Invited review: The evolution of cattle bioacoustics and application for advanced dairy systems

Vocalisations are commonly expressed by gregarious animals, including cattle, as a form of short- and long-distance communication. They can provide conspecifics with meaningful information about the physiology, affective state and physical attributes of the caller. In cattle, calls are individually distinct meaning they assist animals to identify specific individuals in the herd. Consequently, there is potential for these vocalisations to be acoustically analysed to make inferences about how individual animals or herds are coping with their external surroundings, and then act on these signals to improve feed conversion efficiency, reproductive efficiency and welfare. In the case of dairy farming, where herd sizes are expanding and farmers are becoming more reliant on technologies to assist in the monitoring of cattle, the study of vocal behaviour could provide an objective, cost effective and non-invasive alternative to traditional measures of welfare. The vocalisations of cattle in response to calf separation, social isolation and painful husbandry procedures, alongside changes to feeding and oestrous activity are here reviewed. For future application of sound technology, research is first necessary to analyse the acoustic structure of cattle vocalisations and determine the specific information they encode. This review draws together the latest research in field of cattle bioacoustics highlighting how the source–filter theory and affective state dimensional approach can be adopted to decode this information and improve on-farm management.     

The effectiveness of steers and heifers treated with oestrogen or testosterone to detect oestrus in cattle

Two experiments were carried out to determine the effectiveness of steers and heifers, treated with oestrogen or testosterone, in the detection of oestrus in cattle.In the first experiment 17 steers castrated at birth and 16 castrated at 6 months of age were randomly allocated to three groups and received an 800 mg subcutaneous implant of testosterone, subcutaneous injections of 10 mg oestradiol benzoate per week for 16 weeks or no hormone (controls). In addition, six heifers were injected subcutaneously with 10 mg oestradiol benzoate per week for 16 weeks while six untreated heifers served as controls. Animals were observed in a standardised libido test 2, 4, 8, 16, 20 and 24 weeks after treatment commenced. The time to first mount and the number of mounts per animal responding in the presence of oestrous heifers were recorded. Both steers and heifers treated with oestradiol benzoate were superior at detection of oestrus in cattle than animals treated with testosterone or those receiving no hormone. Oestrogen-treated animals generally detected heifers in oestrus in less than 3 min after introduction and mounted these animals between 20 and 30 times in one hour. This response was consistent throughout the duration of the experiment. There was no effect of age at castration of steers on development of male behaviour.The second experiment determined the rate and degree of development of male behaviour in steers in response to weekly subcutaneous injections of 0, 2, 4, 8 or 16 mg oestradiol benzoate per 250 kg body weight, 250 mg testosterone or 150 mg dihydrotestosterone for a period of 15 weeks. Steers treated with oestradiol benzoate again proved to be more successful than untreated or testosterone-treated steers at consistently detecting and mounting oestrous heifers. The best response was obtained from steers treated with 8 mg/250 kg body weight per week. The practical application of this work is discussed.     

BIOACOUSTIC PUBLICATIONS, 1989

ABSTRACT

Coruros Spalacopus cyanus, social fossorial rodents from Chile, use a complex acoustic repertoire with eleven different true vocalisations and one mechanical sound in various behavioural contexts. The complex of contact calls is particularly well differentiated. Juvenile coruros produced six true vocalisations of which four were structurally identical to adult calls. One vocalisation had components of two adult sounds and one occurred only in juvenile animals. Certain calls from the adult repertoire were lacking. The frequencies of sounds of juveniles were considerably higher than those of adults, with many sounds reaching the ultrasonic range. Nevertheless, pure ultrasonic sounds were not recorded.

The frequencies of the analysed sounds of coruros extended from 0.17 to 20.33 kHz with dominant frequency components between 0.17 and 10 kHz. The acoustic properties of calls are suitable for transmission above and below ground, thus providing further indirect evidence that coruros are not strictly confined to an underground way of life. Indeed, the great variability of frequency ranges, with lower frequencies always being included, reflects a specialisation for communication in variable acoustic environments.

The most distinctive and unique vocalisation of coruros is the long duration musical trilling (lasting up to two minutes), which is a long-distance call emitted in alarm and arousal contexts. Recordings of this call from natural burrows in the field in Chile showed similar structural features to vocalisations from captive colonies in the laboratory.

Our findings provide a further example of matching physical properties of vocalisations to the acoustic conditions of the habitat. However, vocalisations in subterranean rodents consist almost exclusively of short-distance calls, the trilling of coruros being the notable exception. Since the selective pressure of the acoustic environment upon the evolution of short-distance vocalisations is probably minimal, we suggest that during their evolution, subterranean mammals have matched their vocalisations primarily to their hearing range and not directly to the acoustics underground. Hearing probably has been the primary target of natural selection, serving not only for communication but also for detection of predators (and, in carnivores, of prey).     

Rookognise: Acoustic detection and identification of individual rooks in field recordings using multi-task neural networks

Individual-level monitoring is essential in many behavioural and bioacoustics studies. Collecting and annotating those data is costly in terms of human effort, but necessary prior to conducting analysis. In particular, many studies on bird vocalisations also involve manipulating the animals or human presence during observations, which may bias vocal production. Autonomous recording units can be used to collect large amounts of data without human supervision, largely removing those sources of bias. Deep learning can further facilitate the annotation of large amounts of data, for instance to detect vocalisations, identify the species, or recognise the vocalisation types in recordings. Acoustic individual identification, however, has so far largely remained limited to a single vocalisation type for a given species. This has limited the use of those techniques for automated data collection on raw recordings, where many individuals can produce vocalisations of varying complexity, potentially overlapping one another, with the additional presence of unknown and varying background noise. This paper aims at bridging this gap by developing a system to identify individual animals in those difficult conditions. Our system leverages a combination of multi-scale information integration, multi-channel audio and multi-task learning. The multi-task learning paradigm is based the overall task into four sub-tasks, three of which are auxiliary tasks: the detection and segmentation of vocalisations against other noises, the classification of individuals vocalising at any point during a sample, and the sexing of detected vocalisations. The fourth task is the overall identification of individuals. To test our approach, we recorded a captive group of rooks, a Eurasian social corvid with a diverse vocal repertoire. We used a multi-microphone array and collected a large scale dataset of time-stamped and identified vocalisations recorded, and found the system to work reliably for the defined tasks. To our knowledge, the system is the first to acoustically identify individuals regardless of the vocalisation produced. Our system can readily assist data collection and individual monitoring of groups of animals in both outdoor and indoor settings, even across long periods of time, and regardless of a species’ vocal complexity. All data and code used in this article is available online.     

The Acoustic Structure and Information Content of Female Koala Vocal Signals

Determining the information content of animal vocalisations can give valuable insights into the potential functions of vocal signals. The source-filter theory of vocal production allows researchers to examine the information content of mammal vocalisations by linking variation in acoustic features with variation in relevant physical characteristics of the caller. Here I used a source-filter theory approach to classify female koala vocalisations into different call-types, and determine which acoustic features have the potential to convey important information about the caller to other conspecifics. A two-step cluster analysis classified female calls into bellows, snarls and tonal rejection calls. Additional results revealed that female koala vocalisations differed in their potential to provide information about a given caller’s phenotype that may be of importance to receivers. Female snarls did not contain reliable acoustic cues to the caller’s identity and age. In contrast, female bellows and tonal rejection calls were individually distinctive, and the tonal rejection calls of older female koalas had consistently lower mean, minimum and maximum fundamental frequency. In addition, female bellows were significantly shorter in duration and had higher fundamental frequency, formant frequencies, and formant frequency spacing than male bellows. These results indicate that female koala vocalisations have the potential to signal the caller’s identity, age and sex. I go on to discuss the anatomical basis for these findings, and consider the possible functional relevance of signalling this type of information in the koala’s natural habitat.     

BIOACOUSTIC PUBLICATIONS, 1988

ABSTRACT

We examined vocalisations of a solitary subterranean rodent, the Silvery Mole-rat Heliophobius argenteocinereus (Bathyergidae). Seven true vocalisations and one mechanical vocalisation were identified. The main frequencies of the analysed sounds (0.34–13.17 kHz) match to a great extent the frequency range suitable for transmission in underground burrows. Due to the narrow frequency range of vocalisations, motivation is predominantly expressed by the rate of tonality rather than by frequency changes. The vocal repertoire of the Silvery Mole-rat perfectly matches to Morton's MS rules, i.e. that low-frequency and harsh vocalisations indicate hostility whereas high tonal calls signalise appeasement or fear. In comparison with social species, this solitary bathyergid produces fewer calls. It lacks contact and alarm calls, but has a rich repertoire of mating calls (mating ends with duet vocalization of male and female). Acoustic signals seem to play a major role in lowering natural aggressiveness during the mating period.     

Pattern and manipulation of follicular development in Bos indicus cattle

Bos indicus cattle are widespread in tropical regions due to their adaptation to these environments. Although data on reproductive performance have indicated both inferior and superior results for B. indicus cattle, there is little doubt that B. indicus cattle are superior than Bos taurus cattle when they are both kept in tropical or subtropical environments, where stressors like hot temperatures, humidity, ectoparasites and low quality forages are greater. Reproductive endocrinology and oestrus behaviour of the B. indicus cattle have been studied for over 30 years; however, the application of technologies such as real time ultrasonography and Heat-Watch systems has expanded our knowledge on the ovarian follicular-wave dynamics during the oestrous cycle and the time of ovulation. Ovarian follicular dynamics in B. indicus cattle is characterised by the occurrence of two, three or sometimes four waves of follicular development. While dominance is similar to that in B. taurus cattle, maximum diameters of the dominant follicle and CL are smaller than those reported in B. taurus and are probably due to a lower capacity for LH secretion than in B. taurus. Duration of oestrus is approximately 10 h and the interval from oestrus to ovulation is about 27 h. However, the variability in response to prostaglandin F2alpha (PGF) treatments and the difficulty for oestrus detection in B. indicus cattle have limited the widespread application of artificial insemination (AI) and emphasizes the need for treatments that control follicular development and ovulation. Follicular-wave development in B. indicus cattle can be controlled mechanically by ultrasound-guided follicle ablation, or hormonally by treatments with GnRH or oestradiol and progestogen/progesterone in combination. Treatments with GnRH plus PGF and a second GnRH (synchronization protocol known as Ovsynch) or oestradiol benzoate (known as GPE) have resulted in acceptable pregnancy rates after fixed-time AI (FTAI) in cycling cows, but results were lower in heifers and cows in postpartum anoestrus. Alternatively, treatments with oestradiol and progestogen/progesterone releasing devices resulted in synchronous emergence of a new follicular wave, and a second oestradiol or GnRH treatment after device removal resulted in synchronous ovulation and acceptable pregnancy rates to FTAI. Furthermore, oestradiol and progesterone treatments combined with eCG (given at the time of device removal) increased pregnancy rates in suckled B. indicus cows and may be useful for the treatment of cows in postpartum anoestrus. In summary, exogenous control of luteal and follicular development facilitates the application of assisted reproductive technologies in B. indicus cattle by offering the possibility of planning AI programs without the necessity of oestrus detection and without sacrificing the overall results.     

Regulation of estrous cycles in dairy cattle: A review

Artificial insemination has allowed rapid genetic progress in dairy cattle through the use of semen from genetically superior sires. Detection of estrus and proper timing of insemination remain as major problems limiting reproductive efficiency in dairy herds. Numerous programs for regulating estrous cycles have been examined in this review. While several programs appear promising, results remain variable and the need for accurate detection of estrus has not been eliminated. Nulliparous heifers seem to respond more consistently than lactating cows. Further research is required to develop a successful program that will consistently produce a precise synchrony of estrus and ovulation with normal fertility and be cost effective.     

NEWS

ABSTRACT

Australian fur seals Arctocephalus pusillus doriferus are colonial breeding animals forming dense social groups during the breeding season. During this time, males establish and defend territories through physical conflicts, stereotyped posturing and vocalisations. While vocalisations are suggested to play an important role in male recognition systems, it has received little attention. Recordings of nine adult male Australian fur seals were made during the 2000 and 2001 breeding seasons at Kanowna Island (39° 10′S, 146° 18′ E), Bass Strait, Australia. The in-air bark vocalisations of territory-holding males were used to characterise the Bark Call and to determine whether males produce individually distinct calls, which could be used as a basis for vocal recognition. Seventeen frequency and temporal variables were measured from a total of 162 barks from nine individual males. The Bark Series was more reliably classified (83%) to the correct caller compared to the Bark Unit. This was assigned with less certainty (68%), although the classification was still relatively high. Findings from this study indicate that there is sufficient stereotypy within individual calls, and sufficient variation between them, to enable vocal recognition in male Australian fur seals.     

Contact calling behaviour in the male ring‐tailed lemur (Lemur catta)

The ring‐tailed lemur (Lemur catta) is a group‐living strepsirhine primate endemic to Madagascar that has a complex vocal repertoire including affiliative moan and hmm calls. Past research has suggested that both vocalisations may be contact calls, and we assessed their usage in addition to examining the effect of individual differences and social factors on male calling behaviour. We tested three hypotheses: the group cohesion, preferred companion and individual differences hypotheses. From March to July 2010, 565 h of focal animal data were collected on 31 males aged ≥1 year at the Beza Mahafaly Special Reserve, Madagascar. Focal males were observed for 30 min, with vocalisations, allogrooming and agonistic interactions noted using one‐zero sampling, and general behaviour, nearest neighbour identity and distance noted using instantaneous point sampling, all at 2.5 min intervals. We found support for the group cohesion hypothesis for both vocalisations, and support for the preferred companion and individual differences hypotheses for the hmm but not the moan vocalisation. Moan and hmm calls maintained the distance between a male and his nearest neighbour, and were made at higher rates during behaviours which may lead to separation from conspecifics, such as travel and vigilance. Males made hmm calls at higher rates when they were low‐ranking, and/or when the nearest neighbour of a male or a preferred companion of either sex. Low‐ranking males may hmm call to maintain proximity to specific individuals within social groups who will show them increased tolerance, with the hmm signalling peaceful intent. Ring‐tailed lemurs are one of the best living models of gregarious primate ancestors, and gaining a better knowledge of the function and range of usage of their contact calls informs our understanding of the evolution of primate cognition.     

Comparison of females treated with oestradiol or testosterone to detect oestrus in dairy cattle maintained indoors year-round

The effectiveness of three females treated with oestradiol and three females treated with testosterone to detect oestrus was examined in 304 dairy cows maintained indoors year-round. Three heifers were treated weekly with 10 mg oestradiol benzoate per 250 kg of body weight. One cow and two heifers were treated with 10 injections of testosterone propionate (200 mg) every other day and an injection of testosterone enanthate (500 mg) every 10 days thereafter. During one year, there were 858 periods of oestrus detected by herdsmen observation - using standing, mounting, mucous discharge and any combinations thereof and, or, the hormone-treated females. Of these, the herdsmen detected 94% compared with 51% by the hormone-treated females. The 6% not detected by the herdsmen were detected by the treated females only. Oestradiol-treated females detected oestrus in cows as effectively as testosterone-treated females.     

An attempt to detect oestrus from changes in Fourier transform infrared spectra of milk from dairy heifers

This study was carried out to investigate if there were systematic changes in milk Fourier transform infrared (FT-IR) spectra relative to stage of the oestrous cycle in cattle. Oestrous cycles of 22 lactating heifers were synchronized with two injections of prostaglandin F2alpha (PGF) administered 11 days apart. The heifers were milked twice daily, and milk samples were collected from each heifer at each milking for a period of 70 days, starting on the day of the second PGF injection. Oestrus was diagnosed by visual detection in conjunction with monitoring rectal temperature. Milk samples were analyzed by FT-IR spectroscopy and the spectra data were analyzed using partial least squares (PLS) methods in relation to time of observed oestrus in heifers. In this investigation, it was not possible to identify reliable changes in milk FT-IR spectra in relation to oestrus on a single heifer basis, though there was a weak correlation between FT-IR spectra and expected time of oestrus when the analysis was carried out across all the heifers.     

What Makes Vocalisation Frequency an Unreliable Signal of Body Size in Birds? A Study on Black Swans

In many animal species, the frequency (pitch) of vocalisations correlates negatively with body size and may thus signal competitive ability. However, this relationship is absent in other species. Understanding why this difference exists across species may help to explain some of the diversity of vocal communication systems. We assessed whether vocalisation frequency signals body size in black swans (Cygnus atratus), and how this is affected by (i) variation in frequency within individuals and (ii) size variation across individuals. Frequency was correlated with body size and mass, with slopes close to the allometry expected if the birds were maximising sound radiation, but the explained variation in frequency was low. Within‐individual variation in vocalisation frequency was greater in male than female swans, and the reliability of frequency as a signal of size in males was correspondingly lower. A review of the literature on the relationship between the frequency of avian vocalisations and body size also showed smaller effect sizes for more variable vocalisations (birdsongs), than for simpler vocalisations. Vocalisation frequency was more reliably correlated with body size when the sexes were pooled (creating a larger range of variation in size) than when the relationship was examined for either sex separately, although male and female data followed the same allometric line. These results show that variation in frequency within individuals and low variation in size across individuals reduce the reliability of vocalisation frequency as a signal of body size, which helps to understand differences among species in the signal value of vocalisation frequency.     

Associations between the manipulation of patterns of follicular development and fertility in cattle

The wave-like patterns of ovarian follicular development in cattle can be manipulated by shortening the luteal phase with prostaglandin F2alpha (PGF), lengthening the period of follicle dominance with progesterone or curtailing follicle development with GnRH or oestradiol as 17beta, benzoate or cypionate. These hormones can also be used to synchronise ovulation allowing timed inseminations without detected oestrus. Progesterone, PGF, GnRH and oestradiol benzoate have each been used to increase conception rates in some situations, but their use has reduced them in others. For example, inseminations made within 96 h of a single injection of PGF administered during the luteal phase were associated with increased conception rates in dairy cows whereas double injection protocols reduced conception rates. The three forms of oestradiol and GnRH have greater effects on follicular development following divergence and dominance than following wave emergence. This can mean that follicles of differing maturity will be present about 7 days later and can result in varied intervals to the onset of oestrus following a PGF injection. The consequent variation in ovulation time can be reduced by injecting GnRH or an oestradiol during pro-oestrus. This means that some less mature follicles will ovulate, forming corpus luteum (CL) associated with a slower rise in plasma progesterone and lower mid-luteal concentrations. The lower conception rates recorded with single timed inseminations with synchronised ovulations have been associated with increased prevalences of short cycles in lactating dairy cows (with GnRH), with long luteal phases in cows and heifers (with oestradiol benzoate) and with embryo loss following positive pregnancy diagnosis (as with Ovsynch in lactating Holstein cows). Extensive Canadian studies have demonstrated that these same hormones can be successfully used without these limitations and reliably obtaining conception rates over 50% and up to 70% in beef cattle that have been supplemented with a progestin during the period of ovarian follicle synchronisation. The inherently lower fertility of Holstein cows during early lactation may be contributing to the reduced effectiveness of hormonal treatments for synchronised follicle development and ovulation. The role of reduced dose rates of GnRH in compromising this effectiveness needs to be determined if the potential of these treatments realised with beef cattle is to be achieved with lactating Holstein cows.     

Vocalisations of wild common marmosets are influenced by diurnal and ontogenetic factors

The vocalisations of wild common marmosets, Callithrix jacchus, were recorded to investigate whether call rate by individuals is affected by time of day, age, sex or dominance rank within a group. We also investigated how vocalisation pitch was affected by age, focussing on a single common call, the trill call. Adults vocalised more than juveniles or infants during the majority of daylight hours. Only the call rate of juveniles varied significantly over the day. No differences were found between either sex or dominance rank with respect to rate of vocalisations. The trill calls emitted by young wild common marmosets were of a higher pitch than those emitted by adults. We conclude that the auditory communication of wild common marmosets is related to the age of the animals, both in terms of call rate and the physical characteristics of their vocalisations.     

Zebra Finch Mates Use Their Forebrain Song System in Unlearned Call Communication

Unlearned calls are produced by all birds whereas learned songs are only found in three avian taxa, most notably in songbirds. The neural basis for song learning and production is formed by interconnected song nuclei: the song control system. In addition to song, zebra finches produce large numbers of soft, unlearned calls, among which “stack” calls are uttered frequently. To determine unequivocally the calls produced by each member of a group, we mounted miniature wireless microphones on each zebra finch. We find that group living paired males and females communicate using bilateral stack calling. To investigate the role of the song control system in call-based male female communication, we recorded the electrical activity in a premotor nucleus of the song control system in freely behaving male birds. The unique combination of acoustic monitoring together with wireless brain recording of individual zebra finches in groups shows that the neuronal activity of the song system correlates with the production of unlearned stack calls. The results suggest that the song system evolved from a brain circuit controlling simple unlearned calls to a system capable of producing acoustically rich, learned vocalizations.     

Seroprevalence of Neospora caninum antibodies in cattle and water buffaloes in India

Neospora caninum is now recognized as a major cause of abortion in cattle worldwide, but there is no report of N. caninum infection in cattle in India. Serum samples from 427 dairy cattle and 32 dairy water buffaloes from 7 organized dairy farms located in Punjab, India, were tested for N. caninum antibodies using a commercial monoclonal antibody-based competitive enzyme-linked immunosorbent assay (ELISA). Antibodies to N. caninum were found in 35 of 427 cattle from 6 of the 7 farms; 9.6% of cows, 5.1% of heifers, and 5.0% of calves were seropositive, suggesting postnatal transmission of N. caninum on the farm. Antibodies to N. caninum were found in 16 of 32 buffaloes tested from 2 dairy farms. In total, 64 cattle and 16 buffalo sera already tested by ELISA were also evaluated by an indirect fluorescent antibody test (IFAT) to verify ELISA results. Of the 64 cattle samples, 29 sera were negative by both tests and of the 35 ELISA-positive sera, 12 had IFAT titers of 1:100 or higher (1 had IFAT titer of 100, 2 had IFAT titer of 200, and 9 had IFAT titers of 400 or higher). Of the 16 buffalo sera positive by ELISA, 1 had an IFAT titer of 1:400. Thus, antibodies to N. caninum were demonstrated in cattle sera by 2 serologic methods. To our knowledge this is the first report of N. caninum infection in cattle and buffaloes in India.     

Control of oestrus in cattle using progesterone coils

Four experiments were conducted to determine the effect of length of treatment, stage of cycle at start of treatment and administration of oestradiol benzoate or progesterone at the start of treatment with intravaginal progesterone coils on oestrous response and fertility. In Experiment 1, the number of heifers in oestrus was affected neither by injection of 5 mg oestradiol benzoate alone or with 200 mg progesterone nor by length of treatment. More heifers (P < 0.05) were in oestrus on day 2 after treatment following a 12-day treatment compared to a 9-day treatment.In Experiment 2, heifers between days 17 and 20 of the oestrous cycle received an injection of either 5 mg oestradiol benzoate alone or with 200 mg progesterone at the start of a 9-day treatment with progesterone coils. Neither the number of heifers in oestrus nor the pattern of onset were affected after treatment. In Experiment 3, heifers between days 0 and 3 of the oestrus cycle received progesterone coils for 9, 12 or 14 days. In addition, animals received (i) no further treatment, (ii) a gelatin capsule adhered to the coil containing 10 mg oestradiol benzoate (iii) a gelatin capsule adhered to the coil containing 200 mg progesterone. Following a 9- or 12-day treatment period heifers receiving the coil with the oestrogen capsule had a high oestrous response ( compared to , P < 0.05). When oestrogen was not given, there was a significant linear effect of duration of treatment on the number in oestrus (9 days, ; 12 days ; 14 days, ; P < 0.05).In Experiment 4, post-partum cows were used to compare a 9- and 12-day treatment period and half the animals in each group received either 5 mg oestradiol benzoate and 200 mg progesterone at the start of treatment or a 10 mg gelatin capsule adhered to the coil. The length of treatment affected the number of heifers in oestrus since were in oestrus after a 12-day treatment period compared with after a 9-day period (P < 0.001). There were no significant differences in the number of cows in oestrus after injection of oestrogen and progesterone ( ) or after the use of the gelatin capsule ( ).     

Vaccination of cattle against Q-fever.

Formalin-killed phase I C. burneti organisms containing the protective antigenic component were used for vaccination of heifers against Q fever. None of the vaccinated heifers contracted Q fever, whereas 8 out of 12 (66.6%) control, non-vaccinated heifers became infected when exposed to infection for 3 months in the breed of naturally infected dairy cows. In the vaccinated cattle C. burneti was detected immediately post partum neither in the placenta nor in the colostrum. No shedding of C. burneti in milk has been found so far during 3 years of post-vaccinal observation period. For detecting Q fever antibodies in the blood of vaccinated as well as naturally infected animals MAR was found more sensitive than CFR.