Chewing through challenges: Exploring the evolutionary pathways to wood-feeding in insects.

Decaying wood, while an abundant and stable resource, presents considerable nutritional challenges due to its structural rigidity, chemical recalcitrance, and low nitrogen content. Despite these challenges, certain insect lineages have successfully evolved saproxylophagy (consuming and deriving sustenance from decaying wood), impacting nutrient recycling in ecosystems and carbon sequestration dynamics. This study explores the uneven phylogenetic distribution of saproxylophagy across insects and delves into the evolutionary origins of this trait in disparate insect orders. Employing a comprehensive analysis of gut microbiome data, from both saproxylophagous insects and their non-saproxylophagous relatives, including new data from unexplored wood-feeding insects, this Hypothesis paper discusses the broader phylogenetic context and potential adaptations necessary for this dietary specialization. The study proposes the "Detritivore-First Hypothesis," suggesting an evolutionary pathway to saproxylophagy through detritivory, and highlights the critical role of symbiotic gut microbiomes in the digestion of decaying wood.

True grit? Comparative anatomy and evolution of gizzards in fishes.

Gut morphology frequently reflects the food organisms digest. Gizzards are organs of the gut found in archosaurs and fishes that mechanically reduce food to aid digestion. Gizzards are thought to compensate for edentulism and/or provide an advantage when consuming small, tough food items (e.g., phytoplankton and algae). It is unknown how widespread gizzards are in fishes and how similar these structures are among different lineages. Here, we investigate the distribution of gizzards across bony fishes to (1) survey different fishes for gizzard presence, (2) compare the histological structure of gizzards in three species, (3) estimate how often gizzards have evolved in fishes, and (4) explore whether anatomical and ecological traits like edentulism and microphagy predict gizzard presence. According to our analyses, gizzards are rare across bony fishes, evolving only six times in a broad taxonomic sampling of 51 species, and gizzard presence is not clearly correlated with factors like gut length or dentition. We find that gizzard morphology varies among the lineages where one is present, both macroscopically (presence of a crop) and microscopically (varying tissue types). We conclude that gizzards likely aid in the mechanical reduction of food in fishes that have lost an oral dentition in their evolutionary past; however, the relative scarcity of gizzards suggests they are just one of many possible solutions for processing tough, nutrient-poor food items. Gizzards have long been present in the evolutionary history of fishes, can be found in a wide variety of marine and freshwater clades, and likely have been overlooked in many taxa.

Heat it up to slow it down: Individual energetics reveal how warming reduces stream decomposition.

Research Highlight: Réveillon, T., Rota, T., Chauvet, É., Lecerf, A., & Sentis, A. (2022). Energetic mismatch induced by warming decreases leaf litter decomposition by aquatic detritivores. Journal of Animal Ecology, https://doi.org/10.1111/1365-2656.13710. Global change holds complex consequences for Earth's ecosystems, with global warming simultaneously affecting multiple aspects including individual physiology, population dynamics and ecosystem processes. In a recent study on stream decomposition under global warming, Réveillon, et al. (2022) combined individual-level laboratory assessments of metabolic rates and leaf-litter ingestion with experimentally parameterized consumer-resource models, designed to reveal how stream-detritivore populations respond to combined impacts of warming and declining body size. Their findings of reduced energetic efficiency, weakened detritivore populations and reduced decomposition in warmed streams expand our understanding of how global change mechanistically links changes from the individual to the ecosystem level.

Gut microbiomes of sympatric Amazonian wood-eating catfishes (Loricariidae) reflect host identity and little role in wood digestion.

Neotropical wood-eating catfishes (family Loricariidae) can occur in diverse assemblages with multiple genera and species feeding on the same woody detritus. As such, they present an intriguing system in which to examine the influence of host species identity on the vertebrate gut microbiome as well as to determine the potential role of gut bacteria in wood digestion. We characterized the gut microbiome of two co-occurring catfish genera and four species: Panaqolus albomaculatus, Panaqolus gnomus, Panaqolus nocturnus, and Panaque bathyphilus, as well as that of submerged wood on which they feed. The gut bacterial community did not significantly vary across three gut regions (proximal, mid, distal) for any catfish species, although interspecific variation in the gut microbiome was significant, with magnitude of interspecific difference generally reflecting host phylogenetic proximity. Further, the gut microbiome of each species was significantly different to that present on the submerged wood. Inferring the genomic potential of the gut microbiome revealed that the majority of wood digesting pathways were at best equivalent to and more often depleted or nonexistent within the catfish gut compared to the submerged wood, suggesting a minimal role for the gut microbiome in wood digestion. Rather, these fishes are more likely reliant on fiber degradation performed by microbes in the environment, with their gut microbiome determined more by host identity and phylogenetic history.

Alterations in the sterol signature of detritivorous fish along pollution gradients in the Río de la Plata basin (Argentina): From plant to sewage-based diet.

In order to assess the impact of sewage pollution on the diet of the strict detritivorous and migratory South American fish, Prochilodus lineatus, 16 sterol biomarkers were analyzed by gas chromatography-mass spectrometry from fish muscle (n: 144) collected along 1200 km in the Rio de la Plata basin. Sterol concentrations were fairly homogeneous (2.4 ± 1.3 mg g-1 dry weight), but their proportion in lipids was highly variable and inversely related to both body mass and lipid contents, reflecting the more conservative character of sterols compared to the rapid accumulation of fat as fish grows. As expected, the muscle sterol signature was widely dominated by cholesterol (92 ± 4.5% of total sterols), but it exhibited a remarkable diversity with variable proportions of fecal coprostanol (4.0 ± 4.4%) and plant sterols (3.1 ± 1.9%, e.g. sitosterol and campesterol). Muscle sterols exhibited contrasting geographical differences associated with dietary shifts from plant-derived detritus in the northern reaches of the basin (N: Paraná and Uruguay Rivers), to sewage dominated inputs at Buenos Aires (BA). Fish from BA are fattier (lipids: 35 ± 18 vs. 15 ± 9.0% at N), with higher total sterol contents (2.6 ± 1.3 vs. 1.9 ± 1.0 mg g-1), abundant coprostanol (5.3 ± 4.4 vs. 0.46 ± 1.1%) and lower plant sterols (2.6 ± 1.6 vs 4.6 ± 2.0%), reflecting a diet shifted to anthropogenic organic matter as opposed to vegetal detritus in the north. Accordingly, BA fish presented lower phyto/fecal sterol ratios (0.37 ± 0.21 vs. 0.91 ± 0.12 at N) and higher copro/epicoprostanol ratios (0.95 ± 0.082 vs 0.51 ± 0.25 at N), indicating fresh fecal inputs which provide a valuable supply of easily absorbed organic matter at this site. In addition, the sterol signature allowed to distinguish migratory fish from BA collected 900 km north (previously identified by their pollutant fingerprint and biochemical composition). In fact, coprostanol concentrations show a direct relationship with human populations along the basin, highlighting the usefulness of fecal sterol biomarkers as tracers of polluted fish stocks.

Modification by earthworms of effects of soil heterogeneity and root foraging in eight species of grass.

Spatial heterogeneity of soil nutrients and earthworm activity can each increase the performance of plant species, but their interactive effects have been little studied. The ability of plants to forage for nutrients by concentrating roots where nutrients are concentrated can partly explain the positive effects of nutrient heterogeneity, but whether root foraging can help explain the positive effects of earthworm activity is untested. We conducted a greenhouse experiment in which we grew eight species of Poaceae in homogeneous and heterogeneous soils with or without the earthworms Eisenia fetida and Metaphire guillelmi and measured net accumulation of plant mass and tillers. Effects of heterogeneity and earthworms on plant performance were positive in most species. The presence of earthworms reduced the directly measured effect of heterogeneity on total mass in some grass species. Most species showed root foraging ability. Ability showed no relationship to effects of heterogeneity or earthworms on final total dry mass. However, earthworms reduced foraging in some species, possibly by lessening heterogeneity. Earthworm activity in heterogeneous soil may thus reduce the benefits of root foraging for nutrients in plants.

Influence of larval density and dietary nutrient concentration on performance, body protein, and fat contents of black soldier fly larvae (Hermetia illucens).

Performance and body composition of insect larvae depend on quality and quantity of their diet, and on biotic factors such as larval density. We investigated the effect of dietary nutrient concentration and larval rearing density on survival, development, growth, and protein and fat contents of larvae of the black soldier fly (BSF), Hermetia illucens L. (Diptera: Stratiomyidae). Neonate larvae were fed with a low (NC1), intermediate (NC2), or high nutrient concentration (NC3), and with four rearing densities (50, 100, 200, or 400 larvae per container). Two feeding regimes (FR) were tested: in FR1, the amount of diet added during the experiment was based on the visually estimated larval mass present, whereas in FR2, a fixed feeding ration of 0.6 g of food per larva was applied at the start. FR1 resulted in food limitation, resulting in significantly lower body crude protein content on diet NC1 than on NC2 at larval densities 100 and 200. Larval crude fat content was higher on diets with higher nutrient concentration and at lower larval densities. For FR2, development time was shorter on diets with higher nutrient concentration and at lower larval densities. Individual larval weight and total larval yield increased with higher nutrient concentration at all four larval densities. At lower nutrient concentration, higher larval density resulted in higher individual larval weight and total larval yield, revealing an interaction between larval density and dietary quality. Larval crude protein content was higher at lower densities and lower nutrient concentration. Larval crude fat was higher at higher larval densities and nutrient concentrations. This study indicates that larval protein content is regulated within narrow limits, whereas larval crude fat content is strongly affected by nutrient concentration and by larval density.

When is an herbivore not an herbivore? Detritivory facilitates herbivory in a freshwater system.

Herbivory is thought to be an inefficient diet, but it independently evolved from carnivorous ancestors in many metazoan groups, suggesting that plant-eating is adaptive in some circumstances. In this study, we tested two hypotheses to explain the adaptive evolution of herbivory: (i) the Heterotroph Facilitation hypothesis (herbivory is adaptive because herbivores supplement their diets with heterotrophic microbes); and (ii) the Lipid Allocation hypothesis (herbivory is adaptive because algae, which have high lipid concentrations, are nutritionally similar to carnivory). We tested these hypotheses using enclosure cages placed in the Everglades and stocked with Sailfin Mollies (Poecilia latipinna), a native herbivore. Using shading and phosphorus addition (P), we manipulated the heterotrophic microbe and lipid composition of colonizing epiphyton and examined the effects of varying food quality on Sailfin Molly life history. Epiphyton grown in "shade only" conditions had a 55% increase in bacterial fatty acids and 34% lower ratios of saturated + monounsaturated to polyunsaturated fatty acids relative to the other treatments. Ratio of autotroph to heterotroph biovolume varied throughout the experiment, with a 697% increase at 3 weeks and 98% decrease at 6 weeks compared to the other treatments. Gut contents revealed that fish fed selectively on epiphyton to compensate for apparent deficiencies in the available food. Fish raised in "shade only" cages experienced the highest survival, which was best explained by autotrophic biovolume and algal- and bacterial-derived fatty acids at 3 weeks (2-6× more likely than alternative models with ∆AICc > 2.00), and by percentage of bacterial fatty acids in the diet at 6 weeks (3-8× more likely than alternative models with ∆AICc > 2.00). There were no differences in fish growth among treatments. Autotrophic lipids play a role in early fish life history, but we did not find these to be the best predictors of life history later in the juvenile period. Instead, heterotrophic lipids facilitated the herbivorous diet and enhanced survival of juvenile fish in our experiment. Bacterial fatty acid content of the diet promoted herbivore survival, consistent with the Heterotroph Facilitation hypothesis. This is the first study to explicitly contrast Heterotrophic Facilitation and Lipid Allocation hypotheses for the adaptive evolution of herbivory in an aquatic system.

A functional evaluation of feeding in the surgeonfish Ctenochaetus striatus: the role of soft tissues.

Ctenochaetus striatus is one of the most abundant surgeonfishes on Indo-Pacific coral reefs, yet the functional role and feeding ecology of this species remain unclear. This species is reported to possess a rigid structure in its palate that is used for scraping, but some authors have reported that this element is comprised of soft tissue. To resolve the nature and role of this structure in the feeding ecology of C. striatus we examined evidence from anatomical observations, scanning electron microscopy, histology, X-ray micro-computed tomography scanning, high-speed video and field observations. We found that C. striatus from the Great Barrier Reef possess a retention plate (RP) on their palates immediately posterior to the premaxillary teeth which is soft, covered in a thin veneer of keratin with a papillate surface. This RP appears to be used during feeding, but does not appear to be responsible for the removal of material, which is achieved primarily by a fast closure of the lower jaw. We infer that the RP acts primarily as a 'dustpan', in a 'dustpan and brush' feeding mechanism, to facilitate the collection of particulate material from algal turfs.

Unpacking brown food-webs: Animal trophic identity reflects rampant microbivory.

Detritivory is the dominant trophic paradigm in most terrestrial, aquatic, and marine ecosystems, yet accurate measurement of consumer trophic position within detrital (="brown") food webs has remained unresolved. Measurement of detritivore trophic position is complicated by the fact that detritus is suffused with microbes, creating a detrital complex of living and nonliving biomass. Given that microbes and metazoans are trophic analogues of each other, animals feeding on detrital complexes are ingesting other detritivores (microbes), which should elevate metazoan trophic position and should be rampant within brown food webs. We tested these hypotheses using isotopic (15N) analyses of amino acids extracted from wild and laboratory-cultured consumers. Vertebrate (fish) and invertebrate detritivores (beetles and moths) were reared on detritus, with and without microbial colonization. In the field, detritivorous animal specimens were collected and analyzed to compare trophic identities among laboratory-reared and free-roaming detritivores. When colonized by bacteria or fungi, the trophic positions of detrital complexes increased significantly over time. The magnitude of trophic inflation was mediated by the extent of microbial consumption of detrital substrates. When detrital complexes were fed to vertebrate and invertebrate animals, the consumers registered similar degrees of trophic inflation, albeit one trophic level higher than their diets. The wild-collected detritivore fauna in our study exhibited significantly elevated trophic positions. Our findings suggest that the trophic positions of detrital complexes rise predictably as microbes convert nonliving organic matter into living microbial biomass. Animals consuming such detrital complexes exhibit similar trophic inflation, directly attributable to the assimilation of microbe-derived amino acids. Our data demonstrate that detritivorous microbes elevate metazoan trophic position, suggesting that detritivory among animals is, functionally, omnivory. By quantifying the impacts of microbivory on the trophic positions of detritivorous animals and then tracking how these effects propagate "up" food chains, we reveal the degree to which microbes influence consumer groups within trophic hierarchies. The trophic inflation observed among our field-collected fauna further suggests that microbial proteins represent an immense contribution to metazoan biomass. Collectively, these findings provide an empirical basis to interpret detritivore trophic identity, and further illuminate the magnitude of microbial contributions to food webs.

Fatty acid alterations in the detritivorous Prochilodus lineatus promoted by opportunistic feeding on sewage discharges in the Río de la Plata estuary.

Muscle fatty acid profiles and PCB contents of the detritivorous species Prochilodus lineatus and its diet (stomach contents, settling particles and sediments) were analysed from reference and polluted areas of the Paraná-Rio de la Plata basin, to evaluate the alterations produced by opportunistic feeding on sewage discharges. Overall muscle fatty acid composition was dominated by saturated and monounsaturated 16 and 18 carbon (18 C-FA) components with reduced long-chain polyunsaturated fatty acids (LC-PUFA). Compared to sediments, settling particles and stomach contents were enriched in lipids and had a similar fatty acid composition. Opportunistic feeding on sewage detritus at Buenos Aires resulted in enhanced PCB and triglyceride accumulation, with higher proportions of 18 C-FA and lower proportions of 16:1 and LC-PUFA compared to fish from northern pristine reaches of the basin. Mid-Paraná showed intermediate values reflecting mixing of the North stock with migrating Buenos Aires P. lineatus identified by their lipid and contaminant profile. According to multivariate analyses, this geographical variation of fatty acid composition was strongly influenced by PCB concentration. Prochilodus lineatus assimilates the energy subsidy of sewage inputs through enhanced lipogenesis with dominant 18 C-FA and significant amounts of valuable LC-PUFA. This lipid alteration facilitates the bioaccumulation of PCBs which in turn may reinforce the adipogenic effect of sewage feeding.

Feeding and body condition of an invasive fish species under different environmental conditions

Diet, energy density (ED) and relative condition factor (Kn ) were used to investigate the energetic assimilation of the invasive fish Hemiodus orthonops under different environmental condition of the upper rio Paraná floodplain. Samples were taken in June and September 2013 and 2014. Nutrient content was determined for sediment. The diet was combined in the Food Index (IAi%), ED was expressed in Kcal/g of dry weight and Kn was calculated by: Kn = Wt/We, where Wt is the total weight and We the expected weight. Detritus/sediment prevailed in the stomachs of specimens from Ivinhema and Baia, while Algae was the main item in Paraná, reflecting the resource availability. ED and Kn from Ivinhema specimens were the greatest, consequence of the quality of food and lower spent on searching and handling food. The Paraná specimens showed lower ED values, but higher Kn values, due to algae consumption, a nutrient-rich resource. Baia presented high aluminum concentration on the sediment and the lower pH values, which contribute to reduce the nutritional value of the detritus and the ED and Kn values of their specimens. In conclusion, H.orthonops is capable to take advantage of the resources availability in the different environments, ensuring their establishment.

Análise de dieta, densidade energética (DE) e fator de condição relativo (Kn ) foram utilizados para investigar a assimilação energética do peixe invasor Hemiodus orthonops sob diferentes condições ambientais da planície de inundação do alto rio Paraná. As coletas ocorreram em junho e setembro de 2013 e 2014. O teor de nutrientes foi obtido para o sedimento. A dieta foi combinada no Índice Alimentar (IAi%), a DE foi expressa em Kcal/g de peso seco, o Kn foi calculado através de: Kn = Wt/We, onde Wt é o peso total e We o peso esperado. Detrito/sedimento prevaleceu nos estômagos dos espécimes do Ivinhema e Baía, enquanto Alga foi o principal item no Paraná, refletindo a disponibilidade de recursos. A DE e Kn dos indivíduos do Ivinhema foram os maiores, consequência da qualidade do alimento e do menor gasto em procura e manipulação do alimento. Os indivíduos do Paraná registraram os menores valores de DE, mas elevados valores de Kn , devido ao consumo de alga, um recurso alimentar rico em nutrientes. Baía apresentou elevada concentração de alumínio no sedimento e reduzidos valores de pH, o que contribuiu com a redução do valor nutricional do detrito e dos valores de DE e Kn dos indivíduos. Concluindo, H. orthonops é capaz de se beneficiar da disponibilidade de recursos nos diferentes ambientes, garantindo seu estabelecimento.

Endogenous cellulase production in the leaf litter foraging mangrove crab Parasesarma erythodactyla.

The sesarmid crab Parasesarma erythodactyla consumes large amounts of mangrove leaf litter but its biochemical capacity for cellulose digestion is poorly known. We demonstrate the presence of endo-ß-1,4-glucanase, ß-glucosidase and total cellulase activities in the digestive juice of this crab. The highest total cellulase activity was observed at mildly acidic pH (5 to 6) and temperature between 30 and 50°C. A 1752bp cDNA containing an open reading frame of 1386bp encoding a putative endo-ß-1,4-glucanase (EG) of 461 amino acids was identified in the crab's hepatopancreas using polymerase chain reaction (PCR), cloning and sequencing techniques. P. erythodactyla endo-ß-1,4-glucanase (PeEG) contains a glycosyl hydrolase family 9 (GHF9) catalytic domain with all catalytically important residues conserved, and shows high sequence identity to GHF9 EGs reported from other arthropods. The endogenous origin of PeEG was confirmed by PCR amplification of a ~1.5kb DNA fragment, containing a phase 1 intron flanked by two exon sequences identical to the cDNA, from genomic DNA isolated from the crab's muscle tissue. PeEG encoding cDNA is the first endogenous EG sequence reported from the brachyuran crabs. Using degenerate primers, we also isolated 204bp cDNA fragments with sequences affiliated to EG from the hepatopancreas of eight other mangrove crabs of the Sesarmidae (Neosarmatium trispinosum and Sesarmoides borneensis), Macrophthalmidae (Ilyograpsus daviei, Australoplax tridentata, and Macrophthalmus setosus), Varunidae (Pseudohelice subquadrata), Heloeciidae (Heloecius cordiformis), and Ocypodidae (Uca perplexa) families, suggesting that endogenous cellulase production may be a common characteristic among the detritivorous mangrove crabs.

Larval biology of anthophagous Eumaeini (Lepidoptera: Lycaenidae, Theclinae) in the cerrado of central Brazil.

The biology and morphology of the early stages of 22 species of Eumaeini (Lepidoptera: Lycaenidae, Theclinae) are presented. Observations were collected through the inspection of inflorescences in the field and the rearing of 214 larvae in laboratory. Allosmaitia strophius (Godart) associated with Malpighiaceae species and the polyphagous Strymon mulucha (Hewitson) were the most frequently collected species. Detritivory was observed in two species, Electrostrymon endymion (F.) and Kisutam syllis (Godman & Salvin), and myrmecophily in four other species, A. strophius, Ministrymon azia (Hewitson), Parrhasius polibetes (Stoll), and S. mulucha. Cannibalism was observed in A. strophius; in addition, the pupa of this and of three other species produced audible sounds. Paiwarria aphaca (Hewitson) was highlighted because of the great difference observed between its first and last instars, as well as the marked difference between that species and the larvae of Paiwarria umbratus (Geyer) documented in Costa Rica. Larvae of Calycopis mimas (Godman & Salvin) displayed "bungee jumping" behavior when stimulated. Parasitoids (Diptera, Hymenoptera) attacked 21 larvae of eight species, A. strophius, K. syllis, M. azia, Pai. aphaca, P. polibetes, Rekoa marius (Lucas), S. mulucha, and Tmolus venustus (H.H. Druce). Illustrations of immatures and parasitoids are provided.

Astyanax paranae Eigenmann, 1914 (Characiformes: Characidae) in the Alagados Reservoir, Paraná, Brazil: diet composition and variation

Aspects of the feeding ecology of a small characin, Astyanax paranae, were studied during 1996/1997 and 1998/1999 in the Alagados Reservoir, Paraná, Brazil (25º01'50.0'' S; 050º03'41.9'' W). Fishes were quarterly captured from the reservoir's riverine and lacustrine zones and stomachs contents of 711 adult individuals were analyzed by volumetric method. Species' feeding spectrum and spatial, temporal and sexual variations on diet were evaluated. Data matrix was summarized by detrented correspondence analysis (DCA) and the axes scores from DCA were used as variables in one-way ANOVA of null models to test diet variations. Astyanax paranae fed on detritus/sediment, plant matter, algae and aquatic and terrestrial invertebrates. The time-space prevalence of detritus/sediment and plant matter on diet characterized the feeding habit as detritivorous tending to herbivory. Significant differences on food items proportions occurred between the sampling months and sampling sites and were related to resources availability, characterizing the species trophic opportunism.

Aspectos da ecologia alimentar de um pequeno caracídeo, Astyanax paranae, foram estudados durante 1996/1997 e 1998/1999 no reservatório de Alagados, Paraná, Brasil (25º01'50,0'' S; 50º03'41,9'' W). Os peixes foram capturados trimestralmente nas zonas fluvial e lacustre do reservatório e os conteúdos gástricos de 711 espécimes adultos foram analisados através do método volumétrico. Foram avaliados o espectro alimentar da espécie e alterações espaciais, temporais e entre os sexos na dieta. A matriz de dados foi sumarizada através da análise de correspondência com remoção do efeito do arco (DCA) e os escores dos eixos resultantes da DCA utilizados como variáveis em análises de variância (ANOVA) unifatoriais de modelos nulos para testar diferenças na dieta. Astyanax paranae consumiu detrito/sedimento, vegetais, algas e invertebrados aquáticos e terrestres. O predomínio espaço-temporal de detrito/sedimento e vegetais na dieta indicou hábito alimentar detritívoro com tendência a herbivoria. Diferenças significativas na proporção dos itens alimentares ocorreram entre os meses e locais amostrados, tendo sido relacionadas à disponibilidade dos recursos, caracterizando o oportunismo trófico da espécie.