Abstract
The planktonic larvae of many marine invertebrates must feed to develop to metamorphosis. The rate at which feeding larvae accumulate energy affects the amount of time they must spend in the plankton, which affects larval dispersal and mortality; it may also affect the amount of energy gained before metamorphosis, and thus limit growth or survivorship of early juveniles. Rates of energy acquisition are partly determined by the quantity of edible particles in the plankton. However, the plankton also contains many particles that are too large to be ingested. Prior studies suggest that high concentrations of such large inedible particles reduce larval feeding rates. This study examines whether the feeding rates of larvae of southern California echinoderms are reduced by lower, more frequently encountered concentrations of large inedible particles. Larvae of a holothuroid, two asteroids, and three echinoids were fed 6-µm beads alone or with large inedible beads at 25–500 inedible beads mL−1. Five of the six species showed reduced clearance rates on 6-µm beads when exposed to as few as 25 inedible beads mL−1. In similar experiments on an asteroid and an echinoid using natural large inedible particles (centric diatoms), larval clearance rates were reduced at 25 cells mL−1 and higher. Larval clearance rates were reduced by ~50% in treatments of 100 or 500 large inedible particles mL−1. These results suggest that in nature, rates of food acquisition by larvae may depend not only on the abundance of food particles, but also on the abundance of potentially interfering non-food particles.
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References
Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics Int 11:36–42
Burke RD (1981) Structure of the digestive tract of the pluteus larva of Dendraster excentricus (Echinodermata: Echinoida). Zoomorphology 98:209–225
Carriker MR (1986) Influence of suspended particles on biology of oyster larvae in estuaries. Am Malacol Bull Spec Ed 3:41–49
Cole M, Lindeque P, Halsband C, Galloway TS (2011) Microplastics as contaminants in the marine environment: a review. Mar Pollut Bull 62:2588–2597
Degerlund M, Eilertsen HC (2010) Main species characteristics of phytoplankton spring blooms in NE Atlantic and Arctic waters (68–80 N). Estuar Coasts 33:242–269
Dekshenieks MM, Donaghay PL, Sullivan JM, Rines JE, Osborn TR, Twardowski MS (2001) Temporal and spatial occurrence of thin phytoplankton layers in relation to physical processes. Mar Ecol Prog Ser 223:61–71
Durham WM, Stocker R (2012) Thin phytoplankton layers: characteristics, mechanisms, and consequences. Annu Rev Mar Sci 4:177–207
Fenaux L, Strathmann MF, Strathmann RR (1994) Five tests of food-limited growth of larvae in coastal waters by comparison of rates of development and form of echinoplutei. Limnol Oceanogr 39:84–98
Fotel FL, Jensen NJ, Wittrup L, Hansen BW (1999) In situ and laboratory growth by a population of blue mussel larvae (Mytilus edulis L.) from a Danish embayment, Knebel Vig. J Exp Mar Biol Ecol 233:213–230
Hansen BW (1999) Cohort growth of planktotrophic polychaete larvae—are they food limited? Mar Ecol Prog Ser 178:109–119
Hansen B, Hansen PJ, Nielsen TG (1991) Effects of large nongrazable particles on clearance and swimming behaviour of zooplankton. J Exp Mar Biol Ecol 152:257–269
Hart MW (1996) Variation in suspension feeding rates among larvae of some temperate, eastern Pacific echinoderms. Invertebr Biol 115:30–45
Hart MW, Strathmann RR (1994) Functional consequences of phenotypic plasticity in echinoid larvae. Biol Bull 186:291–299. doi:10.2307/1542275
Kato S, Tsurumaru S, Taga M, Yamane T, Shibata Y, Ohno K, Fujiwara A, Yamano K, Yoshikuni M (2009) Neuronal peptides induce oocyte maturation and gamete spawning of sea cucumber, Apostichopus japonicus. Dev Biol 326:169–176
McAlister J, Moran A (2013) Effects of variation in egg energy and exogenous food on larval development in congeneric sea urchins. Mar Ecol Prog Ser 490:155–167
Moorthi SD, Countway PD, Stauffer BA, Caron DA (2006) Use of quantitative real-time PCR to investigate the dynamics of the red tide dinoflagellate Lingulodinium polyedrum. Microb Ecol 52:136–150
Morgan SG (1995) Life and death in the plankton: larval mortality and adaptation. In: McEdward L (ed) Ecology of marine invertebrate larvae. CRC Press, Boca Raton, pp 279–321
Olenina I, Susana H, Edler L, Andersson A, Wasmund N, Busch S, Göbel J, Gromisz S, Huseby S, Huttunen M, Jaanus A, Kokkonen P, Ledaine I, Niemkiewcz E (2006) Biovolumes and size-classes of phytoplankton in the Baltic Sea. HELCOM Hels Balt Sea Environ Proc 106:144
Olson RR (1987) In situ culturing as a test of the larval starvation hypothesis for the crown-of-thoms starfish, Acanthaster planci. Limnol Oceanogr 32:895–904
Olson RR, Olson MH (1989) Food limitation of planktotrophic marine invertebrate larvae: does it control recruitment success? Annu Rev Ecol Syst 20:225–247
Pace ML, Bailiff MD (1987) Evaluation of a fluorescent microsphere technique for measuring grazing rates of phagotrophic microorganisms. Mar Ecol Prog Ser 40:185–193. doi:10.3354/meps040185
Paulay G, Boring L, Strathmann RR (1985) Food limited growth and development of larvae: experiments with natural sea water. J Exp Mar Biol Ecol 93:1–10
Pechenik JA (2006) Larval experience and latent effects—metamorphosis is not a new beginning. Integr Comp Biol 46:323–333
Pedersen TM, Almeda R, Fotel FL, Jakobsen HH, Mariani P, Hansen BW (2010) Larval growth in the dominant polychaete Polydora ciliata is food-limited in a eutrophic Danish estuary (Isefjord). Mar Ecol Prog Ser 407:99–110
Pernet B, Strathmann RR (2011) Opposed ciliary bands in the feeding larvae of sabellariid annelids. Biol Bull 220:186–198
Phillips NE (2002) Effects of nutrition-mediated larval condition on juvenile performance in a marine mussel. Ecology 83:2562–2574
Phillips NE, Shima JS (2006) Differential effects of suspended sediments on larval survival and settlement of New Zealand urchins Evechinus chloroticus and abalone Haliotis iris. Mar Ecol Prog Ser 314:149–158
Podolsky RD (1994) Temperature and water viscosity: physiological versus mechanical effects on suspension feeding. Science 265:100–103. doi:10.1126/science.265.5168.100
R Core Team (2016) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rassoulzadegan F, Fenaux L, Strathmann RR (1984) Effect of flavor and size on selection of food by suspension-feeding plutei. Limnol Oceanogr 29:357–361
Reid FM, Fuglister E, Jordan JB (1970) The ecology of the plankton off La Jolla, California, in the period April through September, 1967. Part 5. Phytoplankton taxonomy and standing crop. Bull Scripps Inst Oceanogr 17:51–66
Reitzel AM, Webb J, Arellano S (2004) Growth, development and condition of Dendraster excentricus (Eschscholtz) larvae reared on natural and laboratory diets. J Plankton Res 26:901–908
Rumrill SS (1990) Natural mortality of marine invertebrate larvae. Ophelia 32:163–198
Ryan JP, McManus MA, Sullivan JM (2010) Interacting physical, chemical and biological forcing of phytoplankton thin-layer variability in Monterey Bay, California. Cont Shelf Res 30:7–16
Shanks AL (2009) Pelagic larval duration and dispersal distance revisited. Biol Bull 216:373–385
Strathmann RR (1971) The feeding behavior of planktotrophic echinoderm larvae: mechanisms, regulation, and rates of suspension feeding. J Exp Mar Biol Ecol 6:109–160
Strathmann MF (1987a) Reproduction and development of marine invertebrates of the Northern Pacific Coast. University of Washington Press, Seattle
Strathmann RR (1987b) Larval feeding. In: Giese A (ed) Reproduction of marine invertebrates. Blackwell Scientific Publications, Palo Alto, pp 465–550
Thiyagarajan V, Hung OS, Chiu JMY, Wu RSS, Qian PY (2005) Growth and survival of juvenile barnacle Balanus amphitrite: interactive effects of cyprid energy reserve and habitat. Mar Ecol Prog Ser 299:229–237
Torres G, Giménez L, Pettersen AK, Bue M, Burrows MT, Jenkins SR (2016) Persistent and context-dependent effects of the larval feeding environment on post-metamorphic performance through the adult stage. Mar Ecol Prog Ser 545:147–160
Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice Hall, Upper Saddle River, p 187
Acknowledgements
We thank Y. Ralph (CSULB) and J. Ross (South Coast Bio-Marine) for collection of adult echinoderms, Drs. D. Pace and D. Vaughn for advice on experimental design, and V. Oria, C. Payne, R. Rangel, C. Sojka, A. Von Tungeln, and A. Yee for help performing experiments. Dr. C.J. Lowe gave us helpful advice on the induction of spawning in holothuroids, and Dr. B. Allen on statistical analyses. This material is based on work supported by the National Science Foundation under Grant Nos. OCE-1060801 and DEB-1257355 to BP. Additional support was provided by awards to DL from CSU COAST, the Southern California Tuna Club, the Los Angeles Rod and Reel Club, and a Grant in Aid of Research from the Society for Integrative and Comparative Biology.
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Animals used in the study were collected under the authority of a scientific collecting permit issued to Bruno Pernet, and treated according to all applicable national and institutional guidelines.
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Lizárraga, D., Danihel, A. & Pernet, B. Low concentrations of large inedible particles reduce feeding rates of echinoderm larvae. Mar Biol 164, 102 (2017). https://doi.org/10.1007/s00227-017-3134-9
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DOI: https://doi.org/10.1007/s00227-017-3134-9