Qualitative aspects of grunts vary with pigs' mental states

Isabelle Veissier

doi:10.24072/pci.animsci.100190

Qualitative aspects of grunts vary with pigs' mental states

Isabelle Veissier based on reviews by Matteo Chincarini and 1 anonymous reviewer

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The use of pigs vocalisation structure to assess the quality of human-pig relationship

Avelyne S Villain, Carole Guérin, Céline Tallet (2023), bioRxiv, ver.5, peer-reviewed and recommended by PCI Animal Science https://doi.org/10.1101/2022.03.15.484457

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Abstract

ZH-CN

The use of pigs vocalisation structure to assess the quality of human-pig relationship

Studying human-animal interactions in domestic species and how they affect the establishment of a positive Human-Animal Relationship (HAR) may help us improve animal welfare and better understand the evolution of interspecific interactions associated with the domestication process. Understanding and describing the quality of an HAR requires information on several aspects of the animal biology and emotional states (social, spatial and postural behaviours, physiological and cognitive states). Growing evidence shows that acoustic features of animal vocalisations may be indicators of emotional states. Here, we tested the hypothesis that the quality of vocal expression may indicate the quality of HAR. At weaning, 30 piglets were positively handled by an experimenter who talked to and physically interacted with them three times a day, while 30 other piglets only received the contact necessary for proper husbandry. After two weeks, we recorded the behaviours and vocalisations produced in the presence of the static experimenter for five minutes. We repeated this test two weeks later, after a conditioning period during which human presence with additional positive contact was used as a reward for all piglets. We hypothesized this conditioning period would lead to a positive human-piglet relationship for all piglets. As expected, piglets that were positively handled at weaning expressed a higher attraction toward the experimenter, and, after the conditioning, piglets that were not positively handled at weaning expressed a similar level of attraction than the positively handled ones. Piglets positively handled at weaning generally produced shorter grunts than the other ones. However the latter expressed more flexibility in call structure when vocalising close to a human, with a decrease of grunt duration and an increase in pitch, frequency range and noisiness in their grunt. This differential effect of proximity between groups of piglets was attenuated after the conditioning during a standard reunion with a static human but remained over time when the human was providing additional positive contacts. Results suggest that first, changes in vocal structure are consistent with indicators of positive states in the presence of a human. Second, increasing familiarity and proximity between a human and a pig may induce changes in the acoustic structure of its grunts. Third, a human providing additional positive contacts triggers more changes in vocalisation structure than by their presence only. We show that vocalisation structure may allow us to assess the quality of human-pig relationship.

Positive handling, Acoustic communication, Emotions, Mood, Behaviour, Welfare, Interspecific interactions

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استخدام بنية نطق الخنازير لتقييم جودة العلاقة بين الإنسان والخنزير

قد تساعدنا دراسة التفاعلات بين الإنسان والحيوان في الأنواع المستأنسة وكيفية تأثيرها في إنشاء علاقة إيجابية بين الإنسان والحيوان (HAR) على تحسين رفاهية الحيوان وفهم تطور التفاعلات بين الأنواع المرتبطة بعملية التدجين بشكل أفضل. يتطلب فهم ووصف جودة المناطق الخطرة معلومات عن جوانب عديدة من بيولوجيا الحيوان والحالات العاطفية (السلوك الاجتماعي والمكاني والوضعي والحالات الفسيولوجية والمعرفية). تظهر الأدلة المتزايدة أن السمات الصوتية لأصوات الحيوانات قد تكون مؤشرات على الحالات العاطفية. هنا، قمنا باختبار الفرضية القائلة بأن جودة التعبير الصوتي قد تشير إلى جودة HAR. عند الفطام، تم التعامل مع 30 خنزيرًا صغيرًا بشكل إيجابي من قبل أحد المجربين الذين تحدثوا معهم وتفاعلوا جسديًا معهم ثلاث مرات يوميًا، بينما تلقى 30 خنزيرًا صغيرًا فقط الاتصال اللازم للتربية المناسبة. بعد أسبوعين، سجلنا السلوكيات والأصوات التي تم إنتاجها بحضور المجرب الثابت لمدة خمس دقائق. لقد كررنا هذا الاختبار بعد أسبوعين، بعد فترة تكييف تم خلالها استخدام الوجود البشري مع اتصال إيجابي إضافي كمكافأة لجميع الخنازير. لقد افترضنا أن فترة التكييف هذه ستؤدي إلى علاقة إيجابية بين الإنسان والخنزير الصغير لجميع الخنازير. كما هو متوقع، أعربت الخنازير التي تم التعامل معها بشكل إيجابي عند الفطام عن انجذاب أعلى تجاه المجرب، وبعد التكييف، أعربت الخنازير التي لم يتم التعامل معها بشكل إيجابي عند الفطام عن مستوى مماثل من الانجذاب لتلك التي تم التعامل معها بشكل إيجابي. الخنازير التي يتم التعامل معها بشكل إيجابي عند الفطام تنتج عمومًا همهمات أقصر من الخنازير الأخرى. ومع ذلك، أعرب الأخير عن مرونة أكبر في بنية النداء عند النطق بالقرب من الإنسان، مع انخفاض مدة النخر وزيادة في درجة الصوت ونطاق التردد والضوضاء في النخر. تم تخفيف هذا التأثير التفاضلي للقرب بين مجموعات الخنازير بعد التكييف أثناء لم الشمل القياسي مع إنسان ثابت ولكنه ظل بمرور الوقت عندما كان الإنسان يوفر اتصالات إيجابية إضافية. تشير النتائج إلى أن التغييرات في البنية الصوتية تتوافق أولاً مع مؤشرات الحالات الإيجابية في وجود الإنسان. ثانيًا، قد تؤدي زيادة الألفة والقرب بين الإنسان والخنزير إلى إحداث تغييرات في البنية الصوتية للهمهمات. ثالثًا، يؤدي توفير اتصالات إيجابية إضافية من قبل الإنسان إلى حدوث تغييرات في بنية النطق أكثر من وجودها فقط. لقد أظهرنا أن بنية النطق قد تسمح لنا بتقييم جودة العلاقة بين الإنسان والخنزير.

التعامل الإيجابي، التواصل الصوتي، العواطف، المزاج، السلوك، الرفاهية، التفاعلات بين الأنواع

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El uso de la estructura de vocalización de los cerdos para evaluar la calidad de la relación entre humanos y cerdos.

Estudiar las interacciones entre humanos y animales en especies domésticas y cómo afectan el establecimiento de una relación positiva entre humanos y animales (HAR) puede ayudarnos a mejorar el bienestar animal y comprender mejor la evolución de las interacciones interespecíficas asociadas con el proceso de domesticación. Comprender y describir la calidad de un HAR requiere información sobre varios aspectos de la biología animal y los estados emocionales (comportamientos sociales, espaciales y posturales, estados fisiológicos y cognitivos). Cada vez hay más pruebas que demuestran que las características acústicas de las vocalizaciones de los animales pueden ser indicadores de estados emocionales. Aquí, probamos la hipótesis de que la calidad de la expresión vocal puede indicar la calidad de HAR. En el destete, 30 lechones fueron tratados positivamente por un experimentador que habló con ellos e interactuó físicamente con ellos tres veces al día, mientras que otros 30 lechones solo recibieron el contacto necesario para una cría adecuada. Después de dos semanas, registramos los comportamientos y vocalizaciones producidas en presencia del experimentador estático durante cinco minutos. Repetimos esta prueba dos semanas después, después de un período de acondicionamiento durante el cual se utilizó la presencia humana con contacto positivo adicional como recompensa para todos los lechones. Presumimos que este período de acondicionamiento conduciría a una relación positiva entre humanos y lechones para todos los lechones. Como se esperaba, los lechones que fueron manipulados positivamente al destete expresaron una mayor atracción hacia el experimentador y, después del acondicionamiento, los lechones que no fueron manipulados positivamente al destete expresaron un nivel similar de atracción que los que fueron manipulados positivamente. Los lechones tratados positivamente al destete generalmente produjeron gruñidos más cortos que los demás. Sin embargo, estos últimos expresaron más flexibilidad en la estructura de las llamadas cuando vocalizaban cerca de un humano, con una disminución de la duración del gruñido y un aumento en el tono, el rango de frecuencia y el ruido en su gruñido. Este efecto diferencial de proximidad entre grupos de lechones se atenuó después del acondicionamiento durante una reunión estándar con un humano estático, pero permaneció con el tiempo cuando el humano proporcionaba contactos positivos adicionales. Los resultados sugieren que, en primer lugar, los cambios en la estructura vocal son consistentes con indicadores de estados positivos en presencia de un ser humano. En segundo lugar, la creciente familiaridad y proximidad entre un humano y un cerdo puede inducir cambios en la estructura acústica de sus gruñidos. En tercer lugar, un ser humano que proporciona contactos positivos adicionales desencadena más cambios en la estructura de la vocalización que su sola presencia. Mostramos que la estructura de la vocalización puede permitirnos evaluar la calidad de la relación entre humanos y cerdos.

Manejo positivo, Comunicación acústica, Emociones, Estado de ánimo, Comportamiento, Bienestar, Interacciones interespecíficas

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Utilisation de la structure de vocalisation du porc pour évaluer la qualité de la relation homme-porc

L'étude des interactions homme-animal chez les espèces domestiques et de la manière dont elles affectent l'établissement d'une relation homme-animal (HAR) positive peut nous aider à améliorer le bien-être animal et à mieux comprendre l'évolution des interactions interspécifiques associées au processus de domestication. Comprendre et décrire la qualité d'un HAR nécessite des informations sur plusieurs aspects de la biologie animale et des états émotionnels (comportements sociaux, spatiaux et posturaux, états physiologiques et cognitifs). De plus en plus de preuves montrent que les caractéristiques acoustiques des vocalisations animales peuvent être des indicateurs d'états émotionnels. Ici, nous avons testé l'hypothèse selon laquelle la qualité de l'expression vocale peut indiquer la qualité du HAR. Au sevrage, 30 porcelets ont été manipulés positivement par un expérimentateur qui leur a parlé et interagi physiquement avec eux trois fois par jour, tandis que 30 autres porcelets n'ont reçu que le contact nécessaire à un élevage approprié. Après deux semaines, nous avons enregistré les comportements et les vocalisations produits en présence de l'expérimentateur statique pendant cinq minutes. Nous avons répété ce test deux semaines plus tard, après une période de conditionnement pendant laquelle la présence humaine avec un contact positif supplémentaire a été utilisée comme récompense pour tous les porcelets. Nous avons émis l’hypothèse que cette période de conditionnement conduirait à une relation homme-porcelet positive pour tous les porcelets. Comme prévu, les porcelets qui ont été manipulés positivement au sevrage ont exprimé une plus grande attirance envers l'expérimentateur et, après le conditionnement, les porcelets qui n'ont pas été manipulés positivement au sevrage ont exprimé un niveau d'attraction similaire à celui des porcelets traités positivement. Les porcelets manipulés positivement au sevrage produisent généralement des grognements plus courts que les autres. Cependant, ces derniers ont exprimé plus de flexibilité dans la structure de leurs cris lorsqu'ils vocalisaient à proximité d'un humain, avec une diminution de la durée du grognement et une augmentation de la hauteur, de la gamme de fréquences et du bruit de leur grognement. Cet effet différentiel de proximité entre groupes de porcelets était atténué après le conditionnement lors d'une réunion standard avec un humain statique mais persistait au fil du temps lorsque l'humain assurait des contacts positifs supplémentaires. Les résultats suggèrent que premièrement, les changements dans la structure vocale sont cohérents avec les indicateurs d'états positifs en présence d'un humain. Deuxièmement, la familiarité et la proximité croissantes entre un humain et un porc peuvent induire des changements dans la structure acoustique de ses grognements. Troisièmement, un humain fournissant des contacts positifs supplémentaires déclenche plus de changements dans la structure de la vocalisation que par sa seule présence. Nous montrons que la structure de la vocalisation peut nous permettre d'évaluer la qualité de la relation homme-cochon.

Gestion positive, Communication acoustique, Émotions, Humeur, Comportement, Bien-être, Interactions interspécifiques

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मानव-सुअर संबंधों की गुणवत्ता का आकलन करने के लिए सूअरों की स्वर-संरचना संरचना का उपयोग

घरेलू प्रजातियों में मानव-पशु अंतःक्रियाओं का अध्ययन करना और वे सकारात्मक मानव-पशु संबंध (एचएआर) की स्थापना को कैसे प्रभावित करते हैं, इससे हमें पशु कल्याण में सुधार करने और पालतू बनाने की प्रक्रिया से जुड़े अंतर-विशिष्ट अंतःक्रियाओं के विकास को बेहतर ढंग से समझने में मदद मिल सकती है। एचएआर की गुणवत्ता को समझने और उसका वर्णन करने के लिए पशु जीव विज्ञान और भावनात्मक स्थितियों (सामाजिक, स्थानिक और मुद्रा संबंधी व्यवहार, शारीरिक और संज्ञानात्मक स्थिति) के कई पहलुओं पर जानकारी की आवश्यकता होती है। बढ़ते सबूतों से पता चलता है कि जानवरों की आवाज़ की ध्वनिक विशेषताएं भावनात्मक स्थिति का संकेतक हो सकती हैं। यहां, हमने इस परिकल्पना का परीक्षण किया कि मुखर अभिव्यक्ति की गुणवत्ता एचएआर की गुणवत्ता का संकेत दे सकती है। दूध छुड़ाने के समय, 30 पिगलेट को एक प्रयोगकर्ता द्वारा सकारात्मक रूप से संभाला गया, जिन्होंने दिन में तीन बार उनसे बात की और शारीरिक रूप से बातचीत की, जबकि 30 अन्य पिगलेट को केवल उचित पालन के लिए आवश्यक संपर्क प्राप्त हुआ। दो सप्ताह के बाद, हमने पांच मिनट तक स्थिर प्रयोगकर्ता की उपस्थिति में उत्पन्न व्यवहार और स्वरों को रिकॉर्ड किया। हमने कंडीशनिंग अवधि के बाद दो सप्ताह बाद इस परीक्षण को दोहराया, जिसके दौरान अतिरिक्त सकारात्मक संपर्क के साथ मानव उपस्थिति का उपयोग सभी पिगलेट के लिए पुरस्कार के रूप में किया गया था। हमने अनुमान लगाया कि यह कंडीशनिंग अवधि सभी पिगलेट के लिए एक सकारात्मक मानव-पिगलेट संबंध को जन्म देगी। जैसा कि अपेक्षित था, जिन सूअरों को दूध छुड़ाने के समय सकारात्मक रूप से संभाला गया था, उन्होंने प्रयोगकर्ता के प्रति अधिक आकर्षण व्यक्त किया, और, कंडीशनिंग के बाद, जिन सूअरों को दूध छुड़ाने के समय सकारात्मक ढंग से नहीं संभाला गया था, उन्होंने सकारात्मक ढंग से संभाले गए सूअरों की तुलना में समान स्तर का आकर्षण व्यक्त किया। दूध छुड़ाने के दौरान सकारात्मक रूप से संभाले गए पिगलेट आम तौर पर अन्य पिगलेट की तुलना में कम घुरघुराहट पैदा करते हैं। हालाँकि, बाद वाले ने कॉल संरचना में अधिक लचीलेपन को व्यक्त किया जब एक मानव के करीब आवाज उठाई, ग्रंट अवधि में कमी और पिच, आवृत्ति रेंज और उनके ग्रंट में शोर में वृद्धि के साथ। पिगलेट्स के समूहों के बीच निकटता का यह अंतर प्रभाव एक स्थिर मानव के साथ एक मानक पुनर्मिलन के दौरान कंडीशनिंग के बाद कम हो गया था, लेकिन समय के साथ बना रहा जब मानव अतिरिक्त सकारात्मक संपर्क प्रदान कर रहा था। परिणाम बताते हैं कि सबसे पहले, स्वर संरचना में परिवर्तन मानव की उपस्थिति में सकारात्मक स्थिति के संकेतकों के अनुरूप हैं। दूसरा, मनुष्य और सुअर के बीच बढ़ती परिचितता और निकटता उसके गुर्राने की ध्वनि संरचना में बदलाव ला सकती है। तीसरा, एक मानव जो अतिरिक्त सकारात्मक संपर्क प्रदान करता है, वह केवल उनकी उपस्थिति की तुलना में स्वर-संरचना में अधिक बदलाव लाता है। हम दिखाते हैं कि स्वर-संरचना संरचना हमें मानव-सुअर संबंधों की गुणवत्ता का आकलन करने की अनुमति दे सकती है।

सकारात्मक संचालन, ध्वनिक संचार, भावनाएँ, मनोदशा, व्यवहार, कल्याण, अंतर-विशिष्ट बातचीत

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人間と豚の関係の質を評価するための豚の発声構造の使用

家畜種における人間と動物の相互作用と、それが人間と動物の良好な関係 (HAR) の確立にどのような影響を与えるかを研究することは、動物福祉を改善し、家畜化のプロセスに関連する種間相互作用の進化をより深く理解するのに役立つ可能性があります。 HAR の品質を理解して説明するには、動物の生物学と感情状態 (社会的、空間的、姿勢的行動、生理学的および認知的状態) のいくつかの側面に関する情報が必要です。動物の鳴き声の音響的特徴が感情状態の指標である可能性があることを示す証拠が増えています。ここでは、音声表現の質が HAR の質を示す可能性があるという仮説を検証しました。離乳時、30 頭の子豚は実験者によって 1 日 3 回話しかけられたり物理的に触れられたりしましたが、他の 30 頭の子豚は適切な飼育に必要な接触のみを受けました。 2 週間後、静的実験者の存在下で生成された行動と発声を 5 分間記録しました。人間の存在と追加の陽性接触をすべての子豚への報酬として使用する条件付け期間の後、2 週間後にこのテストを繰り返しました。私たちは、この条件付け期間がすべての子豚にとって良好な人間と子豚の関係につながるだろうと仮説を立てました。予想通り、離乳時に積極的に扱われた子豚は、実験者に対してより高い魅力を示し、条件付け後、離乳時に積極的に扱われなかった子豚は、積極的に扱われた子豚と同様のレベルの魅力を示しました。離乳時に積極的に扱われた子豚は、一般的に他の子豚よりも短いうなり声を出しました。ただし、後者は、人間の近くで発声する場合、うなり声の持続時間が減少し、うなり声のピッチ、周波数範囲、およびノイズが増加することで、通話構造のより柔軟な表現を示しました。子ブタのグループ間の近接性によるこの差異効果は、静止している人間との標準的な再会の間の条件付け後に減衰しましたが、人間が追加の積極的な接触を提供した場合には時間が経っても残りました。結果は、第一に、声の構造の変化が人間の存在下でのポジティブな状態の指標と一致していることを示唆しています。第二に、人間と豚との親密度が増し、距離が近づくと、うなり声の音響構造に変化が生じる可能性があります。第三に、追加のポジティブな接触を提供する人間は、その存在だけによる場合よりも発声構造のより多くの変化を引き起こします。私たちは、発声構造によって人間と豚の関係の質を評価できる可能性があることを示します。

ポジティブハンドリング、音響コミュニケーション、感情、気分、行動、福祉、種間相互作用

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O uso da estrutura de vocalização dos porcos para avaliar a qualidade da relação humano-porco

Estudar as interações humano-animal em espécies domésticas e como elas afetam o estabelecimento de uma Relação Humano-Animal (HAR) positiva pode nos ajudar a melhorar o bem-estar animal e a compreender melhor a evolução das interações interespecíficas associadas ao processo de domesticação. Compreender e descrever a qualidade de um HAR requer informação sobre vários aspectos da biologia animal e dos estados emocionais (comportamentos sociais, espaciais e posturais, estados fisiológicos e cognitivos). Evidências crescentes mostram que as características acústicas das vocalizações dos animais podem ser indicadores de estados emocionais. Aqui testamos a hipótese de que a qualidade da expressão vocal pode indicar a qualidade do HAR. No desmame, 30 leitões foram tratados positivamente por um experimentador que conversou e interagiu fisicamente com eles três vezes ao dia, enquanto outros 30 leitões receberam apenas o contato necessário para um manejo adequado. Após duas semanas, registramos os comportamentos e vocalizações produzidos na presença do experimentador estático durante cinco minutos. Repetimos este teste duas semanas depois, após um período de condicionamento durante o qual a presença humana com contato positivo adicional foi usada como recompensa para todos os leitões. Nossa hipótese é que esse período de condicionamento levaria a uma relação positiva entre humanos e leitões para todos os leitões. Como esperado, os leitões que foram manuseados positivamente ao desmame expressaram uma maior atração pelo experimentador e, após o condicionamento, os leitões que não foram manuseados positivamente ao desmame expressaram um nível de atração semelhante ao dos leitões manuseados positivamente. Leitões manejados positivamente no desmame geralmente produziram grunhidos mais curtos que os demais. No entanto, estes últimos expressaram mais flexibilidade na estrutura do chamado ao vocalizar perto de um humano, com uma diminuição da duração do grunhido e um aumento no tom, na faixa de frequência e no ruído do seu grunhido. Este efeito diferencial de proximidade entre grupos de leitões foi atenuado após o condicionamento durante uma reunião padrão com um humano estático, mas permaneceu ao longo do tempo quando o humano forneceu contactos positivos adicionais. Os resultados sugerem que, primeiro, as mudanças na estrutura vocal são consistentes com indicadores de estados positivos na presença de um ser humano. Em segundo lugar, o aumento da familiaridade e da proximidade entre um humano e um porco pode induzir mudanças na estrutura acústica dos seus grunhidos. Terceiro, um ser humano que fornece contactos positivos adicionais desencadeia mais mudanças na estrutura da vocalização do que apenas pela sua presença. Mostramos que a estrutura de vocalização pode nos permitir avaliar a qualidade da relação humano-porco.

Manejo positivo, Comunicação acústica, Emoções, Humor, Comportamento, Bem-estar, Interações interespecíficas

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Изучение взаимодействия человека и животного у домашних видов и того, как оно влияет на установление позитивных отношений человека и животного (HAR), может помочь нам улучшить благополучие животных и лучше понять эволюцию межвидовых взаимодействий, связанных с процессом одомашнивания. Понимание и описание качества HAR требует информации о нескольких аспектах биологии и эмоционального состояния животных (социальное, пространственное и постуральное поведение, физиологические и когнитивные состояния). Все больше данных показывает, что акустические особенности вокализации животных могут быть индикаторами эмоционального состояния. Здесь мы проверили гипотезу о том, что качество голосовой экспрессии может указывать на качество HAR. При отъеме экспериментатор положительно обращался с 30 поросятами, который разговаривал с ними и физически взаимодействовал с ними три раза в день, в то время как 30 других поросят получали только контакт, необходимый для правильного содержания. Через две недели мы в течение пяти минут записывали поведение и вокализацию в присутствии статического экспериментатора. Мы повторили этот тест через две недели, после периода кондиционирования, в течение которого присутствие человека с дополнительным положительным контактом использовалось в качестве награды для всех поросят. Мы предположили, что этот период кондиционирования приведет к положительным отношениям человека и поросенка для всех поросят. Как и ожидалось, поросята, с которыми положительно обращались при отъеме, проявляли более высокое влечение к экспериментатору, а после кондиционирования поросята, с которыми не обращались положительно при отъеме, проявляли такой же уровень влечения, как и поросята, с которыми обращались положительно. Поросята, с которыми положительно обращались при отъеме, обычно издавали более короткое хрюканье, чем другие. Однако у последних наблюдалась большая гибкость в структуре криков при вокале вблизи человека, с уменьшением продолжительности хрюканья и увеличением высоты тона, частотного диапазона и шумности их хрюканья. Этот дифференциальный эффект близости между группами поросят был ослаблен после кондиционирования во время стандартного воссоединения со статическим человеком, но сохранялся со временем, когда человек обеспечивал дополнительные положительные контакты. Результаты позволяют предположить, что, во-первых, изменения в голосовой структуре согласуются с показателями позитивных состояний в присутствии человека. Во-вторых, увеличение знакомства и близости между человеком и свиньей может вызвать изменения в акустической структуре ее хрюканья. В-третьих, предоставление человеком дополнительных положительных контактов вызывает больше изменений в структуре вокализации, чем просто их присутствие. Мы показываем, что структура вокализации может позволить нам оценить качество отношений человека и свиньи.

62плата315cd5d4a9e9132ef5d25f40270 Использование структуры вокализации свиней для оценки качества взаимоотношений человека и свиньи. 72cdbe2367ff4ba6b16c5db22cac782b Позитивное обращение, Акустическая коммуникация, Эмоции, Настроение, Поведение, Благосостояние, Межвидовые взаимодействия Позитивное обращение, Акустическая коммуникация, Эмоции, Настроение, Поведение, Благосостояние, Межвидовые взаимодействия

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利用猪的发声结构评估人猪关系的质量

研究驯化物种中人与动物的相互作用以及它们如何影响积极的人与动物关系（HAR）的建立可能有助于我们改善动物福利并更好地了解与驯化过程相关的种间相互作用的演变。理解和描述 HAR 的质量需要有关动物生物学和情绪状态（社会、空间和姿势行为、生理和认知状态）多个方面的信息。越来越多的证据表明，动物发声的声学特征可能是情绪状态的指标。在这里，我们测试了声音表达的质量可能表明 HAR 质量的假设。断奶时，实验人员对 30 头仔猪进行了积极的照顾，每天与它们交谈和身体互动 3 次，而其他 30 头仔猪只接受了适当饲养所必需的接触。两周后，我们记录了静态实验者在场时产生的行为和发声五分钟。两周后，在经过一段调节期后，我们重复了这项测试，在此期间，人类的存在和额外的积极接触被用作对所有仔猪的奖励。我们假设这个调节期将为所有仔猪带来积极的人与仔猪关系。正如预期的那样，断奶时受到积极处理的仔猪对实验者表现出更高的吸引力，并且在条件反射后，断奶时未受到积极处理的仔猪表现出与积极处理的仔猪相似的吸引力水平。断奶时得到积极处理的仔猪通常比其他仔猪发出更短的咕噜声。然而，后者在接近人类发声时表现出更灵活的叫声结构，咕噜声持续时间减少，咕噜声的音高、频率范围和噪音增加。在与静态人类的标准团聚期间进行调节后，仔猪群体之间接近度的这种差异效应减弱，但当人类提供额外的积极接触时，随着时间的推移，这种效应仍然存在。结果表明，首先，声音结构的变化与人类在场时的积极状态指标一致。其次，人与猪之间的熟悉程度和接近程度的增加可能会导致其咕噜声的声学结构发生变化。第三，与仅仅存在相比，提供额外积极接触的人会引发更多的发声结构变化。我们证明发声结构可以让我们评估人与猪关系的质量。

积极处理、声音交流、情绪、情绪、行为、福利、种间互动

Submission: posted 23 March 2022
Recommendation: posted 24 March 2023, validated 24 March 2023

Cite this recommendation as:
Veissier, I. (2023) Qualitative aspects of grunts vary with pigs' mental states. Peer Community in Animal Science, 100190. 10.24072/pci.animsci.100190

Recommendation

Villain et al., (2023) investigated the structure of vocalisations in piglets in relation to human-animal-relationship. They first established a positive relationship by habituating piglets to be positively handled at weaning or later on after weaning. They then compared the reactions of piglets previously positively handled at weaning to that of non-handled piglets during tests in presence of a human (interacting or not), and also before and after the conditioning period when all piglets received positive contacts. They showed that the duration and frequency of grunts emitted in the presence of the human depends on previous contacts. More specifically, grunts are shorter and higher pitched in pigs that have been positively handled, in line with a positive human-animal relationship which is also observed through proximity of the piglets with the human. The authors concluded that the structure of pig vocalisation can reflect the quality of their relationship with humans.

The authors also showed that not only the response to humans is modified by positive contacts but also the general mood of piglets, with piglets positively handled at weaning emitting shorter grunts than non-handled piglets, whatever the context.

Another interesting finding is the temporality of behaviour of pigs habituated to positive contacts: during the first tests, they stay close to the human, probably being reassured by the proximity of the human. Then, when tests are repeated, they explore more the test room, using the human as an exploratory basis as already reported in the literature.

The hypotheses of the study are clear. The methods are reported in details so that the work is reproducible. The interpretation of results is sound. The manuscript is clearly written.

This paper brings new and original knowledge in the field of animals’ emotional responses and human-animal relationship: on the structure of grunts in relation to positive affects (positive emotion, positive mood) and on the temporality of the responses to human presence.

I recommend this manuscript for its originality and quality.

Isabelle Veissier

Villain, A.S., Guérin, C., Tallet, C., 2023. The use of pigs vocalisation structure to assess the quality of human-pig relationship. bioRxiv 2022.03.15.484457, ver. 5 peer-reviewed and recommended by Peer Community in Animal Science. https://doi.org/10.1101/2022.03.15.484457

Conflict of interest:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article. The authors declared that they comply with the PCI rule of having no financial conflicts of interest in relation to the content of the article.

Funding:
This project is part of the SoundWel project in the framework of the Anihwa Eranet and funded by ANR 30001199

Reviews

Evaluation round #5

DOI or URL of the preprint: https://doi.org/10.1101/2022.03.15.484457

Version of the preprint: 4

Author's Reply, 24 Mar 2023

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Dear journal,

Please find attached the v5 of our manuscript, after removing Camille Noûs as author.

Decision by Isabelle Veissier, posted 21 Mar 2023, validated 21 Mar 2023

Dear authors,

The recommender handling the evaluation of your manuscript has decided to recommend your paper. You will find enclosed a letter explaining her decision. However, the managing board expressed concerns about listing Camille Noûs as author of your article. The managing board does not agree about the inclusion of a fictive author in papers submitted to PCI Animal Science. We recognize our mistake in overlooking this issue at the moment of your submission and we apologize for our late decision on this matter.

The managing board requests to have the fictive author being removed as a condition for the manuscript being recommended by PCI Animal Science. If you agree, you should upload a new version in bioRxiv without the name of Camille Noûs.

Best regards

Rafael Muñoz-Tamayo for the managing board of PCI Animal Science

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Evaluation round #4

DOI or URL of the preprint: https://www.biorxiv.org/content/10.1101/2022.03.15.484457v3

Version of the preprint: 3

Author's Reply, 05 Mar 2023

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Please find attached the letter to the recommender and the tracked hanges version of the manuscript.

Decision by Isabelle Veissier, posted 02 Jan 2023, validated 05 Jan 2023

I thank you for following my recommendations, especially for reorganising the discussion. The discussion is much clearer now. It is still a bit tortuous and not fully convincing. You conclude both that the HAR is more positive in handled piglets and is increased with conditioning and that the short and high-pitched grunts are indicative of a positive emotion. So there should be more of these grunts at the end of conditioning, which does not seem to be the case. There must be a more elegant interpretation. If I summarise the results:

Behaviour: during the tests, the piglets positively handled stay closer to the human. The same is obtained in piglets not positively handled after they receive the conditioning, so that you can conclude that the same level of HAR is obtained after conditioning in all piglets. Also, the piglets positively handled explore more and are more mobile during the tests (both before and after the conditioning).

Grunts:

- During isolation phase: longer and lower pitch grunts

- Positively handled piglets have shorter and higher pitched grunts compared to non-positively handled ones, whatever the situation à more related to mood than to the specific context of the test

- Piglets emit shorter and higher pitched grunts when in proximity to humans, especially when the human is not familiar (e.g. the difference is more marked in non-handled piglets and – in all piglets- more marked before conditioning)

The behaviour of piglets should help you to interpret these variations in grunts:

- What difference in behaviour do you see in absence vs presence of the human? Such results are not reported. They could help you better relate grunts and behaviour

- The strong parallel I see between behaviour and grunts in your study is about exploration: Handled pigs both explore more the test pen and emit shorter and higher pitched grunts. These two seem to go together. It suggests that short and high-pitched grunts have something to do with exploration (and vice-versa). And probably the handled piglets feel more confident (thanks to a positive HAR) and explore more.

- The fact that short and high-pitched grunts are expressed preferably in proximity to human especially when it is not very familiar goes in the same direction: we can think that the human is more explored when not familiar

My feeling is that the short and high-pitched grunts are related to “positive” exploration (as opposed to “negative” exploration = looking for escape).

You may not agree with such an interpretation. I may have misunderstood your results (I got a bit lost I must admit). Also, like Reviewer 2, I am frustrated by the fact that your analyses are essentially on the quality of grunts and not their quantity. I would like you to consider the above reasoning and try to make your interpretations more convincing.

I also have minor comments on the writing. I include them on your manuscript (file attached).

All the best

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Evaluation round #3

DOI or URL of the preprint: https://www.biorxiv.org/content/10.1101/2022.03.15.484457v2

Version of the preprint: V2

Author's Reply, 16 Dec 2022

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Dear recommender, please find attached:
- the response letter to reviewer and recommender
- the revised version of the manuscript with tracked changes.

Decision by Isabelle Veissier, posted 15 Sep 2022

Dear authors,

I thank you for taking the comments from reviewers into account and for providing detailed explanations on how you handle them. There are still some comments that require further attention. See attached your response where I inserted my suggestions in red text in red to further improve the manuscript. There are still few points that I would like to double check with Rev 2. I invite you to first take my suggestions into account before I liaise with Rev 2.

I thank you in advance.

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Evaluation round #2

DOI or URL of the preprint: https://www.biorxiv.org/content/10.1101/2022.03.15.484457v2

Version of the preprint: V2

Author's Reply, 22 Jul 2022

Download tracked changes file

Please find attached a PDF with the letter to the reviewers followed by the track changes version of the manuscript.

Thank you for your patience.

Decision by Isabelle Veissier, posted 16 Jul 2022

Evaluation round #1

DOI or URL of the preprint: https://www.biorxiv.org/content/10.1101/2022.03.15.484457v1.full.pdf

Author's Reply, 16 Jul 2022

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Decision by Isabelle Veissier, posted 07 May 2022

This manuscript is of high interest. It however deserves amendments before we can recommend it. The two reviewers made detailed and complementary comments that should help the authors.

The writing needs to be improved to help the reading.The English needs also editing by a native english speaker.

Reviewed by Matteo Chincarini, 06 Apr 2022

Dear Editor,

The manuscript “The use of pigs vocalisation structure to assess the quality of human-pig relationship” is addressing an original work on interspecific acoustic communication and explores the non-invasive emotional indicators in swine. The study design is very accurate, and the discussion of the results gives an exhaustive overview of the topic. A couple of concerns could be related to my misunderstanding. The first one regards the pen size where the experiment has been conducted and the second one is on the assumption test for PCA (please, see below). The experiment is well described and even if, working with farm animals and acoustic analysis is very challenging, the authors have worked very hard to set up elegant research. Furthermore, there is growing interest in vocal communication related to animal welfare as well as human-animal relationships. Finally, these results provide potential non-invasive indicators relevant to animal welfare. The manuscript needs also some minor revisions relative to the figures.

Below are some specific comments to the authors for minor revisions:

Title

The title clearly reflects the content of the article.

Abstract

The abstract is concise and presents the main findings of the study. I’ve only one concern regarding the first sentence: “In domestic species, studying human-animal interactions and their consequences on the establishment of a positive Human-Animal Relationship (HAR) would have applications for both improving animal welfare.” I’m not a native English speaker but here maybe it is possible to rephrase. I understand that authors are referring to animals and humans when they use the term “both” but now it seems it is referring to “interactions” and “consequences”.

Introduction

Hypotheses have been explicit very clearly and they are supported by several papers representing the state of the art in this field.

LL 46-47: please consider merging these two very short sentences.

Materials and methods

This section is, in general, well explained and detailed.

Ethical note

L 103: please, consider citing the French and European legislation (this will be relevant for the pen size, see below)

Subject and housing conditions

L 112: please, verify the pen size according to your authorisation. According to the EU Directive 63/2010, the minimum enclosure size should be 2,0 m2 (Table 7.3). This could be not your case but it needs to be justified (it can be smaller due to experimental grounds).

Conditioning

L 137: you say that conditioning took place between day 42 and 62 after weaning, so it would be between 70 and 90 days of life? At L 107 it is reported that piglets involved in the study were from 28 to 62 days of life, please double check it.

L 145: I’m not sure what “Hens” means here

Behavioural monitoring and analysis

Please, specify if the behaviour has been analysed either by the same or different persons.

Acoustic monitoring and analysis

L 178: Even if Praat is well-known software in this field, I think it would be better to cite it using a reference. Especially to be clear about the version that has been used (please, you can give a look here: https://www.fon.hum.uva.nl/praat/manual/FAQ__How_to_cite_Praat.html)

Statistical analysis

I am not a statistician. However, when applying PCA I think it is worth reporting the value of Kaiser-Meyer Olkin (KMO) and Bartlett’s test of sphericity as preliminary tests (or explain why not). Maybe, you could also consider using the Measure of Sampling Adequacy (MSA) if some variable needs to be excluded.

From Table 4, I’m understanding that you transformed some variables (like using log or sqrt). Please, consider adding this information also in the text when you write about symmetrical distribution L 206.

L 207: “pca”, did you mean function “dudi.pca”?

L 254: inside the code, I think ID/time/Phase should be ID/Time/Phase

Results

General: most of the script has been reported, could you add also the PCA analysis?

L 344: figure 3 is not present in the manuscript

L 369: figure 4, I’m not sure that is referring to the actual figure

Tables and figures

Please, see above

Discussion

The discussion is exhaustive and well supported by the literature. Still, the conclusions are not overstated.

L 475: there are two “first”

References

Fine.

Reviewed by anonymous reviewer 1, 04 May 2022

Review of “The use of pigs vocalisation structure to assess the quality of human-pig relationship” by Vilain et al.

This is an interesting study aiming to investigate if (changes in) pig vocalisation reflects the quality of human-animal relationships. I have, however, some major concerns and a few other issues, which I have summarised below.

Major concerns:

The study sets out to analyse pig vocalisation in different situations, comparing changes in sound structure both within and between pigs when treated differently over time. However, the data are immediately reduced to only grunts (line 178) because they were the most frequent. Is frequency important for all calls? One scream may say more than a thousand grunts, to paraphrase Ibsen. I would like to see a couple of phrases explaining this a bit more, as this is an important aspect of your data editing. You also focus on vocal quality, but what about vocal quantity? You mention vocal activity in line97, but refer to some qualitative aspects there, too.

I am missing which specific hypotheses you are testing? Or rather, in the Discussion, you dismiss one of the hypotheses, and then appear to suggest two new ones (lines 539-544).

Was the vocalisation when conspecifics were social partners (line 141) used at all? I may have missed where that is presented. And if not, why was this included? And if used, how did you separate the vocalisation of the different pigs?

The analyses are complex and can be difficult to follow in places. Is a p-value threshold of 0.05 too large for 3-way interactions? Some (many?) of your 3-way interactions have a p-value of 0.03 (even 0.07, which you still keep?), and I am left questioning how relevant they are. It leads to results like “grunts produced closer to the human were shorter… but only in untamed piglets, effect being stronger before the conditioning” and “grunts had a higher frequency range … when produced closer to the human…, but only in untamed piglets and before the conditioning”. On a data set of this size, I wonder to what extent these results can be generalised. It makes the manuscript very long and very difficult to follow in places – and the main results drown. Is there enough power to make such detailed conclusions?

Line 445-449: Is this what you expected? Could your interpretation be affected by the nature of the treatment, in other words, you will describe the response of the H+ pigs as positive (either being touch/attention satiated, or know they can always come back, and therefore disinterested, or confident enough to go exploring). How can this be disproven if you haven’t set out expected outcomes from the start?

The last major concern is the text. The manuscript has a large number of typos (e.g. lines 405, 440, 463, 552 and elsewhere) and missing spaces, which leaves the impression that the uploading was rushed. I am usually quite forgiving when the English is a little bit rustic when the authors are writing in a second language. Unfortunately, there are places where it makes it difficult to understand what is meant (e.g. line 38: “a carrying human”; line 112: “on plastic duckboard and panels visually isolated pens”; line 568: “’AH’ was more entitled to trigger higher positive states”), and as a reviewer, it can be jarring to have to second-guess the content. I would therefore recommend that the revised manuscript is copy-edited by third party before re-submission.

Other issues:

The use of the word ‘taming’ is confusing, as domestic pigs (Sus scrofa domesticus) are all tame compared to the wild boar (Sus scrofa). I suggest to change this to ‘positive handling’.

The authors refer to their study animals as piglets, but they are weaned and thus should be called pigs.

Line 19: objectify the quality?

Line 20: Is not all behaviour spatial?

Line 25: replace breeding with husbandry

Line 50: Animal welfare conveys? Consists of?

Line 69 and elsewhere: associated with, not to

Line 88: What is ‘formant’?

Line 113: metal chain?

Line 145 and elsewhere: Hence

Figure 1. Suggest using ‘area’ for the distal and proximal areas, to not confuse it with the 16 zones. It is not clear where the distal area is (above or below the dashed line).

Line 161: Where the sessions recorded or was the annotation done live?

Line 170: Replace over with other

Table 1: “The number of times the piglet looked at other parts of the room” - as the pig will be looking somewhere at all times, this will always be within 1 of the previous variable (Nb looks toward human).

Table 2: The Table does not show “Behavioural response score for the reunion phase of the Isolation/Reunion test.” but “Percentage of explained variance and variable loadings of the principal component analysis for the first three PCs.”

Table 2 and elsewhere: You use the word ‘parameter’ when ‘variable’ is the correct term.

Table 4: Are these variables on vocalisation characteristics essentially showing the same, leading to a high loading for all of them on PC1, i.e. so highly correlated that they are not all needed?

Line 260: Vocal response variable

Lines 323 and 326: Why are these estimates?

Figure 4: It is not possible to know what comparisons the letters refer to, as some of them have no letter. What is different from what? Question if a three-way interaction on a subset of data is biological relevant? The blue and grey colours are indistinguishable.

Figure 5: What does H:N mean in the legend of A? Figure D is missing (referred to in Table heading). Not sure what C means - failed used in figure heading, missed used in y-axis label, but what does this show?

Line 369: Here you refer to the wrong Figure. This was carried over for the rest of the manuscript, so that wrong Figures were indicated.

Figure 6: Are these slopes based on linear regressions? is this justified?

Table 5: Does this not indicate either that vocal parameters are not very robust measures, or that you were unable to standardise your treatment?

Line 443: attraction instead of attractiveness

Line 467-468: This is using your interpretation of the positively handled pigs to draw conclusions on the limitations on the control group. The set-up did allow them to explore.

Line 514: Double reference

Line 568: More likely to? But does this not show that this test or variable is not generalisable?

Line 577: The major difference to the pigs is more likely to be in the difference in smells of the two handlers. Was there any thought given to soaps and perfume? Even body odours differ.

Lines 586-588: But some variables were not significant for one of the handlers.

Line 600: “We suggest that the use of vocalisations to assess quality of human-pig relationship could help to better monitor the parameters involved…” I don’t know what this means?