Crying wolf to a predator: deceptive vocal mimicry by a bird protecting young

Animals often mimic dangerous or toxic species to deter predators; however, mimicry of such species may not always be possible and mimicry of benign species seems unlikely to confer anti-predator benefits. We reveal a system in which a bird mimics the alarm calls of harmless species to fool a predator 40 times its size and protect its offspring against attack. Our experiments revealed that brown thornbills ( Acanthiza pusilla ) mimic a chorus of other species' aerial alarm calls, a cue of an Accipiter hawk in flight, when predators attack their nest. The absence of any flying predators in this context implies that these alarms convey deceptive information about the type of danger present. Experiments on the primary nest predators of thornbills, pied currawongs ( Strepera graculina ), revealed that the predators treat these alarms as if they themselves are threatened by flying hawks, either by scanning the sky for danger or fleeing, confirming a deceptive function. In turn, these distractions delay attack and provide thornbill nestlings with an opportunity to escape. This sophisticated defence strategy exploits the complex web of interactions among multiple species across several trophic levels, and in particular exploits a predator's ability to eavesdrop on and respond appropriately to heterospecific alarm calls. Our findings demonstrate that prey can fool predators by deceptively mimicking alarm calls of harmless species, suggesting that defensive mimicry could be more widespread because of indirect effects on predators within a web of eavesdropping.

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Trophic Cascades in Grasslands

10.1093/oso/9780198744511.003.0005 ◽

2018 ◽

Author(s):

Brian J. Wilsey

Keyword(s):

Indirect Effects ◽

Prey Species ◽

Trophic Levels ◽

Herbaceous Plant ◽

Direct Effects ◽

Temperate Grasslands ◽

Cascading Effect ◽

Top Predators ◽

Invertebrate Predators ◽

Ecology Of Fear

Top predators have effects that can ‘cascade down’ on lower trophic levels. Because of this cascading effect, it matters how many trophic levels are present. Predators are either ‘sit and wait’ or ‘active’. Wolves are top predators in temperate grasslands and can alter species composition of smaller-sized predators, prey, and woody and herbaceous plant species, either through direct effects or indirect effects (‘Ecology of Fear’). In human derived grasslands, invertebrate predators fill a similar ecological role as wolves. Migrating populations of herbivores tend to be more limited by food than non-migratory populations. The phenology and synchrony of births vary among prey species in a way that is consistent with an adaptation to predation. Precocious species have highly synchronous birth dates to satiate predators. Non-precocious species (‘hiders’) have asynchronous births. Results from studies that manipulate both predators and food support the hypothesis that bottom-up and top-down effects interact.

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Trait-mediated trophic cascade creates enemy-free space for nesting hummingbirds

Science Advances ◽

10.1126/sciadv.1500310 ◽

2015 ◽

Vol 1 (8) ◽

pp. e1500310 ◽

Cited By ~ 8

Author(s):

Harold F. Greeney ◽

M. Rocio Meneses ◽

Chris E. Hamilton ◽

Eli Lichter-Marck ◽

R. William Mannan ◽

...

Keyword(s):

Climate Change ◽

Habitat Fragmentation ◽

Breeding Success ◽

Indirect Effects ◽

Trophic Cascade ◽

Terrestrial Ecosystems ◽

Trophic Levels ◽

Ecological Communities ◽

Top Predators ◽

Enemy Free Space

The indirect effects of predators on nonadjacent trophic levels, mediated through traits of intervening species, are collectively known as trait-mediated trophic cascades. Although birds are important predators in terrestrial ecosystems, clear examples of trait-mediated indirect effects involving bird predators have almost never been documented. Such indirect effects are important for structuring ecological communities and are likely to be negatively impacted by habitat fragmentation, climate change, and other factors that reduce abundance of top predators. We demonstrate that hummingbirds in Arizona realize increased breeding success when nesting in association with hawks. An enemy-free nesting space is created when jays, an important source of mortality for hummingbird nests, alter their foraging behavior in the presence of their hawk predators.

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Trophic cascades in benthic marine ecosystems: lessons for fisheries and protected-area management

Environmental Conservation ◽

10.1017/s0376892900000205 ◽

2000 ◽

Vol 27 (2) ◽

pp. 179-200 ◽

Cited By ~ 304

Author(s):

J.K. PINNEGAR ◽

N.V.C. POLUNIN ◽

P. FRANCOUR ◽

F. BADALAMENTI ◽

R. CHEMELLO ◽

...

Keyword(s):

Indirect Effects ◽

Large Scale ◽

Trophic Cascades ◽

Marine Ecosystems ◽

Trophic Levels ◽

Kelp Forests ◽

Resource Exploitation ◽

Rocky Subtidal ◽

Fishery Exploitation ◽

Cascade Effects

An important principle of environmental science is that changes in single components of systems are likely to have consequences elsewhere in the same systems. In the sea, food web data are one of the few foundations for predicting such indirect effects, whether of fishery exploitation or following recovery in marine protected areas (MPAs). We review the available literature on one type of indirect interaction in benthic marine ecosystems, namely trophic cascades, which involve three or more trophic levels connected by predation. Because many indirect effects have been revealed through fishery exploitation, in some cases we include humans as trophic levels. Our purpose is to establish how widespread cascades might be, and infer how likely they are to affect the properties of communities following the implementation of MPAs or intensive resource exploitation. We review 39 documented cascades (eight of which include humans as a trophic level) from 21 locations around the world; all but two of the cascades are from shallow systems underlain by hard substrata (kelp forests, rocky subtidal, coral reefs and rocky intertidal). We argue that these systems are well represented because they are accessible and also amenable to the type of work that is necessary. Nineteen examples come from the central-eastern and north-eastern Pacific, while no well-substantiated benthic cascades have been reported from the NE, CE or SW Atlantic, the Southern Oceans, E Indian Ocean or NW Pacific. The absence of examples from those zones is probably due to lack of study. Sea urchins are very prominent in the subtidal examples, and gastropods, especially limpets, in the intertidal examples; we suggest that this may reflect their predation by fewer specialist predators than is the case with fishes, but also their conspicuousness to investigators. The variation in ecological resolution amongst studies, and in intensity of study amongst systems and regions, indicates that more cascades will likely be identified in due course. Broadening the concept of cascades to include pathogenic interactions would immediately increase the number of examples. The existing evidence is that cascade effects are to be expected when hard-substratum systems are subject to artisanal resource exploitation, but that the particular problems of macroalgal overgrowth on Caribbean reefs and the expansion of coralline barrens in the Mediterranean rocky-sublittoral will not be readily reversed in MPAs, probably because factors other than predation-based cascades have contributed to them in the first place. More cascade effects are likely to be found in the soft-substratum systems that are crucial to so many large-scale fisheries, when opportunities such as those of MPAs and fishing gradients become available for study of such systems, and the search is widened to less conspicuous focal organisms such as polychaetes and crustaceans.

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Temperature Effects Explain Continental Scale Distribution of Cyanobacterial Toxins

Toxins ◽

10.3390/toxins10040156 ◽

2018 ◽

Vol 10 (4) ◽

pp. 156 ◽

Cited By ~ 74

Author(s):

Evanthia Mantzouki ◽

Miquel Lürling ◽

Jutta Fastner ◽

Lisette De Senerpont Domis ◽

Elżbieta Wilk-Woźniak ◽

...

Keyword(s):

Indirect Effects ◽

Linear Models ◽

Diversity Index ◽

Toxin Production ◽

Direct And Indirect Effects ◽

Cyanobacterial Toxins ◽

Toxic Species ◽

Continental Scale ◽

Production And Distribution ◽

The Relationship

Insight into how environmental change determines the production and distribution of cyanobacterial toxins is necessary for risk assessment. Management guidelines currently focus on hepatotoxins (microcystins). Increasing attention is given to other classes, such as neurotoxins (e.g., anatoxin-a) and cytotoxins (e.g., cylindrospermopsin) due to their potency. Most studies examine the relationship between individual toxin variants and environmental factors, such as nutrients, temperature and light. In summer 2015, we collected samples across Europe to investigate the effect of nutrient and temperature gradients on the variability of toxin production at a continental scale. Direct and indirect effects of temperature were the main drivers of the spatial distribution in the toxins produced by the cyanobacterial community, the toxin concentrations and toxin quota. Generalized linear models showed that a Toxin Diversity Index (TDI) increased with latitude, while it decreased with water stability. Increases in TDI were explained through a significant increase in toxin variants such as MC-YR, anatoxin and cylindrospermopsin, accompanied by a decreasing presence of MC-LR. While global warming continues, the direct and indirect effects of increased lake temperatures will drive changes in the distribution of cyanobacterial toxins in Europe, potentially promoting selection of a few highly toxic species or strains.

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Direct and indirect effects of near-future pCO2 levels on zooplankton dynamics

Marine and Freshwater Research ◽

10.1071/mf15296 ◽

2017 ◽

Vol 68 (2) ◽

pp. 373 ◽

Cited By ~ 5

Author(s):

Cédric L. Meunier ◽

María Algueró-Muñiz ◽

Henriette G. Horn ◽

Julia A. F. Lange ◽

Maarten Boersma

Keyword(s):

Ocean Acidification ◽

Indirect Effects ◽

Trophic Levels ◽

Model Organisms ◽

High Pco2 ◽

Direct And Indirect Effects ◽

Oxyrrhis Marina ◽

Short Term Exposure ◽

Zooplankton Growth ◽

Seawater Pco2

Ocean acidification has direct physiological effects on organisms, for example by dissolving the calcium carbonate structures of calcifying species. However, non-calcifiers may also be affected by changes in seawater chemistry. To disentangle the direct and indirect effects of ocean acidification on zooplankton growth, we undertook a study with two model organisms. Specifically, we investigated the individual effects of short-term exposure to high and low seawater pCO2, and different phytoplankton qualities as a result of different CO2 incubations on the growth of a heterotrophic dinoflagellate (Oxyrrhis marina) and a copepod species (Acartia tonsa). It was observed previously that higher CO2 concentrations can decrease phytoplankton food quality in terms of carbon:nutrient ratios. We therefore expected both seawater pCO2 (pH) and phytoplankton quality to result in decreased zooplankton growth. Although we expected lowest growth rates for all zooplankton under high seawater pCO2 and low algal quality, we found that direct pH effects on consumers seem to be of lesser importance than the associated decrease in algal quality. The decrease in the quality of primary producers under high pCO2 conditions negatively affected zooplankton growth, which may lead to lower availability of food for the next trophic level and thus potentially affect the recruitment of higher trophic levels.

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Better biological control in glasshouses: synergies between biological control agents from different guilds and floral resources

New Zealand Plant Protection ◽

10.30843/nzpp.2019.72.335 ◽

2019 ◽

Vol 72 ◽

pp. 280

Author(s):

Emiliano R. Veronesi ◽

Oluwashola Olaniyan ◽

Stephen D. Wratten ◽

Melanie Davidson ◽

Chris Thompson

Keyword(s):

Biological Control ◽

New Zealand ◽

Single Species ◽

Trophic Levels ◽

Floral Resources ◽

Bactericera Cockerelli ◽

Biological Control Agents ◽

Major Pest ◽

Mirid Bug ◽

Multiple Species

The tomato/potato psyllid (TPP), Bactericera cockerelli (Hemiptera, Triozidae), is an adventive psyllid in New Zealand that is a major pest of solanaceous crops and a serious threat to growers in the glasshouse industry. Worldwide, evaluation of potential biological control (BC) agents is normally conducted using single species and this is the case with some potential BC agents for TPP. However, the idea that multiple species can act synergistically remains largely untested so that is the aim of the current work, which is funded by Tomatoes New Zealand. The introduced parasitoid Tamarixia triozae is a BC agent of TPP that attacks mainly late instars. It lives for just 1 day when provided with water but can live up to 11 days (and consume more pests) when nectar in the flowers of buckwheat (Fagopyrum esculentum) is provided. In addition, another potential BC agent, the mirid bug Engytatus nicotianae, prefers young nymphal instars, while the ladybird Cleobora mellyi is voracious and consumes all instars. We are testing combinations of these species to understand the potential for synergies between and within trophic levels for better biological control.

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The frequency of vocal mimicry associated with danger varies due to proximity to nest and nesting stage in a passerine bird

Behaviour ◽

10.1163/1568539x-00003123 ◽

2014 ◽

Vol 151 (1) ◽

pp. 73-88 ◽

Cited By ~ 6

Author(s):

Eben Goodale ◽

Chaminda P. Ratnayake ◽

Sarath W. Kotagama

Keyword(s):

Sri Lanka ◽

Passerine Bird ◽

Alarm Calls ◽

Mixed Species ◽

Vocal Mimicry ◽

Young Offspring ◽

Mixed Species Flocks ◽

Species Specific ◽

Breeding Seasons ◽

Species Flocks

Several species of birds vocally imitate sounds associated with danger. Two anecdotal studies suggest that such ‘danger mimicry’ increases during nesting, but such a relationship has not been quantitatively demonstrated. Sri Lanka drongos (Dicrurus paradiseus lophorhinus) are known to imitate predators and other species’ mobbing and alarm calls in alarm contexts. Here we investigated whether drongos vary their production of danger mimicry in different nesting stages (building, incubation, nests with hatchlings, fledglings still outside of mixed-species flocks), and when foraging away from young in mixed-species flocks. We recorded drongos over two breeding seasons at 14 different nesting trees, used year-after-year. We found that of all the types of danger mimicry, imitation of predators was the most common and exclusive to drongos that had young offspring. Such predator mimicry was observed at a higher rate during the hatchling and fledgling stages compared to incubation or flocks. Danger mimicry did not, however, increase during this stage in isolation: drongo species-specific alarm calls also increased, and the close connection between these two types of calls did not appear to change. Although it is possible that the association between danger mimicry and species-specific alarm calls could help young birds learn sounds associated with danger, the performance of this behaviour does not seem exclusive enough to interactions between adult drongos and their offspring to meet functional definitions of teaching.

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Meta-Analysis Suggests Differing Indirect Effects of Viral, Bacterial, and Fungal Plant Pathogens on the Natural Enemies of Insect Herbivores

Insects ◽

10.3390/insects11110765 ◽

2020 ◽

Vol 11 (11) ◽

pp. 765

Author(s):

Ussawit Srisakrapikoop ◽

Tara J. Pirie ◽

Mark D. E. Fellowes

Keyword(s):

Natural Enemies ◽

Indirect Effects ◽

Plant Pathogens ◽

Meta Analysis ◽

Trophic Levels ◽

Plant Diseases ◽

Plant Quality ◽

Insect Herbivore ◽

Insect Herbivores ◽

Fungal Plant Pathogens

Indirect effects are ubiquitous in nature, and have received much attention in terrestrial plant–insect herbivore–enemy systems. In such tritrophic systems, changes in plant quality can have consequential effects on the behavior and abundance of insect predators and parasitoids. Plant quality as perceived by insect herbivores may vary for a range of reasons, including because of infection by plant pathogens. However, plant diseases vary in their origin (viral, bacterial or fungal) and as a result may have differing effects on plant physiology. To investigate if the main groups of plant pathogens differ in their indirect effects on higher trophic levels, we performed a meta-analysis using 216 measured responses from 29 primary studies. There was no overall effect of plant pathogens on natural enemy traits as differences between pathogen types masked their effects. Infection by fungal plant pathogens showed indirect negative effects on the performance and preference of natural enemies via both chewing and piercing-sucking insect herbivore feeding guilds. Infection by bacterial plant pathogens had a positive effect on the natural enemies (parasitoids) of chewing herbivores. Infection by viral plant pathogens showed no clear effect, although parasitoid preference may be positively affected by their presence. It is important to note that given the limited volume of studies to date on such systems, this work should be considered exploratory. Plant pathogens are very common in nature, and tritrophic systems provide an elegant means to examine the consequences of indirect interactions in ecology. We suggest that further studies examining how plant pathogens affect higher trophic levels would be of considerable value.

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Mitonuclear interactions and introgression genomics of macaque monkeys ( Macaca ) highlight the influence of behaviour on genome evolution

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2021.1756 ◽

2021 ◽

Vol 288 (1960) ◽

Author(s):

Ben J. Evans ◽

Benjamin M. Peter ◽

Don J. Melnick ◽

Noviar Andayani ◽

Jatna Supriatna ◽

...

Keyword(s):

Genome Evolution ◽

Indirect Effects ◽

Genomic Data ◽

Species Boundaries ◽

Mitochondrial Genomes ◽

Runs Of Homozygosity ◽

Interaction Partners ◽

Significant Enrichment ◽

Compensatory Mutations ◽

Multiple Species

In most macaques, females are philopatric and males migrate from their natal ranges, which results in pronounced divergence of mitochondrial genomes within and among species. We therefore predicted that some nuclear genes would have to acquire compensatory mutations to preserve compatibility with diverged interaction partners from the mitochondria. We additionally expected that these sex-differences would have distinctive effects on gene flow in the X and autosomes. Using new genomic data from 29 individuals from eight species of Southeast Asian macaque, we identified evidence of natural selection associated with mitonuclear interactions, including extreme outliers of interspecies differentiation and metrics of positive selection, low intraspecies polymorphism and atypically long runs of homozygosity associated with nuclear-encoded genes that interact with mitochondria-encoded genes. In one individual with introgressed mitochondria, we detected a small but significant enrichment of autosomal introgression blocks from the source species of her mitochondria that contained genes which interact with mitochondria-encoded loci. Our analyses also demonstrate that sex-specific demography sculpts genetic exchange across multiple species boundaries. These findings show that behaviour can have profound but indirect effects on genome evolution by influencing how interacting components of different genomic compartments (mitochondria, the autosomes and the sex chromosomes) move through time and space.

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Predator encounters have spatially extensive impacts on parental behaviour in a breeding bird community

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2016.0020 ◽

2016 ◽

Vol 283 (1827) ◽

pp. 20160020 ◽

Cited By ~ 7

Author(s):

Kadri Moks ◽

Vallo Tilgar ◽

Robert L. Thomson ◽

Sara Calhim ◽

Pauliina E. Järvistö ◽

...

Keyword(s):

Predation Risk ◽

Indirect Effects ◽

Bird Community ◽

Ficedula Hypoleuca ◽

Alarm Calls ◽

Short Term ◽

Breeding Bird ◽

Individual Behaviour ◽

Parental Behaviour ◽

Visitation Rates

Predation risk has negative indirect effects on prey fitness, partly mediated through changes in behaviour. Evidence that individuals gather social information from other members of the population suggests that events in a community may impact the behaviour of distant individuals. However, spatially wide-ranging impacts on individual behaviour caused by a predator encounter elsewhere in a community have not been documented before. We investigated the effect of a predator encounter (hawk model presented at a focal nest) on the parental behaviour of pied flycatchers ( Ficedula hypoleuca ), both at the focal nest and at nearby nests different distances from the predator encounter. We show that nest visitation of both focal pairs and nearby pairs were affected, up to 3 h and 1 h, respectively. Parents also appeared to compensate initial disrupted feeding by later increasing nest visitation rates. This is the first evidence showing that the behaviour of nearby pairs was affected away from an immediate source of risk. Our results indicate that the impacts of short-term predator encounters may immediately extend spatially to the broader community, affecting the behaviour of distant individuals. Information about predators is probably quickly spread by cues such as intra- and heterospecific alarm calls, in communities of different taxa.

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