Impacts of UVB radiation on food consumption of forest specialist tadpoles
Introduction
Amphibians are ectotherms characterized by having permeable exposed skin and eggs that may readily absorb substances from the environment (Blaustein and Belden, 2003). Moreover, many species have complex life cycles that can potentially expose them to both aquatic and terrestrial environmental changes (Blaustein and Belden, 2003). In addition, amphibian populations around the world have been suffering a general decline that culminated in the extinction of several species (Stuart et al., 2004). Several factors may be contributing to this phenomenon, such as climate changes (Foden et al., 2013), the pathogenic fungus Batrachochytrium dendobatidis (Carvalho et al., 2017), habitat fragmentation and destruction (Cushman, 2006), release of chemicals (Rissoli et al., 2016), and the introduction of exotic species (Kats and Ferrer, 2003). Besides the agents mentioned above, the increased incidence of ultraviolet (UV) radiation due to stratospheric ozone depletion (Kerr and McElroy, 1993) has been proposed as an important factor for amphibian decline due to its genotoxicity on embryonic and larval stages (Alton et al., 2012, Belden and Blaustein, 2002, Blaustein and Belden, 2003, Blaustein et al., 1994, Schuch et al., 2015a, Schuch et al., 2015b).
The UV component of sunlight, which corresponds to ultraviolet B (UVB, 280–315 nm) and ultraviolet A (UVA, 315–400 nm) wavelengths, can induce cell death and mutagenesis as a consequence of DNA lesions induction, known as pyrimidine dimers (Pfeifer et al., 2005, Schuch and Menck, 2010, Schuch et al., 2015b). The most frequent DNA lesions induced by UVB radiation are the cyclobutane pyrimidine dimers (CPDs), which constitute ∼80–90% of the photoproducts, and pyrimidine-pyrimidone (6-4) photoproducts (6,4PPs), which account for the 10–20% of the UVB lesions (Sancar, 2008). The genotoxicity induced by UVB radiation has been shown to be very detrimental to amphibian species (Schuch et al., 2015a, Schuch et al., 2015b).
According to UV-sensitivity hypothesis, the declining amphibian species have lower resistance to UV radiation due to the lower capacity to repair the UV-induced DNA damage (Blaustein et al., 1999, Blaustein et al., 1994). The DNA damage induced by UV radiation can be repaired by enzymes known as photolyases that use visible/UVA light as an energy source to reverse the DNA damage in an error free process called photoreactivation (Blaustein et al., 1994, Friedberg, 2003). In addition to photolyases, the nucleotide excision repair (NER) pathway can restore the UV-induced DNA damage in a process that needs several proteins and ATP consumption (Sancar and Tang, 1993). However, the role of DNA repair pathways in amphibian decline is still a matter of discussion (Blaustein et al., 1999, Smith et al., 2000, Thurman et al., 2014, Schuch et al., 2015b).
Previous published studies regarding the amphibian foraging behavior were focused on the impact of predation risk, quantity and quality of food (Babbitt, 2001, Eklov and Halvarsson, 2000, Kupferberg, 1997), importance of well-maintained labial tooth row for the feeding knematics (Venesky et al., 2013, Venesky et al., 2010b), as well as on the impacts of Batrachochytrium dendrobatidis infection on tadpole oral disc (Smith and Weldon, 2007) and foraging efficiency (Venesky et al., 2009). Despite the well documented effects of UVB light on tadpoles’ weight (Belden and Blaustein, 2002, Lipinski et al., 2016, Schuch et al., 2015a), there is an absence of works focused on the UVB effects on foraging efficiency, which can have an important role in the tadpoles’ weight loss process. Therefore, considering that the UVB radiation reduces tadpoles’ normal activity (Alton et al., 2012), and the reduced foraging behavior causes tadpoles to consume less food (Anholt et al., 1996, Skelly, 1994), here we hypothesized that UVB exposure leads to weight loss due to the decrease of food consumption. Furthermore, we also evaluated if the food consumption decrease is a consequence of the UVB-induced genomic instability. Additionally, considering the fact that UVB radiation can alter keratin structures (Biniek et al., 2012), it becomes necessary to evaluate if UVB exposure can disturb tadpoles’ food consumption activity due to its impact on the keratinized mouthparts (Venesky et al., 2010b).
In this work we chose the treefrog Hypsiboas curupi [Hylidae, Anura] as a model species to evaluate the effects of UVB radiation on tadpoles’ food consumption and body weight. This treefrog species is restricted to highly forested areas in the Southern Atlantic Rainforest (Iop et al., 2011), which is part of the Brazilian Atlantic Rainforest biodiversity hotspot (Myers et al., 2000). However, this environment has being severely fragmented during the last century (ICMbio, 2012, SEMA, 2014), and many species, including H. curupi, are currently present in both national and state list of endangered species (ICMbio, 2012, SEMA, 2014). After exposures of H. curupi tadpoles to a low solar-simulated UVB radiation dose, the food consumption and the total body mass were evaluated. Furthermore, the genotoxic effect of the UVB treatment was assessed through the quantification of micronucleus formation in collected blood samples. In addition, the impact of UVB exposure on tadpoles’ keratinized labial tooth rows was evaluated. In all the experiments the results obtained with tadpoles kept in the dark after UVB treatment or with tadpoles exposed to a photoreactivation treatment were compared to evaluate the efficiency of DNA repair pathways to restore UVB-induced DNA damage. The obtained results clearly demonstrate the severe impact of UVB treatment on this endangered treefrog species, as well as the importance of future studies aiming to assess the impact of increased levels of solar UVB radiation on declining forest specialist species of the Hylidae family.
Section snippets
Animal collection and maintenance
Four freshly laid egg masses of H. curupi were collected in a stream at the Turvo State Park (TSP) (27°07’–27°16'S, 53°48’–54°04’W), which is a remaining fragment of the Southern Atlantic Rainforest (SEMA, 2005). The egg masses were packed in plastic sac half filled with air and water from the stream and transported to the laboratory at Federal University of Santa Maria. The collected egg masses were put together in the same plastic tank and kept aerated until the beginning of hatching. The
Impact of UVB exposure on tadpoles’ total body mass
The results of the first ratio are shown in Fig. 1A, and the results of the second ratio are presented in Fig. 1B. The statistics are presented in Table 2.
Fig. 1A demonstrates that while non-irradiated tadpoles (CTL) readily gained weight after 24 and 48 h with food ad libitum, tadpoles from both groups UVB D and UVB L have lost weight during these food availability times. On the other hand, Fig. 1B shows that tadpoles from both groups UVB D and UVB L were unable to return to the mass values
Discussion
The negative effects of UVB radiation on H. curupi tadpoles’ body mass (Fig. 1) that were kept in the dark (group UVB D) is in accordance with a previously published work of our group performed with tadpoles of the Hypsiboas pulchellus species (Schuch et al., 2015a). However, the authors demonstrated that H. pulchellus tadpoles exposed to photoreactivation treatment after UVB irradiation did not lose weight. In contrast, our results indicate that even after photoreactivation treatment, the H.
Conclusions
Our results show that UVB radiation exposure reduces the food consumption efficiency and the total body mass of H. curupi tadpoles. Also, the micronuclei frequency was higher in tadpoles submitted to UVB treatments, and it was verified a higher number of A-2 keratinized labial tooth row with deformities in UVB-irradiated tadpoles compared to non-irradiated control tadpoles. Therefore, we suggest a new insight regarding the tadpoles’ weight loss process induced by UVB radiation, and a scheme is
Competing interests
The authors declare no competing or financial interests.
Acknowledgments
We thank to CNPq (Brasília, Brazil) for the financial support (proc. 441407/2014-5) and the Ethics Committee on Animal Use of the Federal University of Santa Maria (022/2013) and the Authorization and Information System on Biodiversity of the Brazilian Ministry of Environment (37928-2) for the access to field sites and for allowing us to conduct the experiments. We also thank to Prof. Dr. Élgion Lúcio da Silva Loreto and Profa. Dra Sonia Zanini Cechin from Federal University of Santa Maria for
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