Journal of Zoo and Wildlife Medicine 31(4): 523±531, 2000 Copyright 2000 by American Association of Zoo Veterinarians COMMON CUTTLEFISH (SEPIA OFFICINALIS) MORTALITY AT THE NATIONAL ZOOLOGICAL PARK: IMPLICATIONS FOR CLINICAL MANAGEMENT Johanna Sherrill, D.V.M., M.S., Lucy H. Spelman, D.V.M., Dipl. A.C.Z.M., Carrie L. Reidel, B.S., and Richard J. Montali, D.V.M., Dipl. A.C.V.P., Dipl. A.C.Z.M. Abstract: Six out of seven cuttle®sh acquired by the Smithsonian National Zoological Park in July 1998 died before 1 November 1998. Postmortem examinations showed mantle ulcers, secondary bacterial infections, inanition, and cuttlebone fractures. The surviving cuttle®sh developed a progressive focal mantle ulcer, was treated with oral chlor- amphenicol intermittently for 9 wk, and maintained a normal appetite and growth rate until death at 7 mo of age. The National Zoological Park pathology database showed signalments, histories, and causes of mortality of 186 common cuttle®sh, each 1±14 mo old, that received gross and histologic examinations; for example, the largest group of cuttle®sh of known sex, age, and body weight at postmortem were 7±9 mo old and weighed an average of 376.2 g (males, n 5 18) and 299.0 g (females, n 5 15). Many cuttle®sh had multiple pathologic diagnoses. Signi®cant diseases included in¯ammation and secondary bacterial infections, especially gastrointestinal, cardiovascular, respiratory, reproductive, and ophthalmic, and septicemia due to Vibrio spp. or other gram-negative bacteria. Mantle lesions, including ulceration/ dermatitis, abscess/granuloma, necrosis/®brosis/cellulitis, and laceration/abrasion/erosion, were also identi®ed, along with inanition, cuttlebone lesions, and trauma. Mantle lesions were associated with secondary bacterial infections and death. On the basis of this information, if captive cuttle®sh behavior creates risk for development of mantle lesions, administration of antibiotics effective against gram-negative bacteria may delay or halt disease progression. Cuttle®sh exhibits require proper design, husbandry, economic resources, and staf®ng to minimize disease syndromes and mor- tality. Key words: Sepia of®cinalis, common cuttle®sh, pathology, clinical management, mantle ulcers, gram-negative bacteria. INTRODUCTION mocyte, which functions in basic cellular immunity but is not phagocytic.26,28 Humoral immunity in- Common cuttle®sh (Sepia of®cinalis) and such cephalopod molluscs as squid, octopus, and the volves lectin-like proteins, not antibodies, that hem- 9,26,27,31 nautilus are frequently bred in captivity. Their basic agglutinate foreign antigens. Visible clump- biology and husbandry are reported in the aqua- ing of cephalopod hemocytes has been associated 27,31 culture literature,1,3,12±15,18,22,26 and their complex sen- with septicemia. Although well adapted to nat- sory systems and semiparous life cycles create ural environments, cephalopod immune systems challenges for culture.3,14,15,23 They spawn shortly af- may be compromised by stress related to captivity, ter reaching sexual maturity, then usually die within leading to disease. 60 days.26 Infectious and parasitic19 diseases (pro- Cuttle®sh physiology and behavior affect their 11,12,18,26 tozoal,37 viral35) of cephalopods have been report- management. The apparent curiosity of cut- ed.3,12,13,16,17,33 Literature addressing medical manage- tle®sh makes them interesting to observe but dif®- ment of cuttle®sh is limited in quantity, and reports cult to manage in a small display tank. They may on mortality of this species in zoos and aquaria are be aggressive and highly territorial3,26 and therefore scarce.6,19,26,29 require a large tank. Intermale aggression marks the Captive cephalopods are susceptible to disease transition between juvenile and adult status.26 Aqua- and major health problems17,18,20,33,34 due to their ma- culture and laboratory facilities maintain cuttle®sh rine-adapted immune system and their thin, deli- groups in sizable tanks for propagation or re- cate, microvillar epidermal structure.17,20,24,26±28,31 All search,18,26 but zoos typically keep no more than a cephalopods possess one type of blood cell, or he- dozen cuttle®sh in smaller display tanks21 and may have different husbandry techniques and economic resources as well. Small-scale captive environments From the Departments of Animal Health (Sherrill, Spel- present some disadvantages for cuttle®sh health and man), Invertebrates (Reidel), and Pathology (Montali), longevity. Smithsonian National Zoological Park, 3001 Connecticut Avenue, Washington, D.C. 20008, USA. Present address Life spans of 186 common cuttle®sh in the In- (Sherrill): Department of Husbandry, Aquarium of the Pa- vertebrate Department at the Smithsonian National ci®c, 100 Aquarium Way, Long Beach, California 90802, Zoological Park (NZP) from 1986 to 1998 were 1± USA. 14 mo. Most of these cuttle®sh developed abnormal 523 524 JOURNAL OF ZOO AND WILDLIFE MEDICINE Figure 2. Hemolymph (blood) from a common cuttle- Figure 1. Close-up view of the distal mantle tip of a ®sh (Sepia of®cinalis) that died after developing a mantle common cuttle®sh (Sepia of®cinalis) depicting a severe ulceration. Large blood cells or hemocytes with (large ar- mantle ulceration (white, irregular tissue). Edges of the row) and without (arrowhead) prominent, eosinophilic cy- ulcer are rolled and edematous. Mantle lesions are typi- toplasmic granules are present, admixed with a few gram- cally preceded by agitated swimming behavior and com- negative bacilli (small arrow). The diagnosis was hemo- monly lead to secondary bacterial infections and rapid cytic in¯ammation with intralesional bacilli, compatible death. with bacterial septicemia. Wright stain, 3320. Bar 5 9.76 mm. behavior suggestive of infection or sepsis, includ- ing anorexia, lethargy, dark coloration, hiding, fre- quent inking, or erratic swimming patterns, prior to pies were added to the diet. Water quality was death. When a new group of juvenile cuttle®sh ar- checked weekly with a standard commercial test kit rived at NZP in July 1998, several strategies were (Hach, Loveland, Colorado 80539, USA). Tested implemented to prevent disease and improve lon- parameters were within acceptable cephalopod lim- gevity. its (pH 5 8.2±8.4, ammonia 5 0 mg/L, nitrates 5 This report summarizes case histories of seven 0±10 mg/L, temperature 5 22±268C).3,11,12,26 Water captive-born, hatchling cuttle®sh (Sepia of®cinalis) changes of 30±50%, with arti®cial seawater for- acquired by NZP in July 1998 and postmortem re- mulated from dechlorinated, deionized tap water, cords for 186 juvenile and adult cuttle®sh necrop- were performed approximately every 10 days and sied at NZP from 1986 to 1998 and provides med- after any animal death. ical management recommendations for captive cut- Four of the cuttle®sh in the large tank died within tle®sh in zoological parks and aquaria. 2 wk. Focal mantle lesions and behavioral changes (anorexia, surfacing, acute color changes, aggres- CASE REPORTS sive posturing, bumping into tank walls, inking) Seven captive-born hatchling cuttle®sh, approx- were noted prior to death. Husbandry techniques imately 1 mo of age, were acquired in early July were then changed, including increased water cir- 1998 from the National Resource Center for Ceph- culation, provision of hiding places and visual bar- alopods of the Marine Biomedical Institute (NRCC/ riers, addition of a dark-screened tank cover, and MBI), Galveston, Texas 77555, USA. They were reduced local activity and overall noise levels. Nev- housed in a 0.765-m3 polyvinylchloride and plastic ertheless, anorexia and abnormal behavior persisted mesh bin within a 22,680-L round ®berglass tank in the remaining juveniles, and their mantle ulcers with under-gravel and ultraviolet ®ltration. They ate worsened. The ulcers were dark gray and white and developed normally for 4 wk and were then edematous erosions (up to 2 cm in diameter) at the released into the larger tank. For the ®rst 3 wk, they distal tip of the mantle (Fig. 1). Impression-smear were fed grass shrimp gut-loaded with ®sh ¯ake cytology (Wright and Gram stains) of ulcerated food (Tetra-Mint, Tetra Sales USA, Blacksburg, mantle tissue from the most severely affected ani- Virginia 24060, USA) and vitamins (Vita-®sht, mal revealed colonies of gram-negative rods and Marine Enterprises International, Baltimore, Mary- in¯ammatory cells (Fig. 2). land 21221, USA) and brine shrimp presoaked in Ulcer-induced bacterial septicemia was suspect- an aquarium food supplement (Selcont, American ed. Mantle erosions and ulcers were attributed to Marine, Inc., Ridge®eld, Connecticut 06877, USA). trauma from collision with tank walls and abrasion After 3 wk, thawed shrimp, cray®sh, and live gup- of distal mantle tips in the gravel substrate. Vibrio SHERRILL ET AL.ÐMORTALITY OF COMMON CUTTLEFISH (SEPIA OFFICINALIS) 525 spp. and other gram-negative rods were cultured at postmortem from hemolymph of the ®rst two dead cuttle®sh. Samples were cultured at 258C for 1±3 days in tryptic soy broth (Difco Laboratory, De- troit, Michigan 48232, USA) with 3% NaCl added, as well as on 5% sheep blood trypticase soy agar (Becton-Dickinson Microbiology, Cockeysville, Maryland 21030, USA) and MacConkey agar (Dif- co). Microbiologic identi®cation for gram-negative bacteria was performed with the API 20E system (bioMeÂrieux Vitek, Inc., Hazelwood, Missouri 63042-2320, USA). Antibiotic sensitivity assays were not performed. On the basis of these ®ndings, the three remain- Figure 3. Photograph of a 7-mo-old common cuttle®sh ing cuttle®sh with no discernible mantle lesions (Sepia of®cinalis) in a display tank. The mantle ulceration were treated prophylactically with food bits inject- (white triangular tissue at the distal mantle tip, white ar- ed with chloramphenicol sodium succinate (Chlo- row) developed after the rupture of a large vesicle, diag- romycetint, Parke-Davis, Morris Plains, New Jer- nosed as a supraosseous abscess at postmortem.