Resource limitation of compensatory responses in ecosystem processes after biodiversity loss

Biodiversity loss may result in a decline in important ecosystem processes. The effect of biodiversity loss on ecosystem functioning is determined by the functional contribution of the species lost and the compensatory responses of the remaining species. It is unknown to what extent the strength of the compensatory response of the remaining species depends on resource availability. Here we evaluate how the primary production of an assemblage of salt marsh plants responds to a realistic sequence of species loss in a 7-year experiment, with and without the addition of fertiliser. We found near-full compensation of progressive species loss in gross community primary production by the extinction-resistant species with fertiliser as long as one species (Triglochin maritima) remained. Without fertiliser, at least 4 species, including the particularly abundant species Plantago maritima, were needed to maintain gross community primary production. These results suggest that the magnitude of the compensation by extirpation-resistant species for the decline in ecosystem processes associated with progressive biodiversity loss depends on the resource context, and that compensation after the loss of plant species can be accelerated by increasing resource availability. Ultimately, full compensation appears to be limited by the presence and abundance of species in the remaining community that possess traits that allow them to compensate for the species lost. These findings suggest that the conclusions of a large body of biodiversity-ecosystem experiments cannot be used for informing the management of natural systems, because they do not simulate realistic extinction sequences, and therefore cannot quantify the potential for compensation of ecosystem services in the real world.

Methods
We evaluate how the primary production of an assemblage of salt marsh plants responds to a realistic sequence of species loss in a 7-year experiment, with and without the addition of fertiliser.

Following a previous study by Davies et al. (2012) on algal impact in salt marshes, this paper investigates how plant communities respond to the gradual loss of species caused by increasing fucoid algae deposits. Ninety 1-m2 experimental plots spaced ~ 3 m apart were established in an area of transitional low salt marsh in the Cefni estuary, Anglesey, Wales, UK (53°10′12″ N: 4°23′39″ W). In June 2009, the undisturbed assemblage of salt marsh plants was manipulated. A central 40 x 40 cm area of each of 32 plots was randomly allocated to a stage in the extirpation sequence of species in response to increased volumes of fucoid algae deposited on the marsh surface (see Davies et al., 2012). Species were removed on a species-by-species basis following the derived extirpation sequence (Salicornia ramosissima J. Woods, < Puccinellia maritima (Huds.) Parl. < Armeria maritima (Mill.) < Limonium humile Mill. < Plantago maritima L. < Aster tripolium L. < Triglochin maritima L., from least to most extirpation resistant).

The experiment lasted for 7 years from 2009 to 2017. To quantify whether compensation was context-dependent, and limited by nutrient availability, half the plots for each treatment (n = 2 per treatment) where fertilised in 2013 while the rest of the plots (n = 2 per treatment) were left unfertilised. Fertilisation was carried out by spreading 50g of Osmocote slow release fertiliser pellets per 40x40 cm plot on 07/05/2013. These pellets were not visible anymore in 2015 and therefore the treatment was repeated on 28/05/2015. The experiment was finished after 7 years in 2017.

During every summer growth season, one or more samples were collected for each replicate treatment plot in each year to provide an average value of gross community productivity and % cover per plant species over the peak of each growing season. At the end of the experiment in 2017, the biomass of each plant species in each plot was also measured destructively.

Gross community productivity (GCP, a measure of primary production) was quantified once or more in every year during June, July, August, and/or September (dates given in SM). Gross community productivity (GCP) was estimated as CO2 flux recorded using an LI-840 CO2/H20 gas analyser (LI-COR Biosciences, Lincoln, NE, USA) connected to a clear plexiglass chamber (0.09 m2 internal base area, 0.19 m high, internal volume = 17.1 litres). GCP was estimated using the rate of CO2 flux recorded during consecutive light and dark measurements representing net community productivity (NCP, CO2 utilization by photosynthesis plus CO2 production by respiration) and community respiration (CR, CO2 production during respiration), respectively. GCP was then estimated as GCP = NCP - CR and expressed at the community level as mmol CO2 uptake m-2 h-1. CO2 flux measurements were recorded in a stratified random order between 10:00 h and 14:00 h BST during a neap tidal cycle on days with low cloud cover to minimize imprecision caused by the effect of abiotic factors on photosynthetic rates. In addition, GCP measurements were recorded only where light levels exceeded 700 µmol PPFD m-2 s-1, a previously observed threshold above which variation in ambient light level has minimal impacts on primary production in this salt marsh community.

Total dry-weight biomass by species was measured at the end of the experiment in September 2017 by clipping all vegetation at the soil level. Species biomass could only be estimated before the end of the experiment as this required destructive sampling. To estimate a proxy for total community biomass before the end of the experiment, the abundance of each species in each plot was assessed as % cover using a 0.3 x 0.3 m point quadrat (49 point intersections) in July and/or August. The vegetation cover and GCP were not measured in 2015.