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Complementary endozoochorous seed dispersal by large mammals in the Golestan National Park, Iran

Published online by Cambridge University Press:  22 October 2018

Sorour Karimi ,
Mahmoud-Reza Hemami Open the ORCID record for Mahmoud-Reza Hemami [Opens in a new window] ,
Mostafa Tarkesh Esfahani ,
Hossein Akhani  and
Christophe Baltzinger
Sorour Karimi
Affiliation:
Department of Natural Resources, Isfahan University of Technology, Isfahan 84156-83111, Iran
Mahmoud-Reza Hemami*
Affiliation:
Department of Natural Resources, Isfahan University of Technology, Isfahan 84156-83111, Iran
Mostafa Tarkesh Esfahani
Affiliation:
Department of Natural Resources, Isfahan University of Technology, Isfahan 84156-83111, Iran
Hossein Akhani
Affiliation:
Halophytes and C4 Plants Research Laboratory, Department of Plant Sciences, School of Biology, College of Science, University of Tehran, Tehran 14155-6455, Iran
Christophe Baltzinger
Affiliation:
Irstea, UR EFNO, Domaine des Barres, 45290 Nogent sur Vernisson, France Centre for Invasion Biology, School of Life Sciences, University of KwaZulu-Natal, Scottsville, 3209, Pietermaritzburg, South Africa
*
Author for correspondence: Mahmoud-Reza Hemami, Email: mrhemami@cc.iut.ac.ir
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Abstract

Large animals tend to disperse seeds over long distances via ingestion and defecation due to their large home range and capacity to move among different habitats for feeding. The aim of this study was to investigate the potential of endozoochorous seed dispersal by five herbivores: Ovis vignei, Capra aegagrus, Gazella subgutturosa, Cervus elaphus, Capreolus capreolus and two omnivores: Sus Scrofa and Ursus arctos in the Golestan National Park, northeast of Iran, by a greenhouse germination experiment. A total of 3107 seedlings belonging to 154 different plant taxa were germinated from 655 dung samples collected in three different habitats. Plant families that most frequently germinated were Poaceae and Brassicaceae. Urtica dioica was the most abundant germinating seed, accounting for 20% of all the seedlings recorded in our dung samples, whereas the most frequently observed species was Portulaca oleracea, which occurred in 24% of our samples. We showed that 54% of the seeds germinating were dispersed by only one of the mammals studied. Herbs and graminoids were the most frequently dispersed growth forms by the herbivores and the wild boar, whereas brown bears mostly dispersed shrubs. The seedling composition in the dung samples was strongly correlated with the local flora especially for non-selective feeders, like red deer. The differences observed in the number of plants and frequency of different growth forms dispersed among the studied mammals reflect their body size, digestive physiology, and dietary and habitat preferences. Our findings highlight the different and complementary roles of large herbivores and omnivores as long-distance seed dispersal vectors.

Keywords

endozoochoryHyrcanian forestsIrano-Turanian steppeslarge herbivoreslarge omnivoresseed dispersal
Type
Research Paper
Information
Seed Science Research , Volume 28 , Issue 4 , December 2018 , pp. 294 - 302
Copyright
Copyright © Cambridge University Press 2018 

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References

Akhani, H (1998) Plant biodiversity of Golestan National Park, Iran. Stapfia 53, 1–411.Google Scholar
Akhani, H, Djamali, M, Ghorbanalizadeh, A and Ramezani, E (2010) Plant biodiversity of Hyrcanian relict forests, N Iran: an overview of the flora, vegetation, palaeoecology and conservation. Pakistan Journal of Botany 42, 231–258.Google Scholar
Akhani, H and Khoshravesh, R (2011) Biodiversity and threats of natural ecosystems in Iran: case study Golestan National Park, NE Iran. In Öztürk, M, Mermut, AR and Celik, A (eds), Urbanisation, Land Use, Land Degradation and Environment. NAM, S & T Center.Google Scholar
Akhani, H, Khoshravesh, R and Malekmohammadi, M (2016) Taxonomic novelties from Irano-Turanian region and NE Iran: Oreosalsola, a new segregate from Salsola s.l., two new species in Anabasis and Salvia, and two new combinations in Caroxylon and Seseli. Phytotaxa 249, 159–180.Google Scholar
Akhani, H and Ziegler, H (2002) Photosynthetic pathways and habitats of grasses in Golestan National Park (NE Iran), with an emphasis on the C4-grass dominated rock communities. Phytocoenologia 32, 455–501.Google Scholar
Albert, A, Auffret, AG, Cosyns, E, Cousins, SA, D'hondt, B, Eichberg, C, Eycott, AE, Heinken, T, Hoffmann, M and Jaroszewicz, B (2015) Seed dispersal by ungulates as an ecological filter: a trait-based meta-analysis. Oikos 124, 1109–1120.Google Scholar
Auffret, AG and Plue, J (2014) Scale-dependent diversity effects of seed dispersal by a wild herbivore in fragmented grasslands. Oecologia 175, 305–313.Google Scholar
Bacles, CF, Lowe, AJ and Ennos, RA (2006) Effective seed dispersal across a fragmented landscape. Science 311, 628–628.Google Scholar
Bagherirad, E, Norhayati, A, Abdullah, M, Amirkhani, M and Erfanian, B (2013) Using pellet group counts to estimate the population size of the Persian gazelle in the steppe area of Golestan National Park, Iran. Malaysian Applied Biology 42, 51–57.Google Scholar
Ballari, SA and Barrios-García, MN (2014) A review of wild boar Sus scrofa diet and factors affecting food selection in native and introduced ranges. Mammal Review 44, 124–134.Google Scholar
Beckmann, JP and Berger, J (2003) Rapid ecological and behavioural changes in carnivores: the responses of black bears (Ursus americanus) to altered food. Journal of Zoology 261, 207–212.Google Scholar
Benthien, O, Bober, J, Castens, J and Stolter, C (2016) Seed dispersal capacity of sheep and goats in a near-coastal dry grassland habitat. Basic and Applied Ecology 17, 508–515.Google Scholar
Braun-Blanquet, J (1964) Pflanzensoziologie, Grundzüge der Vegetationskunde. Berlin, Springer-Verlag.Google Scholar
Bruinderink, GG, Van Der Sluis, T, Lammertsma, D, Opdam, P and Pouwels, R (2003) Designing a coherent ecological network for large mammals in northwestern Europe. Conservation Biology 17, 549–557.Google Scholar
Chao, A (1987) Estimating the population size for capture-recapture data with unequal catchability. Biometrics 43, 783–791.Google Scholar
Chapman, NG, Claydon, K, Claydon, M, Forde, P and Harris, S (1993) Sympatric populations of muntjac (Muntiacus reevesi) and roe deer (Capreolus capreolus): a comparative analysis of their ranging behaviour, social organization and activity. Journal of Zoology 229, 623–640.Google Scholar
Chen, H and Boutros, PC (2011) VennDiagram: a package for the generation of highly-customizable Venn and Euler diagrams in R. BMC Bioinformatics 12, 35.Google Scholar
Clauss, M, Nijboer, J, Loermans, JH, Roth, T, Van der Kuilen, J and Beynen, AC (2008) Comparative digestion studies in wild suids at Rotterdam Zoo. Zoo Biology 27, 305–319.Google Scholar
Cosyns, E, Delporte, A, Lens, L and Hoffmann, M (2005) Germination success of temperate grassland species after passage through ungulate and rabbit guts. Journal of Ecology 93, 353–361.Google Scholar
Couvreur, M, Cosyns, E, Hermy, M and Hoffmann, M (2005) Complementarity of epi-and endozoochory of plant seeds by free ranging donkeys. Ecography 28, 37–48.Google Scholar
Couvreur, M, Vandenberghe, B, Verheyen, K and Hermy, M (2004) An experimental assessment of seed adhesivity on animal furs. Seed Science Research 14, 147–159.Google Scholar
Croteau, E (2010) Causes and consequences of dispersal in plants and animals. Nature Education Knowledge 1, 12.Google Scholar
Dovrat, G, Perevolotsky, A and Ne'eman, G (2012) Wild boars as seed dispersal agents of exotic plants from agricultural lands to conservation areas. Journal of Arid Environments 78, 49–54.Google Scholar
Eycott, A, Watkinson, A, Hemami, M.-R and Dolman, P (2007) The dispersal of vascular plants in a forest mosaic by a guild of mammalian herbivores. Oecologia 154, 107–118.Google Scholar
Fllner, S and Shmida, A (1981) Why are adaptations for long-range seed dispersal rare in desert plants? Oecologia 51, 133–144.Google Scholar
Ghoddousi, A, Soofi, M, Hamidi, AK, Lumetsberger, T, Egli, L, Khorozyan, I, Kiabi, BH and Waltert, M (2016a) Assessing the role of livestock in big cat prey choice using spatiotemporal availability patterns. PLOS ONE 11, e0153439.Google Scholar
Ghoddousi, A, Soofi, M, Khorozyan, I, Kiabi, B and Waltert, M (2016b) Effects of ranger stations on predator and prey distribution and abundance in an Iranian steppe landscape. Animal Conservation 19, 273–280.Google Scholar
Guiden, P, Gorchov, DL, Nielsen, C and Schauber, E (2015) Seed dispersal of an invasive shrub, Amur honeysuckle (Lonicera maackii), by white-tailed deer in a fragmented agricultural-forest matrix. Plant Ecology 216, 939–950.Google Scholar
Hargreaves, AL and Eckert, CG (2014) Evolution of dispersal and mating systems along geographic gradients: implications for shifting ranges. Functional Ecology 28, 5–21.Google Scholar
Harries, HC and Clement, CR (2013) Long-distance dispersal of the coconut palm by migration within the coral atoll ecosystem. Annals of Botany 113, 565–570.Google Scholar
Harwell, MC and Orth, RJ (2002) Long-distance dispersal potential in a marine macrophyte. Ecology 83, 3319–3330.Google Scholar
Heinken, T, Hanspach, H, Raudnitschka, D and Schaumann, F (2002) Dispersal of vascular plants by four species of wild mammals in a deciduous forest in NE Germany. Phytocoenologia 32, 627–643.Google Scholar
Heinken, T and Raudnitschka, D (2002) Do wild ungulates contribute to the dispersal of vascular plants in central European forests by epizoochory? A case study in NE Germany. Forstwissenschaftliches Centralblatt 121, 179–194.Google Scholar
Hofmann, RR (1989) Evolutionary steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive system. Oecologia 78, 443–457.Google Scholar
Iravani, M, Schütz, M, Edwards, PJ, Risch, AC, Scheidegger, C and Wagner, HH (2011) Seed dispersal in red deer (Cervus elaphus L.) dung and its potential importance for vegetation dynamics in subalpine grasslands. Basic and Applied Ecology 12, 505–515.Google Scholar
Janzen, DH (1984) Dispersal of small seeds by big herbivores: foliage is the fruit. The American Naturalist 123, 338–353.Google Scholar
Jaroszewicz, B (2013) Endozoochory by European bison influences the build-up of the soil seed bank in subcontinental coniferous forest. European Journal of Forest Research 132, 445–452.Google Scholar
Jaroszewicz, B, Pirożnikow, E and Sondej, I (2013) Endozoochory by the guild of ungulates in Europe's primeval forest. Forest Ecology and Management 305, 21–28.Google Scholar
Kavandi, H, Iravani, M and Kamali, P (2016) Seed dispersal by different-sized herbivores in rangeland habitats of central Iran (case study: Esfahan Kolah Ghazi National Park). Journal of Rangeland 9, 378–391.Google Scholar
Kuiters, A and Huiskes, H (2010) Potential of endozoochorous seed dispersal by sheep in calcareous grasslands: correlations with seed traits. Applied Vegetation Science 13, 163–172.Google Scholar
Lalleroni, A, Quenette, P-Y, Daufresne, T, Pellerin, M and Baltzinger, C (2017) Exploring the potential of brown bear (Ursus arctos arctos) as a long-distance seed disperser: a pilot study in South-Western Europe. Mammalia 81, 1–9.Google Scholar
Malo, JE and Suárez, F (1995) Herbivorous mammals as seed dispersers in a Mediterranean dehesa. Oecologia 104, 246–255.Google Scholar
Malo, JE and Suárez, F (1996) Cistus ladanifer recruitment: not only fire, but also deer. Acta Oecologica 17, 55–60.Google Scholar
Manzaneda, AJ, Fedriani, JM and Rey, PJ (2005) Adaptive advantages of myrmecochory: the predator-avoidance hypothesis tested over a wide geographic range. Ecography 28, 583–592.Google Scholar
McConkey, KR and Brockelman, WY (2011) Nonredundancy in the dispersal network of a generalist tropical forest tree. Ecology 92, 1492–1502.Google Scholar
McConkey, KR, Prasad, S, Corlett, RT, Campos-Arceiz, A, Brodie, JF, Rogers, H and Santamaria, L (2012) Seed dispersal in changing landscapes. Biological Conservation 146, 1–13.Google Scholar
Memariani, F, Zarrinpour, V and Akhani, H (2016) A review of plant diversity, vegetation, and phytogeography of the Khorassan-Kopet Dagh floristic province in the Irano-Turanian region (northeastern Iran-southern Turkmenistan). Phytotaxa 249, 8–30.Google Scholar
Milotić, T and Hoffmann, M (2016a) How does gut passage impact endozoochorous seed dispersal success? Evidence from a gut environment simulation experiment. Basic and Applied Ecology 17, 165–176.Google Scholar
Milotić, T and Hoffmann, M (2016b) Reduced germination success of temperate grassland seeds sown in dung: consequences for post-dispersal seed fate. Plant Biology 18, 1038–1047.Google Scholar
Moser, B, Schütz, M and Hindenlang, KE (2006) Importance of alternative food resources for browsing by roe deer on deciduous trees: the role of food availability and species quality. Forest Ecology and Management 226, 248–255.Google Scholar
Mouissie, AM (2004) Seed dispersal by large herbivores: implications for the restoration of plant biodiversity. PhD dissertation, University of Groningen.Google Scholar
Mouissie, A, Vos, P, Verhagen, H and Bakker, J (2005) Endozoochory by free-ranging, large herbivores: ecological correlates and perspectives for restoration. Basic and Applied Ecology 6, 547–558.Google Scholar
Mueller-Dombois, D and Ellenberg, H (1974) Aims and Methods of Vegetation Ecology. New York, NY, US, Wiley.Google Scholar
Neuschulz, EL, Mueller, T, Schleuning, M and Böhning-Gaese, K (2016) Pollination and seed dispersal are the most threatened processes of plant regeneration. Scientific Reports 6, 29839.Google Scholar
Oksanen, J, Blanchet, FG, Kindt, R, Legendre, P, Minchin, PR, O'Hara, R, Simpson, GL, Solymos, P, Stevens, MHH and Wagner, H (2013) Package ‘vegan’. Community Ecology Package, version 2.Google Scholar
Pakeman, R, Digneffe, G and Small, J (2002) Ecological correlates of endozoochory by herbivores. Functional Ecology 16, 296–304.Google Scholar
Pakeman, R and Small, J (2009) Potential and realised contribution of endozoochory to seedling establishment. Basic and Applied Ecology 10, 656–661.Google Scholar
Panter, CJ and Dolman, PM (2012) Mammalian herbivores as potential seed dispersal vectors in ancient woodland fragments. Wildlife Biology 18, 292–303.Google Scholar
Pellerin, M, Picard, M, Saïd, S, Baubet, E and Baltzinger, C (2016) Complementary endozoochorous long-distance seed dispersal by three native herbivorous ungulates in Europe. Basic and Applied Ecology 17, 321–332.Google Scholar
Pereira, HM, Leadley, PW, Proença, V, Alkemade, R, Scharlemann, JP, Fernandez-Manjarrés, JF, Araújo, MB, Balvanera, P, Biggs, R and Cheung, WW (2010) Scenarios for global biodiversity in the 21st century. Science 330, 1496–1501.Google Scholar
Picard, M and Baltzinger, C (2012) Hitch-hiking in the wild: should seeds rely on ungulates? Plant Ecology and Evolution 145, 24–30.Google Scholar
Picard, M, Chevalier, R, Barrier, R, Boscardin, Y and Baltzinger, C (2016) Functional traits of seeds dispersed through endozoochory by native forest ungulates. Journal of Vegetation Science 27, 987–998.Google Scholar
Plue, J and Cousins, SA (2013) Temporal dispersal in fragmented landscapes. Biological Conservation 160, 250–262.Google Scholar
Polak, T, Gutterman, Y, Hoffman, I and Saltz, D (2014) Redundancy in seed dispersal by three sympatric ungulates: a reintroduction perspective. Animal Conservation 17, 565–572.Google Scholar
Revelle, W (2014) psych: Procedures for psychological, psychometric, and personality research. Northwestern University, Evanston, Illinois 165.Google Scholar
Schleuning, M, Fründ, J and García, D (2015) Predicting ecosystem functions from biodiversity and mutualistic networks: an extension of trait-based concepts to plant–animal interactions. Ecography 38, 380–392.Google Scholar
Schmidt, M, Sommer, K, Kriebitzsch, W-U, Ellenberg, H and von Oheimb, G (2004) Dispersal of vascular plants by game in northern Germany. Part I: Roe deer (Capreolus capreolus) and wild boar (Sus scrofa). European Journal of Forest Research 123, 167–176.Google Scholar
Schupp, EW, Jordano, P and Gómez, JM (2010) Seed dispersal effectiveness revisited: a conceptual review. New Phytologist 188, 333–353.Google Scholar
Soofi, M, Ghoddousi, A, Hamidi, AK, Ghasemi, B, Egli, L, Voinopol-Sassu, A-J, Kiabi, BH, Balkenhol, N, Khorozyan, I and Waltert, M (2017) Precision and reliability of indirect population assessments for the Caspian red deer Cervus elaphus maral. Wildlife Biology http://dx.doi.org/10.2981/wlb.00230Google Scholar
Von Oheimb, G, Schmidt, M, Kriebitzsch, W-U and Ellenberg, H (2005) Dispersal of vascular plants by game in northern Germany. Part II: Red deer (Cervus elaphus). European Journal of Forest Research 124, 55–65.Google Scholar
Wang, S, Lu, W, Waly, N, Ma, C, Zhang, Q and Wang, C (2017) Recovery and germination of seeds after passage through the gut of Kazakh sheep on the north slope of the Tianshan Mountains. Seed Science Research 27, 43–49.Google Scholar
Wei, T, Simko, V, Levy, M, Xie, Y, Jin, Y and Zemla, J (2017) Package ‘corrplot’. Statistician 56, 316–324.Google Scholar
Williams, SC, Ward, JS and Ramakrishnan, U (2008) Endozoochory by white-tailed deer (Odocoileus virginianus) across a suburban/woodland interface. Forest Ecology and Management 255, 940–947.Google Scholar
Willson, MF and Gende, SM (2004) Seed dispersal by brown bears, Ursus arctos, in southeastern Alaska. The Canadian Field-Naturalist 118, 499–503.Google Scholar
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