Body-size changes of latest Permian brachiopods in varied palaeogeographic settings in South China and implications for controls on animal miniaturization in a highly stressed marine ecosystem

https://doi.org/10.1016/j.palaeo.2017.02.024Get rights and content

Highlights

  • Paleobathymetry controlled body-size changes in the latest Permian in South China.

  • Both oxygen and food availability played a more important role in controlling the differences of body sizes.

  • Several depressed factors have compounded and caused small body sizes in deeper waters during the latest Permian.

  • Brachiopod miniaturization near the PTB was collectively driven by anoxia, food restriction and high temperature.

Abstract

Research on the dynamics of body-size changes in varied water depths can provide important insights into the evolution of palaeoenvironments through time. This paper attempts to investigate how the body sizes of two most commonly found chonetid brachiopod species in the uppermost Permian in South China varied with palaeo-bathymetry. The result shows that there is a broadly negative correlation between the latest Permian brachiopod body size and water depth. There is no simple singular variable that could explain this correlation because bathymetry is correlated, either linearly or nonlinearly, to food availability, redox condition and habitat temperature, as well as substrate conditions. Overall, we found that both oxygen and food availability played a more important role in controlling the differences of body sizes, and specifically several depressed factors (low food availability, anoxia, or abnormal temperature) have compounded and caused small body sizes in deeper waters during the latest Permian. We propose that the brachiopod miniaturization during the Permian-Triassic crisis in South China was collectively driven by anoxia, food restriction and high temperature.

Introduction

Body size is a key, intrinsic character of any organism and profoundly affects its biology and ecology (Calder, 1984, Jablonski, 1996). The study of body-size changes in space and time is important for understanding macro-evolution of organisms and ecosystems; it also provides important insights into the evolution history and dynamics of past environments. The commonly proposed controls on body-size changes include oxygen fluctuations (Savrda and Bottjer, 1986, Payne et al., 2008, Payne et al., 2013), food availability (Hallam, 1965, Rheault and Rice, 1996, Twitchett, 2007, He et al., 2010) and temperature changes (Hunt et al., 2010, Sheridan and Bickford, 2011, Edeline et al., 2013), as well as substrate conditions. As many of these factors vary with water depth, the relationship between body size and bathymetry is a critical aspect of studies on body-size changes (Anderson, 1971, Thiel, 1975, Peck and Harper, 2010, Shi et al., 2016). Numerous researches have been undertaken on the Permian-Triassic body-size changes of conodonts, brachiopods, siliceous sponges, ostracods or foraminifers in South China (He et al., 2007a, He et al., 2010, He et al., 2015a, He et al., 2016, Peng et al., 2007, Luo et al., 2008, Song et al., 2011, Liu et al., 2013, Chu et al., 2016, Zhang et al., 2016). Most of these studies have focused on the patterns of body-size changes of individual taxa across time and their possible underlying control mechanisms, and a few (e.g., He et al., 2010, Liu et al., 2013) have addressed the relationship between size changes in relation to primary productivity and redox palaeoproxies in the context of palaeobathymetry. Most recently, based on a global dataset of Changhsingian brachiopod orders, Shi et al. (2016) examined the relationship of Changhsingian brachiopod body-size changes in relation to the onshore-offshore-basin gradient.

The present paper aims to investigate body-size changes of latest Permian brachiopods across different bathymetrically controlled palaeoenvironmental settings within the South China basin. For this purpose, we chose two most commonly found Changhsingian chonetid brachiopod species, Tethyochonetes pigmaea and Tethyochonetes quadrata, from six different sections, which together constituted an approximately-defined basinwide bathymetric gradient spanning the shallow-water clastic shelf, shallow-water carbonate platform and ramp, and deep-water siliceous basinal settings (see below).

Section snippets

Geographical location, palaeogeographical setting and classification on depth-related palaeoenvironments

The studied sections include Zhongzhai, Huangzhishan, Daoduishan, Majiashan, Rencunping and Dongpan sections in South China. Geographically, Huangzhishan is located 12 km west of Huzhou City, Zhejiang Province (Fig. 1A). Daoduishan is located about 2.5 km northeast of the Meishan Section D of Changxing County, Zhejiang Province, where the GSSP of the Permian-Triassic Boundary (PTB) has been defined (Yin et al., 2001) (Fig. 1A). Majiashan is located about 55 km southeast of Hefei City, Anhui

Age analysis and correlation

At Zhongzhai, the PTB has been placed between Beds 29 and 30 (Fig. 3), according to the U-Pb age of 252.24 ± 0.13 Ma in Bed 29, which is basically equivalent to the calibrated PTB age of 252.17 ± 0.06 Ma in Bed 27c at the GSSP section of Meishan (Shen et al., 2011, Zhang et al., 2014). Beds 4 to 28 of this section have been assigned to the Changhsingian, based on the abundance of brachiopod Tethyochonetes pigmaea (typical for the Changhsingian in South China, see Shen and Archbold, 2002, Zhang et

Methods of brachiopod collection, body size measurement and definition

The studied specimens for Tethyochonetes pigmaea and T. quadrata were mainly collected from the Changhsingian (or the upper Changhsingian) at the studied sections (Table 1). All related brachiopods found during excavating were collected, including complete and incomplete individuals, but only the complete individuals of Tethyochonetes pigmaea and T. quadrata were chosen for body-size measuring for the purpose of this paper.

The width of each brachiopod individual refers to the maximum shell

Body-size profiles of T. pigmaea and T. quadrata through studied sections

The mean sizes (X) for T. pigmaea from Beds 18 to 36 of Huangzhishan fluctuated significantly, from 2.88 mm to 7.08 mm, while that of T. quadrata from the same section first slightly fluctuated from 6.22 mm to 7.26 mm from Beds 18 to 24, and then became reduced to the end of Changhsingian (Table 1, Fig. 3).

The mean sizes (X) for T. pigmaea from Beds 4 to 27-6 at Zhongzhai slightly fluctuated, from 4.50 mm to 5.38 mm, while the size profile for T. quadrata from Beds 4 to 27-5 of the same section

Taphonomic features of brachiopods

Brachiopods collected from Huangzhishan and Zhongzhai lack any evidence of abrasion. They are randomly distributed on bedding surfaces without any preferred orientation; they are abundantly preserved with articulated valves, indicating very limited or no post-mortem transportation (Chen and Shi, 1999, Chen et al., 2010). Brachiopods collected from Daoduishan have both complete and incomplete valves, but these valves are randomly-arranged on bedding surface, suggesting limited transportation

Acknowledgments

We wish to express sincere thanks to two reviewers for offering good comments and suggestions for the revision of this manuscript. This paper has been supported by NSFC (Grant Nos. 41372030, 40872008, 40502001), the Foundation of the Geological Survey of China (1212011220529), the Ministry of Education of China (B08030 of 111 Project, NCET-10-0712), and an Australian Research Council (ARC DP150100690) research grant to GRS.

References (86)

  • J.J. Helly et al.

    Global distribution of naturally occurring marine hypoxia on continental margins

    Deep-Sea Res. I

    (2004)
  • A. Immenhauser

    Estimating palaeo-water depth from the physical rock record

    Earth-Sci. Rev.

    (2009)
  • G.S. Li et al.

    Fluctuations of redox conditions across the Permian-Triassic boundary-new evidence from the GSSP section in Meishan of South China

    Palaeogeogr. Palaeoclimatol. Palaeoecol.

    (2016)
  • G.M. Luo et al.

    Size variation of conodont elements of the Hindeodus–Isarcicella clade during the Permian–Triassic transition in South China and its implication for mass extinction

    Palaeogeogr. Palaeoclimatol. Palaeoecol.

    (2008)
  • G.M. Luo et al.

    Vertical δ13Corg gradients record changes in planktonic microbial community composition during the end-Permian mass extinction

    Palaeogeogr. Palaeoclimatol. Palaeoecol.

    (2014)
  • C. Neira et al.

    Meiofaunal distributions on the Peru margin: relationship to oxygen and organic matter availability

    Deep-Sea Res. I

    (2001)
  • Y. Peng et al.

    How and why did the Lingulidae (Brachiopoda) not only survive the end-Permian mass extinction but also thrive in its aftermath?

    Palaeogeogr. Palaeoclimatol. Palaeoecol.

    (2007)
  • M.A. Salamon et al.

    Dwarfism of irregular echinoids (Echinocorys) from Poland during the Campanian-Maastrichtian boundary event

    Palaeogeogr. Palaeoclimatol. Palaeoecol.

    (2016)
  • S.D. Schoepfer et al.

    Total organic carbon, organic phosphorus, and biogenic barium fluxes as proxies for paleomarine productivity

    Earth Sci. Rev.

    (2015)
  • J. Shen et al.

    Marine productivity changes during the end-Permian crisis and Early Triassic recovery

    Earth Sci. Rev.

    (2015)
  • G.R. Shi et al.

    Nearshore-offshore-basin species diversity and body size variation patterns in Late Permian (Changhsingian) brachiopods

    Palaeogeogr. Palaeoclimatol. Palaeoecol.

    (2016)
  • H.J. Song et al.

    Evolutionary dynamics of the Permian-Triassic foraminifer size: evidence for Lilliput effect in the end-Permian mass extinction and its aftermath

    Palaeogeogr. Palaeoclimatol. Palaeoecol.

    (2011)
  • R.J. Twitchett

    The Lilliput effect in the aftermath of the end-Permian extinction event

    Palaeogeogr. Palaeoclimatol. Palaeoecol.

    (2007)
  • H.T. Wu et al.

    Changes of paleobiogeographic distributions of Neochonetes and Fusichonetes (Brachiopoda) in the late Paleozoic and earliest Mesozoic and the causes

    Palaeoworld

    (2016)
  • Y. Zhang et al.

    Restudy of conodont biostratigraphy of the Permian–Triassic boundary section in Zhongzhai, southwestern Guizhou Province, South China

    J. Asian Earth Sci.

    (2014)
  • Y. Zhang et al.

    Significant pre-mass extinction animal body-size changes: evidences from the Permian-Triassic boundary brachiopod faunas of South China

    Palaeogeogr. Palaeoclimatol. Palaeoecol.

    (2016)
  • R.R. Alexander

    Comparative hydrodynamic stability of brachiopod shells on current-scoured arenaceous substrates

    Lethaia

    (1984)
  • E.J. Anderson

    Environmental models for Paleozoic communities

    Lethaia

    (1971)
  • D.P.G. Bond et al.

    Pyrite framboid study of marine Permian-Triassic boundary sections: a complex anoxic event and its relationship to contemporaneous mass extinction

    Geol. Soc. Am. Bull.

    (2010)
  • K.R. Brom et al.

    The Lilliput effect in crinoids at the end of the oceanic anoxic event 2: a case study from Poland

    J. Paleontol.

    (2015)
  • W.A. Calder

    Size, Function, and Life History

    (1984)
  • Z.Q. Chen et al.

    Chuiella gen. nov. (Brachiopoda) and palaeoecology from the Lower Carboniferous of the Kunlun Mountains, NW China

    Alcheringa

    (1999)
  • J. Chen et al.

    Conodont succession around the Permian-Triassic boundary at the Huangzhishan section, Zhejiang and its stratigraphic correlation

    Acta Palaeontol. Sin.

    (2008)
  • Z.Q. Chen et al.

    Environmental and biotic turnover across the Permian-Triassic boundary on a shallow carbonate platform in western Zhejiang, South China

    Aust. J. Earth Sci.

    (2009)
  • B. Chen et al.

    Discovery of cool-water, deep-water facies invertebrates of the latest Permian from Youjiang basin, South China and the geological significance

  • D.L. Chu et al.

    Lilliput effect in freshwater ostracods during the Permian-Triassic extinction

    Palaeogeogr. Palaeoclimatol. Palaeoecol.

    (2016)
  • E. Edeline et al.

    Ecological emergence of thermal clines in body size

    Glob. Chang. Biol.

    (2013)
  • K.M. Empson-Morin

    Depth and latitude distribution of radiolarian in Campanian (Late Cretaceous) tropical and subtropical oceans

    Micropaleontology

    (1984)
  • Q.L. Feng et al.

    Uppermost Changhsingian (Permian) radiolarian fauna from southern Guizhou, southwestern China

    J. Paleontol.

    (2002)
  • Q.L. Feng et al.

    Principles, Methods and Examples on the Regional Stratigraphy in Orogenic Belt

    (2000)
  • S.Z. Gu et al.

    The latest Permian deep-water fauna: latest Changhsingian small foraminfers from southwestern Guangxi, South China

    Micropaleontology

    (2007)
  • B.W. Gui et al.

    Late Changhsingian (latest Permian) radiolarians from Chaohu, Anhui

    J. Earth Sci.

    (2009)
  • L.D. Guo et al.

    Dynamics of dissolved organic carbon (DOC) in oceanic environments

    Limnol. Oceanogr.

    (1995)
  • Cited by (22)

    • Temporal shell-size variations of bivalves in South China from the Late Permian to the early Middle Triassic

      2023, Palaeogeography, Palaeoclimatology, Palaeoecology
      Citation Excerpt :

      Both extrinsic (abiotic) and intrinsic (biotic) factors have been proposed to explain body size changes during the end-Permian mass extinction and subsequent biotic recovery, although only a few studies have discussed the intrinsic controls, i.e., low predation or competition pressure (Payne et al., 2005; Chen et al., 2019). Most studies highlight extrinsic factors such as global warming, ocean anoxia, and food shortages, which are also known as ecophenotypic controls (Twitchett, 2007; Rego et al., 2012; He et al., 2017; Wu et al., 2019; Foster et al., 2020). The Lilliput effect among bivalves in the immediate aftermath of the end-Permian mass extinction could have been caused by the combination of severe environmental factors, including global warming and marine anoxia.

    • Periodic fluctuations of marine oxygen content during the latest Permian

      2020, Global and Planetary Change
      Citation Excerpt :

      The frequent anoxia/euxinia fluctuations across the South China Sea may have represented a major stress factor adversely affecting the stability and resilience of the marine ecosystem prior to the end-Permian mass extinction. Seemingly critical ecosystem-wide changes were already underway and probably even accelerating prior to the EPME, as has already been noted from recent studies on body-size changes of marine benthos and benthic marine community during the Permian–Triassic transition fauna before EPME (Zhang et al., 2016; He et al., 2017). Integration of the results from previous geochemical studies (Xiang et al., 2016) and cyclostratigraphical data (Wu et al., 2013) studies with the analysis of uppermost Permian pyrite framboids and bioturbation structures presented in this study reveals frequent fluctuations of coupled anoxic/euxinic to dysoxic/oxic episodes occurred in the deep water settings of South China, just before the EPME.

    • Evolutionary and ecophenotypic controls on bivalve body size distributions following the end-Permian mass extinction

      2020, Global and Planetary Change
      Citation Excerpt :

      Body size of most faunal groups is, on average, smaller during the Early Triassic than the body size of their pre-extinction and Middle Triassic counterparts, i.e., species within genera and genera within phyla (Twitchett, 2001, 2007; Hautmann and Nützel, 2005; Payne, 2005; Rego et al., 2012; Chu et al., 2015; Forel et al., 2015; Schaal et al., 2015; Chen et al., 2019). High-resolution studies showed that the Lilliput effect associated with the end-Permian mass extinction started prior to the mass extinction (He et al., 2007b; He et al., 2010, 2015; Shi et al., 2016; Zhang et al., 2016; He et al., 2017; Kiessling et al., 2018) and an initial recovery in the late Griesbachian (Twitchett, 1999, 2007; Metcalfe et al., 2011; Posenato et al., 2014). Subsequent size reductions, however, have been recorded in conodonts for the late Griesbachian and late Smithian indicative of subsequent biotic crises following the end-Permian mass extinction (Chen et al., 2013; Leu et al., 2018; Wu et al., 2019).

    • Size variation of brachiopods from the Late Permian through the Middle Triassic in South China: Evidence for the Lilliput Effect following the Permian-Triassic extinction

      2019, Palaeogeography, Palaeoclimatology, Palaeoecology
      Citation Excerpt :

      In general, evolutionary size changes may result from changes in the abiotic or biotic environment (Fig. 8). Previous studies have highlighted three possible selective pressures to explain the generally small sizes of Early Triassic marine organisms: (1) physical environmental constraints (e.g., hypoxia) (Fraiser and Bottjer, 2004; Twitchett, 2007; He et al., 2010, 2017; Song et al., 2011; Shi et al., 2016), (2) low food availability (Twitchett, 2001; He et al., 2010, 2017), and (3) low predation or competition pressure (Payne, 2005). The end-Permian and the earliest Triassic geologic record is rife with evidence of potential environmental constraints on body size.

    View all citing articles on Scopus
    View full text