Examining the Ladinian crisis in light of the current knowledge of the Triassic biodiversity changes

Accepted Manuscript Examining the Ladinian crisis in light of the current knowledge of the Triassic biodiversity changes

Dmitry A. Ruban PII: DOI: Reference:

S1342-937X(16)30263-5 doi: 10.1016/j.gr.2017.05.004 GR 1806

To appear in: Received date: Revised date: Accepted date:

9 October 2016 21 April 2017 8 May 2017

Please cite this article as: Dmitry A. Ruban , Examining the Ladinian crisis in light of the current knowledge of the Triassic biodiversity changes, (2017), doi: 10.1016/ j.gr.2017.05.004

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ACCEPTED MANUSCRIPT Examining the Ladinian crisis in light of the current knowledge of the Triassic biodiversity changes

Dmitry A. Ruban Southern Federal University, 23-ja linija Street 43, Rostov-na-Donu, 344019, Russia

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E-mail address: [email protected] Telephone number: +7(903)4634344

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ABSTRACT

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Several mass extinctions are known from the history of life, but knowledge about "minor" biotic crises remains incomplete. The Ladinian is the second stage of the Middle

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Triassic epoch. Available reconstructions of the diversity dynamics of fossil organisms

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across the entire Triassic allow the proposed Ladinian biotic crisis to be investigated. Total biodiversity curves (both the conventional curve and that based on sampling standardization)

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fail to identify the crisis, but this may be explained by low resolution data or "noise". In fact,

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the global generic diversity of ammonoids, brachiopods, and tetrapods declined significantly (by 1.1–2.5 times) during the Ladinian, as did the species diversity of conodonts. Bivalves radiated, but their origination rate also decreased during the Ladinian. Land plants were

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apparently unaffected. Based on the representative regional record for the Northwestern

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Caucasus, the number of macroinvertebrate genera dropped by ~7.5 times, and brachiopods almost totally disappeared; foraminifers were also affected significantly. Thus, the proposed biotic crisis appears to have been selective. It appears the Ladinian biotic crisis was a relatively long-term event, and its magnitude is comparable to that of other "minor" mass extinctions, e.g., those of the Silurian, Early Jurassic, or end-Cenomanian. There are several possible explanations for what caused the Ladinian biotic crisis. It is possible that global climate cooling was responsible, although it is unclear why the palaeobiogeographical differentiation was not favourable for a biotic radiation. A eustatic explanation for the drop

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ACCEPTED MANUSCRIPT in diversity is unlikely. Instead, the crisis was mostly likely caused by unstable recovery of the Earth's biota after the end-Permian catastrophe. Keywords: Biodiversity; Eustasy; Mass extinction; Palaeobiogeography; Triassic.

1. Introduction

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Several catastrophic perturbations during the Phanerozoic have been previously

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established. These include the so-called "Big Five" mass extinctions (end-Ordovician, Late

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Devonian, end-Permian, end-Triassic, and end-Cretaceous), as well as a series of other crises (e.g., Early Jurassic, late Cenomanian, etc.). Their chronology, magnitude, and possible

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triggers have been discussed in well-known contributions by Raup and Sepkoski (1982), Benton (1995), Hallam and Wignall (1997), Bambach et al. (2004), Jablonski (2005), and

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many others. Thus at first glance, it would appear that mass extinctions are well understood. However, this impression is inaccurate. There is still much to learn about these events (e.g.,

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Twitchett, 2006). On the one hand, the example of the Early Jurassic

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(Pliensbachian/Toarcian) crisis (Wignall et al., 2006; Caruthers et al., 2013; Caswell, Coe, 2014; Krencker et al., 2014; Guex et al., 2016) demonstrates that the real magnitude of some

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events may have been previously underestimated. Additionally, it is likely that other biotic crises can be detected in the palaeontological record when more comprehensive data from

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more fossil groups and from more regions are considered. Of course, it seems to be too optimistic to expect discoveries of additional events as large as the end-Permian or endCretaceous catastrophes. However, biotic crises of smaller magnitude may have been previously overlooked, and the relevant palaeontological and geological facts should be "sieved" with care. The Ladinian is the second stage of the two-fold Middle Triassic Epoch. Our present knowledge of its stratigraphy is summarized by Gradstein et al. (2012). The Ladinian lasted

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ACCEPTED MANUSCRIPT ~5 Ma; it comprises well-established biozones, and its lower and upper boundaries are fixed in global stratotypes (GSSPs) (Brack et al., 2005; Gradstein et al., 2012; Mietto et al., 2012) (Fig. 1). At this time, the Earth had a relatively simple organization with one supercontinent (Pangaea) and two large oceans (Panthalassa and Neotethys) (Stampfli and Borel, 2002; Golonka, 2004, 2007; Stampfli et al., 2013) (Fig. 1). Consequently, the degree of

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palaeobiogeographical differentiation is expected to have been low-to-moderate

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(Westermann, 2000). However, it should be noted that the co-called "Mesozoic Marine

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Revolution" (Vermeij, 1977) initiated, probably, in the first half of the Triassic (McRoberts, 2001; Tu et al., 2016); and it was the Ladinian when infaunalization among bivalves became

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prevalent (Tu et al., 2016).

Some recent evidence (primarily from brachiopods – Ke et al. (2016)) implies that

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something went wrong and the diversity of some fossil groups plummeted, at least in some regions, during the Ladinian. The main objective of the present paper is to reconsider this

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evidence in order to present a new understanding of what may have occurred with the Earth's

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biota during this stage of the Triassic. It should be emphasized that the "Big Five" mass extinctions and the "minor" biotic crises that have been recognized during the Phanerozoic

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are considered to be trustworthy because they had a measurable impact on both global and regional diversity curves for the entire biota as well as particular fossil groups. The

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distinctive features of this study are as follows. First, it deals with biodiversity changes across the entire Triassic, because the only relative magnitude of events on a long time scale permits judgments of whether these changes are significant or not. Second, it focuses on the current knowledge, i.e, the already available information is employed for new interpretations. The different resolution on the previous diversity assessments, as well as the lack of data as precise as substages or biozones do not permit to discuss the biodiversity dynamics within the Ladinian. Third, this study is rather qualitative, due to the above-

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ACCEPTED MANUSCRIPT mentioned heterogeneity and overall lack of palaeontological data, and it provides evidence for the Ladinian crisis that is essentially similar to that provided in the comparable studies that have examined the now well-known mass extinctions, and is sufficient for a first report of the Ladinian biotic crisis.

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2. Global evidence

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2.1. Total biodiversity

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Total biodiversity is based on a calculation of the number of fossil taxa (species, genera, families) per relative time unit (stages, epochs, periods). The latest version of the

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total biodiversity analysis was proposed by Purdy (2008), who employed for this purpose the database compiled by Sepkoski (2002). The resolution of this analysis is limited to genera

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and stages. It has been established that total biodiversity fluctuated through the latest Paleozoic–Mesozoic (Fig. 1). Changes during the Triassic were very simple: there was a

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substantial increase in the number of genera (reflecting taxonomic radiation following the

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end-Permian catastrophe) until the end-Triassic mass extinction (Fig. 1). No deviation in this trend is observed in the Ladinian. In fact, the number of genera (~750) in this stage was ~1.2

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times bigger than in the precedent Anisian stage, which lasted a similar length of time (Gradstein et al., 2012; see stratigraphy.org for updates). This provides support for

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taxonomic radiation, rather than collapse, during the Ladinian. However, conventional total biodiversity estimates, like the one developed by Purdy (2008), are negatively influenced by incompleteness of the original palaeontological information (sampling, taphonomic, and other biases). An appreciation of this has led to the development of some advanced methods of biodiversity reconstruction. Among these is the sampling standardization proposed by Alroy et al. (2008), who also based their estimates on a different palaeontological dataset. Their curve provides important information, but its

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ACCEPTED MANUSCRIPT resolution is, unfortunately, too low to reach any conclusion regarding stage-by-stage changes in the number of genera during the Triassic. The only conclusion relevant to the Ladinian that can be made using the curve developed by Alroy et al. (2008) is that there is no evidence for any long-term diversity decline in the Middle Triassic, including during the Ladinian.

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These observations are discouraging with regard to the goal of the present paper.

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Unfortunately, the curves that depict the biodiversity dynamics for substages or biozones

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cannot be constructed presently because of the lack of the relevant data, the permanent changes of the time scale, and the stratigraphical inconsistency of the regional records (even

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if the latter are accurate when taken alone). Additionally, it is well-known that 1) some organisms were resistant to mass extinctions (e.g., Hallam and Wignall, 1997; Gutak et al.,

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2008), and 2) biotic reactions to catastrophes were not necessarily synchronous (e.g., Alroy, 2010). It is therefore possible that some "minor" biotic crises are "hidden" on generalized

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patterns for different groups.

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total biodiversity curves by the "noise" produced through overlap of non-coherent diversity

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2.2. Diversity of fossil groups

The global dynamics of Triassic ammonoids was reconstructed by Brayard et al.

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(2009) and then discussed with precision by Monnet et al. (2015). Brayard et al. (2009) established that the number of Ladinian genera diminished by ~1.1 times relative to the Late Anisian, and this trend culminated in the Early Carnian. This decline was comparable in magnitude and duration to the Early Norian decline, although the Early Anisian diversity drop was much stronger. A significant early Ladinian extinction event was also noted by Monnet et al. (2015). Extinctions concentrated in the early Ladinian (Monnet et al., 2015), but the diversity decline continued into the Early Carnian (Brayard et al., 2009; Monnet et

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ACCEPTED MANUSCRIPT al., 2015). This evidence implies that ammonoids were stressed throughout the Ladinian, albeit perhaps only moderately. One of the first comprehensive reconstructions regarding bivalve diversity dynamics was made by Miller and Sepkoski (1988). Their curve shows a rapid and unidirectional increase in the number of genera from the beginning of the Triassic (i.e., after the spectacular

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Permian/Triassic drop) to the end of this period, when the number of genera stabilized and

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then declined. No interruption of this trend during the Middle Triassic is visible on this low-

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resolution curve. More recently, McRoberts (2001) attempted a new reconstruction of diversity dynamics and also found that the number of genera rose from the Induan to the

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Carnian without decline. He also noted a slight increase in extinction rate (this is expected with regard to the total diversity rise) and temporary decline in the origination rate in the

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Ladinian. However, a more recent piece by this author (McRoberts, 2010) does not provide any evidence for a bivalve crisis in the Ladinian. The work of Harnik and Lockwood (2011)

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contains low-resolution curves depicting changes in origination and extinction rates for

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bivalves throughout the Phanerozoic. Similar to McRoberts (2001), their curve shows a significant decrease in the intensity of originations in the Middle Triassic. Taken together,

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this evidence implies that bivalves evolved more or less "normally" during the Ladinian.

stress.

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However, the noted decrease in the origination rate can be interpreted as a sign of certain

Brachiopods constitute a fossil group that is essential for discussion of possible Ladinian biotic events. Curry and Brunton (2007) provided the first of the modern compilations of the stratigraphic distribution of brachiopods based on the revised version of the "Treatise on Invertebrate Paleontology". They found that the total generic diversity of brachiopods rose from the Early Triassic to the Norian (Curry and Brunton, 2007). However, this increase in diversity was a stepwise process, and the Ladinian was characterized by a

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ACCEPTED MANUSCRIPT significantly slower increase than other periods during the Triassic; the number of genera in this stage remained slightly higher than Anisian (Fig. 2). However, a new data compilation and subsequent analysis attempted by Ke et al. (2016) seriously challenges this vision. According to these these authors, the number of brachiopod genera and families decreased by ~1.5 times during the Ladinian relative to the Anisian (Fig. 2). Among the several

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diversity drops documented by Ke et al. (2016), the Ladinian drop was the largest except

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only for the end-Permian demise. The decrease in the number of families and genera during

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the Norian–Rhaetian was also (and even more) significant (Ke et al., 2016), but this lasted for a long time with regard to the absolute duration of these Late Triassic stages (Gradstein et

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al., 2012). Moreover, the spatio-temporal analysis presented by Ke et al. (2016) implies that the Ladinian diversity drop was a global-scale event that occurred in both tropical and

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temperate latitudes in the Northern Hemisphere. The number of occurrences of Ladinian brachiopods is roughly ~2.5 times smaller than the Anisian (Ke et al., 2016). Importantly, the

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noted specialists analyzed possible sampling bias and found the absence of its influence on

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their results. Therefore, the available information indicates that brachiopod communities were very strongly stressed during the Ladinian.

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Two in-depth studies have been focused on the diversity of Middle Triassic conodonts. Martínez-Pérez et al. (2014) documented a number of drops in species diversity

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throughout the Triassic (e.g., in the Carnian). They observed a significant drop in conodont species diversity in the Late Ladinian relative to the Early Ladinian, and there was a peak in extinction rate during the Early Ladinian (Martínez-Pérez et al., 2014). Similarly, Chen et al. (2016) documented a peak in conodont species diversity during the early Early Ladinian that was followed by a strong decline with the minimum reached in the end of the late Late Ladinian. Species diversity dropped by ~2 times; the generic diversity also decreased, but not so strongly (Chen et al., 2016). This information implies that conodonts experienced

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ACCEPTED MANUSCRIPT significant stress during the Ladinian. Some data on the diversity of Triassic vertebrates can also be used to evaluate diversity changes during the Ladinian. According to the estimates of Benton et al. (2013), the generic diversity of tetrapods decreased in the early Ladinian by ~2.5 times relatively to the Anisian, and Bardet (1994) recognized significant extinctions (loss of >60% of families)

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among marine reptiles at the Middle–Late Triassic transition.

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The global compilation of palaeobotanical data implies that the generic diversity of

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land plants rose significantly in the Ladinian (Rees, 2002). It remained relatively low in the Early Triassic and even decreased in the Anisian. However, a strong radiation occurred

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through the Ladinian–Carnian interval, when the number of genera rose by ~2.5 times. The Ladinian diversification is documented in all regions of the world except North and South

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China (the diversity decreased a bit there) (Rees, 2002). Therefore, the available palaeobotanical data do not provide any evidence for any perturbation of land plants during

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the Ladinian.

3. Regional evidence

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Verification of mass extinctions and other biotic crises using regional palaeontological records is an important approach. Researchers often focus on the

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stratigraphical intervals of already-known events. In contrast, there have been a few assessments for the entire Triassic diversity dynamics on a regional scale. Two examples come from the Northwestern Caucasus and eastern Iberia. The Northwestern Caucasus is located in the southwest part of Russia. This was a marine basin on the northern Tethyan periphery during the early Mesozoic (Fig. 1). An almost complete stratigraphical succession for the Triassic is established there (Dagis and Robinson, 1973; Rostovtsev et al., 1979; Gaetani et al., 2005; Ruban et al., 2009). The

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ACCEPTED MANUSCRIPT palaeontological record is rich, and deposits of all stages bear representative fossil assemblages. Sampling was so complete and even during previous studies (see review in Ruban, 2010) that bias should not be an issue. The Ladinian deposits are distributed widely in this region (e.g., Dagis and Robinson, 1973; Rostovtsev et al., 1979), and the absolute duration of the Anisian and Ladinian stages were similar (each ~5 million years; Gradstein et

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al., 2012; see stratigraphy.org for updates). This should limit the effects of "artificial" over-

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and underestimations. The regional diversity dynamics of brachiopods and the entire marine

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fauna were reconstructed by Ruban (2006a,b, 2007, 2008, 2010, 2015). These studies established that diversity radiated substantially during the Anisian, but markedly declined

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during the Ladinian (Fig. 3). The number of macroinvertebrate genera dropped by ~7.3 times. According to data compiled by Ruban (2015), all main fossil groups were affected.

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The generic diversity of ammonoids diminished by 8.5 times and bivalves – by 2 times. But the most affected were brachiopods. 18 genera have been identified during the Anisian, but

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only one genus existed in the Ladinian. Moreover, microinvertebrates were also stressed.

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The species diversity of foraminifers decreased by ~1.5 times (Ruban, 2010) (Fig. 3). Generally, this level of regional evidence points to a severe biotic crisis.

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Eastern Iberia is a region located in eastern Spain which was a marine basin with carbonate sedimentation at the western Tethyan edge during the early Mesozoic (Fig. 1).

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Middle Triassic deposits are rich in fossils in eastern Iberia, and their diversity was discussed recently by Escudero-Mozo et al. (2015). There is good stratigraphical distribution for ammonoids, bivalves, brachiopods, chondricthyans, conodonts, foraminifers, and gastropods in Anisian–Ladinian aged deposits. Overall, Escudero-Mozo et al. (2015) found that Ladinian assemblages were more diverse than those from the Anisian. They also found an increase in fossil diversity through the Fassanian– Longobardian transition. In particular, bivalve diversity definitely increased. As for brachiopods, too few taxa are reported from

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ACCEPTED MANUSCRIPT eastern Iberia to be able to interpret patterns (one genus from the Anisian and two genera from the Ladinian; Escudero-Mozo et al., 2015). The diversity of Ladinian conodonts was really low. Generally, there is not any evidence of the Ladinian biotic crisis from eastern Iberia.

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4. Discussion

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4.1. Summary of evidence

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The evidence summarized above allows for insight into what occurred with the Earth's biota during the Ladinian. Ammonoids, brachiopods, conodonts, and tetrapods

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experienced a diversity decline in this stage. There was also a decline in the origination rate of bivalves, although these invertebrates radiated through the Middle Triassic. Land plants to have been unaffected. It should be noted that the knowledge of the different groups

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differs, and the most important evidence of the biotic crisis is provided by brachiopods and

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conodonts. These results are interpreted to mean that there was a true biotic crisis in the

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Ladinian, which influenced many, but not all fossil groups. Taxonomic selectivity is also seen for some mass extinctions (e.g., Hallam and Wignall, 1997), and this phenomenon may

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explain why the available total biodiversity curves do not detect the crisis. The resolution of the available palaeontological data is often limited to stages,

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although more details are known about ammonoids and conodonts. The above-said implies these fossil groups were affected within the entire Ladinian with the peak of the crisis in the midst of this stage. Extinctions were numerous in the Early Ladinian, and the diversity remained relatively low in the Late Ladinian. However, this scenario of long-term perturbation should be checked using data from additional localities and taxonomic groups. The data from the Northwestern Caucasus supports a Ladinian biotic crisis, although those from eastern Iberia provide no evidence of any diversity decline. These differences

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ACCEPTED MANUSCRIPT may relate to the depositional history of the two regions. The Northern Caucasus was occupied by a marginal Tethyan sea that persisted throughout the entire Triassic (Gaetani et al., 2005; Ruban, 2015). This sea and its ecosystems were "open" to external influences. The situation in eastern Iberia was different. In particular, rapid marine transgressions (in the form of sea incursions) in the Middle Triassic facilitated growth of carbonate platforms and

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relevant ecosystems (Escudero-Mozo et al., 2015). In other words, there were only

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"occasional" regional appearances of palaeoenvironments favourable for biotic radiation.

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Finally, both the Northwestern Caucasus and eastern Iberia represent only one palaeo(bio)geographical domain (Fig. 1). If so, the absence of evidence for the Ladinian

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biotic crisis in any given region cannot be interpreted as an argument against this crisis. The available data on various fossil groups (Fig. 5) presented above implies that the

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Ladinian crisis was significant and generally comparable to the other "minor" mass extinctions (e.g., some from the Silurian, Early Jurassic, end-Cenomanian, etc.; see

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descriptions in Hallam and Wignall, 1997;Harries and Little, 1999; Calner, 2005), but

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smaller than the "Big Five" catastrophes. "Minor" mass extinctions differ from the "Big Five" in their relative magnitude, but nevertheless measurably impacted biodiversity

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globally. Different fossil groups could react to the perturbations differently, which explains

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why some groups experienced drops in diversity earlier or later than the others.

4.2. Possible mechanisms To explain the proposed Ladinian biotic crisis it is necessary to consider some of the potential explanations for diversity drops of particular fossil groups (Fig. 5). According to Monnet et al. (2015), Triassic ammonoid diversity dynamics were controlled by climate change. Ke at al. (2016) suggested the same explanation regarding brachiopod diversity. In contrast, Ruban (2006a) explained the Ladinian demise of brachiopods by abrupt basin

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ACCEPTED MANUSCRIPT deepening. Bardet (1994) attributed extinctions among marine reptiles to a regressive episode. Martínez-Pérez et al. (2014) emphasized intrinsic (biological) factors regarding conodont diversity dynamics, although Chen et al. (2016) linked the relatively low diversity of this fossil group in the Middle–early Late Triassic to global stability of marine environments.

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Surprisingly, Triassic climate changes are yet to be fully understood. In their classical

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schemes, Frakes et al. (1992) and Francis et al. (2005) suggested a globally warm climate

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during this period. However, the possible existence of some ice was considered by Price (1999, 2009). Franz et al. (2014) interpreted glacioeustasy first for the Carnian, which was

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followed soon by the same interpretations for the Ladinian (Franz et al., 2015). The noted interpretations of glacioeustasy implicate the appearance of some ice caps and cooling during

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the first half of the Middle Triassic. Undoubtedly, this could have had an influence on the biota, which was adapted to a warm (even hot) climate throughout the stage of recovery after

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the Permian/Triassic catastrophe. However, it should be taken into account that cooling may

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trigger palaeobiogeographical differentiation. According to Westermann (2000), such a differentiation was not strong in the Triassic, although the rank of the Arcto-Pacific biochore

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(a palaeobiogeographical unit) rose in the beginning of the Middle Triassic, which may be a sign of strengthening of paleobiogeographical differentiation. Global data on brachiopods

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allowed Ke et al. (2016) to conclude that an increase in provincialism occurred in the Ladinian. Chen et al. (2016) noted a peak in provincialism in the mid-Ladinian. These observations are in agreement with the idea of climate cooling during this stage. However, it is also known that palaeobiogeographical differentiation can facilitate biotic radiations thanks to multiplication of niches (cf. Valentine, 1968). If this were the case, then Ladinian conditions should have been more favourable for high diversity, not the established crisis. Global sea-level reconstructions remain ambiguous because they are based on

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ACCEPTED MANUSCRIPT different data and approaches (Ruban, 2016). Two alternative curves are available for the Triassic (Fig. 4). The first was proposed by Embry (1997), and the second was developed by Haq and Al-Qahtani (2005), who updated the earlier version of a curve by Haq et al. (1987). Unfortunately, these reconstructions differ substantially for the Ladinian interval, and, thus, two possible scenarios have to be discussed separately. First, if the curve proposed by Embry

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(1997) is correct, then global sea level was stable through the Ladinian and tended to rise

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slightly (Fig. 4). An eustatic fall at the very end of the stage was significant, but not

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extraordinary relative to the other falls documented during the Triassic with this curve. Second, if the reconstruction proposed by Haq and Al-Qahtani (2005) is correct, the

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Ladinian was characterized by long-term global sea-level fall. However, neither duration, nor magnitude of this potential fall make it different from other eustatic events that have been

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documented during the Triassic (Fig. 4). Overall the available data do not provide any evidence for eustasy as the possible trigger of the Ladinian biotic crisis. Regional diversity

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drops are best explained by regional eustatic events caused by regional tectonics-driven

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subsidence (such as the very abrupt and strong sea deepening in the Northwestern Caucasus; Ruban, 2006a) . Moreover, it should be remembered that the relationship between major

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mass extinctions and eustatic fluctuations is very uncertain (Hallam and Wignall, 1999). It is well-known that flood basalt volcanism can trigger mass extinctions (e.g.,

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Wignall, 2001; Courtillot, 2007). Presently, at least two magmatic events can be related to the Ladinian biotic crisis. One is the emplacement of the Tabai basalts (Zhang et al., 2013) and the other is Wrangellian basalt volcanism (Xu et al., 2014). However, the timing of both events suggests they were more likely associated with early Late Triassic environmental perturbations. The discussion of volcanic or tectonic triggers like flood basalt volcanism (as well extraterrestrial impacts) will require more data and specific investigations focusing on the Ladinian interval.

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ACCEPTED MANUSCRIPT An alternative hypothesis to explain the Ladinian crisis can be proposed. The endPermian mass extinction stressed the Earth's biota considerably (Raup and Sepkoski, 1981; Hallam and Wignall, 1997; Benton and Twitchett, 2003; Erwin, 2006; Knoll et al., 2007; Chen et al., 2014; Cascales-Miñana et al., 2016) and, probably within a very short time interval (Erwin, 2006; Li et al., 2016). Recovery after the catastrophe, in contrast, took much

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longer (Erwin and Hua-Zhang, 1996; Pruss and Bottjer, 2004; Fraiser and Bottjer, 2007;

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Chen and Benton, 2012; Lau et al., 2016), and it was highly complex (Greene et al., 2011).

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Ecosystems began to flourish only during the Anisian (Komatsu et al., 2004, 2010; Posenato, 2008; Hu et al., 2011; Ros and Echevarría, 2011; Tintori et al., 2014; Tu et al., 2016). Total

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biodiversity reconstructions indicate that biodiversity did not reach levels comparable to those late Permian during the Triassic (Alroy et al., 2008; Purdy, 2008) (Fig. 1). As they

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recovered from the end-Permian catastsrophe, fossil organisms likely evolved in an unstable manner, which is confirmed by fluctuations in their diversity (Bayard et al., 2009; Martínez-

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Pérez et al., 2014; Ke et al., 2016). One such fluctuation (i.e., a diversity drop) might have

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occurred in the Ladinian. The cause can be any intrinsic factor (cf. "Red Queen model" – Tu

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et al., 2016), i.e., the factor linked to the biotic evolution itself.

5. Conclusions

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The review of available knowledge on Triassic diversity dynamics for fossil organisms attempted here permits four general conclusions to be offered. 1) The Ladinian biotic crisis is as a genuine phenomenon. 2) This crisis influenced several of organisms, but some taxa were unaffected. 3) The Ladinian biotic crisis appears to have been a long-term event comparable in magnitude to other "minor" mass extinctions. 4) There are several potential explanations for the Ladinian crisis, which vary in their

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ACCEPTED MANUSCRIPT likelihood. It is unlikely that eustatic fluctuations related to climate or tectonic events were responsible. Instead, It is more likely that the crisis resulted from an unstable recovery after the end- Permian catastrophe. This paper shows that the Ladinian biotic evolution deserves closer attention by specialists in mass extinctions. Further research should be aimed at high-precision diversity

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reconstructions and incorporating/integrating more palaeontological data for more fossil

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groups from additional regions. Achieving these tasks will require amassing additional

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detailed paleontological and geological data that characterize the Ladinian crisis with

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precision.

Acknowledgements

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The author gratefully thanks R.D. Nance (USA) for his editorial support, three anonymous reviewers for their critical consideration of this paper and useful suggestions,

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B.E. Crowley (USA) for her improvements, and N.M.M. Janssen (Netherlands), W. Riegraf

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(Germany), A.J. van Loon (Spain), and many other colleagues for literature support.

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FIGURE CAPTIONS Fig. 1. Stratigraphical framework of the Ladinian Stage (after Gradstein et al., 2012; see updates on stratigraphy.org) (A), the Late Triassic global plate tectonic reconstructions (simplified from Stampfli et al., 2013) (B), and the total biodiversity curve (after Purdy, 2008) (C). The location of two regions discussed in this paper is indicated by asterisks: NWC – Northwestern Caucasus, eI – eastern Iberia. Grey arrow indicates the Ladinian.

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Fig. 2. Triassic brachiopod diversity dynamics (a – genera after Curry and Brunton (2007), b – genera fater Ke et al. (2016), c – families after Ke et al. (2016)).

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Fig. 3. Diversity dynamics of the Triassic marine biota in the Northwestern Caucasus (macroinvertebrates after Ruban (2015) and foraminifers after Ruban (2010)).

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Fig. 4. Alternative eustatic reconstructions for the Triassic (a – adapted from Embry (1997), b – adapted from Haq andAl-Qahtani (2005)). The interval of the hypothesized biotic crisis is shadowed.

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Fig. 5. The influence of the Ladinian crisis on various fossils and the possible mechanisms of this event: a summary chart.

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ACCEPTED MANUSCRIPT RESEARCH HIGHLIGHTS New mass extinctions can be detected in global fossil record Ladinian diversity decline of ammonoids, brachiopods, conodonts, etc. Land plants resisted Ladinian biotic crisis

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Extrinsic and intrinsic factors could lead to this biotic crisis

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