Graham Olivia J, Aoki Lillian R, Burge Colleen A, Harvell C Drew
Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York, USA.
Institute of Marine and Environmental Technology, University of Maryland Baltimore County, Baltimore, Maryland, USA.
Ecology. 2025 Jan;106(1):e4493. doi: 10.1002/ecy.4493. Epub 2024 Dec 4.
Although invertebrate herbivores commonly impact terrestrial plant diseases by facilitating transmission of plant pathogens and increasing host susceptibility to infection via wounding, less is known about the role of herbivores in marine plant disease dynamics. Importantly, transmission via herbivores may not be required in the ocean since saline ocean waters support pathogen survival and transmission. Through laboratory experiments with eelgrass (Zostera marina), we showed that isopods (Pentidotea wosnesenskii) and snails (Lacuna spp.) created grazing scars that increased disease severity and thus indirectly facilitated transmission of Labyrinthula zosterae (Lz), a protist that causes seagrass wasting disease. Experiments also quantified different feeding preferences among herbivores: Amphipods (Ampithoe lacertosa) selectively consumed diseased eelgrass, while isopods and snails selectively grazed asymptomatic leaves, suggesting different herbivore taxa may have contrasting impacts on disease dynamics. Our experiments show no sign that herbivores directly vector Lz from diseased to asymptomatic eelgrass. However, we isolated live Lz from isopod, amphipod, and snail feces and detected Lz with quantitative polymerase chain reaction in amphipods and snails, suggesting that herbivores eating diseased eelgrass could pass the live pathogen. Finally, field surveys demonstrated a close association between seagrass wasting disease and invertebrate grazing scars; disease prevalence was 29 ± 4.7% (95% CI) higher on eelgrass leaves with herbivore scars. Collectively, these findings show that some herbivores can increase eelgrass disease risk by facilitating the spread of an important pathogen via wounding, but not via direct transmission. Thus, herbivores may play different roles in plant disease dynamics in terrestrial versus marine ecosystems depending on the pathogen's ability to survive and transmit without a vector.
虽然无脊椎食草动物通常通过促进植物病原体的传播以及通过造成伤口增加宿主对感染的易感性来影响陆生植物病害,但关于食草动物在海洋植物病害动态中的作用却知之甚少。重要的是,由于咸海水支持病原体的存活和传播,在海洋中可能不需要通过食草动物进行传播。通过对大叶藻(Zostera marina)进行实验室实验,我们发现等足类动物(Pentidotea wosnesenskii)和蜗牛(Lacuna spp.)造成的啃食伤痕会增加病害严重程度,从而间接促进了Labyrinthula zosterae(Lz)的传播,Lz是一种导致海草消瘦病的原生生物。实验还量化了食草动物之间不同的取食偏好:双足虾(Ampithoe lacertosa)选择性地啃食患病的大叶藻,而等足类动物和蜗牛则选择性地啃食无症状的叶片,这表明不同的食草动物类群可能对病害动态产生不同的影响。我们的实验没有显示出食草动物将Lz从患病大叶藻直接传播到无症状大叶藻的迹象。然而,我们从等足类动物、双足虾和蜗牛的粪便中分离出了活的Lz,并通过定量聚合酶链反应在双足虾和蜗牛中检测到了Lz,这表明啃食患病大叶藻的食草动物可能会传播活的病原体。最后,实地调查表明海草消瘦病与无脊椎动物的啃食伤痕之间存在密切关联;有食草动物啃食伤痕的大叶藻叶片上的病害患病率高出29±4.7%(95%置信区间)。总体而言,这些发现表明,一些食草动物可以通过造成伤口促进重要病原体的传播,而不是通过直接传播,从而增加大叶藻的病害风险。因此,食草动物在陆地和海洋生态系统的植物病害动态中可能扮演不同的角色,这取决于病原体在没有传播媒介的情况下存活和传播的能力。