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Testing of How and Why the Terpios Hoshinota Sponge Kills Stony Corals Siang‑Tai Syue, Chia‑Hsuan Hsu & Keryea Soong*

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Testing of How and Why the Terpios Hoshinota Sponge Kills Stony Corals Siang‑Tai Syue, Chia‑Hsuan Hsu & Keryea Soong* www.nature.com/scientificreports OPEN Testing of how and why the Terpios hoshinota sponge kills stony corals Siang‑Tai Syue, Chia‑Hsuan Hsu & Keryea Soong* An encrusting sponge, Terpios hoshinota, has the potential to infect all species of stony corals in shallow reefs and killing them. It caused a decline in coral coverage in two south‑eastern islands of Taiwan. We proposed two hypotheses to examine how the sponges kill the corals, namely, light blocking and toxins, and tested by in‑situ experiments. The results revealed that both light blocking, sponge toxins, and particularly the combination of both factors were efective at inducing tissue damage in stony corals over a short period. Second, to answer why the sponges killed the corals, we tested two hypotheses, namely, gaining nutrients versus gaining substrates for the sponge. By analyzing the stable isotopes 13C and 15N, as well as exploiting an enrichment experiment, it was possible to determine that only approximately 9.5% of the carbon and 16.9% of the nitrogen in the newly grown sponge tissues originated from the enriched corals underneath. The analysis also revealed that the control corals without isotope enrichment had higher δ13C and δ15N than the control sponges, which was an additional indication that T. hoshinota did not rely heavily on corals for nutrients. Therefore, our results support the hypothesis that the encrusting sponge did not kill corals for food or nutrients, but rather for the substrate. Coral reefs are being threatened by global warming and ocean acidifcation1. In addition, coral diseases and predators have been reported to cause mortality and decline in coral coverage in reefs worldwide 2,3. It remains unclear whether these adverse biological factors are also related to global change, and whether their magnitudes and frequencies may signifcantly contribute to the decline of coral reefs before the physical and chemical efects become manifest4. Sponges are organism that ofen interacts with reef corals; the two groups could interact in the following scenarios: competition when both parties sufer (−, −); predation or parasitism, whereby one sufers but the other benefts (−, +); or mutualism, whereby both parties beneft (+ , +)5. Both groups are sessile, and therefore require a substrate, which is a critical resource in reef habitats6. Both are ofen symbiotic with photosynthetic microbese.g.,7,8 indicating that they may depend on and compete for light as well as energy sources. Teir relationship may be critical to the reef environment when one or both parties become abundant because the dynamics and the future of reefs depends, at least partially, on the relationship. In 2006, a population explosion of an encrusting, black sponge Terpios hoshinota was frst reported in a reef survey of the fringing reefs of Green Island and Orchid Island to the east of Taiwan in the western Pacifc; most of the substrate the sponge covered were once live stony corals9. Te species also caused substantial coral mortality in Guam10, Ryukyu Islands 11, and Yongxing Island 12 and Taiping Island13 in the South China Sea, and has been recorded in a growing number of areas, including American Somoa, Truk Lagoon in Micronesia, Cebu Island in the Philippines, North Mariana Islands, Ryukyu Archipelago, Tailand, Indonesia, Maldives, Mauritius, Palk Bay, and Lizard Island in the Great Barrier Reef10,11,14–21. Despite having several defense mechanisms against benthic neighbors, stony corals appear defenseless when encountering T. hoshinota9,11. Nevertheless, it remains unclear how the sponge kills corals because several types of interaction have been observedsee22. Bryan10 suggested toxins as a possible cause because it was observed that small sponge fragments induce the retraction of the coral polyps, as well as lead to coral tissue death10. Tis hypothesis was supported by the discovery of secondary metabolites isolated from T. hoshinota, such as nakiterpiosin and nakiterpiosinone, which have been reported to have the ability to kill the mouse lymphocytic leukemia cell, P388, in laboratories e.g.,23. However, whether the toxin is released by T. hoshinota when interact- ing with stony corals remains inconclusive. Te second possibility of the killing mechanism is potentially related to the unusual dark color of T. hoshinota see24. Some zooxanthellate corals are known to release ammonia, a nutrient in oligotrophic waters of most coral reef environments, in the dark25. Terefore, it is possible that the black color of T. hoshinota frst evolved as a Department of Oceanography, National Sun Yat-Sen University, Kaohsiung 80424, Taiwan. *email: keryea@mail. nsysu.edu.tw Scientifc Reports | (2021) 11:7661 | https://doi.org/10.1038/s41598-021-87350-4 1 Vol.:(0123456789) www.nature.com/scientificreports/ Treatment/Coral response Bleaching Not afected Terpios hoshinota 9 0 Black cloth 0 9 White cloth 0 7 Table 1. Coral responses in the sponge fragment test. Terpios hoshinota is more likely to cause coral bleaching (T. hoshinota vs. black cloth: p < 0.001; T. hoshinota vs. white cloth: p < 0.001, Chi-square tests). Figure 1. Te color intensity change indices (CICI) of three treatments of the sponge juice experiment. CICI (S + B) > CICI (B) > CICI (T) (n = 19, p < 0.01 in all three pair-wise comparisons, Wilcoxon Signed Rank Tests). S: Sponge, B: Black caps, T: Transparent. mechanism to induce nutrient releasing of corals but resulted in killing corals due to long periods of coverage. Experiments that distinguish darkness from toxins could potentially reveal how the sponge attacks the corals. In addition to proximate factors, such as the killing mechanism, the ultimate factors, i.e., the benefts gained by the sponge from killing corals, could also be investigated. Bryan 10 reported that T. hoshinota grew faster on the massive coral, Porites lutea, than on reef substrate10. Lin and Soong16 reported a similar fnding afer comparing the expansion rates of the sponges on live corals versus those on other substrates16. Te underlying mechanisms could be the nutrients available in coral tissues, although other possibilities, such as the substrate provided by corals, could also be the real incentive for killing the corals. By contrast, Plucer-Rosario14 investigated the growth rates of T. hoshinota on branches of Acropora formosa, comparing live segment controls with segments cleared of tissues14. Te results indicated that the sponge grew faster on the latter, which is incompatible with the nutrient hypothesis. Experiments that focus on various factors (not only growth or expansion rates) could further test the ultimate causes, or the adaptive value of killing corals. Two questions were explored in this study, namely the mechanisms (how) of the sponge, T. hoshinota, and its advantage (why) for killing corals. Two hypotheses were readily available to explain the mechanisms, the light blocking and the toxin hypotheses. It was noted that the two hypotheses were not mutually exclusive. Small patches of darkness and toxins were used in various in-situ experiments. Te adaptive hypotheses for killing the corals were either to gain nutrients or to gain substrates. Results Experiment 1: Sponge fragments. Evidence of bleaching frst occurred 3 days afer the treatment and was only evident in the group with fragments of T. hoshinota. No bleaching was detected in the other 2 groups with the black cloth (to block light) and white cloth (control) (Table 1). Chi-square tests confrmed that the occurrence of bleaching depended on the treatments (p < 0.001 in both tests: sponge fragment vs. black cloth, and sponge fragment vs. white cloth). Experiment 2: Sponge mixture. Signifcant diference in CICI was detected among the 3 treatments (p < 0.001; Friedman Test, n = 19; Fig. 1). Te treatment with sponge and a black cap had the greatest efect, whereas the treatment with the transparent cap demonstrated the smallest response. All 3 pairwise comparisons were signifcant [CICI (sponge and black caps) > CICI (black caps) > CICI (transparent caps), n = 19, p < 0.01 in all 3 pair-wise comparisons, Wilcoxon signed-rank tests]. Scientifc Reports | (2021) 11:7661 | https://doi.org/10.1038/s41598-021-87350-4 2 Vol:.(1234567890) www.nature.com/scientificreports/ Figure 2. Comparison of color intensity change indices (CICI) between “F + B” and “S + B”. Te line in the plot represents Y = X. CICI (S + B) > CICI (F + B) (n = 17, p = 0.028, Wilcoxon Signed Rank Test). F: Fish, B: Black caps, S: Sponge. Figure 3. Te color intensity change indices (CICI) of three treatments in sponge supernatant experiment. CICI (S + B) > CICI (B) = CICI (S) (n = 19, “S + B” vs. “B”: p = 0.055; “S + B” vs. “S”: p < 0.01; “B” vs. “S”: p = 0.12, Wilcoxon Signed Rank Test,). S: Sponge, B: Blackcaps. Experiment 3: Sponge supernatant. Two days afer the treatment, a signifcant diference was detected between the sponge + black cap, and fsh-meat + black cap groups (Fig. 2) with the former showing signifcantly greater efects. Signifcant diference in CICI was observed among the 3 treatments, i.e., only the sponge supernatant, only black caps, and both sponge supernatant and black caps (n = 17; p < 0.01, Friedman Test, Fig. 3), 4 days afer the treatment. Further pair-wise analyses indicated that both factors combined had stronger efects than when single factors were applied [p = 0.055 (against the black cap alone), p < 0.01 (against sponge alone), Wilcoxon signed-rank test, n = 17]. No signifcant diference was observed between the 2 single factors (p = 0.12; Wilcoxon signed-rank test, n = 17). Stable isotope experiment. Six pieces of transplanted corals, 3 from the isotope labeling group, and 3 from the control group, which had been covered by T. hoshinota were successfully retrieved. Te other samples either lost their labels or were not covered by the sponge in the feld. Te control corals had δ13C: − 14.4 ± 1.2‰, δ15N: 4.8 ± 0.6‰ (n = 3).
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