Abstract
Logging and human-induced conversion of natural forests into agricultural areas are major drivers of biodiversity loss in the tropics. Anuran larvae can be highly diverse, can reach high biomass and can play important roles in tropical streams; yet, compared to the adult frog communities, relatively little is known about how larval communities respond to disturbance. Information on larvae is highly relevant for amphibian conservation because larvae represent direct evidence of breeding and thus provide a good indicator of species persistence in disturbed habitats. We studied tadpole assemblages in Ranomafana, southeastern part of Madagascar, in streams in a disturbed forest (previously logged forest), at “forest edge” (streams embedded in matrix nearby forest blocks), and compared these to communities in a primary forest. We sampled tadpoles at the microhabitat level (“pools” and “riffles”) in 9 streams. We recorded 27 species with a maximum of 17 species/stream recorded at edge. The three habitats harbored different assemblages, but, as could be expected, more similarities existed among forest habitats than between forest and non-forest habitats. The most and the least diverse communities were recorded at edge and in the disturbed forest, respectively. Assemblages were dominated by one generalist species, and changes in communities were mostly driven by changes in forest specialists, which either decreased in disturbed forest or were replaced by edge specialists outside forest. Although species richness varied, relative abundances were maintained among habitats, suggesting potential compensatory mechanisms in tadpole biomass. Community structure changed at the microhabitat level: pool environments usually harbored relatively higher species richness and abundance than riffles. Our study highlights the relevance of edge habitats for maintaining amphibian diversity and the pronounced negative effects of past logging activities on tadpole communities. Given the diverse roles of tadpoles in streams, changes in community structure potentially affect critical stream ecosystem processes. The study has strong implications for designing buffer zones around protected areas.
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Acknowledgements
This study was supported by JSPS KAKENHI No. 26640137, the Graduate School of Environmental Studies of Nagoya University, and the Ministry of Education, Sports and Culture of the Government of Japan. The study was conducted under the research permit 256/15/MEEMF/SG/DGF/DAPT/SCBT. We are indebted to Justin Solo for assisting in the fieldwork. Yoda Ken and Kenichiro Sugitani provided valuable comments on earlier drafts of the manuscript. We thank Rio Heriniaina for making the map. We are grateful to the Ethology lab of Kyoto University for hosting N. Ramamonjsoa at the time of finalizing the manuscript. We thank Eileen Larney, MICET/ICTE, and Centre Valbio Ranomafana for logistic supports. We are grateful to Madagascar National Parks and the Ministry of Forest and Environment Madagascar for their collaboration.
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Appendices
Appendix 1
Species of tadpole recorded in streams in primary forest, disturbed forest (selectively logged forest), and at forest edge in Ranomafana.
Mouthpart cluster | IUCN status | |
|---|---|---|
Boophis albilabris | Boophis–generalized | LC |
Boophis andohahela | Suctorial | VU |
Boophis elenae | Boophis–generalized | NT |
Boophis luciae | Suctorial | LC |
Boophis luteus | Boophis–generalized | LC |
Boophis madagascariensis | Boophis–generalized | LC |
Boophis marojezensis | Suctorial | LC |
Boophis narinsi | Boophis–generalized | EN |
Boophis periegetes | Boophis–generalized | NT |
Boophis picturatus | Sand-eater | LC |
Boophis quasiboehmei | Boophis–generalized | NA |
Boophis reticulatus | Boophis–generalized | LC |
Boophis sp. 37 (aff. elenae) | Boophis–generalized | DD |
Boophis tasymena | Boophis–generalized | LC |
Guibemantis liber | Gu.–podgy | LC |
Gephyromantis ventrimatulatus | Ge.–non-feeding | LC |
Mantidactylus aerumnalis | Funnel mouthed | LC |
Mantidactylus betsileonis | Md. generalized | LC |
Mantidactylus majori | Reduced teeth | LC |
Mantidactylus melanopleura | Funnel mouthed | LC |
Mantidactylus opiparus | Md.–funnel mouthed | NA |
Mantidactylus sp. 47 (aff. mocquardi) | Md.–reduced teeth | NA |
Mantidactylus sp. 28 (aff. betsileanus) | Md.–generalized | NA |
Mantidactylus sp. 48 (aff. cowani small) | Md.—fossorial | NA |
Spinomantis aglavei | Spinomantis–generalized | LC |
Spinomantis peraccae | Spinomantis–generalized | LC |
Spinomantis sp2 (fimbriatus) | Spinomantis–generalized | DD |
Appendix 2
Pairwise differences following per MANOVA on species composition between the three habitats.
2014
Primary forest | Disturbed forest | Edge | |
|---|---|---|---|
Primary forest | 0.0003 | 0.0003 | |
Disturbed forest | 0.0003 | 0.0003 | |
Edge | 0.0003 | 0.0003 |
2015
Primary forest | Disturbed forest | Edge | |
|---|---|---|---|
Edge | 0.0003 | 0.0003 | |
Disturbed forest | 0.0003 | 0.0003 | |
Primary forest | 0.0003 | 0.0003 |
Appendix 3
SIMPER analyses on species compositional similarities between primary forest, disturbed forest, and edge.
2014
Primary versus disturbed forests | Primary forest versus edge | Disturbed forest versus edge | |||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|
Overall average dissimilarity 35.43 | Overall average dissimilarity 61.25 | Overall average dissimilarity 54.19 | |||||||||
Taxon | Av. dissim | Contrib. % | Cumulative % | Taxon | Av. dissim | Contrib. % | Cumulative % | Taxon | Av. dissim | Contrib. % | Cumulative % |
M. sp47 | 3.885 | 10.97 | 10.97 | B. picturatus | 7.041 | 11.49 | 11.49 | B.andohahela | 7.095 | 13.09 | 13.09 |
B. reticulatus | 3.704 | 10.45 | 21.42 | B. andohahela | 5.839 | 9.533 | 21.03 | B.picturatus | 6.178 | 11.4 | 24.49 |
M. sp28 | 3.627 | 10.24 | 31.66 | B. elenae | 4.777 | 7.798 | 28.82 | B.elenae | 5.35 | 9.872 | 34.37 |
Spinomantisaglavei | 3.394 | 9.579 | 41.24 | M. sp47 | 3.513 | 5.735 | 34.56 | M.melanopleura | 3.81 | 7.03 | 41.4 |
M. majori | 3.211 | 9.063 | 50.3 | B. reticulatus | 3.487 | 5.693 | 40.25 | M.sp28 | 3.693 | 6.814 | 48.21 |
S. peraccae | 3.103 | 8.758 | 59.06 | M. melanopleura | 3.448 | 5.628 | 45.88 | B.tasymena | 3.604 | 6.651 | 54.86 |
G. liber | 2.401 | 6.775 | 65.83 | B. tasymena | 3.244 | 5.297 | 51.18 | B.madagascariensi | 3.373 | 6.225 | 61.09 |
M. opiparus | 2.322 | 6.553 | 72.38 | B. madagascariensis | 3.005 | 4.905 | 56.08 | M.sp47 | 3.356 | 6.192 | 67.28 |
M. melanopleura | 2.188 | 6.174 | 78.56 | M. majori | 2.988 | 4.879 | 60.96 | B.reticulatus | 2.9 | 5.351 | 72.63 |
B. madagascariensis | 2.121 | 5.987 | 84.55 | S. peraccae | 2.822 | 4.606 | 65.57 | B.sp37 | 2.517 | 4.645 | 77.27 |
B. picturatus | 1.793 | 5.061 | 89.61 | M. sp28 | 2.581 | 4.213 | 69.78 | S.aglavei | 2.396 | 4.422 | 81.7 |
M. sp48 | 1.017 | 2.87 | 92.48 | G. liber | 2.46 | 4.016 | 73.8 | B.marojejiensis | 1.993 | 3.677 | 85.37 |
M. aerumnalis | 0.9716 | 2.742 | 95.22 | S. aglavei | 2.455 | 4.007 | 77.8 | B.luteus | 1.927 | 3.556 | 88.93 |
B. andohahela | 0.7137 | 2.014 | 97.23 | M. opiparus | 2.269 | 3.704 | 81.51 | B.periegetes | 0.9834 | 1.815 | 90.74 |
S. sp2 | 0.4375 | 1.235 | 98.47 | B. sp37 | 2.246 | 3.667 | 85.18 | M.opiparus | 0.7639 | 1.41 | 92.15 |
B. albilabris | 0.2847 | 0.8035 | 99.27 | B. marojejiensis | 1.792 | 2.926 | 88.1 | B.luciae | 0.7536 | 1.391 | 93.55 |
G. ventrimaculatus | 0.2585 | 0.7296 | 100 | B. luteus | 1.738 | 2.837 | 90.94 | B.narinsi | 0.6946 | 1.282 | 94.83 |
B. tasymena | 0 | 0 | 100 | M. sp48 | 0.9557 | 1.56 | 92.5 | B.albilabris | 0.6642 | 1.226 | 96.05 |
B. sp37 | 0 | 0 | 100 | M. aerumnalis | 0.8982 | 1.466 | 93.96 | Guibemantisliber | 0.6642 | 1.226 | 97.28 |
B. narinsi | 0 | 0 | 100 | B. periegetes | 0.8855 | 1.446 | 95.41 | M.majori | 0.5797 | 1.07 | 98.35 |
B. marojejiensis | 0 | 0 | 100 | B. albilabris | 0.8192 | 1.337 | 96.75 | M.betsileonis | 0.345 | 0.6366 | 98.98 |
B. quasiboehmei | 0 | 0 | 100 | B. luciae | 0.6677 | 1.09 | 97.84 | S.peraccae | 0.2842 | 0.5244 | 99.51 |
M. betsileonis | 0 | 0 | 100 | B. narinsi | 0.622 | 1.015 | 98.85 | G.ventrimaculatus | 0.2658 | 0.4906 | 100 |
B. periegetes | 0 | 0 | 100 | S. sp2 | 0.3935 | 0.6423 | 99.5 | S.sp2 | 0 | 0 | 100 |
B. luciae | 0 | 0 | 100 | M. betsileonis | 0.3092 | 0.5048 | 100 | M.aerumnalis | 0 | 0 | 100 |
B. luteus | 0 | 0 | 100 | G. ventrimaculatus | 0 | 0 | 100 | B.quasiboehmei | 0 | 0 | 100 |
B. elenae | 0 | 0 | 100 | B. quasiboehmei | 0 | 0 | 100 | M.sp48 | 0 | 0 | 100 |
2015
Primary versus disturbed forests | Primary forest versus edge | Disturbed forest versus edge | |||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|
Overall average dissimilarity 41.55 | Overall average dissimilarity 66.88 | Overall average dissimilarity 62.67 | |||||||||
Taxon | Av. dissim | Contrib. % | Cumulative % | Taxon | Av. dissim | Contrib. % | Cumulative % | Taxon | Av. dissim | Contrib. % | Cumulative % |
B. msis | 6.568 | 15.81 | 15.81 | B. andohahela | 10.72 | 16.03 | 16.03 | B. andohahela | 13.22 | 21.1 | 21.1 |
M. sp47 | 4.673 | 11.25 | 27.05 | B. elenae | 9.232 | 13.8 | 29.84 | B. elenae | 11.34 | 18.09 | 39.19 |
B. reticulatus | 4.64 | 11.17 | 38.22 | B. picturatus | 9.21 | 13.77 | 43.61 | B. picturatus | 9.602 | 15.32 | 54.51 |
G. liber | 4.548 | 10.94 | 49.16 | M. melanopleura | 6.039 | 9.029 | 52.64 | M. melanopleura | 8.228 | 13.13 | 67.64 |
M. melanopleura | 4.465 | 10.74 | 59.91 | B. msis | 5.893 | 8.811 | 61.45 | B. reticulatus | 5.731 | 9.145 | 76.79 |
S. aglavei | 3.999 | 9.623 | 69.53 | B. reticulatus | 4.727 | 7.068 | 68.52 | B. msis | 5.362 | 8.556 | 85.34 |
S. peraccae | 3.955 | 9.517 | 79.05 | G. liberH | 4.235 | 6.332 | 74.85 | M. sp47 | 4.407 | 7.032 | 92.37 |
B. picturatus | 2.9 | 6.979 | 86.03 | M. sp47 | 3.964 | 5.926 | 80.78 | B. quasiboehmei | 1.715 | 2.737 | 95.11 |
M. majori | 1.485 | 3.575 | 89.6 | S. peraccae | 3.691 | 5.519 | 86.3 | M. sp48 | 1.641 | 2.618 | 97.73 |
M. sp48 | 1.362 | 3.278 | 92.88 | S. aglavei | 3.599 | 5.382 | 91.68 | S. aglavei | 0.5134 | 0.8192 | 98.55 |
B. quasiboehmei | 1.161 | 2.795 | 95.67 | M. sp48 | 1.85 | 2.766 | 94.44 | M. opiparus | 0.4553 | 0.7266 | 99.27 |
M. opiparus | 1.028 | 2.473 | 98.15 | M. majori | 1.378 | 2.061 | 96.5 | G. ventrimaculatus | 0.4553 | 0.7266 | 100 |
G. ventrimaculatus | 0.4085 | 0.983 | 99.13 | B. quasiboehmei | 1.363 | 2.038 | 98.54 | M. sp28 | 0 | 0 | 100 |
M. sp28 | 0.3613 | 0.8696 | 100 | M. opiparus | 0.6333 | 0.947 | 99.49 | S. peraccae | 0 | 0 | 100 |
B. elenae | 0 | 0 | 100 | M. sp28 | 0.341 | 0.5098 | 100 | G. liber | 0 | 0 | 100 |
B. andohahela | 0 | 0 | 100 | G. ventrimaculatus | 0 | 0 | 100 | M. majori | 0 | 0 | 100 |
Appendix 4
Sampling design
In each habitat, we sampled three streams. In each stream, we sampled tadpoles in 4 pools and in 4 riffles.
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Ramamonjisoa, N., Sakai, M., Ndriantsoa, S.H. et al. Hotspots of stream tadpole diversity in forest and agricultural landscapes in Ranomafana, Madagascar. Landscape Ecol Eng 16, 207–221 (2020). https://doi.org/10.1007/s11355-020-00407-w
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DOI: https://doi.org/10.1007/s11355-020-00407-w