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Ecology, management and conservation in natural and modified habitats
RESEARCH ARTICLE

How the goitered gazelle (Gazella subgutturosa) adapts to isolated island: from the perspective of habitat and food

Yuan Wang https://orcid.org/0009-0002-8510-8602 A # , Peng Yuan A # , Chao Liu B , Ying Yang A , Wenbin Yang A , Dazhi Zhang A * and Guijun Yang A *
+ Author Affiliations
- Author Affiliations

A School of Life Science, Ningxia University, Yinchuan 750021, China.

B Luoshan National Nature Reserve Management Bureau, Hongsibu 751999, China.


# These authors contributed equally to this work

Handling Editor: Peter Caley

Wildlife Research 52, WR24116 https://doi.org/10.1071/WR24116
Submitted: 13 July 2024  Accepted: 24 December 2024  Published: 17 January 2025

© 2025 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context

Wild ungulates are an important component of natural ecosystems and one of the most important ecological groups of grassland ecosystems. The goitered gazelle (Gazella subgutturosa) is a species widely distributed in arid and semi-arid desert regions and is listed on the IUCN Red List (2016) as a threatened, vulnerable species at high risk for extinction in the wild. Goitered gazelle often lives in vast habitats; however, it is not yet clear how they adapt to isolated ‘islands’.

Aims

We selected an international nature reserve in the arid region of central Ningxia, China, as our study area, trying to understand how the goitered gazelle adapts to this microenvironment from the perspectives of habitat and diet.

Methods

We employed the optimized maximum entropy model and DNA metabarcoding to investigate the species’ suitable habitat distribution and feeding habits.

Key results

The results showed that the MaxEnt model performed well, with an area under curve value of 0.896 and a true skill statistic value of 0.704 for predicting the species distribution. Suitable habitats accounted for 80.9% of the total area of the reserve. Annual mean temperature, and elevation, together with the distance from water source were the critical factors that affected the goitered gazelle distribution range. Sequencing analysis indicated that among the 35 fecal samples collected, there were 18 plant families, and 21 genera annotated. The bulk food of goitered gazelle was Fabaceae and Rosaceae.

Conclusions

Water sources and altitude significantly influenced the distribution of the goitered gazelle. Trnl, as a DNA barcode, holds potential in the dietary analysis of goitered gazelles and can serve as a complement to traditional research methods.

Implications

This study confirmed the reliability of the optimized maximum entropy model for predicting suitable habitats at a small scale, and it is the first to apply DNA metabarcoding technology to the dietary analysis of the goitered gazelle. We also have more knowledge about how the goitered gazelle adapts to the isolated island habitat, laying the foundation for better protection of this species in the future.

Keywords: DNA metabarcoding, feeding habits, goitered gazelle, habitat selection, MaxEnt, small scale, trnL, ungulates.

References

Ait Baamrane MA, Shehzad W, Ouhammou A, Abbad A, Naimi M, Coissac E, Taberlet P, Znari M (2012) Assessment of the food habits of the Moroccan Dorcas Gazelle in M’Sabih Talaa, West Central Morocco, using the trnL approach. PLoS ONE 7(4), e35643.
| Crossref | Google Scholar | PubMed |

Alberdi A, Aizpurua O, Bohmann K, Gopalakrishnan S, Lynggaard C, Nielsen M, Gilbert MTP (2019) Promises and pitfalls of using high-throughput sequencing for diet analysis. Molecular Ecology Resources 19(2), 327-348.
| Crossref | Google Scholar | PubMed |

Andriollo T, Michaux JR, Ruedi M (2021) Food for everyone: differential feeding habits of cryptic bat species inferred from DNA metabarcoding. Molecular Ecology 30(18), 4584-4600.
| Crossref | Google Scholar | PubMed |

Awasthi A, Uniyal SK, Rawat GS, Sathyakumar S (2003) Food plants and feeding habits of Himalayan ungulates. Current Science 85(10), 719-723 Available at http://www.jstor.org/stable/24109877.
| Google Scholar |

Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30(15), 2114-2120.
| Crossref | Google Scholar | PubMed |

Boulanger V, Dupouey JL, Archaux F, Badeau V, Baltzinger C, Chevalier R, Corcket E, Dumas Y, Forgeard F, Marell A, Montpied P, Paillet Y, Picard JF, Saïd S, Ulrich E (2018) Ungulates increase forest plant species richness to the benefit of non-forest specialists. Global Change Biology 24(2), e485-e495.
| Crossref | Google Scholar | PubMed |

Case MJ, Lawler JJ, Tomasevic JA (2015) Relative sensitivity to climate change of species in northwestern North America. Biological Conservation 187, 127-133.
| Crossref | Google Scholar |

Ceballos G, Ehrlich PR (2002) Mammal population losses and the extinction crisis. Science 296(5569), 904-907.
| Crossref | Google Scholar | PubMed |

Chen X, Lei Y (2012) Effects of sample size on accuracy and stability of species distribution models: a comparison of GARP and MaxEnt. In ‘Recent advances in computer science and information engineering’. Lecture Notes in Electrical Engineering, vol. 125. (Eds Z Qian, L Cao, W Su, T Wang, H Yang) pp. 601–609. 10.1007/978-3-642-25789-6_80

Cheng L, Mahmut H, Shi QD, Chen LH, Wang DH, Rahmutulla A, Ezizian N, Peng J (2016) Habitat suitability assessment for Gazella subgutturosa in Ebinur Lake Wetland Nature Reserve. Acta Ecologica Sinica 36(20), 6583-6590.
| Crossref | Google Scholar |

Cobos ME, Peterson AT, Barve N, Osorio-Olvera L (2019) kuenm: an R package for detailed development of ecological niche models using Maxent. PeerJ 7, e6281.
| Crossref | Google Scholar | PubMed |

Damuth J, Janis CM (2011) On the relationship between hypsodonty and feeding ecology in ungulate mammals, and its utility in palaeoecology. Biological Reviews 86(3), 733-758.
| Crossref | Google Scholar | PubMed |

Deagle BE, Thomas AC, McInnes JC, Clarke LJ, Vesterinen EJ, Clare EL, Kartzinel TR, Eveson JP (2019) Counting with DNA in metabarcoding studies: how should we convert sequence reads to dietary data? Molecular Ecology 28(2), 391-406.
| Crossref | Google Scholar | PubMed |

Dobson A (2009) Food-web structure and ecosystem services: insights from the Serengeti. Philosophical Transactions of the Royal Society B: Biological Sciences 364(1524), 1665-1682.
| Crossref | Google Scholar | PubMed |

Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods 10(10), 996-998.
| Crossref | Google Scholar | PubMed |

Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16), 2194-2200.
| Crossref | Google Scholar | PubMed |

Elith J, Leathwick JR (2009) Species distribution models: ecological explanation and prediction across space and time. Annual Review of Ecology, Evolution, and Systematics 40(1), 677-697.
| Crossref | Google Scholar |

Fahrig L, Merriam G (1994) Conservation of fragmented populations. Conservation Biology 8(1), 50-59.
| Crossref | Google Scholar |

García-Robledo C, Erickson DL, Staines CL, Erwin TL, Kress WJ (2013) Tropical Plant–Herbivore networks: reconstructing species interactions using DNA barcodes. PLoS ONE 8(1), e52967.
| Crossref | Google Scholar | PubMed |

Griffith JA, Martinko EA, Whistler JL, Price KP (2002) Interrelationships among landscapes, NDVI, and stream water quality in the US Central Plains. Ecological Applications 12(6), 1702-1718.
| Crossref | Google Scholar |

Hanley JA, McNeil BJ (1982) The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 143(1), 29-36.
| Crossref | Google Scholar | PubMed |

Higgins SI, O’Hara RB, Römermann C (2012) A niche for biology in species distribution models. Journal of Biogeography 39(12), 2091-2095.
| Crossref | Google Scholar |

Ingala MR, Simmons NB, Wultsch C, Krampis K, Provost KL, Perkins SL (2021) Molecular diet analysis of neotropical bats based on fecal DNA metabarcoding. Ecology and Evolution 11(12), 7474-7491.
| Crossref | Google Scholar | PubMed |

IUCN SASG (2016) IUCN Red List of Threatened Species: Gazella subgutturosa. IUCN Red List of Threatened Species. Available at https://www.iucnredlist.org/en [Accessed 4 March 2023]

Kaky E, Nolan V, Khalil MI, Ameen Mohammed AM, Ahmed Jaf AA, Mohammed-Amin SM, Mahmood YA, Gilbert F (2023) Conservation of the goitered gazelle (Gazella subgutturosa) under climate changes in Iraq. Heliyon 9(2), e12501.
| Crossref | Google Scholar | PubMed |

Kartzinel TR, Chen PA, Coverdale TC, Erickson DL, Kress WJ, Kuzmina ML, Rubenstein DI, Wang W, Pringle RM (2015) DNA metabarcoding illuminates dietary niche partitioning by African large herbivores. Proceedings of the National Academy of Sciences 112(26), 8019-8024.
| Crossref | Google Scholar | PubMed |

Katz TS, Zellmer AJ (2018) Comparison of model selection technique performance in predicting the spread of newly invasive species: a case study with Batrachochytrium salamandrivorans. Biological Invasions 20(8), 2107-2119.
| Crossref | Google Scholar |

Kingswood SC, Blank DA (1996) Gazella subgutturosa. Mammalian Species 518, 1-10.
| Crossref | Google Scholar |

Kowalczyk R, Wójcik JM, Taberlet P, Kaminski T, Miquel C, Valentini A, Craine JM, Coissac E (2019) Foraging plasticity allows a large herbivore to persist in a sheltering forest habitat: DNA metabarcoding diet analysis of the European bison. Forest Ecology and Management 449, 117474.
| Crossref | Google Scholar |

Lawler JJ, Shafer SL, White D, Kareiva P, Maurer EP, Blaustein AR, Bartlein PJ (2009) Projected climate-induced faunal change in the Western Hemisphere. Ecology 90(3), 588-597.
| Crossref | Google Scholar | PubMed |

Lopes CM, De Barba M, Boyer F, Mercier C, Galiano D, Kubiak BB, Maestri R, da Silva Filho PJS, Gielly L, Coissac E, de Freitas TRO, Taberlet P (2020) Ecological specialization and niche overlap of subterranean rodents inferred from DNA metabarcoding diet analysis. Molecular Ecology 29(16), 3143-3153.
| Crossref | Google Scholar |

Ma C, Wang X, Liu C (2019) Evolution of human-land relationship and its ecological isolation in Luoshan Nature Reserve. Acta Ecologica Sinica 39(20), 7709-7721.
| Crossref | Google Scholar |

Madhusudan MD, Johnsingh AJT (1998) Analysis of habitat-use using ordination: the Nilgiri tahr in southern India. Current Science 74(11), 1000-1003 Available at http://www.jstor.org/stable/24102110.
| Google Scholar |

Mallott EK, Garber PA, Malhi RS (2018) trnL outperforms rbcL as a DNA metabarcoding marker when compared with the observed plant component of the diet of wild white-faced capuchins (Cebus capucinus, Primates). PLoS ONE 13(6), e0199556.
| Crossref | Google Scholar |

Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.Journal 17, 10-12.
| Crossref | Google Scholar |

Morris DW (1995) Earth’s peeling veneer of life. Nature 373(6509), 25.
| Crossref | Google Scholar |

Osman NA, Abdul-Latiff MAB, Mohd-Ridwan AR, Yaakop S, Nor SM, Md-Zain BM (2020) Diet composition of the wild stump-tailed macaque (Macaca arctoides) in Perlis State Park, Peninsular Malaysia, using a Chloroplast tRNL DNA metabarcoding approach: a preliminary study. Animals 10(12), 2215.
| Crossref | Google Scholar | PubMed |

Paoli A, Weladji RB, Holand Ø, Kumpula J (2018) Winter and spring climatic conditions influence timing and synchrony of calving in reindeer. PLoS ONE 13(4), e0195603.
| Crossref | Google Scholar | PubMed |

Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecological Modelling 190, 231-259.
| Crossref | Google Scholar |

Pompanon F, Deagle BE, Symondson WOC, Brown DS, Jarman SN, Taberlet P (2012) Who is eating what: diet assessment using next generation sequencing. Molecular Ecology 21(8), 1931-1950.
| Crossref | Google Scholar | PubMed |

Riquelme C, Estay SA, Contreras R, Corti P (2020) Extinction risk assessment of a Patagonian ungulate using population dynamics models under climate change scenarios. International Journal of Biometeorology 64(11), 1847-1855.
| Crossref | Google Scholar | PubMed |

Sheppard SK, Harwood JD (2005) Advances in molecular ecology: tracking trophic links through predator–prey food-webs. Functional Ecology 19(5), 751-762.
| Crossref | Google Scholar |

Shi JY, Xia MX, He GQ, Gonzalez NCT, Zhou S, Lan K, Ouyang L, Shen XB, Jiang XL, Cao FL, Li H (2024) Predicting Quercus gilva distribution dynamics and its response to climate change induced by GHGs emission through MaxEnt modeling. Journal of Environmental Management 357, 120841.
| Crossref | Google Scholar | PubMed |

Srivathsan A, Sha JCM, Vogler AP, Meier R (2015) Comparing the effectiveness of metagenomics and metabarcoding for diet analysis of a leaf-feeding monkey (Pygathrix nemaeus). Molecular Ecology Resources 15(2), 250-261.
| Crossref | Google Scholar | PubMed |

Svizzero S (2019) Issues and Challenges in the Conservation of the Goitered Gazelle (Gazella subgutturosa; Güldenstadt, 1780). Journal of Zoological Research 3(3), 1-9.
| Crossref | Google Scholar |

Swets JA (1988) Measuring the accuracy of diagnostic systems. Science 240(4857), 1285-1293.
| Crossref | Google Scholar | PubMed |

Taberlet P, Coissac E, Pompanon F, Gielly L, Miquel C, Valentini A, Vermat T, Corthier G, Brochmann C, Willerslev E (2007) Power and limitations of the chloroplast trnL (UAA) intron for plant DNA barcoding. Nucleic Acids Research 35(3), e14.
| Crossref | Google Scholar | PubMed |

Warren DL, Seifert SN (2011) Ecological niche modeling in MaxEnt: the importance of model complexity and the performance of model selection criteria. Ecological Applications 21(2), 335-342.
| Crossref | Google Scholar | PubMed |

Warren DL, Glor RE, Turelli M (2010) ENMTools: a toolbox for comparative studies of environmental niche models. Ecography 33(3), 607-611.
| Crossref | Google Scholar |

Wu W, Li Y, Hu Y (2016) Simulation of potential habitat overlap between red deer (Cervus elaphus) and roe deer (Capreolus capreolus) in northeastern China. Peerj 4, e1756.
| Crossref | Google Scholar | PubMed |

Xu W, Qiao J, Liu W, Yang W (2008) Food habits of goitered gazelles (Gazella subgutturosa sairensis) in northern Xinjiang. Acta Theriologica Sinica 28, 280-286.
| Crossref | Google Scholar |