The threat of Peters's Rock Agama (Agama picticauda) to reptile diversity across the Lesser Antilles

IF 2.8 2区 环境科学与生态学 Q1 BIODIVERSITY CONSERVATION
M. P. van den Burg, J. A. Wasilewski, R. S. Thorpe, A. O. Debrot, J. C. Daltry, B. Angin, E. M. Boman, L. Brannon, E. A. Corbett, J. A. Horrocks, F. Mukhida, N. Paranthoën, N. K. Pascoe, C. Petrovic, A. Verhoeven, M. Yokoyama
{"title":"The threat of Peters's Rock Agama (Agama picticauda) to reptile diversity across the Lesser Antilles","authors":"M. P. van den Burg,&nbsp;J. A. Wasilewski,&nbsp;R. S. Thorpe,&nbsp;A. O. Debrot,&nbsp;J. C. Daltry,&nbsp;B. Angin,&nbsp;E. M. Boman,&nbsp;L. Brannon,&nbsp;E. A. Corbett,&nbsp;J. A. Horrocks,&nbsp;F. Mukhida,&nbsp;N. Paranthoën,&nbsp;N. K. Pascoe,&nbsp;C. Petrovic,&nbsp;A. Verhoeven,&nbsp;M. Yokoyama","doi":"10.1111/acv.12889","DOIUrl":null,"url":null,"abstract":"<p>During the ongoing sixth global extinction wave, island ecosystems are among the most impacted due to a high introduction rate of non-native species (Tershy <i>et al</i>., <span>2015</span>; Bellard, Cassey, &amp; Blackburn, <span>2016</span>; Fernández-Palacios <i>et al</i>., <span>2021</span>). Within one of the global biodiversity hotspots (Myers <i>et al</i>., <span>2000</span>), the Caribbean Lesser Antilles are known for their high degree of endemism across numerous taxa, including reptiles (e.g., Smith <i>et al</i>., <span>2004</span>; Losos <i>et al</i>., <span>2006</span>). However, continuing introductions of non-native species are homogenizing the regional herpetofauna diversity (Capinha, Marcolin, &amp; Reino, <span>2020</span>), leading to extinctions and loss of functional trait diversity across islands and ecosystems (Kemp, <span>2023</span>).</p><p>The most common terrestrial non-native vertebrates, throughout the Lesser Antilles, are reptiles (Thorpe, <span>2022</span>). Their interactions with native reptile species have led to local extinctions and continuing declines in both native population sizes and distribution ranges through predation, hybridization, disease transmission, and competition for resources (Daltry, <span>2022</span>). Multiple non-native species have already spread nearly regionwide, including <i>Gymnophthalmus underwoodi</i>, <i>Hemidactylus mabouia</i>, <i>Indotyphlops braminus</i>, <i>Anolis</i>/<i>Norops sagrei</i>, and Latin American <i>Iguana iguana</i> (Thorpe, <span>2022</span>; Thibaudier <i>et al</i>., <span>2023</span>; van den Burg <i>et al</i>., <span>2023</span>), while others are spreading rapidly (e.g., <i>Hemidactylus frenatus</i>: Thibaudier <i>et al</i>., <span>2023</span> and references therein). Importantly, several of these non-native species are known to have been introduced to the Lesser Antilles from non-native populations in Florida (Powell <i>et al</i>., <span>2011</span>); a pattern we fear is likely to be repeated by Peters's Rock Agama (<i>Agama picticauda</i>), although no established population has yet been reported in the Lesser Antilles.</p><p><i>Agama picticauda</i> is a medium-sized lizard native to sub-Saharan western and central Africa, with both sexual dichromatism and size dimorphism. Adult males have a bright orange head and tail, while females are light brown and can have yellow to orange dorsolateral patches (Fig. 1). The species is diurnally active, has a maximum recorded snout–vent length of 15.7 cm (Krishnan <i>et al</i>., <span>2019</span>), and can produce up to three clutches annually, each of 5–12 eggs (Blunden &amp; Krysko, <span>2007</span>; Krysko, Enge, &amp; Moler, <span>2019</span>). It occupies both horizontal and vertical surfaces from where it uses a sit-and-stalk approach to identify and pursue arthropods (Enge, Krysko, &amp; Talley, <span>2004</span>) and small vertebrates (Henigan <i>et al</i>., <span>2019</span>).</p><p>In Florida, the first <i>A. picticauda</i> population was found in 1976 (Wilson &amp; Porras, <span>1983</span>) and it has since extended its range across the state (Enge, Krysko, &amp; Talley, <span>2004</span>). Recent analyses show high genetic variation within the Florida population due to introductions from different native origins (Nuñez, Krysko, &amp; Avery, <span>2016</span>). Given populations across its native range occupy different climatic niches (Krishnan <i>et al</i>., <span>2019</span>), hybridization between populations of differing origins could result in high ecological adaptability (Consuegra <i>et al</i>., <span>2011</span>), that in turn can increase establishment success when Florida individuals are translocated to other regions. Alarmingly, <i>A. picticauda</i> appears to be spreading to Caribbean islands as sightings are being reported from the Bahamas and Tortola (British Virgin Islands) (observations 139983395 and 89972864, https://www.inaturalist.org/). On Tortola, at least two adults as well as three juveniles have been observed, suggestive of an establishing population (C. Petrovic, pers. obs.). Further research on the status and impacts on the Bahamas is urgently needed, while on Tortola immediate action is necessary to remove the existing population.</p><p>Although the native and non-native dietary range and ecology of <i>A. picticauda</i> are poorly studied, when it spreads to the Lesser Antilles, this could have a major impact on numerous native species. There is clear evidence this species preys on smaller lizards. For example, Henigan <i>et al</i>. (<span>2019</span>) dissected a large female that had cannibalized a smaller individual (5 cm snout–vent length) and Florida residents have observed predation of <i>Anolis</i> species (e.g., iNaturalist record 19472282), and a predation attempt on an <i>Ameiva ameiva</i> (J. Wasilewski pers. obs.). These data are highly troubling given many taxa have life stages within these size ranges, while others (or at least one sex) never grow larger. Species of <i>Alinea</i>, <i>Anolis</i>, <i>Bachia</i>, <i>Capitellum</i>, <i>Copeoglossum</i>, <i>Gymnophthalmus</i>, <i>Mabuya</i>, <i>Marisora</i> and <i>Spondylurus</i> would be susceptible to predation, as well as juveniles of <i>Ameiva</i>, <i>Cnemidophorus</i>, <i>Kentropyx</i> and <i>Pholidoscelis</i>: an assemblage of &gt;45 species (Thorpe, <span>2022</span>). Furthermore, native adult lizards are likely to experience interspecific competition and potential displacement. Although <i>Agama picticauda</i> is mainly reported from urban and suburban environments, suggesting a low impact within intact forests, given the high threat to the Caribbean forests and their transition to (sub)urban areas, it is expected that <i>A. picticauda</i> could become widely distributed. Besides, not all native Lesser Antillean species are limited to forests, as (pet-free) suburban gardens can also act as important habitats or even sanctuaries for critically endangered reptiles (e.g., Debrot, Boman, &amp; Madden, <span>2013</span>).</p><p>Finally, given the abundance of <i>A. picticauda</i> in Florida and the high volume of shipments from Florida to ports throughout the Caribbean, we strongly emphasize the responsibility of state authorities (including border control), as well as transport and shipping providers, to prevent animals from leaving those shores. Florida-based conservationists and alien species experts, with <i>A. picticauda</i> experience, are encouraged to help Lesser Antillean stakeholders and authorities through training and knowledge transfer to tackle this major threat to Caribbean biodiversity.</p>","PeriodicalId":50786,"journal":{"name":"Animal Conservation","volume":"27 1","pages":"1-4"},"PeriodicalIF":2.8000,"publicationDate":"2023-06-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/acv.12889","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Animal Conservation","FirstCategoryId":"93","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1111/acv.12889","RegionNum":2,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"BIODIVERSITY CONSERVATION","Score":null,"Total":0}
引用次数: 0

Abstract

During the ongoing sixth global extinction wave, island ecosystems are among the most impacted due to a high introduction rate of non-native species (Tershy et al., 2015; Bellard, Cassey, & Blackburn, 2016; Fernández-Palacios et al., 2021). Within one of the global biodiversity hotspots (Myers et al., 2000), the Caribbean Lesser Antilles are known for their high degree of endemism across numerous taxa, including reptiles (e.g., Smith et al., 2004; Losos et al., 2006). However, continuing introductions of non-native species are homogenizing the regional herpetofauna diversity (Capinha, Marcolin, & Reino, 2020), leading to extinctions and loss of functional trait diversity across islands and ecosystems (Kemp, 2023).

The most common terrestrial non-native vertebrates, throughout the Lesser Antilles, are reptiles (Thorpe, 2022). Their interactions with native reptile species have led to local extinctions and continuing declines in both native population sizes and distribution ranges through predation, hybridization, disease transmission, and competition for resources (Daltry, 2022). Multiple non-native species have already spread nearly regionwide, including Gymnophthalmus underwoodi, Hemidactylus mabouia, Indotyphlops braminus, Anolis/Norops sagrei, and Latin American Iguana iguana (Thorpe, 2022; Thibaudier et al., 2023; van den Burg et al., 2023), while others are spreading rapidly (e.g., Hemidactylus frenatus: Thibaudier et al., 2023 and references therein). Importantly, several of these non-native species are known to have been introduced to the Lesser Antilles from non-native populations in Florida (Powell et al., 2011); a pattern we fear is likely to be repeated by Peters's Rock Agama (Agama picticauda), although no established population has yet been reported in the Lesser Antilles.

Agama picticauda is a medium-sized lizard native to sub-Saharan western and central Africa, with both sexual dichromatism and size dimorphism. Adult males have a bright orange head and tail, while females are light brown and can have yellow to orange dorsolateral patches (Fig. 1). The species is diurnally active, has a maximum recorded snout–vent length of 15.7 cm (Krishnan et al., 2019), and can produce up to three clutches annually, each of 5–12 eggs (Blunden & Krysko, 2007; Krysko, Enge, & Moler, 2019). It occupies both horizontal and vertical surfaces from where it uses a sit-and-stalk approach to identify and pursue arthropods (Enge, Krysko, & Talley, 2004) and small vertebrates (Henigan et al., 2019).

In Florida, the first A. picticauda population was found in 1976 (Wilson & Porras, 1983) and it has since extended its range across the state (Enge, Krysko, & Talley, 2004). Recent analyses show high genetic variation within the Florida population due to introductions from different native origins (Nuñez, Krysko, & Avery, 2016). Given populations across its native range occupy different climatic niches (Krishnan et al., 2019), hybridization between populations of differing origins could result in high ecological adaptability (Consuegra et al., 2011), that in turn can increase establishment success when Florida individuals are translocated to other regions. Alarmingly, A. picticauda appears to be spreading to Caribbean islands as sightings are being reported from the Bahamas and Tortola (British Virgin Islands) (observations 139983395 and 89972864, https://www.inaturalist.org/). On Tortola, at least two adults as well as three juveniles have been observed, suggestive of an establishing population (C. Petrovic, pers. obs.). Further research on the status and impacts on the Bahamas is urgently needed, while on Tortola immediate action is necessary to remove the existing population.

Although the native and non-native dietary range and ecology of A. picticauda are poorly studied, when it spreads to the Lesser Antilles, this could have a major impact on numerous native species. There is clear evidence this species preys on smaller lizards. For example, Henigan et al. (2019) dissected a large female that had cannibalized a smaller individual (5 cm snout–vent length) and Florida residents have observed predation of Anolis species (e.g., iNaturalist record 19472282), and a predation attempt on an Ameiva ameiva (J. Wasilewski pers. obs.). These data are highly troubling given many taxa have life stages within these size ranges, while others (or at least one sex) never grow larger. Species of Alinea, Anolis, Bachia, Capitellum, Copeoglossum, Gymnophthalmus, Mabuya, Marisora and Spondylurus would be susceptible to predation, as well as juveniles of Ameiva, Cnemidophorus, Kentropyx and Pholidoscelis: an assemblage of >45 species (Thorpe, 2022). Furthermore, native adult lizards are likely to experience interspecific competition and potential displacement. Although Agama picticauda is mainly reported from urban and suburban environments, suggesting a low impact within intact forests, given the high threat to the Caribbean forests and their transition to (sub)urban areas, it is expected that A. picticauda could become widely distributed. Besides, not all native Lesser Antillean species are limited to forests, as (pet-free) suburban gardens can also act as important habitats or even sanctuaries for critically endangered reptiles (e.g., Debrot, Boman, & Madden, 2013).

Finally, given the abundance of A. picticauda in Florida and the high volume of shipments from Florida to ports throughout the Caribbean, we strongly emphasize the responsibility of state authorities (including border control), as well as transport and shipping providers, to prevent animals from leaving those shores. Florida-based conservationists and alien species experts, with A. picticauda experience, are encouraged to help Lesser Antillean stakeholders and authorities through training and knowledge transfer to tackle this major threat to Caribbean biodiversity.

Abstract Image

Peters Rock Agama(Agama picticauda)对小安的列斯群岛爬行动物多样性的威胁
在正在发生的第六次全球物种灭绝浪潮中,由于非本地物种的高引入率,岛屿生态系统受到的影响最大(Tershy 等人,2015 年;Bellard、Cassey &amp; Blackburn,2016 年;Fernández-Palacios 等人,2021 年)。加勒比海小安的列斯群岛是全球生物多样性热点地区之一(迈尔斯等人,2000 年),以包括爬行动物在内的众多类群的高度特有性而闻名(例如,史密斯等人,2004 年;洛索斯等人,2006 年)。然而,非本地物种的不断引入正在使该地区的爬行动物多样性趋于单一化(Capinha, Marcolin, &amp; Reino, 2020),导致各岛屿和生态系统之间的物种灭绝和功能特征多样性的丧失(Kemp, 2023)。通过捕食、杂交、疾病传播和资源竞争,它们与本地爬行动物的相互作用导致了本地爬行动物的灭绝,以及本地爬行动物种群数量和分布范围的持续下降(Daltry,2022 年)。多个非本地物种已几乎遍布整个地区,其中包括:Gymnophthalmus underwoodi、Hemidactylus mabouia、Indotyphlops braminus、Anolis/Norops sagrei 和拉丁美洲鬣蜥(Thorpe,2022 年;Thibaudier 等人,2023 年;van den Burg 等人,2023 年),而其他非本地物种正在迅速扩散(如 Hemidactylus frenatus:Thibaudier 等人,2023 年及其中的参考文献)。重要的是,已知这些非本地物种中有几个是从佛罗里达州的非本地种群引入小安的列斯群岛的(Powell 等人,2011 年);我们担心彼得斯岩蜥(Agama picticauda)可能会重蹈覆辙,尽管小安的列斯群岛尚未报告有成熟的种群。成年雄性的头部和尾部为亮橙色,雌性为浅棕色,背侧有黄色至橙色斑块(图 1)。该物种昼伏夜出,记录的最大鼻孔长度为 15.7 厘米(Krishnan 等人,2019 年),每年最多可产三窝卵,每窝 5-12 枚(Blunden &amp; Krysko, 2007; Krysko, Enge, &amp; Moler, 2019 年)。在佛罗里达州,1976年发现了第一个A. picticauda种群(Wilson &amp; Porras, 1983),此后它的活动范围扩展到全州(Enge, Krysko, &amp; Talley, 2004)。最近的分析表明,由于从不同的原生地引入,佛罗里达种群的遗传变异很大(Nuñez, Krysko, &amp; Avery, 2016)。鉴于其原产地的种群占据不同的气候壁龛(Krishnan 等人,2019 年),不同原产地的种群之间的杂交可能会导致较高的生态适应性(Consuegra 等人,2011 年),这反过来又会增加佛罗里达个体迁移到其他地区时的建立成功率。令人担忧的是,A. picticauda 似乎正在向加勒比海岛屿扩散,巴哈马群岛和托尔托拉(英属维尔京群岛)都有目击报告(观察结果 139983395 和 89972864,https://www.inaturalist.org/)。在托尔托拉岛,至少观察到两只成体和三只幼体,这表明该种群正在形成(C. Petrovic,观察者)。尽管对 A. picticauda 的本地和非本地食性范围和生态学研究甚少,但当它扩散到小安的列斯群岛时,可能会对许多本地物种产生重大影响。有明显证据表明,该物种会捕食较小的蜥蜴。例如,Henigan等人(2019年)解剖了一只大型雌性蜥蜴,它吃掉了一只较小的个体(吻端-齿端长度为5厘米),佛罗里达居民也观察到了捕食Anolis物种的现象(例如,iNaturalist记录19472282),还有一次捕食Ameiva ameiva的尝试(J. Wasilewski pers. obs.)。这些数据非常令人担忧,因为许多分类群的生命阶段都在这些大小范围内,而其它分类群(或至少一种性别)却从未变大。Ainea、Anolis、Bachia、Capitellum、Copeoglossum、Gymnophthalmus、Mabuya、Marisora和Spondylurus的物种,以及Ameiva、Cnemidophorus、Kentropyx和Pholidoscelis的幼体:45个物种的集合体(Thorpe,2022年)都很容易遭到捕食。此外,本地成年蜥蜴可能会经历种间竞争和潜在的迁移。
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来源期刊
Animal Conservation
Animal Conservation 环境科学-生态学
CiteScore
7.50
自引率
5.90%
发文量
71
审稿时长
12-24 weeks
期刊介绍: Animal Conservation provides a forum for rapid publication of novel, peer-reviewed research into the conservation of animal species and their habitats. The focus is on rigorous quantitative studies of an empirical or theoretical nature, which may relate to populations, species or communities and their conservation. We encourage the submission of single-species papers that have clear broader implications for conservation of other species or systems. A central theme is to publish important new ideas of broad interest and with findings that advance the scientific basis of conservation. Subjects covered include population biology, epidemiology, evolutionary ecology, population genetics, biodiversity, biogeography, palaeobiology and conservation economics.
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