Skip to main content
SpringerLink
Log in

Associations Between Winter Temperatures and the Timing and Duration of Annual Larval Recruitment of a Non-native Anomuran Crab

  • Published:
Estuaries and Coasts Aims and scope Submit manuscript

Abstract

The green porcelain crab, Petrolisthes armatus, a subtropical/tropical species, was first recorded on intertidal oyster reefs in South Carolina in 1995. Since then, its range has expanded north in a series of surges and setbacks that appear to be associated with particularly cold winters that may cause mortality. Petrolisthes armatus reproduces year-round in its native range whereas its reproductive season in the non-native range is limited to warmer months. Variation in the timing and duration of larval recruitment is not known for the non-native range and these factors may affect further range expansion. To determine whether P. armatus larval recruitment is related to temperature variation, in particular, the severity of winter temperatures, archival biweekly (every 2 weeks) larval samples collected 1994–2018 near its northern range limit in the North Inlet Winyah Bay National Estuarine Research Reserve (NERR) were examined. The goal was to determine whether the timing and duration of larval ingress varied over time and was related to temperature variation. Petrolisthes armatus larvae were first observed in samples collected in 1995. There was considerable interannual variability in the timing of the start of recruitment (coefficient of variation 29%), which ranged from the last week of March at the earliest to the last week of July at the latest, for all years but one. Earlier annual recruitment was positively correlated with a longer recruitment duration. The timing of first larval recruitment was also related to the severity of the preceding winter, with later larval recruitment occurring in years with several consecutive days of cold temperatures. Cold winter temperatures appear to affect overwintering populations and their ability to reproduce in the early spring. A decreasing frequency of severe winters along the coastal South Atlantic Bight may promote further poleward range expansion of P. armatus.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Allen, D.M., V. Ogburn-Matthews, T. Buck, and E.M. Smith. 2008. Mesozooplankton responses to climate change and variability in a southeastern U.S. estuary (1981–2003). Journal of Coastal Research SI 55: 95–110.

    Google Scholar 

  • Annala, J.H., J.L. McKoy, D. Booth, and R.B. Pike. 1980. Size at the onset of sexual maturity in female Jasus edwardsii (Decapoda: Palinuridae) in New Zealand. New Zealand Journal of Marine Freshwater Research 14 (3): 217–228.

    Google Scholar 

  • Armitage, K.B., and M. Landau. 1982. The effects of photoperiod and temperature on growth and reproduction of Daphnia ambigua. Comparative Biochemistry Physiology 71A: 137–140.

    Google Scholar 

  • Byers, J.E., R.S. Smith, H.W. Weiskel, and C.Y. Robertson. 2014. A non-native prey meditates the effects of a shared predator on an ecosystem service. PLoS One 9 (4): e93969. https://doi.org/10.1371/journalpone.0093969.

    Article  Google Scholar 

  • Canning-Clode, J., and J.T. Carlton. 2017. Refining and expanding global climate change scenarios in the sea: poleward creep complexities, range termini, and setbacks and surges. Diversity and Distributions 23: 436–473.

    Google Scholar 

  • Canning-Clode, J., A.E. Fowler, J.E. Byers, J.T. Carlton, and G.M. Ruiz. 2011. “Caribbean creep” chills out: Climate change and marine invasive species. PLoS One 6: 2–6.

    Google Scholar 

  • Crickenberger, S., and A. Moran. 2013. Rapid range shift in an introduced tropical marine invertebrate. PLoS One 8 (10): e78008. https://doi.org/10.1371/journal.pone.0078008.

    Article  CAS  Google Scholar 

  • de Melo, M., R. Schwamborn, S. Neumann-Leitão, and M.N. Paranaguá. 2012. Abundance and instantaneous transport of Petrolisthes armatus (Gibbes, 1850) planktonic larvae in the Catuama inlet, Northeast Brazil. Anais da Academia Brasileria Cienêcias 84 (1): 95–102.

    Google Scholar 

  • Díaz-Ferguson, E., and J.A. Vargas-Zamora. 2001. Abundance of Petrolisthes armatus (Crustacea: Porcellanidae) on a tropical estuarine intertidal rocky beach, Gulf of Nicoya estuary, Costa Rica. Revista de Biología Tropical 49: 97–101.

    Google Scholar 

  • Gaitán-Espitia, J.D., L.D. Bacigalupe, T. Opitz, N.A. Lagos, T. Timmermann, and M.A. Lardies. 2014. Geographic variation in thermal physiological performance of the intertidal crab Petrolisthes violaceus along a latitudinal gradient. Journal of Experimental Biology 217 (24): 4379–4386.

    Google Scholar 

  • Gaylord, B., and S.D. Gaines. 2000. Temperature or transport? Range limits in marine species mediated solely by flow. American Naturalist 155 (6): 769–789.

    Google Scholar 

  • Gore, R.H. 1970. Petrolisthes armatus: a redescription of larval development under laboratory conditions (Decapoda, Porcellanidae 1). Crustaceana 18 (1): 75–89.

    Google Scholar 

  • Gore, R.H. 1972. Petrolisthes armatus (Gibbes, 1850): the development under laboratory conditions of larvae from a Pacific specimen (decapoda , porcellanidae). Crustaceana 22: 67–83.

    Google Scholar 

  • Gribben, P.E., S. I’Ons, N.E. Phillips, S.W. Geange, J.T. Wright, and B.R. Murray. 2013. Biogeographic comparisons of the traits and abundance of an invasive crab throughout its native and invasive ranges. Biological Invasions 15 (8): 1877–1885.

    Google Scholar 

  • Hadley, N.H., M. Hodges, D.H. Wilber, and L.D. Coen. 2010. Evaluating intertidal oyster reef development in South Carolina using associated faunal indicators. Restoration Ecology 18 (5): 691–701.

    Google Scholar 

  • Hale, S.S., H.W. Buffum, J.A. Kiddon, and M.M. Hughes. 2017. Subtidal benthic invertebrates shifting northward along the US Atlantic coast. Estuaries and Coasts 40 (6): 1744–1756.

    Google Scholar 

  • Hameed, S.O., J.W. White, S.H. Miller, K.J. Nickols, and S.G. Morgan. 2016. Inverse approach to estimating larval dispersal reveals limited population connectivity along 700 km of wave-swept open coast. Proceedings of the Royal Society B 283 (1833): 20160370.

    Google Scholar 

  • Hickling, R., D. Roy, J. Hill, R. Fox, and C. Thomas. 2006. The distributions of a wide range of taxonomic groups are expanding polewards. Global Change Biology 12 (3): 450–455.

    Google Scholar 

  • Hiller, A., H. Kraus, M. Almon, and B. Werding. 2006. The Petrolisthes galathinus complex: species boundaries based on color pattern, morphology and molecules, and evolutionary interrelationships between this complex and other Porcellanidae (Crustacea: Decapoda: Anomura). Molecular Phylogenetics and Evolution 40 (2): 547–569.

    CAS  Google Scholar 

  • Hiller, A., and H.A. Lessios. 2017. Phylogeography of Petrolisthes armatus, an invasive species with low dispersal ability. Scientific Reports 7 (1): 3359.

    Google Scholar 

  • Hollebone, A.L., and M.E. Hay. 2008. An invasive crab alters interaction webs in a marine community. Biological Invasions 10 (3): 347–358.

    Google Scholar 

  • Kelley, A.L. 2014. The role thermal physiology plays in species invasion. Conservation Physiology 2: 1–14.

    Google Scholar 

  • Kinney, K.A., L.M. Pintor, and J.E. Byers. 2019. Does predator-driven, biotic resistance limit the northern spread of the non-native gree porcelain crab, Petrolisthes armatus? Biological Invasions 21 (1): 245–260.

    Google Scholar 

  • Knott DM, Bokyo CB, Harvey A (2000) Introduction of the green porcelain crab, Petrolisthes armatus (Gibbes, 1850), into the South Atlantic Bight. In marine bioinvasions: Proceedings of the first National Conference, January 24–27, 1999, ed J. Pederson, 404, Cambridge, MA: MIT Sea Grant College program.

  • Lafferty, K.D., and A.M. Kuris. 1996. Biological control of marine pests. Ecology 77 (7): 1989–2000.

    Google Scholar 

  • Mack KJ (2017) Populations of the green porcelain crab, Petrolisthes armatus, vary in cold tolerance within the species’northernmost invaded range. Masters Thesis, College of Charleston, Charleston, South Carolina. 99 pp.

  • Mack, K.J., R.D. Podolsky, V. Shervette, A.E. Fowler, and D.H. Wilber. 2019. Spatial and temporal associations between native crabs and the invading green porcelain crab, Petrolisthes armatus, throughout its northernmost invaded range. Estuaries and Coasts 42 (2): 537–547.

    CAS  Google Scholar 

  • Margiotta, A.M., V.R. Shervette, N.H. Hadley, C.J. Plante, and D.H. Wilber. 2016. Species-specific responses of resident crabs to vertical habitat complexity on intertidal oyster reefs. Journal of Experimental Marine Biology and Ecology 477: 7–13.

    Google Scholar 

  • Maris, R.C. 1983. A key to the porcellanid crab zoeae (Crustacea: Decapoda: Anomura) of the north central Gulf of Mexico and a comparison of meristic characters of four species. Gulf Research Reports 3: 237–246.

    Google Scholar 

  • Martel, A.L., and J.B. Madill. 2018. Twenty-six years (1990–2015) of monitoring annual recruitment of the invasive zebra mussel (Dreissena polymorpha) in the Rideau River, a small river system in Eastern Ontario, Canada. Canadian Journal of Zoology 96 (10): 1071–1079.

    Google Scholar 

  • Miranda, I., and F.L. Mantelatto. 2009. Estimating population features of the anomuran crab Petrolisthes armatus (Porcellanidae) in a remaining and impacted mangrove area of the western Atlantic. Journal of Natural History 43 (33-34): 2027–2039.

    Google Scholar 

  • Miranda, I., and F.L. Mantelatto. 2010. Sexual maturity and relative growth of the porcellanid crab Petrolisthes armatus (Gibbes, 1850) from a remnant mangrove area, southern Brazil. Nauplius 18: 87–93.

    Google Scholar 

  • Nelson, K., D. Hedgecock, and W. Borgeson. 1988. Effects of reproduction upon molting and growth in female American lobsters (Homarus americanus). Canadian Journal of Fisheries and Aquatic Sciences 45 (5): 805–821.

    Google Scholar 

  • Oliveira, E., and S. Masunari. 1998. Population relationships between the parasite Aporobopyrus curtatus (Richardson 1904) (Isopoda: Bopyridae) and one of its porcelain crab hosts Petrolisthes armatus (Gibbes, 1850) (Decapoda: Porcellanidae) from Farol Island, southern Brazil. Journal of Natural History 32 (10-11): 1707–1717.

    Google Scholar 

  • Osores, S.J.A., G.A. Ruz, T. Opitz, and M.A. Lardies. 2018. Discovering divergence in the thermal physiology of intertidal crabs along latitudinal gradients using an integrated approach with machine learning. Journal of Thermal Biology 78: 140–150.

    Google Scholar 

  • Pimentel, D., L. Lach, R. Zuniga, and D. Morrison. 2000. Environmental and economic costs of nonindigenous species in the United States. Bioscience 50 (1): 53–65.

    Google Scholar 

  • Pimentel, D., R. Zuniga, and D. Morrison. 2005. Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics 52 (3): 273–288.

    Google Scholar 

  • Pinheiro, M.A.A., M.C.A. João, M.H.A. Leme, A.M.F. Matsunaga, J.P.P. Rio, and P. Hernáez. 2017. Insights of the life history in the porcellanid crab Petrolisthes armatus (Gibbes, 1850) (Crustacea: Anomura: Porcellanidae) from the Southwestern Atlantic coast. Invertebrate Reproduction and Development 4259: 1–12.

    Google Scholar 

  • Pintor, L.M., and J.E. Byers. 2015a. Do native predators benefit from non-native prey? Ecological Letters 18 (11): 1174–1180.

    Google Scholar 

  • Pintor, L.M., and J.E. Byers. 2015b. Individual variation in predator behavior and demographics affects consumption of non-native prey. Behavioral Ecology 26 (3): 797–804.

    Google Scholar 

  • Pitt, N.R., E.S. Poloczanska, and A.J. Hobday. 2010. Climate-driven range changes in Tasmanian intertidal fauna. Marine and Freshwater Research 61 (9): 963–970.

    CAS  Google Scholar 

  • Popp, T., V. Shervette, and D.W. Wilber. 2020. Residency and reproductive patterns of the green porcelain crab, Petrolisthes armatus, on an intertidal oyster reef in its non-native range. Journal of Experimental Marine Biology and Ecology 529: 151399.

    Google Scholar 

  • Pringle, J.M., J.E. Byers, R. He, P. Pappalardo, and J. Wares. 2017. Ocean currents and competitive strength interact to cluster benthic species range boundaries in the coastal ocean. Marine Ecology Progress Series 567: 29–40.

    Google Scholar 

  • R Core Team. 2018. R: A language and environment for statistical computing. Vienna: R Foundation for statistical computing URL https://www.R-project.org/.

    Google Scholar 

  • Sanford, E., J.L. Sones, M. García-Reyes, J.H.R. Goddard, and J.L. Largier. 2019. Widespread shifts in the coastal biota of northern California during the 2014–2016 marine heatwaves. Scientific Reports 9: 1–14.

    Google Scholar 

  • Sax, D., J. Stachowicz, and S. Gaines. 2005. Species invasions: Insights into ecology, evolution, and biogeography. Sunderland: Sinauer Associates, Inc..

    Google Scholar 

  • Shumway, S.E. 1983. Oxygen consumption and salinity tolerance in four brazilian crabs. Crustaceana 44 (1): 76–82.

    Google Scholar 

  • Simberloff, D. 2003. How much information on population biology is needed to manage introduced species? Conservation Biology 17 (1): 83–92.

    Google Scholar 

  • Sorte, C.J.B., S.L. Williams, and J.T. Carlton. 2010. Marine range shifts and species introductions: Comparative spread rates and community impacts. Global Ecology and Biogeography 19 (3): 303–316.

    Google Scholar 

  • Stillman, J.H., and G.N. Somero. 2000. A comparative analysis of the upper thermal tolerance limits of eastern Pacific porcelain crabs, genus Petrolisthes: influences of latitude, vertical zonation, acclimation, and phylogeny. Physiological and Biochemical Zoology 73 (2): 200–208.

    CAS  Google Scholar 

  • Thomas, C.D. 2010. Climate, climate change and range boundaries. Diversity and Distributions 16 (3): 488–495.

    Google Scholar 

  • Tilburg, C.E., J.E. Seay, T.D. Bishop, H.L. Miller, and C. Meile. 2010. Distribution and retention of Petrolisthes armatus in a coastal plain estuary: the role of vertical movement in larval transport. Estuarine, Coastal and Shelf Sciences 88 (2): 260–266.

    Google Scholar 

  • Tolley, S.G., B.B. Brosious, and E.B. Peebles. 2013. Recruitment of the crabs Eurypanopeus depressus, Rhithropanopeus harrisii, and Petrolisthes armatus to oyster reefs: the influence of freshwater inflow. Estuaries and Coasts 36 (4): 820–833.

    CAS  Google Scholar 

  • Wassick, A., J.A. Baeza, A. Fowler, and D. Wilber. 2017. Reproductive performance of the marine green porcelain crab Petrolisthes armatus Gibbes, 1850 in its introduced range favors further range expansion. Aquatic Invastions 12 (4): 469–485.

    Google Scholar 

  • Werding, B., A. Hiller, and R. Lemaitre. 2003. Geographic and depth distributional patterns of western Atlantic Porcellanidae (Crustacea: Decapoda: Anomura), with an updated list of species. Memoirs of Museum Victoria 60 (1): 79–85.

    Google Scholar 

  • Yamano, H., K. Sugihara, and K. Nomura. 2011. Rapid poleward range expansion of tropical reef corals in response to rising sea surface temperatures. Geophysical Research Letters 38: 1–6.

    Google Scholar 

Download references

Acknowledgments

We greatly appreciate the generous assistance of Dr. Dennis Allen and staff at the Baruch Marine Laboratory for providing access to the archived mesoplankton samples collected in North Inlet, SC, and guidance with the sample processing protocol. This publication is Grice Marine Laboratory College of Charleston, Charleston, SC, contribution number 545.

Funding

This work was funded by a grant from the Graduate Program in Marine Biology of the University of Charleston, SC, at the College of Charleston.

Author information

Authors and Affiliations

  1. Grice Marine Laboratory, College of Charleston, 205 Ft. Johnson Road, Charleston, SC, 29412, USA

    Teresa Popp & Dara H. Wilber

Authors
  1. Teresa Popp
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dara H. Wilber
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dara H. Wilber.

Additional information

Communicated by Paul A. Montagna

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Popp, T., Wilber, D.H. Associations Between Winter Temperatures and the Timing and Duration of Annual Larval Recruitment of a Non-native Anomuran Crab. Estuaries and Coasts 44, 1074–1082 (2021). https://doi.org/10.1007/s12237-020-00831-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12237-020-00831-z

Keywords

Search

Navigation