Eur. J. Entomol. 122: 173-183, 2025 | DOI: 10.14411/eje.2025.022
Complementary roles of agricultural and natural habitats in supporting moth diversity in semi-arid landscapes of MoroccoOriginal article
- 1 Department of Zoology, Institute of Ecology and Earth Sciences, Faculty of Science and Technology, University of Tartu, 50409 Tartu, Estonia; e-mails: fetnassi.ndl@gmail.com, stenio.foerster@ut.ee, erki.ounap@ut.ee, toomas.tammaru@ut.ee
- 2 Cadi Ayyad University, Faculty of Sciences Semlalia, AquaBioTech Laboratory, Marrakech, Morocco; e-mail: ghamizi@uca.ac.ma
- 3 Cadi Ayyad University, Museum of Natural History of Marrakech (MHNM), Morocco
- 4 Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, Tartu, Estonia
Human activities, particularly those exacerbated by climate change, are major drivers of biodiversity change. While many human actions degrade biodiversity, some anthropogenic habitats can provide refuges for certain species, insects in particular. Research on the human impact on biodiversity remains uneven both geographically and taxonomically. In this study, nocturnal moth assemblages were compared across three habitat types (forest, riverbanks and olive groves) representing a gradient from natural to heavily human-altered environments in a semi-arid landscape of Morocco. Moths were systematically sampled across an altitudinal gradient ranging from 900 to 1600 m using automatic sugar-bait traps. We recorded 105 macroheteroceran species, most of which belonged to the families Noctuidae and Erebidae. The differences in moth assemblages among the studied habitats were statistically significant, with magnitudes comparable to those observed among the study sites. Altitude had a relatively weak influence on abundance and species richness. Olive groves exhibited the highest moth abundance and species richness, though they were dominated by common and widespread species. Forests supported a greater number of rare species, while riverbanks had lower abundance and species richness. In conclusion, while traditional agriculture can support species-rich insect communities in semi-arid landscapes, maintaining natural vegetation remains crucial, as forests, though less species-rich, still enhance overall moth diversity.
Keywords: Lepidoptera, Noctuidae, Erebidae, species composition, abundance, sugar bait, agriculture, conservation, High Atlas Mountains, North Africa
Received: April 5, 2025; Revised: July 1, 2025; Accepted: July 1, 2025; Published online: August 19, 2025 Show citation
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References
- AHT Groupe Ag-Resing 2016: Diagnostic du Sous Bassin de Zat. Association Agir. Programme d'appui à la gestion des ressources en eau, 104 pp.
- Alaoui Haroni S., Alifriqui M. & Simonneaux V. 2009: Recent dynamics of the wet pastures at Oukaimeden plateau (High Atlas mountains, Morroco). - Biodivers. Conserv. 18: 167-189.
Go to original source...
- Anderson M.J. 2006: Distance-based tests for homogeneity of multivariate dispersions. - Biometrics 62: 245-253.
Go to original source...
- Anderson M.J. & Walsh D.C.I. 2013: PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing? - Ecol. Monogr. 83: 557-574.
Go to original source...
- Arora N.K. 2018: Biodiversity conservation for sustainable future. - Environ. Sustain. 1: 109-111.
Go to original source...
- Assahira C., Piedade M.T.F., Trumbore S.E., Wittmann F., Cintra B.B.L., Batista E.S., Resende A.F. de & Schöngart J. 2017: Tree mortality of a flood-adapted species in response of hydrographic changes caused by an Amazonian river dam. - For. Ecol. Manag. 396: 113-123.
Go to original source...
- Aune S., Bryn A. & Hovstad K.A. 2018: Loss of semi-natural grassland in a boreal landscape: impacts of agricultural intensification and abandonment. - J. Land Use Sci. 13: 375-390.
Go to original source...
- Bakker J.D. 2024: Restricting Permutations. Applied Multivariate Statistics in R. University of Washington, Seattle, WA. URL: https://uw.pressbooks.pub/appliedmultivariatestatistics/
- Barrow C.J. & Hicham H. 2000: Two complimentary and integrated land uses of the western High Atlas Mountains, Morocco: The potential for sustainable rural livelihoods. - Appl. Geogr. 20: 369-394.
Go to original source...
- Bell B.A., Hughes P.D., Fletcher W.J., Cornelissen H.L., Rhoujjati A., Hanich L. & Braithwaite R.J. 2022: Climate of the Marrakech High Atlas, Morocco: Temperature lapse rates and precipitation gradient from piedmont to summits. - Arct. Antarct. Alp. Res. 54: 78-95.
Go to original source...
- Bellard C., Bertelsmeier C., Leadley P., Thuiller W. & Courchamp F. 2012: Impacts of climate change on the future of biodiversity. - Ecol. Lett. 15: 365-377.
Go to original source...
- Benabid A. 1982: Bref aperçu sur la zonation altitudinale de la végétation climacique du Maroc. - Ecol. Mediterr. 8: 301-315.
Go to original source...
- Berg Å., Ahrné K., Öckinger E., Svensson R. & Söderström B. 2011: Butterfly distribution and abundance is affected by variation in the Swedish forest-farmland landscape. - Biol. Conserv. 144: 2819-2831.
Go to original source...
- Bernabé-Ruiz P.M., Jiménez-Nieva F.J. & Pérez-Quintero J.C. 2024: Temporal variation in and influence of environmental variables on a lepidopteran community in a Mediterranean mid-mountain area. - Diversity 16(7): 408, 23 pp
Go to original source...
- Bouamri H., Boudhar A., Gascoin S. & Kinnard C. 2018: Performance of temperature and radiation index models for point-scale snow water equivalent (SWE) simulations in the Moroccan High Atlas Mountains. - Hydrol. Sci. J. 63: 1844-1862.
Go to original source...
- Boudhar A., Hanich L., Boulet G., Duchemin B., Berjamy B. & Chehbouni A. 2009: Evaluation of the Snowmelt Runoff model in the Moroccan High Atlas Mountains using two snow-cover estimates. - Hydrol. Sci. J. 54: 1094-1113.
Go to original source...
- Boyes D. & Holland P.W. 2022: The genome sequence of the square-spot rustic, Xestia xanthographa (Schiffermuller, 1775). - Wellcome Open Res. 7: 13 pp.
Go to original source...
- Boyes D.H., Evans D.M., Fox R., Parsons M.S. & Pocock M.J.O. 2021: Is light pollution driving moth population declines? A review of causal mechanisms across the life cycle. - Insect Conserv. Divers. 14: 167-187.
Go to original source...
- Braga L. & Diniz I.R. 2018: Can Saturniidae moths be bioindicators? Spatial and temporal distribution in the Brazilian savannah. - J. Insect Conserv. 22: 487-497.
Go to original source...
- Calabrese G., Tartaglini N. & Ladisa G. 2012: Study on Biodiversity in Century-Old Olive Groves. CIHEAM-Mediterranean Agronomic Institute, Bari, 108 pp.
- Carrara E., Arroyo-Rodríguez V., Vega-Rivera J.H., Schondube J.E., de Freita S.M. & Fahrig L. 2015: Impact of landscape composition and configuration on forest specialist and generalist bird species in the fragmented Lacandona rainforest, Mexico. - Biol. Conserv. 184: 117-126.
Go to original source...
- Chafaa S., Mimeche F. & Chenchouni H. 2019: Diversity of insects associated with olive (Oleaceae) groves across a dryland climate gradient in Algeria. - Can. Entomol. 151: 629-647.
Go to original source...
- Chao A. 1984: Nonparametric estimation of the number of classes in a population. - Scand. J. Stat. 11: 265-270.
- Chao A. 1987: Estimating the population size for capture-recapture data with unequal catchability. - Biometrics 43: 783-791.
Go to original source...
- Chao A. & Chiu C. 2016: Species richness: Estimation and comparison. - Wiley StatsRef: Statistics Reference Online 2016: 26 pp.
Go to original source...
- Chao A., Wang Y.T. & Jost L. 2013: Entropy and the species accumulation curve: A novel entropy estimator via discovery rates of new species. - Methods Ecol. Evol. 4: 1091-1100.
Go to original source...
- Chao A., Gotelli N.J., Hsieh T.C., Sander E.L., Ma K.H., Colwell R.K. & Ellison A.M. 2014: Rarefaction and extrapolation with Hill numbers: A framework for sampling and estimation in species diversity studies. - Ecol. Monogr. 84: 45-67.
Go to original source...
- De Cáceres M. & Legendre P. 2009: Associations between species and groups of sites: Indices and statistical inference. -Ecology 90: 3566-3574.
Go to original source...
- Dudley N. & Alexander S. 2017: Agriculture and biodiversity: a review. - Biodiversity 18: 45-49.
Go to original source...
- Dufrêne M. & Legendre P. 1997: Species assemblages and indicator species: The need for a flexible asymmetrical approach. - Ecol. Monogr. 67: 345-366.
Go to original source...
- El Alami A. 2019: A survey of the vulnerable Cuvier's gazelle (Gazella cuvieri) in the mountains of Ait Tamlil and Anghomar, Central High Atlas of Morocco. - Mammalia 83: 74-77.
Go to original source...
- El Alami A. 2022: Biodiversity loss in the Moroccan central High Atlas, its impact on local ecosystems and national economy, and wildlife conservation strategy: Findings from 20 years of research. - J. Anal. Sci. Appl. Biotechnol. 4: 81-96.
- El Alami A., van Lavieren E., Aboufatima R. & Chait A. 2013: A survey of the endangered barbary macaque Macaca sylvanus in the Central High Atlas Mountains of Morocco. - Oryx 47: 451-456.
Go to original source...
- El Alami A., Fattah A. & Bouzekraoui H. 2021: Biodiversity, an essential component for the M'goun global geopark development (Morocco) - an overview. - J. Anal. Sci. Appl. Biotechnol. 3: 103-106.
- El Harche H., El Hassouni S., Fadli M. & Dahmani J. 2023: Spatial, seasonal variation and impacts of anthropogenic factors on insect assemblages (Arthropoda: Insecta) in Northwest Morocco. - Biodiversitas 24: 5368-5375.
Go to original source...
- Ellero A., Ottria G., Malusà M.G. & Ouanaimi H. 2012: Structural geological analysis of the High Atlas (Morocco): Evidences of a transpressional fold-thrust belt. In Sharkov E. (ed.): Tectonics - Recent Advances. Intech Open Science, London, pp. 229-258.
Go to original source...
- Fetnassi N., Ude K., Kull A. & Tammaru T. 2022: Weather sensitivity of sugar bait trapping of nocturnal moths: A case study from northern Europe. - Insects 13(12): 1087, 11 pp.
Go to original source...
- Fetnassi N., Er-Rguibi O., Aglagane A., Ghamizi M. & Õunap E. 2025: Updates to the checklist of nocturnal Macroheterocera (Lepidoptera) of the Central High Atlas of Morocco: One new species added for Morocco. - Biodivers. Data J. 13: e137839, 37 pp.
Go to original source...
- Fox R., Oliver T.H., Harrower C., Parsons M.S., Thomas C.D. & Roy D.B. 2014: Long-term changes to the frequency of occurrence of British moths are consistent with opposing and synergistic effects of climate and land-use changes. - J. Appl. Ecol. 51: 949-957.
Go to original source...
- Goater B., Ronkay L. & Fibiger M. 2003: Catocalinae and Plusiinae. Noctuidae Europaea. Vol. 10. Entomological Press, Sorø, 452 pp.
- González-Estébanez F.J., García-Tejero S., Mateo-Tomás P. & Olea P.P. 2011: Effects of irrigation and landscape heterogeneity on butterfly diversity in Mediterranean farmlands. -Agric. Ecosyst. Environ. 144: 262-270.
Go to original source...
- Hald-Mortensen C. 2023: The main drivers of biodiversity loss: A brief overview. - J. Ecol. Nat. Resour. 7(3): 7 pp.
Go to original source...
- Hill G.M., Kawahara A.Y., Daniels J.C., Bateman C.C. & Scheffers B.R. 2021: Climate change effects on animal ecology: butterflies and moths as a case study. - Biol. Rev. 96: 2113-2126.
Go to original source...
- Hsieh T.C., Ma K.H. & Chao A. 2016: iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). - Methods Ecol. Evol. 7: 1451-1456.
Go to original source...
- Jankielsohn A. 2023: Sustaining insect biodiversity in agricultural systems to ensure future food security. - Front. Conserv. Sci. 4: 1195512, 8 pp.
Go to original source...
- Khelifa R., Mahdjoub H., Baaloudj A., Cannings R.A. & Samways M.J. 2021: Effects of both climate change and human water demand on a highly threatened damselfly. - Sci. Rep. 11(1): 7725, 11 pp.
Go to original source...
- Legendre P. 2013: Indicator species: Computation. In Scheiner S.M. (ed.): Encyclopedia of Biodiversity. Vol. 4. 2nd ed. Elsevier, Oxford, pp. 264-268.
Go to original source...
- Legendre P. & Legendre L.F. 2012: Numerical Ecology, 3rd ed. Elsevier, Oxford, 1006 pp.
- Ma S., Wang L.J., Jiang J. & Zhao Y.G. 2023: Direct and indirect effects of agricultural expansion and landscape fragmentation processes on natural habitats. - Agric. Ecosyst. Environ. 353: 108555, 15 pp.
Go to original source...
- MacGregor C.J., Pocock M.J.O., Fox R. & Evans D.M. 2015: Pollination by nocturnal Lepidoptera, and the effects of light pollution: A review. - Ecol. Entomol. 40: 187-198.
Go to original source...
- Maicher V., Sáfián S., Murkwe M., Przyby³owicz £., Janeèek ©., Fokam E.B., Pyrcz T. & Tropek R. 2018: Flying between raindrops: Strong seasonal turnover of several Lepidoptera groups in lowland rainforests of Mount Cameroon. - Ecol. Evol. 8: 12761-12772.
Go to original source...
- Maicher V., Sáfián S., Murkwe M., Delabye S., Przyby³owicz £., Potocký P., Kobe I.N, Janeèek ©., Mertens J.E.J., ... & Tropek R. 2020: Seasonal shifts of biodiversity patterns and species' elevation ranges of butterflies and moths along a complete rainforest elevational gradient on Mount Cameroon. - J. Biogeogr. 47: 342-354
Go to original source...
- Mangels J., Fiedler K., Schneider F.D. & Blüthgen N. 2017: Diversity and trait composition of moths respond to land-use intensification in grasslands: generalists replace specialists. - Biodiv. Conserv. 26: 3385-3405.
Go to original source...
- Martínez-Freiría F., Argaz H., Fah S. & Brito J.C. 2013: Climate change is predicted to negatively influence Moroccan endemic reptile richness. Implications for conservation in protected areas. - Naturwissenschaften 100: 877-889.
Go to original source...
- Medail F. & Quezel P. 1999: Biodiversity hotspots in the Mediterranean Basin: Setting global conservation priorities. - Conserv. Biol. 13: 1510-1513.
Go to original source...
- Merckx T., Kaiser A. & Van Dyck H. 2018: Increased body size along urbanization gradients at both community and intraspecific level in macro-moths. - Glob. Change Biol. 24: 3837-3848.
Go to original source...
- Mertens J.E., Brisson L., Janeèek ©., Klomberg Y., Maicher V., Sáfián S., Delabye S., Potocký P., Kobe I.N., Pyrcz T. & Tropek R. 2021: Elevational and seasonal patterns of butterflies and hawkmoths in plant-pollinator networks in tropical rainforests of Mount Cameroon. - Sci. Rep. 11(1): 9710, 12 pp.
Go to original source...
- Mohamed A., DeClerck F., Verburg P.H., Obura D., Abrams J.F., Zafra-Calvo N., Rocha J., Estrada-Carmona N., Fremier A., Jones S.K., Meier I.C. & Stewart-Koster B. 2024: Securing Nature's Contributions to People requires at least 20%-25% (semi-)natural habitat in human-modified landscapes. - One Earth 7: 59-71.
Go to original source...
- Mokbel E.-S. & Huesien A. 2020: Sublethal effects of emamectin benzoate on life table parameters of the cotton leafworm, Spodoptera littoralis (Boisd.). - Bull. Natl. Res. Cente. 44(1): 155, 8 pp.
Go to original source...
- Mostakim L., Guennoun F.Z., Benaissa H., Fetnassi N. & Ghamizi M. 2022a: Effects of land use change on the riparian zones' quality along the Zat river and its tributaries: High Atlas of Morocco. - Appl. Ecol. Environ. Res. 20: 1351-1367.
Go to original source...
- Mostakim L., Guennoun F.Z., Fetnassi N. & Ghamizi M. 2022b: Analysis of floristic diversity of the forest ecosystems of the Zat valley - High Atlas of Morocco: Valorization and conservation perspectives. - J. Adv. Biotechnol. Exp. Ther. 5: 126-135.
Go to original source...
- Mounir M., Dakki M., Douini I., Benka E.M., Abdessamad O., Nouri A., Mansouri I. & Hammada S. 2022:. The avifauna of two High Atlas valleys: breeding assemblages in forest stands and open lands. - J. Anim. Behav. Biometeorol. 10: 2225, 10 pp.
Go to original source...
- Mounir M., Dakki M., Douini I., Benka E.M., Nouri A., Mansouri I. & Hammada S. 2024: Large-scale monitoring of bird communities along an altitudinal gradient in two Central High Atlas valleys. - Int. J. Zool. 2024: 873008, 14 pp.
Go to original source...
- Myers N., Mittermeier R.A., Mittermeier C.G., Da Fonseca G.A. & Kent J. 2000: Biodiversity hotspots for conservation priorities. - Nature 403: 853-858.
Go to original source...
- Newbold T., Scharlemann J.P.W., Butchart S.H.M., ªekercioǧlu Ç.H., Alkemade R., Booth H. & Purves D.W. 2013: Ecological traits affect the response of tropical forest bird species to land-use intensity. - Proc. R. Soc. (B) 280: 20122131, 8 pp.
Go to original source...
- Nguyen T.T., Aderdour N., Rhinane H. & Buerkert A. 2023: Vegetation cover dynamics in the High Atlas mountains of Morocco. - Remote Sens. 15(5): 1366, 6 pp.
Go to original source...
- One Earth 2025: Mediterranean: High Atlas Juniper Steppe. URL: https://www.oneearth.org/ecoregions/mediterranean-high-atlas-juniper-steppe/ (last acessed 15 Jan. 2025).
- Oksanen J., Simpson G.L., Blanchet F.G., Kindt R., Legendre P., Minchin P.R., O'Hara R.B., Solymos P., Stevens M.H.H., … Weedon J. 2022: vegan: Community Ecology Package. URL: https://CRAN.R-project.org/package=vegan
- Peyron M. 1976: Habitat rural et vie montagnarde dans le Haut Atlas de Midelt (Maroc). - Rev. Geogr. Alp. 64: 327-363.
Go to original source...
- Piñero F.S., Tinaut A., Aguirre-Segura A., Miñano J., Lencina J.L., Ortiz-Sánchez F.J. & Pérez-López F.J. 2011: Terrestrial arthropod fauna of arid areas of SE Spain: Diversity, biogeography, and conservation. - J. Arid Environ. 75: 1321-1332
Go to original source...
- Sanjayan K.P. & Chand D.S. 1997: Nutritional preferences of Grammodes stolida (Fab), A defoliator of the forest tree, Lannea coromandelica (Houtt). - Int. J. Trop. Insect Sci. 17: 257-263.
Go to original source...
- Santoro A. 2023: Traditional oases in Northern Africa as multifunctional agroforestry systems: a systematic literature review of the provided Ecosystem Services and of the main vulnerabilities. - Agrofor. Syst. 97: 81-96.
Go to original source...
- Thomas C.D. & Mallorie H.C. 1985: Rarity, species richness and conservation: Butterflies of the Atlas mountains in Morocco. - Biol. Conserv. 33: 95-117.
Go to original source...
- Ude K., Foerster S.I.A., Fetnassi N. & Tammaru T. 2025: Forest clear-cuts support diverse moth fauna but lack common grassland species. - J. Appl. Ecol. 62: 1473-1486.
Go to original source...
- Uhl B., Wölfling M. & Bässler C. 2022: Mediterranean moth diversity is sensitive to increasing temperatures and drought under climate change. - Sci. Rep. 12(1): 14473, 10 pp.
Go to original source...
- Viljur M.L. & Teder T. 2016: Butterflies take advantage of contemporary forestry: Clear-cuts as temporary grasslands. - For. Ecol. Manag. 376: 118-125.
Go to original source...
- Wezel A., Casagrande M., Celette F., Vian J.F., Ferrer A. & Peigné J. 2014: Agroecological practices for sustainable agriculture. A review. - Agron. Sustain. Dev. 34: 1-20.
Go to original source...
- Zhang R., Wang J. & Niu S. 2021: Toward a sustainable grazing management based on biodiversity and ecosystem multifunctionality in drylands. - Curr. Opin. Environ. Sustain. 48: 36-43.
Go to original source...
- Zkhiri W., Tramblay Y., Hanich L. & Berjamy B. 2017: Regional flood frequency analysis in the High Atlas mountainous catchments of Morocco. - Nat. Hazards 86: 953-967.
Go to original source...
- Zucco G., La Cava S., Rijllo G. & Scalercio S. 2024: The contribution of cultivated and semi-natural patches to the beta diversity of nocturnal Lepidoptera within an organic century-old olive grove in a fragmented landscape. - Land 13(4): 532, 15 pp.
Go to original source...
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