Predator responses to prey camouflage strategies: a meta-analysis.

Although numerous studies about camouflage have been conducted in the last few decades, there is still a significant gap in our knowledge about the magnitude of protective value of different camouflage strategies in prey detection and survival. Furthermore, the functional significance of several camouflage strategies remains controversial. Here we carried out a comprehensive meta-analysis including comparisons of different camouflage strategies as well as predator and prey types, considering two response variables: mean predator search time (ST) (63 studies) and predator attack rate (AR) of camouflaged prey (28 studies). Overall, camouflage increased the predator ST by 62.56% and decreased the AR of prey by 27.34%. Masquerade was the camouflage strategy that most increased predator ST (295.43%). Background matching and disruptive coloration did not differ from each other. Motion camouflage did not increase ST but decreases AR on prey. We found no evidence that eyespot increases ST and decreases AR by predators. The different types of predators did not differ from each other, but caterpillars were the type of prey that most influenced the magnitude of camouflage's effect. We highlight the potential evolutionary mechanisms that led camouflage to be a highly effective anti-predatory adaptation, as well as potential discrepancies or redundancies among strategies, predator and prey types.

Warming and top predator loss drive direct and indirect effects on multiple trophic groups within and across ecosystems.

The interspecific interactions within and between adjacent ecosystems strongly depend on the changes in their abiotic and biotic components. However, little is known about how climate change and biodiversity loss in a specific ecosystem can impact the multiple trophic interactions of different biological groups within and across ecosystems. We used natural microecosystems (tank-bromeliads) as a model system to investigate the main and interactive effects of aquatic warming and aquatic top predator loss (i.e. trophic downgrading) on trophic relationships in three integrated food web compartments: (a) aquatic micro-organisms, (b) aquatic macro-organisms and (c) terrestrial predators (i.e. via cross-ecosystem effects). The aquatic top predator loss substantially impacted the three food web compartments. In the aquatic macrofauna compartment, trophic downgrading increased the filter feeder richness and abundance directly and indirectly via an increase in detritivore richness, likely through a facilitative interaction. For the microbiota compartment, aquatic top predator loss had a negative effect on algae richness, probably via decreasing the input of nutrients from predator biological activities. Furthermore, the more active terrestrial predators responded more to aquatic top predator loss, via an increase in some components of aquatic macrofauna, than more stationary terrestrial predators. The aquatic trophic downgrading indirectly altered the richness and abundance of cursorial terrestrial predators, but these effects had different direction according to the aquatic functional group, filter feeder or other detritivores. The web-building predators were indirectly affected by aquatic trophic downgrading due to increased filter feeder richness. Aquatic warming did not affect the aquatic micro- or macro-organisms but did positively affect the abundance of web-building terrestrial predators. These results allow us to raise a predictive framework of how different anthropogenic changes predicted for the next decades, such as aquatic warming and top predator loss, could differentially affect multiple biological groups through interactions within and across ecosystems.

As interações interespecíficas dentro e entre ecossistemas adjacentes dependem fortemente das mudanças de seus componentes abióticos e bióticos. Entretanto, pouco se sabe sobre como mudanças climáticas e a perda de biodiversidade em um ecossistema específico pode impactar as múltiplas interações tróficas de diferentes grupos biológicos dentro e entre ecossistemas. Nós utilizamos micro ecossistemas naturais (bromélias-tanque) como sistema modelo para investigar os efeitos individuais e interativos do aquecimento e da perda de predadores aquáticos (simplificação trófica) nas relações tróficas em três compartimentos integrados da teia alimentar: i) micro-organismos aquáticos, ii) macroorganismos aquáticos e iii) predadores terrestres (via efeito entre ecossistemas). A perda de predadores de topo aquáticos afetou substancialmente os três compartimentos da rede trófica. No compartimento da macrofauna aquática, a simplificação trófica aumentou a riqueza e abundância de filtradores, direta e indiretamente, por meio de um aumento da riqueza de espécies de detritívoros, provavelmente através de uma interação de facilitação. Para o compartimento da microbiota, a perda de predadores de topo aquáticos teve um efeito negativo sobre a riqueza de espécies de algas, provavelmente por meio da diminuição da entrada de nutrientes provenientes das atividades biológicas dos predadores. Além disso, os predadores terrestres mais ativos responderam mais à perda de predadores de topo aquáticos, por meio de um aumento de alguns componentes da macrofauna aquática, do que predadores terrestres mais estacionários. A simplificação trófica aquática alterou indiretamente a riqueza e abundância de predadores cursoriais terrestres, mas esses efeitos tiveram direção diferente de acordo com o grupo funcional aquático, filtradores ou outros detritívoros. Os predadores construtores de teias foram indiretamente afetados pela simplificação trófica aquática devido ao aumento da riqueza de filtradores. O aquecimento aquático não afetou os micro ou macro organismos aquáticos, mas afetou positivamente a abundância de predadores terrestres construtores de teias. Esses resultados nos permitem levantar um quadro preditivo de como diferentes mudanças antropogênicas preditas para as próximas décadas, como o aquecimento e a perda de predadores de topo aquáticos, podem afetar diferencialmente vários grupos biológicos por meio de interações dentro e entre os ecossistemas.

Geographical and experimental contexts modulate the effect of warming on top-down control: a meta-analysis.

Ecologists have extensively investigated the effect of warming on consumer-resource interactions, with experiments revealing that warming can strengthen, weaken or have no net effect on top-down control of resources. These experiments have inspired a body of theoretical work to explain the variation in the effect of warming on top-down control. However, there has been no quantitative attempt to reconcile theory with outcomes from empirical studies. To address the gap between theory and experiment, we performed a meta-analysis to examine the combined effect of experimental warming and top-down control on resource biomass and determined potential sources of variation across experiments. We show that differences in experimental outcomes are related to systematic variation in the geographical distribution of studies. Specifically, warming strengthened top-down control when experiments were conducted in colder regions, but had the opposite effect in warmer regions. Furthermore, we found that differences in the thermoregulation strategy of the consumer and openness of experimental arenas to dispersal can contribute to some deviation from the overall geographical pattern. These results reconcile empirical findings and support the expectation of geographical variation in the response of consumer-resource interactions to warming.

Warming and top predator loss drive ecosystem multifunctionality.

Global change affects ecosystem functioning both directly by modifications in physicochemical processes, and indirectly, via changes in biotic metabolism and interactions. Unclear, however, is how multiple anthropogenic drivers affect different components of community structure and the performance of multiple ecosystem functions (ecosystem multifunctionality). We manipulated small natural freshwater ecosystems to investigate how warming and top predator loss affect seven ecosystem functions representing two major dimensions of ecosystem functioning, productivity and metabolism. We investigated their direct and indirect effects on community diversity and standing stock of multitrophic macro and microorganisms. Warming directly increased multifunctional ecosystem productivity and metabolism. In contrast, top predator loss indirectly affected multifunctional ecosystem productivity via changes in the diversity of detritivorous macroinvertebrates, but did not affect ecosystem metabolism. In addition to demonstrating how multiple anthropogenic drivers have different impacts, via different pathways, on ecosystem multifunctionality components, our work should further spur advances in predicting responses of ecosystems to multiple simultaneous environmental changes.

Environmental change and predator diversity drive alpha and beta diversity in freshwater macro and microorganisms.

Global biodiversity is eroding due to anthropogenic causes, such as climate change, habitat loss, and trophic simplification of biological communities. Most studies address only isolated causes within a single group of organisms; however, biological groups of different trophic levels may respond in particular ways to different environmental impacts. Our study used natural microcosms to investigate the predicted individual and interactive effects of warming, changes in top predator diversity, and habitat size on the alpha and beta diversity of macrofauna, microfauna, and bacteria. Alpha diversity (i.e., richness within each bromeliad) generally explained a larger proportion of the gamma diversity (partitioned in alpha and beta diversity). Overall, dissimilarity between communities occurred due to species turnover and not species loss (nestedness). Nevertheless, the three biological groups responded differently to each environmental stressor. Microfauna were the most sensitive group, with alpha and beta diversity being affected by environmental changes (warming and habitat size) and trophic structure (diversity of top predators). Macrofauna alpha and beta diversity was sensitive to changes in predator diversity and habitat size, but not warming. In contrast, the bacterial community was not influenced by the treatments. The community of each biological group was not mutually concordant with the environmental and trophic changes. Our results demonstrate that distinct anthropogenic impacts differentially affect the components of macro and microorganism diversity through direct and indirect effects (i.e., bottom-up and top-down effects). Therefore, a multitrophic and multispecies approach is necessary to assess the effects of different anthropogenic impacts on biodiversity.

Terrestrial vertebrate predators drive the structure and functioning of aquatic food webs.

Predators that forage at boundaries between ecosystems can affect prey from adjacent ecosystems, thereby triggering consumptive and non-consumptive cascading effects, which may affect diversity and food web structure across ecosystems. In the present study, we manipulated the access of insectivorous birds, lizards, and anurans to tank bromeliads in scrub vegetation in southern Brazil. We measured cascading effects on the community structure of aquatic invertebrates inhabiting bromeliad leaves and on the ecosystem processes of decomposition rate and bromeliad growth. The exclusion of terrestrial vertebrate predators increased the biomass of Odonate and Tabanid apex predators, which shifted the body size structure of the assemblage and generated inverted biomass pyramids that were top-heavy. Within bromeliads with larger aquatic predators, the species composition and abundance of other aquatic invertebrates also changed, resulting in higher abundance of mesopredators and scrapers, and lower abundance of shredders. Under those conditions, the detritus decomposition rate decreased, and bromeliads produced more leaves, perhaps because of the higher deposition of nitrogenous waste by mesopredators. Our results highlight that the effects of terrestrial vertebrate predators can propagate across aquatic ecosystems, altering species composition, body size structure, food web organization, and ecosystem function.

Trade-off between soluble protein production and nutritional storage in Bromeliaceae.

BACKGROUND AND AIMS: Bromeliads are able to occupy some of the most nutrient-poor environments especially because they possess absorptive leaf trichomes, leaves organized in rosettes, distinct photosynthetic pathways [C3, Crassulacean acid metabolism (CAM) or facultative C3-CAM], and may present an epiphytic habit. The more derived features related to these traits are described for the Tillandsioideae subfamily. In this context, the aims of this study were to evaluate how terrestrial predators contribute to the nutrition and performance of bromeliad species, subfamilies and ecophysiological types, whether these species differ in their ecophysiological traits and whether the physiological outcomes are consistent among subfamilies and types (e.g. presence/absence of tank, soil/tank/atmosphere source of nutrients, trichomes/roots access to nutrients). METHODS: Isotopic (15N-enriched predator faeces) and physiological methods (analyses of plant protein, amino acids, growth, leaf mass per area and total N incorporated) in greenhouse experiments were used to investigate the ecophysiological contrasts between Tillandsioideae and Bromelioideae, and among ecophysiological types when a predatory anuran contributes to their nutrition. KEY RESULTS: It was observed that Bromelioideae had higher concentrations of soluble protein and only one species grew more (Ananas bracteatus), while Tillandsioideae showed higher concentrations of total amino acids, asparagine and did not grow. The ecophysiological types that showed similar protein contents also had similar growth. Additionally, an ordination analysis showed that the subfamilies and ecophysiological types were discrepant considering the results of the total nitrogen incorporated from predators, soluble protein and asparagine concentrations, relative growth rate and leaf mass per area. CONCLUSIONS: Bromeliad subfamilies showed a trade-off between two strategies: Tillandsioideae stored nitrogen into amino acids possibly for transamination reactions during nutritional stress and did not grow, whereas Bromelioideae used nitrogen for soluble protein production for immediate utilization, possibly for fast growth. These results highlight that Bromeliaceae evolution may be directly associated with the ability to stock nutrients.

Floral asymmetry and predation risk modify pollinator behavior, but only predation risk decreases plant fitness.

Although predators and floral herbivores can potentially decrease plant fitness by changing pollinator behaviors, studies comparing the strength of these factors as well as their additive and interactive effects on pollinator visitation and plant fitness have not been conducted. In this study, we manipulated the floral symmetry and predator presence (artificial crab spiders) on the flowers of the shrub Rubus rosifolius (Rosaceae) in a 2 × 2 factorial randomized block design. We found that asymmetry and predators decreased pollinator visitation (mainly hymenopterans), and overall these factors did not interact (additive effects). The effect of predation risk on pollinator avoidance behavior was 62 % higher than that of floral asymmetry. Furthermore, path analyses revealed that only predation risk cascaded down to plant fitness, and it significantly decreased fruit biomass by 33 % and seed number by 28 %. We also demonstrated that R. rosifolius fitness is indirectly affected by visiting and avoidance behaviors of pollinators. The strong avoidance behavioral response triggered by predation risk may be related to predator pressure upon flowers. Although floral asymmetry caused by herbivory can alter the quality of resources, it should not exert the same evolutionary pressure as that of predator-prey interactions. Our study highlights the importance of considering simultaneous forces, such as predation risk and floral asymmetry, as well as pollinator behavior when evaluating ecological processes involving mutualistic plant-pollinator systems.

The role of multiple partners in a digestive mutualism with a protocarnivorous plant.

BACKGROUND AND AIMS: The protocarnivorous plant Paepalanthus bromelioides (Eriocaulaceae) is similar to bromeliads in that this plant has a rosette-like structure that allows rainwater to accumulate in leaf axils (i.e. phytotelmata). Although the rosettes of P. bromelioides are commonly inhabited by predators (e.g. spiders), their roots are wrapped by a cylindrical termite mound that grows beneath the rosette. In this study it is predicted that these plants can derive nutrients from recycling processes carried out by termites and from predation events that take place inside the rosette. It is also predicted that bacteria living in phytotelmata can accelerate nutrient cycling derived from predators. METHODS: The predictions were tested by surveying plants and animals, and also by performing field experiments in rocky fields from Serra do Cipó, Brazil, using natural abundance and enriched isotopes of (15)N. Laboratory bioassays were also conducted to test proteolytic activities of bacteria from P. bromelioides rosettes. KEY RESULTS: Analyses of (15)N in natural nitrogen abundances showed that the isotopic signature of P. bromelioides is similar to that of carnivorous plants and higher than that of non-carnivorous plants in the study area. Linear mixing models showed that predatory activities on the rosettes (i.e. spider faeces and prey carcass) resulted in overall nitrogen contributions of 26·5 % (a top-down flux). Although nitrogen flux was not detected from termites to plants via decomposition of labelled cardboard, the data on (15)N in natural nitrogen abundance indicated that 67 % of nitrogen from P. bromelioides is derived from termites (a bottom-up flux). Bacteria did not affect nutrient cycling or nitrogen uptake from prey carcasses and spider faeces. CONCLUSIONS: The results suggest that P. bromelioides derive nitrogen from associated predators and termites, despite differences in nitrogen cycling velocities, which seem to have been higher in nitrogen derived from predators (leaves) than from termites (roots). This is the first study that demonstrates partitioning effects from multiple partners in a digestion-based mutualism. Despite most of the nitrogen being absorbed through their roots (via termites), P. bromelioides has all the attributes necessary to be considered as a carnivorous plant in the context of digestive mutualism.

Spider-fed bromeliads: seasonal and interspecific variation in plant performance.

BACKGROUND AND AIMS: Several animals that live on bromeliads can contribute to plant nutrition through nitrogen provisioning (digestive mutualism). The bromeliad-living spider Psecas chapoda (Salticidae) inhabits and breeds on Bromelia balansae in regions of South America, but in specific regions can also appear on Ananas comosus (pineapple) plantations and Aechmea distichantha. METHODS: Using isotopic and physiological methods in greenhouse experiments, the role of labelled ((15)N) spider faeces and Drosophila melanogaster flies in the nutrition and growth of each host plant was evaluated, as well as seasonal variation in the importance of this digestive mutualism. KEY RESULTS: Spiders contributed 0·6 ± 0·2 % (mean ± s.e.; dry season) to 2·7 ± 1 % (wet season) to the total nitrogen in B. balansae, 2·4 ± 0·4 % (dry) to 4·1 ± 0·3 % (wet) in An. comosus and 3·8 ± 0·4 % (dry) to 5 ± 1 % (wet) in Ae. distichantha. In contrast, flies did not contribute to the nutrition of these bromeliads. Chlorophylls and carotenoid concentrations did not differ among treatments. Plants that received faeces had higher soluble protein concentrations and leaf growth (RGR) only during the wet season. CONCLUSIONS: These results indicate that the mutualism between spiders and bromeliads is seasonally restricted, generating a conditional outcome. There was interspecific variation in nutrient uptake, probably related to each species' performance and photosynthetic pathways. Whereas B. balansae seems to use nitrogen for growth, Ae. distichantha apparently stores nitrogen for stressful nutritional conditions. Bromeliads absorbed more nitrogen coming from spider faeces than from flies, reinforcing the beneficial role played by predators in these digestive mutualisms.

Non-native fishes homogenize native fish communities and reduce ecosystem multifunctionality in tropical lakes over 16 years.

Non-native species are considered a major global threat to biodiversity, and their expansion to new ecosystems has recently increased. However, the effect of non-native species on ecosystem functioning is poorly understood, especially in hyperdiverse tropical ecosystems of which long-term studies are scarce. We analyzed the relationship between richness, biomass, and ß-diversity of non-native and native fishes during 16 years in five hyperdiverse tropical shallow lakes. We further elucidated how an observed increase in the proportion of richness, biomass, and ß-diversity of non-native over native fishes affect crucial multifunctional processes of lakes (decomposition, productivity). We found a general positive relationship between the richness and biomass of non-native and native fishes. However, the slope of this relationship decreased continuously with time, displaying an increase in non-native species richness and a decrease in native species richness over time. We also detected a negative relationship between the ß-diversity of non-native and native fishes over time. Moreover, the increase in the non-native:native ratio of species richness, biomass, and ß-diversity over time decreased ecosystem multifunctionality. Our results suggest that non-native fishes caused a homogenization of the native fish species over time, resulting in impoverishment of ecosystem multifunctionality; in part because non-native fishes are less productive than native ones. Therefore, focus on long-term effects and use of multiple biodiversity facets (α- and ß-diversity) are crucial to make reliable predictions of the effects of non-native fish species on native fishes and ecosystem functioning.

Diet overlap and spatial segregation between two neotropical marsupials revealed by multiple analytical approaches.

Species co-existence depends on how organisms utilize their environment and resources. When two sympatric species are similar in some ecological requirements, their coexistence may arise from differences in resource use over time and/or space. Interactions among coexisting marsupials remain poorly understood, especially in the Neotropics. Here we combine spatial niche measurements, individual-resource networks, and isotopic niche approaches, to investigate the ecological strategies used by the Neotropical marsupials Didelphis aurita and Metachirus nudicaudatus to co-occur in an area of Serra do Mar State Park (southeast of Brazil). Both individual-resource networks and isotopic niche approaches indicate similar patterns of omnivory for both species. Isotopic analysis showed the species' trophic niche to be similar, with 52% of overlap, and no differences between proportional contributions of each resource to their diets. Moreover, individual-resource network analysis found no evidence of diet nestedness or segregation. The trophic niche overlap observed was associated with spatial segregation between species. Despite using the same area over the year, D. aurita and M. nudicaudatus exhibited spatial segregation among seasons. These results illustrate that the detection of spatial segregation is scale-dependent and must be carefully considered. In conclusion, our findings provide a new perspective on the ecology of these two Neotropical marsupials by illustrating how the association of distinct but complementary methods can be applied to reach a more complete understanding of resource partitioning and species coexistence.

Disentangling the phylogenetic and ecological components of spider phenotypic variation.

An understanding of how the degree of phylogenetic relatedness influences the ecological similarity among species is crucial to inferring the mechanisms governing the assembly of communities. We evaluated the relative importance of spider phylogenetic relationships and ecological niche (plant morphological variables) to the variation in spider body size and shape by comparing spiders at different scales: (i) between bromeliads and dicot plants (i.e., habitat scale) and (ii) among bromeliads with distinct architectural features (i.e., microhabitat scale). We partitioned the interspecific variation in body size and shape into phylogenetic (that express trait values as expected by phylogenetic relationships among species) and ecological components (that express trait values independent of phylogenetic relationships). At the habitat scale, bromeliad spiders were larger and flatter than spiders associated with the surrounding dicots. At this scale, plant morphology sorted out close related spiders. Our results showed that spider flatness is phylogenetically clustered at the habitat scale, whereas it is phylogenetically overdispersed at the microhabitat scale, although phylogenic signal is present in both scales. Taken together, these results suggest that whereas at the habitat scale selective colonization affect spider body size and shape, at fine scales both selective colonization and adaptive evolution determine spider body shape. By partitioning the phylogenetic and ecological components of phenotypic variation, we were able to disentangle the evolutionary history of distinct spider traits and show that plant architecture plays a role in the evolution of spider body size and shape. We also discussed the relevance in considering multiple scales when studying phylogenetic community structure.

Mites and leaf domatia: no evidence of mutualism in Coffea arabica plants / Ácaros e domácias foliares: sem evidências de mutualismo em plantas de Coffea arabica

We conducted experiments by blocking off pit-like domatia from old and new leaves of Coffea arabica L., using tiny resin drops, to investigate the role of domatia on i) mite abundance at the community level and on ii) leaf damages. More than 77 percent of the mites collected were predators, whereas 19 and 3.3 percent were omnivores and phytophages, respectively. Domatia blockage treatment had no influence either on mite abundances or leaf damages. However, predatory and omnivorous mites were more abundant on new than on the old leaves; phytophagous mites occurred at very low density and occupied only plants having open domatia. The absence of mutualism between mites and C. arabica probably occurred because the entrances of domatia were too small and did not enable the entry of fitoseid predators in these structures.

Domácias são pequenas estruturas presentes na junção entre as nervuras principal e secundárias das folhas de muitas espécies de plantas, que podem mediar interações mutualísticas entre ácaros e plantas. Em experimento, nós bloqueamos as domácias em formato de covas de folhas novas e velhas de Coffea arabica L. com gotas de resina, a fim de investigar o seu papel i) na abundância de ácaros na comunidade e ii) nos danos foliares. Mais de 77 por cento dos ácaros coletados são predadores, enquanto 19 e 3,3 por cento são onívoros e fitófagos, respectivamente. Não houve influência do bloqueio das domácias tanto na abundância quanto nos danos foliares. Entretanto, os ácaros predadores e micófagos foram mais abundantes nas folhas novas do que nas velhas; os ácaros fitófagos ocorreram em pequena densidade e ocuparam somente as plantas com domácias abertas. A ausência de mutualismo entre os ácaros e plantas de C. arabica pode ter ocorrido porque as entradas das domácias analisadas eram muito pequenas, não permitindo a entrada dos predadores fitoseídeos nessas estruturas.