Cannibalism in northern giant petrels (Macronectes halli) at Possession Island, Southern Indian Ocean

IF 4.3 2区 环境科学与生态学 Q1 ECOLOGY Ecology Pub Date : 2024-11-28 DOI:10.1002/ecy.4491
Alexandre Vong, Karine Delord, Nicolas Croizé, Célia Lesage, Lucía Llorente Zubiri, Florent Sabatier, Christophe Barbraud
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Originally regarded as a single species, Bourne and Warham (<span>1966</span>) described two different species on the basis of differences in both morphology (i.e., the color of the endplate of the bill) and behavior (i.e., the breeding timing): the Northern Giant Petrel with a dark red bill tip and a breeding season starting earlier (<i>Macronectes halli</i>, hereafter northern petrel) and the Southern Giant Petrel with a pale green bill tip (<i>Macronectes giganteus</i>, hereafter southern petrel). Despite these slight differences, both species show remarkable similarities such as their feeding behavior (González-Solís et al., <span>2000</span>). On land, giant petrels are mainly scavengers (Ridoux, <span>1994</span>) but are also fierce predators attacking various prey such as fur seal pups, penguin, and albatross chicks and even adults (Dilley et al., <span>2013</span>; Horswill et al., <span>2014</span>; Nagel et al., <span>2022</span>; Risi et al., <span>2021</span>; Ryan et al., <span>2008</span>). Such an opportunistic feeding repertoire, from scavenging to predation, seems particularly conducive to cannibalism, that is the act of killing and consuming a conspecific (Fouilloux et al., <span>2019</span>), which is an even more likely behavior for a colonial species that breeds in loose aggregations (Voisin, <span>1988</span>). Recently, Grohmann Finger et al. (<span>2021</span>) reported the first case of cannibalism in southern petrels with direct predation of chicks at the South Shetland Islands. It seems then highly probable that northern petrels demonstrate a similar cannibalistic behavior. However, no other observation can be found in the literature, and there is no record of this behavior for northern petrels.</p><p>Possession Island (46°25′ S, 51°45′ E, 146 km<sup>2</sup>) is a sub-Antarctic island located in the Crozet archipelago in the Southern Indian Ocean. Giant petrels form in loose colonies located all around the island and breed on relatively flat areas with tussock or against rocky ridges (Voisin, <span>1988</span>). Based on the last population census, there exist ~220 pairs of southern petrels and ~490 pairs of northern petrels on the island (Delord et al., <span>2008</span>; CEBC-CNRS, Project 109, IPEV, unpublished data). The valley of Petit Caporal (46°21.5′ S, 51°46.2′ E) hosts one of the smallest colonies in the north of the island, with less than 30 breeding pairs of northern petrels per year. The first instance of presumed cannibalism in northern petrels was observed during the annual long-term monitoring of the breeding pairs on 3 December 2021. We recorded the presence of two adult northern petrels around a freshly dead northern petrel chick not far from the colony of Petit Caporal; we photographed one of the adults, probably a male due to bill length and jizz (González-Solís, <span>2004</span>), approaching the carrion and feeding on it (Figure 1).</p><p>In addition to this observation, we recorded several cases of cannibalism during the monitoring of another northern petrel colony situated at Pointe Basse in the northwest of the island (46°21.6′ S, 51°42.5′ E). This is the largest colony of northern petrels on the island, composed of 15 loose breeding patches with only few southern petrels nesting sympatrically in some patches. As part of a long-term demographic study initiated in 2009, every nest of this colony is followed up each year to identify individuals and their breeding status, and all chicks are ringed just before fledging. Following a massive decline during the last 4 years in this colony with a breeding success currently below 10% (≈50% in the 2000s) (Delord et al., <span>2008</span>), nest monitoring with camera traps was set up by the <i>Terres australes et antarctiques françaises</i> for the 2023 breeding season to help understand the causes of the breeding failures. Sixteen camera traps were deployed for the whole breeding season (between August 2023 and March 2024) to monitor high-density patches at Pointe Basse. All devices were set up between 3 and 5 m from nests to avoid disturbance. Whenever a monitored nest failed, camera traps were moved to a new nest occupied by breeding birds to cover a maximum number of nests. Out of 46 nests monitored, 32 of them failed, either at the egg or the chick stage. Photo visualization showed not only a major pressure from Brown Skuas but also a significant impact of giant petrels. We observed five occurrences of predation of adult giant petrels on chicks: Camera traps recorded two northern petrel chicks predated by adult conspecifics (Figures 2 and 3), one northern petrel chick predated by an adult southern petrel, one southern petrel chick predated by an adult northern petrel, and one northern petrel chick predated by an unidentified giant petrel (see Appendix S1: Figures S1–S3). Predation events by giant petrels took place both at night and during the day (Appendix S1: Figure S3). Interestingly, the two cases of northern petrel cannibalism happened in different contexts, with one unguarded chick predated (Figure 2) and one direct depredation of a chick guarded by its parent (Figure 3).</p><p>There is no certainty as to the cause of death of the northern petrel chick in the valley of Petit Caporal. Death was recent given the state of the carrion (Figure 1e) and could have been caused by a cannibalistic adult giant petrel, skuas, or to another cause. On the other hand, our observations at the colony of Pointe Basse clearly showed direct predation events by conspecifics. Interestingly, the photographs taken by the camera traps revealed interspecific predation events between southern petrels and northern petrels. This suggests that cannibalism was not only a species-specific behavior but may have been linked to specific conditions driving the predatory behavior. Studies on other groups of seabirds suggest cannibalism to be more than just an opportunistic behavior, but instead a specialized behavior displayed under particular environmental conditions, usually associated with food shortages or high population density (Fouilloux et al., <span>2019</span>; Hayward et al., <span>2014</span>). We have no information here about what might have triggered these attacks, and we lack information about the identity of the cannibalistic birds and their breeding status; we only know from the monel rings visible on the pictures of the birds in Petit Caporal and the absence of rings on northern petrels in Pointe Basse that the cannibalistic birds at both sites were not the same individuals. For the two cannibalism events in Pointe Basse, the chick was either alone or guarded by a parent. Cannibalism here was thus motivated not only by easier predation conditions but also by a more aggressive and risky behavior adopted by some individuals. Cannibalism among giant petrels might be a behavior more common than expected or might be triggered by particular conditions. Both colonies studied here had an extremely low breeding success, and failed breeders can remain around their nests even several weeks after the loss of their egg or chick (A. Vong, personal observation). Individual experience during the breeding season might be a driver of cannibalism; one could hypothesize that failed breeders who remained attached to their nest or their colony are more likely to display a cannibalistic behavior toward the chicks around them. We could thus expect cannibalism to be dependent on such particular conditions, which might explain the lack of previous reports of cannibalism. Alternatively, the use of monitoring techniques such as camera traps may have facilitated the detection of this behavior that might be more common than expected.</p><p>Interestingly, there is no mention of giant petrel attacks on other surface-nesting Procellariiforms on La Possession Island, whereas such attacks on albatross chicks have recently been observed on other islands (Dilley et al., <span>2013</span>; Risi et al., <span>2021</span>). Given that Wandering Albatrosses can nest very close to some giant petrel colonies on La Possession Island, it would then be interesting to explore potential interspecific attacks by giant petrels. We showed here with multiple records that cannibalism is clearly part of the feeding behavior of northern petrels and partly explains the occurrence of breeding failures at Possession Island. Further research is needed to fully understand the role of cannibalism in the feeding repertoire of giant petrels and to identify the drivers underlying this behavior.</p><p>Alexandre Vong, Karine Delord, and Christophe Barbraud wrote the manuscript. Lucía Llorente Zubiri and Nicolas Croizé compiled camera trap photographs and edited the manuscript. Célia Lesage and Florent Sabatier edited the manuscript.</p><p>The authors declare no conflicts of interest.</p>","PeriodicalId":11484,"journal":{"name":"Ecology","volume":"106 1","pages":""},"PeriodicalIF":4.3000,"publicationDate":"2024-11-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11736339/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Ecology","FirstCategoryId":"93","ListUrlMain":"https://esajournals.onlinelibrary.wiley.com/doi/10.1002/ecy.4491","RegionNum":2,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"ECOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

In the Southern Ocean, giant petrels Macronectes sp. are alongside the Brown Skua (Stercorarius antarcticus lonnbergi) the major terrestrial scavengers and predators feeding on land on penguins and seal carrion, and at sea on dead cetaceans and other prey such as crustaceans and fishes (Ridoux, 1994). Originally regarded as a single species, Bourne and Warham (1966) described two different species on the basis of differences in both morphology (i.e., the color of the endplate of the bill) and behavior (i.e., the breeding timing): the Northern Giant Petrel with a dark red bill tip and a breeding season starting earlier (Macronectes halli, hereafter northern petrel) and the Southern Giant Petrel with a pale green bill tip (Macronectes giganteus, hereafter southern petrel). Despite these slight differences, both species show remarkable similarities such as their feeding behavior (González-Solís et al., 2000). On land, giant petrels are mainly scavengers (Ridoux, 1994) but are also fierce predators attacking various prey such as fur seal pups, penguin, and albatross chicks and even adults (Dilley et al., 2013; Horswill et al., 2014; Nagel et al., 2022; Risi et al., 2021; Ryan et al., 2008). Such an opportunistic feeding repertoire, from scavenging to predation, seems particularly conducive to cannibalism, that is the act of killing and consuming a conspecific (Fouilloux et al., 2019), which is an even more likely behavior for a colonial species that breeds in loose aggregations (Voisin, 1988). Recently, Grohmann Finger et al. (2021) reported the first case of cannibalism in southern petrels with direct predation of chicks at the South Shetland Islands. It seems then highly probable that northern petrels demonstrate a similar cannibalistic behavior. However, no other observation can be found in the literature, and there is no record of this behavior for northern petrels.

Possession Island (46°25′ S, 51°45′ E, 146 km2) is a sub-Antarctic island located in the Crozet archipelago in the Southern Indian Ocean. Giant petrels form in loose colonies located all around the island and breed on relatively flat areas with tussock or against rocky ridges (Voisin, 1988). Based on the last population census, there exist ~220 pairs of southern petrels and ~490 pairs of northern petrels on the island (Delord et al., 2008; CEBC-CNRS, Project 109, IPEV, unpublished data). The valley of Petit Caporal (46°21.5′ S, 51°46.2′ E) hosts one of the smallest colonies in the north of the island, with less than 30 breeding pairs of northern petrels per year. The first instance of presumed cannibalism in northern petrels was observed during the annual long-term monitoring of the breeding pairs on 3 December 2021. We recorded the presence of two adult northern petrels around a freshly dead northern petrel chick not far from the colony of Petit Caporal; we photographed one of the adults, probably a male due to bill length and jizz (González-Solís, 2004), approaching the carrion and feeding on it (Figure 1).

In addition to this observation, we recorded several cases of cannibalism during the monitoring of another northern petrel colony situated at Pointe Basse in the northwest of the island (46°21.6′ S, 51°42.5′ E). This is the largest colony of northern petrels on the island, composed of 15 loose breeding patches with only few southern petrels nesting sympatrically in some patches. As part of a long-term demographic study initiated in 2009, every nest of this colony is followed up each year to identify individuals and their breeding status, and all chicks are ringed just before fledging. Following a massive decline during the last 4 years in this colony with a breeding success currently below 10% (≈50% in the 2000s) (Delord et al., 2008), nest monitoring with camera traps was set up by the Terres australes et antarctiques françaises for the 2023 breeding season to help understand the causes of the breeding failures. Sixteen camera traps were deployed for the whole breeding season (between August 2023 and March 2024) to monitor high-density patches at Pointe Basse. All devices were set up between 3 and 5 m from nests to avoid disturbance. Whenever a monitored nest failed, camera traps were moved to a new nest occupied by breeding birds to cover a maximum number of nests. Out of 46 nests monitored, 32 of them failed, either at the egg or the chick stage. Photo visualization showed not only a major pressure from Brown Skuas but also a significant impact of giant petrels. We observed five occurrences of predation of adult giant petrels on chicks: Camera traps recorded two northern petrel chicks predated by adult conspecifics (Figures 2 and 3), one northern petrel chick predated by an adult southern petrel, one southern petrel chick predated by an adult northern petrel, and one northern petrel chick predated by an unidentified giant petrel (see Appendix S1: Figures S1–S3). Predation events by giant petrels took place both at night and during the day (Appendix S1: Figure S3). Interestingly, the two cases of northern petrel cannibalism happened in different contexts, with one unguarded chick predated (Figure 2) and one direct depredation of a chick guarded by its parent (Figure 3).

There is no certainty as to the cause of death of the northern petrel chick in the valley of Petit Caporal. Death was recent given the state of the carrion (Figure 1e) and could have been caused by a cannibalistic adult giant petrel, skuas, or to another cause. On the other hand, our observations at the colony of Pointe Basse clearly showed direct predation events by conspecifics. Interestingly, the photographs taken by the camera traps revealed interspecific predation events between southern petrels and northern petrels. This suggests that cannibalism was not only a species-specific behavior but may have been linked to specific conditions driving the predatory behavior. Studies on other groups of seabirds suggest cannibalism to be more than just an opportunistic behavior, but instead a specialized behavior displayed under particular environmental conditions, usually associated with food shortages or high population density (Fouilloux et al., 2019; Hayward et al., 2014). We have no information here about what might have triggered these attacks, and we lack information about the identity of the cannibalistic birds and their breeding status; we only know from the monel rings visible on the pictures of the birds in Petit Caporal and the absence of rings on northern petrels in Pointe Basse that the cannibalistic birds at both sites were not the same individuals. For the two cannibalism events in Pointe Basse, the chick was either alone or guarded by a parent. Cannibalism here was thus motivated not only by easier predation conditions but also by a more aggressive and risky behavior adopted by some individuals. Cannibalism among giant petrels might be a behavior more common than expected or might be triggered by particular conditions. Both colonies studied here had an extremely low breeding success, and failed breeders can remain around their nests even several weeks after the loss of their egg or chick (A. Vong, personal observation). Individual experience during the breeding season might be a driver of cannibalism; one could hypothesize that failed breeders who remained attached to their nest or their colony are more likely to display a cannibalistic behavior toward the chicks around them. We could thus expect cannibalism to be dependent on such particular conditions, which might explain the lack of previous reports of cannibalism. Alternatively, the use of monitoring techniques such as camera traps may have facilitated the detection of this behavior that might be more common than expected.

Interestingly, there is no mention of giant petrel attacks on other surface-nesting Procellariiforms on La Possession Island, whereas such attacks on albatross chicks have recently been observed on other islands (Dilley et al., 2013; Risi et al., 2021). Given that Wandering Albatrosses can nest very close to some giant petrel colonies on La Possession Island, it would then be interesting to explore potential interspecific attacks by giant petrels. We showed here with multiple records that cannibalism is clearly part of the feeding behavior of northern petrels and partly explains the occurrence of breeding failures at Possession Island. Further research is needed to fully understand the role of cannibalism in the feeding repertoire of giant petrels and to identify the drivers underlying this behavior.

Alexandre Vong, Karine Delord, and Christophe Barbraud wrote the manuscript. Lucía Llorente Zubiri and Nicolas Croizé compiled camera trap photographs and edited the manuscript. Célia Lesage and Florent Sabatier edited the manuscript.

The authors declare no conflicts of interest.

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南印度洋Possession岛北部巨海燕(Macronectes halli)自相残杀。
巨海燕的捕食活动在夜间和白天都有发生(附录S1:图S3)。有趣的是,这两起北方海燕同类相食的案例发生在不同的背景下,其中一只雏鸟没有受到保护(图2),另一只雏鸟直接被父母保护(图3)。小卡波尔山谷中北方海燕雏鸟的死亡原因尚不确定。死亡是最近给出的腐尸状态(图1e),可能是由食人的成年巨海燕、贼鸥或其他原因造成的。另一方面,我们在巴斯角的观察清楚地显示了同种虫的直接捕食事件。有趣的是,相机陷阱拍摄的照片揭示了南海燕和北海燕之间的种间捕食事件。这表明同类相食不仅是一种物种特有的行为,而且可能与驱动掠食行为的特定条件有关。对其他海鸟群体的研究表明,同类相食不仅仅是一种机会主义行为,而是在特定环境条件下表现出的一种特殊行为,通常与食物短缺或高种群密度有关(Fouilloux等人,2019;Hayward et al., 2014)。我们不知道是什么引发了这些袭击,我们也缺乏关于这种食人鸟的身份和它们的繁殖状况的信息;我们只从小卡波尔鸟类照片上可见的蒙乃尔环和巴斯角北部海鸟身上没有环的情况得知,这两个地点的同类鸟不是同一个人。在波恩特巴斯发生的两次同类相食事件中,小企鹅要么是独自一人,要么是由父母守护。因此,在这里,同类相食的动机不仅是更容易的捕食条件,而且是一些个体采取的更具攻击性和风险的行为。巨型海燕之间的同类相食行为可能比预期的更常见,也可能是由特定条件引发的。这里研究的两个群体都有极低的繁殖成功率,失败的繁殖者甚至在失去蛋或小鸡后几周仍能留在巢穴周围(A. Vong,个人观察)。繁殖季节的个体经历可能是同类相食的驱动因素;人们可以假设,那些仍然依附于巢穴或群体的失败繁殖者更有可能对周围的雏鸟表现出同类相食的行为。因此,我们可以预期同类相食依赖于这些特定的条件,这可能解释了之前缺乏同类相食的报道。另外,使用诸如相机陷阱之类的监测技术可能有助于发现这种可能比预期更常见的行为。有趣的是,没有提到大海燕袭击La Possession岛上其他表面筑巢的Procellariiforms,而最近在其他岛屿上观察到对信天翁雏鸟的袭击(Dilley et al., 2013;Risi et al., 2021)。考虑到流浪信天翁可以在La Possession岛上的一些巨型海燕群落附近筑巢,那么探索巨型海燕潜在的种间攻击将是很有趣的。我们在这里用多种记录表明,同类相食显然是北方海燕进食行为的一部分,这在一定程度上解释了藏岛繁殖失败的原因。需要进一步的研究来充分了解同类相食在巨海燕捕食中的作用,并确定这种行为背后的驱动因素。亚历山大·冯、卡琳·德洛德和克里斯托夫·巴布罗德撰写了手稿。Lucía Llorente Zubiri和Nicolas croiz<e:1>编辑了相机陷阱照片并编辑了手稿。castlia Lesage和Florent Sabatier编辑了手稿。作者声明无利益冲突。
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来源期刊
Ecology
Ecology 环境科学-生态学
CiteScore
8.30
自引率
2.10%
发文量
332
审稿时长
3 months
期刊介绍: Ecology publishes articles that report on the basic elements of ecological research. Emphasis is placed on concise, clear articles documenting important ecological phenomena. The journal publishes a broad array of research that includes a rapidly expanding envelope of subject matter, techniques, approaches, and concepts: paleoecology through present-day phenomena; evolutionary, population, physiological, community, and ecosystem ecology, as well as biogeochemistry; inclusive of descriptive, comparative, experimental, mathematical, statistical, and interdisciplinary approaches.
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