Common Cuttlefish (Sepia Officinalis) Mortality at the National Zoological Park: Implications for Clinical Management

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 chloramphenicol 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 ϭ 18) and 299.0 g (females, n ϭ 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 mortality. 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, ϫ320. Bar ϭ 9.76 ␮m. behavior suggestive of infection or sepsis, including anorexia, lethargy, dark coloration, hiding, frequent 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 ϭ 8.2±8.4, ammonia ϭ 0 mg/L, nitrates ϭ This report summarizes case histories of seven 0±10 mg/L, temperature ϭ 22±26ЊC).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-Min௡, Tetra Sales USA, Blacksburg, mantle tissue from the most severely affected ani- Virginia 24060, USA) and vitamins (Vita-®sh௡, 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 (Selcon௡, 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 25ЊC 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- romycetin௡, Parke-Davis, Morris Plains, New Jer- nosed as a supraosseous abscess at postmortem. sey 07950, USA; 40 mg/kg p.o. s.i.d. for 10 days). Individual treatment doses were based on an estimated body weight of 30 g. All three cuttle®sh ate but ruptured 4 days later, exposing a triangular (2 well and grew larger. Over the following 3 wk, ϫ 1 ϫ 1 cm) section of white, striated subcutaneous however, one cuttle®sh exhibited severe unilateral tissue with rolled, edematous edges. Although the corneal opacity and periocular swelling. Another prognosis was guarded, treatment with oral chlor- developed a ¯uctuant vesicle approximately 2 cm amphenicol continued. The cuttle®sh continued to wide along the distal mantle, and cytology (Wright eat and grow over the next 2 mo, and the ulcer and Gram stains) of a ®ne-needle aspirate of the regressed and ¯attened (Fig. 3), but at the age of 7 vesicle revealed hemocytic in¯ammation with mo, 9 wk after the initial mantle ulceration, a focal, abundant gram-negative rods. Both cuttle®sh were yellow-tan, raised, proliferative area, 3±4 mm in again treated with oral chloramphenicol at the pre- diameter, developed in the center of the lesion. The vious dosage but each subsequently died. Gross ex- cuttle®sh became highly agitated, as indicated by amination, histopathology, and postmortem bacte- frequent inking and rubbing of the irregular distal rial cultures revealed dorsal herniation of the stom- mantle tissue against the sides of the glass aquari- ach and cecum, a fractured cuttlebone, and unilat- um. After refusing food for 36 hr, the cuttle®sh eral hypopion (Vibrio sp.) in the cuttle®sh with died. antemortem ocular lesions. The cuttle®sh with the At postmortem gross examination, this adult distal mantle vesicle had severe mantle erosions, a male cuttle®sh weighed 371.4 g and had a focal fractured cuttlebone, and a supraosseous abscess granuloma associated with a circular, 3±4 cm-di- (Vibrio sp.) diagnosed at postmortem. ameter, distal mantle ulcer and a nondisplaced, par- The surviving cuttle®sh remained clinically nor- tial thickness cuttlebone fracture. mal until 3 mo after arrival, when it was moved to a 1.8- ϫ 0.61- ϫ 0.61-m, 680.4-L, rectangular glass Necropsy database review display tank, maintained at 18±20ЊC with under- gravel and ultraviolet ®ltration, containing a stable The pathology records of 186 common cuttle®sh population of four adult chambered nautilus (Nau- presented to the Department of Pathology at NZP tilus pompilius). Four days after relocation, the cut- from 1986 through 1998, and the records of six of tle®sh intermittently bumped into the sides of the the seven cuttle®sh acquired in July 1998, were re- tank. It developed a focal, grayish-white, nonulcer- viewed. Complete necropsies consisted of gross ative, edematous lesion approximately 1 cm in di- and microscopic examination of all organs and tis- ameter on the distal tip of the dorsal mantle, and sues, as well as cytology or bacteriology in selected oral chloramphenicol (40 mg/kg s.i.d.) was initiated cases. Pertinent data for 186 common cuttle®sh to prevent secondary infection. The cuttle®sh grew were collected from necropsy reports for each cut- normally for 3 wk, then developed a 2- ϫ 1-cm tle®sh and included signalment, body weight, clin- ¯uctuant swelling at the previous site of mantle dis- ical history, gross and histologic descriptions (ex- coloration. This swelling slowly decreased in size cept in cases of severe autolysis or missing car- 526 JOURNAL OF ZOO AND WILDLIFE MEDICINE

Table 1. Signalment, body weight ranges, and aver- Table 2. Frequency (in decreasing order) of signi®- age body weight (in grams) determined at postmortem for cant disease syndromes occurring in common cuttle®sh common cuttle®sh of known age (to the nearest month) before (clinical signs) and after death (postmortem diag- necropsied at the National Zoological Park between 1986 nosis), based on a review of the National Zoological Park and 1998 (n ϭ 99). Individual cuttle®sh with either no necropsy database from 1986 to 1998 (n ϭ 186). For most recorded age (n ϭ 49) or unreported body weight (n ϭ individuals, multiple clinical signs and postmortem diag- 38) were excluded. noses were recorded; however, not all necropsy reports included a detailed clinical history. Total Average Age in Weight range weight Parameter Frequency (mo) Sexa group (g) (g) Clinical signs 1±3 M 5 16.2±68.4 39.8 Anorexia 60 (n ϭ 14) F 6 2.0±92.0 34.8 Mantle lesions 41 NR 3 4.5±36.3 23.7 Ocular lesions 26 4±6 M 8 28.7±193.7 130.8 Depression, lethargy 16 (n ϭ 25) F 12 18.9±439.0 141.9 Agitation, hiding 15 NR 5 49.8±312.0 118.4 Reduced growth (runts) 13 7±9 M 18 44.4±1,135.4 376.2 Trauma (self) 10 (n ϭ 34) F 15 84.7±565.0 299.0 Tentacle lesions 6 NR 1 102.8 102.8 Trauma (others, cannibalism) 5 10±12 M 12 243.0±1,641.0 819.4 Cuttlebone lesions 4 (n ϭ 21) F 9 231.6±1,140.0 677.0 13±14 M 4 632.2±1,418.4 1,137.7 Postmortem diagnosisa (n ϭ 5) F 1 1,414.7 1,414.7 In¯ammation and/or infections Septicemia 43 a M ϭ male, F ϭ female, NR ϭ sex not recorded (n ϭ 9). Other bacteria 30 Vibrio spp. 13 Gastrointestinal 64 cass), special test results (e.g., bacterial cultures or Cardiovascular 53 cytologies), ®nal diagnoses, and cause of death. Respiratory 52 Data are presented in Tables 1 and 2. Between Reproductive 44 1986 and 1998, 186 common cuttle®sh died at NZP Ophthalmic 37 and 166 (89.2%) received complete necropsies. Six Renal 14 carcasses were not retrieved and 14 were markedly Locomotor 8 autolyzed (10.8%). Average body weight for 99 Neurologic 5 cuttle®sh of known sex and age was calculated Total in¯ammation and/or infections 320 from body weight obtained at necropsy (Table 1). Mantle lesions Age analyses to the nearest month at death were Ulceration, dermatitis 72 based on keeper records and/or postmortem assess- Abscess, granuloma 15 ment. The ages of 49 cuttle®sh and weights of 48 Cellulitis 6 were unknown. Laceration, abrasion, erosion 5 Most cuttle®sh received multiple postmortem Necrosis, ®brosis 4 disease diagnoses (Table 2). Anorexia, mantle le- Total mantle lesions 102 sions, and ocular lesions were cited most frequently Inanition 39 in historical descriptions (60, 41, and 26 times, re- Cuttlebone lesions spectively), and other recurrent antemortem clinical Erosion, necrosis 11 signs included depression, dark coloration, lethar- Fracture 10 gy, agitation, hiding, self trauma, and slow growth Supraosseous abscess 7 or failure to thrive. Postmortem ®ndings correlated Deformity 3 with antemortem histories and clinical signs; many Total cuttlebone lesions 31 cuttle®sh had mantle lesions, secondary bacterial Trauma infections, and/or no body stores of fat. Self 8 On microscopic examination, in¯ammatory le- Others, cannibalism 11 sions and infections of multiple body systems were Total trauma 19 documented most frequently (n ϭ 320; Table 2). Reduced growth 3 Typically, an individual cuttle®sh had multiple tis- Maladaptation 3 sues affected. In selected cases, pure and mixed bacteria were cultured postmortem from hemo- a No postmortem was possible in cases of advanced autolysis (n ϭ 16) or unretrieved carcass (n ϭ 4). SHERRILL ET AL.ÐMORTALITY OF COMMON CUTTLEFISH (SEPIA OFFICINALIS) 527

from hemolymph) was present in 43 cases and in- volved primarily gram-negative bacteria, Vibrio spp. (n ϭ 13), Aeromonas hydrophila, Citrobacter freundii, and others. Lesions of the mantle, de®ned as ulceration, dermatitis, granuloma, laceration, abscess, abrasion, erosion, ®brosis, cellulitis, or necrosis, appeared as a ®nal diagnosis 102 times. Lack of body fat detected during gross necropsy, classi®ed as inanition, occurred in 39 individuals. Cuttlebone lesions (n ϭ 31) included deformity, erosion, necrosis, supraosseous abscess, and fracture (Fig. 4). Several cases of fractured cuttlebones directly correlated with a history of observed self- Figure 4. Postmortem appearance of a severely frac- trauma. tured cuttlebone. Common cuttle®sh (Sepia of®cinalis)at On the basis of information collected at NZP, re- the National Zoological Park have been diagnosed with view of the literature, and consults with experts in cuttlebone fractures, erosions, necrosis, and infections fre- cuttle®sh husbandry, preferred water quality param- quently associated with deep, ulcerative mantle lesions. eters and a formulary for captive cuttle®sh are presented as Table 3, and some recommendations for the medical management of captive cuttle®sh in lymph, mantle ulcers, abscesses, and ocular ¯uid. small-scale environments are summarized. Mantle lesions were associated with septicemia, granulomas, and osteomyelitis with or without DISCUSSION pathologic fractures of the cuttlebone. Septicemia Similar in¯ammatory lesions and secondary (in which case bacteria were cultured postmortem bacterial infections of multiple organ systems,

Table 3. Speci®c recommendations for optimal water quality parameters and a formulary for the medical management of captive common cuttle®sh.

Water quality parameters Range References

Temperature (ЊC) 20±24 11, 12 Salinity (parts per thousand) 27±38 3, 11, 12 pH 7.7±8.2 11, 12 Ammonia, nitrites (mg/L) Ͻ0.1 3, 11, 12, 26 Nitrates (mg/L) Ͻ20.0 3, 11, 12, 26

Formulary Dosage/route/frequency References

Treatment options oral, parenteral 13, 17, 26 bath, tank immersion 10, 13, 15, 17, 26 Antibiotics 12, 13, 17, 26 Chloramphenicol 40 mg/kg p.o. or i.m. s.i.d. 26 75±100 mg/kg p.o. or i.m. s.i.d. 12, 13 Gentamicin 20 mg/kg i.m. s.i.d. 26 Nitrofurazone 2 mg/L for 72 hr 10, 26 Tetracycline 10 mg/kg p.o. s.i.d. 29 Antiprotozoals 13, 37 Metronidazole 100 mg/L for 16 hr 13 Anesthesia dose to desired effect 2, 12, 25, 26, 32 Ethanol 2% (diluted 1:1 with seawater) 12, 25, 26, 32 Magnesium chloride 7.5% (diluted 1:1 with seawater) 25, 32 2.5% (diluted 1:1 with seawater) 12 Euthanasia 26, 30 Ethanol 10%, in seawater 26 Magnesium chloride 10%, in seawater 26 528 JOURNAL OF ZOO AND WILDLIFE MEDICINE bacterial septicemia, mantle lesions, and inanition Unless a pure culture of one organism is ob- have been reported in squid,10,20 octopi,15 and cut- tained, however, the signi®cance of mixed bacterial tle®sh12,18,21,26,33,34 at propagation facilities. A cap- cultures is unclear in any aquatic specimen that is tive environment can contribute to the progression not examined immediately after death because of of disease in cuttle®sh for a variety of reasons, the likelihood of rapid postmortem bacterial over- many of which are husbandry related.12,17,20,26,33 growth.4,26,29,30 The invertebrate immune system, adapted to pre- Cuttlebone fractures were seen in 10 cuttle®sh, vent disease in natural or optimal marine environ- including two from the July 1998 group. At post- ments, may be overwhelmed by suboptimal con- mortem, cuttlebones have been characterized as ditions in captive environments with, for example, brittle and, in three cases, were malformed. Possi- ubiquitous micro¯ora, elevated ammonia levels, ble explanations for abnormal cuttlebone develop- overcrowding, or improper tank design.26 Cuttle®sh, ment include suboptimal nutritional and/or water though adaptable and capable of thriving in captiv- quality parameters (J. Scimeca, pers. comm.). For ity,26 are highly sensitive to environmental distur- example, nutritional de®ciencies, water tempera- bances.29 Agitated cuttle®sh will briskly bump into tures outside of normal ranges, or stress induced by or against the sides of the tank when reacting to excessive nitrogenous waste compounds can ad- environmental stressors, such as tankmate aggres- versely affect cuttlebone mineral deposition and sion or poor water quality.34 The resulting damage growth rate.11,22,24 According to NZP case histories, to the distal tip of their mantle compromises their self-induced trauma is the most likely cause of thin, microvillar integument and provides a route mantle ulceration. Self-trauma can affect the cuttle- for bacterial invasion.13,26,34 bone by either spread of infection or fracture at In many NZP cuttle®sh, bacterial infections of impact with tank walls.34 Skin damage at the mantle cardiovascular, respiratory, digestive, reproductive, tip can result in chronic, localized infections, as in and renal tissues were probably secondary to man- several cuttle®sh at NZP, or the infection can spread tle lesions. Cephalopods have an extensive vascular to adjacent tissues and the cuttlebone, leading to system connecting gills to branchial and systemic death.17 hearts and to the peripheral vasculature.4 Hematog- The NRCC/MBI, a major source of squid and enous spread of bacteria has been cited as the most cuttle®sh for scienti®c investigators and for NZP, likely etiology of septicemia in one group of cap- has produced a review26 of speci®c environmental tive cuttle®sh, with possible entry routes via mantle and nutritional parameters that have contributed to ulceration or the anatomically exposed respiratory successful year-round propagation of large numbers and reproductive systems.29 In several NZP cuttle- of cephalopods. Their protocols may apply to cut- ®sh, trauma, particularly self-induced, resulted in tle®sh exhibits in zoos and aquaria. The NRCC/ mantle erosions and ulcerations with rapid bacterial MBI has treated mantle ulcerations with antibiotics invasion and subsequent death due to septicemia. successfully.26,33,34 Another formulary, developed Bacteria on the normal and ulcerated mantle sur- through clinical trials, outlines methods for antibi- face of captive squid may exceed in number those otic treatment of cephalopods in large propagation found on free-living squid.10 Trauma, and not pri- tanks.13 mary bacterial colonization, has been implicated as The individual NZP cuttle®sh receiving oral the initiating cause of mantle compromise.10 Bac- chloramphenicol therapy for almost 10 wk contin- teria (usually gram-negative rods), along with ede- ued eating and growing during treatment. The dose ma and necrosis, have been observed in the sub- of oral chloramphenicol administered intermittently epidermal layer of squid mantles within a few hours may not have increased with increased animal size, of trauma-induced epidermal loss.20 however, resulting in subtherapeutic tissue levels. Ubiquitous aquatic ¯ora, including Aeromonas Although antibiotic treatment may have extended sp., Vibrio sp., and Pseudomonas sp., have been life span by delaying bacterial infections and sep- isolated from both normal and ulcerated mantles of ticemia, an in¯ammatory response eventually de- squid (Lolliguncula brevis), and both prophylactic veloped in the central portion of the healing mantle and therapeutic antibiotics have been suggested for ulcer. We hypothesize that the anorexia and agitated treatment of any squid susceptible to mantle com- behavior observed in this cuttle®sh 48 hr prior to promise or damage.10 Cephalopod skin lesions may death was due to discomfort and stress induced by contain Aeromonas, Vibrio, and Pseudomonas spp., the acute in¯ammatory response, leading to com- usually simultaneously.17 Vibrio sp. was isolated promised physiologic and immune functions, sep- postmortem from hemolymph, abdominal ¯uid, and ticemia, and death. Ideally, body weight would eyes of four captive cuttle®sh with myocarditis.29 have been obtained or more accurately estimated in SHERRILL ET AL.ÐMORTALITY OF COMMON CUTTLEFISH (SEPIA OFFICINALIS) 529 this individual for proper dosage adjustments. mesh. Filtration methods should include a combi- Keepers have successfully weighed juvenile cuttle- nation of mechanical, biologic, and adsorptive ®l- ®sh and chambered nautilus after minimally stress- ters, as well as ultraviolet light sterilization.3,12,36 Ink ful underwater transfer into a smooth plexiglass material, released by excited or stressed cuttle®sh, container ®lled with tank water of known weight, should be promptly removed via activated carbon but weight can be reasonably estimated on the basis or protein skimmer, primarily to prevent fouling of of age group. gill tissue.11,26 The use of oral, parenteral, or tank/bath immer- The rapid growth rate, metabolic rate, and con- sion prophylactic antibiotics in captive cuttle®sh centrated protein diet of cuttle®sh result in the ex- subjected to physiologic stress is reasonable and cretion of two to three times more ammonia waste may delay disease progression and improve lon- product per kilogram than other aquarium spe- gevity. Oral administration by injecting drug solu- cies.3,12,18,26 Toxic ammonia levels accumulate more tion into pieces of food is preferable and less stress- rapidly in aquaria housing cuttle®sh than in com- ful than parenteral administration. Bath treatments parable ones containing teleost ®sh, especially in are prepared with tank water to avoid acute water closed systems.3,22 Water quality limits stocking quality changes, especially temperature. densities.3,12 With the July 1998 group of NZP cut- Preventive management of captive cuttle®sh de- tle®sh, weekly tests of water quality may not have pends on careful husbandry, frequent clinical as- detected spikes in ammonia or nitrite levels, leading sessment, and the appropriate use of antibiotics. to subclinical stress and disease progression. Tem- Case histories of NZP cuttle®sh illustrate the need perature, salinity, ammonia, nitrites, nitrates, pH, to prevent mantle lesions or to treat them early and and dissolved oxygen should be tested at least twice aggressively if they do occur. Alternative therapies weekly and immediately after any deaths to ensure for cuttle®sh are needed. The roles of housing and acceptable levels.3,12,15,18,26,36 environment on the health of captive cuttle®sh are Any substrate should be ®ne and smooth to pre- signi®cant and must be considered.3,29 Such stress- vent mantle trauma. Tank deÂcor or furniture should ful factors as lack of hiding places, excessive hu- provide places for cuttle®sh to hide, establish ter- man activity near the tank, overcrowding, and ritories, and escape aggression. Octopi may become poor water quality should be avoided.3,12,18,26,29 depressed and anorexic if denied adequate hiding Strategies for preventing mantle ulcers include places.15 Sudden change in light intensity may strict attention to tank design, substrate, water cause panic and injury.3,11 One-way glass for dis- quality and temperature, nutrition, and population play sections of tanks limits startling of cuttle®sh density.3,12,17,20,26,29,33,34 on exhibit. Training cuttle®sh (and other cephalopods) to ac- Clinical histories from NZP records describe fre- cept routine gentle handling, including in-water transfers, and medical assessments is possi- quent male sparring and female stress during mating, ble.3,12,18,26 To reduce stress, tanks should be dark- with trauma to eyes, tentacles and mantles. Although ened and/or covered for 2±3 hr after procedures. If cuttle®sh are sensitive to crowding, recommended 3,11,12,15,18,26 necessary, cuttle®sh can be anesthetized for brief optimal population density varies. In dis- procedures with ethanol or magnesium chloride so- play aquaria or exhibits, no more than two adults/ 2 lutions made with tank water,12,25,26,32 with efforts m , and only one male, should be housed in the same 26 made to eliminate self-trauma. Smooth-sided cov- tank (J. Scimeca, pers. comm.). At NZP, trauma ered containers with adequate oxygenation and a was common and included attack and cannibalism separate recovery container with fresh tank water by tank mates, predation by other invertebrates, and should be employed. accidental access to intake valves. There are several different successful types of Studies of the dietary habits and requirements of, tanks and ®ltration schemes.3,12,15,17,18,20,33,36 A round and nutritional recommendations for, captive and tank with a cover and boundaries that are visually wild cephalopods are available.3,5,7,8,11,12,18,22,26 Cuttle- obvious at all times is preferable.3,18,20 Boundaries ®sh can survive for several months at only 10% of can be achieved by painting stripes along interior normal growth rate.3 Given that inanition, based on walls and/or by placing plant deÂcor along swim- absence of intracoelomic fat, was a common post- ming paths. Suggested minimum water depths are mortem ®nding at NZP, either NZP cuttle®sh were Ն5 cm for hatchlings and Ն30±40 cm for adults.11 not always fed adequate amounts or variety of diet A maximum water volume for tank size is ideal, or they were failing to consume offered foods be- and erratic currents or uneven water ¯ow should be cause of health-related reasons. Increased diet va- avoided.3,15 Intakes can be covered with plastic riety and feeding rates may stimulate appetite in 530 JOURNAL OF ZOO AND WILDLIFE MEDICINE partially anorexic cuttle®sh. Buoyancy problems ulceration leading to secondary bacterial infections and the appearance of a longitudinal dark stripe and in¯ammatory lesions. Preventive measures are along the dorsal mantle due to chromatophore con- paramount to the longevity of this species in cap- centration in contracted skin have been observed in tivity. If cuttle®sh are exhibiting behaviors that put starving Sepia spp.3 Similar clinical signs were oc- them at risk for development of mantle lesions, pro- casionally recorded in histories of NZP cuttle®sh. phylactic long-term antibiotic therapy effective Cuttle®sh grow rapidly, with a life span in cap- against gram-negative aquatic bacteria may delay tivity that rarely exceeds 1 yr.11,12,26 Proper growth or halt disease progression. The successful display depends on nutrition, water quality (especially tem- of these unique aquatic invertebrates requires prop- perature), and behavior.7,8,22,26 Captive life spans er exhibit design, husbandry, and medical care. may be shorter at temperatures above 20ЊC.11 Mari- culture of cuttle®sh at temperatures of 20±24ЊC has Acknowledgments: We thank Dr. J. M. Scimeca resulted in growth rates of 3±4% body weight per at the NRCC/MBI for expert consultations; N. day.11 Other reported growth rates in juvenile and Spangler-Huddy, T. Herwig, and B. Roffey for gen- adult cuttle®sh range between 2.5 and 5%8,18,26 and erous help in compiling data from necropsy reports; 3 and 10% per day.18,22 Typical laboratory-reared and Drs. D. Nichols and J. Raymond for postmor- cuttle®sh weigh 139±441 g as juveniles,11,26 500± tem examinations. We acknowledge Dr. I. Berzins, 1,400 g at 10 mo of age,12,18 and 1±2 kg as who produced a detailed cuttle®sh histology and adults.11,26 According to NZP necropsy records, the pictorial study set. We thank NZP staff and vol- most common age group at death was 7±9 mo, and unteers for the husbandry of cuttle®sh included in average body weights were 376.2 and 299.0 g for this report. Partial ®nancial support was provided males and females, respectively. For reasons that by Friends of the National Zoo. remain unclear, perhaps related to husbandry techniques, NZP data re¯ect reduced longevity and LITERATURE CITED growth rates when compared with NRCC/MBI 1. Abbot, N. J., R. Williamson, and L. Maddock. 1995. data.26 Cephalopod Neurobiology Neuroscience Studies in Squid, Monitoring cuttle®sh sizes and rates of growth Octopus, and Cuttle®sh. Oxford University Press, Oxford, can be helpful in evaluating their overall health and United Kingdom. 8,22,26 nutritional status. A common method of as- 2. Andrews, P. L. R., and E. M. Tansey. 1981. The sessing body size and growth rate of cuttle®sh and effects of some anesthetic agents in Octopus vulgaris. squid is the measurement of maximum mantle Comp. Biochem. Physiol. 70(C): 241±247. length.3,12,22 Mantle lengths within a wild cuttle®sh 3. Boletzky, S. V., and R. Hanlon. 1983. A review of population ranged from 1.5 to 24 cm in one survey5 the laboratory maintenance, rearing, and culture of ceph- and between 16 and 17 cm (16 mo of age) and 24 alopod molluscs. Mem. Mus. Vic. 44: 147±187. and 25 cm (21±22 mo of age) in another study.6 4. Bradbury, H. E. 1971. A technique for demonstrat- Unfortunately, mantle lengths were not routinely ing the blood vascular system of squid. Can. J. Zool. 49: recorded either before or after death in NZP cuttle- 505±506. 5. Castro, B. G., and A. Guerra. 1990. The diet of Sepia ®sh. Postmortem weight and mantle length, in com- of®cinalis (Linnaeus, 1758) and Sepia elegans bination with disease syndromes, may help identify (D'Orbigny, 1835) (Cephalopoidea, Sepioidea) from the factors affecting cuttle®sh growth and might be a Ria de Vigo. Sci. Mar. 54: 375±388. better means of classi®cation of juvenile or adult 6. Chichery, M. P., and R. Chichery. 1992. Behavioural age status versus months of age and/or weight at and neurohistological changes in aging Sepia. Brain Res. death only (J. Scimeca, pers. comm.).3,12 574: 77±84. Early detection of illness plays an essential role 7. Clarke, A., P. G. Rodhouse, L. J. Holmes, and P. L. in cuttle®sh management. Once anorexia develops, Pascoe. 1990. 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