Range-extending tropical herbivores increase diversity, intensity and extent of herbivory functions in temperate marine ecosystems

1. Climate change is modifying species distributions around the world, forcing some species poleward, where they can alter trophic interactions. Many tropical herbivorous fishes have successfully expanded their ranges into temperate ecosystems, and while it is clear they drive increases in herbivory rates in specific localities, little is known about how they might affect the diversity of herbivory functions across large spatial scales, considering their interaction with assemblages of native herbivores in temperate habitats.
2. We assessed the spatial overlap and habitat associations of native temperate and range-expanding tropical herbivorous fishes in six sub-regions of south-western Australia to determine how incursions of tropical species may have affected the diversity, redundancy (index of uniqueness) and the ‘spatial extent’ (addition of functions in new areas) and ‘intensity’ (increasing density of functional groups) of specific herbivory functions in recipient ecosystems.
3. Tropical herbivores were more abundant in temperate ecosystems, forming schools from 40 (parrotfish) to 200 (rabbitfish) individuals strongly associated with seagrass meadows and reefs with high cover of turf algae. Overlap with temperate herbivores was highest in the northern sub-regions, forming unique assemblages, with no apparent species displacements. The addition of tropical species increased functional diversity and uniqueness (the complement of redundancy), introducing novel herbivory functions to many locations. Seagrass browsing increased in spatial extent (27%) and intensity (15 x), while seaweed browsing and grazing increased in intensity by up to 2.5 x in regions with high abundances of tropical herbivores.
4. Our results suggest that the diversity, intensity and spatial extent of different herbivory functions can change as tropical species with different habitat affinities, behaviors and diets shift their distributions poleward. Changes in functional redundancy are likely to be heterogeneous in space and might not increase initially because the diversity of herbivory functions is relatively low in some temperate marine ecosystems. However, there is the potential for greater redundancy as further tropical species arrive, their abundances increase and the spatial and functional overlap of communities rises.
Methods
Surveys of herbivorous fish were conducted over inshore habitats along the coastline of south-western Australia during summer (April-May) of 2018 and 2019, from the Perth metropolitan area to Cape Naturaliste in the south of the state. The abundances of temperate (Girella zebra, Olisthops cyanomelas, Pelates octolineatus, Kyphosus cornelii and Kyphosus sydneyanus) and tropical herbivorous fish (Scarus spp. and Siganus fuscescens) were measured via a GPS-tracked roving underwater visual census with 15 minutes per sampling location. One surveyor swam at a constant pace, registering all individuals of the species of interest in an approximate area of 2000 m2 per transect. A second surveyor followed the same path recording the seascape with an underwater camera for subsequent assessment of habitat features. Videos were analyzed with the program TransectMeasure (SeaGIS), each video transect was paused at one minute intervals (n=15 per transect) to extract information on topographic complexity (Wilson, Graham & Polunin 2007), substrate type, species composition, species diversity, and abundance of morpho-functional groups of sessile biota based on the CATAMI classification scheme (Althaus et al. 2015). Fish abundance was standardized to density (individuals 125 m-2); however, we also considered a new metric: MaxS (maximum number of fish per school in each survey), a similar approach to abundance assessments of pelagic schooling fish (i.e. school size; Beare 2002) and abundance estimates from static video methods (i.e. MaxN; Cappo et al. 2003).

1. 气候变化正在改变全球范围内的物种分布格局，迫使部分物种向极地迁移，在此过程中它们可能会改变当地的营养级相互作用（trophic interactions）。诸多热带植食性鱼类（herbivorous fishes）已成功将分布范围扩张至温带生态系统（temperate ecosystems），尽管已有研究明确其在特定区域内会提升植食作用速率，但目前我们对这类鱼类如何影响大空间尺度下的植食功能多样性仍知之甚少——尤其是考虑到它们与温带生境中原生植食鱼类类群的相互作用。
2. 本研究针对澳大利亚西南部的六个亚区域，调查了温带原生植食鱼类与扩张分布范围的热带植食鱼类的空间重叠情况及其与生境的关联，旨在明确热带物种的入侵会如何改变接收生态系统中特定植食功能的多样性、功能冗余（redundancy，以独特性指数表征）、“空间范围（spatial extent，指新区域内功能的新增情况）”以及“强度（intensity，指功能群密度的提升幅度）”。
3. 热带植食性鱼类在温带生态系统中丰度更高，会形成由40尾（鹦嘴鱼（parrotfish））至200尾（蓝子鱼（rabbitfish））个体组成的鱼群（school），且显著偏好海草床（seagrass meadows）与藻席（turf algae）盖度较高的礁体（reef）。与温带植食鱼类的空间重叠在北部亚区域最为显著，形成了独特的类群组合，未出现明显的物种替代现象。热带物种的迁入提升了功能多样性（functional diversity）与独特性（即功能冗余的反向指标），为诸多区域引入了全新的植食功能。在热带植食鱼类丰度较高的区域，海草啃食的空间范围提升了27%、强度提升了15倍，而海藻啃食与牧食作用的强度最高提升至原来的2.5倍。
4. 本研究结果表明，随着具有不同生境偏好、行为模式与食性的热带物种向极地迁移，不同植食功能的多样性、强度与空间范围均会发生改变。功能冗余的变化在空间上可能存在异质性，且在部分温带海洋生态系统中，由于原生植食功能的多样性本就较低，冗余度可能不会在初期出现提升。不过随着更多热带物种迁入、种群丰度上升以及群落的空间与功能重叠度增加，功能冗余具备进一步提升的潜力。

研究方法
本研究于2018年及2019年夏季（4月至5月），在澳大利亚西南部沿岸近岸生境开展植食性鱼类调查，调查范围覆盖从珀斯都会区至该州南部的纳多利斯角（Cape Naturaliste）沿岸海域。
本研究采用GPS追踪的漫游式水下视觉普查（roving underwater visual census）法，对温带植食鱼类（斑纹舵鲼Girella zebra、蓝带盔鱼Olisthops cyanomelas、八带笛鲷Pelates octolineatus、科氏银鲈Kyphosus cornelii与悉尼银鲈Kyphosus sydneyanus）及热带植食鱼类（鹦嘴鱼属Scarus spp.与褐蓝子鱼Siganus fuscescens）的丰度进行量化，每个采样点的普查时长为15分钟。
1名调查员以恒定速度游动，在每个约2000平方米的样带（transect）内记录目标物种的所有个体。另1名调查员沿同一路径行进，使用水下相机拍摄海景，用于后续生境特征的评估。
研究使用TransectMeasure（SeaGIS）软件对视频进行分析，每个视频样带以1分钟为间隔暂停（每个样带共15次），以提取地形复杂度（Wilson、Graham & Polunin, 2007）、底质类型、物种组成、物种多样性，以及基于CATAMI分类方案（CATAMI classification scheme, Althaus et al. 2015）的固着生物（sessile biota）形态功能群（morpho-functional groups）丰度信息。
鱼类丰度被标准化为密度单位（每125平方米个体数）；此外，本研究还采用了一项新指标：MaxS（每次调查中单个鱼群的最大个体数），该方法与中上层集群鱼类（pelagic schooling fish）的丰度评估（即鱼群大小；Beare, 2002）及静态视频法的丰度估算（即MaxN；Cappo et al. 2003）思路一致。