Visual Crypsis Research Articles

Non-flying mammal pollination in Massonia grandiflora

Pollination by small non-flying mammals occurs in Africa, Australia, Asia and the Neotropics. One hotspot is in the winter rainfall zone of the Cape Floral Region of South Africa. This phenomenon is known for a handful of plant lineages, of which one comprises geoflorous monocots including the tribe Hyacintheae of the Asparagaceae. Small mammal pollination has been documented for four members of the Hyacintheae. A further representative of this taxon, Massonia grandiflora, is hypothesized to be pollinated by small mammals as it shares floral characters with other plants adapted to small mammal pollinators. The study aims at the identification of the pollinators and the characterisation of the floral features of M. grandiflora as well as to experimentally test whether the plants’ nectar scent is an attractant to the flower visitors. With direct observations and video monitoring, we demonstrate the fitting between the head of elephant-shrews and rodents and the bowl-shaped flowers with protruding stigmas and styles as well as pollen transfer from the plants’ anthers on the animals’ body parts that made contact with the stigma. We experimentally show the transfer of pollen surrogates by elephant-shrews and rodents from the anthers via the animals’ fur onto the stigmas of conspecific flowers. Pollen loads on the animals’ snout and in their faeces represent indirect evidence for flower visits. Insects and birds were not observed as nectar consumers. Choice tests revealed that mice and elephant-shrews are attracted by nectar scent. We conclude that the fragrant nectar attracts mice and elephant-shrews as pollinators, whereas its bitterness and viscosity as well as the flowers’ visual crypsis might filter out insects (and birds) as less effective pollinators.

Cryptic polymorphic Proteaceae seeds reduce detection by visually-cued predators on post-fire soils

Plant species with large seeds are susceptible to high levels of seed predation. Seeds of serotinous Proteaceae plants display what appears to be background matching, with polymorphic colours or ornamented surfaces reducing their detectability on certain soil types. We investigated whether seed crypsis (background matching) in Proteaceae seeds can reduce seed predation by visually-cued bird granivores using field observations, seed removal trials and spectrophotometry data. We found no difference in seed predation of winged seeds on different substrates by a diurnal rodent granivore. We therefore ruled out rodent granivores as selective agents driving visual seed crypsis in Cape Proteaceae. Light seeds of most polymorphic Leucadendron seeds showed background matching with their native soils, with granivorous birds predicted to have difficulty distinguishing them apart. Monomorphic Protea seeds with hairs generally do not background match with no reduction in detectability from visually cued predators. This is the first widescale documentation of seed colours and first description of crypsis in the seeds of Cape plants. We suggest that seed colour polymorphisms are adaptations to substrate-specific seed predation biases, with visually-cued bird granivores the likely selective agent driving the visual crypsis of Cape fynbos seeds.

Size-dependent predation risk in cryptic prey

Visual crypsis of prey is determined by the interaction between an individual’s physical appearance to their predators and visual aspects of their environment. Physical size will impact visual appearance and thus potentially influence crypsis. However, research on this topic is limited, leaving the effect of size in cryptic prey largely unexplored. To identify if the success of cryptic phenotypes is size-dependent, we conducted a series of field experiments in which we exposed two types of cryptic artificial prey (uniform colored and disruptively patterned) of different sizes to free-living avian predators and recorded attack rate. Despite similar statistical power and methodology, we found increasing predation risk with increasing size only for disruptive phenotypes. Our results suggest that large sizes may break down ability for disruptive patterns to effectively break up the body outline. However, further research in more controlled conditions would be needed to distinguish the effects of initial detection and post-detection preferences on attack rates.

The evolution of crypsis when pigmentation is physiologically costly

Predation is one of the main selective forces in nature, frequently selecting for crypsis in prey. Visual crypsis usually implies the deposition of pigments in the integument. However, acquisition, synthesis, mobilisation and maintenance of pigments may be physiologically costly. Here, I develop an optimisation model to analyse how pigmentation costs may affect the evolution of crypsis. The model provides a number of predictions that are easy to test empirically. It predicts that imperfect crypsis should be common in the wild, but in such a way that pigmentation is less than what is required to maximise crypsis. Moreover, optimal crypsis should be closer to “maximal” crypsis as predation risk increases and/or pigmentation costs decrease. The model predicts for intraspecific variation in optimal crypsis, depending on the difference in the predation risk or the costs of pigmentation experienced by different individuals.

Crypsis Decreases with Elevation in a Lizard

Predation usually selects for visual crypsis, the colour matching between an animal and its background. Geographic co-variation between animal and background colourations is well known, but how crypsis varies along elevational gradients remains unknown. We predict that dorsal colouration in the lizard Psammodromus algirus should covary with the colour of bare soil—where this lizard is mainly found—along a 2200 m elevational gradient in Sierra Nevada (SE Spain). Moreover, we predict that crypsis should decrease with elevation for two reasons: (1) Predation pressure typically decreases with elevation, and (2) at high elevation, dorsal colouration is under conflicting selection for both crypsis and thermoregulation. By means of standardised photographies of the substratum and colourimetric measurements of lizard dorsal skin, we tested the colour matching between lizard dorsum and background. We found that, along the gradient, lizard dorsal colouration covaried with the colouration of bare soil, but not with other background elements where the lizard is rarely detected. Moreover, supporting our prediction, the degree of crypsis against bare soil decreased with elevation. Hence, our findings suggest local adaptation for crypsis in this lizard along an elevational gradient, but this local adaptation would be hindered at high elevations.

Cryptic petal coloration decreases floral apparency and herbivory in nocturnally closing daisies

AbstractFloral apparency is shaped by both mutualistic and antagonistic interactions that can act in opposing ways. Pollinators are expected to select for more visually apparent flowers, but this likely trades off against the potentially severe fitness costs of damage to apparent flowers by floral herbivores. One way in which flowers that close during parts of the day might circumvent this trade‐off is by evolving less visible lower petal surfaces that are inconspicuous to herbivores when flowers are closed.Here, we used visual system modelling and herbivory experiments to test whether petal surfaces that are exposed when flowers are closed are cryptically coloured. We collected lower and upper petal surface spectra for 77 Asteraceae species from Namaqualand, South Africa. This included closing species that expose their lower petal surfaces for 5–6 daylight hours and non‐closing species that do not expose their lower surfaces. We used these contrasting groups to test the expectation of reduced conspicuousness of lower petal surfaces in closing, but not non‐closing species.By modelling reflectance spectra of petal surfaces against a green leaf background in various visual systems, we showed (a) that conspicuousness of upper petal surfaces to pollinators and various herbivores was strongly correlated, suggesting the potential for fitness trade‐offs between attracting mutualists and antagonists to open flowers, (b) that closing species' lower petal surfaces were less visible to herbivores against a leaf background than those of non‐closing species and (c) that closing species had larger differences between upper and lower petal surface coloration than non‐closing species. Behavioural experiments with tortoise herbivores demonstrated that flowers are easily detected when upper surfaces are exposed, but that tortoises were unable to distinguish lower petal surfaces against a leaf background, resulting in reduced flower herbivory.These results are consistent with selection by herbivores for cryptic coloration of lower petal surfaces, and divergence of coloration between lower and upper petal surfaces in species with closing flowers. Visual crypsis of flowers may be an effective anti‐herbivory strategy during times when pollinators are inactive, and provides an alternative to chemical defence, which often involves costs to pollination.A freePlain Language Summarycan be found within the Supporting Information of this article.

Color‐matching between pollen and corolla: hiding pollen via visual crypsis?

Visual signals attractive to friends may also attract enemies. The bright colors of anthers and pollen have generally been thought to attract pollinators. We hypothesize that visual crypsis of anthers, and particularly pollen, should be favored in flowering plants because protection from pollen collectors reduces the loss of male gametes. To understand adaptive strategies relating to the color of pollen, we measured the color of pollen, undehisced anther sacs, and their background, the corolla, with a spectrometer for 104 insect-pollinated flowering species from a natural community in Hengduan Mountains, southwest China. The colors of anthers, pollen and corollas were diverse in these species. The color diversity of exposed pollen was significantly higher than that of concealed pollen (i.e. where anthers are enclosed or shielded by corollas). The color contrast between pollen and corolla was significantly smaller in species with exposed pollen than in those with concealed pollen. Unlike anther color, exposed pollen color tended to match its background corolla color. Our phylogenetic comparative analysis showed contrasting effects of pollen color patterns between flowers with exposed pollen and those with concealed pollen, revealing a strategy of hiding pollen from pollen thieves via visual crypsis.

Tree selection is linked to locomotor performance and associated noise production in a lizard

AbstractMicrohabitat preference can be an important determinant of individual fitness. Differential use of microhabitats (such as substrate type) can confer or facilitate increased ability to evade or escape predators, and catch prey, for example by influencing sprint speed and noise produced by movement. However, there have been few studies that demarcate whether substrate use influences traits like these. Additionally, the importance of auditory crypsis and locomotor performance for microhabitat selection has been historically under‐studied, especially when compared to the importance of facilitating visual crypsis. We investigate substrate (tree) type use, and the influence of substrate types on both sprint performance and level of noise produced by movement, in fence lizards (Sceloporus undulatus). In our study sites, fence lizards inhabit mixed woodland where deciduous and coniferous trees exist at approximately equal frequency. We show a strong bias in tree use, with lizards being found more frequently on deciduous trees. Using acoustic and video recordings of lizards moving on trees of both types, we demonstrate that lizards sprint faster and their movement appears to generate less noise on deciduous trees, providing a possible basis for their increased use of this tree type. These data suggest that lizards use substrates on which they are more likely to evade auditory detection and can sprint quickly to refuge or capture prey. We conclude that factors other than visual camouflage may be important in determining substrate use and should also be considered in studies of microhabitat selection.

Visual crypsis as a possible function of polymorphic shell coloration in the infaunal clam Ruditapes philippinarum

The infaunal clam Ruditapes philippinarum exhibits highly polymorphic shell coloration, but the function of the coloration remains uncertain. Here, a hypothesis that such shell coloration functions to enhance visual crypsis (i.e., background color matching) in juveniles (<15 mm in shell length) was tested with a combination of a field survey and laboratory experiments. Shell and background colorations were expressed as mean brightness values. Firstly, the association between shell and background brightness was investigated. For this, a field survey for two sympatric subpopulations with distinct substrates was conducted on an intertidal sandflat in western Kyushu, Japan. Secondly, the visual-crypsis hypothesis was tested experimentally using half-valve clam shells filled with paste of raw clam meat as prey and the pufferfish Takifugu niphobles as a visually hunting predator, in a tank with one to two dark-colored substrates and one light-colored substrate. The field survey showed that shell brightness significantly differed between the two sympatric subpopulations of juvenile clams and was positively associated with background brightness. The laboratory experiments indicated that prey items with comparatively light (dark) coloration on dark- (light-) colored substrate were consumed by predators more immediately and at a higher rate than in the color-matched combinations. Consequently, shell–background color matching could help juvenile clams avoid attack from visually hunting predators. The results provide a new insight into effective management planning for this clam species, creating sand habitats with a more matched coloration.

An ambusher's arsenal: chemical crypsis in the puff adder (Bitis arietans).

Ambush foragers use a hunting strategy that places them at risk of predation by both visual and olfaction-oriented predators. Resulting selective pressures have driven the evolution of impressive visual crypsis in many ambushing species, and may have led to the development of chemical crypsis. However, unlike for visual crypsis, few studies have attempted to demonstrate chemical crypsis. Field observations of puff adders (Bitis arietans) going undetected by several scent-orientated predator and prey species led us to investigate chemical crypsis in this ambushing species. We trained dogs (Canis familiaris) and meerkats (Suricata suricatta) to test whether a canid and a herpestid predator could detect B. arietans using olfaction. We also tested for chemical crypsis in five species of active foraging snakes, predicted to be easily detectable. Dogs and meerkats unambiguously indicated active foraging species, but failed to correctly indicate puff adder, confirming that B. arietans employs chemical crypsis. This is the first demonstration of chemical crypsis anti-predatory behaviour, though the phenomenon may be widespread among ambushers, especially those that experience high mortality rates owing to predation. Our study provides additional evidence for the existence of an ongoing chemically mediated arms race between predator and prey species.

Red-throated Caracara, a falconid raptor, rivals predatory impact of army ants on social wasps

Paper wasps are diverse in Neotropical rainforests but the factors that affect their abundance are poorly understood. Army ants (Ecitoninae) are generally thought to have the greatest predatory impact on populations of social wasps, but there is emerging evidence that predatory birds could also be a significant source of colony mortality. Our objectives were to (1) identify the genera of wasps preyed upon by Ibycter americanus (Falconidae), a specialist predator of Neotropical social wasps, (2) quantify wasp nest predation by I. americanus, and (3) compare wasp nest predation rates by I. americanus with calculated rates of wasp nest predation by Eciton burchellii army ants. In 2008 and 2009, we video recorded chick provisioning at I. americanus nests in French Guiana and found that adult birds brought nests of at least ten genera of mainly swarm-founding wasps (Epiponini). In 2012, we noted that three of four sympatric Eciton species raided into trees and thus potentially preyed upon the brood of paper wasps at the same site. We quantified the population density of one Eciton species, calculated its rate of wasp nest predation, and compared this predation rate to that of I. americanus. We conclude that I. americanus rivals the predatory impact of E. burchellii army ants on some populations of Neotropical social wasps. Ibycter americanus and other diurnal vertebrate predators may exert strong selection on wasp defensive behavior, resulting in defensive adaptations that include selection of specific nest sites as well as physical fortification and visual crypsis of nests.

Crypsis in Paraxanthus Barbiger (Decapoda: Brachyura): Mechanisms Against Visual Predators

Marine organisms have evolved a suite of responses to minimize the exposure to predators. Visual crypsis is one such strategy to avoid predation. Paraxanthus barbiger (Poeppig, 1836) is a species that exhibits different color morphotypes over heterogeneous substrates as a means of protection against visual predators. Our main objectives were to quantify the occurrence of color morphotypes over a three-year period and to investigate, via an experimental approach, on the possible mechanisms involved that would provide crypsis to this species. Field surveys occurred over a three-year period at two nearby sites on the central Chilean coast. Initial observations indicated that small juvenile P. barbiger exhibited higher degrees of color polymorphism than larger (> 20 mm carapace width) conspecifics. Furthermore, survival rates of small (< 10 mm carapace width) P. barbiger exposed to predators increased on heterogeneous substrata under both natural and laboratory conditions. Laboratory experiments further demonstrated that newly settled P. barbiger actively select heterogeneous substrata. Hence, cryptic responses of this species might reduce predation-mediated mortality through color pattern disruption of individuals with respect to their environment.

CHEMICAL DISCRIMINATION OF FOOD, CONSPECIFICS AND PREDATORS BY APPARENTLY VISUALLY-ORIENTED DIURNAL GECKOS, NAULTINUS MANUKANUS

Animal life history strategies evolve in response to a range of selective pressures, and often are tightly linked to sensory cues. Squamate reptiles possess well-developed chemosensory systems, which evolved early in their history and remain highly conserved. However, chemosensory abilities are secondarily reduced in primarily visual agamid and chameleonid lizards, which casts doubt on the ubiquity of reliance on chemosensory cues among squamates. Diurnal geckos from New Zealand avoid predators using visual crypsis and are primarily ambush foragers; reliance on visual cues may be a product of strong avian predation pressure and minimal influence from mammals and snakes for the past 80 my. We used New Zealand's diurnal geckos to test the role of local adaptation versus evolutionary conservatism in defining chemosensory systems. Specifically, we tested whether Marlborough green geckos, Naultinus manukanus, use chemoreception to detect and behaviorally respond to (1) food, (2) opposite-sex conspecifics, and (3) native reptilian predators (tuatara, Sphenodon punctatus). Chemosensory cues mediated gecko interactions with all three stimuli tested: (1) the scent of fruit induced greater exploratory behavior, (2) male geckos responded to scent of female conspecifics by increasing lingual sampling and activity, and (3) tuatara fecal cues (but not skin secretions) elicited characteristic antipredator freeze behavior in geckos. Neither the primarily visual life history strategies nor the reduced range of predators of New Zealand's diurnal geckos appears to have reduced their chemosensory abilities relative to other noniguanid squamate reptiles. Instead, our findings support the notion that chemosensory traits remain highly conserved.

DOES VARIABLE COLORATION IN JUVENILE MARINE CRABS REDUCE RISK OF VISUAL PREDATION?

We discovered that newly settled marine rock crabs, Cancer irroratus, exhibit a variety of non-adult colors early in life. This color polymorphism predominates in populations of minute juvenile crabs living in polychromatic habitats where it apparently renders them inconspicuous to visual predators such as fish. Experiments revealed lower frequencies of non-adult color morphs in monochromatic three-dimensional habitats with predators and polychromatic habitats from which predators were excluded. These patterns result from selective predation on visually contrasting color morphs. Adult crabs are monochromatic, conspicuous, and not associated with shelters. Both polymorphic newly settled and monochromatic large individuals occur in environments dominated by small predatory fish where larger adult crabs are at low risk of predation. Behavioral and visual crypsis may only be important early in life when post-settlement mortality is high, and survival at that stage determines recruitment and ultimately population densities. The well-known examples of camouflage among insects usually apply to adults who, unlike these marine counterparts, are small relative to their predators and thus remain vulnerable throughout their lives. Many other large marine crustaceans are cryptic only early in life, suggesting that this early developmental color polymorphism might be an important difference between marine and terrestrial arthropods.

Does Variable Coloration in Juvenile Marine Crabs Reduce Risk of Visual Predation?

We discovered that newly settled marine rock crabs, Cancer irroratus, exhibit a variety of non-adult colors early in life. This color polymorphism predominates in populations of minute juvenile crabs living in polychromatic habitats where it apparently renders them inconspicuous to visual predators such as fish. Experiments revealed lower frequencies of non-adult color morphs in monochromatic three-dimensional habitats with predators and polychromatic habitats from which predators were excluded. These patterns result from selective predation on visually contrasting color morphs. Adult crabs are monochromatic, conspicuous, and not associated with shelters. Both polymorphic newly settled and monochromatic large individuals occur in environments dominated by small predatory fish where larger adult crabs are at low risk of predation. Behavioral and visual crypsis may only be important early in life when post-settlement mortality is high, and survival at that stage determines recruitment and ultimately population densities. The well-known examples of camouflage among insects usually apply to adults who, unlike these marine counterparts, are small relative to their predators and thus remain vulnerable throughout their lives. Many other large marine crustaceans are cryptic only early in life, suggesting that this early developmental color polymorphism might be an important difference between marine and terrestrial arthropods.

Microhabitat use and hindwing phenotype in Hipparchia semele (Lepidoptera, Satyrinae): thermoregulation and background matching

Abstract. 1. Microhabitat use and background matching by adult Hipparchia semele (L.) in a coastal sand dune site in south Wales were studied during the flight period of 1986.2. Microhabitat use by both sexes is related to temperature and activity. When settling substrates are cool, typically during the early morning, most individuals are located on the warmest basking substrate, lichen patches. After a period of warming, males perch to locate mates on exposed areas of sand where there is a large field of view and where they are visually apparent. Egg‐laying females tend to settle on lichen patches throughout the day.3. Overall, females are maximally visually cryptic when settled on lichen patches with unexposed forewings. Male crypsis on lichen is less effective, but greater on most other substrates, than that of females. It is argued that individuals match lichen patches because this substrate is used when they are most liable to detection and capture by vertebrate predators. Male crypsis is probably a compromise between maximizing protection on lichen patches and requirements for resemblance to other substrates.4. The underside hindwing phenotype does not match sand. Background matching to this substrate is probably not important because it tends to be used when individuals are active and can effectively use secondary defence mechanisms.5. It is suggested that the apical eyespot and orange patch on the forewing underside have a dual role in secondary defence, acting as a startling and deflective device, being exposed by disturbed individuals and by those engaged in activities which may disrupt the visual crypsis afforded by the hindwing underside.