Skip to main content
Log in

Effects of organic additions to sediment, and maternal age and size, on patterns of offspring investment and performance in two opportunistic deposit-feeding polychaetes

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The investment made by a reproducing organism in its offspring can be affected by both extrinsic (environmental) and intrinsic (female condition) factors. The purpose of this study, conducted between December 1990 and June 1992, was to examine the influence of organic additions to sediment, and female age and size, on patterns of offspring investment and performance in the opportunistic polychaete Capitella sp. I (cf. Capitella capitata Farbricius). Sediment treatments were composed of marsh mud enriched with sewage or algae, or spiked with #2 fuel oil. All three of these additions are associated with opportunistic responses in Capitella sp. I populations in the laboratory and field. As a means of comparison,effects of sewage additions were also examined on the spionid Streblospio benedicti Webster. Organic additions to mud had no detectable effect on the C or N content of embryos in either species. However, sewage had a positive effect on juvenile performance in Capitella sp. I. Juveniles produced by adult Capitella sp. I in the sewage treatment grew 2 times larger (in 2 wk) than juveniles produced by adults in the mud treatment when these juveniles were raised in the same sediment type (mud). Such effects may facilitate opportunistic responses in Capitella sp. I offspring by reducing time to first reproduction. In addition to treatment sediment effects, maternal age and size had a strong influence on patterns of offspring investment in Capitella sp. I. The material investiment measured in collected embryos declined with maternal age in the oil and sewage treatments. The C:N ratio of embryos increased with maternal age for Capitella sp. I except in the algae treatment, which showed no effect of maternal age. Juvenile growth decreased with maternal age in the sewage treatment for Capitella sp. I. Maternal size appeared to have a positive effect on embryo investment in the mud and oil treatments, where reproducing worms were smallest. Previous studies of Capitella sp. I have documented a broad range of environmentally induced responses in growth and fecundity.The results of this study emphasize the importance of maternal environment, age, and size effects on the relationship between offspring investment and performance.Such effects may have profound consequences for the dynamics of populations and the fitness of individuals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alongi DM, Tenore KR (1985) Effect of detritus supply on trophic relationships within experimental benthic food webs. I. Meiofauna-polychaete [Capitella capitata (Type I) Fabricius] interactions. J exp mar Biol Ecol 88:153–166

    Google Scholar 

  • Bagenal TB (1969) Relationship between egg size and fry survival in brown trout Salmo trutta L. J Fish Biol 1:349–353

    Google Scholar 

  • Bayne BL, Gabbott PA, Widdows J (1975) Some effects of stress in the adults on the eggs and larvae of Mytilus edulis L. J mar Biol Ass UK 55:675–689

    Google Scholar 

  • Begon M, Parker GA (1986) Should egg size and clutch size decrease with age? Oikos 47:293–302

    Google Scholar 

  • Bridges TS (1992) Effects of development mode, contaminated sediments, and maternal characteristics on growth and reproduction in the polychaetes Streblospio benedicti (Spionidae) and Capitella sp. I (Capitellidae). PhD thesis, North Carolina State University, Raleigh

    Google Scholar 

  • Bridges TS, Heppell S (1996) Fitness consequences of maternal effects in Streblospio benedicti (Annelida: Polychaeta). Am Zool (in press)

  • Bridges TS, Levin LA, Cabrera D, Plaia G (1994) Effects of sediment amended with sewage, algae, or hydrocarbons on growth and reproduction in two opportunistic polychaetes. J exp mar Biol Ecol 177:99–119

    Google Scholar 

  • Brody MS, Lawlor LR (1984) Adaptive variation in offspring size in the terrestrial isopod, Armadillidium vulgare. Oecologia, 61:55–59

    Google Scholar 

  • Butlin RK (1987) Male spermatophore investment increases female fecundity in a grashopper. Evolution 41:221–225

    Google Scholar 

  • Capinera JL, Barbosa P, Hagedorn HH (1977) Yolk and yolk depletion of gypsy moth eggs: implications for population quality. Ann ent Soc Am 70:40–42

    Google Scholar 

  • Carr RS, Reish DJ (1977) The effects of petroleum hydrocarbous on the survival and life history of polychaetous annelids. In: Wolfe DA (ed) Fate and effects of petroleum hydrocarbons in marine organisms and ecosystems. Pergamon Press, Oxford, pp 168–173

    Google Scholar 

  • Cavers PB, Steel MG (1984) Patterns of change in seed weight over time on individual plants. Am Nat 124:324–335

    Google Scholar 

  • Charlesworth B, Leon JA (1976) The relation ofreproductive effort to age. Am Nat 110:449–459

    Google Scholar 

  • Chesney EJ Jr, Tenore KR (1985) Oscillations of laboratory populations of the polychaete Capitella capitata (Type I): their causes and implications for natural populations. Mar Ecol Prog Ser 20: 289–296

    Google Scholar 

  • Christiansen FB, Fenchel TM (1979) Evolution of marine invertebrate reproductive patterns. The Pop Biol 16: 267–282

    Google Scholar 

  • Chu JW, Levin LA (1989) Photoperiod and temperature regulation of growth and reproduction in Streblospio benedicti (Polychaeta: Spionidae). Invert Reprod Dev 15: 131–142

    Google Scholar 

  • Cole LC (1954) The population consequences of life history phenomena. Q Rev Biol 29: 103–137

    Google Scholar 

  • Day RL, Simon JL (1984) Larval energetics of the spionid polychaete Polydora websteri Hartman. In: Hutchings PA(ed) Proceedings of the 1st international polychaete conference, Sydney. The Linnean Society of New South Wales, Sydney

    Google Scholar 

  • Eckelbarger KJ (1986) Vitellogenic mechanisms and the allocation of energy to offspring in polychaetes. Bull mar Sci 39: 426–443

    Google Scholar 

  • Forbes TL (1989) The importance of size-dependent processes in the ecology of deposit-feeding benthos. In: Lopez G, Taghon G (eds) Ecology of deposit feeders. Springer Verlag, New York

    Google Scholar 

  • Forbes TL, Lopez GR (1987) The allometry of deposit feeding in Capitella species I (Polychaeta: Capitellidae): the role of temperature and pellet weight in the control of egestion. Biol Bull mar biol Lab, Woods Hole 172: 187–201

    Google Scholar 

  • Gadgil M, Bossert WH (1970) Life historical consequences of natural selection. Am Nat 104: 1–24

    Google Scholar 

  • Gallager SM, Mann R (1986) Growth and survival of larvae of Mercenaria mercenaria (L.) and Crassostrea virginica(Gmelin) relative to broodstock conditioning and lipid content of eggs. Aquaculture, Amsterdam 56: 105–121

    Google Scholar 

  • Gearing PJ, Gearing JN, Maughan JT, Oviatt CA (1991) Isotopic distribution of carbon from sewage sludge and cutrophication in the sediments and food web of estuarine ecosystems. Envir Sci Technol 25: 295–301

    Google Scholar 

  • George SB (1990) Population and seasonal differences in egg quality of Arbacia lixula (Echinodermata: Echinoidea). Invert Reprod Dev 17: 111–121

    Google Scholar 

  • George SB (1994) Population differences in maternal size and offspring quality for Leptasterias epichlora (Brandt) (Echinodermata: Asteroidea). J exp mar Biol Ecol 175: 121–131

    Google Scholar 

  • George SB, Lawrence JM, Fenaux L (1991) The effect of food ration on the quality of eggs of Luidia clathrata (Say) (Echinodermata: Asteroidea).Invert Reprod Dev 20: 237–242

    Google Scholar 

  • Glazier DS (1992) Effects of food, genotype, and maternal size and age on offspring investment in Daphnia magna. Ecology 73: 910–926

    Google Scholar 

  • Grahame J, Branch G (1985) Reproductive patterns of marine invertebrates. Oceanogr mar Biol A Rev 23: 373–398

    Google Scholar 

  • Grassle JP, Grassle JF (1974) Opportunistic life histories and genetic systems in marine benthic polychaetes. J mar Res 32: 253–284

    Google Scholar 

  • Grassle JP, Grassle JF (1976) Sibling species in the marine pollution indicator Capitella(Polychaeta). Science, NY 192: 567–569

    Google Scholar 

  • Grémare A, Marsh AG, Tenore KR (1988) Short-term reproductive responses of Capitella sp. I (Annelida: Polychaeta) fed on different diets. J exp mar Biol Ecol 123: 147–162

    Google Scholar 

  • Grémare A, Marsh AG, Tenore KR (1989) Secondary production and reproduction of Capitella capitata Type I (Annelida: Polychaeta) during a population cycle. Mar Ecol Prog Ser 51: 99–105

    Google Scholar 

  • Helm MM, Holland DL, Stephenson RR (1973) The effect of supplementary algal feeding of a hatchery breeding stock of Ostreaelulis L. on larval vigour. J mar biol Ass UK 53: 673–684

    Google Scholar 

  • Kaplan RH, Cooper WA (1984) The evolution of developmental plasticity in reproductive characteristics: an application of the “adaptive coin-flipping” principle. Am Nat 123: 339–410

    Google Scholar 

  • Kessler A (1971) Relation between egg production and food consumption in species of the genus Pardosa (Lycosidae, Araneae) under experimental conditions of food abundance and food shortage. Oecologia 8: 93–109

    Google Scholar 

  • Kirkpatrick M, Lande R (1989) The evolution of maternal characters. Evolution 43: 485–503

    Google Scholar 

  • Kozlowski J, Uchmanski J (1987) Optimal individual growth and reproduction in perennial species with indeterminate growth. Evolutionary Ecol 1: 214–230

    Google Scholar 

  • Kraeuter JN, Castagna M, Van Dessel R (1982) Egg size and larval survival of Mercenaria mercenaria (L.) and Argopecten irradians (Lamarck). J exp mar Biol Ecol 56: 3–8

    Google Scholar 

  • Kuznetsov VA (1973) Fecundity of the bream (Abramis brama L.) and the quality of its eggs. J Ichthyol (USSR) 13: 669–679

    Google Scholar 

  • Levin LA (1984) Multiple patterns of development in Streblospio benedicti Webster (Spionidae) from three coasts of North America. Biol Bull mar biol Lab, Woods Hole 166: 494–508

    Google Scholar 

  • Levin LA (1986) Effects of enrichment on reproduction in the opportunistic polychaete Streblospio benedicti (Webster): a mesocosm study. Biol Bull mar biol Lab, Woods Hole 171: 143–160

    Google Scholar 

  • Levin L, Caswell H, Bridges T, Cabrera D, Plaia G, DiBacco C (1996) Demographic responses of estuarine polychaetes to sewage, algal and hydrocarbon additions: life table response experiments. Ecol Applics (in press)

  • Lewontin RC (1965) Selection for colonizing ability. In: Baker HG, Stebbins GL (eds) The genetics of colonizing species. Academic Press, New York,pp 79–94

    Google Scholar 

  • Lipstein B, Kary S, Hurwitz S (1982) The nutritional value of activated sludge for poultry. Nutr Rep Int, Los Altos, Calif 25: 829–836

    Google Scholar 

  • Marsh AG, Grémare A, Dawson R, Tenore KR (1990a) Translocation of algal pigments to oocytes in Capitella sp. I (Annelida: Polychaeta). Mar Ecol Prog Ser 67: 301–304

    Google Scholar 

  • Marsh AG, Grémare A, Tenore KR (1989) Effect of food type and ration on growth of juvenile Capitella sp. I (Annelida: Polychaeta) macro-and micronutrients. Mar Biol 102: 519–527

    Google Scholar 

  • Marsh AG, Harvey HR, Grémare A, Tenore KR (1990b) Dietary effects on oocyte yolk-composition in Capitella sp. I (Annelida: Polychaeta): fatty acids and sterols. Mar Biol 106: 369–374

    Google Scholar 

  • Marsh AG, Tenore KR (1990) The role of nutrition in regulating the population dynamics of opportunistic, surface deposit feeders in a mesonaline community.Limnol Oceanogr 35: 710–724

    Google Scholar 

  • McGinley MA, Temme DH, Geber MA (1987) Parental investment in offspring in variable environments: theoretical and empirical considerations. Am Nat 130: 370–398

    Google Scholar 

  • Mousseau TA, Dingle H (1991) Maternal effects in insect life histories. A Rev Ent 36: 511–534

    Google Scholar 

  • Nisbet ICT (1978) Dependence of fledging success on egg size, parental performance and egg composition among common and roseate terns, Sterna hirundo and S. dougallii. Ibis 120: 207–215

    Google Scholar 

  • Orton RA, Sibly RM (1990) Egg size and growth rate in Theodoxus fluviatilis (L.). Funct Ecol 4: 91–94

    Google Scholar 

  • Parker GA, Begon M (1986) Optimal egg size and clutch size: effects of environment and maternal phenotype. Am Nat 128: 573–592

    Google Scholar 

  • Pearson TH, Rosenberg R (1978) Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceanogr mar Biol A Rev 16: 229–311

    Google Scholar 

  • Qian P-Y (1994) Effect of food quantity on growth and reproductive characteristics of Capitella sp. (Annelida: Polychaeta). Invert Repro Dev 26: 175–185

    Google Scholar 

  • Qian P-Y, Chia F-S (1991) Fecundity and egg size are mediated by food quality in the polychaete worm Capitella sp. J exp mar Biol Ecol 148: 11–25

    Google Scholar 

  • Qian P-Y, Chia F-S (1992) Effect of aging on reproduction in a marine polychaete Capitella sp. J exp mar Biol Ecol 156: 23–38

    Google Scholar 

  • Roff DA (1992) The evolution of life histories. Chapman and Hall, New York

    Google Scholar 

  • Sanders HL, Grassle JF, Hampson GR,Morse LS, Garner-Price S, Jones CC (1980) Anatomy of an oil spill: long term effects from the grounding of the barge Florida off West Falmouth, Massachusetts. J mar Res 38: 265–380

    Google Scholar 

  • Sibly RM, Calow P (1986) Physiological ecology of animals: an evolutionary approach. Blackwell Scientific Publications, Oxford

    Google Scholar 

  • Sibly R, Calow P, Smith RH (1988) Optimal size of seasonal breeders. J theor Biol 133: 13–21

    Google Scholar 

  • Sinervo B, McEdward LR (1988) Developmental consequences of an evolutionary change in egg size:an experimental test. Evolution 42: 885–899

    Google Scholar 

  • Skadsheim A (1984) Coexistence and reproductive adaptations of amphipods: the role of environmental heterogeneity. Oikos 43: 94–103

    Google Scholar 

  • Stearns SC (1976) Life-history tactics: a review of the ideas. Q Rev Biol 51: 3–47

    Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  • Steinwascher K (1984) Egg size variation in Aedes aegypti: relationship to body size and other variables. Am Midl Nat 112: 76–84

    Google Scholar 

  • Strathmann RR, Fenaux L, Strathmann MF (1992) Heterochronic developmental plasticity in larval sea urchins and its implications for evolution of nonfeeding larvae. Evolution 46: 972–986

    Google Scholar 

  • Tenore KR, Chesney EJ Jr (1985) The effects of interaction of rate of food supply and population density on the bioenergetics of the opportunistic polychaete, Capitella capitata (Type I). Limnol Oceanogr 30: 1188–1195

    Google Scholar 

  • Thomas CS (1983) The relationships between breeding experience, egg volume and reproductive success of the kittiwake Rissa tridactyla. Ibis 125: 567–574

    Google Scholar 

  • Thompson RJ (1982) The relationship between food ration and reproductive effort in the green sea urchin, Strongylocentrotus droebachiensis. Oecologia 56: 50–57

    Google Scholar 

  • Thorson G (1946) Reproduction and larval development of Danish marine bottom invertebrates with special reference to the planktonic larvae of the Sound (Oresund). Meddr Komm Danm Fiskog Havunders (Ser Plankton) 4: 1–523

    Google Scholar 

  • Thorson G (1950) Reproduction and larval ecology of marine bottom invertebrates. Biol Rev 25: 1–45

    Google Scholar 

  • Vance RR (1973a) On reproductive strategies in marine benthic invertebrates. Am Nat 107: 339–352

    Google Scholar 

  • Vance RR (1973b) More on reproductive strategies in marine benthic invertebrates. Am Nat 107: 353–361

    Google Scholar 

  • Wiklund C, Karlsson B (1984) Egg size variation in satyrid butterflies: adaptive vs. historical, “bauplan”, and mechanistic explanations. Oikos 43: 391–400

    Google Scholar 

  • Wong WH, Leung KL (1979) Sewage sludge and seaweed (Ulva sp.) as supplementary feed for chicks. Envir Pollut 20: 93–101

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by J. P. Grassle, New Brunswick

Present address: WES-ES-F, USAE Waterways Experiment Station, 3909 Halls Ferry Rd., Vicksburg, Mississippi 39180-6199, USA

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bridges, T.S. Effects of organic additions to sediment, and maternal age and size, on patterns of offspring investment and performance in two opportunistic deposit-feeding polychaetes. Marine Biology 125, 345–357 (1996). https://doi.org/10.1007/BF00346315

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00346315

Keywords

Navigation