Abstract
Upon settlement after a pelagic larval phase, brown shrimp Crangon crangon depend on intertidal flats. During low as well as high tide the young brown shrimp play roles as predators of meiofauna and as prey for fish and birds. Unlike the biology of the commercially important adults, knowledge on these juveniles remains sketchy. Here we provide an analysis of 35 years (1984–2018) of brown shrimp monitoring in May–June on intertidal flats in the westernmost Dutch Wadden Sea. Intertidal shrimp densities were sampled bi-weekly at three stations during low tide, using sampling corers. We show that over this 35-year period the appearance of shrimp on mudflats advanced by 12 days (− 0.34 days yr−1). Simultaneously, densities on 7 May increased by more than 2.4 times, from 28 shrimp m−2 in 1984 to 69 shrimp m−2 in 2018. Across years, mean shrimp length decreased from 12.6 to 10.7 mm, but length in early May did not change. The advancement in settlement and the increasing shrimp densities correlated with increases in the seawater temperatures in April more than during earlier times of the year. We propose four interpretations of these changes: (1) shrimp settle on the mudflat when they reach a certain ‘threshold’ length, (2) settlement of shrimp is controlled by a critical period of ‘threshold’ temperature sensitivity, (3) timing of shrimp settlement is a response to food availability on mudflats or (4) a direct response to inferred predation pressure. The different interpretations will lead to different scenarios of change in a warming world.
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Data availability
The datasets generated during and/or analyzed during the current study will become available in the Zenodo Repository (http://doi.org/10.5281/zenodo.4792217).
References
Al-Adhub AHY, Naylor E (1975) Emergence rhythms and tidal migrations in the brown shrimp Crangon crangon (l.). J Mar Biol Assoc UK 55:801–810. https://doi.org/10.1017/S0025315400017720
Andresen H, van der Meer J (2010) Brown shrimp (Crangon crangon, L.) functional response to density of different sized juvenile bivalves Macoma balthica (L.). J Exp Mar Biol Ecol 390:31–38. https://doi.org/10.1016/j.jembe.2010.04.027
Beukema JJ (1992) Dynamics of juvenile shrimp Crangon crangon in a tidal-flat nursery of the Wadden Sea after mild and cold winter. Mar Ecol Prog Ser 83:157–165
Beukema JJ, Cadée GC (1997) Local differences in macrozoobenthic response to enhanced food supply caused by mild eutrophication in a Wadden Sea area: food is only locally a limiting factor. Limnol Oceanogr 42:1424–1435
Beukema JJ, Dekker R (2005) Decline of recruitment success in cockles and other bivalves in the Wadden Sea: possible role of climate change, predation on postlarvae and fisheries. Mar Ecol Prog Ser 287:149–167. https://doi.org/10.3354/meps287149
Beukema JJ, Dekker R (2014) Variability in predator abundance links winter temperatures and bivalve recruitment: correlative evidence from long-term data in a tidal flat. Mar Ecol Prog Ser 513:1–15. https://doi.org/10.3354/meps10978
Boddeke R (1976) The seasonal migration of the brown shrimp Crangon crangon. Neth J Sea Res 10:103–130. https://doi.org/10.1016/0077-7579(76)90006-5
Boddeke R (1982) The occurrence of winter and summer eggs in the brown shrimp (Crangon crangon) and the pattern of recruitment. Neth J Sea Res 162:151–162. https://doi.org/10.1016/0077-7579(82)90026-6
Boddeke R (1996) Changes in the brown shrimp (Crangon crangon L.) population off the Dutch coast in relation to fisheries and phosphate discharge. ICES J Mar Sci 53:995–1002. https://doi.org/10.1006/jmsc.1996.0124
Boddeke R, Becker R (1979) A quantitative study of the fluctuations of the stock of brown shrimps along the coast of the Netherlands. Rapp P-v R é Un Cons Int Explor Mer 175:253–258
Boddeke R, Hagel P (1991) Eutrophication on the North Sea continental zone, a blessing in disguise. ICES Council Meeting Papers, ICES CM 1991/E:7
Boddeke R, Driessen G, Doesburg W, Ramaekers G (1985) Settlement and growth of brown shrimp (Crangon crangon) in a coastal area. IJmuiden, The Netherlands: International Council for the Exploration of the Sea Conference Meeting 1985/K 16:8
Broekema MMM (1941) Seasonal movements and the osmotic behaviour of the shrimp, Crangon crangon L. Arch Néerl Zool 6:1–102
Burnham KP, Anderson DR (2002) Model selection and multimodel inference. Springer, New York
Campos J (2009) The eco-geography of the brown shrimp Crangon crangon in Europe. Disstertation, Vrije Universiteit, Amsterdam, The Netherlands, p 171
Campos J, van der Veer HW (2008) Autecology of Crangon crangon (L.) with an emphasis on latitudinal trends. Oceanogr Mar Biol 46:65–104. https://doi.org/10.1201/9781420065756.ch3
Christianen MJA, Middelburg JJ, Holthuijsen SJ et al (2017) Benthic primary producers are key to sustain the Wadden Sea food web: stable carbon isotope analysis at landscape scale. Ecology 98:1498–1512. https://doi.org/10.1002/ecy.1837
Christy JH, Morgan SG (1998) Estuarine immigration by crab postlarvae: mechanisms, reliability and adaptive significance. Mar Ecol Prog Ser 174:51–65. https://doi.org/10.3354/meps174051
Criales MM, Anger K (1986) Experimental studies on the larval development of the shrimps Crangon crangon and C. allmanni. Helg Meeresunters 40:241–265. https://doi.org/10.1007/BF01983735
Daewel U, Schrum C, Temming A (2011) Towards a more complete understanding of the life cycle of brown shrimp (Crangon crangon): modelling passive larvae and juvenile transport in combination with physically forced vertical juvenile migration. Fish Oceanogr 20:479–496
Dapper R, van der Veer HW (1981) Onderzoek naar de ruimtelijke variatie van de bodemsamenstelling op het Balgzand. Internal report no. 1981-9. Royal Netherlands Institute for Sea Research, Texel
del Norte Campos AGC, Temming A (1994) Daily activity, feeding and rations in gobies and brown shrimp in the northern Wadden Sea. Mar Ecol Prog Ser 115:41–54. https://doi.org/10.3354/meps115041
Gibson RN, Yin MC, Robb L (1995) The behavioural basis of predator-prey size relationships between shrimp (Crangon crangon) and juvenile plaice (Pleuronectes platessa). J Mar Biol Assoc UK 75:337–349. https://doi.org/10.1017/S002531540001821X
Hartsuyker L (1966) Daily tidal migrations of the shrimp, Crangon crangon L. Neth J Sea Res 3:52–67. https://doi.org/10.1016/0077-7579(66)90006-8
Hufnagl M, Temming A (2011) Growth in the brown shrimp Crangon crangon. II. meta-analysis and modelling. Mar Ecol Prog Ser 435:155–172. https://doi.org/10.3354/meps09224
Hufnagl M, Temming A, Pohlmann T (2014) The missing link: tidal-influenced activity a likely candidate to close the migration triangle in brown shrimp Crangon crangon (Crustacea, Decapoda). Fish Oceanogr 23:242–257. https://doi.org/10.1111/fog.12059
Hünerlage K, Siegel V, Saborowski R (2019) Reproduction and recruitment of the brown shrimp Crangon crangon in the inner German Bight (North Sea): An interannual study and critical reappraisal. Fish Oceanogr 28:708–722. https://doi.org/10.1111/fog.12453
ICES (2015) Report of the Working Group on Crangon Fisheries and Life History (WGCRAN), 18–20 May 2015, Ijmuiden, the Netherlands. ICES CM 2015/SSGEPD:07
Janssen GM, Kuipers BR (1980) On tidal migration in the shrimp Crangon crangon. Neth J Sea Res 14:339–348. https://doi.org/10.1016/0077-7579(80)90007-1
Jensen KT, Jensen JN (1985) The importance of some epibenthic predators on the density of juvenile benthic macrofauna in the Danish Wadden Sea. J Exp Mar Biol Ecol 89:157–174
Jouta J, de Goeij P, Lok T et al (2018) Unexpected dietary preferences of Eurasian spoonbills in the Dutch Wadden Sea: spoonbills mainly feed on small fish not shrimp. J Ornithol 159:839–849. https://doi.org/10.1007/s10336-018-1551-2
Kuipers BR, Dapper R (1984) Nursery function of Wadden Sea tidal flats for the brown shrimp Crangon crangon. Mar Ecol Prog Ser 17:171–181
Kuipers BR, Dapper R (1981) Production of Crangon crangon in the tidal zone of the Dutch Wadden Sea. Neth J Sea Res 15:33–53
Lazaridis E (2014) lunar: Lunar phase & distance, seasons and other environmental factors (Version 0.1-04). Available from http://statistics.lazaridis.eu
Lloyd AJ, Yonge CM (1947) The biology of Crangon vulgaris in the Bristol Channel and Severn Estuary. J Mar Biol Assoc UK 26:626–661
Marchand J (1981) Observations sur l’écologie de Crangon crangon (Linné) et Palaemon longirostris (H. Milne Edward) (Crustacea, Decapoda, Natantia). Estuaire interne de la Loire (France). Vie Milieu 31:83–92
Mathot KJ, Piersma T, Elner RW (2019) Shorebirds as integrators and indicators of mudflat ecology. In: Beninger PG (ed) Mudflat ecology. Springer-Nature, Cham, pp 309–338
Mense DJ, Posey MH, West T, Kincheloe K (1995) Settlement of brachyuran postlarvae along the North Carolina coast. Bull Mar Sci 57:793–806
Muggeo VMR (2008) Segmented: an R package to fit regression models with broken-line relationships. R News 8(1):20–25
Nehls G, Tiedemann R (1993) What determines the densities of feeding birds on tidal flats? A case study on dunlin Calidris alpina in the Wadden Sea. Neth J Sea Res 31:375–384. https://doi.org/10.1016/0077-7579(93)90054-V
Oh CW, Hartnoll RG, Nash RDM (1999) Population dynamics of the common shrimp, Crangon crangon (L.), in Port Erin Bay, Isle of Man, Irish Sea. ICES J Mar Sci 56:718–733. https://doi.org/10.1006/jmsc.1999.0501
Paschke KA, Gebauer P, Buchholz F, Anger K (2004) Seasonal variation in starvation resistance of early larval North Sea shrimp Crangon crangon (Decapoda: Crangonidae). Mar Ecol Prog Ser 279:183–191
Philippart CJM, van Aken HM, Beukema JJ et al (2003) Climate-related changes in recruitment of the bivalve Macoma balthica. Limnol Oceanogr 48:2171–2185. https://doi.org/10.4319/lo.2003.48.6.2171
Philippart CJM, Beukema JJ, Cadée GC et al (2007) Impacts of nutrient reduction on coastal communities. Ecosystems 10:95–118. https://doi.org/10.1007/s10021-006-9006-7
Piersma T, de Goeij P, Tulp I (1993) An evaluation of intertidal feeding habitats from a shorebird perspective: towards comparisons between temperate and tropical mudflats. Neth J Sea Res 31:503–512. https://doi.org/10.1016/0077-7579(93)90062-W
Pihl L, Rosenberg R (1984) Food selection and consumption of the shrimp Crangon crangon in some shallow marine areas in Western Sweden. Mar Ecol Prog Ser 15:159–168. https://doi.org/10.3354/meps015159
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
Rakhimberdiev E, Duijns S, Karagicheva J et al (2018) Fuelling conditions at staging sites can mitigate Arctic warming effects in a migratory bird. Nat Commun 9:1–10. https://doi.org/10.1038/s41467-018-06673-5
Rochanaburanon T, Williamson DI (1976) Laboratory survival of larvae of Palaemon elegans Rathke and other Caridean shrimps in relation to their distribution and ecology. Estuar Coast Mar Sci 4:83–91
Siegel V, Damm U, Neudecker T (2008) Sex-ratio, seasonality and long-term variation in maturation and spawning of the brown shrimp Crangon crangon (L.) in the German Bight (North Sea). Helgol Mar Res 62:339–349. https://doi.org/10.1007/s10152-008-0121-z
Smaldon G (1979) British Coastal Shrimps and Prawns. Keys and notes for the Identification of the Species. Synopses of the British Fauna. Academic Press, London
Spaargaren DH (2000) Seasonal and annual variations in the catches of Crangon crangon (L., 1758) (Decapoda, Natantia) near the coast of Texel, The Netherlands. Crustaceana 73:547–563. https://doi.org/10.1163/156854000504651
Temming A, Damm U (2002) Life cycle of Crangon crangon in the North Sea: a simulation of the timing of recruitment as a function of the seasonal temperature signal. Fish Oceanogr 11:45–58. https://doi.org/10.1046/j.1365-2419.2002.00184.x
Temming A, Günther C, Rückert C, Hufnagl M (2017) Understanding the life cycle of North Sea brown shrimp Crangon crangon: a simulation model approach. Mar Ecol Prog Ser 584:119–143. https://doi.org/10.3354/meps12325
Tielmann M, Reiser S, Hufnagl M, Herrmann J-P, Eckardt A, Temming A (2015) Hydrostatic pressure affects selective tidal stream transport in the North Sea brown shrimp (Crangon crangon). J Exp Biol 218:3241–3248. https://doi.org/10.1242/jeb.125773
Tiews K (1970) Synopsis of biological data on the common shrimp Crangon crangon. FAO Fish Rep 57:1166–1224
Tulp I, Chen C, Haslob H et al (2016) Annual brown shrimp (Crangon crangon) biomass production in Northwestern Europe contrasted to annual landings. ICES J Mar Sci 73:141. https://doi.org/10.1093/icesjms/fsw141
Tulp I, Glorius S, Rippen A et al (2020) Dose-response relationship between shrimp trawl fishery and the macrobenthic fauna community in the coastal zone and Wadden Sea. J Sea Res 156:1–13. https://doi.org/10.1016/j.seares.2019.101829
van Aken H (2008) Variability of the water temperature in the western Wadden Sea on tidal to centennial time scales. J Sea Res 60:227–234. https://doi.org/10.1016/j.seares.2008.09.001
van de Kam J, Ens B, Piersma T, Zwarts L (2004) Shorebirds: an illustrated behavioural ecology. KNNV Publishers, Utrecht
van der Baan S (1975) Migration of Crangon crangon in surface waters near the “Texel” lightship. Neth J Sea Res 9:287–296. https://doi.org/10.1016/0077-7579(75)90004-6
van der Heide T, Tielens E, van der Zee EM, Weerman EJ, Holthuijsen S, Eriksson BK, Piersma T, van de Koppel J, Olff H (2014) Predation and habitat modification synergistically interact to control bivalve recruitment on intertidal mudflats. Biol Cons 172:163–169. https://doi.org/10.1016/j.biocon.2014.02.036
van der Veer HW, Bergman MJN (1987) Predation by crustaceans on a newly settled 0-group plaice Pleuronectes platessa population in the Western Wadden Sea. Mar Ecol Prog Ser 35:203–215. https://doi.org/10.3354/meps035203
van der Veer HW, Feller RJ, Weber A, Witte JI (1998) Importance of predation by crustaceans upon bivalve spat in the intertidal zone of the Dutch Wadden Sea as revealed by immunological assays of gut contents. J Exp Mar Biol Ecol 231:139–157. https://doi.org/10.1016/S0022-0981(98)00090-2
Wear RG (1974) Incubation in British decapod crustacea, and the effects of temperature on the rate and success of embryonic development. J Mar Biol Assoc UK 54:745–762. https://doi.org/10.1017/S0025315400022918
Zuur A, Ieno EN, Smith GM (2007) Analyzing ecological data. Springer-Verlag, New York
Acknowledgements
This study was part of project ‘Behoud van een dynamisch Griend’ managed by Natuurmonumenten and funded by Waddenfonds, the provinces of Fryslân, Groningen and Noord-Holland, and Rijkswaterstaat. LLG was funded by NWO grant 016.Veni.181.087. Exploratory analyses were carried out by Arjen de Boer and Lies Bosma during their BSc course in 2019 at the University of Groningen. We would like to thank all assistants who helped with collecting and sorting the Balgzand dataset. Thanks to Sonja van Leeuwen for maintaining the NIOZ jetty temperature database. We are grateful to the anonymous reviewers for their most constructive feedback.
Funding
EP was funded by Waddenfonds grant WF-223011 to a consortium of Natuurmonumenten, Royal NIOZ and University of Groningen for the restoration of Griend, the Dutch Wadden Sea provinces (Friesland, Groningen, Noord-Holland) and Rijkswaterstaat. LLG was funded by NWO grant 016.Veni.181.087.
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EP, LG, TP and RD contributed to the concept and design of the study. RD conducted the data collection together with Jan Beukema and EP ran the statistical analysis. EP wrote the main sections of the manuscript supervised by TP and with input from LG and RD. All authors approved the submitted version.
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Penning, E., Govers, L.L., Dekker, R. et al. Advancing presence and changes in body size of brown shrimp Crangon crangon on intertidal flats in the western Dutch Wadden Sea, 1984–2018. Mar Biol 168, 160 (2021). https://doi.org/10.1007/s00227-021-03967-z
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DOI: https://doi.org/10.1007/s00227-021-03967-z