DOI: 10.5061/dryad.sqv9s4n40
title: Changes in salt marsh detritivore identity influences on ecosystem multifunctionality

description: Ecosystems world-wide experience changes in species composition in
 response to natural and anthropogenic changes in environmental conditions.
  Research to date has greatly improved our understanding of how
 species affect focal ecosystem functions.  However, because
 measurements of multiple ecosystem functions have not been consistently
 justified for any given trophic group, it is unclear whether
 interpretations of research syntheses adequately reflect the contributions
 of consumers to ecosystems.  Using model communities assembled in
 experimental microcosms, we examined the relationship between four
 numerically dominant detritivore species and six ecosystem functions that
 underpin fundamental aspects of carbon and nitrogen cycling above- and
 below-ground.  We tested whether ecosystem responses to changes
 in detritivore identity depended upon species trait dissimilarity, food
 web compartment (aboveground, belowground, mixed), or number of responses
 considered (one to six). We found little influence of detritivore species
 identity on brown (i.e. soil-based) processes.  Only one of four
 detritivore species uniquely influenced decomposition, and detritivore
 species did not vary in their influence on soil nitrogen pools (NO3- and
 NH4+), or root biomass.  However, changes in detritivore identity
 influenced multiple aboveground ecosystem functions.  That is, by
 serving as prey, ecosystem engineers, and occasionally also as herbivores
 as well as detritivores, these species altered the strength of aboveground
 predator-herbivore interactions and plant-shoot biomass.  Yet,
 dissimilarity of detritivore functional traits was not associated with
 dissimilarity of ecosystem functioning.  These results serve as
 an important reminder that consumers influence ecosystem processes via
 multiple energy channels and that food web interactions set important
 context for consumer-mediated effects on multiple ecosystem
 functions.  Given that species are being lost, gained, and
 redistributed at unprecedented rates, we can anticipate that changes in
 species identity will have additional ecosystem consequences beyond those
 predicted by species’ primary functional role.
description: <i>Experimental design: </i>To determine the
 influence of changes in detritivore species on multiple ecosystem
 functions, we established 5 detritivore treatments in microcosms.  Species
 densities were chosen to fall within the range of naturally variable field
 densities, and also to establish communities with comparable detritivore
 biomasses: no detritivore, 50 <i>Littorophiloscia vittata</i>,
 50 <i>Orchestia grillus</i>, 50 <i>Melampus bidentatus,
 </i>or 5 <i>Littoraria irrorata</i>) (Graça et al. 2000,
 Zimmer et al. 2002, 2004).  These microcosm densities correspond to 52
 <i>Pardosa</i> m<sup>-2</sup>, 130
 <i>Littoraria </i>m<sup>-2</sup>, and 1315
 individuals m<sup>-2</sup> for each the species stocked at 50
 individuals per microcosm.  To tease apart the influences of detritivores
 that are realized via nutrient/decomposition pathways from influences on
 ecosystem functioning that are a consequence of their role as prey (Hines
 and Gessner 2012, Hines et al. 2015), the detritivore treatments were
 crossed with two levels of spider predation (4 <i>Pardosa littoralis
 </i>present or absent).  The full experimental was a randomized
 complete block, 5 ⅹ 2 factorial design experiment, which consisted of 10
 treatments that were replicated in each of 9 spatial blocks, resulting in
 90 microcosms. The experiment was located in a common garden habitat, at
 the Smithsonian Environmental Research Center in Edgewater, MD. 
    Each microcosm consisted of a sand-filled pot (22 cm
 diameter x 21 cm deep) with five transplants of small <i>Spartina
 </i>plants, 25 g <i>S. alterniflora </i>leaf litter, and
 30 adult <i>Prokelisia </i>herbivores<i> </i>(25
 females and 5 males, corresponding to 825 individuals
 m<sup>-2</sup>).  Potted plants were enclosed in clear plastic
 tube cages (21.5 cm diameter x 30 cm tall), capped with a mesh top, and
 pots were placed in plastic pans (30 cm diameter x 10 cm deep) filled with
 water.  Treatments were established in a sequential fashion that
 approximated the phenology of field interactions.  Detritivore species,
 which remain in meadow habitats year-round, were added on 7 June 2007 and
 were allowed to settle and feed before herbivores emerged. 
 <i>Prokelisia </i>herbivores, which overwinter as nymphs in
 leaf litter and emerge as adults by the end of June, were added to
 microcosms on 25-27 June 2007 and allowed to settle for 4 days, before 4
 juvenile <i>Pardosa </i>spiders were added to half of the
 microcosms. The experiment was terminated on day 60,
 when visual counts indicated that the second generation adult planthoppers
 began a slight natural decline (Denno and Roderick 2003).  Because
 detritivores and spiders were often hidden in the leaf litter, it was not
 possible to obtain a visual assessment of their densities throughout the
 course of the experiment.  Therefore, final invertebrate densities were
 obtained by collecting all animals from microcosms using a vacuum sampler
 fitted with mesh bags (Shop-vac®, Williamsport, PA, USA).  Arthropods were
 killed using ethyl acetate, transferred into plastic bags, before they
 were counted in the laboratory.  To assess plant growth
 and litter mass loss, <i>S. alterniflora </i>litter, root, and
 shoot biomass was harvested, washed and sieved through 1.7 mm sieves,
 freeze-dried, and weighed to the nearest 0.01 g.  Because damage imposed
 by phloem feeders can be difficult to detect, we did not distinguish
 between loss of plant biomass caused by detritivore grazing and phloem
 feeding herbivores.  Instead, herbivore abundance was used as a proxy for
 herbivory by strict herbivores, which is in line with rationale for energy
 flux to herbivores (Barnes et al. 2018, Gauzens et al. 2019), but could
 overlook the potential for non-linear density dependent feeding rates
 (Hines et al. 2016) or non-consumptive effects of predators (Peckarsky et
 al. 2008).  That is, herbivory was considered as ability of the ecosystem
 to support two generations of herbivore populations during the course of
 the experiment, and is a proxy related to secondary production of
 herbivores.  <i>Pardosa </i>predators molted to adults but,
 due to longer generation times, they did not reproduce during the time
 course of the experiment.  Nonetheless, for consistency, we also consider
 persistence of predators as a measure of predation potential.  Soil
 inorganic soil nitrogen
 (NH<sub>4</sub><sup>+</sup> and
 NO<sub>3</sub><sup>-</sup>) was extracted using
 2.0 M KCL (Mulvaney 1996).  <i>Statistical
 analysis: </i> We used a mixed model ANOVA (lme4: Bates et al. 2014)
 to assess the influence two fixed factors (<i>i.e.
 </i>detritivore identity and predator presence) on six individual
 functions as well as ecosystem multifunctionality.  For all analyses, the
 microcosm was considered as the experimental unit in which response
 variables were reported and spatial block was included as a random
 factor.  To calculate average ecosystem multifunctionality, we used the
 averaging approach (Byrnes et al. 2014), and included the average of all
 possible reported response variables in each microcosm (shoot biomass,
 root biomass, litter decomposition rate <i>k</i>, nutrient
 concentration [NO<sub>3</sub><sup>-</sup>],
 herbivore abundance, predator abundance).  Predator abundance was not
 included in the calculation when predators were absent.  Because
 standardized nutrient concentrations of
 NH<sub>4</sub><sup>+</sup> and
 NO<sub>3</sub><sup>-</sup> were similar, and
 neither molecule was sensitive to treatments in this experiment, we chose
 to report NO<sub>3</sub><sup>-</sup> in the
 average ecosystem multifunctionality metric and text.
 We used another mixed model analysis to consider how two
 additional factors (<i>i.e. </i>food web compartment, and
 number of functions included in the average multifunctionality metric)
 influenced the average multifunctionality responses in the original 2 ⅹ 5
 factorial experimental.  In this analysis, we calculated average
 multifunctionality for each microcosm using all viable combinations of 1,
 2, 3, 4, 5, and 6 standardized functions that filled the criteria of being
 from aboveground compartment, belowground compartment, or mixed
 compartment multifunctionality metric that included a combination of at
 least one aboveground and one belowground function.  The experimental
 design was necessarily unbalanced as some combinations of covariate
 calculations were not possible (e.g. mixed aboveground-belowground
 compartment with only one function, or aboveground compartment with three
 functions when predators were absent); For this analysis, we were
 interested in how the number of functions and/ or the focal compartment
 influenced variation in multi-functionality results, rather than the
 specific combination of functions included in calculations for each
 microcosm. Therefore, we included the identity of function combinations in
 the model as a random factor.  Spatial block was also included in the
 model as a random factor.  All data met assumptions of homogeneity of
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