Journal of Ecology ( IF 5.3 ) Pub Date : 2024-09-02 , DOI: 10.1111/1365-2745.14407 S. J. Sharp 1 , K. E. Davidson 2 , C. Angelini 3, 4 , H. S. Fischman 3 , S. Pennings 5 , M. S. Fowler 2 , J. N. Griffin 2
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1 INTRODUCTION
Large herbivores, particularly equids and bovids, exert top-down control on the structure and diversity of vegetated ecosystems (Augustine & Frank, 2001; Waldram et al., 2008). Large grazers were likely more abundant and functionally relevant in the past than in modern ecosystems (Malhi et al., 2016), leading to calls for their inclusion in rewilded systems (Svenning et al., 2016). Large equids form free-roaming, wild or semi-wild populations in many parts of the world, and may already be, at least partially, functionally replacing extinct herbivorous megafauna (Lundgren et al., 2018). Yet, while large grazers are often associated with increased landscape heterogeneity and vegetation diversity (Oldén & Halme, 2016; Waldram et al., 2008), in some contexts they shift communities to non-desirable states (e.g. low vegetation cover; Hempson et al., 2019; McSherry & Ritchie, 2013). Systems with low plant diversity may be especially sensitive to large grazers, particularly when combined with other stressors such as invasive species or climatic extremes because other plant species are not present to replace those targeted by grazers (Biggs et al., 2020). While there is growing understanding of context-dependent effects of large grazers on terrestrial systems (Maestre et al., 2022), progress in coastal wetlands such as saltmarshes has been hampered by a geographic bias in study effort and an emphasis on farmed rather than wild or semi-wild grazers (Davidson et al., 2017).
Saltmarshes are socially and economically important systems, with large biogeographic structural variation that may have implications for their responses to large grazers (Davidson et al., 2017; Yando et al., 2023). These coastal wetlands form extensively around the world's wave-sheltered temperate coastlines (Mcowen et al., 2017), where they provide multiple ecosystem services that mitigate environmental hazards, and provide material goods, recreational opportunities and wildlife habitat (Barbier et al., 2011; Costanza et al., 1997; Pétillon et al., 2023). Saltmarshes are generally characterised by high primary and secondary production, which drives much of their ecosystem service provisioning (Barbier et al., 2011). Although large grazers occur on saltmarshes in all major saltmarsh-containing regions world-wide (Gaskins et al., 2020), their impacts have been most extensively studied in European marshes (Davidson et al., 2017). European marshes host rich floral assemblages, and substantial experimental and observational research has documented that they are resistant to grazing (Elizabeth et al., 2022; Harvey et al., 2019). While grazing reduces above-ground biomass, it tends to increase plant diversity and can even increase soil carbon storage (Elschot et al., 2015; Meirland et al., 2013; Olsen et al., 2011). In comparison, the role of large grazers in structurally varied marshes elsewhere in the world has been largely neglected (Davidson et al., 2017). Saltmarshes in North America, for example, are some of the most extensive in the world, with a long history of grazing by introduced horses and other livestock dating back over 400 years (Mcowen et al., 2017). In the US, although this practice has now declined (Gedan et al., 2009; Gruenberg, 2015; Reimold et al., 1975; Smith et al., 1989), free-ranging horses and cows graze on saltmarshes on multiple barrier islands along the eastern seaboard (Gruenberg, 2015). Most studies of grazing impacts in North American saltmarshes have been purely observational, comparing neighbouring grazed and ungrazed islands (Dolan, 2002; Hay & Wells, 1991; Reimold et al., 1975), or focused strictly on plant dynamics (Furbish & Albano, 1994; Turner, 1987). Yet, previous synthesis tentatively supports a greater sensitivity of these marshes to large grazers than their European counterparts (Davidson et al., 2017).
A key issue underlying the expected sensitivity of North American marshes to large grazers—and other compounding stressors—is a lack of capacity for functional compensation at both the individual plant and community levels. Many Eastern North American saltmarshes are dominated by a single foundation species, Spartina alterniflora (hereafter Spartina), which has a powerful influence on ecosystem structure and function (Bortolus et al., 2019). This species forms some of the most productive vegetated systems on Earth, donates substantial root and leaf tissue to soil organic carbon (SOC), provides tall and dense canopies that facilitate deposition of clay particles known to enhance SOC, and supports a diversity of infauna (Altieri et al., 2007; Fagherazzi et al., 2012; Oades, 1988; Reichle, 2023). In turn, soil quality (SOC) and infaunal communities have strong effects on ecosystem functioning and resilience (Angelini et al., 2015, 2016, 2018; Bastida et al., 2021; Bertness, 1985; Carney & Matson, 2005; Daleo et al., 2007; Gittman & Keller, 2013; Griffin & Silliman, 2018; Hensel & Silliman, 2013; Holdredge et al., 2009; Silliman et al., 2005). Spartina shows little capacity for compensatory responses to grazing by, for example, shifting to below-ground production (Valdez et al., 2023), and is reduced or eliminated by high densities of invertebrates or vertebrates (Hensel et al., 2021; Silliman et al., 2005). Although succulents may increase in abundance following Spartina declines (Bertness et al., 1992), they are unlikely to functionally compensate due to their lower productivity, shorter stature, and lack of mutualistic partnership with resident invertebrates. Despite the dominance and uniqueness of Spartina compared with succulent replacements, few studies have investigated how grazing from large herbivores impacts Spartina, and how potential vegetation community shifts cascade to saltmarsh soil properties and invertebrate communities, for example crabs, snails, and mussels (Reimold et al., 1975; Turner, 1987). Furthermore, grazing takes place—in the United States and globally—in the context of changing stressors and disturbances, such as invasive species and climate change (Angelini et al., 2018; Gedan et al., 2009; Sharp & Angelini, 2016; Silliman et al., 2005). If large grazers are having strong negative effects on saltmarsh vegetation in US saltmarshes, especially given limits to their functional redundancy, they could undermine ecological stability in the face of other stressors, thereby compromising important ecosystem functions including the accumulation of SOC.
In this study, we combined experimental exclusion and a broad-scale observational survey to investigate how large grazers affect a coastal ecosystem dominated by a single foundation species: US East Coast saltmarshes dominated by Spartina. To test causal effects of grazers on community and ecosystem properties when combined with other stressors, we used replicated grazer exclusion plots in Spartina saltmarsh on Cumberland Island, Georgia, maintained over 51 months. During this period, the experimental sites underwent marsh die-off, a mass mortality of S. partina associated with drought and consumer pressure (Alber et al., 2008; McKee et al., 2004; Silliman et al., 2005), allowing us to explore how large grazers impact marsh ‘resilience’, as indicated by the capacity of marshes to maintain living Spartina cover in the face of die-off. We also experimentally tested how grazing influenced marsh recovery by simulating invasive hog disturbance, a common stressor of eastern US marshes (Sharp & Angelini, 2019). To evaluate the generality of experimental results and assess the effects of long-term (>100 years) grazing across a large spatial scale, we measured similar properties in 14 grazed and 12 ungrazed saltmarshes over ~1100 km of coast between Florida and Maryland, USA. We hypothesised that in contrast to well-studied European marshes, eastern US saltmarshes would be highly sensitive to large grazers due to their dependence on a single foundation grass species. Specifically, we predicted that grazers would reduce Spartina above- and below-ground biomass, and since these marshes lack a functional replacement for Spartina, grazers would reduce invertebrates, shift soil texture, and ultimately suppress SOC concentration. We further expected grazing to reduce resilience to other stressors such as drought and feral hog disturbance as grazing was expected to reduce plant energy reserves, leaving marshes more vulnerable to compounding disturbances. Finally, we predicted that the long-term grazed/ungrazed sites would reflect the dynamics and interactions of both fast processes whose rates change or saturate over time (e.g. plant growth) and slow processes that may require several years to become detectable (e.g. slow change in soil carbon), while the measurable response of short-term exclusion plots would mostly reflect fast processes but depend on the recovery rates of individual variables.
中文翻译：
大型食草动物抑制了美国东部盐沼的一棵基础植物，降低了土壤的碳浓度
1 引言
大型食草动物，特别是马科动物和牛科动物，对植被生态系统的结构和多样性施加自上而下的控制（Augustine & Frank，2001;Waldram et al.， 2008）。与现代生态系统相比，大型食草动物在过去可能更丰富且功能更相关（Malhi et al.， 2016），因此呼吁将它们纳入再野化系统（Svenning et al.， 2016）。大型马科动物在世界许多地方形成自由漫游、野生或半野生种群，并且可能至少部分地在功能上取代了已灭绝的食草巨型动物（Lundgren 等，2018）。然而，虽然大型食草动物通常与景观异质性和植被多样性的增加有关（Oldén & Halme，2016 年;Waldram et al.， 2008），在某些情况下，它们将群落转变为不理想的状态（例如，植被覆盖率低;Hempson等人，2019 年;McSherry & Ritchie，2013 年）。植物多样性低的系统可能对大型食草动物特别敏感，特别是当与其他压力源（如入侵物种或极端气候）相结合时，因为不存在其他植物物种来取代食草动物所针对的植物物种（Biggs et al.， 2020）。虽然人们对大型放牧者对陆地系统的环境依赖性影响有了越来越多的了解（Maestre et al.， 2022），但盐沼等沿海湿地的进展受到研究工作中的地理偏见和强调养殖而不是野生或半野生放牧动物的阻碍（Davidson et al.， 2017）。
盐沼是具有重要社会和经济意义的系统，具有巨大的生物地理结构变化，这可能对它们对大型食草动物的反应产生影响（Davidson 等人，2017 年;Yando等人，2023 年）。这些沿海湿地广泛形成于世界各地的波浪遮蔽的温带海岸线周围（Mcowen et al.， 2017），它们提供多种生态系统服务，减轻环境危害，并提供物质商品、娱乐机会和野生动物栖息地（Barbier et al.， 2011;Costanza et al.， 1997;Pétillon等人，2023 年）。盐沼通常以初级和次级产量高为特征，这推动了其大部分生态系统服务的提供（Barbier et al.， 2011）。尽管全球所有主要盐沼包含地区的盐沼上都存在大型食草动物（Gaskins 等，2020），但它们的影响在欧洲沼泽中得到了最广泛的研究（Davidson 等，2017）。欧洲沼泽地拥有丰富的花卉组合，大量的实验和观察研究表明它们对放牧有抵抗力（Elizabeth 等人，2022 年;Harvey et al.， 2019）。虽然放牧减少了地上生物量，但它往往会增加植物多样性，甚至会增加土壤碳储存（Elschot et al.， 2015;Meirland等人，2013 年;Olsen et al.， 2011）。相比之下，世界其他地方结构多样的沼泽地中大型食草动物的作用在很大程度上被忽视了（Davidson 等，2017）。 例如，北美的盐沼是世界上面积最大的盐沼之一，引入的马和其他牲畜放牧的历史可以追溯到 400 多年前（Mcowen 等，2017）。在美国，尽管这种做法现在已经下降（Gedan et al.， 2009;Gruenberg，2015 年;Reimold 等人，1975 年;Smith et al.， 1989），自由放养的马和奶牛在东海岸多个堰洲岛上的盐沼上吃草（Gruenberg，2015）。 大多数关于北美盐沼放牧影响的研究都是纯粹的观察性研究，比较了邻近的放牧和未放牧的岛屿（Dolan，2002 年;Hay & Wells， 1991;Reimold等人，1975年），或者严格关注植物动力学（Furbish & Albano，1994年; Turner，1987 年）。然而，以前的合成初步支持这些沼泽对大型食草动物比欧洲同类更敏感（Davidson et al.， 2017）。
北美沼泽地对大型食草动物和其他复合压力源的预期敏感性的一个关键问题是在单个植物和群落层面缺乏功能补偿能力。许多北美东部盐沼以单一的基础物种为主，即互花斯巴蒂娜（Spartina），它对生态系统的结构和功能具有强大的影响（Bortolus et al.， 2019）。该物种形成了地球上一些生产力最高的植被系统，为土壤有机碳 （SOC） 提供大量的根和叶组织，提供高大而密集的树冠，促进已知可增强 SOC 的粘土颗粒的沉积，并支持动物群的多样性（Altieri 等人，2007 年;Fagherazzi 等人，2012 年;Oades， 1988;Reichle，2023 年）。反过来，土壤质量 （SOC） 和动物群落对生态系统功能和复原力有很大影响（Angelini 等人，2015、2016、2018;Bastida et al.， 2021;Bertness， 1985;Carney & Matson， 2005;Daleo 等人，2007 年;Gittman & Keller， 2013;Griffin & Silliman， 2018;Hensel & Silliman，2013 年;Holdredge 等人，2009 年;Silliman et al.， 2005）。Spartina 对放牧的补偿反应能力很小，例如，通过转向地下生产（Valdez 等人，2023 年），并且被高密度的无脊椎动物或脊椎动物减少或消除（Hensel 等人，2021 年;Silliman et al.， 2005）。 尽管多肉植物的数量可能会在 Spartina 下降后增加（Bertness 等人，1992 年），但由于它们的生产力较低、身材矮小以及与常驻无脊椎动物缺乏互惠伙伴关系，它们不太可能在功能上进行补偿。尽管与多肉替代品相比，Spartina 具有主导地位和独特性，但很少有研究调查大型食草动物的放牧如何影响 Spartina，以及潜在的植被群落如何级联转移到盐沼土壤特性和无脊椎动物群落，例如螃蟹、蜗牛和贻贝（Reimold 等人，1975 年;Turner，1987 年）。此外，在美国和全球范围内，放牧发生在不断变化的压力源和干扰（如入侵物种和气候变化）的背景下（Angelini 等人，2018 年;Gedan 等人，2009 年;Sharp & Angelini， 2016;Silliman et al.， 2005）。如果大型食草动物对美国盐沼的盐沼植被产生强烈的负面影响，特别是考虑到它们的功能冗余有限，它们可能会在面对其他压力因素时破坏生态稳定，从而损害重要的生态系统功能，包括 SOC 的积累。
在这项研究中，我们将实验排除和大规模观察调查相结合，以调查大型食草动物如何影响由单一基础物种主导的沿海生态系统：以 Spartina 为主的美国东海岸盐沼。为了测试放牧者与其他压力源相结合时对群落和生态系统特性的因果影响，我们在佐治亚州坎伯兰岛的 Spartina 盐沼中使用了重复的放牧者排除图，维持了 51 个月以上。在此期间，实验地点经历了沼泽死亡，与干旱和消费者压力相关的 S. partina 的大规模死亡（Alber 等人，2008 年;McKee et al.， 2004;Silliman 等人，2005 年），使我们能够探索大型食草动物如何影响沼泽的“恢复力”，正如沼泽在面临死亡时保持活的 Spartina 覆盖的能力所表明的那样。我们还通过模拟侵入性猪干扰（美国东部沼泽地的常见压力源）实验测试了放牧如何影响沼泽恢复，这是美国东部沼泽地的常见压力源（Sharp & Angelini，2019）。为了评估实验结果的普遍性并评估在大空间尺度上长期 （>100 年） 放牧的影响，我们在佛罗里达州和美国马里兰州之间 ~1100 公里海岸的 14 个放牧和 12 个未放牧的盐沼中测量了类似的特性。我们假设，与经过充分研究的欧洲沼泽相比，美国东部盐沼对大型食草动物高度敏感，因为它们依赖于单一的基础草种。 具体来说，我们预测放牧者会减少 Spartina 地上和地下生物量，并且由于这些沼泽缺乏 Spartina 的功能替代品，放牧者会减少无脊椎动物，改变土壤质地，并最终抑制 SOC 浓度。我们进一步预计放牧会降低对其他压力源（如干旱和野猪干扰）的适应能力，因为预计放牧会减少植物的能量储备，使沼泽更容易受到复合干扰。最后，我们预测长期放牧/未放牧地点将反映速率随时间变化或饱和的快速过程（例如植物生长）和可能需要几年才能检测到的缓慢过程（例如土壤碳的缓慢变化）的动态和相互作用，而短期排除图的可测量响应将主要反映快速过程，但取决于单个变量的恢复率。
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