Ecosystem functions greatly depend on trophic interactions between consumers and their resources. Resource consumption depends on ingestion, digestion, and allocation processes. Mechanical constraints are expected to influence ingestion, while metabolic and nutritional constraints are expected to influence allocation. Leaf litter are resources presenting a high mechanical and nutritional heterogeneity that depends on plant identity and on physical and microbial processing over the course of decomposition. Litter consumption by detritivores is known to depend on metabolic and nutritional constraints but the importance of mechanical constraints is yet unknown. After accounting for metabolic constraints on consumption rate, we tested the relative importance of mechanical and nutritional constraints in explaining litter consumption rates by detritivores. For this, we exposed 16 leaf treatments (8 leaf species either just leached or leached and microbially conditioned) to 4 aquatic and 5 terrestrial detritivore taxa in laboratory no-choice consumption experiments. We investigated two mechanical constraints: grabbing and fragmenting the resource, by measuring suitable couples of mechanical traits for both litter and detritivores. We also investigated four nutritional constraints related to N, P, K, and Ca contents in both detritivores and litter. For each constraint, we also tested if trait matching significantly contribute to explain consumption. Our analysis revealed that both mechanical and nutritional constraints are influencing mass-independent consumption rate but that mechanical constraints predominate over nutritional constraints. Litter fragmentation, studied through litter toughness and detritivore biting force, was especially important to explain consumption rate. Nutritional constraints were dominated by P constraints. Trait-matching had very weak importance and was significant only for P constraints. Our findings highlight the importance of mechanical constraints for litter consumption by detritivores.

This dataset is based on consumption tests: In small plastic boxes we quantified the consumption rate of a given litter by a given detritivore individual. Detritivore species and leaf litter batches were characterized by the measurements of traits.

Experimental design

We selected 8 leaf litter species with a large range of mechanical and nutritional trait values to cover a wide spectrum of potentially different constraints. Each leaf litter species was then either just leached, or leached and microbially conditioned before being offered to detritivores. This ensured enlarging the range of initial mechanical and nutritional litter traits values while limiting the content of chemical deterrents. We performed leaf litter consumption tests by offering one of 16 different leaf litter types to one of 9 macrodetritivore taxa (four aquatic and five terrestrial species). Detritivore taxa were chosen to be representative of coarse lifeforms commonly encountered in aquatic and terrestrial ecosystems. As we aimed to assess fundamental rules of pairwise interactions between detritivores and litter, we tested the consumption of a single litter by a single detritivore individual at the time. We also offered litter species that detritivores could not encounter in their natural habitat. We thus sampled litter in a geographical site (Canal du Midi: Toulouse, 31000 and Ramonville-Sainte-Agne, 31520, France) distant from the geographical sites where we sampled detritivores (Montagne Noire, France). We performed a total of 576 consumption tests, corresponding to 144 detritivore-litter pairs: 9 detritivores taxa * 16 litter treatments (8 leaf litter species * 2 litter conditioning treatments (leaching or leaching plus microbial conditioning)) * 4 replicates. Replicates spread out from week to week and were associated with corresponding control tests without detritivores (Supplementary Material, Table S3). We performed a total of 128 control tests without detritivores: 16 litter treatments (8 litter species * 2 litter conditioning treatments (leaching or microbial conditioning)) * 2 ecosystem types (aquatic or terrestrial) * 4 replicates.

We performed consumption tests in microcosms made of clean plastic containers with 50 g of clean sand in the dark at 10°C. For aquatic detritivores, we added 200 mL of water collected from their stream. For terrestrial ones, we sprayed 5 mL of tap water on the sand. We starved detritivores for 3 days prior to the consumption test. In each microcosm we placed one individual (assigned randomly) and five discs of one litter treatment (litter species * conditioning treatment) that were previously freeze-dried, weighted, and rehydrated in tap water for 1 h. Tests were stopped when consumption visually reached 75% of initial discs surface or after three days. At the end of the consumption tests, remaining discs fragments larger than 1 mm were collected, freeze-dried and weighted. When one individual died during the first 24 h of the test, we immediately replaced it with a new individual. When the individual died later during the test, we repeated the consumption test the week after, with corresponding control treatments. At the end of consumption tests, detritivores were starved for 24 h, and were weighted (aquatic animals were gently blotted with paper towel). We converted fresh body mass into dry mass using a linear relationship established for each taxon (See Macrodetritivores’ section). For each detritivore taxon, we conserved half of the individuals in 70% ethanol for dissection and we froze the other half for chemical analyses. All weight measurements were determined at the nearest 0.1 mg.

Leaf Litter

We collected dead leaves at abscission from October to November along the Canal du Midi (Toulouse, 31000, and Ramonville-Sainte-Agne, 31520, France) from a limited number of individuals (£ 5) for each species. We used 8 tree species belonging to 8 different families, namely Ailanthus altissima (Simaroubacea), Robinia pseudoacacia (Fabacea), Juglans regia (Juglandacea), Carpinus betulus (Betulacea), Acer platanoides (Aceracea), Prunus avium (Rosacea), Quercus petrea (Fagacea), Platanus ×hispanica (Platanacea). Leaves were air-dried and stored in the dark until being leached with tap water during 24 h. We then cut 1-cm diameter leaf discs with a cork-borer, avoiding main veins. Some leached discs were microbially conditioned. They were incubated in a mix of decomposing dead leaves until they were visually microbially colonized (soft and discolored). For aquatic conditioning specifically, we collected 50 L of stream water and dead leaves from the same stream where we collected aquatic individuals. We added Fertiligène Naturen® fertilizer (NPK: 3 – 2 – 5) at 0.5 mL.L^-1. We left it three days in a greenhouse with constant oxygenation for microorganisms’ development. We then filled tanks with filtered (63 mm) water and placed one fine-mesh bag of monospecific litter discs of each litter species per tank with constant oxygenation. For terrestrial conditioning, we collected dead leaves from Montagne Noire forest soil (beech, chestnut, hazelnut) and grinded it with a garden shredder. We left it three days in a green house after humidification with the same fertilizer at 0.5 mL.L^-1. We then placed monospecific leaf discs in a fine-mesh bag of each litter species between two layers of fragmented litter in each tank. Tanks were regularly humidified with the same fertilizer.

To test for mechanical constraints of grabbing and fragmenting litter, we measured thickness and toughness on 8 discs from controls, respectively. We measured limb thickness to the nearest 0.001 mm with a Helios-Preisser® digital micrometer, avoiding main veins. We measured litter toughness as the penetration pressure (kPa) needed for a 2.2-mm diameter steel rod to penetrate through a leaf disc. We used a custom-made penetrometer, such as described in Graça et al. (2005), fitted to a digital force tester (CS225 Series, Chatillon®) measuring force to the nearest 0.1 N. To test for nutritional constraints, we quantified nitrogen (N) content using a Total nitrogen and Organic Carbon analyzer (TOC L, Shimadzu) on three replicates of 20 mg. We quantified phosphorus (P), potassium (K) and calcium (Ca) content with an Induced Coupled Plasma – Mass Spectrometer (ICP-MS) on three replicates of 5 mg.

Macrodetritivores

We collected macrodetritivores in la Montagne Noire, a metamorphic forested massif east of Toulouse (France) (Supplementary Material, Table S1 and Table S2). We hand-captured aquatic detritivores from February to March in a stream mainly boarded by beech (Fagus sp.), hazelnut (Corylus sp.), and chestnut (Castanea sp.) trees. We hand-captured terrestrial detritivores in April in a site dominated by ash (Fraxinus sp.). We identified all taxa to the lowest taxonomic level, mostly species. Only Plecoptera and Tipula larvae were identified to the genus, Nemoura and Tipula, respectively (Tachet et al., 2010). Case-bearing Trichoptera larvae were identified as Potamophylax cingulatus (Stephens, 1837) (Waringer and Graf, 2011), and Amphipods as Gammarus fossarum (Koch, 1835) (Tachet et al., 2010). Terrestrial detritivores were either Isopods (Philoscia affinis (Verhoeff, 1908) and Porcellio monticola (Lereboullet, 1853)) (Oliver and Meechan, 1993; Vandel, 1962) or Diplopods (Cylindroiulus londinensis (Leach, 1815), Polydesmus inconstans (Latzel, 1884), and Glomeris marginata (Villiers, 1789)) (Blower, 1985; David, 1995). At the laboratory we sorted them by taxon, and left them 1 – 3 days in the dark at 10°C for acclimatation before being starved.

We performed dissections on at least five individuals per taxon, from several random experimental conditions, under an Olympus SZX10 stereomicroscope equipped with a digital camera. To assess the ability of detritivores to overcome litter thickness constraints, we measured mandible gape (distance between the axis of rotation of both mandibles; Supplementary Material, Figure S1) to the nearest 0.01 mm. To asses biting force as the ability to overcome litter toughness, we measured head width (H_W, behind the eyes), mandible length (M_L, distance between the incisive tip and the axis of rotation which was identified with condyles), and mandible width (M_W, distance between the adductor muscle insertion and the axis of rotation) to the nearest 0.01 mm (Clissold, 2007; Supplementary Material, Figure S1). We used these metrics to calculate an index of biting force at the taxa level (F, (Brousseau et al., 2018; Wheater and Evans, 1989)): F = H_W * M_W / M_L

To assess metabolic constraints, we converted detritivore fresh body mass into dry mass using a linear relationship established for each taxon with a subset of individuals both fresh- and freeze-dry-weighted (n ≥ 30, p < 0.001, R² ≥ 0.57). Other individuals were only fresh-weighted before being conserved in 70%-ethanol for dissection. Their dry mass was then inferred with the estimated linear relationship. To assess nutritional constraints, four pools of at least four individuals for each detritivore taxon (resulting in a total of four analytical replicates per taxon) were grinded into powder and analyzed following the same procedure as for litter samples. For Nemoura alone, only two pools were analyzed due to the very small body weight of this taxon.