Peer Reviewed Science June ’17

 

Welcome to June’s edition of Zoo Science for Keepers and Aquarists. Whether its the beginning of your winter or summer the new season is here!

Aquaculture Research- June 2017 Volume 48  Issue 6

Balamurugan J., Ajith Kumar T. T., Kathiresan K., Meenakumari, B. (2017), Determination of growth, colour and other traits in F1 hybrid of Amphiprion percula (male) × A. ocellaris (female). Aquac Res, 48: 2989–3003. doi:10.1111/are.13132

Abstract: This study reported the traits values such as colour, feed conversion ratio (FCR), specific growth rate (SGR) and fluorescence capacity of F1 hybrids of Amphiprion percula (male) and A. ocellaris(female). The hybrids exhibited significant variation in FCR (3.63 ± 0.56) and SGR (3.63% ± 0.44) compared with the pure breeds, A. percula (3.12 ± 0.42; 2.80% ± 0.42) and A. ocellaris (3.17 ± 0.43; 3.02% ± 0.19). An exponential relationship was found between FCR and SGR in both the breeds. Image analysis displayed a better colour performance of hybrid than the pure breeds. Individual body parts of the hybrid and pure breeds showed significant colour variation between each other. However, colour contrast of whole body of hybrid was found closer to A. ocellaris in hue cone and towards A. percula in saturation and brightness values. Hence, hybrid displays combination colour reflexion of both the parents. The total pigment content of hybrid (65.71 μg g−1 ± 2.81) was found higher than A. ocellaris (62.01 μg g−1 ± 2.29) and A. percula (56.71 μg g−1 ± 2.56). Further, the spectroflurometric analysis revealed that the both hybrid and pure breeds having poor fluorescence on skin pigmentation. A direct positive heterosis was observed on the SGR, FCR, total pigment and spawning frequency, while negative effect was noted on total length of newly hatched larvae (TL), fertilization rate (FrR), hatching rate (HR), deformation rate (DFR) and survival rate (SR). Hence, multiple cross-breeding programmes will help in developing high-quality traits in successive generations.

Yu J., Tian J.,Yang G. (2017), Ingestion, fecundity and population growth of Harpacticus sp. (Harpacticoida, copepod) fed on five species of algae. Aquac Res, 48: 2209–2220. doi:10.1111/are.13057

Abstract: We investigated the ingestion, fecundity and population growth of Harpacticus sp. fed on monodiet or mixed diets to evaluate the effects of different algae on Harpacticus sp. Harpacticussp. fed on diatoms (Skeletonema costatum and Chaetoceros curvisetus) had higher ingestion and pellet production. Time to attain 100% in proportions of gravid females differed, with quickest to slowest: S. costatum, C. curvisetus, Gymnodinium sp. and Heterosigma akashiwo, with the exception of Prymnesium parvum (≤16.67%). S. costatum or C. curvisetus produced higher populations than the other three diets, supported complete development to adulthood, and resulted in doubling copepod population within four days, while no population growth occurred for the other three diets. Mixed-diet experiments showed that egg production and gross growth efficiencies reduced significantly when fed on Hakashiwo, Gymnodinium sp. or P. parvum mixed with Isochrysis galbana, in comparison with 100% Igalbana. Thus, S. costatum and C. curvisetus were beneficial foods while the other three diets were potentially toxic for Harpacticus sp. The data in this article provide further recognition of nutrient deficiency or toxicity of different algae on copepods.

Bayrami A., Allaf Noverian H., Asadi Sharif E. (2017), Effects of background colour on growth indices and stress of young sterlet (Acipenser ruthenus) in a closed circulated system. Aquac Res, 48: 2004–2011. doi:10.1111/are.13033

Abstract: In this study, the physiological response and growth performances of Acipenser ruthenus were investigated after a long-term background colour adaptation (12 weeks). Twelve groups of 10 individuals with initial mean body weight of 183 g were reared in black, dark blue, grey and white tanks (three replicates for each colour). At the end of the experiments, growth (initial body weight, final body weight, weight gain per cent, food efficiency ratio, protein efficiency ratio, specific growth rate), blood (cortisol, glucose, pO2, pCO2, pH, haematocrit, osmolality, triglycerides, cholesterol, total lipids) and liver (hepatosomatic index, total lipids, glycogen) parameters were analyzed. Plasma cortisol in the dark-adapted sterlet (21.95 ± 3.9 ng mL−1) was significantly lower than those in white-adapted fish (39.44 ± 6.5 ng mL−1), whereas there were no significant differences in cortisol levels between the grey-adapted fish (23.05 ± 4.1 ng mL−1) and dark blue-adapted fish (24.2 ± 3.6 ng mL−1). A remarkable increase in mean of body weight (%) was detected in dark-adapted sterlet (45.2 ± 3.2) being 27.67%, 12.1% and 11.8% higher than the white, grey and dark blue-adapted fish respectively. The obtained results verified that different background colours lead to different growth performances and physiological responses of starlet, depending on rearing conditions.

 

North American Journal of Aquaculture – June 2017 Volume 79 Issue 3

Degidio J. L. A., Yanong R. P. E., Watson C. A., Ohs C. L., Cassiano E. J., Barden K., (2017) Spawning, Embryology, and Larval Development of the Milletseed Butterflyfish Chaetodon miliaris in the Laboratory, N. American Journal of Aqua., 79:3 205-215, doi.org/10.1080/15222055.2017.1302025

Abstract: As part of the Rising Tide Conservation effort to advance marine ornamental aquaculture the Milletseed Butterflyfish Chaetodon miliaris (also known as Millet Butterflyfish) was chosen as a candidate species for developing butterflyfish aquaculture methodologies. Thirty-five mature Milletseed Butterflyfish were imported to University of Florida’s Tropical Aquaculture Laboratory in Ruskin, Florida, from The Rainbow Reef exhibit at Aulani, a Disney Resort and Spa in Ko Olina, Hawaii, for evaluation. Spawning behavior was documented through personal and video observation five times. Eggs were collected immediately after spawning and checked for fertilization, and a sample of 100 ± 10 eggs were photographed every hour until hatching to document embryological development. Larval development was monitored through multiple rearing trials. Larvae were stocked into 128-L, cylindrical, rearing tanks at 15–20 larvae/L and fed nauplii of the copepod, Parvocalanus crassirostris, and the microalgae, Tisochrysis lutea, was added to green the water. Samples of larvae were measured using notochord length from the tip of the snout to the edge of the notochord prior to flexion, SL from the tip of the snout to the edge of the hypural plate, and TL. Spawning occurred in broodstock tanks between one dominant male and a single female with a large, swollen abdomen. Eggs of the Milletseed Butterflyfish were small, spherical, pelagic, and transparent and hatched after a 28-h period at 25.5°C. Newly hatched larvae had unpigmented eyes and a closed digestive tract and measured 1.20–1.24 mm in notochord length. Larvae were capable of feeding at 4 d posthatch (dph), fully absorbed the yolk sac by 7 dph, and began forming the tholichthys plates at 24 dph. Larvae survived to 44 dph in preliminary culture trials and measured 6.49–6.56 mm TL. Further investigation into the culture requirements of Milletseed Butterflyfish will supply a crucial base for developing aquaculture protocols for other marine ornamental species.

The Veterinary Record

Justice, W.S.M., O’Brien, M.F., Szyszka, O., Shotton, J., Gilmour, J.E.M., Riordan, P. and Wolfensohn, S., 2017. Adaptation of the animal welfare assessment grid (AWAG) for monitoring animal welfare in zoological collections. The Veterinary record.

http://dx.doi.org/10.1136/vr.104309

Animal welfare monitoring is an essential part of zoo management and a legal requirement in many countries. Historically, a variety of welfare audits have been proposed to assist zoo managers. Unfortunately, there are a number of issues with these assessments, including lack of species information, validated tests and the overall complexity of these audits which make them difficult to implement in practice. The animal welfare assessment grid (AWAG) has previously been proposed as an animal welfare monitoring tool for animals used in research programmes. This computer-based system was successfully adapted for use in a zoo setting with two taxonomic groups: primates and birds. This tool is simple to use and provides continuous monitoring based on cumulative lifetime assessment. It is suggested as an alternative, practical method for welfare monitoring in zoos.

Zoo Biology – In Press articles

Kearns, P.J., Bowen, J.L. and Tlusty, M.F., 2016. The skin microbiome of cow-nose rays (Rhinoptera bonasus) in an aquarium touch-tank exhibit (No. e2341v1).

DOI: 10.1002/zoo.21362

Public aquaria offer numerous educational opportunities for visitors while touch-tank exhibits offer guests the ability to directly interact with marine life via physical contact. Despite the popularity of touch-tanks, there is a paucity of research about animal health in these exhibits and, in particular, there is little research on the microbial communities in these highly interactive exhibits. Microbial community structure can have implications for both host health and habitat function. To better understand the microbiome of a touch-tank we used high-throughput sequencing of the 16S rRNA gene to analyze the microbial community on the dorsal and ventral surfaces of cow-nose rays (Rhinoptera bonasus) as well as their environment in a frequently visited touch-tank exhibit at the New England Aquarium. Our analyses revealed a distinct microbial community associated with the skin of the ray that had lower diversity than the surrounding habitat. The ray skin was dominated by three orders: Burkholderiales (∼55%), Flavobacteriales (∼19%), and Pseudomonadales (∼12%), taxonomic groups commonly associated with other fish species. Our results provide a survey of ray-associated bacterial communities in a touch-tank environment, thereby laying the foundation for future studies examining the role of potential challenges to ray microbiota and their associated health.

Orban DA, Soltis J, Perkins L, Mellen JD. Sound at the zoo: Using animal monitoring, sound measurement, and noise reduction in zoo animal management. Zoo Biology. 2017

https://doi.org/10.1002/zoo.21366

A clear need for evidence-based animal management in zoos and aquariums has been expressed by industry leaders. Here, we show how individual animal welfare monitoring can be combined with measurement of environmental conditions to inform science-based animal management decisions. Over the last several years, Disney’s Animal Kingdom® has been undergoing significant construction and exhibit renovation, warranting institution-wide animal welfare monitoring. Animal care and science staff developed a model that tracked animal keepers’ daily assessments of an animal’s physical health, behavior, and responses to husbandry activity; these data were matched to different external stimuli and environmental conditions, including sound levels. A case study of a female giant anteater and her environment is presented to illustrate how this process worked. Associated with this case, several sound-reducing barriers were tested for efficacy in mitigating sound. Integrating daily animal welfare assessment with environmental monitoring can lead to a better understanding of animals and their sensory environment and positively impact animal welfare.

Maclachlan, N., Hunt, G., Fowkes, S., Frost, M., Miller, J., Purcell‐Jones, G., Sullivan, P., Barbon, A., Routh, A., López, F.J. and Price, E.C., 2017. Successful treatment of infertility in a female Sumatran orangutan Pongo abelii. Zoo Biology36(2), pp.132-135.

https://doi.org/10.1002/zoo.21350

In 2011, a female Sumatran orangutan housed at Durrell Wildlife Conservation Trust became infertile following a massive antepartum hemorrhage in labor and the delivery of a stillborn infant. The placenta was infected with Pantoea sp. Hysterosalpingography (HSG) revealed blocked fallopian tubes, and pressurized fallopian tube perfusion was used to reverse the tubal occlusion. She subsequently conceived and following an intensive training program, we were able to measure umbilical artery waveform analysis for fetal well-being and placental localization to exclude placenta previa, which could complicate pregnancy and lead to catastrophic hemorrhage. The female went on to deliver a healthy offspring. We suggest that these techniques should be considered for other infertile females in the global captive population.

Schell CJ, Young JK, Lonsdorf EV, Mateo JM, Santymire RM. Investigation of techniques to measure cortisol and testosterone concentrations in coyote hair. Zoo Biology. 2017

https://doi.org/10.1002/zoo.21359

Long-term noninvasive sampling for endangered or elusive species is particularly difficult due to the challenge of collecting fecal samples before hormone metabolite desiccation, as well as the difficulty in collecting a large enough sample size from all individuals. Hair samples may provide an environmentally stable alternative that provides a long-term assessment of stress and reproductive hormone profiles for captive, zoo, and wild mammals. Here, we extracted and analyzed both cortisol and testosterone in coyote (Canis latrans) hair for the first time. We collected samples from 5-week old coyote pups (six female, six male) housed at the USDA-NWRC Predator Research Facility in Millville, UT. Each individual pup was shaved in six different locations to assess variation in concentrations by body region. We found that pup hair cortisol (F5,57.1 = 0.47, p = 0.80) and testosterone concentrations (F5,60 = 1.03, p = 0.41) did not differ as a function of body region. Male pups generally had higher cortisol concentrations than females (males = 17.71 ± 0.85 ng/g, females = 15.48 ± 0.24 ng/g; F1,57.0 = 5.06, p = 0.028). Comparatively, we did not find any differences between male and female testosterone concentrations (males = 2.86 ± 0.17 ng/g, females = 3.12 ± 0.21 ng/g; F1,60 = 1.42, p = 0.24). These techniques represent an attractive method in describing long-term stress and reproductive profiles of captive, zoo-housed, and wild mammal populations.

Applied Animal Behaviour Science – June 2017, Volume 191 and In Press articles

Robinson, L.M., Altschul, D.M., Wallace, E.K., Úbeda, Y., Llorente, M., Machanda, Z., Slocombe, K.E., Leach, M.C., Waran, N.K. and Weiss, A., 2017. Chimpanzees with positive welfare are happier, extraverted, and emotionally stable. Applied Animal Behaviour Science, 191. pp. 90-97.

http://dx.doi.org/10.1016/j.applanim.2017.02.008

Facilities housing captive animals are full of staff who, every day, interact with the animals under their care. The expertise and familiarity of staff can be used to monitor animal welfare by means of questionnaires. It was the goal of our study to examine the association between chimpanzee (Pan troglodytes) welfare, happiness, and personality. To these ends we collected two waves of welfare and subjective well-being ratings of 18 chimpanzees housed at the Edinburgh Zoo and one set of ratings of 13 chimpanzees housed at Fundació Mona. Ratings were made on a welfare questionnaire that included 12 items related to stress, psychological stimulation, and behavioural indicators of negative and positive welfare states, and a 4-item subjective well-being questionnaire. In addition, ratings were made on the 54-item Hominoid Personality Questionnaire and an abbreviated version of this scale consisting of 37 antonym pairs. We used generalizability theory to test whether welfare ratings generalized across items, raters, chimpanzees, and time. We then assessed the validity of the welfare and subjective well-being questionnaires by examining their associations with behaviour. Finally, we tested whether the welfare and subjective well-being ratings were associated with personality. Welfare ratings generalized across items, raters, chimpanzees, and time. Principal components analysis and regularized exploratory factor analysis indicated that ten welfare items and all four subjective well-being items formed a single dimension (welfareSWB). LASSO regression found that lower welfareSWB was associated with regurgitation, coprophagy, urophagy, and decreased proximity to nearest neighbour. A linear model that adjusted for age, sex, and facility, indicated that higher Extraversion and lower Neuroticism were related to higher welfareSWB. Welfare ratings were reliable and associated with subjective well-being and personality, demonstrating that staff ratings are a valid and potentially valuable tool for chimpanzee welfare assessment.

Colchen, T., Elodie, F., Teletchea, F. and Pasquet, A., 2017. Is personality of young fish consistent through different behavioural tests?. Applied Animal Behaviour Science.

http://dx.doi.org/10.1016/j.applanim.2017.05.012

Most studies carried out on personality recognized that personality is defined by behavioural traits consistent through time and/or contexts. In fish, most studies on personality were performed either on juveniles (aged between 6 months and 1 year) or adults, but very few focused on the early life stages. The main goal of this study is to characterize behavioural syndromes and to highlight the existence of a personality in young juvenile pikeperch, a species with a strong economic value. To study the consistency of behavioural responses of juvenile (50 and 64 days post-hatch) pikeperch Sander lucioperca (n = 41, total length = 5.8 ± 1.0 cm and mass = 1.6 ± 0.7 g), we performed three tests per fish in one day: exploration (cross-maze), dyadic and restraint test. In the cross-maze test, exploratory fish were more active and bolder. In the dyadic test, fish with the highest number of contacts, showed also more approaches, orientations and avoidance behaviours. In the restraint test, bolder fish were more active and tried to escape more often. Consequently, the investigation of the different behavioural responses of each fish highlighted behavioural syndromes in this species. Furthermore, for the first time, we showed, with a cross-context analysis, that young juvenile pikeperch, responded in the same way to exploration and dyadic test but their responses were opposite in the restraint test. Our results opened new opportunities for testing individual personality in very young fish that may help solving some aquaculture problems, such as intra-cohort cannibalism.

Bouchard, B., Lisney, T.J., Campagna, S. and Célérier, A., 2017. Do bottlenose dolphins display behavioural response to fish taste?. Applied Animal Behaviour Science.

http://dx.doi.org/10.1016/j.applanim.2017.05.013

The chemosensory abilities (i.e. taste, smell and trigeminal perception) of odontocete cetaceans are still widely unknown. However, a better understanding of their potential use of these senses would not only improve our knowledge of their behavioural ecology, but also allow us to develop behavioural enrichment strategies for captive odontocetes using sensory stimulation. While studies on taste bud anatomy and the taste receptor genes in these animals have provided useful information, ultimately behavioural experiments are crucial to assess whether odontocetes use their sense of taste in water. Go/no go and conditioning experiments in bottlenose dolphins (Tursiops truncatus) have previously shown that they can perceive basic tastes, but it is still unclear whether they are able to detect food-related chemical mixtures. We thus designed a spontaneous choice experiment using floating taste diffusers in order to test whether captive bottlenose dolphins could detect and display attraction behaviours towards a natural fish taste stimulus. Four dolphins, two adult males and two juvenile females, were involved in the experiment. Our results show that the juvenile females interacted with the fish taste diffuser significantly more than with the control. However, the adult males did not seem to make a clear choice. Also, the juvenile females showed a significantly greater level of motivation towards the test, spending more time interacting with the diffusers and holding them in their open mouth more often than the adult males. These findings corroborate previous behavioural studies suggesting that taste perception is functional in bottlenose dolphins, at least in young individuals. They also suggest that the taste of their natural prey could be attractive to them. Finally, the methodology used in this study proved to be easy to implement in captive odontocetes and will allow for investigating further their use of taste in feeding and social contexts without the need for conditioning experiments that require long periods of training. This experimental design could also be included in behavioural enrichment initiatives in captive marine mammals.

Greco, B.J., Meehan, C.L., Heinsius, J.L. and Mench, J.A., 2017. Why pace? The influence of social, housing, management, life history, and demographic characteristics on locomotor stereotypy in zoo elephants. Applied Animal Behaviour Science.

http://dx.doi.org/10.1016/j.applanim.2017.05.003

Stereotypic behaviors (SB) are common in zoo-housed elephants, and these behaviors can be performed at high rates. Elephants perform different SB forms (e.g., weaving, pacing), but no published studies have evaluated the factors contributing to the development or performance of these different forms. Instead, as with most SB studies across species, elephant studies have relied on analyses that aggregate all SB forms, which limits the development and testing of form-specific hypotheses or abatement practices. Our objectives were to characterize the SB forms of North American zoo elephants and use multivariable epidemiological models to test form-specific hypotheses. We videotaped 77 elephants (African: N = 5 males, 31 females; Asian N = 8 males, 33 females) at 39 zoos who performed SBs and used a novel classification scheme and 5-minute instantaneous samples to characterize their SB forms. Locomotor and whole-body SBs were the most common, but most elephants who performed locomotor SBs also performed whole-body SBs. Thus, we characterized each elephant according to whether it included locomotion in its SB repertoire [Locomotor Presence (LP)] or only whole-body movements. We used binomial regression models fitted with generalized estimating equations to test hypotheses about which of 26 social, housing, management, life history, and demographic variables were most associated with LP. The odds of LP increased by 26% for every 10% increase in time housed separately (odds ratio = 1.026, p = 0.04), 96.2% for every additional social group with which an elephant had contact (odds ratio = 1.962, p = 0.01), and 46% for every 10% increase in time housed indoors (odds ratio = 1.046, p = 0.01). Age was non-significantly confounded with all three variables. We hypothesize that the social variables in our models increase LP risk because they are associated with uncontrollable social group changes, anticipation of potentially rewarding social experiences, or the frustration of social behaviors. The housing variable included in our model likely increases LP risk because indoor spaces are less complex, resulting in the channeling of walking or social avoidance behaviors into more simplistic movements. Overall, our results suggest that elephant managers may best be able to prevent locomotor SB by enhancing their elephants’ social environment and the spatial complexity of their enclosures. Future research should focus on determining whether addressing the risk factors for LP results in less frequent performance and identifying other temporally proximate eliciting factors.

Animal Welfare (UFAW)- May 2017, Volume 26(2)

Clegg, I.L.K., Van Elk, C.E. and Delfour, F., 2017. Applying welfare science to bottlenose dolphins (Tursiops truncatus). Animal Welfare26(2), pp.165-176.

Animal welfare science is a burgeoning field, but research on cetaceans (whales, dolphins and porpoises) is lacking. Bottlenose dolphins (Tursiops truncatus) are the most well-known and studied cetaceans, particularly in captivity, and thus are used in this review as a model for other cetacean species. Despite the public interest and need for such research, studies specifically investigating dolphin welfare are lacking. This review uses the three broad categories of behaviour, health, and cognition, to discuss how dolphin welfare has been assessed thus far, and could be assessed in future. We present welfare indicators validated in other species that could be applied to dolphins, including innovative measures, such as cognitive appraisal of emotions. We provide a summary of practical recommendations for validating the indicators of bottlenose dolphin welfare. This paper aims to stimulate further research into dolphin welfare which could improve the lives of the animals themselves and ultimately support regulatory decisions. We recommend uniting expertise in cetology and welfare science in order to develop a holistic approach to dolphin welfare assessment.

Scientific Reports – April 2017, Volume 7

Guida, L., Awruch, C., Walker, T.I. and Reina, R.D., 2017. Prenatal stress from trawl capture affects mothers and neonates: a case study using the southern fiddler ray (Trygonorrhina dumerilii). Scientific Reports7.

doi:10.1038/srep46300

Assessing fishing effects on chondrichthyan populations has predominantly focused on quantifying mortality rates. Consequently, sub-lethal effects of capture stress on the reproductive capacity of chondrichthyans are largely unknown. We investigated the reproductive consequences of capture on pregnant southern fiddler rays (Trygonorrhina dumerilii) collected from Swan Bay, Australia, in response to laboratory-simulated trawl capture (8 h) followed immediately by air exposure (30 min). Immediately prior to, and for up to 28 days post trawling, all females were measured for body mass (BM), sex steroid concentrations (17-β estradiol, progesterone, testosterone) and granulocyte to lymphocyte (G:L) ratio. At parturition, neonates were measured for total length (TL), BM and G:L ratio. Trawling reduced maternal BM and elevated the G:L ratio for up to 28 days. Trawling did not significantly affect any sex steroid concentrations relative to controls. Neonates from trawled mothers were significantly lower in BM and TL than control animals, and had an elevated G:L ratio. Our results show that capture of pregnant T. dumerilii can influence their reproductive potential and affect the fitness of neonates. We suggest other viviparous species are likely to be similarly affected. Sub-lethal effects of capture, particularly on reproduction, require further study to improve fisheries management and conservation of chondrichthyans.

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