamount of energy for body maintenance, and theenergy diverted to osmotic regulation may adverselyaffect growth and reproduction (Hessen and Rukke,2001).

Although most studies on the biology of brackishcladocerans have focused on a single factor of eithertemperature or salinity (Gordo et al., 1994; He et al.,2001), a few studies have examined the differentialresponse of brackish water species to the simultaneousmanipulation of temperature and salinity in relation tovarious life history variables. For instance, the survivalof the brackish copepod, Gladioferens pectinatus, is lessimpacted by the combination of low temperature andlow salinity, but is adversely affected by the combi-nation of high temperature and high salinity (Hall andBurns, 2002a). In contrast, the development of thebrackish copepod, Eurytemora velox, is less sensitive tolow salinity at high temperature, but is more sensitiveto high salinity at lower temperature (Nagaraj, 1988).These studies suggest a species-specific discrepancy ofbrackish water species in responding to temperature

and salinity variations and a lack of pattern in thesynergistic effect of temperature and salinity on clado-ceran life history. Our current knowledge on the lifehistory of cladocerans is mainly derived from fresh-water species. However, there is a need to understandthe life history alternation of cladoceran species inbrackish environments especially with the currenttrend of temperature rise associated with globalwarming and the creation of more saline waters dueto water evaporation.

Daphniopsis australis is a cladoceran species found inephemeral salt lakes in southeastern Australia (Sergeevand Williams, 1985). Lakes in these regions experiencegreat temperature and salinity fluctuations due to dryand hot weather and water evaporation in summer(Timms, 2007). To our knowledge, no comprehensiveinformation is available on its life history in relation toenvironmental changes. The occurrence of D. australis ishighly seasonal, with high and low abundances, respect-ively, observed in spring and winter, and becomesundetectable during summer and autumn (Campbell,1994). This suggests that there is an adaptive life strat-egy of this species in response to the seasonality oftemperature and precipitation in southeastern Australia.In terms of salinity, laboratory tests have showed theeuryhalinity of this species which survives over salinitiesfrom 5 to 33 under 228C (Ismail et al., 2010). However,field observations show the occurrence of this species indifferent ranges of salinity, i.e. 4–30 (Sergeev andWilliams, 1985), 14.4–34.0 (Hebert and Wilson, 2000)and 5–17 (Campbell, 1994) inferring salinity toleranceability. Therefore, D. australis is an appropriate model ofephemeral brackish cladoceran species to explore theimpact of temperature and salinity on the life history ofsaline cladocerans. In this study, we aimed to addressthe lack of understanding of the life history of brackishwater cladocerans by demonstrating the significance oftemperature and salinity for the life history of thisspecies and its adaptive response to environmentalchanges.

M E T H O D

Stock culture

Daphniopsis australis has been continuously cultured inthe Animal House of Flinders University over 100 gen-erations since December 2005. The stock cultures weremaintained in 10 L plastic containers at 20–228C. Thesalinity in the stock culture was 22–23 which wassimilar to the salinity where these animals were col-lected in the field. Photoperiod was controlled at 12 h

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light and 12 h dark at a light intensity of 1800 lux.Animals were fed every 2 days with the green algaTetraselmis suecica at a density of 105–106 cells mL21.The animal density was restricted in each container toa maximum of 1000 individual L21 to avoid populationcrash due to overcrowding.

Experimental design

Prior to the life history experiment, a single parthenoge-netic female was isolated and reared in a jar containing50 mL medium similar to the stock culture condition.Starting from the first generation, newborn neonateswere individually introduced to the containers withexperimental conditions: i.e. three temperatures (16, 20and 258C) cross-classified with three salinities (17, 22and 27). These ranges of temperature and salinity wereselected based on a previous study on thermal and halotolerance of this species (Ismail et al., 2010). Each exper-imental animal was transferred daily to a jar with freshalgal suspension, but only the third-generation animals(age , 24 h) were used for the life history study. Theprocedure of using the third-generation animals from asingle clone was to offset the maternal effect carriedover from the stock culture as suggested by Lynch andEnnis (Lynch and Ennis, 1983).

The life history experiment was designed to observethe response of D. australis to various treatments of temp-erature and salinity. Acclimatized animals from thethird-generation (age , 24 h) were individually inocu-lated in a 50 mL medium for each treatment.Altogether, there were nine treatments with 25 replicateseach. The culture medium was prepared using filteredseawater diluted with demineralized water to reachdesired salinities. Food was given at a density of 105–106 cells mL21 using the green microalga Tetraselmis

suecica. This algal density was suggested as optimum formost cladoceran species (Delbare and Dhert, 1996) andwas above the incipient limiting level for most daphniidor non-daphniid species (Kersting and van der Leeuw,1976). The media were renewed daily to avoid possibleanimal starvation and the animal cohorts were keptunder relevant treatment temperatures. The photo-period was the same as in the stock culture.

Life history study

The life history of each individual was studied to esti-mate how the animals responded to each treatmentcondition. Life history variables of longevity (day), ageat first maturation (day), total egg clutch (no. female21),egg development time (day), total offspring (no.female21) and total moulting (no. female21) were

recorded from the first day of birth until all the exper-imental animals died. The body length (mm day21) atbirth, primipara and death were measured daily usingan eyepiece micrometer attached to a stereomicroscope(30�). Any newborn neonates during the study periodwere enumerated and then removed soon after birth.

Population study

The response of the animal to the environmentalchanges at the population level was conducted througha life table following Pianka (Carey, 1993). Populationparameters included the age-specific survivorship (Ix),age-specific fecundity (mx), net reproductive rate (Ro),generation time (GT) and the intrinsic growth rate (r)estimated following (Krebs, 1985) as:

Ro ¼XN

x¼0

Ix:mx

where x is the age class (0,1,2,. . ., N), Ix is the pro-portion of survivorship per day, and mx is the numberof offspring produced per female per day.

GT ¼PN

x¼0 ðIx:mxÞ:xRo

The intrinsic growth rate (r) was calculated using theEuler–Lotka equation:

XN

x¼0

e�rxðIx:mxÞ ¼ 1

where r is the intrinsic growth rate (day21). As r is apopulation parameter, the estimation of variance wasgenerated using the Jack–Knife method according toMeyer et al. (Meyer et al., 1986).

Statistical analysis

Prior to the analysis, exploratory data analyses wereconducted to assess normality and homogeneity ofvariances using SPSS (ver. 18.0). In order to meet thenormality and homogeneity variance assumptions,some variables were transformed following Tabachnickand Fidell (Tabachnick and Fidell, 2007). Log-transformation was used for the age at first reproduction(AFR) and inverse square-root transformation was usedfor the intrinsic growth rate. Square-root transform-ations were used for longevity, total egg clutch size andtotal offspring production, while power-root transform-ation was used for the net reproductive rate and eggdevelopment time. After data transformation,

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parametric analysis was conducted using two-wayANOVA for each variable. The post hoc test was con-ducted using Tukey HSD for data showing homoscedas-ticity, while the Games–Howell test was used in thecase of heteroscedasticity (Games et al., 1983; Jaccardet al., 1984). Pearson correlation analysis was used tocorrelate life history variables and independent vari-ables. To interpret the strength between the indepen-dent variables of temperature and salinity, we comparedthe size effect using partial h2 test (Leech et al., 2008).During the analyses, the significant levels for two-wayANOVA and Pearson correlation were set up at P ,

0.05 and P , 0.01, respectively.

R E S U LT S

Life history characteristics

LongevityThere was a significant interaction between temperatureand salinity on longevity (two-way ANOVA; P , 0.05;Table I). Further analysis revealed that the impact ofthe interactive effect was dominated by temperature(partial h2¼ 0.593; Table I) rather than salinity (h2¼

0.238) with both temperature (Pearson correlationr¼ 20.662; P , 0.01; n¼ 225; Table II) and salinity(r¼ 20.339; P , 0.01; n¼ 225) being negatively corre-lated with longevity. The longevity was significantlyshortened as temperature increased from 16 to 258C inall salinity conditions (Tukey HSD; P , 0.05; Fig. 1a).However, longevity was significantly shortened with anincrease in salinity from 22 to 27 at 168C (P , 0.05).No significant difference in longevity was found with anincrease in salinity from 17 to 27 at 20 and 258C,respectively (P . 0.05).

Age at first reproduction (AFR)AFR was significantly affected by the interactive effectof temperature and salinity (two-way ANOVA; P ,

0.05; Table I). Salinity (h2¼ 0.601; Table I) had a stron-ger impact on AFR than temperature (h2¼ 0.560).Temperature was negatively correlated with AFR(r¼ 20.478; P , 0.01; n¼ 207, Table II), but salinitywas positively correlated with AFR (r¼ 0.569; P , 0.01;n¼ 207). An increase in salinity from 17 to 27 signifi-cantly prolonged the AFR at 258C (Games–Howell;P , 0.05; Fig. 1b). Meanwhile, at 16 or 208C, AFR wasonly affected when salinity increased from 22 to 27(P , 0.05). In comparison, as temperature increasedfrom 16 to 258C at salinity of 17, animals significantlyshortened the time required for maturation (P , 0.05).

However, at higher salinities (22 or 27), AFR was shor-tened when temperature increased from 16 to 208C(P , 0.05). AFR was not affected when temperatureincreased from 20 to 258C at a salinity of either 22 or27 (P . 0.05).

Egg developmental time (EDT)The impact of temperature on egg developmental time(EDT) was significantly dependent on salinity (two-wayANOVA; P , 0.05; Table I) with a predominant effect

Table I. Two-way ANOVA results of thetemperature (8C) and salinity effects on lifehistory parameters of D. australis

Source df SS MS FF-value PP-valuePartialhh2

LongevityT 2 12428.72 6214.36 152.60 0.001 0.593S 2 3211.39 1605.69 39.43 0.001 0.238T � S 4 2293.89 573.47 14.08 0.001 0.170Error 216 8796.00 40.72

Age at first reproductionT 2 177.52 88.76 125.86 0.001 0.560S 2 210.47 105.24 149.21 0.001 0.601T � S 4 20.82 5.20 7.38 0.001 0.130Error 198 139.64 0.70

Egg developmental timeT 2 54.70 27.35 284.67 0.001 0.766S 2 5.08 2.54 26.42 0.001 0.233T � S 4 3.38 0.84 8.79 0.001 0.168Error 174 16.72 0.10

Total egg clutchT 2 575.66 287.83 123.28 0.001 0.553S 2 363.12 181.56 77.77 0.001 0.381T � S 4 108.11 27.03 11.58 0.001 0.130Error 209 487.95 2.33

Total offspringT 2 590843.67 295421.83 205.71 0.001 0.657S 2 415612.02 207806.01 144.70 0.001 0.574T � S 4 268604.28 67151.07 46.76 0.001 0.465Error 215 308756.24 1436.08

Total moultsT 2 248.347 124.17 46.92 0.001 0.303S 2 242.907 121.45 45.90 0.001 0.298T � S 4 143.147 35.79 13.52 0.001 0.200Error 216 571.600 2.65

Size at birthT 2 0.09 0.05 52.11 0.001 0.326S 2 0.01 0.01 5.63 0.004 0.050T � S 4 0.02 0.01 4.87 0.001 0.083Error 215 0.19 0.01

Size at primiparaT 2 6.86 3.43 592.91 0.001 0.856S 2 0.98 0.49 84.56 0.001 0.459T � S 4 0.49 0.12 21.16 0.001 0.298Error 199 1.15 0.01

Size at deathT 2 32.06 16.03 257.54 0.001 0.706S 2 12.54 6.27 100.72 0.001 0.484T � S 4 6.46 1.61 25.93 0.001 0.325Error 215 13.38 0.06

df, degree of freedom; SS, sum of squares; MS, mean squares.


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of temperature (h2¼ 0.766; Table I) compared with sal-inity (h2¼ 0.233). Temperature was negatively corre-lated with EDT (r¼ 20.855; P , 0.01; n¼ 183;Table II), but salinity was positively correlated withEDT (r¼ 0.280; P , 0.01; n¼ 183). Further analysesshowed that an increase in temperature from 16 to258C significantly reduced the EDT at all salinities(Games–Howell; P , 0.05; Fig. 1c). In contrast, anincrease in salinity from 22 to 27 significantly length-ened EDT at 20 or 258C (P , 0.05). At 168C, EDT didnot differ irrespective of salinity increase (P . 0.05).

Total egg clutchThe number of egg clutches depended on both temp-erature and salinity (two-way ANOVA; P , 0.05;Table I) with stronger temperature (h2¼ 0.553; Table I)contribution than salinity (h2¼ 0.381). Temperature(r¼ 20.467; P , 0.01; n¼ 225; Table II) and salinity(r¼ 20.457; P , 0.01; n¼ 225) were negatively corre-lated with longevity. An increase in temperature from20 to 258C significantly lowered the total egg clutch atall salinities (Games–Howell; P , 0.05; Fig. 1d). Whensalinity increased from 22 to 27, the number of totalegg clutches was lowered at 16 and 208C (P , 0.05).Meanwhile, at 258C, the egg clutch number at salinityof 17 was significantly greater than that at a salinity ofeither 17 or 27 (P , 0.05).

Offspring productionThere was an interactive effect of temperature and sal-inity on offspring production (two-way ANOVA; P ,

0.05; Table I). Temperature (r¼ 20.585; P , 0.01; n¼

225) and salinity (r¼ -0.479; P , 0.01; n¼ 225) werenegatively correlated with longevity (Table II). Anincrease in temperature from 16 to 258C significantlyreduced the offspring production at salinity of 17(Games–Howell; P , 0.05; Fig. 1e). However, at sali-nities of 22 and 27, the total offspring production was

only affected by increasing temperature from 20 to258C (P , 0.05). Similarly, offspring number was signifi-cantly reduced with an increase in salinity from 17 to27 at 16 or 258C (P , 0.05). However, the number ofoffspring at 208C significantly reduced when salinityincreased from 22 to 27 (P , 0.05). Statistically, temp-erature (h2¼ 0.657; Table I) dominated over salinity(h2¼ 0.574) in its effect on offspring production.

Total number of moultsThe total number of moults was significantly affected bythe interactive effect between temperature and salinity(two-way ANOVA; P , 0.05; Table I) with both temp-erature (r¼ 20.371; P , 0.01; n¼ 225; Table II) andsalinity (r¼ -0.426; P , 0.01; n¼ 225) being negativelycorrelated with longevity. However, both temperatureand salinity had a similar impact on moulting (h2¼

0.303 and h2¼ 0.298, respectively, Table I). Whentemperature increased from 20 to 258C, the totalnumber of moults was significantly reduced at salinity ofeither 17 or 22 (Games–Howell; P , 0.05; Fig 1e).However, at salinity of 27, the total number of moultswas not different when temperature increased from 16to 258C (P . 0.05). Similarly, an increase in salinityfrom 17 to 27 significantly reduced the total number ofmoults at 168C, whereas at 208C, the reduction ofnumber of moults only occurred when salinity increasedfrom 22 to 27 (P , 0.05). At 258C, the number ofmoults was unaffected by salinity changes (P . 0.05).

Body lengthTemperature and salinity had a significant interactiveeffect on the body length of animals at all life stages(two-way ANOVA; P , 0.05; Table I) with temperaturebeing dominant over salinity in all cases. In Pearsonanalyses, both temperature and salinity were negativelycorrelated with the body length for all life stages (P ,

0.01; Table II). The size of the interactive effect wassmaller at birth, but subsequently became larger asanimals reached maturation and death (birth: h2¼

0.083; maturation: h2¼ 0.298; death: h2¼ 0.325;Table I).

At birth, an increase in temperature from 16 to 208Csignificantly reduced the body length at salinity of 17(Games–Howell; P , 0.05; Fig. 2a). At a salinity of 22,the body size was significantly reduced with tempera-ture increasing from 16 to 258C (P , 0.05). However, atsalinity of 27, the body length was significantly reducedwith an increase in temperature from 20 to 258C (P ,

0.05), but no significant difference with an increase intemperature from 16 to 208C (P . 0.05). Regardingelevation of salinity, the increase in salinity from 22 to27 reduced the body length at 168C (P , 0.05), but the

Table II. Pearson correlation (r) between lifehistory variables and independent variables

Parameters Temperature Salinity PP-values nn

Longevity 20.66 20.34 ,0.01 225Age at first maturation 20.48 þ0.57 ,0.01 207a

Total egg clutch 20.47 20.46 ,0.01 225Egg development time 20.85 þ0.28 ,0.01 183a

Total offspring 20.58 20.48 ,0.01 225Total moults 20.37 20.43 ,0.01 225Birth 20.54 20.15 ,0.01 224Primipara 20.84 20.30 ,0.01 208a

Death 20.65 20.42 ,0.01 224

aMissing value from replicates.


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body length was unaffected by an increase in salinity(17–27) at either 20 or 258C (P . 0.05).

At primipara, an increase in temperature from 16 to258C significantly reduced the body length at salinitiesof 17 and 22 (Games–Howell; P , 0.05; Fig. 2b). Incontrast, at a salinity of 27, the body length was only

affected with an increase in temperature from 20 to258C (P , 0.05). An increase in salinity from 22 to 27significantly reduced the body length at 16 or 208C(P , 0.05). Meanwhile, at 258C, the body length wasunaffected irrespective of the salinity change (P . 0.05).

Fig. 1. Responses of life history parameters to temperature (8C) and salinity changes: (a) longevity, (b) age at first reproduction (AFR), (c) eggdevelopment time (EDT), (d) total egg clutch, (e) total offspring and (f ) total mouls.


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At death, the body length was significantly reducedwhen temperature increased from 16 to 258C at a sal-inity of 17 (Games–Howell; P , 0.05; Fig. 2c).However, at salinities of 22 and 27, the body length wasonly affected when the temperature increased from 20to 258C (P , 0.05). An increase in salinity from 22 to27 significantly reduced the body length at 16 and208C (P , 0.05). In contrast, at 258C, the body lengthwas only affected by an increase in salinity from 17 to22 (P , 0.05).

Population characteristics

Age-specific survivorship (Ix)The age-specific survivorship pattern consistently showedthat mortality occurred sharply as temperature increasedfrom 16 to 258C. However, the pattern of survival withsalinity increases was inconsistent at different tempera-tures. At 168C, the survivorship declined with an increasein salinity (Fig. 3a). In contrast, the survivorships weresimilar with an increase in salinity at 20 and 258C, butanimals died earlier at 258C than 208C (Fig. 3b and c).

Age-specific fecundity (mx)The curve of age-specific fecundity showed a unimodaldistribution at 168C and 208C at all salinities except atthe salinity of 27 (Fig. 4a and b). At 168C, the peak offecundity (.800 offspring day21) occurred at a salinity of17, while at 208C the fecundity peak ( . 600 offspringday21) was observed at a salinity of 22. The age to reachthe peak of fecundity at 208C was approximately 5 daysearlier than that at 168C. The lifetime fecundity waslonger at 168C than that at 208C. At 258C, animals dis-played peak fecundity at the first reproduction with agesof 8–10 days in all salinities. However, the peak offecundity was sharply reduced when the salinity increasedto 27. The lifetime fecundity at 258C was shorter thanthat at 16 or 208C and reproduction completely stoppedwhen the animal reached 15 days old (Fig. 4c).

Net reproduction rate (Ro)Temperature and salinity had a significant interactiveeffect on the net reproductive rate (two-way ANOVA;P , 0.05; Table III) with both temperature (r¼ 20.520;P , 0.01; n¼ 225; Table IV) and salinity (r¼ 20.412;P , 0.01; n¼ 225) being negatively correlated with Ro.Further analyses showed that an increase in temperaturefrom 16 to 258C significantly reduced Ro at salinities of17 and 27 (Games–Howell; P , 0.05; Fig. 5a).

Fig. 2. Variation in body length (mm day21) in response totemperature (8C) and salinity at different life stages: (a) birth, (b)primipara and (c) death.


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However, at a salinity of 22, Ro was affected by anincrease in temperature from 20 to 258C (P , 0.05).Similarly, Ro was significantly reduced with an increasein salinity from 17 to 27 at 16 and 258C (P , 0.05). At208C, the Ro was significantly reduced with an increase

in salinity from 22 to 27 (P , 0.05). Statistically, theinteractive effect was more dominated by temperature(h2¼ 0.432; Table III) than salinity (h2¼ 0.347).

Fig. 3. Age-specific survivorship (Ix) of D. australis with varying temperatures (a) 168C, (b) 208C and (c) 258C and salinities.


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Generation time (GT)There was a significant interactive effect of temperatureand salinity on GT (two-way ANOVA; P , 0.05;Table III). The GT was affected by temperature (h2¼

0.978; Table III) more than salinity (h2¼ 0.669) with

both temperature (r¼ 20.931; P , 0.01; n¼ 223;Table IV) and salinity (r¼ 20.189; P , 0.01; n¼ 223)being negatively correlated with GT. An increase intemperature from 16 to 258C significantly reduced theGT irrespective of salinity (Games–Howell; P , 0.05;

Fig. 4. Age-specific fecundity (mx; no. of offspring day21) of D. australis with varying temperature (a) 168C, (b) 208C and (c) 258C and salinities.


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Fig. 5b). Meanwhile, an increase in salinity from 17 to27 significantly reduced the GT at temperatures 16 and208C, respectively (P , 0.05). However, the GTincreased significantly with an increase in salinity from22 to 27 at 258C (P , 0.05).

Intrinsic growth rate (r)The intrinsic growth rate was significantly affected bythe interactive effect of temperature and salinity(two-way ANOVA; P , 0.05; Table III) with tempera-ture (r¼ 20.436; P , 0.01; n¼ 225; Table IV) and sal-inity (r¼ -0.499; P , 0.01; n¼ 225) being negativelycorrelated with the intrinsic growth rate (Table IV).Statistically, the effect of temperature (h2¼ 0.689) onthe intrinsic growth rate was greater than that of salinity(h2¼ 0.575). An increase in temperature from 16 to258C produced a unimodal distribution with the intrin-sic growth rate peaking at 208C at all salinities(Games–Howell; P , 0.05; Fig. 5c). When the salinityincreased from 17 to 27, the intrinsic growth rate dif-fered at each temperature. At 168C, an increase in sal-inity significantly reduced the intrinsic growth rate (P ,

0.05) except for an increase in salinity from 17 to 22(P . 0.05). At 208C, a significant unimodal distributionoccurred with a peak of the intrinsic growth rate at asalinity of 22 (P , 0.05). At 258C, the intrinsic growthrate was significantly reduced with an increase in sal-inity from 17 to 27 (P , 0.05).

Table III. Two-way ANOVA results oftemperature (8C) and salinity effects onpopulation parameters of D. australis

Source df SS MS FF-value PP-value Partial hh2

Net reproductive rate (Ro)T 2 73921007.52 36960503.76 82.29 0.001 0.432S 2 51546933.20 25773466.60 57.38 0.001 0.347T � S 4 35579448.66 8894862.17 19.80 0.001 0.268Error 216 97013588.89 449136.99

Generation time (GT)T 2 4900.63 2450.31 4723.83 0.001 0.978S 2 224.79 112.39 216.68 0.001 0.669T � S 4 302.30 75.57 145.70 0.001 0.731Error 214 111.00 0.52

Intrinsic growth rate (r)T 2 2.70 1.35 247.66 0.001 0.689S 2 1.64 0.82 150.75 0.001 0.575T � S 4 0.40 0.10 18.14 0.001 0.242Error 216 1.18 0.01

df, degree of freedom; SS, sum of squares; MS, mean squares.

Table IV. Pearson correlation (r) betweenpopulation variables and independent variables

Parameters Temperature Salinity Sig. value nn

Net reproductive rate 20.52 20.41 P , 0.01 225Generation time 20.93 20.19 P , 0.01 223a

Intrinsic growth rate 20.44 20.50 P , 0.01 225

aMissing value from replicates.

Fig. 5. Analyses of population parameters in response to bothtemperature (8C) and salinity changes: (a) net reproductive rate,(b) generation time and (c) intrinsic growth rate (r).


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D I S C U S S I O N

This study reveals that the impact of temperature onmost life history parameters depends on salinity.Temperature elevation had a greater influence thanincreasing salinity. The synergistic effect of temperatureand salinity could either enhance or suppress thegrowth and reproductive performances of D. australis.However, their antagonistic effect occurred only onsome developmental variables.

Life history parameters

LongevityTemperature is regarded as a limiting factor for the dis-tribution of aquatic animals because it strongly influ-ences the longevity of these organisms. An increase intemperature from 15 to 258C decreased the longevity ofa freshwater rotifer Brachionus havanaensis (Pavon-Mezaet al., 2005) and a marine copepod Tisbe battagliai

(Williams and Jones, 1999) by 2–3-fold. Similarly, sig-nificant reductions in longevity were reported in thefreshwater cladoceran Moina macrocopa and saline clado-ceran M. salina when temperatures increased from 18 to338C (Xi et al., 2005) and from 5 to 308C (Gordo et al.,1994), respectively. In this study, the increases of temp-erature significantly reduced longevity of D. australis.Interestingly, the negative impact of increasing salinityon longevity occurred only at low temperature (168C).These findings suggest that the negative impact of temp-erature on longevity is a generic trend among zooplank-ton regardless of ambient salinities while the impact ofsalinity on longevity depends on temperature.

Maturation and developmentThe development of D. australis was evaluated based onthe performance of AFR and EDT. Temperature is adominant factor in regulating the AFR and EDT inmany zooplankton species (Venkataraman and Job,1980; Goss and Bunting, 1983). In D. australis, however,salinity produced a stronger antagonistic effect thantemperature. The time to reach first reproduction waslonger as salinity increased at low temperature, whereasincreasing temperature accelerated maturation only atlow salinity. This is consistent with the response of thebrackish water copepod, Eurytemora velox (Nagaraj, 1988),but inconsistent with other zooplankton species. UnlikeD. australis and E. velox, the maturation of the hypersa-line species Artemia fransiscana is significantly enhancedby increasing temperature from 8 to 268C and increas-ing salinity from 80 to 140 with a stronger contributionof temperature (Wear et al., 1986). The temperate

cladoceran, Daphnia carinata, matures quicker as temp-erature increases, but is not affected by the increase insalinity from 0.05 to 3.61 (Hall and Burns, 2002b). Thissuggests a species-specific pattern of maturation depend-ing on the range of temperature or salinity. Maturationis mainly controlled by temperature for a variety ofspecies but this generality only applies to D. australis

when salinity is below 22. The impact of salinity gradu-ally became predominant at salinities of 22 or 27.Consequently, our results suggest that the impact oftemperature on D. australis maturation can be overrid-den by salinity higher than 27.

In contrast to AFR, the EDT in D. australis wasmainly influenced by temperature. Egg developmenttime decreased significantly as temperature increasedfrom 16 to 258C at all salinities. This pattern was alsofound in the brackish water copepod, Sinocalanus tenellus

(Kimoto et al., 1986) where the EDT decreased withincreasing temperature while the effect of salinity wasnot significant. The quickest egg development inD. australis was at 258C and 22 salinity, but its develop-ment was impeded as salinity increased to 27. In com-parison, another euryhaline cladoceran species, Moina

mongolica, develops much faster than D. australis at thesame temperature over a salinity range of 2–50(He et al., 2001). Although both species are euryhaline,salinity retards the egg development of D. australis morethan that of M. mongolica, indicating the significance ofsalinity in regulating egg development.

Although the increase in temperature could enhancethe egg development of D. australis, signs of egg degener-ation were observed at 258C during egg development.In a previous study, egg degeneration was also observedin the euryhaline cladoceran, Moina salina, but itoccurred at 15 and 208C (Gordo et al., 1994). The eggsof the freshwater cladoceran, Daphnia pulex, start todegenerate at 208C (Gulbrandsen and Johnsen, 1990),while D. catawba aborts its eggs at 308C (Chen and Folt,2002). The unsuccessful egg development in D. australis,

Moina salina, D. pulex and D. catawba seems to be exclu-sively due to temperature elevation.

Reproductive performanceTemperature had a stronger impact on the number oftotal egg clutch and offspring production than salinity.The highest offspring production occurred at 168C and17 salinity, but the egg clutch number was similar from16 to 208C and salinity from 17 to 22. In contrast, themaximum reproductive output in a saline cladoceran,Moina mongolica, occurs at 208C and salinity between 5and 15 (He et al., 2001), while M. salina seems to beadapted to different temperature and salinity with themaximum reproduction at 308C and 36 salinity (Gordo


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et al., 1994). In other studies, the temperature of 258Cwas considered the upper threshold limiting the fecund-ity of temperate Daphnia spp. (Goss and Bunting, 1983;Moore et al., 1996). In comparison, D. australis producedthe lowest egg production due to egg degeneration, andthe lowest offspring production was observed at 258C atall salinities. Among species in the Daphniidae, Daphnia

magna can tolerate salinity ,12, but its reproductiveperformance is adversely affected when the salinityreaches 8 (Arner and Koivisto, 1993). This study revealsthat even though the reproductive performance ofD. australis is adversely affected at a salinity of 27, thisspecies has a greater salinity tolerance than otherspecies in the same family.

Growth performanceMoulting is not only an indicator of growth, but it isalso associated with reproduction in crustacea(Robertson, 2006). Devreker et al. (Devreker et al., 2004)reported that temperature influenced the number ofmoults more than salinity did when these two factorswere simultaneously compared. In contrast, this studyshowed that an increase in salinity from 22 to 27lowered the number of moults at 16 or 208C. When thetemperature increased to 258C, the moulting ofD. australis was significantly lowered at a salinity of 27.As moulting and reproduction are costly energetically,somatic growth decreases as an animal reaches maturity(Allan and Goulden, 1980). In the present study,somatic growth was suppressed by the manipulation oftemperature and salinity. As the temperature andsalinity increased, the body length of D. australis at birth,primipara and death gradually decreased. The samepattern has been observed in Daphnia magna

(Giebelhausen and Lampert, 2001), Daphniopsis ephemeralis

(Stirling and McQueen, 1986) and Simocephalus vetulus

(Perrin, 1988) where individuals in warm water are oftensmaller than those in cool water. We found that theincrease in salinity did not significantly affect the bodysize at birth, but the body length at primipara started todecrease when the salinity increased to either 20 or258C. The body length at death also decreased withincreasing salinity at all temperatures. The impacts ofsalinity on body size of the brackish water copepod,S. tenellus (Kimoto et al., 1986), and the cladoceran, Moina

micrura (Santangelo et al., 2008), also vary with develop-mental stages. In D. australis, the temperature effect ongrowth was dominant at all life stages, while the salinityimpact occurred only at a later stage.

The occurrence of smaller D. australis at high temp-erature (258C) and high salinity (27) is possibly due toless energy allocation towards somatic growth atextreme conditions. Similarly, Daphnia magna (Mc Kee

and Ebert, 1996) and Daphniopsis ephemeralis (Stirling andMcQueen, 1986) become smaller as temperatureincreases owing to more energy expenditure on repro-duction. In addition, the stress of high temperature andsalinity may also add additional energetic costs formetabolism and osmoregulation to divert energy fromsomatic growth. Animals investing more energy onreproduction are an adaptation to high mortality in astressful environment (Taylor and Gabriel, 1992).Therefore, it is reasonable to believe that under anunfavourable condition, D. australis will allocate moreenergy towards reproduction instead of somatic growth.

Population parameters

The response of animals to environmental changes atthe population level can provide a reliable measurementfor ecological impact because population dynamics inte-grates the complex interactions among life historyvariables (Krebs, 1985). In this study, temperature wasthe main factor regulating population parameters ofD. australis, while salinity was of secondary importance.

The age-specific survivorship curves of D. australis aresimilar to other cladoceran species under stressful con-ditions (Nandini et al., 2004). The survivorship consist-ently declined as temperature increased from 16 to258C. However, the salinity impact occurred only at168C, where the population started to wane in responseto elevated salinity. Salinity did not affect survival whentemperature increased from 20 to 258C, but animals at258C died earlier than at 208C. This indicates thatwhen animals are exposed to unfavourable tempera-tures, survival is determined more by temperature thansalinity. Similarly, temperature dominates the impactover salinity on the survival in 13 Artemia species(Vanhaecke et al., 1984). Although temperature above258C is detrimental for both Artemia and D. australis, thesalinity tolerance in Artemia is 5–120, which is fargreater than in D. australis. On the other hand, the sur-vival of a brackish water copepod, E. velox, increases asa function of temperature increase from 10 to 208Cbefore salinity reaches 25 (Nagaraj, 1988). These find-ings indicate that brackish water crustaceans can toler-ate a wide range of temperature and salinity.Considering survivorship, the optimal temperature andsalinity for D. australis should be below 258C and 27,respectively.

The age-specific fecundity curve contains cumulativeinformation over time on reproductive performanceassociated with a population, and thereby influences thepopulation dynamics of species (Dorazio and Lehman,1983). Pollupuu et al. (Pollupuu et al., 2010) reported thatthe fecundity peak between two populations of a marine


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cladoceran, Pleopis polyphemoides, depended on tempera-ture more than on salinity. Despite constant salinity of4–5, the fecundity of P. polyphemoides in the coastal areapeaked at 20–238C and P. polyphemoides in the open seadisplayed a fecundity peak at 14–228C. Other studies onmarine cladocerans revealed that the highest fecundity ofPenilia avirostris was at 24–288C and 30–35 salinity, whilethe fecundity of Evadne tergestina peaked at 248C and30 salinity (Tang et al., 1995). In the present study, thefecundity curve of D. australis indicates that environmentsbetween 16–208C and 17–22 salinity are desirable forreproductive activities. Furthermore, fecundity was poorat either 258C or 27 salinity, suggesting the importanceof both temperature and salinity in regulating the repro-ductive success of D. australis.

Ro and GT can encompass most physiologicaloutcome observed at the individual level and these vari-ables contribute to the estimate of intrinsic growth rate(r), an index referring to population growth and fitness(Porter et al., 1983). The present study showed that overthe range of environmental changes tested (i.e. tempera-ture: 16–258C and salinity: 17–27), the populationgrowth was more affected by increasing temperaturethan salinity elevation despite a stronger contribution ofsalinity changes to maturation. Temperature was by farthe most important factor regulating the individualresponse and population growth of this brackish watercladoceran. The similar role of temperature in regulat-ing population growth has also been observed in themarine copepod Tisbe holothuriae over the salinity rangeof 26–44 (Miliou and Moraitu-Apostolopoulou, 1991).In fact, under a hypersaline condition with salinitygoing up to 260, the reproductive parameters, gener-ation time and maturity of Artemia franciscana are morestrongly influenced by increasing temperature than sal-inity elevation (Wear et al., 1986). Among saline species,the optimal temperature and salinity for populationgrowth vary greatly. The optimal temperature and sal-inity for T. holothuriae are 198C and 38, respectively(Miliou and Moraitu-Apostolopoulou, 1991), while therange of 20–288C and 120–200 salinity is optimal forA. franciscana (Wear et al., 1986). In the present study,however, the optimal temperature and salinity forD. australis are 208C and 22, respectively.

Our laboratory-derived data from temperature vari-ation support the seasonal pattern of D. australis foundin the field. Campbell (Campbell, 1994) reported thatthe appearance of this species was dominant duringwinter and spring and became less abundant insummer and autumn in saline waters in southernAustralia. This seasonal succession coincides with ourlaboratory observations on the life history of D. australis

where the population growth is fast in the temperature

range of 16–208C, which is the normal temperaturerange during winter and spring in southern Australia(Bureau-of-Meteorology, 2010). Similarly, the poorpopulation growth over 258C is concomitant with thesummer or autumn temperature in this region.Therefore, it is reasonable to expect that the seasonaldynamics of this species will occur in other similar tem-perate regions.

This study identified the requirement for maximumpopulation growth of D. australis which is important forits mass production. The use of a saline cladoceran asan alternative live food for marine aquaculture hasbeen considered to reduce the dependence on the brineshrimp, Artemia sp. due to unreliable supply (VanStappen, 1996). This study shows that the intrinsicgrowth rate of D. australis was 0.56 day21 at 208C and22 salinity, which is the highest among other reportedcladoceran species. For instance, the population ofM. mongolica grows at 0.14 day21 (He et al., 2001) andmany of the Daphnia spp. exhibit intrinsic growth ratesof ,0.44 day21 (Lennon et al., 2001). Other cladocer-ans that display comparable intrinsic growth ratesinclude Moina macrocopa (0.51 day21) and Ceriodaphnia

dubia (0.27 day21) at 228C (Nandini and Sarma, 2002),and M. micrura (0.50 day21) and Diaphanosoma birgei

(0.37 day21) at 258C (Sipauba-Tavares and Bachion,2002). Our study demonstrates that D. australis maintainshigh growth at low temperature, which is an excellentfeature to serve as a live food for cold-water fish larvae.

CO N C LU S I O N

The life history of D. australis varied in response to thechange of temperature and salinity regimes with temp-erature having a greater impact than salinity. At lowtemperature, the life history of D. australis was adaptedthrough increased longevity, greater survival and higherreproductive output. However, low temperature wasassociated with slow egg development, late maturationand long generation times. In contrast, high tempera-ture led to early maturation, fast development and smallbody size. The reproductive cycle was shorted by therapid formation of a new clutch of eggs in parthenoge-netic reproduction. However, the drawback of fastdevelopment at high temperature was a low reproduc-tive output due to short longevity. All life history vari-ables were negatively related to salinity elevation above17. The increasing temperature and salinity producednegative impacts on longevity, survivorship, growth andreproductive variables. The positive effect on matu-ration and development by increasing temperature wascount-balanced by the increased salinity. The most


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suitable conditions for D. australis should be less than258C and 27 salinity. It is finally stressed that in thispreliminary work, the effect of predation was notincluded, but may impact the life-history of D. australis.While this issue is, however, well beyond the scope ofthe present work, further work is needed to understandthe relative impact of predation pressure, but also fooddensity on D. australis life history and populationdynamics.

AC K N OW L E D G E M E N T S

The authors would like to express their appreciation tostatisticians, Dr Greg Kirby and Pawel Skuza.

F U N D I N G

This research was partially supported by a Scholarshipfrom Universiti Teknologi MARA Malaysia andMalaysian Ministry of Higher Education. L.S. is therecipient of an Australian Professorial Fellowship(project number DP0988554).

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