Functional Ecology ( IF 4.6 ) Pub Date : 2022-10-09 , DOI: 10.1111/1365-2435.14198 A. E. L. Walker 1, 2 , M. P. Robertson 3 , P. Eggleton 4 , K. Bunney 3 , C. Lamb 3 , A. M. Fisher 5 , C. L. Parr 1, 3, 6
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1 INTRODUCTION
Decomposition is a fundamental ecosystem process that recycles carbon and nutrients from plant litter and organic matter (Swift et al., 1979). It therefore has a major influence on carbon flux (Griffiths et al., 2021), nutrient dynamics (Freschet et al., 2013) and below-ground ecosystem functioning (Meier & Bowman, 2008; Wardle et al., 2004). Determining the biotic drivers of decomposition rates will, therefore, be vital for predicting how ecosystem change will affect ecosystem functioning. This may be particularly relevant in tropical ecosystems, which play a critical role in carbon cycling and storage (Mitchard, 2018; Scurlock & Hall, 1998), yet are undergoing rapid change.
Traditionally, climate and litter quality have been considered the dominant controls on decomposition rate, and the impact of decomposer organisms was considered to be relatively small (Swift et al., 1979). Recent studies, however, have suggested that variation in populations of decomposer organisms can influence decomposition rates globally (Bradford et al., 2017; García-Palacios et al., 2013) and that these effects can be independent of climate (Allison, 2012; McGuire & Treseder, 2010). Moreover, several studies have investigated whether interspecific interactions, via effects on decomposer organisms, can drive variation in decomposition rates (see Sitvarin et al., 2016 for a review). However, the magnitude and direction of the relationships shown is highly variable across the aforementioned studies (Sitvarin et al., 2016).
Predation is arguably one of the most ecologically influential interspecies interactions, as it can as it can indirectly and directly determine coexistence of species and alter species abundances (Salo et al., 2010; Sheriff et al., 2020). Predation can also affect the diversity of non-prey species via trophic cascades (Pace et al., 1999). Consequently, predation can strongly affect the structure and functioning of ecosystems (Duffy, 2002; Schmitz et al., 2010). Predatory species are currently in global decline (Estes et al., 2011), with climate change likely to alter predator–prey interactions further (Gilg et al., 2009; Laws, 2017; Wilmers et al., 2007). For example, increased metabolisms due to higher temperatures may lead to higher predation rates, and CO2-induced physiological changes in predators may decrease predation rates (Laws, 2017). Therefore, having a holistic understanding of the direct and indirect ecosystem effects of predators is important for predicting future ecosystem changes.
Although there is consistent evidence to suggest that predation can regulate abundances of herbivores and have cascading effects on herbivory (the green food web; reviewed in Schmitz et al., 2000), evidence for the impact of predation on decomposers and decomposition (the brown food web) is somewhat mixed. Studies have found positive (Lawrence & Wise, 2000; Melguizo-Ruiz et al., 2020), negative (Liu et al., 2014; Wu et al., 2011; Wu et al., 2014) and neutral (Cates et al., 2021; Denmead et al., 2017; Hocking & Babbitt, 2014; Namba & Ohdachi, 2016) relationships between predation and decomposition across studies (reviewed in Sitvarin et al., 2016). Why predation has been found to have variable effects on decomposition is not fully understood but may be caused by differences in predator trophic guild – that is, predators that directly consume decomposer species may have negative cascading effects on decomposition (Lawrence & Wise, 2000; Wu et al., 2011; Wyman, 1998), whereas higher-trophic level predators that prey on the predators of decomposers, or on microbivores, may release decomposers from predation and, therefore, have positive cascading effects (Lawrence & Wise, 2004; McGlynn & Poirson, 2012; Melguizo-Ruiz et al., 2020). Moreover, a number of studies reported no predation effect on decomposition, which was attributed to high levels of functional redundancy within brown food webs (Cates et al., 2021), the complexity of food web pathways (Miyashita & Niwa, 2006; Namba & Ohdachi, 2016) and other biotic or abiotic factors overshadowing any predation effect (Denmead et al., 2017; Hocking & Babbitt, 2014; Homyack et al., 2010; López-Rodríguez et al., 2018). Notably, there is a lack of large-scale (>8 × 8 m), open plot experiments in previous literature (though see Parr et al., 2016 and Cates et al., 2021), as the vast majority of studies employed mesocosms, which run the risk of artefacts arising due to small scales and enclosure of the study organisms (Petersen & Hastings, 2001). Previous studies are also biased towards non-tropical systems, which is a concern given the vital importance of biomes such as savannas and rainforests to carbon cycling and storage (Mitchard, 2018; Scurlock & Hall, 1998). Thus, we lack a comprehensive understanding of the factors determining the existence, direction and strength of predation effects on decomposition, and studies are needed to broaden the experimental and geographical scale upon which our knowledge is based.
Macroinvertebrates, particularly termites, play a crucial role in decomposition in tropical and subtropical ecosystems (Griffiths et al., 2019; Wood & Sands, 1978). As such, determining the controls on termite-mediated decomposition is a critical part of understanding how these ecosystems function. Research into the determinants of termite abundance and activity has largely focussed on bottom-up controls such as climate (e.g. Cerezer et al., 2020, Davies et al., 2015), and top-down controls such as predation have received little attention. Recent work suggests that termite-feeding mammals may exert top-down pressures on termite activity and decomposition rates, although it is not clear whether this is due to direct predation of termites or to physical disturbance of termites by the predator (Coggan et al., 2016). Yet, in most tropical and subtropical ecosystems ants are the major invertebrate predator of termites (Tuma et al., 2020). Being far more widespread and abundant than termite-feeding mammals, ants have the potential to influence termite-mediated processes to a much greater extent (Parr et al., 2016). However, anthropogenic pressures, such as invasive species, land-use change and climate change, are likely to alter ant abundance patterns and species distributions (Bertelsmeier et al., 2015; Bertelsmeier et al., 2018; Parr & Bishop, 2022). For example, climate change may have particularly strong negative impacts on ant abundances in tropical systems, yet potentially positive impacts in temperate regions (Parr & Bishop, 2022). This means that predator–prey interactions involving ants may shift in the future, which could have cascading consequences for processes such as decomposition, that are mediated by prey species such as termites.
Here, we suppressed the abundance of ants on 1 ha open plots in a South African savanna and measured how this affected macroinvertebrate-mediated decomposition in three common organic substrates, which represent the dominant vegetation in the system: grass and wood, and less-well studied but common organic inputs, herbivore dung. Specifically, we quantified how ant suppression (1) affected the abundance and activity of termite decomposers; (2) affected macroinvertebrate-mediated decomposition across substrates, and evaluated the importance of termites to decomposition (to establish their role as key macroinvertebrate decomposers in our study system) and finally, (4) we determined whether ant suppression altered the balance of macroinvertebrate versus microbial decomposition rates. We predicted that ant suppression would positively influence termite abundance and activity, resulting in an increase in macroinvertebrate decomposition across all substrates. We demonstrate a strong indirect effect of ants on macroinvertebrate-mediated decomposition rates across a range of common decomposition substrates and propose that these trends are largely due to a release of the major decomposer, termites, from ant predation.
中文翻译：
无脊椎动物捕食者对分解的间接控制
1 简介
分解是一个基本的生态系统过程，它从植物凋落物和有机物中回收碳和养分（Swift 等人， 1979 年）。因此，它对碳通量（Griffiths 等人， 2021 年）、营养动态（Freschet 等人， 2013 年）和地下生态系统功能（Meier & Bowman， 2008 年；Wardle 等人， 2004 年）有重大影响。因此，确定分解率的生物驱动因素对于预测生态系统变化将如何影响生态系统功能至关重要。这可能与热带生态系统特别相关，热带生态系统在碳循环和储存中起着至关重要的作用（Mitchard， 2018 年；Scurlock 和 Hall， 1998 年）)，但正在发生快速变化。
传统上，气候和垫料质量被认为是分解速率的主要控制因素，而分解生物的影响被认为相对较小（Swift 等， 1979）。然而，最近的研究表明，分解生物种群的变化会影响全球分解率（Bradford 等人， 2017 年；García-Palacios 等人， 2013 年），并且这些影响可能与气候无关（Allison， 2012 年； McGuire 和 Treseder， 2010 年）。此外，一些研究调查了种间相互作用是否通过对分解生物体的影响来驱动分解率的变化（参见 Sitvarin 等人， 2016 年）审查）。然而，在上述研究中，所示关系的大小和方向变化很大（Sitvarin 等人， 2016 年）。
捕食可以说是最具生态影响力的种间相互作用之一，因为它可以间接和直接地决定物种共存并改变物种丰度（Salo 等人， 2010 年；Sheriff 等人， 2020 年）。捕食还可以通过营养级联影响非猎物物种的多样性 (Pace et al., 1999 )。因此，捕食会强烈影响生态系统的结构和功能（Duffy， 2002 年；Schmitz 等， 2010 年）。掠食性物种目前在全球范围内正在减少（Estes 等人， 2011 年），气候变化可能会进一步改变捕食者与猎物之间的相互作用（Gilg 等人， 2009 年；Laws， 2017 年）; 威尔默斯等人， 2007 年）。例如，由于更高的温度而增加的新陈代谢可能导致更高的捕食率，而 CO 2诱导的捕食者的生理变化可能会降低捕食率（Laws， 2017）。因此，全面了解捕食者对生态系统的直接和间接影响对于预测未来的生态系统变化非常重要。
虽然有一致的证据表明捕食可以调节食草动物的丰度并对食草动物产生级联效应（绿色食物网；Schmitz 等人， 2000 年综述），但捕食对分解者和分解物（棕色食物网）影响的证据web) 有点混杂。研究发现阳性（Lawrence & Wise， 2000；Melguizo-Ruiz 等， 2020）、阴性（Liu 等， 2014；Wu 等， 2011；Wu 等， 2014）和中性（Cates 等， ., 2021 年；Denmead 等人， 2017 年；Hocking 和 Babbitt， 2014 年；Namba 和 Ohdachi， 2016 年) 捕食和分解之间的关系跨研究（综述于 Sitvarin 等人， 2016 年）。为什么发现捕食对分解有不同的影响尚不完全清楚，但这可能是由捕食者营养集团的差异引起的——也就是说，直接消耗分解物种的捕食者可能对分解有负面的级联效应 (Lawrence & Wise, 2000 ; Wu等人， 2011 年；Wyman， 1998 年），而捕食分解者捕食者或微生物的高营养级捕食者可能会释放分解者免于捕食，因此具有正级联效应（Lawrence & Wise， 2004；McGlynn & Poirson， 2012 年；Melguizo-Ruiz 等人， 2020 年）。此外，许多研究报告说捕食对分解没有影响，这归因于棕色食物网中的高水平功能冗余（Cates 等人， 2021 年）、食物网途径的复杂性（Miyashita & Niwa， 2006 年；Namba & Ohdachi, 2016 ) 和其他生物或非生物因素掩盖了任何捕食效应 (Denmead et al., 2017 ; Hocking & Babbitt, 2014 ; Homyack et al., 2010 ; López-Rodríguez et al., 2018 )。值得注意的是，在以前的文献中缺乏大规模（>8 × 8 m）的开放地块实验（尽管参见 Parr 等人， 2016 年和 Cates 等人， 2021 年), 因为绝大多数研究都采用了中观宇宙, 由于研究生物体的小规模和封闭, 这有产生人工制品的风险 (Petersen & Hastings, 2001 )。以前的研究也偏向于非热带系统，考虑到稀树草原和热带雨林等生物群落对碳循环和储存的至关重要性，这是一个令人担忧的问题（Mitchard， 2018 年；Scurlock 和 Hall， 1998 年）。因此，我们对决定捕食对分解作用的存在、方向和强度的因素缺乏全面的了解，需要进行研究以扩大我们知识所依据的实验和地理范围。
大型无脊椎动物，尤其是白蚁，在热带和亚热带生态系统的分解中起着至关重要的作用（Griffiths 等人， 2019 年；Wood & Sands， 1978 年）。因此，确定对白蚁介导的分解的控制是了解这些生态系统如何运作的关键部分。对白蚁数量和活动的决定因素的研究主要集中在自下而上的控制，例如气候（例如 Cerezer 等人， 2020 年，Davies 等人，2015 年）), 而捕食等自上而下的控制则很少受到关注。最近的研究表明，以白蚁为食的哺乳动物可能对白蚁活动和分解率施加自上而下的压力，尽管尚不清楚这是由于白蚁的直接捕食还是捕食者对白蚁的物理干扰（Coggan 等人， 2016 年）。然而，在大多数热带和亚热带生态系统中，蚂蚁是白蚁的主要无脊椎动物捕食者（Tuma 等人， 2020 年）。与以白蚁为食的哺乳动物相比，蚂蚁分布更广、数量更多，因此有可能在更大程度上影响白蚁介导的过程（Parr 等人， 2016 年）). 然而，入侵物种、土地利用变化和气候变化等人为压力可能会改变蚂蚁丰度模式和物种分布（Bertelsmeier 等人， 2015 年；Bertelsmeier 等人， 2018 年；Parr 和 Bishop， 2022 年）。例如，气候变化可能对热带系统中的蚂蚁数量产生特别强烈的负面影响，但对温带地区可能产生积极影响（Parr 和 Bishop， 2022 年）。这意味着涉及蚂蚁的捕食者与猎物的相互作用在未来可能会发生变化，这可能会对分解等过程产生连锁反应，这些过程是由白蚁等猎物介导的。
在这里，我们抑制了南非大草原 1 公顷开阔地上的蚂蚁数量，并测量了这如何影响三种常见有机基质中大型无脊椎动物介导的分解，这些基质代表系统中的主要植被：草和木材，以及不太好的研究过但常见的有机投入物，食草动物的粪便。具体来说，我们量化了蚂蚁抑制 (1) 如何影响白蚁分解者的丰度和活动；(2) 影响大型无脊椎动物介导的基质分解，并评估白蚁对分解的重要性（以确立它们在我们研究系统中作为关键大型无脊椎动物分解者的作用），最后，(4) 我们确定蚂蚁抑制是否改变了大型无脊椎动物与大型无脊椎动物之间的平衡微生物分解率。我们预测，抑制蚂蚁会对白蚁的数量和活动产生积极影响，从而导致大型无脊椎动物在所有基质上的分解增加。我们证明了蚂蚁在一系列常见分解底物上对大型无脊椎动物介导的分解速率的强烈间接影响，并提出这些趋势主要是由于主要分解者白蚁从蚂蚁捕食中释放出来的。
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