Abstract
Maternal investment (MI), the energy allocated by mothers to offspring, has important effects on the life-history traits of marine organisms. Variation in such traits shows strong correlation with latitude for several marine taxa (Thorson’s rule). Large-scale latitudinal variation in MI within a single species suggests population genetic divergence, while temporal changes in MI, rather, reflect plasticity. At higher latitudes (i.e., colder waters), traits associated with MI (brood weight, fecundity, egg volume, and energy content) increase. To identify phenotypic plasticity along a latitudinal gradient in MI traits (brood weight, egg volume, density number, and egg lipid composition), five populations of the kelp crab Taliepus dentatus along the coast of Chile (30°S–42°S) were investigated during the summer (December–February) and winter months (June–August) of 2015–2016. Despite this wide latitudinal range, the sea surface temperature (SST) difference between the northernmost and the southernmost sites was only approximately 2.0 °C in winter and 5.5 °C in summer. In summer, when latitudinal variation in SST was highest, brood weight, egg density, fecundity, and egg lipids increased with latitude, while egg volume decreased. No trends in MI were observed in winter when the SST gradient was almost non-existent. These results suggest that the relationship between MI and latitude is shaped by temperature rather than being site-specific. The seasonality of latitudinal MI traits also suggests a trade-off between the costs of female maintenance and/or brooding behaviours and MI. When investigating latitudinal and temporal variation in marine brooder MI, the effect of temperature on life-history traits and the associated costs of female brooding should be quantified.
Similar content being viewed by others
References
Anger K (2001) The biology of decapod crustacean larvae. AA Balkema, Lisse Oceanographic observations in Chilean coastal waters between Valdivia and Concepcio´n
Atkinson LP, Valle-Levinson A, Figueroa D, De Pol-Holz R, Gallardo VA, Schneider W, Schmidt M (2002) Oceanographic observations in Chilean coastal waters between Valdivia and Concepcion. J Geophys Res 107(18):1–6
Baeza JA, Fernández M (2002) Active brood care in Cancer setosus (Crustacea: Decapoda): the relationship between female behaviour, embryo oxygen consumption, and the cost of brooding. Funct Ecol 16:241–251
Baldanzi S, McQuaid CD, Porri F (2015) Temperature effects on reproductive allocation in the sandhopper Talorchestia capensis. Biol Bull 228:181–191
Barnes H, Barnes M (1965) Egg size, nauplius size, and their variation with local, geographical, and specific factors in some common cirripedes. J Anim Ecol 34:391–402
Brante A, Fernández M, Eckerle L, Mark F, Pörtner H-O, Arntz W (2003) Reproductive investment in the crab, Cancer setosus, along a latitudinal cline: egg production, egg losses and egg ventilation. Mar Ecol Prog Ser 251:221–232
Brante A, Cifuentes S, Pörtner H-O, Arntz W, Fernández M (2004) Latitudinal comparisons of reproductive traits in five brachyuran species along the Chilean coast. Rev Chi His Nat 77:15–27
Christiansen FB, Fenchel TM (1979) Evolution of marine invertebrate reproductive patterns. Theor Popul Biol 16:267–282
Clarke A (1983) Life in cold water: the physiological ecology of polar marine ectotherms. Oceanogr Mar Biol Annu Rev 21:341–453
Clarke A (1991) Egg size and egg composition in polar shrimps (Caridea: Decapoda). J Exp Mar Biol Ecol 168:189–203
Collin R, Salazar MZ (2010) Temperature-mediated plasticity and genetic differentiation in egg size and hatching size among populations of Crepidula (Calyptraeidae: Gastropoda). Biol J Linn Soc 99:489–499
Coutteau P, Geurden I, Camara MR, Bergot P, Sorgeloos P (1997) Review on the dietary effects of phospholipids in fish and crustacean larviculture. Aquaculture 155:149–164
D’Abramo LR, Bordner CE, Conklin DE (1982) Relationship between dietary phosphatidylcholine and serum cholesterol in the lobster Homarus sp. Mar Biol 67:231–235
D’Abramo LR, Baum NA, Bordner CE, Conklin DE, Chang ES (1985) Diet-dependent cholesterol transport in the American lobster. J Exp Biol Ecol 87:83–96
Dahlhoff EP (2004) Biochemical indicators of stress and metabolism: applications for marine ecological studies. Annu Rev Physiol 66:183–207
Deutsch C, Ferrel A, Seibel B, Pörtner H-O, Huey RB (2015) Climate change tightens a metabolic constraint on marine habitat. Science 348:1132–1135
Emlet RB, Høegh-Guldberg O (1997) Effects of egg size on postlarval performance: experimental evidence from a sea urchin. Evolution 51:141–152
Fagetti E, Campodonico I (1971) Desarollo larval en el laboratorio de Taliepus dentatus (Milne-Edwards) (Crustacea Brachyura: Magjidae, Acanthonychinae). Rev Biol Mar Valparaiso 14(3):1–14
Fernández M, Brante A (2003) Brood care in brachyuran crabs: the effect of oxygen provision on reproductive costs. Rev Chil Hist Nat 76:157–168
Fernández M, Bock C, Pörtner HO (2000) The cost of being a caring mother: the ignored factor in the reproduction of marine invertebrates. Ecol Lett 3:487–494
Fernández M, Pardo LM, Baeza JA (2002) Patterns of oxygen supply in embryo masses of Brachyuran crabs throughout development: the effect of oxygen availability and chemical cues in determining female behaviour. Mar Ecol Prog Ser 245:181–190
Fernández M, Pappalardo P, Jeno K (2006) The effects of temperature and oxygen availability on intracapsular development of Acanthina monodon (Gastropoda: Muricidae). Rev Chil Hist Nat 79:155–167
Fischer S, Thatje S, Graeve M, Paschke K, Kattner G (2009) Bioenergetics of early life-history stages of the brachyuran crab Cancer setosus in response to changes in temperature. J Exp Mar Bio Ecol 374:160–166
Folch J, Lees M, Stanley GHS (1959) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509
Fox CW (1994) The influence of egg size on offspring performance in the seed beetle, Callosobruchus maculatus. Oikos 71:321–325
García-Guerrero M, Villarreal H, Racotta IS (2003) Effect of temperature on lipids, proteins, and carbohydrates levels during development from egg extrusion to juvenile stage of Cherax quadricarinatus (Decapoda: Parastacidae). Comp Biochem Physiol 138A:147–154
Geister TL, Lorenz MW, Hoffmann KH, Fischer K (2009) Energetics of embryonic development: effects of temperature on egg and hatchling composition in a butterfly. Comp Physiol 179:87–98
Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL (2001) Effects of size and temperature on metabolic rate. Science 293:2248–2251
Giménez L (2006) Phenotypic links in complex life cycles: conclusions from studies with decapod crustaceans. Integr Comp Biol 46:615–622
Gonzalez-Ortegón E, Giménez L (2014) Environmentally mediated phenotypic links and performance in larvae of a marine invertebrate. Mar Ecol Prog Ser 502:185–195
Graeve M, Jenssen D (2009) Improved separation and quantification of neutral and polar lipid classes by HPLC–ELSD using a monolithic silica phase: application to exceptional marine lipids. J Chromatogr B 877:1815–1819
Graeve M, Wehrtmann IS (2003) Lipid and fatty acid composition of Antarctic shrimp eggs (Decapoda: Caridea). Polar Biol 26:55–61
Hines AH (1986) Larval patterns in the life histories of Brachyuran crabs (Crustacea, Decapoda, Brachyura). Bull Mar Sci 39:444–466
Jarošík V, Kratochvil L, Honek A, Dixon AFG (2004) A general rule for the dependence of developmental rate on temperature in ectothermic animals. Proc R Soc Lond B 271:219–221
Kattner G, Wehrtmann IS, Merck T (1994) Interannual variations of lipids and fatty acids during larval development of Crangon spp. in the German Bight, North Sea. Comp Biochem Physiol 107B:103–110
Laptikhovsky V (2006) Latitudinal and bathymetric trends in egg size variation: a new look at Thorson’s and Rass’s rules. Mar Ecol 27:7–14
Lardies M, Castilla JC (2001) Latitudinal variation in the reproductive biology of the commensal crab Pinnaxodes chilensis (Decapoda: Pinnotheridae) along the Chilean coast. Mar Biol 139:1125–1133
Lessios HA (1990) Adaptation and phylogeny as determinants of egg size in echinoderms from the two sides of the isthmus of Panama. Am Nat 135:1–13
Letelier J, Pizarro O, Nuñez S (2009) Seasonal variability of coastal upwelling and the upwelling front off central Chile. J Geophys Res. https://doi.org/10.1029/2008JC005171
Levitan DR (2006) The relationship between egg size and fertilization success in broadcast-spawning marine invertebrates. Int Comp Biol 46:298–311
Lonsdale DJ, Levinton JS (1985) Latitudinal differentiation in embryonic duration, egg size, and newborn survival in a harpacticoid copepod. Biol Bull (Woods Hole) 168:419–431
Lorioux S, DeNardo DF, Gorelick R, Lourdais O (2012) Maternal influences on early development: preferred temperature prior to oviposition hastens embryogenesis and enhances offspring traits in the Children’s python, Antaresia children. J Exp Biol 215:1346–1353
Lu W, Bennett BD, Rabinowitz JD (2008) Analytical strategies for LC-MS-based targeted metabolomics. J Chromatogr B Analyt Technol Biomed Life Sci 871:236–242
Lucey NM, Lombardi C, DeMarchi L, Schulze A, Gambi MC, Calosi P (2015) To brood or not to brood: are marine invertebrates that protect their offspring more resilient to ocean acidification? Sci Rep 5:12009. https://doi.org/10.1038/srep12009
Marshall D, Keough MJ (2007) The evolutionary ecology of offspring size in marine invertebrates. Adv Mar Biol 53:1–60
Marshall DJ, Uller T (2007) When is a maternal effect adaptive? Oikos 116:1957–1963
Marshall DJ, Bonduriansky R, Bussiére LF (2008) Offspring size variation within broods as a bet-hedging strategy in unpredictable environments. Ecology 89:2506–2517
Moran AL (2004) Egg size evolution in tropical American arcid bivalves: the comparative method and the fossil record. Evolution 58:2718–2733
Moran AL, Emlet RB (2001) Offspring size and performance in variable environments: field studies on a marine snail. Ecology 82:1597–1612
Moran AL, McAlister LR (2009) Egg size as a life history character of marine invertebrates: is it all it’s cracked up to be? Biol Bull (Woods Hole) 216:226–242
Moya-Laraño J, Macías-Ordoñez R, Blanckenhorn WU, Fernández-Montraveta C (2008) Analysing body condition: mass, volume or density? J Anim Ecol 77:1099–1108
Murúa P, Westermeier R, Patiño DJ, Müller DG (2013) Culture studies on early development of Lessonia trabeculata (Phaeophyceae, Laminariales): seasonality and acclimation to light and temperature. Phycol Res 61:145–153. https://doi.org/10.1111/pre.12013
Narváez DA, Poulin E, Leiva GE, Hernandez-Miranda E, Castilla JC (2004) Seasonal and spatial variation of nearshore hydrographic conditions in central Chile. Cont Shelf Res 24:279–292. https://doi.org/10.1016/j.csr.2003.09.008.29
Navarrete SA, Wieters EA, Broitman BR, Castilla JC (2005) Scales of benthic-pelagic coupling and the intensity of species interactions: from recruitment limitation to top-down control. Proc Natl Acad Sci 102:18046–18051. https://doi.org/10.1073/pnas.0509119102
Naylor JK, Taylor EW, Bennett DB (1999) Oxygen uptake of developing eggs of Cancer pagurus (Crustacea: Decapoda: Cancridae) and consequent behaviour of ovigerous females. J Mar Biol Assoc UK 79:305–315
Oh CW, Hartnoll RG (2004) Reproductive biology of the common shrimp Crangon crangon (Decapoda: Crangonidae) in the central Irish Sea. Mar Biol 144:303–316
Oliphant A, Thatje S (2013) Per offspring investment implications for crustacean larval development: evolutionary insights into endotrophy and abbreviated development. Mar Ecol Prog Ser 493:207–217
Parichy DM, Kaplan RH (1992) Maternal effects on offspring growth and development depend on environmental quality in the frog Bombina orientalis. Oecologia 91:579–586
Reinsel KA, Pagel K, Kissen M, Foran E, Clare AS, Rittschof D (2014) Egg mass ventilation by caridean shrimp: similarities to other decapods and insight into pheromone receptor location. J Mar Biol Assoc UK 94(05):1009–1017
Rey F, Alves E, Melo T, Domingues P, Queiroga H, Rosa R, Rosário M, Domingues M, Calado R (2016) Unravelling polar lipid dynamics during embryonic development of two sympatric brachyuran crabs (Carcinus maenas and Necora puber) using lipidomics. Sci Rep 5:145–149
Sasaki GC, Capuzzo JM, Biesiot P (1986) Nutritional and bioenergetic considerations in the development of the American lobster Homarus americanus. Can J Fish Aquat Sci 43:2311–2319
Schulte PM, Timothy MH, Fangue NA (2011) Thermal performance curves, phenotypic plasticity, and the time scales of temperature exposure. Integ Comp Biol 51:691–702
Silva G, Lima FP, Martel P, Castilho R (2014) Thermal adaptation and clinal mitochondrial DNA variation of European anchovy. Proc R Soc B 281:1093. https://doi.org/10.1098/rspb.2014.1093
Smith CC, Fretwell SD (1974) The optimal balance between size and number of offspring. Am Nat 108:499–506
Storch D, Santelices P, Barria J, Cabeza K, Pörtner HO, Fernández M (2009) Temperature tolerance of zoea I from two different populations of the kelp crab Taliepus dentatus. J Exp Biol 212:1371–1376
Strathmann RR (1985) Feeding and non-feeding larval development and life history evolution in marine invertebrates. Annu Rev Ecol Syst 16:339–361
Strathmann RR, Strathmann M (1995) Oxygen supply and limits on aggregation of embryos. J Mar Biol Assoc UK 75:413–428
Strub PT, Mesías JMJM, Montecino V, Rutllant JA, Salinas S et al (1998) Coastal ocean circulation off western South America. In: Robinson AR, Brink KH (eds) The sea, vol 11. John Wiley and Sons, New York, pp 273–313
Tapia FJ, Navarrete SA, Castillo MI, Menge BA, Castilla JC et al (2009) Thermal indices of upwelling effects on inner-shelf habitats. Prog Oceanogr. https://doi.org/10.1016/j.pocean.2009.07.035
Tapia FJ, Largier JL, Castillo M, Wieters EA, Navarrete SA (2014) Latitudinal discontinuity in thermal conditions along the nearshore of central-northern Chile. PLoS ONE 9(10):e110841. https://doi.org/10.1371/journal.pone.0110841
Thatje S, Hall S (2016) The effect of temperature on the evolution of per offspring investment in a globally distributed family of marine invertebrates (Crustacea: Decapoda: Lithodidae). Mar Biol 163:48–57
Thiel M (1999) Duration of extended parental care in marine amphipods. J Crust Biol 19:60–71
Thorson G (1950) Reproductive and larval ecology of marine bottom invertebrates. Biol Rev Camb Philos Soc 25:1–45
Tropea C, Stumpf L, López Greco LS (2015) Effect of temperature on biochemical composition, growth and reproduction of the ornamental red cherry shrimp Neocaridina heteropoda (Decapoda, Caridea). PLoS ONE 10(3):e0119468
Tuset VM, Espinosa DI, García-Mederos A, Santana JI, González JA (2011) Egg development and fecundity estimation in deep-sea red crab, Chaceon affinis (Geryonidae), off the Canary Islands (NE Atlantic). Fisheries Res 109:373–378
Urzúa Á, Paschke K, Gebauer P, Anger K (2012) Seasonal and interannual variations in size, biomass and chemical composition of the eggs of the North Sea shrimp, Crangon crangon (Decapoda: Caridea). Mar Biol 159:583–599
Vance RR (1973) On reproductive strategies in marine benthic invertebrates. Am Nat 107:339–352
Vargas LM (1995) Descripción del desarrollo embrionario de Cancer polyodon Poepping 1836 (Crustacea: Decapoda: Brachyura) y efectos de la temperatura, bajo condiciones de laboratorio. BSc thesis, Universidad Católica del Norte, Coquimbo
Vogt G (2013) Abbreviation of larval development and extension of brood care as key features of the evolution of freshwater Decapoda. Biol Rev Camb Philos Soc 88:81–116
Wehrtmann IS, Lopez GA (2003) Effects of temperature on the embryonic development and hatchling size of Betaeus emarginatus (Decapoda: Caridea: Alpheidae). J Nat Hist 37:2165–2178
Wieters EA, Kaplan DM, Navarrete SA, Sotomayor A, Largier JL (2003) Alongshore and temporal variability in chlorophyll a concentration in Chilean nearshore waters. Mar Ecol Prog Ser 249:93–105. https://doi.org/10.3354/meps249093
Zhang HM, Reynolds RW, Smith TM (2007) Bias characteristics in the AVHRR sea surface temperature. Geophys Res Lett 31:L01307
Acknowledgements
We thank Dr A. J. Brante (Universidad Católica de la Ssma Concepción, Chile), Dr M. L. Pardo (Universidad Austral, Chile), and several divers for their precious help during the field surveys. We thank Dieter Jenssen and Valeria Adrian (Alfred Wegener Institute for Polar and Marine Research, Germany) for the lipid analysis. We are grateful to N. Osiadacz, Dr. N. Weidberg, Alexandra Tissot, and Katalin Plummer (Estación Costera de Investigaciones Marinas, Chile) for their valuable help in the laboratory, field, and manuscript editing. We also thank two anonymous reviewers for their detailed revisions.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Funding
This work was fully funded by Comisión Nacional de Investigación Científica y Tecnológica (CONICYT) and Fondo Nacional de Desarrollo Científico y Tecnológico (FONDECYT POSTDOCTORADO), Grant number 3150020 assigned to SB. This work was supported by the Deutsche Forschungsgemeinschaft (DFG) in the framework of the priority programme “Antarctic research with comparative investigations in Arctic ice areas” by a Grant STO 857/2 to D. S. and by the Alexander von Humboldt foundation in the framework of its alumni programme “Research Group Linkage” to D. S. and M. F.
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable international, national, and institutional guidelines for the care and use of animals were followed.
Additional information
Responsible Editor: J. Grassle.
Reviewed by R. Calado and an undisclosed expert.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Baldanzi, S., Storch, D., Navarrete, S.A. et al. Latitudinal variation in maternal investment traits of the kelp crab Taliepus dentatus along the coast of Chile. Mar Biol 165, 37 (2018). https://doi.org/10.1007/s00227-018-3294-2
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-018-3294-2