Journal of Threatened
Taxa | www.threatenedtaxa.org | 26 February 2022 | 14(2): 20672–20676
ISSN 0974-7907
(Online) | ISSN 0974-7893 (Print)
https://doi.org/10.11609/jott.7558.14.2.20672–20676
#7558 | Received 05
July 2021 | Final received 06 February 2022 | Finally accepted 11 February 2022
Lichens and animal camouflage:
some observations from central Asian ecoregions
Mahmood Soofi
1, Sandeep Sharma 2, Barbod Safaei-Mahroo 3, Mohammad Sohrabi
4 ,
Moosa Ghorbani
Organli 5
& Matthias Waltert 6
1,2,6 Department of Conservation
Biology, University of Goettingen, Bürgerstr. 50, 37073 Goettingen,
Germany.
1 CSIRO Land and Water, PMB 44, Winnellie, Darwin, 0822, Northern Territory, Australia.
3 Pars Herpetologists Institute,
Corner of third Jahad alley, Arash
Str., Jalal-e Ale-Ahmad Boulevard, Tehran, Iran.
4 Department of Biotechnology,
Iranian Research Organization for Science and Technology, Tehran, Iran.
5 Haj-Asadi
alley, 20-Metri-e Jey, Yadegar-e
Emam, Dampezeshki Str.,
Tehran, Iran.
1 mahmood.soofi@biologie.uni-goettingen.de
(corresponding author), 2 sandeeps17@gmail.com, 3 barbodsafaei@gmail.com,
4 sohrabi.mycolich@gmail.com, 5
ghorbanigeo@gmail.com, 6 mwalter@gwdg.de
Editor: Anonymity
requested. Date of
publication: 26 February 2022 (online & print)
Citation: Soofi,
M., S. Sharma, B. Safaei-Mahroo, M. Sohrabi, M.G. Organli & M. Waltert (2022). Lichens and
animal camouflage: some observations from central Asian ecoregions. Journal of Threatened Taxa 14(2): 20672–20676. https://doi.org/10.11609/jott.7558.14.2.20672-20676
Copyright: © Soofi
et al. 2022. Creative Commons Attribution
4.0 International License. JoTT allows unrestricted use, reproduction, and
distribution of this article in any medium by providing adequate credit to the
author(s) and the source of publication.
Funding: See Acknowledgements section.
Competing interests: The authors
declare no competing interests.
Acknowledgements: The work leading to this
publication was supported by the PRIME programme of the German Academic
Exchange Service (DAAD-PRIME, project No. 57436650, 2019-2021) with funds from
the German Federal Ministry of Education and Research (BMBF) and Feodor Lynen
Fellowship of the Alexander von Humboldt Foundation (award No. DEU 1220304
FLF-P, 2021-2023) provided to M.S. There are no conflicts of interests and all
relevant parties involved in the underlying research are either co-authors or
listed in here.
Abstract: Camouflage is
a fitness-relevant trait that
supports survival and fosters evolutionary
adaptation by which animals match
their body pattern to a background
setting. Lichens are among the most
common of these backgrounds that several animal
species use for camouflage. Lichens are omnipresent and grow in wide
arrays of colorations and compositions. Their composition and phenotypic diversity might facilitate cryptic coloration and habitat matching
by various animal species. Here, we describe
the role of lichens in providing
camouflage to various animal species in central Asian and Caucasus mountain
ecoregions, which are categorized as global biodiversity hotspots. Despite multiple ecological studies, no information is available on the role of
this regions‘ lichen diversity in providing animal camouflage. Casual field observations of lichen camouflage
are reported for four (one
mammal and three reptile) species: the Persian Leopard’s
Panthera pardus saxicolor body coat seems to
closely match the colors and
patterns of saxicolous lichens (Acarospora sp. and Circinaria sp.) in their habitat. A similar background matching pattern was observed in both morphs of
the Caucasian Rock Agama Paralaudakia caucasia upon crustose
lichens: Caloplaca spp., Circinaria spp., and the
Radde’s Rock Lizard Darevskia raddei to the crustose lichens
Acarospora sp. and Caloplaca sp. Likewise, the
Horny-scaled Agama’s Trapelus ruderatus grey matches with the
color of multiple lichens (Lecanora spp., Circinaria spp., Protoparmeliopsis spp., Rinodina spp., and Anaptychia
spp.). Our observations preliminarily suggest that lichens
play an important role for species
of different trophic levels, ensuring adaptation and survival through camouflage. We call for more
field-based empirical and experimental studies in various terrestrial ecosystems in other parts of the
world to test the role
of lichens in local adaption and evolutionary plasticity of regional species.
Keywords: Caucasus, climate change,
cryptic coloration, dry ecosystems, Irano-Anatolian,
mammals, plasticity, phenotypic traits, reptiles, saxicolous.
Wildlife
populations of various taxa are experiencing an unprecedented loss worldwide.
The 2020 Global Living Planet Index reported an average 68% decline in the
populations of mammals, birds, amphibians, reptiles, and fishes within a period
of 46 years (1970–2016). Many of the listed species are subjected to
anthropogenic impacts and environmental alterations such as climate change, pollution,
disease, invasive species, and land degradation (Kettlewell
1955; Gomulkiewicz & Holt 1995; Gonzalez et al.
2013; Maxwell et al. 2016). Species persistence may also depend on phenotypic
plasticity or adaptive evolution (Carlson et al. 2014). The inherent genetic
variation in a species may help species to adapt towards stressors if these
exert strong selection pressure (Gonzalez et al. 2013).
One of the
fitness-relevant traits that support survival and foster evolutionary
adaptation is camouflage (Pèrez i
de Lanuza & Font 2016; Cuthill
2019; Price et al. 2019; Smith & Ruxton 2020). Camouflage is a trait or
mechanism by which animals match or tune their body pattern to the background
of their habitat, often varying over time and space and across populations
(Baling et al. 2019; Cuthill 2019; Smith & Ruxton
2020). Animals employ camouflage in multiple ways to facilitate various
strategies including; background matching (i.e., animals resemble the shape of
the habitat background) and disruptive coloration (i.e., developing high
contrast patches to break up the body’s edge). Cryptic coloration and display
of specific behaviours may reduce visual detection or recognition by predators
(Cuthill 2019). Cryptic coloration can occur
seasonally (e.g., as in the form of change of coat colour from brown in summer
to white in winter) and may change with patterns and color
of habitat, affecting the selection of phenotypic traits for crypsis (Mills et al. 2013). A recent study identified
polymorphic regions for some color molting mammal species (e.g., Snowshoe Hare Lepus americanus, Arctic Fox Vulpes lagopus),
suggesting that these regions can function as evolutionary rescue sites in the
rapidly changing world due to climate change (Mills et al. 2013).
The most quoted classic example of rapid
plasticity in response to anthropogenic climate change affecting the
effectiveness of camouflage is that of the Peppered Moth Biston
betularia (Grant & Howlett
1988; Majerus et al. 2000; Cuthill 2019). During the
industrial revolution (ca. 1760–1840), the Silver Birch Trees’ Betula
pendula bark became darker due to pollution (Grant & Howlett 1988). As a result, the melanic forms of the
Peppered Moth (dark) in polluted regions had low predation pressure over
lichen-like individuals (pale speckled), which were easily spotted by their
avian predators due to contrasting dark background. When pollution levels in
these regions declined, and the lichens grew back on the trees, the pale
speckled morphs regained abundance (Kettlewell 1955;
Grant & Howlett 1988). In an experimental study
Walton & Stevens (2018) showed that the pale-speckled form of the Peppered
Moth closely resembles the crustose lichen found on tree barks, making them
less vulnerable to predation by birds, compared to melanic forms. This example
provides striking evidence about the importance of the rapid evolutionary
response of animals to environmental alterations under the influence of strong
selection pressure. It also emphasizes the role of lichens in sustaining
populations by providing important ecosystem services such as camouflage that
helped reversing population decline (Walton & Stevens 2018).
There are
several other examples reported from various parts of the world, where lichens
were employed by various species not only as habitat and food source, but also
for camouflage (Zedda & Rambold
2011). The larvae of insect species such
as Lacewing (Neuroptera: Chrysopidae)
and Bagworm (Lepidoptera: Psychidae) use lichens as
food and camouflage to escape from predators (Skorepa
& Sharp 1971; Cannon 2010). Another
interesting case of lichen camouflage is reported in the nymph of the katydid Lichenodraculus matti
that mimics epiphytic lichens. A species
of beetle Gymnopholus lichenifer
and a land snail species Napaeus barquini use lichens as food and cover their body with
live lichen to actively carry the camouflage with them (Gressit
1977; Allgaier 2007). The Lichen Huntsman Spider Pandercetes gracilis
hides among lichens for predation (Botsford-Comstock 1986; Mukherjee et al.
2010). There are several other species
of frogs and lizards that use tree and rock lichens for camouflage (Braun et
al. 1997; Hocking & Semlitsch 2007; Zedda & Rambold 2011; Sumotha et al. 2012).
Lichens and
animal camouflage in central Asian mountain ecoregion
Lichens are
a symbiotic group of organisms that occur in terrestrial ecosystems. They cover
approximately 8% of the global land surface (Nash 2008), and grow in wide
arrays of colorations, compositions and patterns on substrates such as rocks,
trees or shrubs’ bark, and even anthropogenic material such as concrete (Nash
2008). They are specifically more diverse and abundant in dry high altitude
grasslands and tundra ecosystems (Asplund & Wardle
2017). Lichens are sensitive to a wide range of pollutants and climatic
alterations and thus serve as indicators of ecosystem health (Munzi et al. 2014; Root et al. 2015). For instance, the
depletion of lichens also indicates population decline of Caribou in the arctic
ecosystem (Joly et al. 2009).
Here, we
describe the importance of lichens in providing camouflage to various animal
species of central Asian mountain ecoregion. The Irano-Anatolian,
Caucasus, and central Asian mountains ecoregions are mainly characterized by
vast dry scrublands, grasslands and steppic
mountainous landscapes and are categorized amongst the global biodiversity
hotspots (Olson & Dinerstein 2008; Marchese
2015). These ecoregions are vulnerable to climate change as well as intense
human use (Stone 2015). Despite several long-term ecological studies on many
species from this region, no information is available on the role of regional
lichen species in providing animal camouflage. We here present examples from
four animal species (one mammal and three reptilian) that represent and occupy
different trophic levels in the Irano-Anatolian,
Caucasus, and central Asian mountains ecoregions.
The Persian
Leopard Panthera pardus
saxicolor, synonym: P. p. tulliana
was described by R.I. Pocock in 1927. The etymological meaning of ’saxicolor’ in its scientific name is ‘stone-grey’ or
‘stone-color’ (Pocock 1927). Persian Leopard has a
grey and yellowish-buff coat interspersed with black rosette patterns (Pocock
1927) that seem to closely match and merge with the colors
and patterns of regional saxicolous lichen species such as Acarospora
sp. (Ascosporaceae) and Circinaria
sp. (Megasporaceae) (Image 1), and other families of
lichens including Candelariaceae, Collemataceae,
Lecanoraceae, Lecideaceae, Lichinaceae, Megasporaceae, Parmeliaceae, Physciaceae, Rhizocarpaceae, Teloschistaceae, Umbilicariaceae, and Verrucariaceae
that are also found in their habitat in these ecoregions. The Persian Leopard is an apex predator of
these ecoregions, that inhabits rocky mountainous habitats in western and
central Asia (Jacobson et al. 2016). Their arid and rocky habitat is covered by
saxicolous lichens that help them in camouflage, which is often useful in their
ambush hunting technique. It reduces their chances of visual detection by their
prey species and might improve their ambush predation success.
To further
illustrate the importance of lichens in animal camouflage, we present examples
of three species of reptiles, which are adapted to rocky high steppe habitats.
They are Radde’s Rock Lizard Darevskia
raddei (Lacertidae),
Caucasian Rock Agama Paralaudakia caucasia (Agamidae) and
Horny-scaled Ground Agama Trapelus ruderatus (Agamidae) (Images
1, 2). The Radde’s Rock Lizard is a polymorphic group
of lizards. Their dorsal coloration largely corresponds to the lichen-covered
rocks on which they live. A similar background matching pattern occurs in both
morphs of the Caucasian Rock Agama Paralaudakia
caucasia. The dorsal coloration of both morphs
matches to the crustose lichens Caloplaca sp.
and Circinaria sp. (Image 1c,d). Several
crustose lichens Circinaria sp. (Megasporaceae) and Protoparmeliopsis
sp. (Lecanoraceae) and Rinodina
sp. (Physciaceae) appear to enhance their background
matching (Image 1c). Likewise, the Horny-scaled Agama’s grey head matches with
the color of the following lichens: lim lichen Lecanora sp. (Lecanoraceae), sunken disk lichen Circinaria
sp. (Megasporaceae), Protoparmeliopsis
sp. (Lecanoraceae), and Rinodina
sp. and Anaptychia sp. (Physciaceae).
The dark-orange spots on the dorsal side correspond to the color
and pattern of Caloplaca sp. (Teloschistaceae) (Image 2a). The dorsal coloration of the
Horny-scaled Ground Agama can change seasonally, which also corresponds to
growth stage changes in Verrucaria sp. (Verrucariaceae),
or Anema sp., and or Peccania
sp. (Lichinaceae) (Image 2b).
We
acknowledge that the camouflage of various animal species as described above
due to the lichen species in their habitat might just be a perception due to
limitations of human vision, which is different from what these animal species
and their predators or prey perceive. An experimental study by Majerus et al.
(2000) compared the ultra-violate characteristics of both forms of the Peppered
Moths in the backdrop of foliose and crustose lichens. They report that the
colour patterns of the pale-speckled moth is an effective cryptic match to the
crustose lichen Lecanora conizaeoides, in both human-vision and ultra-violate
visions to the crustose lichens. However, the camouflage behaviour in animals
via matching habitat does not essentially depend on lichens (Walton &
Stevens 2018), because habitat types and their background characteristics can
largely vary across time and space and other factors like vegetation might play
a role in camouflage as well (Baling et al. 2019). For example, the melanic
form of the peppered moth is adapted closely to plain tree barks, whereas the
speckled form adapted to the crustose lichens (Walton & Stevens 2018). In
urban ecosystems, even the plain anthropogenic substrates such as roads and
pavements are voluntarily selected by animal species that can play a crucial
role in their adaptation and population persistence (Camacho et al. 2020).
We conclude
that despite several examples of the role of lichens in animal camouflage for a
handful of faunal species from a few selected ecosystems, there is insufficient
knowledge about lichens and their role in animal camouflage in various
terrestrial ecosystems of the world. Lichens are omnipresent and their species
composition, richness, and phenotypic diversity might facilitate crypsis coloration and habitat matching by various animal
species across different trophic levels. Under variable environments and
changing climate scenarios, these traits would also be able to ensure
adaptation and survival of those species. We therefore call for more field and
experimental studies in various terrestrial ecosystems in other parts of the
world to document more examples of habitat matching by animals utilizing local
lichen species, and the role of lichens in local adaption and evolutionary
plasticity.
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