Our assessment of the CTF involved both objective observation as well as limited subjective observation where the WSPA’s evidence was being assessed. Where standard observations could not be made, subjective assessments of animal welfare were used and found to correlate well with objective assessments (for example for evaluating stress in food animals from stress-related vocalisations) (Warriss et al. 1994). We felt that our dual approach using both objective and subjective assessments (both of which involved objective evaluation) reasonably represents conditions and issues of animal welfare at the CTF.
Although we established two distinct categories of primary consideration, ‘physical’ and ‘behavioural’, it should be noted that there was often considerable overlap between these scenarios. For example, physical injuries from bites, which may then additionally result in infections, were frequently causally related to feeding frenzies (due largely to overcrowding) and co-occupant aggression. Underlying management failures promulgated these scenarios (for example, stocking densities and spatial provisions, feeding regimens, and poor water quality).
Certain management- and behaviour-related problems led to physical injuries and in turn, these can invite potential infection and disease. The Cayman Turtle Farm incorporates both multiple-occupation ponds in addition to interconnected ponds using shared water systems. This questionable arrangement includes introduced direct risk of cross-contamination of potentially pathogenic microbes and macroparasites to many animals and represented a persistent and enduring animal health risk.
Under natural conditions, marine algae may establish and grow in patches on sea turtle shells and provide incidental food for symbiotes such as fishes that predate on ectoparasites (Losey et al. 1994; Sazima et al. 2010). However, in the absence of symbiotic grazer species and the presence of certain concomitant environmental and immune scenarios, such algae growth is capable of degrading keratinised shell layers and result in significant morbidity among farmed turtles. Furthermore, the presence of dense mats of algae serves to mask other potentially problematic issues, most specifically, signs of injury and disease.
In our view, overcrowding affected all turtles in all ponds. In some enclosures, for example the commercial production ponds, as distinct from the display ponds, overcrowding may have appeared obvious (Fig. 8). In others, for example the display and in particular the breeder lake, the presence of larger bodies of water and artificial beaches prima facie appeared ‘spacious’. However, overcrowding can be considered as having two ‘forms’: ‘overt overcrowding’ and ‘covert (or ‘crypto’) overcrowding’. Overt overcrowding may be estimated by the number of animals occupying a certain amount of space, whereas crypto overcrowding essentially refers to the accessibility of all facilities to which all animals have free access whenever required (Warwick et al. 2011a, b). Accordingly, an enclosure that appeared large and abundant but that lacked the ability to provide for the needs of all the animals at any time was capable of being overcrowded. By this measure, all facilities throughout the CTF were subject to overt or crypto overcrowding. Marine turtles are coastal- and oceanic-going animals that, like all reptiles, possess hard-wired traits, which typically includes extensive home ranges (Warwick 1990; Warwick et al. 2013a).
Numerous individual turtles were affected either by managemental (for example, poor incubation) or genetically related birth defects. These included anophthalmia blindness (congenital absence of one or both eyes) and marked skeletal deformities (particularly of the cranium).
Ross (1999) commented that questions of sea turtle maintenance and husbandry have only indirect application to wild turtle conservation. However, we consider that the release of the CTF turtles to the wild as well as discharged farm water into the sea includes the potential risk of disseminating both farm-present pathogens and biologically unfit or carrier-state animals to natural turtle populations and the wider environment.
Godley (2002) described turtle farming as no different from other animal farming for consumption. We would agree that in some respects this is a reasonable assumption. However, key differences do exist between sea turtle and other animal (for example, cattle) husbandry. Cattle have been domesticated for a period of at least 5,000 years and possess particular pre-adaptive traits that lend these animals to human-environment sharing. Turtles are reptiles and possess strong innate drive states evolved within a naturally spacious and diverse oceanic environment. Accordingly, the animal welfare implications for turtles in a captive lifestyle associated with human control warrant different considerations from other farmed animals. In brief, it is our view that sea turtle farming involves greater captivity-stress for these animals than cattle farming imposes on those animals. Additionally, it needs to be emphasized that, unlike cattle, all species of sea turtle are endangered species and as such “should not have to earn their survival through commercialization” (Ehrinfield, as cited in Reiser 2012, pp. 122–123).
Dorsal aspect neck lesions (Fig. 9) were extremely common in the adult breeder population, and other injuries, for example, to the tail were occasionally observed (Fig. 10). The turtles frequently bite each other in the neck region during competition for food and other co-occupant harassment episodes (Fig. 11). This ‘breeder’ population is a long-term feature of the farm and thus more ‘mature’ these turtles have more time than others in which to accumulate injuries and compounding factors.
A recent (2012) CTF-sponsored investigation of the farm reported the following issues: concern at the incidence of skin lesions and early juvenile mortality levels; a notable proportion of severe skin lesions including deep ulceration to the shoulder, forelimbs, head and hind limbs; high mortality levels in younger classes; potentially emerging enteritis conditions; and a notable apparent proportion of moderately emaciated animals (Balazs et al. unpublished). Those findings further confirm aspects of our assessment of the WSPA (unpublished) evidence regarding ongoing presence of important disease at the facility. The CTF itself reports mortality-rates during the years 2007–2011 at: 2007 = 4.4 %; 2008 = 5.4 %; 2009 = 7.2 %; 2010 = 4.9 %; and 2011 = 8.1 % (CTF FOI declaration to WSPA 2012).
It is unclear whether or to what extent the CTF farm water that is subsequently returned to the sea may harbour actively pathogenic or environmentally destructive agents. It is known that diseases in sea turtles, for example lung, eye and tracheal disease, grey-patch disease and fibropapillomatosis, all constitute potential infectious pathogens and have all been reported from the CTF (Godley 2002). These diseases involve herpesviruses and are capable of remaining in an infective state in seawater for up to 120 h (Curry et al. 2000). Glazebrook and Campbell (1990) provided a list of bacterial diseases of farmed green turtles (Chelonia mydas) and hawksbill turtles (Eretmochelys imbricata), which included the following pathogens: Vibrio alginolyticus; Aeromonas hydrophila; Pseudomonas fluorescens; P. aeruginosa; Cytophaga-Flavo-bacterium sp.; Mycobacterium sp.; Salmonella enteritidis; Escherichia coli H2S+ve, Arizona hinshairi; and Streptococcus sp. Norton (2005a) cites Enterococcus sp. as being common in some Kemp’s ridley turtles (Lepidochelys kempii). Water samples obtained for the present study (presented in Table 6) demonstrated the ongoing presence of these and other important turtle-pathogenic bacteria (several of which are also zoonotic) even from these limited tests.
In addition to potentially ‘contaminated’ water impacting on wild populations of turtles, this source of possible infection may also find its way back into the facility, exacerbate the general contaminant load, and threaten the health of all captive individuals, regardless of level of immunity.
Problematic behaviours indicated maladaptation and captivity-stress. At the most basic level, common problematic issues included unsuccessful attempts by turtles to bask and thus precisely regulate physiology using normal behavioural means. Signs of hunger were also observed in many turtles and this is a significant welfare concern in itself, for in addition to nutritional deprivation, the hunger state promoted feeding frenzies and cannibalism (Fig. 7), which is a notable issue at the facility.
The CTF feeding policy, which involved sporadic introductions of food, additionally appeared to exacerbate feeding competition and co-occupant aggression. Feeding competition (which is highly significant in the overcrowded conditions at the CTF) is not a typical behaviour for free-living sea turtles. In the case of intensive farming situations, less competitive feeders and individuals weakened by injury, disease or existing malnutrition may ‘lose-out’ to stronger individuals, with potentially serious health and welfare consequences. Green sea turtles are typical grazers and require abundant food sources on which to casually browse. Food dosing is in conflict with typical sea turtle biology and behaviour. Feeding competition also serves to bring large powerful turtles together inviting contact abrasions, and other injuries from co-occupant bites and from forceful contact with housing walls and structures. The extremely common dorsal aspect neck lesions in the adult breeder population are an example of both a physical and a behavioural problem. These incidents also offer opportunities for the spread of infection from water to open wounds or from turtle to turtle. Reproductive stress was also a potential factor where male harassment of females in intensive conditions can result in both psychological stress and injury for individuals of both sexes.
Fundamental underlying causes for co-occupant aggression and cannibalism include stress, overcrowding, deficient and inappropriate environments, hunger and possibly also nutritional deficiencies (Fig. 11). The possibility and extent to which nutritional deficiencies may be relevant is yet to be determined.
The nature and severity of what are frequently observed injuries in the CTF turtles has profound welfare ramifications beyond the obvious. At one level, these injuries will be painful and expose afflicted animals to subsequent infection and disease and aid to attract cannibalism. Further, animals with massive flipper trauma where digits and even gross flipper loss is involved are simply less able to swim to avoid co-occupant and cannibalistic assaults. The psychological stress involved for these compromised and traumatised individuals is likely to add considerably to their existing levels of stress. Signs of understimulation, as represented in Tables 2 and 5, were grossly evident throughout the facility. Although the breeder lake is larger than other enclosures, boundary exploration (Fig. 12) was common or extremely common and constitutes search and escape behaviour that is causally-related to overly restrictive conditions (Warwick 1990). Apart from the adult breeder lake, which possessed an artificial beach for egg-laying, and the naturalistic lagoon which accommodated only a few small display turtles, none of the turtle enclosures possessed environmental enrichment features.
In nature, green turtles are largely solitary animals that occupy large spatial ranges, and diverse and stimulating environments. Important essential innate drive states and biological needs cannot be provided for in the highly limited captive conditions of the CTF and these deficiencies probably importantly underline numerous problematic stress-related physical and behavioural manifestations.
Historically, public handling of turtles at the CTF was often unsupervised and arbitrary, and incidental handling abuses, including falls, were recorded (WSPA unpublished). Impact injuries from ‘drops’ may result in covert fractures and other harm and this presented an additional welfare concern. Turtle handling was supervised during the direct onsite inspection and it was noted that a revised policy has resulted in turtle handling being confined to holding the animals ‘over water’ for their protection. However, the majority of turtles were clearly stressed by the handling experience and manifested antipredator and escape behaviours (Gillingham 2004; Mellgren and Mann 2003; Smith and Salmon 2009).
Occasional acute stressors, while disturbing for animals, are not necessarily harmful experiences and physiological conditions can rapidly re-stabilise following an event (Guillette et al. 2004; Warwick 2004). However, this does not imply that arbitrarily subjecting the turtles to acute stressors is consistent with good animal care, and there exists the potential that repeated acute stress episodes may lead to compromised wound healing and pathology (French et al. 2005; Warwick 2004).
The contrast in behaviour that we observed between turtles in the general display enclosures and those in the relatively large and naturalistic lagoon was considerable, with turtles in the naturalistic lagoon showing no signs of captivity-stress, besides occasional boundary exploration, which probably emerges from the hard-wired behaviour for these animals to travel long distances and encounter novel environments.
It is also concerning that the farm holds numerous very large individuals of hawksbill turtles (Eretmochelys imbricata) and Kemp’s ridley turtles (Lepidochelys kempii) as apparent long-term attractions in spatially extremely restrictive and understimulating enclosures. One mature specimen of the latter species possessed signs of both extensive physical injury and symptoms of microbial infection concomitant with poor animal welfare and husbandry.