Echolocation variability of franciscana dolphins (Pontoporia blainvillei) between estuarine and open-sea habitats, with insights into foraging patterns.

Environmental and ecological factors can trigger changes in the acoustic repertoire of cetaceans. This study documents the first use of a well-established passive acoustic monitoring device (C-POD) to analyze echolocation sounds and behavior of franciscana dolphins in different habitats: estuary [Babitonga Bay (BB)] and open sea [Itapirubá Beach (IB)]. A total of 10 924 click trains were recorded in BB and 6 093 in IB. An inter-click interval < 10 ms (so called "feeding buzzes") was used as a proxy for foraging activity. The main difference in the acoustic parameters between the two habitats was related to the frequency spectrum, with higher maximum and lower modal and minimum click frequencies in BB, and a train frequency range of 17 kHz, against 10 kHz in IB. Also, the click emission rate (clicks/s) was almost 20% higher in BB. Both studied habitats showed a high proportion of feeding buzzes (BB = 68%; IB = 58%), but with a higher probability of occurrence in BB (p < 0.001) and at night (p < 0.001) in both habitats. The C-PODs showed great potential to monitor occurrence, bioacoustics parameters, and echolocation behavior of franciscana dolphins. Longer-term temporal and spatial monitoring are necessary for elucidating several issues raised in this study.

Cross-fostering in gray wolves (Canis lupus lupus).

Cross-fostering in canids, with captive-bred pups introduced into endangered wild populations, might aid conservation efforts by increasing genetic diversity and lowering the risk of inbreeding depression. The gray wolf (Canis lupus lupus) population in Scandinavia suffers from severe inbreeding due to a narrow genetic base and geographical isolation. This study aimed at evaluating the method to cross-foster wolf pups from zoo-born to zoo-born litters. The following was assessed: female initial acceptance of foster pups, growth rate in relation to age difference between foster pups and pups in recipient litters and survival over the first 33 weeks. The study included four litters added by two foster pups in each. The age differences between the foster pups and the recipient litters were 2-8 days. After augmentation, all four females accepted the foster pups, demonstrated by her moving the entire litter to a new den site. Growth rate was dependent on the age difference of the pups in the foster litters, with a considerably slower growth rate in the 8 days younger pups. However, these pups later appeared to be at no disadvantage. Foster pups had a higher survival rate than females' pups, however, the causes of death were probably not kin or non-kin related. The results indicate that cross-fostering works in gray wolves and that this might be a plausible way to increase genetic variation in the wild population.

Olfactory discrimination ability of Asian elephants (Elephas maximus) for structurally related odorants.

Using a food-rewarded two-choice instrumental conditioning paradigm, we assessed the ability of Asian elephants, Elephas maximus, to discriminate between 2 sets of structurally related odorants. We found that the animals successfully discriminated between all 12 odor pairs involving members of homologous series of aliphatic 1-alcohols, n-aldehydes, 2-ketones, and n-carboxylic acids even when the stimuli differed from each other by only 1 carbon. With all 4 chemical classes, the elephants displayed a positive correlation between discrimination performance and structural similarity of odorants in terms of differences in carbon chain length. The animals also successfully discriminated between all 12 enantiomeric odor pairs tested. An analysis of odor structure-activity relationships suggests that a combination of molecular structural properties rather than a single molecular feature may be responsible for the discriminability of enantiomers. Compared with other species tested previously on the same sets of odor pairs (or on subsets thereof), the Asian elephants performed at least as well as mice and clearly better than human subjects, squirrel monkeys, pigtail macaques, South African fur seals, and honeybees. Further comparisons suggest that neither the relative nor the absolute size of the olfactory bulbs appear to be reliable predictors of between-species differences in olfactory discrimination capabilities. In contrast, we found a positive correlation between the number of functional olfactory receptor genes and the proportion of discriminable enantiomeric odor pairs. Taken together, the results of the present study support the notion that the sense of smell may play an important role in regulating the behavior of Asian elephants.

Olfactory discrimination ability of South African fur seals (Arctocephalus pusillus) for enantiomers.

Using a food-rewarded two-choice instrumental conditioning paradigm we assessed the ability of South African fur seals, Arctocephalus pusillus, to discriminate between 12 enantiomeric odor pairs. The results demonstrate that the fur seals as a group were able to discriminate between the optical isomers of carvone, dihydrocarvone, dihydrocarveol, menthol, limonene oxide, α-pinene, fenchone (all p < 0.01), and ß-citronellol (p < 0.05), whereas they failed to distinguish between the (+)- and (-)-forms of limonene, isopulegol, rose oxide, and camphor (all p > 0.05). An analysis of odor structure-activity relationships suggests that a combination of molecular structural properties rather than a single molecular feature may be responsible for the discriminability of enantiomeric odor pairs. A comparison between the discrimination performance of the fur seals and that of other species tested previously on the same set of enantiomers (or subsets thereof) suggests that the olfactory discrimination capabilities of this marine mammal are surprisingly well developed and not generally inferior to that of terrestrial mammals such as human subjects and non-human primates. Further, comparisons suggest that neither the relative nor the absolute size of the olfactory bulbs appear to be reliable predictors of between-species differences in olfactory discrimination capabilities. Taken together, the results of the present study support the notion that the sense of smell may play an important and hitherto underestimated role in regulating the behavior of fur seals.

From echolocation clicks to animal density--acoustic sampling of harbor porpoises with static dataloggers.

Monitoring abundance and population trends of small odontocetes is notoriously difficult and labor intensive. There is a need to develop alternative methods to the traditional visual line transect surveys, especially for low density areas. Here, the prospect of obtaining robust density estimates for porpoises by passive acoustic monitoring (PAM) is demonstrated by combining rigorous application of methods adapted from distance sampling to PAM. Acoustic dataloggers (T-PODs) were deployed in an area where harbor porpoises concurrently were tracked visually. Probability of detection was estimated in a mark-recapture approach, where a visual sighting constituted a "mark" and a simultaneous acoustic detection a "recapture." As a distance could be assigned to each visual observation, a detection function was estimated. Effective detection radius of T-PODs ranged from 22 to 104 m depending on T-POD type, T-POD sensitivity, train classification settings, and snapshot duration. The T-POD density estimates corresponded to the visual densities derived concurrently for the same period. With more dataloggers, located according to a systematic design, density estimates would be obtainable for a larger area. This provides a method suitable for monitoring in areas with densities too low for visual surveys to be practically feasible, e.g., the endangered harbor porpoise population in the Baltic.

Estimating the abundance of the critically endangered Baltic Proper harbour porpoise (Phocoena phocoena) population using passive acoustic monitoring.

Knowing the abundance of a population is a crucial component to assess its conservation status and develop effective conservation plans. For most cetaceans, abundance estimation is difficult given their cryptic and mobile nature, especially when the population is small and has a transnational distribution. In the Baltic Sea, the number of harbour porpoises (Phocoena phocoena) has collapsed since the mid-20th century and the Baltic Proper harbour porpoise is listed as Critically Endangered by the IUCN and HELCOM; however, its abundance remains unknown. Here, one of the largest ever passive acoustic monitoring studies was carried out by eight Baltic Sea nations to estimate the abundance of the Baltic Proper harbour porpoise for the first time. By logging porpoise echolocation signals at 298 stations during May 2011-April 2013, calibrating the loggers' spatial detection performance at sea, and measuring the click rate of tagged individuals, we estimated an abundance of 71-1105 individuals (95% CI, point estimate 491) during May-October within the population's proposed management border. The small abundance estimate strongly supports that the Baltic Proper harbour porpoise is facing an extremely high risk of extinction, and highlights the need for immediate and efficient conservation actions through international cooperation. It also provides a starting point in monitoring the trend of the population abundance to evaluate the effectiveness of management measures and determine its interactions with the larger neighboring Belt Sea population. Further, we offer evidence that design-based passive acoustic monitoring can generate reliable estimates of the abundance of rare and cryptic animal populations across large spatial scales.

Separating overlapping click trains originating from multiple individuals in echolocation recordings.

Recordings of the acoustic activity of free-swimming groups of echolocating dolphins increase the likelihood of collecting overlapping click trains, originating from multiple individuals, in the same set of data. In order to evaluate the click properties of each individual based on such recordings it is necessary to identify which clicks originate from which animal. This paper suggests a computationally efficient strategy to separate overlapping click trains originating from multiple free-swimming bottlenose dolphins, enabling echolocation analysis at an individual level on several animals. This technique is based on sequential matching of the frequency spectra of successive clicks. The clicks are grouped together as individual click trains if the correlation coefficients between clicks are higher than a pre-set threshold level. The robustness of the algorithm is tested by adding artificially generated white Gaussian noise and comparing the results with other comparable commonly used methods based on inter-click intervals, centroid frequencies, and amplitude levels. The described method is applicable to a variety of experimental and observational contexts, e.g., those regarding echolocation development of calves, the hypothesized acoustic "etiquette" among dolphins when investigating the same object, and the possible occurrence of eavesdropping in large dolphin pods.

47-channel burst-mode recording hydrophone system enabling measurements of the dynamic echolocation behavior of free-swimming dolphins.

Detailed echolocation behavior studies on free-swimming dolphins require a measurement system that incorporates multiple hydrophones (often >16). However, the high data flow rate of previous systems has limited their usefulness since only minute long recordings have been manageable. To address this problem, this report describes a 47-channel burst-mode recording hydrophone system that enables highly resolved full beamwidth measurements on multiple free-swimming dolphins during prolonged recording periods. The system facilitates a wide range of biosonar studies since it eliminates the need to restrict the movement of animals in order to study the fine details of their sonar beams.

Meerkats (Suricata suricatta) are able to detect hidden food using olfactory cues alone.

Meerkats (Suricata suricatta) are known to strongly rely on chemical signals for social communication. However, little is known about their use of the sense of smell in foraging and food detection. The aim of the present study was therefore to assess whether captive meerkats are able to (1) detect hidden food using olfactory cues alone, (2) discriminate between the odor of real food and a single food odor component, and (3) build an association between the odor of real food and a novel odor. We employed the buried food test, widely used with rodents to assess basic olfactory abilities and designed to take advantage of the propensity of certain species to dig. We found that the meerkats were clearly able to find all four food types tested (mouse, chicken, mealworm, banana) using olfactory cues alone and that they successfully discriminated between the odor of real food (banana) and a food odor component (iso-pentyl acetate). In both tasks, the animals dug in the food-bearing corner of the test arena as the first one significantly more often than in the other three corners. No significant association-building between a food odor and a novel odor was found within the 60 trials performed per animal. We conclude that meerkats are able to use olfactory cues when foraging for hidden food. Further, we conclude that the buried food test, employed for the first time with a non-rodent species, is a useful means of assessing basic olfactory capabilities in meerkats.

Successful acquisition of an olfactory discrimination paradigm by South African fur seals, Arctocephalus pusillus.

The present study demonstrates that South African fur seals, Arctocephalus pusillus, can successfully be trained to discriminate between objects on the basis of odor cues. Using a task based on a food-rewarded two-choice discrimination of simultaneously presented odor stimuli the animals acquired the basic operant conditioning paradigm within 480 to 880 stimulus contacts. Moreover, the fur seals could readily transfer to new S+ and S- stimuli, were capable of distinguishing between fish- and non-fish odors as well as between two fish odors, and were able to remember the reward value of previously learned odor stimuli even after 2- and 15-week breaks. The precision and consistency of the fur seals' performance in tests of discrimination ability and memory demonstrate the suitability of this paradigm for assessing olfactory function in this pinniped. An across-species comparison of several measures of olfactory learning capabilities such as speed of initial task acquisition and ability to master transfer tasks shows that A. pusillus is similar in performance to non-human primates, but inferior to rodents such as mice and rats. The results support the assumption that fur seals may use olfactory cues for social communication and food selection and that the sense of smell may play an hitherto underestimated role in the control of their behavior.

An echolocation visualization and interface system for dolphin research.

The present study describes the development and testing of a tool for dolphin research. This tool was able to visualize the dolphin echolocation signals as well as function as an acoustically operated "touch screen." The system consisted of a matrix of hydrophones attached to a semitransparent screen, which was lowered in front of an underwater acrylic panel in a dolphin pool. When a dolphin aimed its sonar beam at the screen, the hydrophones measured the received sound pressure levels. These hydrophone signals were then transferred to a computer where they were translated into a video image that corresponds to the dynamic sound pressure variations in the sonar beam and the location of the beam axis. There was a continuous projection of the image back onto the hydrophone matrix screen, giving the dolphin an immediate visual feedback to its sonar output. The system offers a whole new experimental methodology in dolphin research and since it is software-based, many different kinds of scientific questions can be addressed. The results were promising and motivate further development of the system and studies of sonar and cognitive abilities of dolphins.

Attractant or Repellent? Behavioral Responses to Mammalian Blood Odor and to a Blood Odor Component in a Mesopredator, the Meerkat (Suricata suricatta).

It is well-established that the odor of mammalian blood is attractive to top predators such as tigers and wolves and aversive to prey species such as mice and rats. Recent studies have shown that the mammalian blood odor component trans-4,5-epoxy-(E)-2-decenal (TED) elicits corresponding behavioral responses in these two groups of mammals. Here we assess whether a mesopredator, that is, a small-bodied carnivorous mammal that is both predator and prey, is attracted to or repelled by the odor of mammalian blood and TED. To this end, we assessed the behavior of a group of 15 captive meerkats (Suricata suricatta) when presented with wooden logs that were impregnated either with horse blood or with TED, and compared it to their behavior toward a fruity odor (iso-pentyl acetate) and a near-odorless solvent (diethyl phthalate). We found that the meerkats displayed significantly more interactions with the odorized wooden logs such as sniffing and pawing when these were impregnated with the two prey-associated odors compared to the two non-prey-associated odors. Most importantly, no significant difference was found in the number of interactions with the wooden logs impregnated with horse blood and TED, respectively. These results demonstrate that meerkats, despite being small-bodied mesopredators, are clearly attracted to the odor of mammalian blood. Further, the results suggest that a single blood odor component can be as efficient as the odor of real blood in eliciting behavioral responses in this herpestid mammal, similar to previous findings in feline and canine top predators.

Taste responsiveness to two steviol glycosides in three species of nonhuman primates.

Primates have been found to differ widely in their taste perception and studies suggest that a co-evolution between plant species bearing a certain taste substance and primate species feeding on these plants may contribute to such between-species differences. Considering that only platyrrhine primates, but not catarrhine or prosimian primates, share an evolutionary history with the neotropical plant Stevia rebaudiana, we assessed whether members of these three primate taxa differ in their ability to perceive and/or in their sensitivity to its two quantitatively predominant sweet-tasting substances. We found that not only neotropical black-handed spider monkeys, but also paleotropical black-and-white ruffed lemurs and Western chimpanzees are clearly able to perceive stevioside and rebaudioside A. Using a two-bottle preference test of short duration, we found that Ateles geoffroyi preferred concentrations as low as 0.05 mM stevioside and 0.01 mM rebaudioside A over tap water. Taste preference thresholds of Pan troglodytes were similar to those of the spider monkeys, with 0.05 mM for stevioside and 0.03 mM for rebaudioside A, whereas Varecia variegata was slightly less sensitive with a threshold value of 0.1 mM for both substances. Thus, all three primate species are, similar to human subjects, clearly more sensitive to both steviol glycosides compared to sucrose. Only the spider monkeys displayed concentration-response curves with both stevioside and rebaudioside A which can best be described as an inverted U-shaped function suggesting that Ateles geoffroyi, similar to human subjects, may perceive a bitter side taste at higher concentrations of these substances. Taken together, the results of the present study do not support the notion that a co-evolution between plant and primate species may account for between-species differences in taste perception of steviol glycosides.

A mammalian blood odor component serves as an approach-avoidance cue across phylum border - from flies to humans.

Chemosignals are used by predators to localize prey and by prey to avoid predators. These cues vary between species, but the odor of blood seems to be an exception and suggests the presence of an evolutionarily conserved chemosensory cue within the blood odor mixture. A blood odor component, E2D, has been shown to trigger approach responses identical to those triggered by the full blood odor in mammalian carnivores and as such, is a key candidate as a food/alarm cue in blood. Using a multidisciplinary approach, we demonstrate that E2D holds the dual function of affecting both approach and avoidance behavior in a predator-prey predicted manner. E2D evokes approach responses in two taxonomically distant blood-seeking predators, Stable fly and Wolf, while evoking avoidance responses in the prey species Mouse. We extend this by demonstrating that this chemical cue is preserved in humans as well; E2D induces postural avoidance, increases physiological arousal, and enhances visual perception of affective stimuli. This is the first demonstration of a single chemical cue with the dual function of guiding both approach and avoidance in a predator-prey predicted manner across taxonomically distant species, as well as the first known chemosignal that affects both human and non-human animals alike.

Behavioral responses to mammalian blood odor and a blood odor component in four species of large carnivores.

Only little is known about whether single volatile compounds are as efficient in eliciting behavioral responses in animals as the whole complex mixture of a behaviorally relevant odor. Recent studies analysing the composition of volatiles in mammalian blood, an important prey-associated odor stimulus for predators, found the odorant trans-4,5-epoxy-(E)-2-decenal to evoke a typical "metallic, blood-like" odor quality in humans. We therefore assessed the behavior of captive Asian wild dogs (Cuon alpinus), African wild dogs (Lycaon pictus), South American bush dogs (Speothos venaticus), and Siberian tigers (Panthera tigris altaica) when presented with wooden logs that were impregnated either with mammalian blood or with the blood odor component trans-4,5-epoxy-(E)-2-decenal, and compared it to their behavior towards a fruity odor (iso-pentyl acetate) and a near-odorless solvent (diethyl phthalate) as control. We found that all four species displayed significantly more interactions with the odorized wooden logs such as sniffing, licking, biting, pawing, and toying, when they were impregnated with the two prey-associated odors compared to the two non-prey-associated odors. Most importantly, no significant differences were found in the number of interactions with the wooden logs impregnated with mammalian blood and the blood odor component in any of the four species. Only one of the four species, the South American bush dogs, displayed a significant decrease in the number of interactions with the odorized logs across the five sessions performed per odor stimulus. Taken together, the results demonstrate that a single blood odor component can be as efficient in eliciting behavioral responses in large carnivores as the odor of real blood, suggesting that trans-4,5-epoxy-(E)-2-decenal may be perceived by predators as a "character impact compound" of mammalian blood odor. Further, the results suggest that odorized wooden logs are a suitable manner of environmental enrichment for captive carnivores.

Successful acquisition of an olfactory discrimination test by Asian elephants, Elephas maximus.

The present study demonstrates that Asian elephants, Elephas maximus, can successfully be trained to cooperate in an olfactory discrimination test based on a food-rewarded two-alternative instrumental conditioning procedure. The animals learned the basic principle of the test within only 60 trials and readily mastered intramodal stimulus transfer tasks. Further, they were capable of distinguishing between structurally related odor stimuli and remembered the reward value of previously learned odor stimuli after 2, 4, 8, and 16 weeks of recess without any signs of forgetting. The precision and consistency of the elephants' performance in tests of odor discrimination ability and long-term odor memory demonstrate the suitability of this method for assessing olfactory function in this proboscid species. An across-species comparison of several measures of olfactory learning capabilities such as speed of initial task acquisition and ability to master intramodal stimulus transfer tasks shows that Asian elephants are at least as good in their performance as mice, rats, and dogs, and clearly superior to nonhuman primates and fur seals. The results support the notion that Asian elephants may use olfactory cues for social communication and food selection and that the sense of smell may play an important role in the control of their behavior.

A new acoustic portal into the odontocete ear and vibrational analysis of the tympanoperiotic complex.

Global concern over the possible deleterious effects of noise on marine organisms was catalyzed when toothed whales stranded and died in the presence of high intensity sound. The lack of knowledge about mechanisms of hearing in toothed whales prompted our group to study the anatomy and build a finite element model to simulate sound reception in odontocetes. The primary auditory pathway in toothed whales is an evolutionary novelty, compensating for the impedance mismatch experienced by whale ancestors as they moved from hearing in air to hearing in water. The mechanism by which high-frequency vibrations pass from the low density fats of the lower jaw into the dense bones of the auditory apparatus is a key to understanding odontocete hearing. Here we identify a new acoustic portal into the ear complex, the tympanoperiotic complex (TPC) and a plausible mechanism by which sound is transduced into the bony components. We reveal the intact anatomic geometry using CT scanning, and test functional preconceptions using finite element modeling and vibrational analysis. We show that the mandibular fat bodies bifurcate posteriorly, attaching to the TPC in two distinct locations. The smaller branch is an inconspicuous, previously undescribed channel, a cone-shaped fat body that fits into a thin-walled bony funnel just anterior to the sigmoid process of the TPC. The TPC also contains regions of thin translucent bone that define zones of differential flexibility, enabling the TPC to bend in response to sound pressure, thus providing a mechanism for vibrations to pass through the ossicular chain. The techniques used to discover the new acoustic portal in toothed whales, provide a means to decipher auditory filtering, beam formation, impedance matching, and transduction. These tools can also be used to address concerns about the potential deleterious effects of high-intensity sound in a broad spectrum of marine organisms, from whales to fish.

Olfactory discrimination of aliphatic odorants in South African fur seals (Arctocephalus pusillus).

Using a food-rewarded, two-choice, instrumental conditioning paradigm we assessed the ability of South African fur seals, Arctocephalus pusillus, to discriminate between members of five chemical classes of aliphatic odorants presumed to differ in their abundance in the marine chemical environment. We found that the fur seals were able to distinguish between 24 of the 25 odor pairs presented and thus have a well-developed ability to discriminate between structurally related odorants, that aliphatic n-acetic esters were significantly more poorly discriminated by the fur seals than aliphatic n-aldehydes and n-carboxylic acids, and a lack of correlations between discrimination performance and structural similarity of odorants in terms of differences in carbon chain length. These results suggest that the sense of smell may play an important and hitherto underestimated role in regulating the behavior of fur seals. Further, they support the notion that regular connections between the perceived quality of odorants and their molecular structural properties are not a general phenomenon but appear to be odorant class- and species-specific. Our data support the hypothesis that a species' chemical environment may affect its olfactory capabilities.