Pointed-snout wrasse builds nest on Sarcotragus foetidus sponges

IF 4.3 2区 环境科学与生态学 Q1 ECOLOGY Ecology Pub Date : 2025-01-22 DOI:10.1002/ecy.4531
Francesca Strano, Francesco Tiralongo, Valerio Micaroni
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The Pointed-snout wrasse (<i>Symphodus rostratus</i>), a common Mediterranean species, exhibits complex nesting behaviors (Hanel et al., <span>2002</span>), which are essential for mate selection (Alonzo &amp; Heckman, <span>2010</span>).</p><p>During a rebreather training dive along the Apulian coast (Santa Caterina, Ionian Sea; 40°08′15.4″ N, 17°58′52.3″ E), the 20th of March 2024, at a depth between 12 and 17 m, we encountered large specimens (40 cm in diameter) of the sponge <i>Sarcotragus foetidus</i> with systematically arranged mounds of biogenic material, including shell, sea urchin test, and bryozoan fragments on their surface (Figure 1). In this context, we observed a mature male of the Pointed-snout wrasse actively transporting these fragments and placing them on one of these sponges (Video S1), engaging in nest-building behavior (Taborsky et al., <span>1987</span>). Throughout our dive, we documented nine instances of <i>S. rostratus</i> nests constructed on <i>S. foetidus</i>, each between 30 and 40 cm in diameter. In one case, we observed and filmed (GoPro HERO 8 Black) a female engaging in mating behavior with a reproductive male (Video S2). This observation is significant, as the use of calcareous biogenic materials and the selection of sponges as a nesting substrate in <i>S. rostratus</i> had never been reported until now. The Pointed-snout wrasse indeed, typically builds its nets using algae as the primary material, selecting areas rich in vegetation. This species is commonly observed constructing nests among algal beds, which provide both camouflage and structural support to eggs. The finding of several nests on different sponges within the same site suggests the possibility of observational learning or “copy-cat” behavior among reproductive male <i>S. rostratus</i>. Copying behavior have been documented in Ocellated wrasse (<i>Symphodus ocellatus</i>), where female mate choice copying can influence sexual selection (Alonzo, <span>2008</span>), and if confirmed, this would represent a novel example of observational learning in the nesting behaviors of <i>S. rostratus</i>.</p><p>Sponges play crucial ecological functions in marine ecosystems, often providing habitats for other organisms at various spatial scales (Bell et al., <span>2023</span>). Deep-sea glass sponge reefs are known to be refuge and nursery grounds for demersal fish (Barthel, <span>1997</span>; Maldonado et al., <span>2017</span>). For example, the Antarctic painted notie (<i>Nototheniops larseni</i>) has been reported to lay egg masses in the central cavity of the glass sponge <i>Rossella nuda</i> (Konecki &amp; Targett, <span>1989</span>). Other examples of fish using sponges as nesting sites include the Sea raven (<i>Hemitripterus americani</i>), which lays egg masses between the branches of the sponge <i>Chalina</i> sp. (Warfel &amp; Merriman, <span>1944</span>), and the Bigmouth sculpin (<i>Hemitripterus bolini</i>) using several sponge species as nests in the Gulf of Alaska and Bering Sea (Busby et al., <span>2012</span>). In addition, two fish species from the Japanese coasts, the Silver-spotted sculpin (<i>Blepsias cirrhosus</i>) and the Filefish (<i>Brachaluteres ulvarum</i>), also lay eggs within the sponge tissue and in the sponge suboscular cavity, respectively (Akagawa et al., <span>1995</span>; Munehara, <span>1991</span>). However, the use of sponges as direct nesting sites for wrasses is scarcely reported in the literature.</p><p>This unexpected nesting behavior raises several questions. Could the water circulation from the sponge's pumping activity enhance eggs ventilation? Sponges can pump substantial volumes of water daily, and this water movement could provide excellent ventilation for fish eggs during development. Does the typical central depression of <i>S. foetidus</i> (Pulido Mantas et al., <span>2024</span>) provide an advantageous structure for nest building? The distinctive central depression occurring in this sponge may help the fish retain biogenic fragments forming the nest and keep eggs in place, protecting them from wave action. Could this behavior be an adaptive response to environmental changes, such as alterations in algal availability or shifts in breeding season timing due to climate change or other environmental alterations? 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引用次数: 0

Abstract

Fishes belonging to the genus Symphodus, commonly called wrasses (Labridae family), exhibit diverse nesting behaviors among different species, ranging from elaborate to rudimentary nests, and in some cases no nests at all (Hanel et al., 2002; Warner & Lejeune, 1985). The nests, when built, are primarily constructed using algae of various species, which provide a secure environment for egg deposition and protection, playing a crucial role in the reproductive success of these species (Quignard & Pras, 1986). The Pointed-snout wrasse (Symphodus rostratus), a common Mediterranean species, exhibits complex nesting behaviors (Hanel et al., 2002), which are essential for mate selection (Alonzo & Heckman, 2010).

During a rebreather training dive along the Apulian coast (Santa Caterina, Ionian Sea; 40°08′15.4″ N, 17°58′52.3″ E), the 20th of March 2024, at a depth between 12 and 17 m, we encountered large specimens (40 cm in diameter) of the sponge Sarcotragus foetidus with systematically arranged mounds of biogenic material, including shell, sea urchin test, and bryozoan fragments on their surface (Figure 1). In this context, we observed a mature male of the Pointed-snout wrasse actively transporting these fragments and placing them on one of these sponges (Video S1), engaging in nest-building behavior (Taborsky et al., 1987). Throughout our dive, we documented nine instances of S. rostratus nests constructed on S. foetidus, each between 30 and 40 cm in diameter. In one case, we observed and filmed (GoPro HERO 8 Black) a female engaging in mating behavior with a reproductive male (Video S2). This observation is significant, as the use of calcareous biogenic materials and the selection of sponges as a nesting substrate in S. rostratus had never been reported until now. The Pointed-snout wrasse indeed, typically builds its nets using algae as the primary material, selecting areas rich in vegetation. This species is commonly observed constructing nests among algal beds, which provide both camouflage and structural support to eggs. The finding of several nests on different sponges within the same site suggests the possibility of observational learning or “copy-cat” behavior among reproductive male S. rostratus. Copying behavior have been documented in Ocellated wrasse (Symphodus ocellatus), where female mate choice copying can influence sexual selection (Alonzo, 2008), and if confirmed, this would represent a novel example of observational learning in the nesting behaviors of S. rostratus.

Sponges play crucial ecological functions in marine ecosystems, often providing habitats for other organisms at various spatial scales (Bell et al., 2023). Deep-sea glass sponge reefs are known to be refuge and nursery grounds for demersal fish (Barthel, 1997; Maldonado et al., 2017). For example, the Antarctic painted notie (Nototheniops larseni) has been reported to lay egg masses in the central cavity of the glass sponge Rossella nuda (Konecki & Targett, 1989). Other examples of fish using sponges as nesting sites include the Sea raven (Hemitripterus americani), which lays egg masses between the branches of the sponge Chalina sp. (Warfel & Merriman, 1944), and the Bigmouth sculpin (Hemitripterus bolini) using several sponge species as nests in the Gulf of Alaska and Bering Sea (Busby et al., 2012). In addition, two fish species from the Japanese coasts, the Silver-spotted sculpin (Blepsias cirrhosus) and the Filefish (Brachaluteres ulvarum), also lay eggs within the sponge tissue and in the sponge suboscular cavity, respectively (Akagawa et al., 1995; Munehara, 1991). However, the use of sponges as direct nesting sites for wrasses is scarcely reported in the literature.

This unexpected nesting behavior raises several questions. Could the water circulation from the sponge's pumping activity enhance eggs ventilation? Sponges can pump substantial volumes of water daily, and this water movement could provide excellent ventilation for fish eggs during development. Does the typical central depression of S. foetidus (Pulido Mantas et al., 2024) provide an advantageous structure for nest building? The distinctive central depression occurring in this sponge may help the fish retain biogenic fragments forming the nest and keep eggs in place, protecting them from wave action. Could this behavior be an adaptive response to environmental changes, such as alterations in algal availability or shifts in breeding season timing due to climate change or other environmental alterations? Climate change often causes mismatches in ecological interactions, so it is possible that this fish is using biogenic materials instead of algal fragments due to the absence of those algae, which could also be attributed to environmental changes.

Our observation corroborates the occurrence of complex behaviors in wrasses and indicates a potential new ecological interaction between sponges and fish reproduction in coastal environments. We only recognized the unusual behavior's importance months after documenting it, and this prevented our return to the site. Indeed, additional research is necessary to determine the frequency and distribution of this behavior, its potential benefits, and its implications for both S. rostratus reproduction and S. foetidus ecology. This observation presents opportunities for investigating the adaptability of fish breeding strategies and the diverse ecological functions of sponges in marine ecosystems.

The authors declare no conflicts of interest.

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尖嘴濑鱼在海绵上筑巢。
合鳃鱼属的鱼类,通常被称为濑鱼(唇鱼科),在不同的物种中表现出不同的筑巢行为,从精致的巢穴到简陋的巢穴,在某些情况下根本没有巢穴(Hanel等人,2002;华纳和勒,1985)。筑巢时主要使用各种藻类,为产卵提供安全的环境和保护,对这些物种的繁殖成功起着至关重要的作用(Quignard &amp;普拉斯,1986)。尖嘴濑(Symphodus rostratus)是一种常见的地中海物种,表现出复杂的筑巢行为(Hanel等人,2002),这对择偶至关重要(Alonzo &amp;赫克曼,2010)。在沿着阿普利亚海岸(爱奥尼亚海的圣卡特琳娜;(40°08′15.4″N, 17°58′52.3″E), 2024年3月20日,在12 - 17米的深度,我们发现了大的(直径40厘米)海绵胎儿肉头(Sarcotragus foetidus)标本,其表面有系统地堆积着生物物质,包括贝壳、海胆试验和苔藓虫碎片(图1)。在这种情况下,我们观察到一只成熟的雄性尖鼻鱼主动运输这些碎片,并将它们放在其中一块海绵上(视频S1)。参与筑巢行为(Taborsky et al., 1987)。在整个潜水过程中,我们记录了9个在卵螺上筑巢的竹螺,每个直径在30到40厘米之间。在一个案例中,我们观察并拍摄了(GoPro HERO 8 Black)一只雌性与一只正在繁殖的雄性进行交配行为(视频S2)。这一发现具有重要的意义,因为迄今为止还没有报道过利用钙质生物材料和选择海绵作为顶孔螺筑巢基质的情况。事实上,尖鼻濑鱼通常以藻类为主要材料,选择植被丰富的地区织网。该物种通常在藻床中筑巢,为卵提供伪装和结构支持。在同一地点的不同海绵上发现了几个巢穴,这表明雄性繁殖雌螺之间可能存在观察学习或“复制猫”行为。复制行为在Ocellated wrasse (Symphodus ocellatus)中有记录,雌性配偶选择复制可以影响性选择(Alonzo, 2008),如果得到证实,这将代表S. rostratus筑巢行为中观察学习的新例子。海绵在海洋生态系统中发挥着至关重要的生态功能,通常为不同空间尺度上的其他生物提供栖息地(Bell et al., 2023)。众所周知,深海玻璃海绵礁是底栖鱼类的避难所和繁殖地(Barthel, 1997;Maldonado等人,2017)。例如,据报道,南极彩绘笔记(Nototheniops larseni)在玻璃海绵Rossella nuda的中心腔中产卵。Targett, 1989)。其他鱼类使用海绵作为筑巢地点的例子包括海鸦(美洲半翅鸦),它们在海绵水母的分支之间产卵。Merriman, 1944),以及在阿拉斯加湾和白令海使用几种海绵作为巢穴的Bigmouth sculpin (Hemitripterus bolini) (Busby et al., 2012)。此外,来自日本海岸的两种鱼类,银斑鱼(Blepsias肝硬化)和细鳍鱼(Brachaluteres ulvarum)也分别在海绵组织和海绵骨下腔内产卵(Akagawa等人,1995;Munehara, 1991)。然而,使用海绵作为濑鱼的直接筑巢地点在文献中几乎没有报道。这种意想不到的嵌套行为引发了几个问题。海绵抽水活动产生的水循环能增强鸡蛋的通风吗?海绵每天可以泵出大量的水,这种水的运动可以为鱼卵在发育过程中提供良好的通风。S. foetidus典型的中央洼地(Pulido Mantas et al., 2024)是否为筑巢提供了有利的结构?这种海绵中独特的中央凹陷可能有助于鱼类保留形成巢穴的生物碎片,并将卵保存在适当的位置,保护它们免受波浪作用。这种行为是否可能是对环境变化的适应性反应,例如由于气候变化或其他环境变化而导致的藻类可用性的改变或繁殖季节时间的变化?气候变化经常导致生态相互作用的不匹配,因此由于缺乏藻类,这种鱼可能使用生物源材料而不是藻类碎片,这也可能归因于环境变化。我们的观察证实了濑鱼复杂行为的发生,并表明在沿海环境中海绵和鱼类繁殖之间可能存在新的生态相互作用。
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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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