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Palaeogeography, Palaeoclimatology, Palaeoecology 516 (2019) 336–341

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Palaeogeography, Palaeoclimatology, Palaeoecology

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Environment deterioration and related fungal infection of Upper horseshoe with remarks on their exceptional preservation T ⁎ Błażej Błażejowskia, , Piotr Gieszczb, Andrew P. Shinnc, Rodney M. Feldmannd, Ewa Durskae a Institute of Paleobiology, Polish Academy of Sciences, Twarda 51/55, 00-818 Warszawa, Poland b Association of Polish Climatologists, Krakowskie Przedmieście 30, 00-927 Warszawa, Poland c Fish Vet Group Asia Ltd, Chonburi, Thailand and Benchmark Health Ltd, Edinburgh Technopole, Milton Bridge, Scotland, UK d Department of Geology, Kent State University, Kent, OH 44242, USA e University of Warsaw, Faculty of Geology, Żwirki i Wigury 93, 02-089 Warszawa, Poland

ARTICLE INFO ABSTRACT

Keywords: Approximately 10% of Late Jurassic () horseshoe crabs collected from the Kcynia Formation in the Owadów-Brzezinki Quarry, Central Poland, display microborings covering the entire carapace of specimens. Limulidae Detailed examination of the surrounding sediment indicates the occurrence of short-term fluctuations in the Tithonian oxygenation level of bottom waters and their salinities. The identified palynomorph assemblage from the sediment Poland suggests pathogenic algal blooms as the probable cause for mass mortality. Anoxic conditions resulting from Algal bloom algal blooms in restricted environments facilitated fungal infection evidenced by the damage (microborings) Mass mortality caused by the hyphae on the surface of the . Associated biochemical factors contributed to the excellent preservation of diversified fauna with soft tissues.

1. Introduction 2. Material and methods

Xiphosurid horseshoe crabs are rare in the record (Rudkin and The material for this study consists of approximately 200 specimens Young, 2009; Sekiguchi and Shuster Jr., 2009; Loveland and Botton, assigned to two genera within the Limulidae: O. F. Müller, 2015; Lamsdell, 2016). Their unmineralized and predilec- 1785, and Crenatolimulus Feldmann et al., 2011 (see Błażejowski, 2015) tion for dynamic marginal environments may be the factors responsible collected within the Kcynia Formation of Tithonian (Late Jurassic) age. for their scarcity in the stratigraphic record (Babcock et al., 2000); Approximately 75% of the specimens are preserved three-dimension- however, their preservation potential seems to be relatively better than ally, and the cuticular surface of the exoskeletons is suitable for detailed some other marine from among and che- microscopic examination (Błażejowski et al., 2015). Field work col- licerate species (Klompmaker et al., 2017). The discovery of many ex- lecting the horseshoe crabs in the Owadów-Brzezinki Quarry (lat. ceptionally well preserved Late Jurassic small, presumed to be juvenile, 51.374238o, lon. 20.136343o) was conducted in 2013–2017. The col- horseshoe crabs from the Owadów-Brzezinki Quarry in Central Poland lected material is housed at the Institute of Paleobiology, Polish (Kin et al., 2013; Kin and Błażejowski, 2014; Błażejowski, 2015) has Academy of Science in Warsaw (ZPAL X.1/O-B). provided critical material for the study of their paleobiology. The purpose of the present study is to provide convincing evidence 3. Geological and paleoecological settings of a mortality episode of horseshoe crabs resulting from deterioration of the paleoenvironment. An associated algal bloom resulting in O2 de- The abundant occurrence of fossil horseshoe crabs in the Kcynia pletion is considered as the possible primary cause of death and con- Formation exposed in the Owadów-Brzezinki Quarry (Błażejowski comitant fungal infestation of the carapace of the organisms. et al., 2016) may have resulted from specific ecological settings, when numerous benthic , mostly monospecific small, elongated- shelled bivalves (protobranchs or corbuloids), formed a feeding ground for bottom dwelling organisms (Fig. 1). Judging by the modern

⁎ Corresponding author. E-mail addresses: [email protected] (B. Błażejowski), [email protected] (P. Gieszcz), andy.shinn@fishvetgroup.com (A.P. Shinn), [email protected] (R.M. Feldmann), [email protected] (E. Durska). https://doi.org/10.1016/j.palaeo.2018.12.015 Received 23 August 2018; Received in revised form 17 December 2018; Accepted 20 December 2018 Available online 21 December 2018 0031-0182/ © 2018 Elsevier B.V. All rights reserved. ł ż B. B a ejowski et al. Palaeogeography, Palaeoclimatology, Palaeoecology 516 (2019) 336–341

or shallow subtidal setting, consistent with the behavioural pattern of extant Limulus polyphemus (von Linnaeus, 1758) (see Shuster Jr, 1979). Absence of fully grown adults is probably attributable to their pre- ference for deeper water, offshore settings. Horseshoe crabs are known for their high environmental tolerance. Modern Limulidae are classified as opportunistic feeders, and they are able to live and reproduce in exceptionally diverse environments (Ehlinger and Tankersley, 2009), with a broad range of temperatures and salinities (Shuster Jr, 1982; Walls et al., 2002). The paleoenvir- onment of the studied fossiliferous horizon at Owadów-Brzezinki con- taining numerous specimens of horseshoe crabs is interpreted to be a periodically restricted lagoon of limited depth (Błażejowski et al., 2016). Results obtained in the course of microfacies and geochemical analyses, conducted to recognize the depositional environment, in- dicate that the Owadów-Brzezinki lagoon experienced episodic sudden hypoxic to anoxic conditions of benthic waters and concurrent salinity variations (from hypersaline to brackish), followed by a return to normal oxygenation (see Wierzbowski et al., 2016). A similar en- vironment with fluctuating oxygenation and related mass occurrences of small elongated bivalves has been described from Kimmeridgian clays of England (Wignall, 1990). During episodes of favorable condi- tions, horseshoe crabs gathered in large numbers in the lagoon for feeding. The subsequent degradation of the environment (restricted water exchange, drop in the water level, an increase in salinity due to evaporation, decreases in dissolved concentrations) appears to have occurred in association with extensive blooms. The parti- cular stratum in the quarry (layer D12), where the horseshoe crabs were found, revealed a ditypic assemblage composed of abundant prasino- phycean algae (Pterospermella sp.) and acritarchs (Leiosphaeridia sp.) (Fig. 2). These organisms are called “disaster species” (Tappan, 1980) because of their ability to thrive under conditions hazardous to other organisms (Guy-Ohlson, 1996). Mass occurrence of representatives of these taxa, possibly a bloom episode, is usually interpreted as an in- dicator of ecological disturbances, such as reduced salinity (Prauss and

Riegel, 1989; Dreyer et al., 2004) or increase in pCO2 (Van de Schootbrugge et al., 2007).

4. Epibionts

Colonisation by sessile fouling organisms (epibionts) is a common fate for solid surfaces in the marine environment. Among extant adult horseshoe crabs, a commonly observed phenomenon is the presence of differentiated epibiont associations (e.g. , bryozoans, and Fig. 1. Limestone slab with mass-accumulation of microbivalves with well- slipper shells) which may cover large regions of the carapaces of some preserved Late Jurassic limuline horseshoe from Owadów-Brzezinki, individuals (Botton et al., 2003; Tan et al., 2011). Juveniles rarely have Poland (ZPAL X.1/O-B/XAC.8.3). epibionts owing to their mechanical, abrasive removal by burrowing into the sediment and also by the release of fatty acid and lipid-based behaviour of Limulus, it is likely that in these rich feeding grounds, secretions onto the surface that function as an anti-bacterial barrier perhaps close to zones of breeding areas, large numbers (Harrington and Armstrong, 2003) and deter the colonisation by fouling of small horseshoe crabs, herein interpreted to be juveniles, would have organisms (Barthel, 1974). Juvenile horseshoe crabs moult frequently congregated, where they would have rapidly increased in size, prior to venturing out into deeper waters (Carmichael et al., 2003; Chiu and Morton, 2004; Kin and Błażejowski, 2014). The interpretation that the horseshoe crabs from the Owadów- Brzezinki Quarry are juvenile or immature individuals is based upon several lines of reasoning which is supported by their small size, by their unusual occurrence in very large numbers and, by the substrate upon which they rest. Horseshoe crabs are typically not gregarious, although they are more so as juveniles and become less so as adults (Sekiguchi and Shuster Jr., 2009). As the specimens are uniformly small, ranging in prosomal width from 24.25 to 86.54 mm, and because they occur in a large number of closely spaced individuals, the prob- ability that they are juveniles is increased. Further, the specimens are Fig. 2. Palynomorphs of the Owadów-Brzezinki sections (layer D12), revealed preserved on a bed of tiny bivalve shells, all in a position of repose, black, rectangular organic palynoclasts, abundant acritarch (Leiosphaeridia sp. - which supports the interpretation that they accumulated in an intertidal A) and prasinophycean (Pterospermella sp. - B) algae.

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Błażejowski, 2014), seems to support their interpretation as juveniles. However, epibiont evidence from specimens of Crenatolimulus collected from the Lower Cretaceous has been described (Feldmann et al., 2011). The specimen of C. paluxyensis Feldmann et al., 2011, from the Glen Rose Formation (north-central ), is remarkable in that the car- apace exterior is faithfully replicated by a massive overgrowth of ser- pulid worms interpreted to have been a post mortem event. In the collection from the Owadów-Brzezinki quarry, the presence of serpu- lids, as single tubes, on the carapace of the horseshoe crabs is very rare (Fig. 3), and we interpret these also to represent post-mortem coloni- sation. The availability of a suitable substratum is a critical factor in the colonisation of sessile species. Horseshoe crabs and decapod carapaces are frequently used as hard substrata available for the attachment of sessile organisms, together with other epifaunal organisms such as in- larvae, molluscs, and corals (Botton, 1981; Abelló et al., 1990; Gutt and Schickan, 1998; Schejter and Bremec, 2006). Although epibiont species commonly associated with horseshoe crabs are not usually considered to be harmful, in certain circumstances they may interfere with basic life functions resulting in the death of their (Shinn et al., 2015). Degenerative lesions on the carapace of horseshoe crabs appear to be the most frequently reported disorder, attributed to pathogenic algae, fungi, and Gram-negative bacteria (Nolan et al., 2009; Shinn et al., 2015). A related phenomenon has been reported for modern L. polyphemus Fig. 3. Three-dimensionally preserved horseshoe crab from Owadów-Brzezinki, reared in a commercial hatchery, where overstocking, high organic Poland. (ZPAL X.1/O-B/2014/2), no preserved. Prosoma has a single loading of the culture environment, and inadequate water exchange serpulid worm tube. rates resulted in conditions conducive for the proliferation of epibiont species that led to the consequent loss of stock (Shinn et al., 2015). and do not provide a suitable long-lasting substrate for many epibionts (Key Jr. et al., 1996). The absence of comparable epibionts on small to 5. Endobionts moderately large exoskeletons of extinct forms, such as the Late Jur- assic Mesolimulus walchi (Desmarest, 1822) from Germany and Limulus Information gathered so far during studies of the Owadów-Brzezinki darwini Kin and Błażejowski, 2014, from Poland (Barthel, 1974; Kin and lagoon and its seem to suggest some analogies with condi- tions in modern horseshoe crab hatcheries; notably that the evidence

Fig. 4. A-D. Late Jurassic juvenile horseshoe crabs showing severe damage created by endolithic boring organisms. A-B. Limulus darwini, ZPAL X.1/O-B/2013/7; C-D. Limulus darwini, ZPAL X.1/O-B/2015/4. Dorsal side. Owadów-Brzezinki Quarry, Kcynia Formation (Unit III), Upper Jurassic (Tithonian).

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Fig. 5. A-E. Late Jurassic limuline horseshoe crabs showing severe damage created by endolithic boring organisms. A-B. ZPAL X.1/O-B/2015/11; C-E. ZPAL X.1/O-B/ 2014/9. Prosomal doublure (ventral side). Rather irregular Mycelites sp. on the surface of a juvenile horseshoe crab. F. Explanatory drawing of the microborings. Width of the bored channels 100 μm to 240 μm. concerns closely related taxa (Kin and Błażejowski, 2014; Shinn et al., adults. In the course of an ongoing episode of deterioration, young, 2015; Lamsdell, 2016). Approximately 10% of the collected specimens smaller and weaker specimens were particularly prone to external pa- bear visible marks (microborings) interpreted as the traces of hyphae of thogenic factors. The hard bottom surface of the Owadów-Brzezinki fungi or fungal-like organisms covering the carapace (Fig. 4). These lagoon, covered with a layer of small bivalves (Fig. 1), may have pre- organisms most probably colonised specimens post mortem, but are vented the horseshoe crabs from burrowing into the sediment which equally able to infect live and dead horseshoe crabs as a direct or as a would possibly have helped to clean the carapace in the initial stage of secondary, opportunistic infection on weakened individuals sharing the infection. A subsequent and progressive bloom of algae would have led same environment. It is likely that there would also be a proliferative to hypoxic/anoxic conditions which might have helped to preserve the growth of algae in these environments. A case of mass mortality of exoskeleton and soft tissues (Błażejowski et al., 2014). juvenile L. polyphemus was described by Shinn et al. (2015), where Algal blooms would have facilitated the transition from hypoxic to deterioration in culture conditions, which did not include a sediment anoxic conditions, which would create conditions ideal for the pro- into which crabs could burrow, facilitated the growth of the sessile, liferation of certain aquatic fungi and fungal-like organisms. colonial peritrich Zoothamnium duplicatum Kahl, 1933. This conse- Microborings observed on the surface of carapaces of horseshoe crabs, quently resulted in a 96% mortality of the juvenile population. In the on both the dorsal (Fig. 4) and ventral (Fig. 5) surfaces, allude to the course of the infection, mass and rapid growth of peritrichs extended to infection of horseshoe crabs by a fungal or fungal-like . The the gill chamber, resulting in mechanical obstruction and impaired observed traces seem to belong to the ichnogenus cf. Mycelites Roux, respiratory function. 1887. Although Mycelites may exhibit horizontal and vertical burrow In their natural habitat juvenile horseshoe crabs are more vulner- penetrations (Häntzschel, 1975), there are no obvious vertical compo- able to rapidly changing environmental conditions and less able to es- nents observed on the horseshoe crabs under investigation. Mycelites is cape or to survive extended travel between pools of water than are very widely distributed in the fossil record, especially on the remains of

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The horseshoe crabs died and were preserved in fine 205–206. detail that was promoted by the oxygen-deficient environment. In this Kahl, A. 1933. Ciliata Libera et Ectocommensalia. p. 29-146. In Grimpe, G. & Wagler, E. (eds.). Die Tierwelt der Nord- und Ostsee, 2. environment proliferation of aquatic fungi, now documented by cf. Key Jr., M.M., Jeffries, W.B., Voris, H.K., Yang, C.M., 1996. Epizoic bryozoans and mobile Mycelites traces. Whether the deteriorated environment, pathogenic ephemeral host substrata. (Reprinted from Gordon, D.P., Smith, A.M. and Grant- algae infection was the most probable cause of death of the horseshoe Mackie, J.A. 1995. Bryozoans in space and time. Proceedings of the 10th crabs is difficult to assess; however, the presence of cf. Mycelites cer- International Bryozoology Conference, Wellington, New Zealand, 1995. National Institute of Water and Atmospheric Research Ltd, Wellington, 1–442) (1996). tainly provides indelible evidence of the unfavorable environment. Kin, A., Błażejowski, B., 2014. The horseshoe crab of the genus Limulus: or stabilomorph? PLoS One 9, e108036. https://doi.org/10.1371/journal.pone. Acknowledgements 0108036. Kin, A., Gruszczyński, M., Martill, D., Marshall, J., Błażejowski, B., 2013. The pa- leoenvironment and taphonomy of a Late Jurassic (Late Tithonian) Lagerstätte from We deeply appreciate the help of Robert Siuda provided in the field central Poland. Lethaia 46, 71–81. (Owadów-Brzezinki Quarry, Nordkalk Company). We also would like to Klompmaker, A.A., Portell, R.W., Frick, M.G., 2017. Comparative experimental taph- onomy of eight marine indicates distinct differences in preservation po- acknowledge Russell D.C. Bicknell (University of New England, tential. Palaeontology 60 (6), 773–794. 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