Hostname: page-component-76fb5796d-zzh7m Total loading time: 0 Render date: 2024-04-26T20:03:36.977Z Has data issue: false hasContentIssue false
  • English
  • Français

Gill grooming in middle Cambrian and Late Ordovician trilobites

Published online by Cambridge University Press:  15 February 2023

Jin-bo Hou Open the ORCID record for Jin-bo Hou [Opens in a new window] ,
Nigel C. Hughes Open the ORCID record for Nigel C. Hughes [Opens in a new window]  and
Melanie J. Hopkins
Jin-bo Hou*
Affiliation:
State Key Laboratory for Mineral Deposits Research, School of Earth Sciences and Engineering and Frontiers Science Center for Critical Earth Material Cycling, Nanjing University, Nanjing 210023, China Department of Earth and Planetary Sciences, University of California, Riverside, CA 92521, USA
Nigel C. Hughes
Affiliation:
Department of Earth and Planetary Sciences, University of California, Riverside, CA 92521, USA
Melanie J. Hopkins
Affiliation:
Division of Paleontology (Invertebrates), American Museum of Natural History, New York, NY 10024, USA
*
Author for correspondence: Jin-bo Hou, Email: hou@nju.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

Efficient extraction of oxygen from ambient waters played a critical role in the development of early arthropods. Maximizing gill surface area enhanced oxygen uptake ability but, with gills necessarily exposed to the external environment, also presented the issue of gill contamination. Here we document setae inserted on the dorsal surface of walking legs of the benthic-dwelling middle Cambrian Olenoides serratus and on the gill shaft of the Late Ordovician Triarthrus eatoni. Based on their physical positions relative to gill filaments, we interpret these setae to have been used to groom the gills, removing particles trapped among the filaments. The coordination between setae and gill filaments is comparable to that seen among modern crustaceans, which use a diverse set of setae-bearing appendages to penetrate between gill filaments when grooming. Grooming is known relatively early in trilobite evolutionary history and would have enhanced gill efficiency by maximizing the surface area for oxygen uptake.

Keywords

ethologyrespirationbehaviourearly metazoanLower PalaeozoicTrilobita
Type
Original Article
Information
Geological Magazine , Volume 160 , Issue 5 , May 2023 , pp. 905 - 910
Copyright
© The Author(s), 2023. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alpert, SP (1976) Trilobite and star-like trace fossils from the White-Inyo Mountains, California. Journal of Paleontology 50, 226–39.Google Scholar
Baets, KD, Budil, P, Fatka, O and Geyer, G (2021) Trilobites as hosts for parasites: from paleopathologies to etiologies. In The Evolution and Fossil Record of Parasitism (eds Baets, KD and Huntley, JW), pp. 173–201. Cham: Springer. https://doi.org/10.1007/978-3-030-52233-9_6 CrossRefGoogle Scholar
Batang, ZB and Suzuki, H (2003) Gill-cleaning mechanisms of the burrowing thalassinidean shrimps Nihonotrypaea japonica and Upogebia major (Crustacea: Decapoda). Journal of Zoology 261, 69–77. https://doi.org/10.1017/S0952836903003959 CrossRefGoogle Scholar
Bauer, RT (1979) Antifouling adaptations of marine shrimp (Decapoda: Caridea): gill cleaning mechanisms and grooming of brooded embryos. Zoological Journal of the Linnean Society 65, 281–303. https://doi.org/10.1111/j.1096-3642.1979.tb01097.x CrossRefGoogle Scholar
Bauer, RT (1981) Grooming behavior and morphology in the decapod Crustacea. Journal of Crustacean Biology 1, 153–73. https://doi.org/10.2307/1548154 CrossRefGoogle Scholar
Bauer, RT (1989) Decapod crustacean grooming: functional morphology. In Functional Morphology of Feeding and Grooming in Crustacea (eds Flelgenhauer, BE, Watling, L and Thistle, AB). pp. 49–73. Rotterdam: A. A. Balkema.Google Scholar
Bauer, RT (2013) Adaptive modification of appendages for grooming (cleaning, antifouling) and reproduction in the Crustacea. In Functional Morphology and Diversity (eds Watling, L and Thiel, M). pp. 327–64. New York: Oxford University Press.Google Scholar
Brandt, DS (1996) Epizoans on Flexicalymene (Trilobita) and implications for trilobite paleoecology. Journal of Paleontology 70, 442–9. https://doi.org/10.1017/S0022336000038373 CrossRefGoogle Scholar
Briggs, DEG, Bottrell, SH and Raiswell, R (1991) Pyritization of soft-bodied fossils: Beecher’s Trilobite Bed, Upper Ordovician, New York State. Geology 19, 1221–4. https://doi.org/10.1130/0091-7613(1991)019<1221:POSBFB>2.3.CO;2 2.3.CO;2>CrossRefGoogle Scholar
Briggs, DEG, Erwin, DH and Collier, FJ (1994) The Fossils of the Burgess Shale. Washington, DC, and London: Smithsonian Institution Press, 238 pp.Google Scholar
Cong, P, Ma, X, Williams, M, Siveter, DJ, Siveter, DJ, Gabbott, SE, Zhai, D, Goral, T, Edgecombe, GD and Hou, X (2017) Host-specific infestation in early Cambrian worms. Nature Ecology & Evolution 1, 1465–9. https://doi.org/10.1038/s41559-017-0278-4 CrossRefGoogle ScholarPubMed
Crimes, TP and Droser, ML (1992) Trace fossils and bioturbation: the other fossil record. Annual Review of Ecology and Systematics 23, 339–60. https://doi.org/10.1146/annurev.es.23.110192.002011 CrossRefGoogle Scholar
Farrell, ÚC, Martin, MJ, Hagadorn, JW, Whiteley, T and Briggs, DEG (2009) Beyond Beecher’s Trilobite Bed: widespread pyritization of soft tissues in the Late Ordovician Taconic foreland basin. Geology 37, 907–10. https://doi.org/10.1130/G30177A.1 CrossRefGoogle Scholar
Fortey, RA and Owens, RM (1999) Feeding habits in trilobites. Palaeontology 42, 429–65. https://doi.org/10.1111/1475-4983.00080 CrossRefGoogle Scholar
Hou, J-B, Hughes, NC and Hopkins, MJ (2021) The trilobite upper limb branch is a well-developed gill. Science Advances 7, eabe7377. https://doi.org/10.1126/sciadv.abe7377 CrossRefGoogle ScholarPubMed
Hughes, NC (2001) Ecologic evolution of Cambrian trilobites. In The Ecology of the Cambrian Radiation (eds Zhuravlev, AY and Riding, R). pp. 370–403. New York: Columbia University Press. https://doi.org/10.7312/zhur10612-017 Google Scholar
Key, MM, Schumacher, GA, Babcock, LE, Frey, RC, Heimbrock, WP, Felton, SH, Cooper, DL, Gibson, WB, Scheid, DG and Schumacher, SA (2010) Paleoecology of commensal epizoans fouling Flexicalymene (Trilobita) from the Upper Ordovician, Cincinnati Arch region, USA. Journal of Paleontology 84, 1121–34. https://doi.org/10.1666/10-018.1 CrossRefGoogle Scholar
Li, Y, Williams, M, Harvey, THP, Wei, F, Zhao, Y, Guo, J, Gabbott, S, Fletcher, T, Hou, X and Cong, P (2020) Symbiotic fouling of Vetulicola, an early Cambrian nektonic animal. Communications Biology 3, 1–9. https://doi.org/10.1038/s42003-020-01244-1 CrossRefGoogle ScholarPubMed
Losso, SR and Ortega-Hernández, J (2022) Claspers in the mid-Cambrian Olenoides serratus indicate horseshoe crab–like mating in trilobites. Geology 50, 897–901. https://doi.org/10.1130/G49872.1 CrossRefGoogle Scholar
Nanglu, K and Caron, J-B (2021) Symbiosis in the Cambrian: enteropneust tubes from the Burgess Shale co-inhabited by commensal polychaetes. Proceedings of the Royal Society B 288, 20210061. https://doi.org/10.1098/rspb.2021.0061 CrossRefGoogle ScholarPubMed
Pohle, G (1989) Structure, function, and development of setae on gill-grooming appendages and associated mouthparts of pinnotherid crabs (Decapoda: Brachyura). Canadian Journal of Zoology 67, 1690–707. https://doi.org/10.1139/z89-243 CrossRefGoogle Scholar
Raff, RA and Raff, EC (1970) Respiratory mechanisms and the metazoan fossil record. Nature 228, 1003–5. https://doi.org/10.1038/2281003a0 CrossRefGoogle ScholarPubMed
Seilacher, A (1985) Trilobite palaeobiology and substrate relationships. Transactions of the Royal Society of Edinburgh 76, 231–7. https://doi.org/10.1017/S0263593300010464 CrossRefGoogle Scholar
Seilacher, A (2007) Trace Fossil Analysis. Berlin: Springer, 266 pp.Google Scholar
Sekiguchi, K, Seshimo, H and Sugita, H (1988) Post-embryonic development of the horseshoe crab. Biological Bulletin 174, 337–45. https://doi.org/10.2307/1541959 CrossRefGoogle Scholar
Siveter, DJ, Briggs, DEG, Siveter, DJ and Sutton, MD (2018) A well-preserved respiratory system in a Silurian ostracod. Biology Letters 14, 20180464. https://doi.org/10.1098/rsbl.2018.0464 CrossRefGoogle Scholar
Spruijt, BM, Van Hooff, JA and Gispen, WH (1992) Ethology and neurobiology of grooming behavior. Physiological Reviews 72, 825–52.CrossRefGoogle ScholarPubMed
Stein, M (2013) Cephalic and appendage morphology of the Cambrian arthropod Sidneyia inexpectans Walcott, 1911. Zoologischer Anzeiger 253, 164–78. https://doi.org/10.1016/j.jcz.2013.05.001 CrossRefGoogle Scholar
Stein, M, Waloszek, D and Maas, A (2005) Oelandocaris oelandica and the stem lineage of Crustacea. In Crustacea and arthropod relationships (eds Koenemann, S and Jenner, RA). pp. 55–71. Boca Raton, Florida: CRC Press.Google Scholar
Vanmaurik, LN and Wortham, JL (2014) Grooming as a secondary behavior in the shrimp Macrobrachium rosenbergii (Crustacea, Decapoda, Caridea). Zookeys 457, 55–77. https://doi.org/10.3897/zookeys.457.6292 CrossRefGoogle Scholar
Waloszek, D (2003) Cambrian ‘Orsten’-type preserved arthropods and the phylogeny of Crustacea. In Proceedings of the 18th International Congress of Zoology (eds Legakis, A, Sfenthourakis, S, Polymeni, R and Thessalou-Legaki, M). pp. 69–87. Sofia and Moscow: Pensoft.Google Scholar
Whittington, HB (1975) Trilobites with appendages from the Middle Cambrian, Burgess Shale, British Columbia. Fossils and Strata 4, 97–136.Google Scholar
Whittington, HB and Almond, JE (1987) Appendages and habits of the Upper Ordovician Trilboite Triarthrus eatoni . Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 317, 1–46. https://doi.org/10.1098/rstb.1987.0046 Google Scholar
Wood, RA and Erwin, DH (2018) Innovation not recovery: dynamic redox promotes metazoan radiations. Biological Reviews 93, 863–73. https://doi.org/10.1111/brv.12375 CrossRefGoogle Scholar
Wortham, JL and Pascual, S (2017) Grooming behaviors and gill fouling in the commercially important blue crab (Callinectes sapidus) and stone crab (Menippe mercenaria). Nauplius 25, e2017028. https://doi.org/10.1590/2358-2936e2017028 CrossRefGoogle Scholar
Wortham, JL and Pascual, S (2019) Setal morphology of grooming appendages in blue crabs Callinectes sapidus Rathbun, 1896 and stone crabs Menippe mercenaria (Say, 1818)(Decapoda: Brachyura: Portunidae, Menippidae). Journal of Crustacean Biology 39, 357–77. https://doi.org/10.1093/jcbiol/ruz032 CrossRefGoogle Scholar
Yang, X-Y, Vannier, J, Yang, J, Wang, D and Zhang, X-G (2021) Priapulid worms from the Cambrian of China shed light on reproduction in early animals. Geoscience Frontiers 12, 101234. https://doi.org/10.1016/j.gsf.2021.101234 CrossRefGoogle Scholar
Zhang, Z, Han, J, Wang, Y, Emig, CC and Shu, D (2010) Epibionts on the lingulate brachiopod Diandongia from the Early Cambrian Chengjiang Lagerstatte, South China. Proceedings of the Royal Society B: Biological Sciences 277, 175–81. https://doi.org/10.1098/rspb.2009.0618 CrossRefGoogle ScholarPubMed