Skip to main content
Log in

Active parental care in the peppermint shrimp Lysmata boggessi: the effect of embryo age and circadian cycle

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The presence/absence of active parental care (APC) was tested in the simultaneously hermaphroditic shrimp Lysmata boggessi. Lysmata boggessi was predicted to engage in APC given that the egg masses spawned by hermaphrodites are > 1 mm thick, the theoretical limit that allows sufficient oxygen supply by diffusion in living tissue. Furthermore, APC was predicted to increase in intensity with embryo development. Lastly, the ultrastructure of appendages used for APC was examined and it was predicted that these appendages will bear specialized structures to aid in this function. Hermaphrodites brooding early and late embryos were collected August–November 2017 from near Tavernier, Florida, USA (25.0115°N, 80.5151°W), transported to the laboratory, and maintained in aquaria to describe and quantify APC during day and night. The morphology of an appendage involved in APC was compared with two other appendages not associated with APC using scanning electron microscopy. Lysmata boggessi engaged in APC likely using some behaviors to clean (e.g., grooming using second pereiopods) and provide oxygen to the eggs (e.g., pleopod fanning). Pleopod fanning was performed more frequently by hermaphrodites carrying late compared to early embryos, likely permitting hermaphrodites to minimize problems related to oxygen limitation in older more metabolically active embryos. Lysmata boggessi also engaged in APC both day and night. The 2nd pereiopods have setae that may be well suited for aiding in APC. This study supports evidence that small brooding marine invertebrates that produce small but compact embryo masses engage in APC.

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.

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

Similar content being viewed by others

Data availability statement

All data generated or analyzed during this study are included in this published article (and its supplementary information files).

References

  • Ache BW, Derby CD (1985) Functional organization of olfaction in crustaceans. Trends Neurosci 8:356–360

    Google Scholar 

  • Baeza JA (2006) Testing three models on the adaptive significance of protandric simultaneous hermaphroditism in a marine shrimp. Evolution 60:1840–1850

    PubMed  Google Scholar 

  • Baeza JA (2007a) Sex allocation in a simultaneously hermaphroditic marine shrimp. Evolution 61:2360–2373

    PubMed  Google Scholar 

  • Baeza JA (2007b) No effect of group size on sex allocation in a protandric-simultaneous hermaphroditic shrimp. J Mar Biol Assoc UK 87:1169–1174

    Google Scholar 

  • Baeza JA (2007c) Male mating opportunities affect sex allocation in a protandric simultaneous hermaphroditic marine shrimp. Behav Ecol Sociobiol 61:365–370

    Google Scholar 

  • Baeza JA (2008) Protandric simultaneous hermaphroditism in the shrimps Lysmata bahia and L. intermedia. Invertebr Biol 127:181–188

    Google Scholar 

  • Baeza JA (2009) Protandric simultaneous hermaphroditism is a conserved trait in Lysmata (Caridea: Lysmatidae): implications for the evolution of hermaphroditism in the genus. Smithson Contrib Mar Sci 38:95–110

    Google Scholar 

  • Baeza JA (2013) Multi-locus molecular phylogeny of broken-back shrimps (genus Lysmata and allies): a test of the ‘Tomlinson-Ghiselin’ hypothesis explaining the evolution of simultaneous hermaphroditism. Mol Evol Phylogenetics 69:46–62

    Google Scholar 

  • Baeza JA (2018a) Sexual selection and mixed sex expression: adolescent protandry, phenotypic tradeoffs and ‘unconventional’ sex allocation estimates in a protandric-simultaneous hermaphrodite. Front Mar Sci 5:260. https://doi.org/10.3389/fmars.2018.00260

    Article  Google Scholar 

  • Baeza JA (2018b) Sexual systems in shrimp (Infraorder Caridea Dana, 1852), with special reference to the historical origin and adaptive value of protandric simultaneous hermaphroditism. In: Leonard J (ed) Transitions between sexual systems. Springer, New York, pp 269–310

    Google Scholar 

  • Baeza JA, Bauer RT (2004) Experimental test of socially mediated sex change in a protandric simultaneous hermaphrodite, the marine shrimp Lysmata wurdemanni (Caridea: Hippolytidae). Behav Ecol Sociobiol 55:544–550

    Google Scholar 

  • Baeza JA, Behringer DC (2017) Integrative taxonomy of the ornamental ‘peppermint’ shrimp public market and population genetics of Lysmata boggessi, the most heavily traded species worldwide. PeerJ 5:e3786. https://doi.org/10.7717/peerj.3786

    Article  PubMed  PubMed Central  Google Scholar 

  • Baeza JA, Fernández M (2002) Active brood care in Cancer setosus (Crustacea: Decapoda: Cancridae): the relationship between female behaviour, embryo oxygen consumption, and the cost of brooding. Funct Ecol 16:241–251

    Google Scholar 

  • Baeza JA, Reitz J, Collin R (2007) Protandric simultaneous hermaphroditism and sex ratio in the shrimp Lysmata nayaritensis. J Nat Hist 41:2843–2850

    Google Scholar 

  • Baeza JA, Schubart CD, Zillner P, Fuentes S, Bauer RT (2009) Molecular phylogeny of shrimps from the genus Lysmata (Caridea: Hippolytidae): the evolutionary origins of protandric simultaneous hermaphroditism and pair-living. Biol J Linnean Soc 96:415–424

    Google Scholar 

  • Baeza JA, Behringer DC, Hart R, Dickson M, Anderson JR (2014) Reproductive biology of the marine ornamental shrimp Lysmata boggessi in the south-eastern Gulf of Mexico. J Mar Biol Assoc UK 94:141–149

    Google Scholar 

  • Baeza JA, Guéron R, Simpson L, Ambrosio LJ (2016a) Population distribution, host-switching, and chemical sensing in the symbiotic shrimp Lysmata pederseni: implications for its mating system in a changing reef seascape. Coral Reefs 35:1213–1224

    Google Scholar 

  • Baeza JA, Simpson L, Ambrosio LJ, Mora N, Childress M (2016b) Active parental care, reproductive performance, and a novel egg predator affecting reproductive investment in the Caribbean spiny lobster Panulirus argus. BMC Zool 1:6. https://doi.org/10.1186/s40850-016-0006-6

    Article  Google Scholar 

  • Bauer RT (1975) Grooming behaviour and morphology of the caridean shrimp Pandalus danae Stimpson (Decapoda: Natantia: Pandalidae). J Linn Soc (Zool) 56:45–71

    Google Scholar 

  • Bauer RT (1981) Grooming behavior and morphology in the decapod Crustacea. J Crustac Biol 1:153–173

    Google Scholar 

  • Bauer RT (1989) Decapod crustacean grooming: functional morphology, adaptive value, and phylogenetic significance. Functional morphology of feeding and grooming in Crustacea. Crustac Issues 6:49–73

    Google Scholar 

  • Bauer RT (2004) Remarkable shrimps: adaptations and natural history of the carideans. University of Oklahoma Press, Norman

    Google Scholar 

  • Bauer RT (2013) Adaptive modification of appendages for grooming (cleaning, antifouling) and reproduction in the Crustacea. Funct Morph Divers 1:327–364

    Google Scholar 

  • Bauer RT, Holt GJ (1998) Simultaneous hermaphroditism in the marine shrimp Lysmata wurdemanni (Caridea: Hippolytidae): an undescribed sexual system in the decapod Crustacea. Mar Biol 132:223–235

    Google Scholar 

  • Bauer RT, Newman WA (2004) Protandric simultaneous hermaphroditism in the marine shrimp Lysmata californica (Caridea: Hippolytidae). J Crustac Biol 24:131–139

    Google Scholar 

  • Bruce AJ (1983) Lysmata debelius, new species, a new hippolytid shrimp from the Philippines. Revue Francaise d’Aquariologie et Herpetol 4:115–120

    Google Scholar 

  • Calvo NS, Roldan-Luna M, Argáez-Sosa JA, Martínez-Moreno GL, Mascaró M, Simões N (2016) Reflected-light influences the coloration of the peppermint shrimp, Lysmata boggessi (Decapoda: Caridea). J World Aquacult Soc 47:701–711

    Google Scholar 

  • Chaffee C, Strathmann RR (1984) Constraints on egg masses. I. Retarded development within thick egg masses. J Exp Mar Biol Ecol 84:73–83

    Google Scholar 

  • Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, Princeton

    Google Scholar 

  • De Vries MC, Rittschof D, Forward RB Jr (1991) Chemical mediation of larval release behaviors in the crab Neopanope sayi. Biol Bull 180:1–11

    PubMed  Google Scholar 

  • Eriksson SP, Nabbing M, Sjöman E (2006) Is brood care in Nephrops norvegicus during hypoxia adaptive or a waste of energy? Funct Ecol 20:1097–1104

    Google Scholar 

  • Essock-Burns T, Wepprich A, Thompson A, Rittschof D (2016) Enzymes manage biofilms on crab surfaces aiding in feeding and antifouling. J Exp Mar Biol Ecol 479:106–113

    CAS  Google Scholar 

  • Felgenhauer BE (1987) Techniques for preparing crustaceans for scanning electron microscopy. J Crustac Biol 7:71–76

    Google Scholar 

  • 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

    Google Scholar 

  • Fernández M, Ruiz-Tagle N, Cifuentes S, Portner HO, Arntz W (2003) Oxygen-dependent asynchrony of embryonic development in embryo masses of brachyuran crabs. Mar Biol 142:559–565

    Google Scholar 

  • Fleischer J, Grell M, Høeg JT, Olesen J (1992) Morphology of grooming limbs in species of Petrolisthes and Pachycheles (Crustacea: Decapoda: Anomura: Porcellanidae): a scanning electron microscopy study. Mar Biol 113:425–435

    Google Scholar 

  • Förster C, Baeza JA (2001) Active brood care in the anomuran crab Petrolisthes violaceus (Decapoda: Anomura: Porcellanidae): grooming of brooded embryos by the fifth pereiopods. J Crustac Biol 21:606–615

    Google Scholar 

  • Garm A (2004) Revising the definition of the crustacean seta and setal classification systems based on examinations of the mouthpart setae of seven species of decapods. Zool J Linnean Soc 142:233–252

    Google Scholar 

  • Garm A, Watling L (2013) The Crustacean integument: setae, setules, and other ornamentation. Funct Morph Divers 1:167–198

    Google Scholar 

  • Hertzler PL (2005) Cleavage and gastrulation in the shrimp Penaeus (Litopenaeus) vannamei (Malacostraca, Decapoda, Dendrobranchiata). Arthropod Struct Dev 34:455–469

    Google Scholar 

  • Jacques F (1989) The setal system of crustaceans: types of setae, groupings, and functional morphology. Functional morphology of feeding and grooming in Crustacea. Crustac Issues 6:1–13

    Google Scholar 

  • Keiler J, Richter S (2011) Morphological diversity of setae on the grooming legs in Anomala (Decapoda: Reptantia) revealed by scanning electron microscopy. Zool Anz 250:343–366

    Google Scholar 

  • Limbaugh C, Pederson H, Chace FA Jr (1961) Shrimps that clean fishes. Bull Mar Sci 11:237–257

    Google Scholar 

  • Martin P, Bateson P (1986) Measuring behaviour—an introductory guide. Cambridge University Press, Cambridge

    Google Scholar 

  • Naylor JK, Taylor EW (1999) Heart rate and gill ventilation in ovigerous and non-ovigerous edible crabs, Cancer pagurus: the effect of disturbance, substrate and starvation. Mar Behav Physiol 32:129–145

    Google Scholar 

  • Phillips G (1971) Incubation of the English prawn Palaemon serratus. J Mar Biol Assoc UK 51:43–48

    Google Scholar 

  • Pohle G (1989) Gill and embryo grooming in lithodid crabs: comparative functional morphology based on Lithodes maja. Crustac Issues 6:75–94

    Google Scholar 

  • Prosser CL (1973) Comparative animal physiology. Saunders, Philadelphia

    Google Scholar 

  • Reinsel KA, Pagel K, Kissel 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 94:1009–1017

    CAS  Google Scholar 

  • Rhyne AL, Lin J (2006) A western Atlantic peppermint shrimp complex: redescription of Lysmata wurdemanni, description of four new species, and remarks on Lysmata rathbunae (Crustacea: Decapoda: Hippolytidae). Bull Mar Sci 79:165–204

    Google Scholar 

  • Ritchie LE, Høeg JT (1981) The life history of Lernaeodiscus porcellanae (Cirripedia: Rhizocephala) and co evolution with its porcellanid host. J Crustac Biol 1:334–347

    Google Scholar 

  • Rittschof D (1992) Chemosensation in the daily life of crabs. Am Zool 32:363–369

    CAS  Google Scholar 

  • Rittschof D, Cohen JH (2004) Crustacean peptide and peptide-like pheromones and kairomones. Peptides 25:1503–1516

    CAS  PubMed  Google Scholar 

  • Romero A, Turnbull MW, Baeza JA (2018) Embryonic development in the peppermint shrimp, Lysmata boggessi (Caridea: Lysmatidae). Biol Bull 234:165–179

    Google Scholar 

  • Royle NJ, Smiseth PT, Kolliker M (2012) The evolution of parental care. Oxford University Press, Cambridge

    Google Scholar 

  • Ruiz-Tagle N, Fernández M, Pörtner HO (2002) Full time mothers: daily rhythms in brooding and nonbrooding behaviors of brachyuran crabs. J Exp Mar Biol Ecol 276:31–47

    Google Scholar 

  • Saigusa M (1994) A substance inducing the loss of premature embryos from ovigerous crabs. Biol Bull 186:81–89

    CAS  PubMed  Google Scholar 

  • Silva P, Luppi TA, Spivak ED (2003) Limb autotomy, epibiosis on embryos, and brooding care in the crab Cyrtograpsus angulatus (Brachyura: Varunidae). J Mar Biol Assoc UK 83:1015–1022

    Google Scholar 

  • Silva PV, Luppi TA, Spivak ED (2007) Epibiosis on eggs and brooding care in the burrowing crab Chasmagnathus granulatus (Brachyura: Varunidae): comparison between mudflats and salt marshes. J Mar Biol Assoc UK 87:893–901

    Google Scholar 

  • Strathmann RR, Strathmann MF (1995) Oxygen supply and limits on aggregation of embryos. J Mar Biol Assoc UK 75:413–428

    Google Scholar 

  • Thiel M (2003) Extended parental care in crustaceans: an update. Rev Chil Hist Nat 76:205–218

    Google Scholar 

  • VanMaurik LN, Wortham JL (2014) Grooming as a secondary behavior in the shrimp Macrobrachium rosenbergii (Crustacean, Decapoda, Caridea). ZooKeys 457:55–77

    Google Scholar 

  • Watling L (1989) A classification system for crustacean setae based on the homology concept. Crustac Issues 6:15–26

    Google Scholar 

  • Wortham JL, LaVelle AD (2016) Setal morphology of grooming appendages in the spider crab, Libinia dubia. J Morph 277:1045–1061

    PubMed  Google Scholar 

  • Wortham JL, Pascual S (2017) Grooming behaviors and gill fouling in the commercially important blue crab (Callinectes sapidus) and stone crabs (Menippe mercenaria). Nauplius 25:1–18

    Google Scholar 

  • Wortham JL, VanMaurik LN (2012) Morphology and morphotypes of the Hawaiian river shrimp, Macrobrachium Grandimanus. J Crustac Biol 32:545–556

    Google Scholar 

  • Wortham JL, VanMaurik LN, Price WW (2014) Setal morphology of the grooming appendages of Macrobrachium rosenbergii (Crustacea: Decapoda: Caridea: Palaemonidae) and review of decapod setal classification. J Morph 275:634–649

    PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by Creative Inquiry, a program at Clemson University that engages undergraduates in research, learning and cross-disciplinary interactions. We also thank The Department of Biology, College of Natural and Health Sciences. Dr. Stan Rice provided assistance using the scanning electron microscope and Dr. Raymond Bauer provided guidance on grooming structures. Tom Gariepy provided editorial comments. We also thank the editor and two anonymous referees whose comments permitted us to improve the quality of the manuscript.

Funding

This study was funded by Creative Inquiry Project Number 1560107, Clemson University and by the Evan Chipouras Award, The University of Tampa, for microscopy work.

Author information

Authors and Affiliations

Authors

Contributions

JAB contributed to the study conception and design. Material preparation, data collection and analysis were performed by JAB, XL, LK, and JW. The first draft of the manuscript was written by JAB and JLW; all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to J. Antonio Baeza.

Ethics declarations

Conflict of interest

Author J. Antonio Baeza declares that he has no conflict of interest. Author Xiaomi Liu declares that she has no conflict of interest. Author Laurie Kostecka declares that she has no conflict of interest. Author Jennifer Wortham declares that she has no conflict of interest.

Ethical approval

All applicable international, national and/or institutional guidelines for sampling, care and experimental use of organisms for the study have been followed.

Additional information

Responsible Editor: J. Grassle.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Reviewed by A. A. David, J. T. Hoeg and D. Rittschof.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (AVI 53284 kb)

Supplementary material 2 (AVI 36401 kb)

Supplementary material 3 (PDF 211 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Baeza, J.A., Liu, X., Kostecka, L. et al. Active parental care in the peppermint shrimp Lysmata boggessi: the effect of embryo age and circadian cycle. Mar Biol 166, 132 (2019). https://doi.org/10.1007/s00227-019-3579-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-019-3579-0

Navigation