Persistence of Chironomids in Metal Polluted Andean High Altitude Streams: Does Melanin Play a Role?

Loayza‐Muro, Raúl; Marticorena-Ruíz, Jenny K.; Palomino, Edwin J.; Merritt, Camille; Baat, Milo L. de; Gemert, M. van; Verweij, Rudo A.; Kraak, Michiel H.S.; Admiraal, Wim

doi:10.1021/es302779b

Cited by 17 publications

(20 citation statements)

References 46 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…However, pigmentation in these species is not known to be plastic. Since G. maculosus can self-fertilize, the capacity of an individual to express either black or brown phenotype in response to differential UV exposure may have been selected over non-plastic melanic morphs, which are known to occur as adaptations to altitudinal gradients in UV intensity in some lizards [12] and insects [57–59]. Skin colour in G. maculosus most likely plays a photoprotective role, leading to incidental camouflage against the different substrate types of each habitat.…”

Section: Discussionmentioning

confidence: 99%

Quantifying phenotype-environment matching in the protected Kerry spotted slug (Mollusca: Gastropoda) using digital photography: exposure to UV radiation determines cryptic colour morphs

et al. 2017

View full text Add to dashboard Cite

BackgroundAnimal colours and patterns commonly play a role in reducing detection by predators, social signalling or increasing survival in response to some other environmental pressure. Different colour morphs can evolve within populations exposed to different levels of predation or environmental stress and in some cases can arise within the lifetime of an individual as the result of phenotypic plasticity. Skin pigmentation is variable for many terrestrial slugs (Mollusca: Gastropoda), both between and within species. The Kerry spotted slug Geomalacus maculosus Allman, an EU protected species, exhibits two distinct phenotypes: brown individuals occur in forested habitats whereas black animals live in open habitats such as blanket bog. Both colour forms are spotted and each type strongly resembles the substrate of their habitat, suggesting that G. maculosus possesses camouflage.ResultsAnalysis of digital images of wild slugs demonstrated that each colour morph is strongly and positively correlated with the colour properties of the background in each habitat but not with the substrate of the alternative habitats, suggesting habitat-specific crypsis. Experiments were undertaken on laboratory-reared juvenile slugs to investigate whether ultraviolet (UV) radiation or diet could induce colour change. Exposure to UV radiation induced the black (bog) phenotype whereas slugs reared in darkness did not change colour. Diet had no effect on juvenile colouration. Examination of skin tissue from specimens exposed to either UV or dark treatments demonstrated that UV-exposed slugs had significantly higher concentrations of black pigment in their epithelium.ConclusionsThese results suggest that colour dimorphism in G. maculosus is an example of phenotypic plasticity which is explained by differential exposure to UV radiation. Each resulting colour morph provides incidental camouflage against the different coloured substrate of each habitat. This, to our knowledge, is the first documented example of colour change in response to UV radiation in a terrestrial mollusc. Pigmentation appears to be correlated with a number of behavioural traits in G. maculosus, and we suggest that understanding melanisation in other terrestrial molluscs may be useful in the study of pestiferous and invasive species. The implications of colour change for G. maculosus conservation are also discussed.Electronic supplementary materialThe online version of this article (doi:10.1186/s12983-017-0218-9) contains supplementary material, which is available to authorized users.

show abstract

Section: Discussionmentioning

confidence: 99%

Quantifying phenotype-environment matching in the protected Kerry spotted slug (Mollusca: Gastropoda) using digital photography: exposure to UV radiation determines cryptic colour morphs

et al. 2017

View full text Add to dashboard Cite

show abstract

“…The presence of only one species in metal-rich streams may indicate a strong reduction in genetic variability, as previously described for populations of invertebrates inhabiting sites heavily contaminated by metals (van Straalen & Timmermans, 2002;Fratini et al, 2008;Ungherese et al, 2010). Recently, it was observed that chironomids from higher altitudes and from metalrich sites in the Andes contained more melanin than species from reference and from lower sites, which suggests that melanin may function both as a UV-B radiation protector and metal chelator (Loayza-Muro et al, 2013). Physiological adjustments may be responsible for such tolerance, since Chironomus species from contaminated sites are better able to regulate their body concentrations of metals than other taxa (Krantzberg & Stokes, 1989).…”

Section: Discussionmentioning

confidence: 62%

“…Physiological adjustments may be responsible for such tolerance, since Chironomus species from contaminated sites are better able to regulate their body concentrations of metals than other taxa (Krantzberg & Stokes, 1989). Allocation of energy towards tolerance mechanisms, such as metal-binding metallothioneins (Gillis, Reynoldson & Dixon, 2006), melanin production or cuticle sclerotisation in chironomids (Loayza-Muro et al, 2013), may enforce a trade-off evidenced in a reduced growth (Sibly & Calow, 1989). Genetic adaptation has also been considered as a general mechanism of metal tolerance in insects from heavily polluted environments, including Chironomus species (Groenendijk et al, 2002;van Straalen & Timmermans, 2002).…”

Section: Discussionmentioning

confidence: 99%

“…Penetration of biologically active UV radiation into the water is accentuated by the sparse riparian canopy providing hardly any shade and by high water transparency due to low levels of dissolved organic matter (Laurion et al, 2000;Kelly, Clare & Bothwell, 2001;Clements et al, 2008). Indeed, the maximum UV-B levels E-mails: raul.loayza@upch.pe; raulloayza@hotmail.com in this region, particularly in the dry season (Loayza-Muro et al, 2013), are well above those causing significant drift and mortality of invertebrates in artificial streams and structuring natural invertebrate communities in other mountain areas (Kiffney, Clements & Cady, 1997b;Kiffney, Little & Clements, 1997a).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Metals and altitude drive genetic diversity of chironomids in Andean streams

et al. 2013

Self Cite

View full text Add to dashboard Cite

Summary Andean streams cover steep altitude gradients and locally leach metal‐rich bedrock, creating highly selective habitat conditions. Chironomids are among the few dominant insect taxa present under the harshest conditions in Andean high altitude streams, but it remains unclear whether their dominance is due to the adaptive capacity of a few species (population differentiation) or to a diversity of species with different capacities to cope with environmental extremes (species composition). Therefore, the aim of this study was to assess whether metals and altitude drive the genetic diversity of chironomids in Andean streams. We measured metal concentrations and altitude‐related conditions, such as UV‐B radiation, water temperature and oxygen, in reference and metal‐rich streams located at both 3000 and 4000 m a.s.l. The genetic composition of the chironomid communities from these streams was determined by mitochondrial cytochrome oxidase I (COI) gene sequencing, and a phylogenetic tree was constructed. The concentrations of all metals were higher in the metal‐rich streams than in the references streams. The UV‐B radiation level at 4000 m was notably higher than at 3000 m, while the water temperature followed the opposite trend. At 3000 m, the reference site was inhabited by six putative species, completely different from the three present at 4000 m. Only one putative species, which did not occur at the reference sites, was present at both the metal‐rich sites at 3000 and 4000 m. The differences in putative species composition between 3000 and 4000 m indicated a strong sorting of species according to altitude. However, the unique putative species present at the metal‐rich sites at both 3000 and 4000 m indicated that altitude‐driven selection was overridden by the extreme selection pressure exerted by metal exposure. We conclude that altitude limits the distribution of chironomid taxa, but metal selection leads to predominance of a unique metal‐tolerant taxon.

show abstract

“…In the high Andes (>3000 m), UV-B radiation presents a strong temporal and spatial variation, increasing with altitude and being particularly intense during the summer, when radiation peaks and reduced cloudiness and shallow water leave benthic communities more exposed to solar radiation (Cabrera, Bozzo & Fuenzalida, 1995;Zaratti, 2003;Loayza-Muro et al, 2013). Given these strong UV-B gradients, we hypothesised that pigment concentration in macroinvertebrates may be an adaptive response to particularly high UV-B radiation, especially during the dry season at the highest altitude sites.…”

Section: Introductionmentioning

confidence: 99%

Ultraviolet‐B‐driven pigmentation and genetic diversity of benthic macroinvertebrates from high‐altitude Andean streams

et al. 2013

Self Cite

View full text Add to dashboard Cite

1. Photoprotective pigments in benthic macroinvertebrates may reduce the damage caused by the blistering UV-B radiation in Andean high-altitude streams above 3500 m. The aim of this study was therefore to determine whether melanisation in macroinvertebrates inhabiting high-altitude Andean streams is an adaptive response to high UV-B radiation. To explore whether altitude-related differences in melanin concentration between taxa were due to a variable community composition or due to population differentiation, mayfly species were identified genetically. 2. We measured UV-B radiation from 650 to 4000 m and compared body melanin concentrations from several benthic macroinvertebrate orders sampled at these altitudes. Five genera belonging to the mayfly family Baetidae were genetically identified to the species level. DNA sequencing was performed in individual larval legs to group genetically similar individuals before pigment analysis in the corresponding bodies. 3. The UV-B radiation at 4000 m was twice that at 3200 m, four times that at 1900 m and five times that at 650 m. The melanin concentration in families belonging to Ephemeroptera, Trichoptera, Diptera and Turbellaria was twice as high at 4000 m as at 3200 m, but did not differ among taxa or between seasons. Five genera of the family Baetidae were identified: Americabaetis, Dactylobaetis, Tupiara, Baetodes and Thraulodes. Genetic differences were evident between Americabaetis sp. at 4000 m from the Cordillera Blanca and at 3200 m from the R ımac River valley, and between Tupiara taxa at 650 and 1900 m in the R ımac River. In Americabaetis, melanin increased fivefold from 1900 to 4000 m, while in Dactylobaetis and Tupiara, it was twice as high at 1900 m as at 650 m. In Baetodes, melanin at 4000 m was twice that at 650 and 1900 m, while in Thraulodes, it was almost three times higher at 4000 m than at 3200 m. 4. In Tupiara, the differences in melanin levels were probably associated with species with different vertical distribution, while in Dactylobaetis, these differences were interpreted as phenotypic plasticity. Our results thus indicate that mayfly species within a single family have both constitutive and adjustable melanin concentrations, enabling them to cope with the strong selective UV-B environment. Adjustable melanin levels have commonly been observed under moderate UV-B regimes, while the constitutive, high melanin concentration is probably an attribute of high-altitude invertebrate fauna in the tropics.

show abstract

Persistence of Chironomids in Metal Polluted Andean High Altitude Streams: Does Melanin Play a Role?

Cited by 17 publications

References 46 publications

Quantifying phenotype-environment matching in the protected Kerry spotted slug (Mollusca: Gastropoda) using digital photography: exposure to UV radiation determines cryptic colour morphs

Quantifying phenotype-environment matching in the protected Kerry spotted slug (Mollusca: Gastropoda) using digital photography: exposure to UV radiation determines cryptic colour morphs

Metals and altitude drive genetic diversity of chironomids in Andean streams

Ultraviolet‐B‐driven pigmentation and genetic diversity of benthic macroinvertebrates from high‐altitude Andean streams

Contact Info

Product

Resources

About