Fillable Form 1: and hatching of Temora longicornis eggs (Inter Research Science Publisher)

Fill Online, Printable, Fillable, Blank Form 1: and hatching of Temora longicornis eggs (Inter Research Science Publisher) Form

Use Fill to complete blank online INTER RESEARCH SCIENCE PUBLISHER pdf forms for free. Once completed you can sign your fillable form or send for signing. All forms are printable and downloadable.

Form 1: and hatching of Temora longicornis eggs (Inter Research Science Publisher)

The Form 1: and hatching of Temora longicornis eggs (Inter Research Science Publisher) form is 0 pages long and contains:

0 signatures
0 check-boxes
0 other fields

Country of origin: US
File type: PDF

Use our library of forms to quickly fill and sign your Inter Research Science Publisher forms online.

BROWSE INTER RESEARCH SCIENCE PUBLISHER FORMS

Related forms

Fill has a huge library of thousands of forms all set up to be filled in easily and signed.

Fill in your chosen form

Sign the form using our drawing tool

Send to someone else to fill in and sign.

find another form

MARINE ECOLOGY PROGRESS SERIES

Mar Ecol Prog Ser

Vol. 382: 139–150, 2009

doi: 10.3354/meps07985

Published April 30

INTRODUCTION

To date studies on marine copepod nutritional

requirements have yielded widely varying results

regarding what limits egg production, hatching and

ontogenic development. Compounds that have been

shown to be potential controlling factors of these

growth categories include many different fatty acids,

sterols and amino acids. A summary of 20 studies in

which fatty acid composition of the potential food was

measured along with copepod production (Table 1)

shows that a suite of specific fatty acids have been sig-

nificantly correlated (positively and negatively) with

copepod egg production rates (EPR) and hatching suc-

cess. From this list one can see that one study may find

a significant positive relationship between egg pro-

duction rates and the concentration of a specific

dietary fatty acid, while another study might find a

negative, or lack of (not listed in Table 1) relationship

with the same fatty acid. An example of this is the cor-

relation of EPR with the fatty acid 20:5n-3 in the diet,

whereby Broglio et al. (2003) found a positive relation-

ship, Arendt et al. (2005) found no correlation, and

Koski et al. (2006) reported a negative relationship.

The possible reasons for the inconsistent results are

numerous: different zooplankton species may have

had different requirements for growth (Hassett 2004),

the food concentrations offered have ranged from lim-

iting to super-saturating levels, the lengths of experi-

ments have varied from 1 to >10 d, and correlations in

one study may have been based on food available

(Jónasdóttir 1994) and in other studies on food

ingested (e.g. Broglio et al. 2003, Dutz et al. 2008).

However, the most likely reason for the observed

inconsistencies between the investigations is that the

different studies might have been dealing with differ-

ent nutrient limitations, that is, that some limiting com-

ponent is measured in one study but not in the others.

For example, when diatoms are offered as food, the

fatty acid 20:5n-3 (EPA) will not be the limiting compo-

nent, while specific sterols may be limiting (Hassett

2004, Klein Breteler et al. 2005). When the chlorophyte

Dunaliella, which totally lacks EPA, is used as food,

EPA is always limiting. However, Dunaliella is also

Assessing the role of food quality in the production

and hatching of Temora longicornis eggs

Sigrún Huld Jónasdóttir

, André W. Visser

, Carsten Jespersen

Technical University of Denmark, National Institute of Aquatic Resources (DTU-Aqua), Kavalergaarden 6,

2920 Charlottenlund, Denmark

University of Southern Denmark, Department of Biology, Campusvej 55, 5230 Odense M, Denmark

ABSTRACT: We utilized the varying fatty acid composition of phytoplankton to create 19 different

food treatments based on different ratios of 5 potentially important fatty acids and offered these to the

copepod Temora longicornis. Egg production and hatching was monitored and related to ingested

carbon, dietary fatty acids and the utilization of maternal fatty acid reserves. Egg production rates

depended on ingested carbon and the fatty acid 20:5n-3 from the diet and from the female reserves.

Hatching success showed a significant dependence on the ingested and maternal fatty acids 22:6n-3,

18:5n-3 and 18:3n-3. Production of nauplii as a combination of egg production and hatching was

highly dependent on the fatty acid 22:6n-3 and carbon ingestion. The study confirms the importance

of n-3 polyunsaturated fatty acids for copepod reproduction and indicates that the female differen-

tially utilizes its fatty acid reserves depending on dietary fatty acid availability during reproduction

and that egg production and hatching are dependent on different dietary fatty acids.

KEY WORDS: Egg production · Hatching · Food quality · Fatty acid · Temora longicornis

Resale or republication not permitted without written consent of the publisher

Mar Ecol Prog Ser 382: 139–150, 2009

deficient in other essential components, such as other

long-chain polyunsaturated fatty acids (PUFAs) and

essential sterols (Klein Breteler et al. 1999). Therefore,

artificially adding EPA to a Dunaliella diet will not

reveal an improvement in growth as the other essential

components will still limit growth. Thus, studies with a

variable availability of nutritional components have

the best potential in helping us to understand how

140

Fatty acid/sterol Fatty acid Correlation Source

short name + –

Copepod species

Egg production rates

14:0 3 A, T, C 4, 7

16:0 2 T 18

18:0 2 A, C 7, 8

SAFA 1 T 16

16:1n-7 3 2 A, C 2, 7, 10

18:1 5 A, T, C 2, 7, 19

MUFA 2 T, C 7, 16

16:2n-x 1 C 10

18:2n-6 LA 2 A 4

18:3n-3 ALA 2 1 A, C 2, 12, 17

18:4n-3 SDA 3 3 A, T, C 2, 4, 13, 17

18:5n-3 1 A 2

20:4n-6 ARA

20:5n-3 EPA 7 3 A, P, C, T 2, 3, 7, 8, 10, 11, 16, 17, 18, 19

22:6n-3 DHA 8 1 A, T, C 2, 4, 7, 11, 13, 20

PUFA 3 A, C 7, 10

Total fatty acids 3 A, T, C 2, 7, 16

n-6 series 2 2 A, T 4

n-3 series 2 A 2

n-3/n-6 4 2 A, T, C 2, 4, 6, 7

22:6n-3/20:5n-3 DHA/EPA 6 2 A, T 1, 2, 4, 6, 19

16:1n-7/16:0 1 1 T, C 10, 16

Cholesterol 4 A, C 14, 15

Hatching

14:0 1 C 10

16:0 2 C 10

18:0 1 A, C 6, 10

SAFA 3 A, C, T 10, 16, 19

16:1n-7 1 C 10

18:1 1 3 A, C, T 6, 10, 16

MUFA 2 A, C 5, 7

16:2n-x 3 A, P, C 5, 9, 17

18:2n-6 3 A, P, C 5, 9, 17

18:3n-3 1 C 7

18:4n-3 2 1 T 16, 18

18:5n-3 4 A, P, T, C 5, 9, 16, 17

20:4n-6

20:5n-3

22:6n-3

PUFA 1 A 3, 11

Total fatty acids

n-6 series

n-3 series

n-3/n-6 3 1 A, C, T 6, 7, 11, 13

22:6n-3/20:5n-3 6 A, T 6, 11, 16, 19

16:1n-7/16:0 1 T 16

Cholesterol 1 A 14

Table 1. Summary of reported significant correlations between marine copepod egg production rates or egg hatching success and

various fatty acids and sterols (including ratios). +: number of studies showing significant positive correlation; –: number of stud-

ies showing significant negative correlation; SAFA: sum of saturated fatty acids; MUFA: sum of monounsaturated fatty acids;

PUFA: sum of polyunsaturated fatty acids; A: Acartia tonsa, A. hudsonica and/or A. omorii; T: Temora longicornis; C: Calanus fin-

marchicus and/or C. helgolandicus; P: Pseudocalanus newmani; Sources—1: Støttrup & Jensen (1990); 2: Jónasdóttir (1994);

3: Ederington et al. (1995); 4: Jónasdóttir et al. (1995); 5: Kleppel & Burkart (1995); 6: Jónasdóttir & Kiørboe (1996); 7: Pond et al.

(1996); 8: Kleppel et al. (1998); 9: Lee et al. (1999); 10: Jónasdóttir et al. (2002); 11: Broglio et al. (2003); 12: Hazzard & Kleppel

(2003); 13: Shin et al. (2003); 14: Hassett (2004); 15: Crockett & Hassett (2005); 16: Arendt et al. (2005); 17: Jónasdóttir et al. (2005);

18: Koski et al. (2006); 19: Peters et al. (2007); 20: Evjemo et al. (2008)

Jónasdóttir et al.: Temora reproduction and food quality

dietary nutrient composition affects production and

growth.

Another potentially important factor in nutritional

studies is the ability of the female to channel stored

body reserves into production. Some copepod species

have a better ability to store body reserves than others

(Evjemo et al. 2003), and the utilization of body

reserves for egg production also appears to be species

specific (Hassett 2006). This ability to channel stored

nutritional elements or compounds, such as nitrogen,

fatty acids and sterols, towards egg production and

growth is often not considered in copepod nutritional

studies.

The goal of the present study was to better differen-

tiate the role of certain fatty acids in the reproduction

of marine copepods. We specifically tested several

PUFAs, naturally occurring in phytoplankton at differ-

ent ratios, and related the ingested fatty acids to the

egg production and hatching success of the copepod

Temora longicornis. The choice of the phytoplankton

species used in the experiments was based on 2 crite-

ria. Firstly, they were selected according their ratios of

the fatty acids 18:3n-3, 18:5n-3, 20:4n-6, 20:5n-3 and

22:6n-3. All of these fatty acids have previously been

shown to be of some nutritional importance in repro-

ductive growth (Table 1). The second criterion was to

select phytoplankton types that had, in previous stud-

ies, been shown to result in mediocre reproduction

success, indicating that they lacked one or more nutri-

tional compounds for copepod reproduction. We pre-

sent results from a statistical model with the underly-

ing premise that certain dietary compounds control

both the rate at which copepods produce eggs and the

success rate at which they eventually hatch into nau-

plii. A portion of these dietary compounds comes

immediately from the copepod’s diet, while others are

obtained from the female’s internal reserves. Concep-

tually, we treat the female as a reservoir of various

dietary components that is continually topped up by

ingestion and emptied by the production of new eggs.

MATERIALS AND METHODS

Copepods. Experiments were conducted using the

calanoid copepod Temora longicornis originally ob-

tained from the central North Sea but cultured at the

DTU-Aqua laboratory for over a year. The cultures

were kept at about 15°C in the dark and maintained on

a mixture of the cryptophyte Rhodomonas sp., the

diatom Thalassiosira weissflogii and the dinoflagellate

Heterocapsa triquetra at a concentration of ca. 400 µg

C l

–1

. Three weeks prior to the experiments, a new cul-

ture was started with the naupliar stages only. This

ensured that at the time of the experiment the females

were at the same age, and also ensured that females

were in the same condition between experiments.

Phytoplankton. The phytoplankton used in the exper-

iments were the diatoms Thalassiosira weissflogii (TW)

and Leptocylindricus danicus (LD); the chlorophyte

Dunaliella tertriolecta (DT); the prasinophyte Tetra-

selmis suecica (TS); and the dinoflagellates Amphi-

dinium carterii (AC) and Heterocapsa triquetra (HT).

Phytoplankton was grown at 18°C in 1 to 2 l batch

cultures and B1 medium (Hansen 1989) with silica

added to the diatom cultures. The cultures were

exposed to an irradiance of 100 µmol photons m

–2

–1

a 16:8 h light:dark cycle. The algae were kept in the

exponential growth phase by daily dilutions of the cul-

ture. Cell densities were estimated by cell counts of a

minimum of 300 cells using Sedgwidge-Rafter count-

ing chambers. Average algal cell volumes were mea-

sured using a Coulter Counter with the exception of

LD for which length and width of >50 cells were mea-

sured using an inverted microscope. Cell concentra-

tions were converted to carbon using the volume-

based size according to Menden-Deuer & Lessard

(2000). Sizes, fatty acid and carbon content of the

phytoplankton are listed in Table 2.

Experiments. Six sets of experiments were con-

ducted, each with a series of phytoplankton mixtures

as shown in Table 3. Each food suspension was

adjusted to a final concentration of ca. 250 µg C l

–1

(actual range in all experiments from 225 to 276 µg C

–1

). Then, 13 mixture experiments and 12 single-diet

experiments were carried out. As 4 of the single diets

were repeated in some of the sets (TW [2], DT [3], LD

[3], TS [2]) this resulted in 19 different food treatments.

Ten females and 3 males were put into 630 ml exper-

imental bottles with the food suspensions. Each treat-

ment was run with 5 replicates. The bottles were

sealed without head space and placed on a rotating

(1 rpm) plankton wheel. The experiment was run for

9 d at 15°C in darkness. To avoid the potential negative

effect of the experimental food on the sperm quality

(Ianora et al. 1999), the males were replaced each day

with new ones from the stock culture. Consequently,

the fertilization potential of the produced eggs was

kept the same among all treatments and throughout

the experiment. Each day, new food suspensions were

made, females and eggs were gently sieved out of the

previous suspension (with 180 and 64 µm sieves,

respectively) and counted, and females were put into

fresh food suspensions. Empty egg membranes were

also counted to account for cannibalized eggs. After

Days 2, 6 and 9, eggs from each food treatment were

checked for hatching. The eggs from the 5 replicate

experimental bottles were pooled into one 630 ml bot-

tle containing 0.2 µm filtered seawater; the bottle was

sealed without headspace and placed on the rotating

141

Mar Ecol Prog Ser 382: 139–150, 2009

plankton wheel. After 72 h the content of the bottle

was fixed, and hatched nauplii were counted.

Ingestion rates were estimated on Days 3 to 4 and 7

to 8. In addition to the experimental bottles, 3 control

bottles without females or males were added to the

series of each of the food treatments, and initial con-

centrations were recorded. These bottles were also put

on the plankton wheel for 24 h. Cell concentrations in

each bottle were counted 24 h later, and ingestion

rates were calculated according to Frost (1972). For the

mixtures, the food selection index α was calculated

(Chesson 1983). This index relates the ingestion of the

different phytoplankton cells to their abundance,

where, for a 2 species mixture, α = 0.5 indicates no

selection (Chesson 1978). One-sample t-tests (SPSS)

were used to test for significant deviations of α from 0.5

(no selection).

At the end of each experiment (Day 9) the prosome

lengths of the females were measured with a dissec-

tion microscope using a calibrated ocular stage micro-

meter. A female carbon content of 8.25 µg C was as-

sumed based on the average female carbon content

measured on 2 occasions from the same copepod cul-

tures over a 1 yr period (M. Koski pers. comm.).

Chemical analysis. At 2 dates during the 9 d experi-

ment, samples from the phytoplankton cultures were

taken for fatty acid analysis. A triplicate sample of each

culture (> 500 µg C) was filtered onto pre-combusted GF/F

filters. In addition, at the termination of the experiments,

the females from each treatment were pooled and

analysed for fatty acid content (26 to 40 females sample

–1

Similarly, 3 × 40 females from the stock culture were

analysed to attain the initial fatty acid composition of the

females. Samples were stored at –80°C until analysed.

142

Thalassiosira Leptocylidricus Dunaliella Tetraselmis Amphidinium Heterocapsa

weissflogii danicus tertriolecta suecica carteri triquetra

(TW) (LD) (DT) (TS) (AC) (HT)

14:0 0.93 0.95 ± 0.33 0.01 ± 0.01 0.02 ± 0.01 0.99 ± 0.31 4.17 ± 1.44

16:0 2.16 0.63 ± 0.18 1.02 ± 0.28 1.45 ± 0.34 6.53 ± 1.32 7.24 ± 2.47

18:0 0.38 0.01 ± 0.01 0.01 ± 0.01 0.01 ± 0.01 0.84 ± 0.18 0.20 ± 0.16

20:0 0.22 0.01 ± 0.004 0.01 ± 0.32 0.06 ± 0.03 0.77 ± 0.21 0.18 ± 0.18

SAFA 3.44 1.60 ± 0.51 1.05 ± 0.30 1.54 ± 0.35 9.12 ± 1.65 11.79 ± 3.86

16:1n-7 1.61 1.67 ± 0.56 0.03 ± 0.01 0.06 ± 0.02 0.76 ± 0.24 0.38 ± 0.04

18:1n-9 0.48 0.10 ± 0.03 0.16 ± 0.03 0.44 ± 0.08 0.43 ± 0.13 0.35 ± 0.18

18:1n-7 0.29 ± 0.04 0.04 ± 0.02 0.20 ± 0.08 0.21 ± 0.12 0.06 ± 0.03

MUFA 2.41 1.67 ± 1.18 0.03 ± 0.01 0.11 ± 0.02 0.76 ± 0.24 0.38 ± 0.04

16:2n-4 0.00 0.61 ± 0.28 0.05 ± 0.01 0.02 ± 0.01 0.02 ± 0.01

16:3n-4 0.04 1.18 ± 0.62

16:3n-6 0.20 ± 0.04 0.05 ± 0.01

16:4n-3 0.88 ± 0.18 1.44 ± 0.36

16:4n-1 0.15 ± 0.07

18:2n-6 0.18 0.01 ± 0.01 0.28 ± 0.05 0.08 ± 0.02 0.03 ± 0.03 0.44 ± 0.17

18:3n-6 0.03 ± 0.02 0.05 ± 0.04

18:3n-3 ALA 0.14 2.01 ± 0.32 0.95 ± 0.24 1.03 ± 0.25

18:4n-3 0.15 0.02 ± 0.004 0.02 ± 0.04 0.43 ± 0.16 0.97 ± 0.14 1.95 ± 0.34

18:5n-3 0.02 0.13 ± 0.04 2.42 ± 0.52

20:4n-6 ARA 0.08 0.33 ± 0.14

20:5n-3 EPA 0.81 0.13 ± 0.06 0.04 ± 0.02 0.01 ± 0.003

22:6n-3 DHA 0.18 0.29 ± 0.08 1.03 ± 0.35

PUFA 2.06 2.47 ± 1.18 3.49 ± 0.62 3.13 ± 0.84 1.31 ± 0.18 6.87 ± 0.94

Total FAs 9.64 6.37 ± 2.36 4.99 ± 1.00 5.80 ± 1.27 14.82 ± 2.73 22.10 ± 3.10

Other FAs 0.80 0.24 ± 0.10 0.22 ± 0.05 0.37 ± 0.07 2.99 ± 1.06 2.64 ± 0.23

Carbon (pg cell

–1

) 76 59 29 56 190 325

Volume (µm

) 878 716 262 353 764 1472

% FA of total C 12.7 10.8 17.2 10.4 7.8 6.8

Table 2. Characteristics of the phytoplankton: fatty acid and carbon content (pg cell

–1

, ±1 SE), size (µm

) and percent of total fatty

acids in carbon content. Total FAs: sum of all fatty acids; SAFA: saturated fatty acids; MUFA: monounsaturated fatty acids; PUFA:

polyunsaturated fatty acids. The fatty acids 18:3n-3 (ALA), 18:5n-3, 20:4n-6 (ARA), 20:5n-3 (EPA) and 22:6n-3 (DHA) used in our

analysis are given in bold print. Fatty acid data for TW calculated from Arendt et al. (2005); carbon content calculated from

volume after Menden-Deuer & Lessard (2000)

Jónasdóttir et al.: Temora reproduction and food quality

Fatty acid analysis was conducted according to the

method described by Klein Breteler et al. (1999). The

samples were extracted in KOH:MeOH, including a

known amount of an internal standard (23:0), and

saponified for 35 min at 85°C. After acidification of the

sample to pH 3, double-distilled water, MeOH and

dichloromethane were added. The sample was treated

with ultrasound, and the lipid fraction was drawn off

and passed through a NaSO

column to remove all

traces of water. Samples were transmethylated using

to form fatty acid methyl esters (FAME), eluted

over a silica column with ethyl acetate, and subse-

quently analysed on a gas chromatograph–mass spec-

trometer (GC-MS, Agilent 6890 with PTV inlet and

Agilent 5973 mass selective detector) on an Agilent

DB23 (60 m × 0.25 mm) column using helium as carrier

gas. Retention times were compared to those of known

FAME mixtures (Matreya PUFA3, SUPELCO 18919

and an extract from the dinoflagellate Prorocentrum

minimum to locate the 18:5n-3 fatty acid).

Model calculations. The underlying premise for a

food-quality model is that certain dietary compounds

control both the rate at which copepods produce eggs

and the success rate at which they eventually hatch into

nauplii. Some quantity of these dietary compounds

comes immediately from the copepod’s diet, while

other quantities are stored and can be released from the

female’s reserves. In this model, we treat the female as

a reservoir of various dietary components (the 5 fatty

acids of interest) that is continually

recharged by ingestion and emptied

by the production of eggs. That is:

where A is a vector representing the

various compounds in the female, A

represents the compounds in the food,

and A

represents these compounds in

the eggs. The vector I represents the

ingestion rate of each compound, and

is the egg production. Integrating

over time gives:

While there are doubtless other loss

terms, we can use the vector quantity

to indicate the potential contribution

of various compounds in influencing

egg quantity and quality from both

maternal and dietary sources.

A forward, stepwise regression of

the elements of P, as well as total

ingested C, was performed against

total egg production (EP, Days 3 to 9), total nauplii pro-

duction (NP, Days 3 to 9) and the percent of hatching

success (Day 9) using SPSS. The forward, stepwise

regression seeks the best possible statistical model, by

successively introducing variables into a multiple

regression. The F-value for a new variable to be

entered into the regression was set at 4.0, essentially

equal to a p-value of 0.06. Five different dietary com-

ponents were tested. In order to fulfil the constancy of

variance requirement, hatching success values (in %)

were arcsine and log transformed prior to analysis.

RESULTS

The experiments were carried out over a 1 yr period,

from March 2005 to March 2006, and tested to deter-

mine if the performance of the females was different in

the experiments over time. Egg production rates (EPR)

measured after the first incubation day of acclimation

on the non-mixed diets (100%) showed no significant

differences in average EPRs between the 6 experi-

ments (2-way ANOVA: F

5,5

= 1.76, p = 0.15). It can be

said with confidence that the different generations of

cultured females were not performing differently over

the period of the experiment.

Female size did not differ between the experiments

(mean ± SD: 1.027 ± 0.008 mm, 1-way ANOVA, F

1.11, p = 0.32).

PIA A A=⋅ + −

tt() ()0

AA IA A() ( )tEt−=⋅−

()

fre

IA A

E=⋅ −

143

Expt Treatment Carbon Total FA Total PUFA

No. Phytoplankton

1, 2 1 TW100 258 ± 10 36 ± 0.1 8 ± 0.03

1 2 TW66/DT33 250 ± 16 37 ± 2.2 15 ± 0.7

1 3 TW33/DT66 230 ± 9 36 ± 1.3 22 ± 0.8

1, 3, 6 4 DT100 248 ± 3 40 ± 0.8 30 ± 0.3

2 5 TW75/LD25 260 ± 10 32 ± 1.2 8 ± 0.4

2 6 TW50/LD50 250 ± 16 27 ± 2.4 8 ± 0.4

2 7 TW25/LD75 239 ± 3 28 ± 0.4 9 ± 0.1

2, 3, 4 8 LD100 251 ± 4 27 ± 0.5 10 ± 1.0

3 9 LD66/DT33 247 ± 4 30 ± 0.5 18 ± 0.2

3 10 LD33/DT66 260 ± 17 37 ± 1.8 25 ± 0.7

4, 5 11 TS100 249 ± 4 21 ± 1.1 13 ± 0.2

4 12 TS66/LD33 238 ± 6 23 ± 0.7 11 ± 0.2

4 13 TS33/LD66 260 ± 14 25 ± 1.3 9 ± 0.6

5 14 TS66/AC33 253 ± 4 21 ± 0.5 9 ± 0.4

5 15 TS33/AC66 250 ± 0.4 18 ± 0.03 6 ± 0.01

5 16 AC100 238 ± 15 15 ± 0.9 2 ± 0.1

6 17 HT100 260 ± 1 15 ± 0.03 5 ± 0.01

6 18 HT66/DT33 250 ± 13 25 ± 1.1 14 ± 0.6

6 19 HT33/DT66 247 ± 4 35 ± 0.5 21 ± 0.3

Table 3. Specifics of the 19 treatments. Carbon and fatty acid compositions in the

19 treatments offered. Phytoplankton treatment (abbreviations as in Table 2)

followed by the carbon-based percent ratio of the phytoplankton type in the

mixture. Carbon, total fatty acid (FA) and polyunsaturated fatty acid (PUFA)

concentrations (µg l

–1

, ±1 SE)

Mar Ecol Prog Ser 382: 139–150, 2009

Ingestion rates

Temora longicornis ingested 7 to 70% of its body car-

bon per day, with the lowest value observed when

Dunaliella tertriolecta was used as food (Fig. 1). There

was a significant difference between the treatments in

carbon-specific ingestion (1-way ANOVA, F

= 23.58,

p < 0.001), with the lowest ingestion rates being signif-

icantly different from the highest (results from 171

pairwise comparisons using the Holm-Sidak post hoc

method). The results from t-tests on the difference of

the measured selection index α from 0.5 are shown

next to the bars of the mixed diets in Fig. 1. D. tertri-

olecta was not ingested at high rates or in proportion to

144

LD TS AC HTTW DT

100%TW

33%DT

66%TW

66%DT

33%TW

100%DT

0.0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.39

0.61

0.19

***

0.81

0.44

0.56

0.46

0.54

0.0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

100%TW

25%LD

75%TW

100%LD

50%LD

50%TW

75%LD

25%TW

0.39

0.61

0.0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.47

0.53

0.42

0.58

100%TS

33%LD

66%TS

66%LD

33%TS

100%LD

100%TS

33%AC

66%TS

66%AC

33%TS

100%AC

0.0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.37

0.63

0.34

***

0.66

100%HT

33%DT

66%HT

66%DT

33%HT

100%DT

0.0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.45

0.55

0.30

***

0.70

33%DT

66%LD100%LD

66%DT

33%LD

100%DT

Ingestion rate (µgC µgC

–1

)

0.0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.34

***

0.66

0.31

0.69

Fig. 1. Temora longicornis. Carbon-based ingestion rates, I (µg C µg

–1

female C d

–1

) of T. longicornis feeding on the phytoplank-

ton species mixtures offered in the 6 experiments, (a) TW + DT, (b) TW + LD, (c) LD + DT, (d) TS + LD (e) AC + TS and (f) HT + DT.

Different shading patterns in the bars correspond to the phytoplankton types TW, DT, LD, TS, AC and HT (see Table 2 for full

species names). The selection index α is shown next to the bars of the mixtures they represent, where α > 0.5 indicates positive se-

lection; whiskers: +1 SE of the total carbon ingestion. Results of t-tests representing the difference of α from 0.5 are indicated

with: ns: nonsignificant difference; **: p < 0.001; ***: p < 0.0001

Jónasdóttir et al.: Temora reproduction and food quality

its availability (selection index α < 0.5). Therefore, T.

longicornis showed a significant preference for Thalas-

siosira weissflogii, Leptocylindricus danicus and Hete-

rocapsa triquetra (33HT/66DT) over D. tertriolecta, but

in the 66HT/33DT diet mixture an α-value of 0.45 was

not significantly different from 0.5. No selection was

detected when L. danicus and T. weissflogii were

offered together, except for a positive selection for T.

weissflogii with the 75TW/25LD mixture. T. longicor-

nis selected Tetraselmis suecica over Amphidinium

carterii, as well as over L. danicus, in the 33TS/66LD

mixture.

In the 19 food treatments Temora longicornis

ingested very different proportions and concentrations

of the 5 PUFAs of interest (PUFA

; Fig. 2a). The PUFA

ingestion is a combination of the fatty acid composition

of the different phytoplankton types offered (Fig. 2b,

Table 2) and the ingestion rates of each of these diets

(selection). The lowest total PUFA

ingested was on a

100% AC diet (3 ng PUFA

female

–1

), and the high-

est, with the TW66/DT33 mixture (168 ng PUFA

female

–1

). There was a significant difference

between the ingested PUFA

in the 19 treatments (1-

way ANOVA, F

= 18.14, p < 0.001). The composition

of these ingested fatty acids was tested in the model.

Reproduction

EPRs varied depending on the phytoplankton mix-

ture offered, ranging from 1 to 20 eggs female

–1

being significantly highest when a diet of TW alone

was offered (Fig. 3a). The difference between the 2

highest rates, with TW and 75TW/25LD diets (Fig. 3b),

was highly significant (2-way ANOVA: F

1,70

= 185.9,

p < 0.001). Acclimation to the food offered took 2 d, and

all statistical analyses were performed on rates

observed on Days 3 to 9. Out of 171 pairs, a significant

difference was found between 137 pairs (Holm-Sidak

multiple post hoc comparison, p < 0.001).

Hatching declined with time on most but not all of

the treatments; after 9 d of incubation it ranged from

15 to 81% (Fig. 3c,d). The highest hatching percents

(65 to 81%) were achieved on the diet mixtures 33TW/

66DT, 66HT/33DT, 75TW/25LD and 66TW/33DT

(Fig. 3d) and on the single diet 100AC (Fig. 3c), while

the lowest hatching rates (15 to 20%) were achieved

on the diet mixtures 25TW/75LD, 66TS/33LD,

33TS/66LD and 50TW/50LD (Fig. 3d). Statistical com-

parisons of the different treatments were done on mea-

surements from Days 6 and 10, and, of 171 pairs, signif-

icant differences were found between 37 pairs

(Holm-Sidak multiple post hoc comparison, p < 0.001).

Female composition

The total fatty acid content and the PUFA

ratios in

the females are shown in Fig. 4. The data is composed

of 1 to 3 measurements of 24 to 40 females each, but

due to the lack of variance estimate in many of the

averages, these cannot be statistically compared. Gen-

erally, the fatty acid content ranged from 0.03 to 1.8 µg

female

–1

(Fig. 4a). The females from the initial culture

appeared to have a higher PUFA content (0.4 µg

female

–1

) compared to females from the experimental

treatment. Some females appeared to be drained of

fatty acids after 9 d on the diet mixtures. Of the 5 fatty

acids of interest (PUFA

), the initial ratio was com-

posed of ca. 20% of 18:3n-3, 40% of 20:5n-3 and 40%

of 22:6n-3. The factions of these fatty acids were quite

variable at the end of the experiments depending on

the food treatments offered (Fig. 4b). The dietary fatty

acid 18:5n-3 did not appear in the females, and females

145

TW100

W66DT3

W33DT6

T10

75LD25

TW50LD50

TW25LD

LD1

66DT

33DT

S100

S66LD

S33LD6

S66

C33

33A

C66

100

66D

HT33DT6

Ingestion rate (ng FA female

–1

)

100

120

140

160

180

200

18:3n-3

18:5n-3

20:4n-6

20:5n-3

22:6n-3

66DT33

33DT66

DT100

TW75LD2

TW50LD5

TW25LD

LD66DT3

LD33DT66

TS100

66LD

33L

HT66DT

T33

FA concentration (ng ml

–1

)

Fig. 2. Temora longicornis. (a) Ingested specific fatty acids (pg

FA female

–1

), (b) concentration of the 5 fatty acids, 18:3n-

3, 18:5n-3, 20:4n-6, 20:5n-3 and 22:6n-3, offered. The shading

patterns in the bars indicate the 5 fatty acid types, and the 19

treatments specified in Table 3 are labelled on the x-axis

Mar Ecol Prog Ser 382: 139–150, 2009

from 4 diet mixtures only had 22:6n-3 out of the 5

PUFAs of interest at the end of the experiment. The

fatty acid 20:5n-3 was not measurable in the females in

9 of the 19 treatments.

The model

Results from the multiple regression model are

shown in Table 4. In each of the 3 production parame-

ters tested (egg production, hatching success, nauplii

production), a parsimonious and significant model was

found.

Egg production was highly correlated with the

amount of the fatty acid 20:5n-3 ingested (singular R

0.66, p = 0.006) in combination with carbon (combined

= 0.76). In contrast, hatching success showed a sig-

nificant but weaker dependence on the fatty acids

22:6n-3, 18:3n-3 and 18:5n-3 (combined R

= 0.65), but

no relationship with total ingested carbon. Nauplii pro-

duction was highly correlated with the fatty acid 22:6n-

3 (singular R

= 0.79) together with total carbon (com-

bined R

= 0.87). Fig. 5 illustrates the results for the

best model of the 2 most significant parameters for egg

production: hatching and naupliar production.

DISCUSSION

All organisms need several types of nutritional com-

ponents for successful growth (see e.g. Harrison 1990).

However, the apparent importance of these various

nutritional components depends on the particular

aspect of growth that is measured. Further, it is clear

146

EPR (eggs female

–1

)

123456789 123456789

100TW

100DT

100LD

100TS

100AC

100HT

Time (d) Time (d)

Hatching success (%)

66TW/33DT

33TW/66DT

75TW/25LD

50TW/50LD

25TW/75LD

66LD/33DT

33LD/66DT

66DL/33TS

33LD/66TS

66TS/33AC

33TS/66AC

66HT/33DT

33HT/66DT

Single diets

Mixed diets

Fig. 3. Temora longicornis. Egg production rates (EPR, eggs female

–1

, ±1 SE) in (a) single-diet and (b) mixed-diet experiments,

and percent hatching success of the eggs in (c) single diet and (d) mixed diet experiments over 9 d

Jónasdóttir et al.: Temora reproduction and food quality

that various reproductive and growth aspects (gonad

development, egg production, egg quality, naupliar

and juvenile growth) have requirements for >1 nutri-

tional component, and these may change during differ-

ent stages of development. It has complicated nutri-

tional studies that particular nutritional needs are not

the same for these different growth phases. Reproduc-

tion involves maternal mobilization, biosynthesis and

bioaccumulation of materials that are transferred to

eggs (Harrison 1990). When the egg is fertilized, it has

to be able to support the development of the embryo,

e.g. for 2 naupliar non-feeding stages as in the case of

Temora longicornis and most copepod species. The

diet has to supply sufficient energy and nutrients to

meet the reproductive cost of egg production, and the

number of eggs produced is dependent on the quantity

147

TW100

TW66D

TW33DT66

T100

5LD

TW50LD50

TW25LD

LD1

LD66D

T33

LD3

T66

TS100

66LD

TS33LD66

TS33A

100

HT3

T66

FA content (µg female

–1

)

Proportion of PUFA (µg female

–1

)

0.0

0.2

0.4

0.6

0.8

1.0

1.2

1.4

1.6

1.8

2.0

Start

TW100

66DT

TW33D

T66

DT100

5LD25

50L

25LD75

3DT6

66LD33

S33LD

S66

TS33

AC10

66D

3DT

0.00

0.05

0.10

0.15

0.20

0.25

0.30

18:3n-3

20:4n-6

20:5n-3

22:6n-3

PUFA

Fig. 4. Temora longicornis. Fatty acid content of females at the

start of the experiment (start) and after 9 d in the 19 different

treatments specified in Table 3. (a) Total fatty acids (µg fe-

male

–1

), where the lighter shade indicates polyunsaturated

fatty acids (PUFA) and the dark bars the non-PUFAs and (b)

the proportion of specific fatty acids 18:3n-3, 20:4n-6, 20:5n-3

and 22:6n-3 (µg female

–1

) in the PUFA fraction of the female

Fig. 5. Temora longicornis. Correlations of (a) cumulative egg

production (EP, Day 3 to 9 of the experiment), (b) percent

hatching success (Day 9) and (c) naupliar production (NP, Day

3 to 9 of the experiment) against the maternal and ingested

fatty acids (available) and total ingested carbon (µg), giving

the best statistical fit (see Table 4). ALA: 18:3n-3 (µg);

EPA: 20:5n-3 (µg); DHA: 22:6n-3 (ng)

Mar Ecol Prog Ser 382: 139–150, 2009

and quality of the food (Jónasdóttir 1994). The eggs

can vary greatly in size and fatty acid composition

depending on the diet, resulting in great variation in

hatching success (Pond et al. 1996). Successful hatch-

ing often seems to have different requirements than

does egg production. This is well demonstrated when

EPR and hatching are plotted against one another,

where the general pattern seems to be that when EPR

is high, hatching success is high, while at lower EPR,

hatching can be quite variable (Jónasdóttir & Kiørboe

1996, Shin et al. 2003). This pattern is also evident in

our results (relationship not shown). In the same way, it

should not be assumed that somatic growth and repro-

ductive growth have the same requirements. This is

one of the main misconceptions in the literature when

discussing the nutritional needs for growth. The stud-

ies on nutritional requirements for somatic growth

indicate that sterols and protein might be of more

importance than specific fatty acids (Klein Breteler et

al. 2005, Koski et al. 2006).

In the present study, we used mixtures of mediocre

or poor diets to try to establish which fatty acids limit

copepod egg production and egg quality and, conse-

quently, naupliar production. The idea was to use non-

artificially treated food (instead of fatty acid supple-

ments) with different fatty acid profiles, reflecting

various food mixtures, to simulate different ratios of

some of the potentially important fatty acids. The 19

different phytoplankton mixtures gave a wide range in

concentrations and ratios of the 5 fatty acids (Fig. 2b,

Table 2) and resulted in very different proportions and

concentrations of the fatty acids ingested (Fig. 2a). In

agreement with some of the studies listed in Table 1,

our results show the importance of the fatty acid

20:5n-3 for egg production, together with carbon. The

fatty acid 20:5n-3 is one of the main membrane lipids

and a precursor for eicosanoids, e.g. hormone acti-

vities. However, the direct pathway for this fatty acid

in the copepod egg production process is not fully

understood.

Because of large differences in the ingestion rates of

the different diets (0.9 to 6 µg C female

–1

), Temora

longicornis may have been food limited in some of the

treatments, resulting in the observed quantitative

dependence. While carbon limitation could possibly be

avoided by providing higher initial food concentra-

tions, food selection and ingestion rates will always

control the carbon availability for growth. The inges-

tion rates and residence time of food in the gut are

dependant on the quality of the available food (Tirelli

& Mayzaud 2005). Egg production rates in the present

study were highest on TW, at about 20 eggs female

–1

, while the expected maximum for the same size

T. longicornis would be about 60 eggs female

–1

148

Variable Status F-to-remove F-to-enter p

var

Total egg production Total C In 13.7 – 0.002*

= 0.76, df = 16, p < 0.001) 18:3n-3 Out – 0.048 0.829

18:5n-3 Out – 0.624 0.441

20:4n-6 Out – 1.187 0.292

20:5n-3 In 9.4 – 0.007*

22:6n-3 Out – 3.338 0.086

Hatching success Total C Out – 0.991 0.335

(log

arcsine transformed) 18:3n-3 In 8.6 – 0.010*

= 0.65, df = 15, p = 0.001) 18:5n-3 In 4.3 – 0.057*

20:4n-6 Out – 0.468 0.504

20:5n-3 Out – 0.002 0.970

22:6n-3 In 17.5 – <0.001*

Total naupliar production Total C In 10.9 – 0.004*

= 0.88, df = 16, p < 0.001) 18:3n-3 Out – 0.371 0.551

18:5n-3 Out – 0.004 0.951

20:4n-6 Out – 0.086 0.773

20:5n-3 Out – 0.465 0.505

22:6n-3 In 38.3 – <0.001*

Table 4. Results from multiple, stepwise regression on egg production (eggs female

–1

), total naupliar production (nauplii female

–1

)

and hatching success (%) against the maternal and ingested 5 fatty acids and total ingested carbon. The stepwise process selects

only those variables (labelled ‘in’) that contribute to the best regression. Variables not in the regression are labelled ‘out’. R

: co-

efficient of determination of the multiple regression; df: degrees of freedom; p: significance value of the multiple regression; p

var

significance of the variable within the regression (asterisks indicate the most significant variables contributing to the model). For

each variable in the model, ‘F-to-remove’ is the F-statistic for its coefficient within the regression; for each variable not in the

model, ‘F-to-enter’ is the F-statistic that its coefficient would have if it were the next variable added in the regression

Jónasdóttir et al.: Temora reproduction and food quality

(S. H. Jónasdóttir unpubl. obs.). This indicates that

some additional food limitation for egg production

occurred even for the best diet tested.

Hatching success is an estimate of the quality of the

eggs produced and was strongly associated with the

ingestion and female contribution of the long-chain

PUFA 22:6n-3 and, to a lesser extent, the 18:3n-3 and

18:5n-3 fatty acids. The first 2 fatty acids have previ-

ously been positively related to hatching success

(Table 1). As for 20:5n-3, 22:6n-3 is metabolized to

form docosanoids, a group of potent hormones that

have been associated with neural functions in verte-

brates. The 18:5n-3 fatty acid, here found in HT and

TS, was not observed in females, and it is likely that it

was directly metabolized. A second possibility is that it

was elongated to 20:5n-3 and/or further desaturated to

22:6n-3. However, the ability to elongate and desatu-

rate 18:3n-3 to a 20 PUFA may be limited (Bell et al.

2007).

The combined coefficient of determination (Table 4)

shows that 35% of the variance in hatching was not

explained and indicates that some limiting variables

were not taken into account in the measurements and

subsequent model. These could, for example, be some

specific sterols (Crockett & Hassett 2005) that are

important for membrane function and are precursors

for many hormones, such as steroid hormones (Harri-

son 1990), and/or specific amino acids (Guisande et al.

2000). The total reproductive sum, i.e. the total nau-

pliar production, was very well explained (R

= 0.88) by

ingested carbon and the fatty acid 22:6n-3 — the 2

factors that best explained EPR and hatching, re-

spectively.

The contribution of maternal protein towards egg

production is reported for some larger copepod species

(Paraeucheta: Alonzo et al. 2000, 2001; Calanus: Rey-

Rassat et al. 2002), but using the potential female

reserves is, to our knowledge, a new approach in food-

quality studies. The present study shows that the

female selectively utilizes PUFAs (Fig. 4a) and espe-

cially 20:5n-3 (Fig. 4b). The female composition is oth-

erwise related to the intake of the dietary fatty acids. In

some treatments (e.g. 100% AC), the females were

totally depleted of PUFAs, while non-PUFA fatty acids

increased compared to values for the initial females

(Fig. 4a). The magnitude of this female contribution is,

however, not clear, and the importance of this contri-

bution would require complete stoichiometric balance,

where the fatty acid composition of eggs and faecal

pellets would specifically have to be known.

The approach used in the present study is promising.

Ultimately, however, the production and growth mea-

sured depend on the nutrient components fuelling the

underlying physiological processes. These can come

from the diet, but the maternal contribution through

stored reserves may play a crucial role when essential

nutrients are limiting. Therefore, to identify the under-

lying nutritional needs for reproduction, it is vital that

the maternal contribution is taken into account.

Observing a positive reproductive response when a

suspected essential component is totally absent from

the diet is no guarantee that that particular nutritional

component is unimportant, if the organism can retrieve

it from its own body reserves. Therefore, female condi-

tion and specific lipid accumulation is an important

factor in reproductive success.

The present study shows the importance of certain

long-chain fatty acids for successful reproduction in

copepods and underlines that >1 fatty acid is important

for the total reproductive process. The study also

underlines that the nutritional need for making a

viable egg is different from simply making an egg

itself. Therefore, meeting nutritional needs for success-

ful reproduction is a multi-tiered process. The ecologi-

cal implication of these results may be that during

phytoplankton blooms containing species rich in EPA

(diatoms), Temora longicornis may produce many eggs

with low or variable naupliar production. Later, phyto-

plankton succession of dinoflagellates high in DHA,

and often in 18:5n-3, may result in lower egg produc-

tion rates, but, due to higher hatching, the naupliar

production is higher, resulting in similar reproductive

output during the season.

It is apparent that one of the major shortcomings in

many food-quality studies, including some of our own,

is the black box approach, where correlations are

made directly between the food available and repro-

duction. It is clear that food selection (ingestion) plays

a critical role in availability of nutrient components

for growth, and to obtain meaningful correlations

between diet and growth, measurements of ingestion

rates are essential.

Acknowledgements. The present study was funded by the

Danish Research Agency Grant Number: 21-03-0487 to S.H.J.

We thank P. Christiansen for assistance with fatty acid ana-

lysis, Dr. E. Toby for discussions and advice on statistics, and

M. Koski and 4 anonymous reviewers for useful comments.

LITERATURE CITED

Alonzo F, Mayzaud P, Razouls S (2000) Egg-production

dynamics, biochemical composition and hatching success

of the subantarctic copepod Paraeuchaeta antarctica:

laboratory studies. Mar Ecol Prog Ser 205:219–227

Alonzo F, Mayzaud P, Razouls S (2001) Egg production and

energy storage in relation to feeding conditions in the

subantarctic calanoid copepod Drepanopus pectinatus: an

experimental study of reproductive strategy. Mar Ecol

Prog Ser 209:231–242

Arendt K, Jónasdóttir SH, Hansen P, Gärtner S (2005) Effects

149

➤

Mar Ecol Prog Ser 382: 139–150, 2009

of dietary fatty acids on the reproductive success of the

calanoid copepod Temora longicornis. Mar Biol 146:

513–530

Bell M, Dick J, Anderson T, Pond D (2007) Application of lipo-

some and stable isotope tracer techniques to study polyun-

saturated fatty acid biosynthesis in marine zooplankton.

J Plankton Res 29:417–422

Broglio E, Jónasdóttir SH, Calbet A, Jakobsen HH, Saiz E

(2003) Effect of heterotrophic versus autotrophic food on

feeding and reproduction of the calanoid copepod Acartia

tonsa: relationship with prey fatty acid composition. Aquat

Microb Ecol 31:267–278

Chesson J (1978) Measuring preference in selective preda-

tion. Ecology 59:211–215

Chesson J (1983) The estimation and analysis of preference

and its relationship to foraging models. Ecology 64:

1297–1304

Crockett EL, Hassett RP (2005) A cholesterol-enriched diet

enhances egg production and egg viability without alter-

ing cholesterol content of biological membranes in the

copepod Acartia hudsonica. Physiol Biochem Zool 78:

424–433

Dutz J, Koski M, Jónasdóttir SH (2008) Copepod reproduction

is unaffected by diatom aldehydes or lipid composition.

Limnol Oceanogr 53:225–235

Ederington M, McManus G, Harvey H (1995) Trophic transfer

of fatty acids, sterols, and triterpenoid alcohol between

bacteria, a ciliate, and the copepod Acartia tonsa. Limnol

Oceanogr 40:860–867

Evjemo J, Reitan K, Olsen Y (2003) Copepods as live food

organisms in the larval rearing of halibut larvae (Hip-

poglossus hippoglossus L.) with special emphasis on the

nutritional value. Aquaculture 227:191–210

Evjemo JO, Tokle N, Vadstein O, Olsen Y (2008) Effect of

essential dietary fatty acids on egg production and hatch-

ing success of the marine copepod Temora longicornis.

J Exp Mar Biol Ecol 365:31–37

Frost B (1972) Effects of size and concentration of food parti-

cles on the feeding behavior of the marine planktonic

copepod Calanus pacificus. Limnol Oceanogr 17:805–815

Guisande C, Riveiro I, Maneiro I (2000) Comparisons among

the amino acid composition of females, eggs and food to

determine the relative importance of food quantity and

food quality to copepod reproduction. Mar Ecol Prog Ser

202:135–142

Hansen PJ (1989) The red tide dinoflagellate Alexandrium

tamarense: effects on behaviour and growth of a tintinnid

ciliate. Mar Ecol Prog Ser 53:105–116

Harrison K (1990) The role of nutrition in maturation, repro-

duction and embryonic development of decapod crus-

taceans: a review. J Shellfish Res 9:1–28

Hassett R (2004) Supplementation of a diatom diet with cho-

lesterol can enhance copepod egg-production rates. Lim-

nol Oceanogr 49:488–494

Hassett R (2006) Physiological characteristics of lipid-rich ‘fat’

and lipid-poor ‘thin’ morphotypes of individual Calanus

finmarchicus C5 copepodites in nearshore Gulf of Maine.

Limnol Oceanogr 51:997–1003

Hazzard SE, Kleppel GS (2003) Egg production of the cope-

pod Acartia tonsa in Florida Bay: role of fatty acids in the

nutritional composition of the food environment. Mar Ecol

Prog Ser 252:199–206

Ianora A, Miralto A, Buttino I, Romano G, Poulet S (1999) First

evidence of some dinoflagellates reducing male copepod

fertilization capacity. Limnol Oceanogr 44:147–153

Jónasdóttir SH (1994) Effects of food quality on the reproduc-

tive success of Acartia tonsa and Acartia hudsonica: labo-

ratory observations. Mar Biol 121:67–81

Jónasdóttir SH, Kiørboe T (1996) Copepod recruitment and

food composition: Do diatoms affect hatching success?

Mar Biol 125:743–750

Jónasdóttir SH, Fields D, Pantoja S (1995) Copepod egg

production in Long Island Sound, USA, as a function of

the chemical composition of seston. Mar Ecol Prog Ser

119:87–98

Jónasdóttir SH, Gudfinsson H, Gislason A, Astthorsson O

(2002) Diet composition and quality for Calanus fin-

marchicus egg production and hatching success off south-

west Iceland. Mar Biol 140:1195–1206

Jónasdóttir SH, Trung N, Hansen F, Gärtner S (2005) Egg pro-

duction and hatching success in the calanoid copepods

Calanus helgolandicus and Calanus finmarchicus in the

North Sea from March to September 2001. J Plankton Res

27:1239–1259

Klein Breteler WCM, Schogt N, Baas M, Schouten S, Kraay G

(1999) Trophic upgrading of food quality by protozoans

enhancing copepod growth: role of essential lipids. Mar

Biol 135:191–198

Klein Breteler WCM, Schogt N, Rampen S (2005) Effect of

diatom nutrient limitation on copepod development: role

of essential lipids. Mar Ecol Prog Ser 291:125–133

Kleppel G, Burkart C (1995) Egg production and the nutri-

tional environment of Acartia tonsa: the role of food qual-

ity in copepod nutrition. ICES J Mar Sci 52:297–304

Kleppel G, Burkart C, Houchin L (1998) Nutrition and the reg-

ulation of egg production in the calanoid copepod Acartia

tonsa. Limnol Oceanogr 43:1000–1007

Koski M, Klein Breteler W, Schogt N, Gonzalez S, Jakobsen H

(2006) Life-stage-specific differences in exploitation of

food mixtures: diet mixing enhances copepod egg produc-

tion but not juvenile development. J Plankton Res 28:

919–936

Lee HW, Ban S, Ando Y, Ota T, Ikeda T (1999) Deleterious

effect of diatom diets on egg production and hatching suc-

cess in the marine copepod Pseudocalanus newmani.

Plankton Biol Ecol 46:104–112

Menden-Deuer S, Lessard E (2000) Carbon to volume rela-

tionships for dinoflagellates, diatoms, and other protist

plankton. Limnol Oceanogr 45:569–579

Peters J, Dutz J, Hagen W (2007) Role of essential fatty acids

on the reproductive success of the copepod Temora longi-

cornis in the North Sea. Mar Ecol Prog Ser 341: 153–163

Pond D, Harris R, Head R, Harbour D (1996) Environmental

and nutritional factors determining seasonal variability in

the fecundity and egg viability of Calanus helgolandicus

in coastal waters off Plymouth, UK. Mar Ecol Prog Ser

143:45–63

Rey-Rassat C, Irigoien X, Harris R, Head R, Carlotti F (2002)

Egg production rates of Calanus helgolandicus females

reared in the laboratory: variability due to present and

past feeding conditions. Mar Ecol Prog Ser 238:139–151

Shin K, Jang M, Jang P, Ju S, Lee T, Chang M (2003) Influ-

ence of food quality on egg production and viability of the

marine planktonic copepod Acartia omorii. Prog Oceanogr

57:265–277

Støttrup J, Jensen J (1990) Influence of algal diet on feeding

and egg-production of the calanoid copepod Acartia tonsa

Dana. J Exp Mar Biol Ecol 141:87–105

Tirelli V, Mayzaud P (2005) Relationship between functional

response and gut transit time in the calanoid copepod

Acartia clausi: role of food quantity and quality. J Plankton

Res 27:557–568

150

Editorial responsibility: William Peterson,

Newport, Oregon, USA

Submitted: October 17, 2008; Accepted: February 19, 2009

Proofs received from author(s): April 20, 2009

➤

➤➤

➤

Download
Save PDF to desktop

Email
Email completed PDF

Send for Signing
Email for others to sign

Print
Print document

NAME

Form 1: and hatching of Temora longicornis eggs (Inter ResearchScience Publisher)

View Audit Log
Print With Audit Log
Duplicate Document

Fillable Form 1: and hatching of Temora longicornis eggs (Inter Research Science Publisher)

Fill Online, Printable, Fillable, Blank Form 1: and hatching of Temora longicornis eggs (Inter Research Science Publisher) Form

Related forms

First 20 documents completely FREE!