A biogeographical appraisal of the threatened South East Africa Montane Archipelago ecoregion.

Recent biological surveys of ancient inselbergs in southern Malawi and northern Mozambique have led to the discovery and description of many species new to science, and overlapping centres of endemism across multiple taxa. Combining these endemic taxa with data on geology and climate, we propose the 'South East Africa Montane Archipelago' (SEAMA) as a distinct ecoregion of global biological importance. The ecoregion encompasses 30 granitic inselbergs reaching > 1000 m above sea level, hosting the largest (Mt Mabu) and smallest (Mt Lico) mid-elevation rainforests in southern Africa, as well as biologically unique montane grasslands. Endemic taxa include 127 plants, 45 vertebrates (amphibians, reptiles, birds, mammals) and 45 invertebrate species (butterflies, freshwater crabs), and two endemic genera of plants and reptiles. Existing dated phylogenies of endemic animal lineages suggests this endemism arose from divergence events coinciding with repeated isolation of these mountains from the pan-African forests, together with the mountains' great age and relative climatic stability. Since 2000, the SEAMA has lost 18% of its primary humid forest cover (up to 43% in some sites)-one of the highest deforestation rates in Africa. Urgently rectifying this situation, while addressing the resource needs of local communities, is a global priority for biodiversity conservation.

Culturally determined interspecies communication between humans and honeyguides.

Species interactions that vary across environments can create geographical mosaics of genetic coevolution. However, traits mediating species interactions are sometimes culturally inherited. Here we show that traditions of interspecies communication between people and wild birds vary in a culturally determined geographical mosaic. Honey hunters in different parts of Africa use different calls to communicate with greater honeyguides (Indicator indicator) that lead them to bees' nests. We show experimentally that honeyguides in Tanzania and Mozambique discriminate among honey hunters' calls, responding more readily to local than to foreign calls. This was not explained by variation in sound transmission and instead suggests that honeyguides learn local human signals. We discuss the forces stabilizing and diversifying interspecies communication traditions, and the potential for cultural coevolution between species.

Guides and cheats: producer-scrounger dynamics in the human-honeyguide mutualism.

Foraging animals commonly choose whether to find new food (as 'producers') or scavenge from others (as 'scroungers'), and this decision has ecological and evolutionary consequences. Understanding these tactic decisions is particularly vital for naturally occurring producer-scrounger systems of economic importance, because they determine the system's productivity and resilience. Here, we investigate how individuals' traits predict tactic decisions, and the consistency and pay-offs of these decisions, in the remarkable mutualism between humans (Homo sapiens) and greater honeyguides (Indicator indicator). Honeyguides can either guide people to bees' nests and eat the resulting beeswax (producing), or scavenge beeswax (scrounging). Our results suggest that honeyguides flexibly switched tactics, and that guiding yielded greater access to the beeswax. Birds with longer tarsi scrounged more, perhaps because they are more competitive. The lightest females rarely guided, possibly to avoid aggression, or because genetic matrilines may affect female body mass and behaviour in this species. Overall, aspects of this producer-scrounger system probably increase the productivity and resilience of the associated human-honeyguide mutualism, because the pay-offs incentivize producing, and tactic-switching increases the pool of potential producers. Broadly, our findings suggest that even where tactic-switching is prevalent and producing yields greater pay-offs, certain phenotypes may be predisposed to one tactic.

Chase-away evolution maintains imperfect mimicry in a brood parasite-host system despite rapid evolution of mimics.

We studied a brood parasite-host system (the cuckoo finch Anomalospiza imberbis and its host, the tawny-flanked prinia Prinia subflava) to test (1) the fundamental hypothesis that deceptive mimics evolve to resemble models, selecting in turn for models to evolve away from mimics ('chase-away evolution') and (2) whether such reciprocal evolution maintains imperfect mimicry over time. Over only 50 years, parasites evolved towards hosts and hosts evolved away from parasites, resulting in no detectible increase in mimetic fidelity. Our results reflect rapid adaptive evolution in wild populations of models and mimics and show that chase-away evolution in models can counteract even rapid evolution of mimics, resulting in the persistence of imperfect mimicry.

Repeatable randomness, invariant properties, and the design of biological signatures of identity.

What makes a perfect signature? Optimal signatures should be consistent within individuals and distinctive between individuals. In defense against avian brood parasitism, some host species have evolved "signatures" of identity on their eggs, comprising interindividual variation in color and pattern. Tawny-flanked prinia (Prinia subflava) egg signatures facilitate recognition and rejection of parasitic cuckoo finch (Anomalospiza imberbis) eggs. Here, we show that consistency and distinctiveness of patterns are negatively correlated in prinia eggs, perhaps because non-random, repeatable pattern generation mechanisms increase consistency but limit distinctiveness. We hypothesize that pattern properties which are repeatable within individuals but random between individuals ("invariant properties") allow hosts to circumvent this trade-off. To find invariant properties, we develop a method to quantify entire egg phenotypes from images taken from different perspectives. We find that marking scale (a fine-grained measure of size), but not marking orientation or position, is an invariant property in prinias. Hosts should therefore use differences in marking scale in egg recognition, but instead field experiments show that these differences do not predict rejection of conspecific eggs by prinias. Overall, we show that invariant properties allow consistency and distinctiveness to coexist, yet receiver behavior is not optimally tuned to make use of this information.

When perfection isn't enough: host egg signatures are an effective defence against high-fidelity African cuckoo mimicry.

Most mimicry systems involve imperfect mimicry, whereas perfect and high-fidelity mimicry are rare. When the fidelity of mimicry is high, mimics might be expected to have the upper hand against their antagonists. However, in coevolving systems, diversification of model phenotypes may provide an evolutionary escape, because mimics cannot simultaneously match all model individuals in the population. Here we investigate high-fidelity mimicry in a highly specialized, Afrotropical brood parasite-host system: the African cuckoo and fork-tailed drongo. Specifically, we test whether host egg polymorphisms are an effective defence against such mimicry. We show, using a combination of image analysis, field experiments and simulations, that: (1) egg colour and pattern mimicry of fork-tailed drongo eggs by African cuckoos is near-perfect on average; (2) drongos show fine-tuned rejection of foreign eggs, exploiting unpredictable pattern differences between parasitic eggs and their own; and (3) the high degree of interclutch variation (polymorphic egg 'signatures') exhibited by drongos gives them the upper hand in the arms race, with 93.7% of cuckoo eggs predicted to be rejected, despite cuckoos mimicking the full range of drongo egg phenotypes. These results demonstrate that model diversification is a highly effective defence against mimics, even when mimicry is highly accurate.

Eggshell composition and surface properties of avian brood-parasitic species compared with non-parasitic species.

The eggs of avian obligate brood-parasitic species have multiple adaptations to deceive hosts and optimize development in host nests. While the structure and composition of the eggshell in all birds is essential for embryo growth and protection from external threats, parasitic eggs may face specific challenges such as high microbial loads, rapid laying and ejection by the host parents. We set out to assess whether eggshells of avian brood-parasitic species have either (i) specialized structural properties, to meet the demands of a brood-parasitic strategy or (ii) similar structural properties to eggs of their hosts, due to the similar nest environment. We measured the surface topography (roughness), wettability (how well surfaces repel water) and calcium content of eggshells of a phylogenetically and geographically diverse range of brood-parasitic species (representing four of the seven independent lineages of avian brood-parasitic species), their hosts and close relatives of the parasites. These components of the eggshell structure have been demonstrated previously to influence such factors as the risk of microbial infection and overall shell strength. Within a phylogenetically controlled framework, we found no overall significant differences in eggshell roughness, wettability and calcium content between (i) parasitic and non-parasitic species, or (ii) parasitic species and their hosts. Both the wettability and calcium content of the eggs from brood-parasitic species were not more similar to those of their hosts' eggs than expected by chance. By contrast, the mean surface roughness of the eggs of brood-parasitic species was more similar to that of their hosts' eggs than expected by chance, suggesting brood-parasitic species may have evolved to lay eggs that match the host nest environment for this trait. The lack of significant overall differences between parasitic and non-parasitic species, including hosts, in the traits we measured, suggests that phylogenetic signal, as well as general adaptations to the nest environment and for embryo development, outweigh any influence of a parasitic lifestyle on these eggshell properties.

Combined measures of mimetic fidelity explain imperfect mimicry in a brood parasite-host system.

The persistence of imperfect mimicry in nature presents a challenge to mimicry theory. Some hypotheses for the existence of imperfect mimicry make differing predictions depending on how mimetic fidelity is measured. Here, we measure mimetic fidelity in a brood parasite-host system using both trait-based and response-based measures of mimetic fidelity. Cuckoo finches Anomalospiza imberbis lay imperfectly mimetic eggs that lack the fine scribbling characteristic of eggs of the tawny-flanked prinia Prinia subflava, a common host species. A trait-based discriminant analysis based on Minkowski functionals-that use geometric and topological morphometric methods related to egg pattern shape and coverage-reflects this consistent difference between host and parasite eggs. These methods could be applied to quantify other phenotypes including stripes and waved patterns. Furthermore, by painting scribbles onto cuckoo finch eggs and testing their rate of rejection compared to control eggs (i.e. a response-based approach to quantify mimetic fidelity), we show that prinias do not discriminate between eggs based on the absence of scribbles. Overall, our results support relaxed selection on cuckoo finches to mimic scribbles, since prinias do not respond differently to eggs with and without scribbles, despite the existence of this consistent trait difference.

Aggressive hosts are undeterred by a cuckoo's hawk mimicry, but probably make good foster parents.

Parasites face a trade-off if the highest quality hosts are also most resistant to exploitation. For brood parasites, well-defended host nests may be both harder to parasitize and harder to predate, leading to better survival of parasitic chicks. This trade-off could be accentuated if brood-parasitic adaptations to reduce front-line defences of hosts, such as mimicry of hawks by Cuculus cuckoos, do not deter hosts which aggressively mob raptors. Here we investigate the costs and benefits to the African cuckoo (Cuculus gularis) of specializing on a highly aggressive host species, the fork-tailed drongo (Dicrurus adsimilis). Field experiments showed that drongos strongly attacked and mobbed both cuckoo and hawk models, implying that hawk mimicry does not deter front-line defences against African cuckoos. Attacks on cuckoo and hawk models generally declined after the egg stage but attacks on snake models sharply increased, suggesting drongos may treat hawks more like cuckoos than predators. We suggest that the cost to cuckoos of parasitizing an aggressive host may be alleviated by subsequent benefits to their offspring, since drongo nests survived better than nests of other species with similar nesting ecology. These results are indicative of a trade-off between host quality and susceptibility for a brood parasite.

When wax wanes: competitors for beeswax stabilize rather than jeopardize the honeyguide-human mutualism.

Many mutualisms are exploited by third-party species, which benefit without providing anything in return. Exploitation can either destabilize or promote mutualisms, via mechanisms that are highly dependent on the ecological context. Here we study a remarkable bird-human mutualism, in which wax-eating greater honeyguides (Indicator indicator) guide humans (Homo sapiens) to wild bees' nests, in an exchange of knowledge about the location of nests for access to the wax combs inside. We test whether the depletion of wax by mammalian and avian exploiter species either threatens or stabilizes the mutualism. Using camera traps, we monitored feeding visits to wax comb made available following honey harvests. We found that greater honeyguides face competition for wax from conspecifics and nine exploiter species, five of which were not previously known to consume wax. Our results support the hypothesis that heterospecific exploiters stabilize the mutualism, because wax depletion by these competitors probably limits feeding opportunities for conspecific exploiters, favouring the early-arriving individual that guided humans to the bees' nest. These findings highlight the importance of the ecological context of species interactions and provide further evidence for how mutualisms can persist because of, and not in spite of, exploitation by third-party species.

Safeguarding human-wildlife cooperation.

Human-wildlife cooperation occurs when humans and free-living wild animals actively coordinate their behavior to achieve a mutually beneficial outcome. These interactions provide important benefits to both the human and wildlife communities involved, have wider impacts on the local ecosystem, and represent a unique intersection of human and animal cultures. The remaining active forms are human-honeyguide and human-dolphin cooperation, but these are at risk of joining several inactive forms (including human-wolf and human-orca cooperation). Human-wildlife cooperation faces a unique set of conservation challenges, as it requires multiple components-a motivated human and wildlife partner, a suitable environment, and compatible interspecies knowledge-which face threats from ecological and cultural changes. To safeguard human-wildlife cooperation, we recommend: (i) establishing ethically sound conservation strategies together with the participating human communities; (ii) conserving opportunities for human and wildlife participation; (iii) protecting suitable environments; (iv) facilitating cultural transmission of traditional knowledge; (v) accessibly archiving Indigenous and scientific knowledge; and (vi) conducting long-term empirical studies to better understand these interactions and identify threats. Tailored safeguarding plans are therefore necessary to protect these diverse and irreplaceable interactions. Broadly, our review highlights that efforts to conserve biological and cultural diversity should carefully consider interactions between human and animal cultures. Please see AfricanHoneyguides.com/abstract-translations for Kiswahili and Portuguese translations of the abstract.

Honeyguides.

Claire Spottiswoode and colleagues introduce the ancient partnership between wild honeyguides and human honey hunters.

Visual complexity of egg patterns predicts egg rejection according to Weber's law.

Visual complexity is ubiquitous in nature. Drivers of complexity include selection in coevolutionary arms races between antagonists. However, the causes and consequences of biological complexity and its perception are largely understudied, partly because complexity is difficult to quantify. Here, we address this by studying egg pattern complexity and its perception in hosts (tawny-flanked prinia Prinia subflava), which visually recognize and reject mimetic eggs of their virulent brood parasite (cuckoo finch Anomalospiza imberbis). Using field data and an optimization algorithm, we compute a complexity metric which predicts rejection of experimentally placed conspecific eggs in prinia nests. Real cuckoo finch eggs exhibit significantly lower pattern complexity than prinia eggs, suggesting that high complexity benefits hosts because it distinguishes host eggs from parasitic eggs. We show that prinias perceive complexity differences according to Weber's law of proportional processing (i.e. relative, rather than absolute, differences between stimuli are processed in discrimination, such that two eggs with simple patterns are more easily discriminable than two with complex patterns). This may influence coevolutionary trajectories of hosts and parasites. The new methods presented for quantifying complexity and its perception can help us to understand selection pressures driving the evolution of complexity and its consequences for species interactions.

Genetic architecture facilitates then constrains adaptation in a host-parasite coevolutionary arms race.

In coevolutionary arms races, interacting species impose selection on each other, generating reciprocal adaptations and counter adaptations. This process is typically enhanced by genetic recombination and heterozygosity, but these sources of evolutionary novelty may be secondarily lost when uniparental inheritance evolves to ensure the integrity of sex-linked adaptations. We demonstrate that host-specific egg mimicry in the African cuckoo finch Anomalospiza imberbis is maternally inherited, confirming the validity of an almost century-old hypothesis. We further show that maternal inheritance not only underpins the mimicry of different host species but also additional mimetic diversification that approximates the range of polymorphic egg "signatures" that have evolved within host species as an escalated defense against parasitism. Thus, maternal inheritance has enabled the evolution and maintenance of nested levels of mimetic specialization in a single parasitic species. However, maternal inheritance and the lack of sexual recombination likely disadvantage cuckoo finches by stifling further adaptation in the ongoing arms races with their individual hosts, which we show have retained biparental inheritance of egg phenotypes. The inability to generate novel genetic combinations likely prevents cuckoo finches from mimicking certain host phenotypes that are currently favored by selection (e.g., the olive-green colored eggs laid by some tawny-flanked prinia, Prinia subflava, females). This illustrates an important cost of coding coevolved adaptations on the nonrecombining sex chromosome, which may impede further coevolutionary change by effectively reversing the advantages of sexual reproduction in antagonistic coevolution proposed by the Red Queen hypothesis.

Embryo movement is more frequent in avian brood parasites than birds with parental reproductive strategies.

Movement of the embryo is essential for musculoskeletal development in vertebrates, yet little is known about whether, and why, species vary. Avian brood parasites exhibit feats of strength in early life as adaptations to exploit the hosts that rear them. We hypothesized that an increase in embryonic movement could allow brood parasites to develop the required musculature for these demands. We measured embryo movement across incubation for multiple brood-parasitic and non-parasitic bird species. Using a phylogenetically controlled analysis, we found that brood parasites exhibited significantly increased muscular movement during incubation compared to non-parasites. This suggests that increased embryo movement may facilitate the development of the stronger musculoskeletal system required for the demanding tasks undertaken by young brood parasites.

Why and how to apply Weber's Law to coevolution and mimicry.

In mimicry systems, receivers discriminate between the stimuli of models and mimics. Weber's Law of proportional processing states that receiver discrimination is based on proportional, not absolute, differences between stimuli. Weber's Law operates in a variety of taxa and modalities, yet it has largely been ignored in the context of mimicry, despite its potential relevance to whether receivers can discriminate models from mimics. Specifically, Weber's Law implies that for a given difference in stimulus magnitude between a model and mimic, as stimulus magnitudes increase, the mimic will be less discriminable from their model. This implies that mimics should benefit when stimulus magnitudes are high, and that high stimulus magnitudes will reduce selection for mimetic fidelity. Whether models benefit from high stimulus magnitudes depends on whether mimicry is honest or deceptive. We present four testable predictions about evolutionary trajectories of models and mimics based on this logic. We then provide a framework for testing whether receiver discrimination adheres to Weber's Law and illustrate it using coevolutionary examples and case studies from avian brood parasitism. We conclude that, when studying mimicry systems, researchers should consider whether receiver perception conforms to Weber's Law, because it could drive stimulus evolution in counterintuitive directions.

Dehydration risk is associated with reduced nest attendance and hatching success in a cooperatively breeding bird, the southern pied babbler Turdoides bicolor.

High air temperatures have measurable negative impacts on reproduction in wild animal populations, including during incubation in birds. Understanding the mechanisms driving these impacts requires comprehensive knowledge of animal physiology and behaviour under natural conditions. We used a novel combination of a non-invasive doubly labelled water (DLW) technique, nest temperature data and field-based behaviour observations to test effects of temperature, rainfall and group size on physiology and behaviour during incubation in southern pied babblers Turdoides bicolor, a cooperatively breeding passerine endemic to the arid savanna regions of southern Africa. The proportion of time that clutches were incubated declined as air temperatures increased, a behavioural pattern traditionally interpreted as a benefit of ambient incubation. However, we show that (i) clutches had a <50% chance of hatching when exposed to daily maximum air temperatures of >35.3°C; (ii) pied babbler groups incubated their nests almost constantly (99% of daylight hours) except on hot days; (iii) operative temperatures in unattended nests frequently exceeded 40.5°C, above which bird embryos are at risk of death; (iv) pied babblers incubating for long periods of time failed to maintain water balance on hot days; and (v) pied babblers from incubating groups lost mass on hot days. These results suggest that pied babblers might leave their nests during hot periods to lower the risk of dehydration associated with prolonged incubation at high operative temperatures. As mean air temperatures increase and extreme heat events become more frequent under climate change, birds will likely incur ever greater thermoregulatory costs of incubation, leading to compromised nest attendance and increased potential for eggs to overheat, with implications for nest success and, ultimately, population persistence.

Hosts elevate either within-clutch consistency or between-clutch distinctiveness of egg phenotypes in defence against brood parasites.

In host-parasite arms races, hosts can evolve signatures of identity to enhance the detection of parasite mimics. In theory, signatures are most effective when within-individual variation is low ('consistency'), and between-individual variation is high ('distinctiveness'). However, empirical support for positive covariation in signature consistency and distinctiveness across species is mixed. Here, we attempt to resolve this puzzle by partitioning distinctiveness according to how it is achieved: (i) greater variation within each trait, contributing to elevated 'absolute distinctiveness' or (ii) combining phenotypic traits in unpredictable combinations ('combinatorial distinctiveness'). We tested how consistency covaries with each type of distinctiveness by measuring variation in egg colour and pattern in two African bird families (Cisticolidae and Ploceidae) that experience mimetic brood parasitism. Contrary to predictions, parasitized species, but not unparasitized species, exhibited a negative relationship between consistency and combinatorial distinctiveness. Moreover, regardless of parasitism status, consistency was negatively correlated with absolute distinctiveness across species. Together, these results suggest that (i) selection from parasites acts on how traits combine rather than absolute variation in traits, (ii) consistency and distinctiveness are alternative rather than complementary elements of signatures and (iii) mechanistic constraints may explain the negative relationship between consistency and absolute distinctiveness across species.

High temperatures drive offspring mortality in a cooperatively breeding bird.

An improved understanding of life-history responses to current environmental variability is required to predict species-specific responses to anthopogenic climate change. Previous research has suggested that cooperation in social groups may buffer individuals against some of the negative effects of unpredictable climates. We use a 15-year dataset on a cooperative breeding arid zone bird, the southern pied babbler Turdoides bicolor, to test (i) whether environmental conditions and group size correlate with survival of young during three development stages (egg, nestling, fledgling) and (ii) whether group size mitigates the impacts of adverse environmental conditions on survival of young. Exposure to high mean daily maximum temperatures (mean Tmax) during early development was associated with reduced survival probabilities of young in all three development stages. No young survived when mean Tmax > 38°C, across all group sizes. Low survival of young at high temperatures has broad implications for recruitment and population persistence in avian communities given the rapid pace of advancing climate change. Impacts of high temperatures on survival of young were not moderated by group size, suggesting that the availability of more helpers in a group is unlikely to buffer against compromised offspring survival as average and maximum temperatures increase with rapid anthropogenic climate change.