Peer Reviewed Science February ’17


Hello, new home with new science for you guys on the ground. We would love any and all feedback about the new site and always looking for ways to get you what you need, so do please contact us via the mail logo on each page.

Absolute monster volume with a load of papers to get your teeth sunk into – grrrrr science!


Island, H. D., Wengeler, J. and Claussenius-Kalman, H. (2017), The flehmen response and pseudosuckling in a captive, juvenile Southern sea otter (Enhydra lutris nereis). Zoo Biology.


A juvenile, female sea otter (Enhydra lutris nereis) was observed in 43 instances of the flehmen response over 19 days from May through July of 2015 at the Oregon Zoo. In all flehmen grimace observations, the juvenile sea otter engaged in nibbling, nosing, or licking the peri-mammary or anogenital areas of a non-lactating, geriatric female sea otter. The flehmen behavior observed was consisted with the sequences of behavior documented in other mammals, lifting the head, elevating the nose to the air, retracting the upper lip slightly, and manipulating her mystacial vibrissae back and forth while rapidly inspiring air through her mouth in quick succession, tongue extruded. The occurrence of this behavior was not specific to visitor density, visitor impact rating, day of the month, time of day, or exhibit zone. However, it did occur more frequently in one area of the enclosure. Among the three sea otters (two females, one male) currently housed at the Oregon Zoo, the juvenile female’s flehmen response only occurred following interactions with the older female and was always preceded by the pseudosuckling or anogenital nosing, licking or nibbling behavior.

Stannard, H. J., Bekkers, J. M., Old, J. M., McAllan, B. M. and Shaw, M. E. (2017), Digestibility of a new diet for captive short-beaked echidnas (Tachyglossus aculeatus). Zoo Biology.


Short-beaked echidnas (Tachyglossus aculeatus) are myrmecophages, or ant and termite insectivore specialists, and replicating their exact diet in captivity is problematic. Diets for captive animals often incorporate raw meat, eggs and cat food mixed together with water, and vitamin and mineral supplements. These diets have promoted a number of health problems in captive echidnas, such as gastritis, cystitis, gut impaction, obesity, and diarrhea. A manufactured diet was designed and three echidnas from two zoos were transitioned onto this diet to assess the acceptability and digestibility of this diet for echidnas. The new “test” diet was readily accepted by the echidnas with a 1 week transition period. Daily digestible energy intake was 280 kJ kg−0.75 d−1, similar to another myrmecophagous species. Digestibility values were above 74% for all macronutrients. It was determined that this diet was an acceptable replacement for the previous diets and it was decided that the remaining echidnas at both institutions would be transitioned to the new diet. The diet will also be used for wild echidnas being rehabilitated in the zoo hospitals prior to release and commercially available within Australia. Further data are being collected to assess the use of this diet for seasonal weight management, transitioning hand-reared puggles and effects on gastrointestinal tract health.

Cabana F, Plowman A, Van Nguyen T, Chin S-C, Wu S-L, Lo H-Y, Watabe H, and Yamamoto F. Feeding Asian pangolins: An assessment of current diets fed in institutions worldwide.


Pangolins are ant specialists which are under intense threat from the illegal wildlife trade. Nutrition has notoriously been their downfall in captivity and is still an issue in regards to rescue and rehabilitation. We analyzed the nutrient content of diets used by institutions that are successfully keeping Asian pangolins and to assess the variety of the ingredients and nutrients, compared these with the nutritional requirements of potential nutritional model species. We performed intake studies at five institutions and also had data from three other institutions. We also analyzed five different wild food items to use as a proxy of wild diet. We observed two categories of captive diets: those mostly or completely composed of insects and those high in commercial feeds or animal meat. Nutrient values were broad and there was no clear rule. The non-protein energy to protein energy ratio of the diets were much higher than the wild food items, more so for those which receive less insects. The average contribution of carbohydrate, fat, and protein energy were also further away from the wild samples the less insects they contained. The previously suggested nutritional model for pangolins is the domestic dog which is supported by our relatively large nutrient ranges of apparently successful diets, however, due to their highly carnivorous nature; the upper most nutrient intake data are not consistent with this and favor the feline nutrient recommendations. We are unable to render a conclusion of what model is more appropriate based on our data collected.


February 2017  Volume 187, Pages 85–92

David Benhaïm, Mathieu Ramos, Sébastien Ferrari, Kouakou Yao, Marie-Laure Bégout. 2017. Self-feeding behaviour and personality traits in tilapia: A comparative study between Oreochromis niloticus and Sarotherodon melanotheron
Hybridization aims at combining valuable traits from two species into a single group. Nile tilapia Oreochromis niloticus (NT) and Black-chinned tilapia Sarotherodon melanotheron (BCT) are respectively characterized by fast growth and water salinity tolerance which attract the breeders who could take advantage of both species. The first step is to characterize both species behavior in different contexts. The aim of this study was to compare the self-feeding behaviour between NT and BCT with a design allowing to reveal individual and group feed demand behaviour and then to identify the individual specialization that builds around the device and the food dispenser. The second objective was to estimate the links between the individual specialization and personality traits. To this aim, we recorded feed demand behaviour of both species using a computerized self-feeding device (two tanks for each species containing 20 PIT-tagged individuals with a male-female ratio of about 47%). Personality traits of all individuals were subsequently characterized with an open field test (OFT). The links between feed-demand and personality were then analyzed. Growth performances were not significantly different between NT and BCT but there was a strong tank effect. The individual specialization was similar in NT and BCT and similar to that previously observed in sea bass i.e. 1–3 individuals responsible for most of the feed demand activity in the tanks. Most NT individuals stayed in the shelter during the open field test while most of BCT individuals moved out of it. Overall, NT were shyer than BCT or the OFT was not adapted to NT. Linking the results of the self-feeding experiment and OFT in BCT, we found a strong positive correlation between the triggering activity and females’ shyness. Fish that spent more time inside than outside the shelter and which latency to emerge from shelter was longer, were characterized by a higher triggering activity (high-triggering fish). This study confirms the NT ability to use self-feeder devices and provides the first insight into the same ability in BCT and demonstrates links with personality traits. These results have a potential interest for the success of BCT and NT hybridization.
Animal Welfare Volume 26, Number 1, February 2017

Mancera, KF; Murray, PJ; Lisle, A; Dupont, C; Faucheux, F; Phillips, CJC 

The effects of acute exposure to mining machinery noise on the behaviour of eastern blue-tongued lizards (Tiliqua scincoides)  Number 1, February 2017, pp. 11-24(14)

The mining industry is an important source of noise for wildlife, and the eastern blue-tongued (EBT) lizard (T) is an Australian animal that may be impacted. We analysed the behaviour of nine EBT lizards during and after exposure for 5 s to one of five combinations of mining machinery noise frequency and amplitude (frequency < or > 2 kHz, low [60 65 dB (A)] and high [70 75dB (A)] amplitude, or a control treatment). Following exposure, lizards could leave the test chamber and enter an escape chamber, which led into a small hiding chamber. Chambers were monitored for 15 min after initial exposure. In the test chamber, lizards exposed to high frequency, high amplitude noise spent more time freezing, a typical stress response in reptiles, when compared with animals in all the other treatments. This was especially the case for lizards exposed to high frequency noise. In the hiding chamber, high frequency noise at high amplitudes decreased durations of head positioning to the right and downwards, suggesting a lateralised fear reaction, but decreased standing and freezing behaviours. We hypothesise that lizards have lateralised behaviour reactions to mining noise, with high frequency, high amplitude noise being the most detrimental. Our results demonstrate that acute exposure to mining noise had negative effects on EBT lizards behaviour and welfare, which may suggest a threat for lizards experiencing chronic mining noise in the wild, making the study of mining machinery noise a research priority.

[might have some relevance to zoo collections when infrastructure work is being carried out]


Olfactory Enrichment in California Sea Lions (Zalophus californianus): An Effective Tool for Captive Welfare? Journal of Applied Animal Welfare Science Vol. 20 , Iss. 1,2017
In the wild, California sea lions (Zalophus californianus) are exposed to a wide variety of sensory information, which cannot be replicated in captive environments. Therefore, unique procedures are necessary for maintaining physiological and psychological health in nonhuman animals in captivity. The effects of introducing natural scents to captive enclosures have been investigated in a variety of species, yet they have not been examined in marine mammals. This project explored the behavioral effect of scent added to the environment, with the goal of improving the welfare of sea lions in captivity. Two scent types were introduced: (a) natural scents, found in their native environment, and (b) non-natural scents, not found in their native environment. This study examined not only scent enrichment but also the possible evolutionary underpinnings of pinniped olfaction. Scent enrichment was found to significantly impact sea lion behavior as demonstrated by a reduction in pattern swimming, an increase in habitat utilization, and a reduction in stereotypical behavior. However, there were no differences in behavior between natural and non-natural scent conditions.
Liu H, Duan H, Wang C (2017) Effects of Ambient Environmental Factors on the Stereotypic Behaviors of Giant Pandas (Ailuropoda melanoleuca). PLoS ONE 12(1): e0170167.
Stereotypies are commonly observed in zoo animals, and it is necessary to better understand whether ambient environmental factors contribute to stereotypy and how to affect animal welfare in zoo settings. This study investigated the relationships between stereotypic behaviors and environmental factors including ambient temperatures, humidity, light intensity, sound intensity and number of visitors. Seven giant pandas were observed in three indoor enclosures and three outdoor enclosures. Environmental factors were measured for both indoor and outdoor enclosures and the effect they had on stereotypical behaviors was investigated. Our research found that light intensity significantly correlated with all stereotypies behaviors. Higher environmental temperature reduced the duration of pacing but increased the frequency of pacing, the duration and frequency of door-directed, meanwhile the duration of head-toss. However, we found no noticeable effect of humidity on stereotypic behaviors except for the frequency of head-toss. We also found that sound intensity was not correlated with stereotypies. Finally, the growth of visitors was negatively associated with the duration of door-directed. These results demonstrated that various environmental factors can have significant effects on stereotypic behaviors causing the expression of various stereotypies. Thus, stereotypies in zoo animals may not simply represent suboptimal welfare, but rather might be adopted as a means of coping with an aversive environment.
Byosiere S-E, Espinosa J, Marshall-Pescini S, Smuts B, Range F (2016) Investigating the Function of Play Bows in Dog and Wolf Puppies (Canis lupus familiaris, Canis lupus occidentalis). PLoS ONE 11(12): e0168570
Animals utilize behavioral signals across a range of different contexts in order to communicate with others and produce probable behavioral outcomes. During play animals frequently adopt action patterns used in other contexts. Researchers have therefore hypothesized that play signals have evolved to clarify communicative intent. One highly stereotyped play signal is the canid play bow, but its function remains contested. In order to clarify how canid puppies use play bows, we used data on play bows in immature wolves (ages 2.7–7.8 months) and dogs (ages 2 to 5 months) to test hypotheses evaluated in a previous study of adult dogs. We found that young dogs used play bows similarly to adult dogs; play bows most often occurred after a brief pause in play followed by complementary highly active play states. However, while the relative number of play bows and total observation time was similar between dog and wolf puppies, wolves did not follow this behavioral pattern, as play bows were unsuccessful in eliciting further play activity by the partner. While some similarities for the function of play bows in dog and wolf puppies were documented, it appears that play bows may function differently in wolf puppies in regards to re-initiating play.

Vol 5, No 1 (2017)


Christian Schiffmann, Marcus Clauss, Stefan Hoby, Jean-Michel HattVisual body condition scoring in zoo animals – composite, algorithm and overview approaches


Various body condition scoring (BCS) methods have been developed as management tools in zoo animal husbandry. In contrast to BCS for farm animals, where visual and palpable features are used, these protocols are mainly restricted to visual cues. Considering their inherent subjectivity, such methods face scepticism as their reliability is questioned. In terms of their respective methodology, composite BCS (where individual body regions are scored and a sum or mean is calculated), algorithm BCS (where a score is achieved by following a flow chart) and overview BCS protocols (where a score is given based on overall appearance) can be distinguished. In order to compare their practicability and consistency, we conducted a test with veterinary students (n=18) scoring an equal number (n=15) of African (Loxodonta africana) and Asian elephant (Elephas maximus) photographs using three different protocols. The composite approach showed least inter-observer consistency, while the overview protocol led to the highest differentiation of individual elephant condition. When regularly assessed, visual body condition scoring may serve as an important tool for the health surveillance and complete the medical history of individual zoo animals. Nonetheless, a validation process for each protocol developed should be carried out before its application. Further research might concentrate on long-term, individual-based body condition monitoring, using archives of standardised photographs.


Recapturing the canopy: stimulating Bornean orang-utan (Pongo pygmaeus) natural locomotion behaviour in a zoo environment

Tom S Roth, Thomas R Bionda, Elisabeth H M Sterck

Orang-utans are the largest mainly arboreal animal: wild orang-utans rarely come to the forest floor. In contrast, the locomotion behaviour of captive orang-utans encompasses more time on the ground and they spend less time on locomotion than their wild conspecifics. Moreover, their most frequently employed climbing postures differ from those of wild orang-utans. More natural locomotion behaviour may be stimulated by the design of appropriate enclosures. This study aimed to investigate how the design of orang-utan enclosures influences locomotion behaviour both quantitatively (i.e. time spent above ground and on locomotion) and qualitatively (i.e. types of movement). We collected continuous focal samples from 11 captive Bornean orang-utans (Pongo pygmaeus) at Apenheul Primate Park (Apeldoorn, The Netherlands). During the study, Apenheul offered two types of outdoor enclosures to their orang-utans: horizontal trunk enclosures with a relatively high number of large-diameter, horizontal tree trunks; and multiple rope enclosures with a relatively high number of small-diameter ropes. The results showed that the orang-utans’ quantitative locomotion behaviour was more natural in the horizontal trunk than in the multiple rope enclosures: they spent less time on the ground and more time on above-ground locomotion. However, the orang-utans’ qualitative locomotion behaviour seemed more natural in the multiple rope enclosures than in the horizontal trunk enclosures. This indicates that both horizontal trunks and small-diameter substrates are required to stimulate natural quantitative and qualitative locomotion behaviour. Zoos can apply our recommendations to stimulate natural locomotion behaviour in captive orang-utans, which may improve their physical condition and thereby increase their wellbeing.


Infrared Thermography as a Diagnostic Tool for Pododermatitis in Captive Greater Flamingos (Phoenicopterus roseus)

Anita Tolpinrud, Michelle F O’Brien, Will S. M. Justice, Michelle Barrows, Oliver D.M Steele, Sophie Gent, Anna Meredith

This cross-sectional study investigated the use of infrared thermography as a diagnostic tool for pododermatitis in captive greater flamingos (Phoenicopterus roseus). Photographs and thermal images were obtained for 775 feet from 408 flamingos held at three UK zoological collections. The feet were divided into eight regions, which were assigned a score for hyperkeratosis, fissures, nodules and papillomatous growths according to a previously defined scoring system. Minimum, mean and maximum temperatures were recorded for each region. 97 feet (12.5%) were scored as normal (no lesions or only mild hyperkeratosis), whilst 678 (87.5%) were scored as abnormal. It was found that 99.9% (95% confidence interval (CI): 99.3–100%) of the scored feet exhibited hyperkeratosis, 61.7% (95% CI: 58.2–65.1%) fissures, 16.0% (95% CI: 13.5–18.8%) nodules and 38.5% (95% CI: 35.0–42.0%) papillomatous growths. Thermal data assessed using general linear mixed effect modelling showed that regional and individual bird temperature differences accounted for most of the temperature variation, but there was a statistically significant (P<0.05) difference between regions with nodules versus regions without when using maximum temperatures. Intra- and inter-foot variation, using a regional correction factor and ankle temperatures, was assessed for 272 birds, where temperature distributions for each lesion type were compared with that of normal regions using t-tests. A statistically significant difference (P<0.05) was found between corrected values for regions with hyperkeratosis and papillomatous growths compared with normal, but no difference was found for fissures or nodules. Despite the differences found, the results suggest that infrared thermography may not be a practical diagnostic tool for pododermatitis in flamingos due to wide temperature variations between and within normal feet and a great degree of overlap of temperatures between normal and abnormal feet.


Feeding practices for captive giraffes (Giraffa camelopardalis) in Europe: A survey in EEP zoos

Isabel Gussek, Stefan Hirsch, Monika Hartmann, Karl-Heinz Südekum, Jürgen Hummel

As with other browsing ruminants, the nutrition of giraffes (Giraffa camelopardalis) can be challenging. Feeding browse in very large amounts is not feasible. Therefore, substitutes need to be provided that have to meet requirements and the species’ digestive capacity to the greatest possible extent. To achieve a comprehensive overview of current giraffe feeding practice in Europe, a survey was conducted among 153 member zoos of the European Endangered Species Programme. Information from 81 returned questionnaires showed a considerable variety of feeds being provided in varying proportions. The use of lucerne hay (89% of zoos) and fresh browse as trees or branches (96% of zoos) was more common than stated in previous studies. The use of a pelleted compound feed was almost standard practice, but many diets additionally contained cereal grains, as concentrate feeds high in rapidly fermentable starch. Eighty-five percent of the zoos reported feeding fresh fruits and vegetables, even though this is not recommended due to high sugar contents with a potentially negative influence on ruminal fermentation. The estimated non-forage proportion (sum of concentrate feeds and fresh fruits and vegetables) in the overall dietary dry matter (DM) was 37% in summer and 43% in winter (median), which is in accordance with recommendations. However, a considerable range of non-forage proportions was found, with 43% of the zoos providing amounts that were likely to be exceeding 50% of the potential daily DM intake. Data on dietary proportions revealed a geographical variation, with zoos from Western Europe showing the lowest and zoos from Eastern Europe showing the highest proportion of concentrate feeds in rations. An index of feeding appropriateness, oriented towards conformity with feeding recommendations, may be useful to evaluate and improve feeding management precisely and individually, as room for improvement was revealed for half of the participating zoos.


Hand-rearing the critically endangered blue-eyed black lemur (Eulemur flavifrons): milk formula, feeding and socialisation protocols

Benoît Quintard, Thierry Petit, Brice Lefaux

The blue-eyed black lemur (Eulemur flavifrons) is critically endangered in the wild and managed by ex-situ programmes in zoos. The breeding success in the European population is low and within the last five years, there have only been three births that survived. To try to increase the rate of infant survival, a systematic hand-rearing protocol was developed in 2013 and used on five infants from two different females that did not properly raise their infants. Milk formula was created with a mix of human newborn formula and kitten replacement milk. The lemur infants were fed ten times a day at the beginning, on a 24-hour round-the-clock basis. Solid food was offered as early as Day 7 and complete weaning was achieved without any medical issues around Day 107. The socialisation protocol consisted of maintaining permanent visual, olfactory and auditory contact with the parents from the day of the birth. First attempts to put the infants on their mother began as early as Day 2, but results varied, including successes with the parents, with conspecifics or lemurs from another Eulemur species. More work is needed to develop a feeding protocol which would also include the physiological variations in milk composition during the lactation period. Although many studies and reports have described hand rearing mammals, and more specifically lemurs, none of them describe a successful and complete protocol for five infants of the critically endangered blue-eyed black lemur.


Aquaculture Nutrition – December 2016 Volume 22 Issue 6


Farías A., Martínez-Montaño E., Espinoza V., Hernández,J., Viana M.T. and Uriarte I. (2016), Effect of zooplankton as diet for the early paralarvae of Patagonian red octopus, Enteroctopus megalocyathus, grown under controlled environment. Aquaculture Nutrition, 22: 1328–1339.


Growing octopus paralarvae is still very hard, with proper prey selection the major problem.  Artemia enriched with phytoplankton or commercial enrichment showed improved survival over cab zoea or standard Artemia, but maximum survival was still only 33%


Aquaculture Research- December 2016 Volume 47 Issue 12




Mélo R. C. S., Santos L. P. d. S., Brito A. P. M., Gouveia A. d. A., Marçal,C. and Cavalli R. O. (2016), Use of the microalga Nannochloropsis occulata in the rearing of newborn longsnout seahorse Hippocampus reidi (Syngnathidae) juveniles. Aquaculture Research, 47: 3934–3941.

 Adding the green microalgae (aprox. 2million cells per ml) to the water used for rearing the animals improved growth and survival rate, probably due to the live food (copepods and Artemia) consuming the algae before themselves being eaten, improving the nutritional benefits for the juvenile seahorses.


Journal of Experimental Marine Biology and Ecology- February 2017 Volume 487



O’Donnell K. E, Lohr K.E, Bartels E, Patterson J.T. (2017) Evaluation of staghorn coral (Acropora cervicornis, Lamarck 1816) production techniques in an ocean-based nursery with consideration of coral genotype. Journal of Exp. Marine Biology and Ecol. 487:53-58

A. cervicornis grown free hanging in the water column (the “tree” method), grow up to three times faster than the same propagations affixed to blocks on the sea floor.


Marine Biology- January 2017 Volume 164, Issue 22


Kohda M., Yamanouchi H., Hirata T. (2017) A novel aspect of goby–shrimp symbiosis: gobies provide droppings in their burrows as vital food for their partner shrimps. Marine Biology, 164:22


The communal benefits of the goby/shrimp symbiosis seem to go deeper than somewhere to live and some protection.  The shrimp are seldom seen eating outside of the burrow and the goby is seldom seem defecating outside as well.  After experimentation it seems that the shrimp consume the feces of the goby as a primary food source.

Schmiege P.F.P., D’Aloia C.C. & Buston P.M. (2017) Anemonefish personalities influence the strength of mutualistic interactions with host sea anemones. Marine Biology. 164: 24.


“Shy” anemones, those that stayed closer to their anemone, boosted the growth of the host, either by increased oxygenation, increased nutrition from waste and introduced food, or by increased parasite and predator protection.


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