Clonal variation in depth distribution of Daphnia pulex in response to predator kairomones

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Arch. Hydrobiol. 166 2 241–260 Stuttgart, June 2006

Clonal variation in depth distribution of Daphniapulex in response to predator kairomones

Wiebke J. Boeing1, 2, Charles W. Ramcharan3 andHoward P. Riessen4

Louisiana State University, Baton Rouge

With 4 figures and 4 tables

Abstract: In this laboratory study, we explored the variability of 47 Daphnia pulexclones in migration behavior to predator (Chaoborus and fish) kairomones in 1.6 mlong tubes. The preferred mean vertical distribution in control water (no predator kai-romone) is diverse among clones and responses to predator kairomone are highly vari-able. Some migration patterns were opposite to our expectations in clones exhibitingan upward migration in response to fish kairomone. A literature comparison indicatedthat this is not an unusual finding. In general, more clones responded to Chaoborusthan to fish kairomone, stressing the importance of Chaoborus as a predator for Daph-nia in nature. Dilution of Chaoborus kairomone led to a reduced upward migration bymost Daphnia pulex clones tested and adult Daphnia exhibited a strongly reducedresponse to Chaoborus in comparison to juvenile Daphnia. This indicates that Daph-nia may be able to respond to the actual predation threat.

Key words: fish kairomone, invertebrate predators, depth selection, induced response.

Introduction

The phenotype typically reflects only a part of the full range of the informa-tion that is encoded in its genetic material. Different environmental factors cantrigger morphological, life-history, or behavioral changes that were previously

1 Authors’ addresses: Louisiana State University, Department of Biological Scien-ces, 508 Life Sciences Building, Baton Rouge, LA, 70803–1715, USA.2 Current address: Department of Fishery and Wildlife Sciences, New Mexico StateUniversity, P. O. Box 30003, MSC 4901, Las Cruces, NM, 88003, USA. (E-mail:[email protected])3 School of the Coast & Environment, Louisiana State University, Baton Rouge, LA,70803, USA.4 State University of New York College at Buffalo, Department of Biology, 1300Elmwood Ave., Buffalo, NY, 14222, USA.

DOI: 10.1127/0003-9136/2006/0166-0241 0003-9136/06/0166-0241 $ 5.00 2006 E. Schweizerbart’sche Verlagsbuchhandlung, D-70176 Stuttgart

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242 Wiebke J. Boeing et al.

unexpressed in the same individual (Mayr 1963). The relationship betweengenetic potential and the response of the phenotype to a range of environ-mental conditions is known as the ‘reaction norm’ (Woltereck 1909, Kühn1955). Flexibility in the phenotypic expression may help ensure fitness, espe-cially in environments that can rapidly change in critical characteristics suchas quality and quantity of food, and danger from various types of predators.In aquatic environments where a reliable chemical cue (kairomone) of thepresence of predators is typically found, several inducible defenses are com-mon (reviewed by Tollrian & Harvell 1999, Lass & Spaak 2003). Thesedefense mechanisms are considered adaptive, as they are effective in reducingpredation (Havel & Dodson 1984, Lampert 1989). For example, the clado-ceran Daphnia is known to mitigate impacts of predators by altered behav-ioral, morphological, and life-history responses (De Meester et al. 1999,Tollrian & Dodson 1999). Antipredator defenses are often complex and canbe conflicting, as a defense against one predator can make an organism morevulnerable to another predator (Tollrian & Dodson 1999). When visuallyfeeding fish are abundant, Daphnia typically react with a downward migrationduring daytime to hide in darker, colder water-layers (Ringelberg 1991, vanGool & Ringelberg 1995), known as diel vertical migration (DVM). Con-versely, in the presence of invertebrate predators Chaoborus, Daphnia migrateupward during daytime (reverse DVM) (Dodson 1988b) as Chaoborususually stay in deeper water to avoid fish themselves (Luecke 1986, Dawido-wicz et al. 1990, Voss & Mumm 1999). The behavioral (migration) responseto predator kairomone can be triggered within 20 minutes (Dodson 1988 b).Daphnia are cyclic parthenogens and the ability to detect predator kairomonesas well as the type of response and its strength vary among clones (Weider1984, Spitze 1992, De Meester 1993, Reede & Ringelberg 1995, DeMeester 1996).

Since the migration defense is inducible and only employed when needed,it must entail a cost (Harvell 1990, Loose & Dawidowicz 1994, Boeing etal. 2005). Therefore, we might assume that populations are able to assess pred-ation risk and react accordingly. At low predator density the migration of indi-viduals might be weaker or only a smaller percentage of individuals undergomigration. Likewise, life-stages that are less vulnerable to a predator might notmigrate. For example, bigger adult Daphnia are less vulnerable to mouth-gaplimited Chaoborus predators, while juvenile Daphnia are not as easily seen byvisually foraging fish.

The purpose of this study was to investigate how common the behavioraldefense to fish and invertebrate predator Chaoborus is and how diverse reac-tion norms in migration behavior are. Furthermore, we studied the importanceof kairomone concentration and body size for different clonal lineages ofDaphnia pulex when exposed to Chaoborus kairomone. We hypothesize that

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Depth distribution of Daphnia clones 243

the strength of response to predator chemical is dependent on chemical con-centration and that more susceptible life stages exhibit a stronger behavioralresponse than less susceptible individuals.

Material and methods

Culture conditions and clonal distinctions

Fifty-nine Daphnia pulex females were collected in the spring of 1997 and late springto summer of 1999 from 18 different water bodies (lakes to temporary ponds) locatedin upper New York State (USA) and south-central Ontario (Canada). Animals werecollected with vertical hauls of a 130-µm zooplankton net and each female (hapha-zardly chosen from the live collection) was maintained in the laboratory as a separatelineage (Table 1).

Daphnia were cultured in 1-L glass jars under controlled temperature conditions(20 ± 1˚C) and fed Chlamydomonas above the limiting level (Lampert 1987). Culturewater (aged tap water with added algae) was changed every 2–3 weeks before any fe-male could release ephippial eggs, and five to ten individuals were retained to continuethe lineage.

To confirm distinctness among the Daphnia lineages, we used a combination ofa genetic approach and examination of behavioral differences. Some of the Daphnialineages did not survive in the laboratory after we had conducted some of the ex-periments, and were not available for genetic analysis. For the genetic evidence weused Polymerase Chain Reactions (PCR) to amplify microsatellites because they

Table 1. Origin of Daphnia pulex clones.

Location collected Name of water body Habitat Description Clone(s)

NY State Archery Course Pond small permanent pond ACP 1, 3NY State Alran Drive small temporary pond ALR 3, 5Ontario (Algonquin) Brewer Lake brownwater lake BRE 3, 4NY State Bryant Woods small temporary pond BRY 3, 4Ontario (Algonquin) Clarke Lake brownwater lake CLA 2, 5Ontario (Algonquin) Costello Lake brownwater lake COS 1, 2, 4NY State Cuba Lake small man-made lake CUB 1, 3NY State East Summerset small temporary pond ESUM 1, 2, 3NY State Friendship Luthern Church large temporary pond FLC 1, 2, 3Ontario (Algonquin) Found Lake clear, deep lake FND 2, 3, 4NY State Honeoye Lake mesotrophic, deep lake HON 3NY State Hopkins drainage ditch overflow HOP 1, 2, 3, 4, 5Germany Konstanz eutrophic lake KNNY State Margaret Louise Park small permanent pond MLP 3, 5NY State Miller Pond small permanent pond MLR 1, 4Wisconsin α-Gardner Pond small permanent pond SBLOntario (Algonquin) Scott Lake clear, deep lake SCO 2, 3, 5Ontario Walker Lake clear, deep lake WAL 2, 3, 5, 6, 7, 8, 10, 11

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Table 2. Genotypes and mean vertical distribution (MVD) of Daphnia pulex clones incontrols and in response to predator kairomones, and experiments used in (Dilut. =various concentrations of Chaoborus spp. kairomone, Ad-juv. = comparison betweenadult and juvenile Daphnia in response to Chaoborus kairomone). Numbers indicatemean values ± 1 S. E.; positive numbers indicate upward migration, negative numbersdownward migration; numbers or X marked in bold indicate significant response(p<0.05).

Clone MVD AdultDaphnia(Control)(cm)

∆ MVD ofAdultDaphnia(FishKairomone)(cm)

MVDJuvenileDaphnia(Control)(cm)

∆ MVD ofJuvenileDaphnia(Chaob.Kairomone(cm)

Dilut. Ad-juv.

GenotypesPrimer1

1 2 3

ACP 1 25.14± 2.96 2.26 ±0.32 24.62± 2.21 2.87 ±2.70 X 1 1ACP 3 45.55± 3.62 1.70 ±1.55 1

ALR 3 35.91± 2.51 –14.82 ±1.29 20.23± 0.87 16.32 ±1.21 X XALR 5 47.17± 10.16 22.20 ±6.67

BRE 3 56.41± 14.55 11.79 ±2.37BRE 4 47.89± 18.36 –6.93 ±5.16 2

BRY 3 29.06± 4.80 1.63 ±0.67 67.69± 2.64 51.01 ±3.70 X X 2 2 3BRY 4 8.88± 0.50 –2.33 ±0.48 43.02± 1.36 32.19 ±3.06

CLA 2 51.66± 16.52 21.89 ±7.69 3CLA 5 57.31± 15.11 6.61 ±3.32 2

COS 1 30.50± 11.40 –8.86 ±3.09 3COS 2 55.64± 9.18 15.53 ±2.38COS 4 18.97± 9.66 8.14 ±3.90

CUB 1 49.20± 15.18 –12.25 ±9.03CUB 3 49.26± 4.14 36.51 ±1.83

ESUM 1 6.34± 0.46 –1.34 ±1.14 33.05± 2.75 26.62 ±2.17ESUM 2 21.18± 3.54 1.92 ±2.85 41.85± 17.26 15.11 ±5.93 3 1ESUM 3 3.57± 0.16 –2.36 ±0.54 15.82± 1.49 7.25 ±1.84 2 1

FLC 1 30.41± 3.05 23.65 ±3.80FLC 2 63.67± 4.00 37.07 ±2.10 20.45± 1.77 13.64 ±2.83 X XFLC 3 29.16± 3.77 2.78 ±1.34 28.29± 2.21 12.67 ±1.58

FND 2 29.11± 7.01 11.89 ±2.76FND 3 38.96± 18.66 0.80 ±9.81 3FND 4 27.51± 13.60 –2.43 ±4.28 3 1 2

HON 3 103.66± 6.41 –21.38 ±5.83 31.42± 5.13 –13.72 ±4.93 X 3

HOP 1 16.77± 6.96 –8.28 ±1.55 48.53 ±3.64 24.71 ±3.71 X X 1HOP 2 34.19± 3.34 –8.88 ±1.73 22.95± 2.49 8.65 ±2.14 1HOP 3 13.25± 1.50 0.58 ±0.84 25.15± 1.13 5.37 ±1.38 1HOP 4 37.33± 3.99 0.18 ±2.54 26.74± 2.63 7.37 ±4.89 1 4HOP 5 11.07± 1.98 –6.23 ±1.73 28.23± 2.35 13.46 ±1.86 5

KN 36.47± 4.82 –6.26 ±2.04 75.82± 4.50 50.56 ±3.27

MLP 3 37.58± 3.26 32.17 ±4.38MLP 5 20.65± 5.01 4.20 ±2.72 40.16± 4.10 –2.27 ±2.24 X 1 5

MLR 1 83.19± 2.35 –4.61 ±5.85 28.96± 1.12 7.49 ±3.61MLR 4 32.95± 0.70 7.28 ±0.80 41.30± 1.60 17.89 ±4.03 31 6

SBL2 29.57±9.99 14.67 ±7.26 41.68± 1.61 16.19 ±3.21 1 3 7

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Table 2. Continued.

Clone MVD AdultDaphnia(Control)(cm)

∆ MVD ofAdultDaphnia(FishKairomone)(cm)

MVDJuvenileDaphnia(Control)(cm)

∆ MVD ofJuvenileDaphnia(Chaob.Kairomone(cm)

Dilut. Ad-juv.

GenotypesPrimer1

1 2 3

SCO 2 61.71± 15.16 22.31 ±3.79SCO 3 11.38± 3.45 –16.42 ±5.56 1SCO 5 29.33± 12.85 6.81 ±4.06 2

WAL2 66.30± 14.09 –2.26 ±6.47 36.89± 3.46 14.71 ±2.65WAL3 24.62± 9.58 –5.06 ±2.96 78.81± 14.76 40.49 ±14.20WAL5 82.71± 9.83 –1.24 ±1.73 81.03± 12.85 54.31 ±11.96 X XWAL6 47.93± 13.40 23.23 ±4.83 53.65± 11.49 32.62 ±7.91 1WAL7 63.16± 13.99 4.73 ±3.02 52.80± 7.64 33.93 ±2.21 2 1WAL9 29.44± 8.94 8.82 ±1.31 40.07± 10.39 27.42 ±9.48 X XWAL10 17.66± 2.53 8.06 ±1.14WAL11 32.68± 13.01 22.50 ±9.64 41.60± 6.39 9.00 ±2.061 blanks indicate repeatedly unsuccessful amplification or extinction of clone in laboratory before analysis.2 clone from Dodson (1988b).

provide a high resolution (Sunnucks 2000). We then analyzed size difference of themicrosatellites among clones using acrylamide gels (difference detection limit of twobase-pairs) (Rousseau et al. 1994), following the approach described by Noor et al.(2001). The DNA of the different D. pulex lineages was isolated with a Puregene DNAisolation kit 400 (Gentra Systems, Minnesota). With ten primers (five forward and fivereverse) for microsatellite sequences of D. pulex provided by ‘GenBank’(http://www.ncbi.nlm.nih.gov) (Colbourne unpublished), we were unable to amplifytwo microsatellites (Dpu46 and Dpu45) and, therefore, worked with just three microsa-tellites. One primer for each sequence was obtained with an M13 tail at the 5’ end. Thefirst (Dpu122), second (Dpu40), and third (Dpu7) pair of primers, amplified segmentsof 132, 119, and 114 base pairs, respectively. The PCRs were conducted in a 10-µlreaction volume with 0.5 picomoles of each primer, 0.4 fluorescent dye labeled M13,200 µM dNTP’s, 1µl 10 X buffer (100 mM Tris pH 8.3, 500 mM KCl, 15 mM MgCl2), 1U Taq polymerase, and 1 µl from the DNA prep of a single D. pulex lineage with atouchdown cycle (Palumbi 1996). Then, we added 3 µl of LiCor (Lincoln, NE) stopp-ing buffer to the PCR products and 1µl of each reaction was loaded onto an acrylamidegel (National Diagnostics Sequagel, Atlanta, GA) on a LiCor 4200 DNA sequencerfor visualization.

To be conservative in terms of finding differences in genetic lines, we only distin-guished between three genotypes for the Dpu122 and the Dpu40 microsatellites andseven genotypes for the Dpu7 microsatellite (Table 2). Although many of the lineagesthat were assayed could be identified as different clones by the genetic approach, wealso designated D. pulex lineages that showed significant differences in behavioral,morphological, or life-history traits as distinct clones. Also, individuals derived fromdifferent water bodies were assumed to be genetically distinct, as they had to hatchfrom different resting eggs (Lynch 1983). We were unable to assure a unique genetic

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make-up or different phenotypic traits for a total of twelve Daphnia lineages, which donot appear in the analyses presented here.

Migration in response to fish kairomone

In these experiments we assayed adults of 41 Daphnia pulex clones for their migrationresponse to fish kairomone in transparent acrylic columns (2 m long, 6.9 cm inner di-ameter) that were marked in 10 cm intervals. Migration response was estimated by cal-culating mean vertical distribution (MVD) as followed:

MVD = Σ(Di * i) / ΣDi

‘Di’ is the number of Daphnia pulex in each depth interval and ‘i’ is the median ofthe corresponding depth interval. The columns were stationed in a room where thefloor and walls were blackened to minimize light reflection and lighting came fromfour 40 Watt halogen lamps installed in the ceiling.

The water in the control columns consisted of aged tap water conditioned withaquarium fish food pellets. To create fish-kairomone, 28 L of aged tap water was con-ditioned with six golden shiner (Notemigonus crysoleucas) individuals (total weight of20 g) that were fed to saturation starting three hours before the start of the experimentwith fish food pellets. Loose et al. (1993) and von Elert & Loose (1996) showedthat the chemical signal is released by fish into the water within one hour and neitherfish species nor nutritional state of the fish influence kairomone production.

We had conducted preliminary experiments which indicated that type of food (ei-ther food pellets or Daphnia), amount and duration of feeding, as well as fish type(golden shiner, Notemigonus crysoleucas or pumpkinseed, Lepomis gibbosus) had noeffect on the strength of reaction. Furthermore, comparison between aged tap waterand aged tap water conditioned with food pellets did not result in any differences inmean vertical position of the D. pulex (Boeing, unpubl. data).

Each trial began by filling one tube with control water up to 160 cm (control tube)and the other with water including the fish kairomone (treatment tube). Fifty mL ofChlamydomonas algae (from a continuous culture) were mixed into each tube as food.The algae concentration had been determined photometrically at 470 nm and was di-luted so that about 150 µg L–1 chlorophyll-a was added to the tubes. We run the experi-ments three times to determine Chlorophyll-a values at different depths (30, 70, 110,and 150 cm) and times (30, 60, 90, and 120 minutes after addition) in the tubes. Wewithdrew 200 mL samples, kept them in the dark and filtered them through GF/C fil-ters (1.2 µm pore size) within one hour. The filters were kept in a freezer for two daysand then extracted overnight in 100 % acetone. Chlorophyll-a concentrations weremeasured with a fluorometer (Turner Designs Inc. Sunnyvale, CA; model 10–005R)following standard methods (Greenberg et al. 1981). The chlorophyll-a concentrationstayed above 50 µg/L at all depths throughout the experiments.

For the actual experiments, fifty adult (> 1.3 mm) Daphnia pulex from one clonewere poured through a funnel and hose into the experimental tubes at 1m depth afterthe algae addition. This procedure prevented the animals from either getting caught inthe surface layer or capturing air under their carapace, and also assured that they all

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started out near the middle of the columns. All D. pulex in each 10-cm interval werethen counted every 30 minutes for two hours. In each experimental session, we testedthree haphazardly-chosen D. pulex clones for their MVD in response to fish kairomoneby comparing the average depth of the control versus the treatment group (∆ MVD =control MVD – treatment MVD). Tests for each of the 41 clones were replicated atleast three times. Replicates were taken on different days over the course of sixmonths.

Migration in response to Chaoborus spp. kairomone

Here, we evaluated the migration response of juvenile Daphnia pulex(< 1.1 mm) from 33 clones to Chaoborus kairomone, following the same ex-perimental procedure as described above for fish kairomone and adult Daph-nia.

To obtain a large amount of Chaoborus spp. kairomone with identical ac-tivity, we extracted the chemical from the larvae and kept it frozen at –20 ˚C(Tollrian 1995). The kairomone was extracted following Hebert & Grewe(1985) by crudely cutting up 4th instar Chaoborus trivitattus and C. flavicans.The animals were then boiled for three minutes in water, and all particles wereremoved from the mixture by stepwise filtration down to 0.1µm with celluloseacetate filters. We conducted the experiments within six months of kairomoneextraction, with the filtrate kept frozen at –20 ˚C until use. There was no evi-dence for degradation of the Chaoborus kairomone over time as measured byresponse strength of the Daphnia clones (repeated measure ANOVA,p > 0.05).

The control water was again aged tap water, while the treatment water wasa mixture of freshly thawed kairomone and aged tap water. The added concen-tration was equal to kairomone extracted from ten Chaoborus/L.

Dilution of Chaoborus kairomone and response by adults

The purpose of these experiments was to compare juvenile migration behaviorto different Chaoborus kairomone concentrations as well as to compare migra-tion response between adult and juvenile Daphnia.

Seven D. pulex clones with differing strengths of juvenile responses (twohad reacted strongly to Chaoborus spp. kairomone with more than a 40 cm dif-ference in MVD, four intermediate with a 10–30 cm difference, and one non-reactive clone) were then selected in order to examine the effect of varyinglevels of the kairomone on strength of response. We diluted the Chaoborusspp. kairomone to concentrations that equaled 5, 2.5, 1.25, and 0.625 crushedup Chaoborus/L. For each clone we continued the dilution series until no be-havioral response could be detected. For the clone that did not react, we in-creased the kairomone concentration equivalent to material extracted from 20

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Chaoborus spp./L. Additionally, eight D. pulex clones (two with a strong, fourwith intermediate, and two with no juvenile response to Chaoborus spp. kairo-mone) were examined for differences in MVD between adults (> 1.3 mm) andjuveniles (<1.1mm) (Table 2).

Statistical analysis

Statistical analyses were conducted with SAS software (SAS 2002). We ap-plied repeated measures ANOVA with time as the repeated variable and clonesand treatment as fixed effects to analyze depth selection behavior. P-valueswere Tukey-adjusted. We examined differences in frequency of responses toChaoborus and fish with a χ2 analysis.

Results

Different clones behaved differently in the absence of kairomone, producing astatistically significant clone effect in mean vertical distribution (MVD) foradult and juvenile Daphnia in control water (F = 10.08, df = 40 for adult and F

Table 3. ANOVA results.

Source df MS F p

MVD of adult Daphnia in controlClone 40 6994.07 10.08 <0.0001Error 107 693.94

∆ MVD in response to fish kairomoneClone 40 2601.32 5.47 <0.0001Error 107 475.70

MVD of juvenile Daphnia in controlClone 32 2977.89 4.28 <0.0001Error 75 696.13

∆ MVD in response to Chaoborus kairomoneClone 32 1682.85 3.57 <0.0001Error 75 471.10

Dilution of Chaoborus kairomoneClone 6 3847.96 7.62 <0.0001Dilution 5 4068.22 8.05 <0.0001C* D 7 2671.25 5.29 <0.0001Error 36 505.08

Adult-juvenile comparisonClone 7 5397.29 12.55 <0.0001Age 1 10906.31 25.36 <0.0001C* T 7 1831.26 4.26 <0.0001Error 31 430.08

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Fig.1. Boxplots of Daphnia mean vertical distribution (MVD) of some selected clonesin response to fish kairomone after 60 minutes. The control for each clone is on the left(white) and the treatment on the right (gray). MVD is indicated by squares, while themedian is the line dividing the box. The upper half of the box represents the 2nd quar-tile, the lower half the 3rd quartile of all data. The deviation bar includes 90 % of thepopulation, while × presents 99 % and – shows maximum and minimum value.

= 4.28, df = 32 for juvenile Daphnia) (Tables 2 and 3). There was also a sig-nificant effect of clones in response to both predator kairomones (p < 0.0001)(F = 5.47, df = 40 for fish and F = 3.57, df = 32 for Chaoborus kairomone) (Ta-ble 3). For both predator kairomones, there was no significant change instrength of reaction over the two hour time period (p > 0.05) as tested by re-peated measures ANOVA.

Five of the 41 clones (12 %) responded significantly to fish kairomone (Ta-ble 2), however only one clone exhibited the expected downward migration(–21cm, HON 3) while four clones migrated upwards (between 22 and 37cm)(Table 2). We selected nine clones to illustrate the variability in MVD of adultDaphnia in the controls and fish kairomone water (Fig.1). The distributions ofthose clones that exhibited a significant response to fish kairomone were allmore variable in the controls than in the treatment tubes (Table 2, Fig.1).

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Fig. 2. Boxplots of Daphnia mean vertical distribution (MVD) of some selected clonesin response to Chaoborus kairomone after 60 minutes. The control for each clone is onthe left (white) and the treatment on the right (gray). MVD is indicated by squares,while the median is the line dividing the box. The upper half of the box represents the2nd quartile, the lower half the 3rd quartile of all data. The deviation bar includes 90 %of the population, while × presents 99 % and – shows maximum and minimum value.

When exposed to Chaoborus kairomone, 19 of 33 clones (58 %) showedsignificant upward movement (between 14 and 54 cm) (Table 2). Again, fornine clones we present the reaction norms of MVD for juvenile Daphnia in thecontrols and Chaoborus conditioned water (Fig. 2). The MVD of the controlwas often more variable than the treatment group. The treatment group mostlystayed relatively close to the surface. In some cases the MVD of the controlwas already close to the surface (ALR 3, FLC 2) (Table 2, Fig. 3).

The χ2 analysis revealed that significantly more Daphnia pulex clones re-sponded to Chaoborus than to fish (p ≤0.001).

We had assayed 22 clones that were collected from nine permanent andtemporary ponds (pond clones) and 25 clones from nine lakes (lake clones)(Table 1). Of the pond clones, 21 clones were tested for their response toChaoborus kairomone, and 19 for their response to fish kairomone. Fifty-two

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Fig. 3. Boxplots of Daphnia mean vertical distribution (MVD) of one selected clone(WAL 5) in response to various concentrations of Chaoborus kairomone after 60minutes. MVD indicated by squares, while the median is the line dividing the box. Theupper half of the box represents the 2nd quartile, the lower half the 3rd quartile of alldata. The deviation bar includes 90 % of the population, while × presents 99 % and –shows maximum and minimum value.

percent of the pond clones had a significant upward migration in response toChaoborus kairomone, and 5 % a significant upward migration in the presenceof fish kairomone. Of the 12 lake clones that were tested with Chaoborus kai-romone, 67% exhibited a significant upward migration, while only one of the22 clones (4.5 %) significantly migrated down in presence of fish kairomone,and three clones (14 %) significantly migrated up (Table 2).

Diluting the Chaoborus kairomone concentration led to a decrease instrength of response for five out of the seven clones (71 %) that had signifi-cantly moved upward in response to the full strength kairomone (F = 8.05, df= 5) (Table 2 and 3, Fig. 3).

Adult Daphnia showed either no, or reduced, upward migration when ex-posed to Chaoborus kairomone compared to juvenile Daphnia (F = 25.36, df= 1). There was a significant difference in migration pattern between adultsand juvenile Daphnia in four out of eight tested clones (50 %) (Table 2 and 3,Fig.4).

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Fig. 4. Boxplots of Daphnia mean vertical distribution (MVD) of one selected clones(FLC 2) comparing MVD of adults vs. juveniles in response to Chaoborus kairomoneafter 60 minutes. MVD is indicated by squares, while the median is the line dividingthe box. The upper half of the box represents the 2nd quartile, the lower half the 3rd

quartile of all data. The deviation bar includes 90 % of the population, while × pre-sents 99 % and – shows maximum and minimum value.

Discussion

The mean vertical distribution (MVD) varied among clones even in the con-trols that had no predator chemicals. This indicates that different clones havebeen selected for different preferred vertical distributions that may be ex-plained by preferences in food quality/quantity, UV tolerance, predator avoi-dance, temperature and oxygen requirement, etc. Other studies have indeedshown that Daphnia pulicaria show clonal habitat specialization in stratifiedlakes, with smaller clones occurring at shallower depths (Tessier & Leibold1997). Furthermore, a field study demonstrated that body size, habitat use andtype of predator all influence MVD of Daphnia during day and night (Gonza-lez & Tessier 1997). Our study included Daphnia from both lakes and ponds.Those Daphnia are genetically very similar and belong to the same speciescomplex (Lehman et al. 1995), however, many ecologists recognize the lake

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form as Daphnia pulicaria (Pfrender et al. 2000). Although the microsatelli-tes were developed for D. pulex, we can assume that at least some of the lakeclones were actually D. pulicaria. However, Daphnia from lakes did not showdistinct differences from pond Daphnia and the two species are phenotypicallyas well as in their behavioral response to predators very similar. Thus, we donot think that combining the two species affects our conclusion.

Despite the fact that MVD was different in the controls, the majority ofclones that were tested for their response to both predators (27 clones) re-sponded to at least one of the two predators (67%). This may show that pred-ator losses have been a significant factor in shaping Daphnia behavior, inde-pendent of other abiotic factors that are ecologically important to the differentclones. Even though predators are an important factor, the defense againstthem should have a cost (Harvell 1990, Boeing et al. 2005). Two main linesof evidence support the cost hypothesis. First, the response is inducible. Sec-ond, animals in little danger (i. e., adults in presence of Chaoborus kairomone)do not respond. Some studies have found that response was all-or-nothing (DeMeester & Pijanowska 1996), but other work, including this current studysays that most clones do have a graded antipredator response to Chaoborus(Parejko & Dodson 1991, Ramcharan et al. 1992, Tollrian 1993, Bran-celj et al. 1996) and fish (Loose 1993, Loose & Dawidowicz 1994, vonElert & Pohnert 2000). A graded response should be expected if prey isable to respond to the actual predation risk. At low predator density, the costfor the defense might not offset the predation risk and therefore, the responsewould be gradual. We did not observe a bimodal distribution which indicatesthat individuals reacted less strongly to the cue rather than just a lower per-centage of individuals responding. Similarly, we found that adult Daphnia didnot respond to Chaoborus kairomone, even when the juveniles of the sameclone did. This is again an indication that Daphnia are able to react accordingto vulnerability toward a certain predator.

More clones responded to Chaoborus than fish. This finding might not rep-resent a general result for an entire season, but it might indicate that in someregions, Chaoborus can seasonally be the dominating predator. Furthermore,many fishless ponds, where invertebrate predation dominates the zooplanktoncommunity, have often been neglected in the past although they make up alarge proportion of water bodies. Daphnia clones were collected from twofairly narrow regions (NY state and south-central Ontario) over a few weeksin spring 1997 and late spring/summer 1999 (only south-central Ontario). Inmany cases, high densities of large Chaoborus (C. americanus and C. trivitta-tus) were observed during collection of the Daphnia clones (Riessen andBoeing, pers. observ.). Other studies confirm that Chaborous is indeed an im-portant predator for Daphnia (Dodson 1972, Benndorf et al. 2000, Ramcha-ran et al. 2001) and were able to put some selective pressure on Daphniathroughout evolution.

eschweizerbartxxx

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When a Daphnia clone stays up higher in the water column in the absenceof Chaoborus kairomones, it reduces the distance a clone can react to the sur-face in the presence of kairomone. In some cases, most of the individuals inthe Chaoborus kairomone treatment were actually found within the top 5 cmof the water column. Other laboratory studies also found the mean vertical dis-tribution during daylight to be close to the surface (Dodson 1988 b, Ramcha-ran et al. 1992). This shows the limitation in applying laboratory results to thefield. A scenario with Daphnia staying that close to the surface would mostlikely not be found in a real lake situation, and field experiments have demon-strated indeed a much deeper vertical distribution even in the presence ofChaoborus (Nesbitt et al. 1996, Boeing et al. 2005). Two characteristics innature prevent Daphnia from staying too close to the surface. First, UV light isknown as an important factor to drive zooplankton deeper down in the watercolumn (Leech & Williamson 2001, Rhode et al. 2001). In shallow pondsthis might actually lead to a narrow habitat in which Daphnia are safe fromboth damaging radiation and invertebrate predation (Boeing et al. 2004). Sec-ondly, Daphnia might be more likely to be trapped at the surface because ofwind and wave action and, therefore, avoid the top of the water column.

The clones that had a significant response, showed the expected upwardmigration to Chaoborus. For fish, they were mostly an unexpected upward mi-gration. With this unexpected response, there are two possibilities: A. We arewrong and this is a fluky result due to e. g. short observation time after Daph-nia were exposed to fish kairomone (De Meester & Cousyn 1997) that is notfound elsewhere. However, a literature survey indicated that upward migrationdue to fish kairomone has been found in 9 % of all Daphnia clones examinedin laboratory experiments (Table 4). B. It is an adaptive response but we justdo not yet know the benefit. This is certainly possible. Perhaps in nature, theseupward migrations might be manifest as a movement toward the upper, openwaters of a lake where – in northern temperate lakes – there are often fewplanktivorous fishes, which hide in the littoral zone and hypolimnion to escapepiscivorous fish predation (Alfonso et al. 2004, Balcombe & Closs 2004,Okun & Mehner 2005). Or the clones adapted to other factors that are moreimportant than the predation risk caused by fish, e. g., temperature, food, in-vertebrate predators or parasites in deeper waters (Decaestecker et al. 2002).

The second unexpected result in our study as well as in previous studies(Table 4) was that a high percentage of Daphnia did not respond to fish kairo-mone at all. Like above, this could be a flaw in the experimental design. An al-ternative explanation is that the costs of errors (migrating downward when theperceived predation threat is not actually present) are very high. Costs ofdownward migration are due to lower temperature, sometimes threat of inver-tebrate predators and enhanced competition (Tollrian & Dodson 1999). Inthat case having no defense at all might be positively selected for. Apparently,

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kairomones from different fish species cannot be easily distinguished fromeach other (Loose et al. 1993, von Elert & Loose 1996, Ringelberg & vanGool 1998, but see Weber 2003). If only large, piscivorous fish are present,the antipredator defense would not be necessary. Furthermore, common antip-redator responses have been found counter-adaptive in some situations(McKelvey & Forward 1995, Hülsmann et al. 2004). The predators are al-most everywhere, so it is unlikely that random genetic drift over a long timewith no predators could so often result in loss of the capacity for a response.

The food concentration in our experiments was always very high (Lam-pert 1987) in all depths throughout the entire time of the experiment. The con-sequences of food concentration for vertical migration are still debated. Somestudies found an increase in antipredator responses with higher food levels(Dodson 1988 a), others show that defenses are expressed most significantlyat lower food concentrations (Parejko & Dodson 1991), while some studiesfind no effect of food level at all (Riessen 1999). In our columns, we did nothave a food or temperature gradient and the light gradient between control andtreatment tubes was identical. Most of work on food quantity and quality looksat depth gradients. Perhaps it is possible that the animals would show differentaverage depth distributions in response to food even in homogenous tubes butmore research on zooplankton distribution as a response to food levels and itsimplications is needed. Therefore, we assume that the predator-incubated wa-ter was the primary influence on depth selection behavior.

We conclude that the reactions to predator chemical can be as manifold asthe clonal diversity found in nature. Almost all D. pulex clones could be distin-guished from each other by their varying reaction norms towards predatorchemicals. Daphnia also seem to be able to estimate predation pressure andtheir own vulnerability to the given predation threat accurately and respondwith a scaled defense. The importance of Chaoborus as a predator on Daphniashould not be underestimated.

Acknowledgements

We would like to thank Emily Smith, Eric Triche and Jessica Mangro for help inthe laboratory. We also than William Kelso, John Fleeger, David Foltz, Mo-hamed Noor, William DeMott and one anonymous reviewer for comments on themanuscript. Special thanks go to Mohammed Noor for allowing access to his labora-tory and equipment to do the genetic analyses.

References

Alfonso, C., Rocco, V., Barriga, J. P., Battini, M. A. & Zaragese, H. (2004):Surface avoidance by freshwater zooplankton: Field evidence on the role of ultra-violet radiation. – Limnol. Oceanogr. 49: 225–232.

eschweizerbartxxx


Balcombe, S. R. & Closs, G. P. (2004): Spatial relationships and temporal variabilityin a littoral macrophyte fish assemblage. – Mar. Freshwat. Res. 55: 609–617.

Benndorf, J., Wissel, B., Sell, A. F., Hornig, U., Ritter, P. & Böing, W. (2000):Food web manipulation by extreme enhancement of piscivory: An invertebratepredator compensates for the effects of planktivorous fish on a plankton commu-nity. – Limnologica 30: 235–245.

Boeing, W. J., Williamson, C. E., Leech, D. M., Cooke S. & Torres, L. (2004):Damaging UV radiation and invertebrate predation: Conflicting selective pressu-res for zooplankton vertical distribution in the water column of low DOC lakes. –Oecologia 138: 603–612.

Boeing, W. J., Wissel, B. & Ramcharan, C. W. (2005): Costs and benefits of Daph-nia defense against Chaoborus in nature. – Can. J. Fish. Aquat. Sci. 62: 1286–1294.

Boersma, M., Spaak, P. & De Meester, L. (1998): Predator-mediated plasticity inmorphology, life history, and behavior in Daphnia: The uncoupling of responses.– Amer. Nat. 152: 237–248.

Brancelj, A., Celhar, T. & Sisko, M. (1996): Four different head shapes in Daph-nia hyalina (Leydig) induced by the presence of larvae of Chaoborus flavicans(Meigen). – Hydrobiologia 339: 37–45.

Dawidowicz, P., Pijanowska, J. & Ciechomski, K. (1990): Vertical migration ofChaoborus larvae is induced by the presence of fish. – Limnol. Oceanogr. 35:1631–1637.

Decaestecker, E., De Meester, L. & Ebert, D. (2002): In deep trouble: habitat se-lection constrained by multiple enemies in zooplankton. – Proc. Natl Acad. Sci.USA 99: 5481–5485.

De Meester, L. (1993): Genotype, fish-mediated chemicals and phototaxis in Daph-nia. – Ecology 74: 1467–1474.

– (1996): Evolutionary potential and local genetic differentiation in a phenotypicallyplastic trait of a cyclical parthenogens, Daphnia magna. – Evolution 50: 1293–1298.

De Meester, L. & Cousyn, C. (1997): The change in phototactic behaviour of aDaphnia magna clone in the presence of fish kairomones: the effect of exposuretime. – Hydrobiologia 360: 169–175.

De Meester, L., Dawidowicz, P., van Gool, E. & Loose, C. J. (1999): Ecology andEvolution of Predator-Induced Behavior of Zooplankton: Depth Selection Behav-ior and Diel Vertical Migration. – In: Tollrian R. & Harvell C. D. (eds): TheEcology and Evolution of Inducible Defenses. – Princeton University Press, Prin-ceton, New Jersey, pp.160–176.

De Meester, L. & Pijanowska, J. (1996): On the trait-specificity of the response ofDaphnia genotypes to the chemical presence of a predator. – In: Lenz, P. H.,Harline, D. K., Purcell, J. E. & Macmillan, D. L. (eds): Zooplankton: sensoryecology and physiology. – Gordon & Breach, Amsterdam, pp. 407–417.

Dodson, S. I. (1972): Mortality in a population of Daphnia rosea. – Ecology 53:1011–1023.

– (1988 a): Cyclomorphosis in Daphnia galeata mendotae Birge and D. retrocurvaForbes as a predator-induced response. – Freshwat. Biol. 19: 109–114.

– (1988 b): The ecological role of chemical stimuli for zooplankton: Predator-avoi-dance behavior in Daphnia. – Limnol. Oceanogr. 33: 1431–1439.

eschweizerbartxxx


Gonzalez, M. J. & Tessier, A. J. (1997): Habitat segregation and interactive effectsof multiple predators on a prey assemblage. – Freshwat. Biol. 38: 179–191.

Greenberg, A. E., Connors, J. J., Jenkins, D. & Franson M. A. H. (eds) (1981):Standard methods for the examination of water and wastewater. 15th edition. –American Public Health Association, Washington DC, USA.

Harvell, C. D. (1990): The ecology and evolution of inducible defenses. – Q. Rev.Biol. 65: 323–340.

Havel, J. E. & Dodson, S. I. (1984): Chaoborus predation on typical and spinedmorphs of Daphnia pulex: Behavioral observations. – Limnol. Oceanogr. 29: 487–494.

Hebert, P. D. N. & Grewe, P. M. (1985): Chaoborus-induced shifts in the morphol-ogy of Daphnia ambigua. – Limnol. Oceanogr. 30: 1291–1297.

Hülsmann, S., Vijverberg, J., Boersma, M. & Mooij, W. M. (2004): Effects of in-fochemicals released by gape-limited fish on life history traits of Daphnia: a mala-daptive response? – J. Plankton Res. 26: 535–543.

Kühn, A. (1955): Vorlesungen über Entwicklungsphysiologie. – Springer Verlag,Berlin.

Lampert, W. (1987): Feeding and nutrition in Daphnia. – In: Peters, R. H. & DeBernardi, R. (eds): Daphnia. – Mem. Ist. Ital. Idrobiol. 45: 143–192.

– (1989): The adaptive significance of diel vertical migration of zooplankton. –Funct. Ecol. 3: 21–27.

Lass, S. & Spaak, P. (2003): Chemically induced anti-predator defences in plankton: areview. – Hydrobiologia 491: 221–239.

Leech, D. M. & Williamson, C. E. (2001): In situ exposure to ultraviolet radiationalters the depth distribution of Daphnia. – Limnol. Oceanogr. 46: 416–420.

Lehman, N., Pfrender, M. E., Morin, P. A., Crease, T. J. & Lynch, M. (1995): Ahierarchical molecular phylogeny with the genus Daphnia. – Mol. Phylogenet.Evol. 4: 395–407.

Loose, C. J. (1993): Daphnia diel vertical migration behavior: Response to vertebratepredator abundance. – Arch. Hydrobiol., Spec. Issues Advanc. Limnol. 39: 29–36.

Loose, C. J. & Dawidowicz, P. (1994): Trade-offs in diel vertical migration by zoo-plankton: the costs of predator avoidance. – Ecology 75: 2255–2263.

Loose, C. J., von Elert, E. & Dawidowicz, P. (1993): Chemically-induced dielvertical migration in Daphnia: a new bioassay for kairomones exuded by fish. –Arch. Hydrobiol. 126: 329–337.

Luecke, C. (1986): A change in the pattern of vertical migration of Chaoborus flavi-cans after the introduction of trout. – J. Plankton Res. 8: 649–657.

Lynch, M. (1983): Ecological genetics of Daphnia pulex. – Evolution 37: 358–374.Mayr, E. (1963): Animal species and evolution. – The Belknap Press of Harvard Uni-

versity Press, Cambridge, Massachusetts.McKelvey, L. M. & Forward, R. B. Jr. (1995): Activation of brine shrimp nauplii

photoresponses involved in diel vertical migration by chemical cues from visualand non-visual planktivores. – J. Plankton Res. 17: 2191–2206.

Nesbitt, L. M., Riessen, H. P. & Ramcharan, C. W. (1996): Opposing predationpressures and induced vertical migration responses in Daphnia. – Limnol. Ocea-nogr. 41: 1306–1311.

eschweizerbartxxx


Noor, M. A. F., Grams, K. L., Bertucci, L. A., Almendarez, Y., Reiland, J. &Smith, K. R. (2001): The genetics of reproductive isolation and the potential forgene exchange between Drosophila pseudoobscura and D. persimilis via back-cross hybrid males. – Evolution 55: 512–521.

Okun, N. & Mehner, T. (2005): Distribution and feeding of juvenile fish on inverte-brates in littoral reed (Phragmites) stands. – Ecol. Freshwat. Fish 14: 139–149.

Palumbi, S. R. (1996): Nucleic acids II: the polymerase chain reaction. – In: Hillis,D. M., Moritz, C. & Mable, B. K. (eds): Molecular systematics. – Sinauer Asso-ciates, Sunderland, MA, pp. 205–247.

Parejko, K. & Dodson, S. I. (1991): The Evolutionary Ecology of an AntipredatorReaction Norm: Daphnia pulex and Chaoborus americanus. – Evolution 45:1665–1674.

Pfrender, M. E., Spitze, K. & Lehman, N. (2000): Multi-locus genetic evidence forrapid ecologically based speciation in Daphnia. – Mol. Ecol. 9: 1717–1735.

Ramcharan, C. W., Dodson, S. I. & Lee, J. (1992): Predation Risk, Prey Behavior,and Feeding Rate in Daphnia pulex. – Can. J. Fish. Aquat. Sci. 49: 159–165.

Ramcharan, C. W., Yan, N. D., McQueen, D. J., Perez-Fuentetaja, A., Demers,E. & Russak, J. A. (2001): Dynamics of zooplankton productivity under two dif-ferent predatory regimes. – Arch. Hydrobiol., Spec. Issues Advanc. Limnol. 56:151–169.

Reede, T. & Ringelberg, J. (1995): The influence of a fish exudates on two clones ofthe hybrid Daphnia galeata × hyalina. – Hydrobiologia 307: 129–140.

Rhode, S. C., Pawlowski, M. & Tollrian, R. (2001): The impact of ultraviolet ra-diation on the vertical distribution of zooplankton of the genus Daphnia. – Nature412: 69–72.

Riessen, H. P. (1999): Predator-induced life history shifts in Daphnia: a synthesis ofstudies using meta-analysis. – Can. J. Fish. Aquat. Sci. 56: 2487–2494.

Ringelberg, J. (1991): A mechanism of predator-mediated induction of diel verticalmigration in Daphnia hyalina. – J. Plankton Res. 13: 83–89.

Ringelberg, J. & van Gool, E. (1998): Do bacteria, not fish, produce ‘fish kairo-mone’? – J. Plankton Res. 20: 1847–1852.

Rousseau, F., Rehel, R., Rouillard, P., Degranpre, P. & Khandjian, E. W.(1994): High-throughput and economical mutation detection and RFLP analysisusing a minimethod for DNA preparation from whole-blood and acrylamide-gelelectrophoresis. – Human Mutation 4: 51–54.

SAS Institute Inc. (2002): Installation Instructions for Release 8.2 (TS2MO) of theSAS System for Microsoft Windows, Caryu, NC: SAS Institute Inc., 2002.

Spaak, P. & Hoekstra, J. R. (1993): Clonal structure of the Daphnia population inLake Maarsseveen: Its implications for diel vertical migration. – Arch. Hydrobiol.,Spec. Issues Advanc. Limnol. 39: 157–165.

Spitze, K. (1992): Predator-mediated plasticity of prey life history and morphology:Chaoborus americanus predation on Daphnia pulex. – Amer. Nat. 148: 108–123.

Sunnucks, P. (2000): Efficient genetic markers for population biology. – TREE 15:199–203.

Tessier, A. J. & Leibold, M. A. (1997): Habitat use and ecological specializationwithin lake Daphnia populations. – Oecologia 109: 561–570.

eschweizerbartxxx


Tollrian, R. (1993): Neckteeth formation in Daphnia pulex as an example of contin-uous phenotypic plasticity: Morphological effects of Chaoborus kairomone con-centration and their quantification. – J. Plankton Res. 15: 1309–1318.

– (1995): Predator-induced morphological defenses: Costs, life-history shifts, andmaternal effects in Daphnia pulex. – Ecology 76: 1691–1705.

Tollrian, R. & Dodson, S. I. (1999): Inducible Defenses in Cladocera: Constrains,Costs, and Multipredator Environments. – In: Tollrian, R. & Harvell, C. D.(eds). The Ecology and Evolution of Inducible Defenses. – Princeton UniversityPress, Princeton, New Jersey.

Tollrian, R. & Harvell, C. D. (eds) (1999): The Ecology and Evolution of Indu-cible Defenses. – Princeton University Press, Princeton, New Jersey.

van Gool, E. & Ringelberg, J. (1995): Swimming of Daphnia galeata × hyalina inresponse to changing light intensities: Influence of food availability and predatorkairomone. – Mar. Freshwat. Behav. Physiol. 26: 259–265.

von Elert, E. & Loose, C. J. (1996): Predator-induced diel vertical migration inDaphnia: Enrichment and preliminary chemical characterization of a kairomoneexuded by fish. – J. Chem. Ecol. 22: 885–895.

von Elert, E. & Pohnert, G. (2000): Predator specificity of kairomones in diel vert-ical migration of Daphnia: a chemical approach. – Oikos 88: 119–128.

Voss, S. & Mumm, H. (1999): Where to stay by day and night: Size-specific and sea-sonal differences in horizontal and vertical distribution of Chaoborus flavicanslarvae. – Freshwat. Biol. 42: 201–213.

Weber, A. (2003): More than one ‘fish kairomone’? Perch and stickleback kairomo-nes affect Daphnia life history traits differently. – Hydrobiologia 498: 143–150.

Weber, A. & van Noordwijk, A. J. (2002): Swimming behaviour of Daphnia clones:differentiation through predator infochemicals. – J. Plankton Res. 24: 1335–1348.

Weider, L. J. (1984): Spatial heterogeneity of Daphnia genotypes: Vertical migrationand habitat partitioning. – Limnol. Oceanogr. 29: 225–235.

Woltereck, R. (1909): Weitere experimentelle Untersuchungen über Artenverände-rung, speziell über das Wesen quantitativer Artunterschiede bei Daphniden. –Verh. dt.. Tsch. Zool. Ges. 1909: 110–172.

Submitted: 10 May 2005; accepted: 31 January 2006.

Clonal variation in depth distribution of Daphnia pulex in response to predator kairomones

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