JOURNAL OF PLANKTON RESEARCH j VOLUME 34 j NUMBER 7 j PAGES 642–645 j 2012

SHORT COMMUNICATION

A weight- and temperature-dependent model of respiration in flexuosus (Crustacea, ) Downloaded from https://academic.oup.com/plankt/article/34/7/642/1465303 by guest on 01 October 2021

MARTIN OGONOWSKI*, KRISTOFFER ANDERSSON AND STURE HANSSON DEPARTMENT OF SYSTEMS ECOLOGY, STOCKHOLM UNIVERSITY, SE-106 91 STOCKHOLM, SWEDEN

*CORRESPONDING AUTHOR: [email protected]

Received February 1, 2012; accepted in principle March 15, 2012; accepted for publication March 20, 2012

Corresponding editor: Marja Koski

The mysid shrimp Praunus flexuosus is common in littoral habitats in the Baltic Sea and other marine areas, but its bioenergetic characteristics have not been studied. We present the first model of its routine respiration rate as a function of size and a natural temperature range. The model explained 87% of the variance in respir- ation, indicating that it could be useful in a larger modeling framework. Specific respiration rates and temperature dependence were consistent with previous reports for this and other littoral mysids at low-to-moderate temperatures. Respiration at higher temperatures was lower, indicating that previous reports may have been biased by residual SDA (specific dynamic action) effects. Increased res- piration due to SDA was detectable over a longer period than previously reported, 30 h.

KEYWORDS: respiration; Praunus flexuosus; fasting; specific dynamic action; routine metabolism

compared with what are available for fish (Hanson INTRODUCTION et al., 1997). One important component of such models Mysids are a significant component of aquatic ecosys- is respiration, since it constitutes a major component in tems and are important links between different trophic the energy budget. Respiration can, however, be some- levels (Mauchline, 1980). They are important zooplank- what problematic to describe with a model, since it is ton predators (Rudstam et al., 1986) as well as a food influenced by many factors, both biotic (e.g. size, repro- source for many of fish (Arndt and Jansen, duction, ontogeny) and abiotic (e.g. temperature, salin- 1986). To understand their role in the food web, we ity, season). Among these, temperature and size are need quantitative analyses of their food consumption regarded as being particularly influential (Winberg, and bioenergetics models can provide such estimates. 1956). Although there are some studies that have There are some bioenergetics models published for reported on mysid respiration in the past (Vlasblom and mysids (Rudstam, 1989; Gorokhova, 1998), but few Elgershuizen, 1977; Laughlin and Linden, 1983; Weisse

doi:10.1093/plankt/fbs030, available online at www.plankt.oxfordjournals.org. Advance Access publication April 16, 2012 # The Author 2012. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected] M. OGONOWSKI ET AL. j PRAUNUS RESPIRATION AND EFFECTS OF FASTING

and Rudstam, 1989), few have produced an adequate Table I: Summary of the experimental design model of respiration that could be incorporated in a showing the four different temperature larger modeling framework. treatments (Temp, 8C), number of mysids (n), In this study, we present a weight- and temperature- number of controls (c), average specific dependent respiration model for the common littoral respiration (mgO dw21 h21), dry weight of mysid Praunus flexuosus, based on experiments that 2 covered substantial temperature and size ranges (3–198C mysids (DW, mg) and duration of the and 2–9 mg dry weight). To our knowledge, this is the experiments (h) first model relating the effects of temperature and weight Respiration 21 21 on oxygen consumption in P. fl e x u o s u s . Temp (8C) nc(mgO2 dw h ) DW (mg) Duration (h)

Mysids were collected with a hand net (300 mm 18.7 + 0.6 17 4 2.3 + 0.44 4.9 + 1.6 30 Downloaded from https://academic.oup.com/plankt/article/34/7/642/1465303 by guest on 01 October 2021 mesh) in a bladder wrack () belt in the 16.4 + 0.5 16 4 1.6 + 0.45 5.9 + 1.5 29 0 0 8.2 + 0.6 17 4 0.8 + 0.15 6.2 + 1.1 37 northern Baltic Proper (58849 N, 17838 E), where 3.1 + 0.3 17 4 0.7 + 0.18 6.8 + 1.5 35 surface temperature ranged 10–128C. Specimens for All values are expressed as the average + standard deviation when experiments [immature males, immature females and applicable. undifferentiated juveniles (88% of sample)] were cap- tured between 21 September and 9 October 2009 and acclimated to the experimental temperature by keeping cone was put on the top of every bottle. Although all them in a constant temperature room in 10-L buckets experiments were conducted in darkness, the black with aerated, micropore (0.22 mm) filtered sea water plastic cover was applied to minimize any stress on the (salinity, 6.8 psu). Mysids were first starved for 17–27 h that might have arisen from temporary light depending on the temperature treatment as gut evacu- when measurements were taken. To avoid effects of ation time is negatively related to temperature, making hypoxic stress, we did not allow any experimental unit sure that all potential food in the gut had been pro- to fall below 65% air saturation. After each experiment, cessed. Gut residence times in Mysis relicta are ,6h at the animals were dried for 48 h at 608C and weighed 5–158C(Chipps, 1998) and 4–12 h for integer to the nearest milligram. Oxygen concentrations were fed Artemia salina nauplii at 158C(Fockedey, 2005) and measured with a Fiber-optic oxygen mini-sensor (Fibox we have assumed similar values for P. flexuosus.To 3 PreSens Precision sensing GmbH Regensburg, further standardize conditions, following starvation, the Germany). Prior to the experiments, sensor spots were mysids were allowed to feed ad libitum on newly hatched attached with silica glue to the inside of the bottles, and A. salina nauplii for 6 h before the start of the experi- during the experiments, oxygen concentration was mea- ments. This was done in order to more closely reflect sured from the outside of the bottle using a DP-PSt3 natural conditions since mysids normally feed several fiber-optic probe. The temperature was measured separ- times per day (Tattersall and Tattersall, 1951; Garnacho ately, in a water filled bottle, by a Fibox 3 unit with a et al., 2001). However, as there are metabolic costs asso- PT 1000 Sensor. 21 21 ciated with the processing of food (specific dynamic Individual respiration y (mgO2 ind. h ) at time t action, SDA), we only used respiration rates at the end was calculated by fitting an exponential function of the of the experiments to derive model parameters for form: routine respiration, i.e. when SDA effects were assumed bt to be negligible. yðtÞ ¼ ae ð1Þ A total of four experiments with different tempera- tures (3, 8, 16 and 198C, Table I) were conducted. where a is the intercept, b a constant and t the time Oxygen concentration in the incubation water (see (h).Taking the first derivative of that function yielded below) was measured at 1–1.5 h intervals over a weight-specific routine respiration at time t expressed as: period of 30 h. All experiments were run in a con- stant temperature room. Single mysids were placed in ab ebt V ¼ ð2Þ 330-mL plastic bottles wrapped in black light- ðtÞ w impermeable plastic. In addition to these bottles, there were four bottles in each experiment that contained no where w is the dry weight (mg) (r2 of exponential model mysid and were used to control for background oxygen fit: 25–75% interquartile range ¼ 0.94–0.99, min ¼ consumption. The bottles were filled with filtered sea 0.71, max ¼ 0.99). All controls (bottles without mysids) water and a watch glass was slid on the top of the bottle displayed a low, but linear, decrease in oxygen concen- in order to expel any air bubbles. Finally, a black plastic tration over time. To account for this, background

643 JOURNAL OF PLANKTON RESEARCH j VOLUME 34 j NUMBER 7 j PAGES 642–645 j 2012

3°C 4 1:1 line 3 2 1

8°C

) 4 –1 ) –1

h 3 h

–1 2 2 O

dw

1 2 O 16°C

Predicted respiration (µg 4 R (µg 3

2 Downloaded from https://academic.oup.com/plankt/article/34/7/642/1465303 by guest on 01 October 2021 1

19°C 4 0 5 10 15 20 3 2 0 5 10 15 20 1 Observed respiration 10 20 30 –1 (µg O2 h ) Time (h) 21 21 Fig. 1. Observed versus predicted respiration values (mgO2 ind. h ). ¼ 2 ¼ Fig. 2. Mean (circles) + standard deviation (whiskers) weight-specific Dashed line represents a theoretical 1:1 relationship. n 67, r 0.87. 21 21  respiration (mgO2 ind. h ) over the course of the 30-h incubation at four temperatures (3, 8, 16 and 198C). n ¼ 17 in all cases except at 168C where n ¼ 16. respiration (estimated by the slope of a linear regression) was substracted from individual mysid respiration values. All statistical calculations were made in R et al.(Garnacho et al., 2001) studied seasonal effect on v. 2.13.0 R (R development core team 2011). Praunus respiration and reported values of 0.97– 21 21 We used the non-linear least squares “nls” function in 1.82 mgO2 mg dw h at 58CinFebruaryandan 21 21 the “nlme” package (Pinheiro et al., 2011) to find the average 3.0 O2 mg dw h at 208C in August. In parameters for our model. Routine metabolic rate R (i.e Garnacho’s study, the slightly higher values of respiration standard respiration including the swimming activity of at the highest temperatures can be explained by the fact 21 21 mysids, mgO2 ind. h ) was modeled as a function of that SDA was included in the measured respiration. In temperature T (8C) and mysid weight w (mg dry weight) Vlasblom and Elgerhuizen’s case, mysids were starved as: for 24 h before the experiments. The feeding history of these mysids was, however, unknown as it is in most R ¼ awbedT ð3Þ cases when field caught animals are used and it is prob- able that at least some of the respiration could be where a, b and d are the constants (estimate + 95% ascribed to residual SDA effects. In this study, we moni- CI: a ¼ 1.014 + 0.295, b ¼ 0.597 + 0.135 and d ¼ tored the effect of fasting on respiration by frequent mea- 0.072 + 0.008). Model residuals plotted against tem- surements over a period of 30 h. During this time, perature and weight were normally distributed without respiration decreased more or less constantly without any clear patterns, and the observed versus the pre- reaching a clearly defined level (Fig. 2). This demon- dicted values were significantly related to each other in- strates that the metabolic costs of processing food may dicating a good model fit (Fig. 1, ANOVA, F1,65¼ 453, extend over a considerable time in mysids and that our P , 0.0001, r2 ¼ 0.87). respiration values actually also may be slight overestima- The respiration values predicted by the model are in tions because of remaining SDA. agreement with previous reports on mysid respiration, al- Chipps and Bennett (Chipps and Bennett, 2002) though our values tend to be somewhat lower, especially demonstrated that even small perturbations of respira- at higher temperatures. Vlasblom and Elgershuizen tory parameters become influential on bioenergetic (Vlasblom and Elgershuizen, 1977) reported the respir- model performance which makes the accurate estima- 21 21 ation values from 0.67 to 3.11 mgO2 mg dw h at tion of basal metabolic rates important. Despite this 5–208CforP. flexuosus (recalculated from mLO2 mg wet fact, many studies reporting respiration assume that weight21 h21, using dw-ww relationship from standard or routine metabolism has been reached at the Morgan, 1976) compared with this study (0.71– onset of the experiments. In a study on N. integer,a 21 21 2.10 mgO2 mg dw h for a 6 mg mysid). Garnacho sympatric, littoral species with similar temperature

644 M. OGONOWSKI ET AL. j PRAUNUS RESPIRATION AND EFFECTS OF FASTING

preferences as P. flexuosus, Weisse and Rudstam (Weisse REFERENCES and Rudstam, 1989) assumed SDA effects to be gone Arndt, E. A. and Jansen, W. (1986) (Leach) in the chain after 6 h as weight-specific respiration did not differ sig- of Boddens south of Darss Zingst (Western Baltic)—ecophysiology nificantly after 6 versus 30 h. However, it is implicit that and population-dynamics. Ophelia Suppl., 4, 1–15. there in fact was an effect of SDA on respiration in Chipps, S. R. (1998) Temperature-dependent consumption and Weisse & Rudstam’s study, since the temperature de- gut-residence time in the opossum shrimp Mysis relicta. J. Plankton Res. pendence (Q10) on respiration was twice as high at 6 h , 20, 2401–2411. compared with 30 h (1.7–1.8 at 6 h versus 3.1–3.3 at Chipps, S. R. and Bennett, D. H. (2002) Evaluation of a Mysis bio- 30 h), indicating respiration rates above routine metab- energetics model. J. Plankton Res., 24, 77–82. olism for at least 6 h post-feeding. The Q10 coefficient Fockedey, N. (2005) Diet and growth of Neomysis integer (Leach, 1814) (10/T22 T1) (Crustacea, Mysidacea). PhD-thesis, University of Ghent, Belgium.

[Q10 ¼ (R2 2 R1) ] reported here [Q10¼ 1.62 Downloaded from https://academic.oup.com/plankt/article/34/7/642/1465303 by guest on 01 October 2021 (8, 198C)] was similar to that reported by Weisse and Garnacho, E., Peck, L. S. and Tyler, P. A. (2001) Effects of copper ex- Rudstam (Weisse and Rudstam, 1989) for N. integer posure on the metabolism of the mysid Praunus flexuosus. J. Exp. Mar. Biol. Ecol., 265, 181–201. [1.7–1.8 (6, 168C)] after 30 h of fasting and Garnacho Gorokhova, E. (1998) Exploring and modelling the growth dynamics et al.(Garnacho et al., 2001) for P. flexuosus [1.76 (10, of Mysis mixta. Ecol. Model., 110, 45–54. 208C)] that had an experimental setup similar to ours Hanson, P. C., Johnson, T. B., Schindler, D. E. et al. (1997) bioener- but included SDA in the routine metabolism. Thus, our getics 3.0. University of Wisconsin Sea Grant Institute, Madison, WI. results indicate that post-prandial effects on respiration Laughlin, R. and Linden, O. (1983) Oil pollution and Baltic mysids: should be taken more carefully into consideration when Acute and chronic effects of the water soluble fractions of light fuel estimating basal metabolic rates in mysids. Despite the oil on the mysid shrimp Neomysis integer. Mar. Ecol. Prog. Ser., 12, fact that we did not observe respiration to level out to a 29–41. constant rate after 30 h of starvation, we did obtain Mauchline, J. (1980) The biology of mysids and euphausiids. Part one, lower rates of oxygen consumption than have previously the biology of mysids. In Blaxter, J. H. S., Russell, F. S. and Yonge, been reported for P. flexuosus, indicating that these values M. (eds), Advances in Marine Biology, Vol. 18. Academic Press, London, pp. 1–369. better represent routine metabolism in this species in Morgan, M. D. (1976) Life history and annual net secondary product- comparison with previous reports. Thus, we also believe ivity of Mysis relicta (Love´n) in west central Lake Michigan. MSc that the weight- and temperature-dependent model of thesis, University of Milwaukee. respiration in this study could be used successfully in a Pinheiro, J., Bates, D., Debroy, S. et al. (2011) nlme: Linear and Nonlinear larger ecological modeling framework. Mixed Effects Models. R package version 3.1-101. Rudstam, L. G. (1989) A bioenergetic model for Mysis growth and consumption applied to a Baltic population of Mysis mixta. J. Plankton Res., 11, 971–983. ACKNOWLEDGEMENTS Rudstam, L. G., Hansson, S. and Larsson, U. (1986) Abundance, species composition and production of mysid shrimps in a coastal We would like to thank PreSens Precision Sensing, area of the northern Baltic proper. Ophelia Suppl., 4, 225–238. GmbH, Regensburg, Germany, for the use of the Tattersall, W. M. and Tattersall, O. S. (1951) The British Mysidacea. optical oxygen probe and the staff at Asko¨ field station Bartholomew Press, London. for help during the experimental setup. We would also Vlasblom, A. G. and Elgershuizen, J. H. B. W. (1977) Survival and like to thank two anonymous reviewers for valuable oxygen consumption of Praunus flexuosus and Neomysis integer, and em- comments on the manuscript. bryonic development of the latter species, in different temperature and chlorinity combinations. Neth. J. Sea Res., 11, 305–315. Weisse, T. and Rudstam, L. G. (1989) Excretion and respiration rates of Neomysis integer (Mysidacea): Effects of temperature, sex and star- FUNDING vation. Hydrobiologia, 178, 253–258. Winberg, G. G. (1956) Rate of Metabolism and Food Requirements of . This study was supported by Stockholm University, Belorussian State University, Minsk (Translated from Russian by Department of Systems Ecology, Sweden. Fish. Res. Bd Can. Transl. Ser. No. 194, 1960).

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