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Understanding Irregular Shell Formation of Nautilus in Aquaria: Chemical Composition and Structural Analysis

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Understanding Irregular Shell Formation of Nautilus in Aquaria: Chemical Composition and Structural Analysis Zoo Biology 33: 285–294 (2014) RESEARCH ARTICLE Understanding Irregular Shell Formation of Nautilus in Aquaria: Chemical Composition and Structural Analysis Mehdi Moini,1 Aoife O'Halloran,2 Alan M. Peters,3* Christine A.M. France,2 Edward P. Vicenzi,2 Tamsen G. DeWitt,3 Esther Langan,3 Tim Walsh,3 and Robert J. Speakman4 1George Washington University, Department of Forensic Sciences, Washington, District of Columbia 2Smithsonian Institution, Museum Conservation Institute, Suitland, Maryland 3Smithsonian Institution, National Zoo Animal Care Sciences, Washington, District of Columbia 4University of Georgia, Center for Applied Isotope Studies, Athens, Georgia Irregular shell formation and black lines on the outside of live chambered nautilus shells have been observed in all adult specimens at aquariums and zoos soon after the organisms enter aquaria. Black lines have also been observed in wild animals at sites of broken shell, but continued growth from that point returns to a normal, smooth structure. In contrast, rough irregular deposition of shell continues throughout residence in aquaria. The composition and reasons for deposition of the black material and mitigation of this irregular shell formation is the subject of the current study. A variety of analytical techniques were used, including stable isotope mass spectrometry (SI‐MS), inductively coupled plasma mass spectrometry (ICP‐MS), micro x‐ray fluorescence (mXRF), X‐ray diffraction (XRD), and scanning electron microscopy (SEM) based X‐ray microanalysis. Results indicate that the black material contains excess amounts of copper, zinc, and bromine which are unrelated to the Nautilus diet. The combination of these elements and proteins plays an important role in shell formation, growth, and strengthening. Further study will be needed to compare the proteomics of the shell under aquaria versus natural wild environments. The question remains as to whether the occurrence of the black lines indicates normal healing followed by growth irregularities that are caused by stress from chemical or environmental conditions. In this paper we begin to address this question by examining elemental and isotopic differences of Nautilus diet and salt water. The atomic composition and light stable isotopic ratios of the Nautilus shell formed in aquaria verses wild conditions are presented. Zoo Biol. 33:285–294, 2014. © 2014 Wiley Periodicals, Inc. Keywords: cephalopods; shell formation; black line; isotopic abundances; Mollusca INTRODUCTION [Teichart and Matsumoto, 1987]. Nautilus research has fi Nautilus is the sole surviving genus of the ectocochliate signi cantly increased with the availability of living speci- fi (external shelled) cephalopods. The depth range at which mens in aquariums and zoos [Davis, 1987]. The rst public ’ Nautilus live in their wild native environment makes human display of Nautilus was in New Caledonia s Noumea ’ observation of their general life habits difficult except with Aquarium in 1958 [Catala, 1996]. Hawaii s Waikiki fi remote cameras. Despite an increase in the number of studies, Aquarium was the rst United States aquarium to success- ‐fi the details of their natural environment and the extent to which fully keep Nautilus in 1976 [Carlson, 1977]. Twenty ve environmental changes impact development and survival of aquariums and zoos report to have maintained Nautilus in Nautilus are not well known. Exploring the degree to which shell formation in aquaria diverge from shell formed in natural ÃCorrespondence to: Alan M. Peters, National Zoological Park, 3001 conditions will begin to uncover these details. Connecticut Avenue, NW, Washington, DC 20008‐2598. ‐ Nautiloids date to the Late Cambrian (520–540 Ma). E mail: [email protected] Descriptions of chambered nautilus appear in literature and scholarly writings since Aristotle’s time. Unfortunately, Received 30 September 2013; Revised 26 March 2014; Accepted 07 April determining the accuracy of these references is complicated 2014 by inconsistent descriptions and by large gaps in the fossil DOI: 10.1002/zoo.21132 record. Fossils most similar to modern Nautilus are in the Published online 5 May 2014 in Wiley Online Library order Nautilida and are abundant in Jurassic sediments (wileyonlinelibrary.com). © 2014 Wiley Periodicals, Inc. 286 Moini et al. their collection according to the International Species isotope mass spectrometry (SI‐MS) was used to examine Information System (ISIS), questionnaires [Carlson, 1987], differences in temperature, food sources, and trophic and the Association of Zoos and Aquariums (AZA) structure between aquaria and wild environments. Inductively institutional registrars (personal communication). coupled plasma mass spectrometry (ICP‐MS) and micro Nautilus inhabit the waters of the Indo‐Pacific seas, X‐ray fluorescence (mXRF) were used to identify the with a range from southern Japan to northern Australia differences in elemental compositions of tissue, shell, water, [House, 2009]. Chronic overfishing and recognition of shell and food sources between aquaria and wild conditions. value prompted the establishment of an inter‐agency group to Energy dispersive spectrometry in the scanning electron determine if Nautilus should be added to Appendix II of the microscope (SEM‐EDS) was used to examine the physical Convention on International Trade in Endangered Species of structure of aquaria and wild shell formation, and to provide Wild Flora and Fauna [Saunders and Landman, 2009]. information for a wide range of elements present in the shell. Ongoing census studies suggest the situation is worse than Finally, morphological imaging with SEM was used to anticipated, with one species possibly extinct [Broad, 2011]. compare the crystalline structure of the shell between the Even though no official declaration of the status of Nautilus aquaria and wild timeframes. has been made, wild populations are thought to be threatened by habitat shrinkage. The United Nation’s International Panel Materials on Climate Change (IPCC) predicts that continued dissolu- National Zoo N. pompilius shell and soft tissue samples tion of atmospheric carbon dioxide into oceans will promote recovered during necropsies were selected for analysis shoaling of the calcite compensation depth [Kleypas (Table 1) and N. macromphalus soft tissue only from animals et al., 1999], decreasing the depth at which calcareous shells that never lived in the aquaria environment (Table 2). Shells are stable and so eliminating deeper habitats [Sarma et al., were bisected along the vertical plane. One half was used for 2002]. Portions of the 0–600 m functional depth range of current analyses and the other preserved for future studies. Nautilus was brought into view with remote camera traps at Soft tissue samples varied between individuals but included 73–538 m [Saunders, 1984]. More recently many hours of at least one sample of mantle, tentacle, and/or hood. All soft remote video filming was made at 450 m in 2013 as reported tissue samples were frozen at À80°C prior to analyses. Instant by Gregory Barord (personal communication). Aquariums 1 Ocean salt was freshly mixed with deionized (DI) water to and zoos have become crucial both as a potential species artificially simulate sea water in the aquaria. Aquaria tank refuge and for facilitating behavioral and developmental waters were frozen within 12 hr of sampling and were thawed studies of Nautilus. However, abnormal shell growth in before analyses. aquaria specimens has been reported since the 1970s [Keupp and Riedel, 1995] and, to date, only four aquariums have Sample Preparation successfully bred and reared live Nautilus with two captive offspring living 376 days [Carlson et al., 1992]. Prior to analyses, shells were hand‐washed with DI One of six extant species, Nautilus pompilius, has been water to remove any clinging salts. Shells were then either kept at numerous institutions including the Smithsonian’s broken apart into small chunks with pliers for coarse National Zoo, Washington, DC. Most specimens kept at the sampling or powdered with a rotary tool for high‐resolution, National Zoo survive 2–5 years in residence (not a direct small‐quantity sampling. Shell pieces were powdered by reference to age). All inquiries indicate that all Nautilus hand in an agate mortar and pestle. It was observed that the entering aquaria exhibit abnormal shell growth. This study aquaria formed shell is thicker and harder than wild formed examines the atomic composition and structural differences shell. Black material from the aquaria formed shell was of shells within individuals as they have formed under both retrieved via scraping with forceps. All soft tissue samples natural and aquaria conditions. Nautilus pompilius shell and were washed, cut into small pieces, and lyophilized before soft tissue samples collected from necropsies at the National analyses. Remnants were re‐frozen at À80°C. For carbon and Zoo (post‐2005) were compared to soft tissue samples from oxygen isotope analyses, samples were taken from three wild wild Nautilus macromphalus. Additionally, chemical varia- and three aquaria formed shell areas, including both the bles such as food and water were compared. The long‐range exterior and interior shell surfaces. Interior samples consisted goal of this research is to determine preventative measures, of the septa, while ten exterior samples were taken from each effective treatment for the irregular shell formation of shell. Samples were powdered and soaked in 2.5% sodium Nautilus, potential impacts
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