Abstract

The presence of black material associated with cracks, grooves, fractures, and growth deformation, noted herein as “black shell syndrome,” was observed on the shells of a collection of chambered nautilus (Nautilus pompilius) at the Smithsonian National Zoological Park (NZP). According to relevant literature and consults with experts, this condition affects a high percentage of captive nautilus in a number of aquaria and zoos but is not apparent in free-living nautilus. The pathologic effects of shell disease on the health of these cephalopod mollusks are significant in that affected individuals may have weakened and deformed shells, microorganisms and parasites within the compromised shell in some cases, and reduced shell growth rates and body weights over time.

Characterization of the black shell syndrome observed in NZP nautilus is based on a review of the NZP pathology database from 1987 to 1999 (n=46), as well as results of serial diagnostics (cytology, bacterial culture, biopsy) performed on a recent group of juvenile nautilus (n=6). Within a 12-year period, a large number of nautilus (n=31, 67.4%) had descriptions of shell deformity with black discoloration on postmortem examination, yet no specific etiologies were delineated.

In 1999, a group of six wild-caught, sub-adult chambered Nautilus pompilius were acquired by the Department of Invertebrates. All had grossly normal shells on arrival. Thus, in an effort to maintain optimal shell health, a preventive management program was initiated. The husbandry staff trained these unique cephalopods to accept food while being handled for minor procedures, including scrubbing different parts of the shell, determining weights, and taking photographs. Typically, the nautilus stayed calm, accepted food pieces during handling and ate them shortly after release; however, animals were determined to be mildly stressed if they refused or dropped food morsels and/or retreated to corners of the tank after release.

Groups of two animals each were assigned to three different treatment protocols which included gentle manual scrubbing of affected shell regions with a gauze sponge either once weekly, twice weekly, or not at all (controls), respectively, for a period of 4 months. At an average of once per month, cytologies of sloughed abnormal shell material, bacterial cultures of black deposits on the shells, and biopsies of any weakened, fractured shell pieces were obtained. Photographs of lateral and ventral surfaces of each individual’s shell were taken up to four times per month. Weight and shell measurements were recorded monthly. All nautilus were fed a diet high in calcium content consisting of blue crab appendages, shrimp with shells, and commercial aquatic animal gel diet. Water quality was maintained within acceptable limits.

The group receiving scrubbing treatment twice weekly had the least amount of black material present on their shell surfaces, maintained the highest shell growth and weight gain rates during the study, and exhibited no signs of overt stress during treatment. The control group (no scrubbing) exhibited visible shell abnormalities (black discoloration, grooves, fractures, ridges), slower shell growth rates, less weight gain overall, and mild signs of stress (e.g., rapid propulsion away from the keeper, dropping of food items) when handled for photographs and measurements.

Results of serial cytologies, biopsies, and bacterial cultures of abnormal shell material in the most recent group of six nautilus revealed no discernible patterns or consistent microorganisms associated with affected shells. Past and present findings in NZP nautilus include: gross descriptions of affected shells as discolored, deeply grooved, and fractured; an association with nematodes and bacterial colonies within layers of biopsied abnormal shell material; and occasional growth of bacteria, primarily gram-negative rods (e.g., Vibrio and Aeromonas spp.), from multiple serial bacterial cultures of the black material.

We hypothesize that the black material is either a carbon or sulfur-containing compound associated with shell decomposition. Based on our results thus far, black shell syndrome in captive chambered nautilus does not appear to be due to primary infections of the shell with bacteria, fungi, algae, or parasites; however, bacteria and nematodes can occur as secondary invaders in the decomposing shell material. We propose that the black shell syndrome seen in NZP nautilus has a multi-factorial etiology related to environmental factors, including water quality, mineral content of diet and tank water, and behavioral stress levels. Mineral analyses of shells (abnormal and normal), tank water, and diet may be performed in future investigations.

In conclusion, light scrubbing once or twice weekly with gauze to remove the black deposits and flaky, irregular material from shells of affected nautilus appears to slow progression of the deposition, maintain better shell appearance, and improve shell growth rates and weight gain in captive chambered nautilus that are acclimated to handling procedures.

Acknowledgments

We thank the members of the NZP pathology department for their expertise in handling and processing samples and the hardworking husbandry staff and volunteers of the Invertebrates exhibit. Special gratitude is extended to: Ms. Athena Mylonas for tracking slide development, Ms. Nancy Huddy and her group of volunteers for pathology database assistance, and Dr. Don Nichols for pathology mentorship. This work was supported in part by the Friends of the National Zoo.