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UntitledJOURNAL OF PLANKTON RESEARCH j VOLUME 32 j NUMBER 10 j PAGES 1405–1411 j 2010 Osmoregulatory and demographicresponses to salinity of the exoticcladoceran Daphnia exilis INGER HEINE-FUSTER 1,2*, CAREN VEGA-RETTER 1,2, PABLO SABAT 2,3 AND RODRIGO RAMOS-JILIBERTO 1,21CENTRO NACIONAL DEL MEDIO AMBIENTE, FUNDACIO´N DE LA UNIVERSIDAD DE CHILE, AV. LARRAI´N 9975, LA REINA, SANTIAGO, CHILE, 2DEPARTAMENTO DE ´ GICAS, FACULTAD DE CIENCIAS, UNIVERSIDAD DE CHILE, CASILLA 653, SANTIAGO, CHILE AND CENTER FOR ADVANCED STUDIES IN ECOLOGY AND BIODIVERSITY, DEPARTAMENTO DE ECOLOGIA, FACULTAD DE CIENCIAS BIOLO ´ GICAS, PONTIFICIA UNIVERSIDAD CATO´LICA DE CHILE, SANTIAGO, CHILE *CORRESPODNING AUTHOR: firstname.lastname@example.org Received December 9, 2009; accepted in principle April 8, 2010; accepted for publication April 15, 2010 Corresponding editor: Mark J. Gibbons Daphnia exilis is a halophylic species that was recently found in Chile, distant from its natural range. In this study, we analyze the osmoregulatory and life-historyresponses to salinity exhibited by Daphnia exilis, as a first step towards understand-ing the ecology of this exotic species whose invasion potential has been related toits ability to tolerate saline environments. A set of laboratory experiments were carried out, in which we exposed organisms to a salinity gradient, and measuredinternal and environmental osmolality, assessed the effect of acclimation time andmeasured life-history traits that were used to perform a demographic retrospectiveanalysis. Our results showed that (i) D. exilis exhibited a hyper-osmoconformerresponse, (ii) acclimation time did not exert effects on the osmoregulatoryresponse, (iii) salinity up to 6 g L21 did not alter the population growth rate, (iv) at8 g L21 population growth rate declined, mainly due to a delayed age at maturityand reduced fertility. Based on this information, we suggest that the responses tosalinity exhibited by the exotic D. exilis confer an advantage over its naturalenemies and may facilitate colonization through exploiting disturbed places aschemical refuges.
KEYWORDS: osmolality; LTRE; zooplankton; invasion; Daphnia exilis capabilities of the exposed organisms (; Salinization of lakes and ponds constitutes an acute form which can affect higher level processes such as of environmental perturbation (, recog- feeding rate, body growth, reproduction and survival nized as a serious environmental problem globally ). Consequently, knowing the . In freshwaters, an increase in salt levels physiological and life-history responses of residents and has been shown to affect zooplankton abundance also of potential invaders to osmotic stress improves our ability to understand the underlying mechanisms of bio- ; . The mechanistic basis of these detrimental effects is primarily related to the phys- Daphnia exilis has been described as a halophilic iological stress resulting from limited osmoregulatory species (), with a range doi:10.1093/plankt/fbq055, available online at www.plankt.oxfordjournals.org. Advance Access publication May 20, 2010 # The Author 2010. Published by Oxford University Press. All rights reserved. For permissions, please email: email@example.com JOURNAL OF PLANKTON RESEARCH j VOLUME 32 j NUMBER 10 j PAGES 1405–1411 j 2010 of salt tolerance between 0.07 and 6.8 g L21 Osmoregulatory response of D. exilis It is usually found in temporary and shallow ponds ), and its natural dis-tributional range covers the southwestern USA and northeastern Mexico. However, this species was later The internal ion concentration of Daphnia, as a function found more than 1000 km outside of its natural range, of environmental salinity, was tested under two different in Onondaga Lake north of New York acclimation levels: 10 generations (i.e. long-term acclim- ). This site had been contaminated and salinized ation allowing for maternal effects) and 6 h (short-term as a result of industrial activity. Due to this, Hairston acclimation). The acclimation levels were crossed with et al. suggested that the invasive five salinity levels: 0, 2, 4, 6 and 8 g of salt per liter of ability of D. exilis could be facilitated by an increase in reconstituted hard water The salt solution was prepared with In the past few years, D. exilis has also been found in commercial sea salt (SERA Premium, Heinsemberg, Chile, inhabiting an artificial lake (Huechu´n) and a set of nearby ponds chemically disturbed to different For the long-term acclimation level, we used 120 degrees by local mining activities. We sampled this females per salinity level born from the second or third population of D. exilis over three consecutive years brood from sisters from a single-line culture acclimated (2007 – 2009). No previous records on the occurrence of during 10 generations to each of the salt levels. The this species exist, considering both studies on fresh and experimental organisms were grown in reconstituted brackish waters systems over the entire country (see ), at a density of 80 ind. L21 during their first 5 days of life, and 40 ind. L21 thereafter. For the short-term In this contribution, we studied the osmoregulatory acclimation level, we used 120 females grown in ASTM and life-history responses to salinity exhibited by the water without added salt. These Daphnia were then trans- exotic cladoceran Daphnia exilis from Chile. The organ- ferred to the five salinity levels 6 h prior to hemolymph isms' tolerance to perturbed (i.e. salinized) environments extraction. During the execution of all procedures, temp- confers them opportunities for exploiting predator-free erature was kept at 20 + 18C, with a photoperiod of habitats, thus increasing population growth and inva- 14:10 L:D, and pH was adjusted to 7.9 + 0.1. The sion potential in those areas. Consequently, this study organisms were fed daily with the green alga Chlorella vul- represents a first step towards understanding the garis, at 106 cells mL21, and enriched with 2.5 mL L21 ecology of an exotic species of a southern hemisphere of nutritional supplement ), com- freshwater habitat whose invasion potential has been posed of algal extract (Phyllum by ANASAC, Lampa, related to its capabilities of tolerating saline environ- Chile). The medium was renewed every 48 h.
ments. In addition, we present new empirical infor-mation Hemolymph extraction and osmolality measurements significance of conformer/regulator strategies of aquatic We extracted hemolymph from a set of adult females, organisms facing stressful environments. The objectives which had just released their first clutch. For each sal- of this work were: (i) to determine the osmoregulatory inity level and acclimation treatment, a measurement of response exhibited by D. exilis over a salinity gradient, internal osmolality was made on a sample of 10 mL (ii) to assess the effects of acclimation time on its osmor- obtained from 120 organisms. Prior to hemolymph egulatory response and (iii) to assess the effects of sal- extraction, each organism was quickly dried externally inity on life-history traits of this exotic cladoceran.
on a piece of filter paper. Hemolymph from eachanimal was removed by piercing the carapace near theheart using a microcapillary, connected to a micro-screwed syringe. Each sample was immediately frozen until measurement. Osmolality of both hemolymph andexternal media was measured using a 5520 Westcor Experimental organisms vapor pressure osmometer.
The experimental organisms used in this study were iso-lated from a clone of D. exilis, recently collected from Huechu´n reservoir (33840000S; 7084706000W) located The osmoregulatory response of Daphnia to salinity (i.e.
45 km north of Santiago, Chile.
conformer, regulator and mixed) was assessed through
I. HEINE-FUSTER ET AL. j RESPONSES OF DAPHNIA EXILIS TO SALINITY the statistical relationship between internal and environ- Matrix for each treatment, using the formulae proposed mental osmolality. For this purpose, we fitted four by Caswell (for birth-flow populations.
alternative models: (a) linear: y ¼ k1x þ k2, (b) hyper- Following Levin et al. (the full Leslie bolic: y ¼ k1 þ(k2 2 k1)/(1 þ(x/k3)), (c) three-parameter Matrix was reduced to a two-stage model with juveniles sigmoid: y ¼ k1/(1þ exp ((k2 2 x)/k3)) and (d) four- and adults as state variables (Fig. This parameteriza- parameter sigmoid: y ¼ k1 þ(k2/1 þ (x/k3)k4), where x is tion allows assessing the effects of time to maturity on the the osmolality of the medium, y is the internal osmolality observed changes in population growth rate. Time to and k are fitting parameters. These models were chosen maturity often exerts major influences on population due to their simplicity, and because they include a broad growth rates of Daphnia ). In range of expected osmolality responses. Strict confor- addition, this two-stage parameterization aggregates the mers are expected to show a linear response with positive many age-specific survival and fertility values into a small slope. Strict regulators are expected to show their set of parameters, allowing a more straightforward internal osmolality independent of environmental osmol- interpretation of effects. Here, juveniles survive with prob- ality. A mixed response should show a curve including ability PJ to reach maturity, spending a time units (days) increasing and horizontal zones, a shape captured by in the process, thus PJ ¼ sa, where s 1 is the character- istic juvenile survival from one time unit to the next and is Hyperosmotic and hyposmotic responses can be deter- directly taken from the corresponding sub-diagonal mined by inspecting the curvature of the response.
elements of the Leslie Matrix. Adults survive with prob- Model selection was carried out by means of the cor- ability s2 during one projection interval (i.e. 1 day).
rected Akaike's information criterion (AICc). The indi- Parameter a is the average number of days from birth to the day on which first reproduction occurred, it AICc2AICcmin, where AICcmin is the minimum among was calculated from the age class at maturity m as a ¼ AICc values calculated for the different models. This m 2 1. We obtained the age class at maturity m from transformation forces the best model to have DAICc ¼ 0, the individual life tables, as the rounded arithmetic with the rest having positive values. Models with mean of the first age classes with non-zero maternity DAICc 2 are considered to have substantial support Finally, adult survivorship s2 and fertility F werecalculated according to Levin et al. ( Demographic response of D. exilis P1 wi, where Si and Fi are survival and fertility of age class i from the Leslie Matrix, and wi are elements of For this experiment, organisms were individually main- the stable stage distribution vector, obtained as the right tained in beakers with 40 mL of filtered lake water eigenvector associated to the dominant eigenvalue.
(GF75 ADVANTEC, Tokyo, Japan). Temperature, pH, The effect of each salt concentration on population photoperiod and food conditions were the same as growth rate was measured relative to the control described above. The experimental organisms were animals (0 g L21) from which we obtained the reference obtained from the fourth brood of three parthenoge- projection matrix A(r). The total effect of each salt netic sisters. To avoid pseudoreplication ( concentration on l is decomposed into contributions ), these newborns were randomly allocated to treat-ments with different nominal salt concentrations: 0, 2,4, 6, 8 and 10 g L21, with six replicates each. Thesenewborns were individually grown in beakers with40 mL of medium, which was renewed daily, untilrearing their third brood. Each 24 h, survival andreproduction were recorder for each animal. The exper-iment was finished after each individual released itsthird brood ( From our daily records of age-specific survival and fertility, we conducted a life table response experiment(LTRE) analysis ) in order to identifywhich demographic rates are responsible for the Fig. 1. Two-stage life cycle graph: (J) juveniles and (A) adults, with observed effect of salinity on the population growth transition rates defined by time to maturity a, probability PJ of rate. First, we constructed a parameterized Leslie surviving to maturity, adult survival probability s2 and fertility F.
JOURNAL OF PLANKTON RESEARCH j VOLUME 32 j NUMBER 10 j PAGES 1405–1411 j 2010 from the four defined vital rates to the observed differ- Demographic response ence between the l value of the treatment l(k) and the The values of the population growth rate (l) did not reference l(r). Each contribution is composed by the show significant differences among treatments, with the observed change in the vital rate parameter, and the exception of the treatment of 8 g L21, where l was the sensitivity of l to changes in the parameter, lowest, although indeed larger than one (Fig. It is important to note that in this experiment Daphnia did lðkÞ lðrÞ þ not released males.
Our LTRE results revealed that in the 8 g L21 treat- ment, fertility F and time to maturity a contributed negatively to population growth, relative to the control.
i are the vital rate parameters (i: 1 – 4, for s1, In the treatment of 2 g L21, the contributions of adult 2, a and F) at treatment k and reference r, and sensi- tivities are evaluated as the mean of both parameter survival and fertility were positive and negative, respect- sets (A/2). We used a bootstrap resampling procedure to ively, and thus they cancelled out. In treatments 4 and calculate 95% confidence intervals for l and the vital 6 g L21, the contributions of the parameters were not rate parameters, with a resampling size of 3000.
different from zero (Fig. ).
In this study, we analyzed some osmoregulatory and life-history responses of the exotic cladoceran Daphniaexilis, faced with a salinity gradient. Our results show Osmoregulatory response that (i) this clone exhibits a hyper-osmoconformer phys- The results of the model selection procedure by AICc iological response, (ii) acclimation time did not exert dis- clearly favored the linear model, independent of the cernible effects on the osmoregulatory response, (iii) acclimation regime of the organisms (Table ).
salinity up to 6 g L21 did not alter the population The values of the fitted parameters of the linear growth rate, (iv) at 8 g L21 population growth rate model, and their corresponding 95% confidence inter- declined, mainly due to a delayed age at maturity and vals are shown in the legend of Fig. There were no reduced fertility.
differences in the constant or slope parameters between The osmoconformer response found in D. exilis has short- and long-acclimation levels. The slope did not evolved in most marine crustaceans and in brackish- depart from unity, and the intercept is significantly water species as a mean to minimize ion and water dif- higher than zero.
fusive movements along with the associated energetic These results indicate that the exotic cladoceran cost (Although osmoregulation allows D. exilis exhibited an osmoregulatory response that exploiting a variety of habitats, the costs of this strategy are relatively high ). Thus osmoconfor- (Fig. On the other hand, acclimation time did not mers should have, in general, lower energetic demands exert any significant effect on the response.
than their osmosrregulator counterparts. The same kind Table I: Results of the model selection procedure for the osmoregulatory response of D. exilis in a salinitygradient Animals were acclimated for 6 h and 10 generations. Four models with number (n) of parameters were evaluated. The best models, according to thecorrected Akaike's Information Criterion (AICc), are shown in bold.
I. HEINE-FUSTER ET AL. j RESPONSES OF DAPHNIA EXILIS TO SALINITY Fig. 2. Osmolality of Daphnia acclimated during 10 generations (black Fig. 4. Contribution of population parameters: juvenile survivorship circles, best fit shown by continuous line) and 6 h (white triangles, best fit shown by dashed line) as a function of environmental osmolality.
1), adult survivorship (s2), time to maturity (a) and fertility (F) to changes in l, for different salt concentrations relative to the control.
Fitted parameters and their 95% confidence intervals for long-time Error bars correspond to 95% confidence intervals. Asterisks show acclimation were 57.92 (32.30– 83.54) and 0.93 (0.71 – 1.15) for intercept and slope, respectively. For short-time acclimation, the valueswere 63.04 (26.03– 100.06) and 1.09 (0.77 – 1.42).
In this study, both short- and long-acclimated organ- isms displayed the same osmoregulatory response to thesalinity gradient. This reflects rapid changes in hemo-lymph osmotic concentration during salinity acclim-ation. Accordingly, Burton and Feldman found that the copepod Tigriopus califor-nicus showed detectable accumulation of free aminoacids within 3 h. We suspect that this rapid osmoticadjustment, together with the relatively wide tolerancerange exhibited by D exilis, may facilitate colonization ofcontrasting environments ) wheneverother ecological constraints are less important.
At the demographic level, our results reveal that the detrimental effects of salinity at 8 g L21 on both fertilityand development of Daphnia translated into a decreased, Fig. 3. Population growth rate l of Daphnia under different salt although still positive, rate of population growth.
concentrations. Error bars represent 95% confidence intervals. A Although we cannot discard a negative effect of salinity significant decrease in l is shown by an asterisk.
on the resource, we assume that this effect is not largesince Daphnia were fed daily. In addition, similar life- of osmoconformer response has been observed by history shifts caused by increased salinity have been Fritsche in D. magna at salinities above found in other cladocerans ; 5 g L21, and in D. pulex living in brackish ponds (In addition, we found that These demographic effects D. exilis exhibited a hyperosmotic response, i.e. the crus- derive from energetic demands, at higher environmental tacean maintains a positive and constant osmolality difference with the environment. In this case, Daphnia between body organs and the texternal medium.
showed a difference of 60 mOsm kg21, which is It is relevant to emphasize that this clone of D. exilis, slightly higher than typical values for hyperosmotic a species recently found in Chile, survived and repro- crustaceans (ca. 10 – 40 mOsm kg21, duced at salinities as high as 8 g L21, which extends the ). Hyperosmotic responses have been reported pre- tolerance limit reported for this species in other lati- viously for D. pulex (), and have tudes (). Freshwater microin- been postulated as a mechanism that facilitates ecdysis vertebrates exhibit, in general, low tolerances to salinity, lethal effects being observed at concentrations below JOURNAL OF PLANKTON RESEARCH j VOLUME 32 j NUMBER 10 j PAGES 1405–1411 j 2010 2 g L21 ; ). Small differences in salinity tolerance could lead to important This work is partially supported by project FONDECYT differences in population growth of competing zoo- 1090132. C.V.-R. acknowledges a CONICYT doctoral plankters (Therefore, our results support that the tolerance to salinity exhibited by theexotic D. exilis confers an advantage over potentialcompetitors.
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