Identifying how ecological relationships change with temperature is a crucial step towards understanding the consequences of climate change on ecosystem functioning. Where ecosystem engineering is influenced by warming, large impacts on biological non-trophic interactions may result (Byers et al. 2006; Zhou et al. 2022). On the land and in the sea, seed burial influences both small- and large-scale distributions and abundances of adult plants (Warr et al. 1993). Alongside abiotic processes and seed-mediated burial, the activities of fauna are critical to seed burial processes (Chambers and MacMahon 1994; Blackburn and Orth 2013; Zhu et al. 2016a). In marine sediments, bioturbating infauna can dislodge seeds or, alternatively bury seeds below their critical depths (Philippart 1994; Valdemarsen et al. 2011; Blackburn and Orth 2013), and as a metabolically driven process, their activity may be expected to change as the climate warms. In this study we found strong interacting effects of bioturbators and heatwaves on seagrass seed burial and germination. These results suggest that where germination rate is limiting of adult seagrass populations, climate warming may have large indirect effects on seagrass.
How infaunal invertebrates ecologically engineer their sediment environments is dependent on functional traits of infaunal species, such as their feeding guild, mode of locomotion and morphology (Aller 1982; Gerino et al. 2003; Jumars et al. 2015). Though all three infaunal species examined by this study enhanced seed burial over what was observed in control (fauna-free) sediment, as in previous studies (Blackburn and Orth 2013; Zhu et al. 2016a; Li et al. 2017) the magnitude of this effect varied with functional group. Despite predictions, based on previous studies (e.g. (Mermillod-Blondin et al. 2004; Delefosse and Kristensen 2012; Blackburn and Orth 2013; Zhu et al. 2016b, a; Schenone et al. 2019) that polychaetes might have particularly strong effects on seed burial, to the contrary it was cockles that had the greatest effect. This may reflect the larger body size of the cockles as compared to the other bioturbators manipulated in this study, as biomass is generally a good predictor of sediment reworking potential (Braeckman et al. 2010; Valdemarsen et al. 2011). Additionally, it may reflect functional differences between the taxa. Though upward conveying polychaetes oxygenate deeper sediment layers while ventilating their burrows (Michaud et al. 2005; Schenone et al. 2019), their sediment particle displacement capacity is limited mostly to the formation of the burrows (Kristensen et al. 2012). On a contrary, cockles as biodifussers, have lower capacity to oxygenate deeper sediments but are more efficient in mixing sediment particles up to their burial depth (~ 2 cm, depending on cockle size, Cozzoli et al., 2020; Li et al., 2017; Mermillod-Blondin et al., 2004). We observe cockle burying and reburying in most replicate cores.
Despite predictions that heatwaves might universally affect infaunal activity, and hence seed burial, we only found an effect of the heatwave on seed burial in the mixed species treatment. Ecological interactions such as competition, facilitation and predation may dampen or exacerbate stressor impacts (Christensen et al. 2006; Blake and Duffy 2010; Hicks et al. 2011). Additionally, biomass compensation between single and mixed species treatments may lead to differences in densities of individual taxa that may also contribute (Jolliffe 2000; Facelli 2003). Direct assessments of changes to the behaviors of macrofauna in heatwaves would assist in determining the mechanism for this species mixing effect. Irrespective of the mechanism, this result supports a growing literature demonstrating differential effects of environmental stressors on species when they are within versus isolated from their ecological communities (Petchey 2004; Nagelkerken and Munday 2016; Carrier-Belleau et al. 2021). It result reinforces the need to test ecological responses to environmental change using communities rather than individual organisms, as buffering or multiplicative effects may be seen (Duggins 1981; Gilman et al. 2010; Kordas et al. 2011; Wernberg et al. 2012).
Seed burial may influence seed survival, and hence also germination, by influencing seed anchoring and retention at suitable settlement sites, by providing escape from predation, and by placing seeds in suitable sediment conditions (Chambers and MacMahon 1994; Zhu et al. 2016a; Jørgensen et al. 2019). In our laboratory experiment, in which seeds were free of predators and strong hydrodynamic forces, seeds on the sediment surface overall had a higher rate of germination than buried seeds. This pattern of greater germination at the surface was also found for Zostera nigricaulis and Zostera marina seagrass seeds in similar mesocosm experiments (Cumming et al. 2017; Jørgensen et al. 2019). Other studies with Z. marina, however, found that seeds placed at or near the sediment surface had delayed germination, with optimal germination success achieved for shallowly buried seeds (Moore et al. 1993; Jarvis and Moore 2015). The variable effects of seed burial on germination may indicate population (Jarvis and Moore 2015) and species-level (Orth et al. 2000) variation in the optimal conditions for germination and/or variation among studies in sediment conditions, that determine their suitability for germination. Despite the controlled experimental conditions of our study, we found up to 6.4% of seeds were lost during an experimental run, probably through the process of water renewal. This suggests that in natural systems, with greater hydrodynamic forces, transport of unburied seeds may be considerable, highlighting the importance of burial to the seed bank.
One of the most widely investigated roles of bioturbators in soft bottom systems is the improvement of sediment quality, by facilitating nutrient and gas exchange between sediment layers and overlying water column, as well as sediment enrichment with nutrients via biodeposition (Reusch et al. 1994; Braeckman et al. 2010; Mermillod-Blondin 2011). Although we did not measure changes in sediment conditions in response to bioturbators, our results support a role for bioturbators influencing sediment suitability for germination. Under ambient conditions, the negative effect of seed burial on germination seen in the absence of fauna was not replicated when infauna were present. To the contrary, in treatments with infauna there were neutral or, in one instance, even with positive effects of burial on seed germination. Under the heat wave scenario, though, such positive effects of seed burial disappeared, and to the contrary, seed germination was negatively affected by burial in the polychaete treatment. High lugworm (Arenicola marina) densities have been implicated in the decline of Zostera marina in the Dutch Wadden Sea (Valdemarsen et al. 2011; Govers et al. 2014). The results suggest that the effects of bioturbators on seagrass habitats might be of a fine balance between improving the sediment suitability for plant growth and hampering seagrass establishment by removing the seeds from their optimal germination conditions.
Overall this study highlights the potential for strong ecosystem level effects of heat-waves on seagrass to arise from changes in non-trophic interactions. We demonstrated that seed burial and germination is influenced by the bioturbating activities of sediment-living invertebrates and these processes are altered by realistic warming events. Yet, the extent of heat impact on this interaction depended on the functional composition of the bioturbating community, as the increased capacity to bury seagrass propagules due to warming was only observed in the diverse fauna treatment where we mimicked a more natural composition of bioturbation traits by mingling species of different functional groups. In natural ecosystems, bioturbators of distinct functional traits co-exist in wide varieties. Moreover, effects of seed burial on germination, and seedling development, may be dependent on local biological and physical factors, such as the abundance and foraging method of seed predators, the magnitude of waves and currents that can dislodge seeds, as well as sediment properties. Field and laboratory tests are required across a boarder range of conditions to understand thresholds beyond which major shifts in seagrass ecosystems will occur.
There is growing evidence from terrestrial (Berg et al. 2010), freshwater (Beebee 1995) and marine environments (Draper and Weissburg 2019), that global warming can have large disruptive effects on ecosystems arising from the modification of species interactions (Memmott et al. 2007; Filbee-Dexter et al. 2016). Though most studies have focused on disruptions to trophic interactions (Ings et al. 2009; Ellison 2019), our study highlights the need to consider non-tropic interactions too. Small-scale experiments are useful in developing mechanistic understanding of non-trophic interactions and their sensitivity to environmental change. However, these need to be coupled with field observations of shifts in ecosystems following major weather events to understand the land- and sea-scape ramifications of shifting ecological interactions. The understanding thereby developed can guide conservation, restoration, and eco-engineering efforts aimed at building ecosystem resilience.