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PeerJ
2018 Mar 15;6:e5891. doi: 10.7717/peerj.5891.
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Novel findings on the impact of chytridiomycosis on the cardiac function of anurans: sensitive vs. tolerant species.
Salla RF
,
Rizzi-Possignolo GM
,
Oliveira CR
,
Lambertini C
,
Franco-Belussi L
,
Leite DS
,
Silva-Zacarin ECM
,
Abdalla FC
,
Jenkinson TS
,
Toledo LF
,
Jones-Costa M
.
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BACKGROUND: Understanding of the physiological effects of chytridiomycosis is crucial to worldwide amphibian conservation. Therefore, we analyzed the cardiac function of two anuran species (Xenopus laevis and Physalaemus albonotatus) with different susceptibilities to infection by the causative agent of chytridiomycosis, Batrachochytrium dendrobatidis (hereafter Bd).
METHODS: We analyzed the in situ heart rate (f H - bpm), relative ventricular mass (RVM -%), and Ca2+ handling in heart of Bd infected animals compared to uninfected controls of both study species.
RESULTS: Bd infection resulted in a 78% decrease in contraction force values in P. albonotatus when compared to the less susceptible X. laevis. This negative effect was even more evident (82%) for the cardiac pumping capacity. The time to reach peak tension was 125% longer in P. albonotatus than in X. laevis, and cardiac relaxation was 57% longer.
DISCUSSION: These results indicate a delay in the cardiac cycle of P. albonotatus on a beat-to-beat basis, which was corroborated by the bradycardia observed in situ. In summary, Bd-sensitive species present impaired cardiac function, which could be a factor in mortality risk. The more pronounced effects of Bd in P. albonotatus may not only result from electrolyte imbalance, as previously reported, but also could be an effect of toxins produced by Bd. For X. laevis, the ability to promote cardiac adjustments seems to be an important homeostatic feature that allows greater tolerance to chytridiomycosis. This study provides new physiological mechanisms underlying the tolerance or susceptibility of amphibian species to chytridiomycosis, which determine their adaptability to survive in the affected environments.
Figure 1. Effects of chytridiomycosis on the Contraction Force.Effects of increasing stimulation frequency on the contraction force (CF: mN mm−2) developed by the ventricular strips of P. albonotatus (1A; Bd−: n = 10, and Bd+: n = 10) and X. laevis (1B; Bd−
n = 8, and Bd+: n = 9). The point values represent mean ± S.E. Blank markers denote significant difference (P < 0.05) between the CF developed by the same species in relation to the initial frequency (0.2 Hz). Significant differences (P < 0.05) between different treatments (Bd− and Bd+) are represented by an asterisk “*” above the error bars of the Bd+ group.
Figure 2. Correlation: Bd load vs. Contraction Force.Correlation between the Bd load acquired by each specimen and the contraction force (CF: mN mm−2) developed by the respective ventricular strips (at 0.2 Hz of stimulation frequency) of P. albonotatus (A: Line equation y = 20.986 × − 0.617; r2 = 0.8999) and X. laevis (note that there was no correlation for this species).
Figure 3. Cardiac pumping capacity of control and infected animals.Effect of the successive increase in stimulation frequencies on the cardiac pumping capacity (CPC: mN mm−2 min−1) developed by the ventricular strips of P. albonotatus (A: squares represent Bd− group - n = 10, and circles represent Bd+ group - n = 10) and X. laevis (B: squares represent Bd− group - n = 8, and triangles represent Bd+ group : n = 9). Points represent the means ± S.E. White markers denote significant difference (Tukey-Kramer test - P < 0.05) between the CPC developed by the same species at each stimulation frequency in relation to the initial frequency (0.2 Hz). Significant differences (Dunnett’s test - P < 0.05) between different treatments (Bd− and Bd+) were observed only in P. albonotatus, in all stimulation frequencies.
Figure 4. Time to peak tention and to relaxation of control and infected P. albonotatus.Effect of increased stimulation frequency over the time to reach peak tension (A: TPT - ms;) and the time to reach 50% of relaxation (B: THR - ms) of the ventricular strips of P. albonotatus (squares represent Bd− group - n = 10, and circles represent Bd+ group - n = 10). The points represent mean values ±SE. Significant differences (Dunnett’s test - P < 0.05) between different treatments (Bd− and Bd+) were observed in TPT and THR of P. albonotatus, in all stimulation frequencies. Note different scales in the figures.
Figure 5. Time to peak tention and relaxation of heart strips os control and infected X. laevis.Effect of increased stimulation frequency over time to reach the peak tension (A: TPT - ms) and the time to reach 50% of relaxation (B: THR - ms) of the ventricular strips of X. laevis (squares represent Bd− group - n = 8, and triangles represent Bd+ group - n = 9). The points represent the mean values ± S.E. White markers denote significant difference (Tukey-Kramer test - P < 0.05) between the TPT or THR developed by the same species at each stimulation frequency in relation to the initial frequency (0.2 Hz). There were no significant differences (Dunnett’s test - P > 0.05) between different treatments (Bd− and Bd+) TPT and THR.
Figure 6. Comparative diagram of Bd infection effects in P. albonotatus and X. laevis.Comparative diagram of Bd infection (% of Bd− at 0.2 Hz) of P. albonotatus (black bars) and X. laevis (white bars) in relation to the in vitro parameters (CF, CPC, TPT and THR). The values within the bars represent the percentage differences of each parameter obtained to the infected animals (Bd−) at 0.2 Hz in relation to their respective controls (Bd−). Significant differences (P < 0.05) were observed between species in all the parameters analyzed.
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