Abstract
The brown bear (Ursus arctos L.) is an omnivorous large mammal that has an essential function in many ecosystems as a seed disperser. We studied the brown bear’s role as a seed dispersal agent in a mixed temperate forest in northern Anatolia, Turkey. We collected 197 fecal samples from the field during the brown bear’s active period for two consecutive years. We extracted seeds of 34 plant taxa from fecal samples. Among these taxa, 29 had intact seeds, whereas seeds of 5 were found to be entirely or mostly physically damaged. Damaged seeds belonged to fruits of acorn, capsule, nut, and drupe-like nut types, while no or few seeds from fleshy fruits such as berry, drupe, pome, and rosehip types had damage. Seeds from pome type fruits of Malus sylvestris and Pyrus elaeagnifolia had a higher germination percentage in feces than in the control (fresh seeds collected from the field), but that was quite the opposite in berries of Lonicera caucasica and Vaccinium arctostaphylos. No difference in germination percentage was found between feces and control groups in seeds from rosehips. Our results reveal that seeds of several species found in the study area are dispersed by the brown bear, especially those with fleshy fruits (e.g., Rosaceae members). In this study, we established the role of the brown bear as a seed dispersal agent in northern Anatolian mixed temperate forests. Our study suggests that fruit type is a determinant of the success of endozoochorous seed dispersal by the brown bear.
Similar content being viewed by others
References
Albert A, Auffret AG, Cosyns E, Cousins SA, D'hondt B, Eichberg C, Eycott AE, Heinken T, Hoffmann M, Jaroszewicz B, Malo JE, Mårell A, Mouissie M, Pakeman RJ, Picard M, Plue J, Poschlod P, Provoost S, Schulze KA, Baltzinger C (2015) Seed dispersal by ungulates as an ecological filter: a trait-based meta-analysis. Oikos 124(9):1109–1120
Ambarlı H (2016) Litter size and basic diet of brown bears (Ursus arctos, Carnivora) in northeastern Turkey. Mammalia 80:235–240
Ambarlı H, Ertürk A, Soyumert A (2016) Current status, distribution, and conservation of brown bear (Ursidae) and wild canids (gray wolf, golden jackal, and red fox; Canidae) in Turkey. Turk J Zool 40(6):944–956
Ambarlı H, Bilgin CC (2008) Human–brown bear conflicts in Artvin, northeastern Turkey: encounters, damage, and attitudes. Ursus 19(2):146–153
Anderson S, Ertug-Yaras F (1998) Fuel fodder and faeces: an ethnographic and botanical study of dung fuel use in Central Anatolia. Environ Archaeol 1(1):99–109
Anderson TM, Schütz M, Risch AC (2014) Endozoochorous seed dispersal and germination strategies of Serengeti plants. J Veg Sci 25(3):636–647
Barcelos AR, Bobrowiec PED, Sanaiotti TM, Gribel R (2013) Seed germination from lowland tapir (Tapirus terrestris) fecal samples collected during the dry season in the northern Brazilian Amazon. Integr Zool 8:63–73
Baskin CC, Baskin JM (2014) Seeds: ecology, biogeography, and evolution of dormancy and germination, 2nd edn. Elsevier/Academic Press, San Diego
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Bobadilla SY, Marchetta A, Dacar MA, Ojeda RA, Cuevas MF (2020) Food habits of European rabbit and its role as seed dispersal of two Mosqueta roses: facilitation among non-native species in a semiarid protected area of Argentina? Biol Invasions 22:1565–1571
Bojarska K, Selva N (2012) Spatial patterns in brown bear Ursus arctos diet: the role of geographical and environmental factors. Mammal Rev 42(2):120–143
Boitani L, Jdeidi T, Masseti M, Nader I, de Smet K, Cuzin F (2010) Ursus arctos. The IUCN red list of threatened species 2010: e.T41688A10514336. Accessed on 15.01.2020
Bruun H, Poschlod P (2006) Why are small seeds dispersed through animal guts: large numbers or seed size per se? Oikos 113:402–411
Bustamante RO, Simonetti JA, Mella JE (1992) Are foxes legitimate and efficient seed dispersers? A field test. Acta Oecol 13(2):203–208
Campos-Arceiz A, Blake S (2011) Megagardeners of the forest–the role of elephants in seed dispersal. Acta Oecol 37(6):542–553
Can ÖE, Togan İ (2004) Status and management of brown bears in Turkey. Ursus 15:48–53
Cavallero L, Aizen MA, Raffaele E (2012) Endozoochory decreases environmental filtering imposed to seedlings. J Veg Sci 23:677–689
Ciucci P, Tosoni E, Di Domenico G, Quattrociocchi F, Boitani L (2014) Seasonal and annual variation in the food habits of Apennine brown bears, Central Italy. J Mammal 95(3):572–586
Clevenger AP, Purroy FJ, Pelton MR (1992) Food habits of brown bears (Ursus arctos) in the Cantabrian Mountains, Spain. J Mammal 73(2):415–421
Chynoweth M, Coban E, Altin Ç, Şekercioğlu Ç (2016) Human-wildlife conflict as a barrier to large carnivore management and conservation in Turkey. Turk J Zool 40(6):972–983
Correia M, Heleno R, Vargas P, Rodríguez-Echeverría S (2018) Should I stay or should I go? Mycorrhizal plants are more likely to invest in long-distance seed dispersal than non-mycorrhizal plants. Ecol Lett 21(5):683–691
Cosyns E, Delporte A, Lens L, Hoffmann M (2005) Germination success of temperate grassland species after passage through ungulate and rabbit guts. J Ecol 93(2):353–361
Çilingir FG, Akın Pekşen Ç, Ambarlı H, Beerli P, Bilgin CC (2016) Exceptional maternal lineage diversity in brown bears (Ursus arctos) from Turkey. Zool J Linnean Soc 176(2):463–477
Davis PH (ed) (1965-1985) Flora of Turkey and the East Aegean Islands. Vols. 1-9, Edinburgh University Press
Edizer Y, Hancı F, Güneş M (2009) Determination of seed germination of some wild cherry (Prunus avium L.) genotypes grown in Kastamonu province. Gaziosmanpaşa Üniversitesi Ziraat Fakültesi Dergisi 26(1):7–11
Fahimi H, Qashqaei AT, Chalani M, Asadi Z, Broomand S, Ahmadi N, Yusefi GH (2018) Evidence of seed germination in scats of the Asiatic black bear Ursus thibetanus in Iran (Mammalia: Carnivora). Zool Middle East 64(2):182–184
Fedriani JM, Delibes M (2009) Seed dispersal in the Iberian pear, Pyrus bourgaeana: a role for infrequent mutualists. Ecoscience 16(3):311–321
Gill RMA, Beardall V (2001) The impact of deer on woodlands: the effects of browsing and seed dispersal on vegetation structure and composition. Forestry 74(3):209–218
Güner S, Tilki F (2009) Dormancy breaking in Cotinus coggygria Scop. Seeds of three provenances. Sci Res Essays 4(2):73–77
Harrer LE, Levi T (2018) The primacy of bears as seed dispersers in salmon-bearing ecosystems. Ecosphere 9(1):e02076
Herrera C (1989) Frugivory and seed dispersal by carnivorous mammals, and associated fruit characteristics, in undisturbed Mediterranean habitats. Oikos 55(2):250–262
Herrera CM (1995) Plant-vertebrate seed dispersal systems in the Mediterranean: ecological, evolutionary, and historical determinants. Annu Rev Ecol Syst 26(1):705–727
Herrera CM, Jordano P (1981) Prunus mahaleb and birds: the high-efficiency seed dispersal system of a temperate fruiting tree. Ecol Monogr 51(2):203–218
Jordano P (1995) Angiosperm fleshy fruits and seed dispersers: a comparative analysis of adaptation and constraints in plant-animal interactions. Am Nat 145(2):163–191
Karimi S, Hemami MR, Esfahani MT, Akhani H, Baltzinger C (2018a) Complementary endozoochorous seed dispersal by large mammals in the Golestan National Park, Iran. Seed Sci Res 28(4):294–302
Karimi S, Hemami MR, Esfahani MT, Baltzinger C (2018b) The role of brown bear (Ursus arctos) in the plant seed dispersal of Golestan National Park. Iran J Appl Ecol 7(2):29–42
Karimi S, Hemami MR, Esfahani MT, Baltzinger C (2020) Endozoochorous dispersal by herbivores and omnivores is mediated by germination conditions. BMC Ecol 20:49
Kollmann J, Schill HP (1996) Spatial patterns of dispersal, seed predation and germination during colonization of abandoned grassland by Quercus petraea and Corylus avellana. Vegetatio 125(2):193–205
Lalleroni A, Quenette PY, Daufresne T, Pellerin M, 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):1–9
Loacker K, Kofler W, Pagitz K, Oberhuber W (2007) Spread of walnut (Juglans regia L.) in an Alpine valley is correlated with climate warming. Flora 202(1):70–78
Manzano P, Malo JE, Peco B (2005) Sheep gut passage and survival of Mediterranean shrub seeds. Seed Sci Res 15:21–28
McLellan BN, Proctor MF, Huber D, Michel S (2017) Ursus arctos (amended version of 2017 assessment). The IUCN red list of threatened species 2017: e.T41688A121229971. https://doi.org/10.2305/IUCN.UK.2017-3.RLTS.T41688A121229971.en. Accessed 15 Jan 2020
Moles AT, Westoby M (2004) Seedling survival and seed size: a synthesis of the literature. J Ecol 92:372–383
Moles AT, Westoby M (2006) Seed size and plant strategy across the whole life cycle. Oikos 113:91–105
Naves J, Fernández-Gil A, Rodríguez C, Delibes M (2006) Brown bear food habits at the border of its range: a long-term study. J Mammal 87:899–908
Nawaz MA, Valentini A, Khan NK, Miquel C, Taberlet P, Swenson JE (2019) Diet of the brown bear in Himalaya: combining classical and molecular genetic techniques. PLoS One 14(12):e0225698
Niedziałkowska M, Hayward MW, Borowik T, Jędrzejewski W, Jędrzejewska B (2019) A meta-analysis of ungulate predation and prey selection by the brown bear Ursus arctos in Eurasia. Mammal Res 64(1):1–9
Otani T, Shibata E (2000) Seed dispersal and predation by Yakushima macaques, Macaca fuscata yakui, in a warm temperate forest of Yakushima Island, southern Japan. Ecol Res 15:133–144
Pakeman RJ, Digneffe G, Small JL (2002) Ecological correlates of endozoochory by herbivores. Funct Ecol 16(3):296–304
Paralikidis NP, Papageorgiou NK, Kontsiotis VJ, Tsiompanoudis AC (2010) The dietary habits of the brown bear (Ursus arctos) in western Greece. Mamm Biol 75:29–35
Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sci Discuss 4(2):439–473
Persson IL, Wikan S, Swenson JE, Mysterud I (2001) The diet of the brown bear Ursus arctos in the Pasvik Valley, northeastern Norway. Wildl Biol 7(3):27–37
Pesendorfer MB, Sillett TS, Koenig WD, Morrison SA (2016) Scatter-hoarding corvids as seed dispersers for oaks and pines: a review of a widely distributed mutualism and its utility to habitat restoration. Condor 118(2):215–237
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna https://www.R-project.org
Ribeiro RC, Figueiredo MLN, Picorelli A, Oliveira DM, Silveira FA (2016) Does seed coat structure modulate gut-passage effects on seed germination? Examples from Miconieae DC. (Melastomataceae). Seed Sci Res 26(2):139–147
Sádlo J, Chytrý M, Pergl J, Pyšek P (2018) Plant dispersal strategies: a new classification based on the multiple dispersal modes of individual species. Preslia 90(1):1–22
Samuels IA, Levey DJ (2005) Effects of gut passage on seed germination: do experiments answer the questions they ask? Funct Ecol 19:365–368
Schlägel UE, Grimm V, Blaum N, Colangeli P, Dammhahn M, Eccard JA, Hausmann SL, Herde A, Hofer H, Joshi J, Kramer-Schadt S, Litwin M, Lozada-Gobilard SD, Müller MEH, Müller T, Nathan R, Petermann JS, Pirhofer-Walzl K, Radchuk V, Rillig MC, Roeleke M, Schäfer M, Scherer C, Schiro G, Scholz C, Teckentrup L, Tiedemann R, Ullmann W, Voigt CC, Weithoff G, Jeltsch F (2020) Movement-mediated community assembly and coexistence. Biol Rev 95:1073–1096
Seryodkin IV (2016) Behavior of brown bears during feeding in the Sikhote-Alin. Ach Life Sci 10:38–47
Smith P (ed) (2018) The book of seeds: a life size guide to six hundred species from around the world. Ivy Press, The University of Chicago Press
Soons MB, Van Der Vlugt C, Van Lith B, Heil GW, Klaassen M (2008) Small seed size increases the potential for dispersal of wetland plants by ducks. J Ecol 96:619–627
Soyumert A (2010) Kuzeybatı Anadolu ormanlarında fotokapan yöntemiyle büyük memeli türlerinin tespiti ve ekolojik özelliklerinin belirlenmesi. PhD Thesis. Hacettepe University, Turkey, 141 pp.
Steyaert SM, Hertel AG, Swenson JE (2019) Endozoochory by brown bears stimulates germination in bilberry. Wildl Biol 1:1–5
Tavşanoğlu Ç, Pausas JG (2018) A functional trait database for Mediterranean basin plants. Sci Data 5:180135
The Plant List (2013) The Plant List, version 1.1. http://www.theplantlist.org. Accessed 20 April 2020
Toyran K, Aşan N, Pamukoğlu N (2009) A brief study on diet components of red fox (Vulpes vulpes Linnaeus, 1758) from Central Anatolia (Mammalia: Carnivora). Kafkas Üniversitesi Fen Bilimleri Enstitüsü Dergisi 2(1):37–40
Traveset A, Willson MF (1997) Effect of birds and bears on seed germination of fleshy-fruited plants in temperate rainforests of Southeast Alaska. Oikos 80:89–95
Traveset A, Verdú M (2002) A meta-analysis of the effect of gut treatment on seed germination. In: Levey DJ, Silva WR, Galetti M (eds) Seed dispersal and frugivory: ecology, evolution, and conservation. Wallingford, UK, CABI Pub, pp 339–350
Traveset A, Bermejo T, Willson M (2001) Effect of manure composition on seedling emergence and growth of two common shrub species of Southeast Alaska. Plant Ecol 155(1):29–34
Traveset A, Robertson AW, Rodríguez-Pérez J (2007) A review on the role of endozoochory in seed germination. In: Dennis AJ, Schupp EW, Green RA, Westcott DA (eds) seed dispersal: theory and its application in a changing world. CAB international, pp. 78-103
Urbisz A, Urbisz A (2007) European chestnut (Castanea sativa mill.)-a tree naturalized on the Baltic Sea coast? Pol J Ecol 55(1):175–179
Willson MF (1993) Mammals as seed-dispersal mutualists in North America. Oikos 67:159–176
Willson MF, Gende SM (2004) Seed dispersal by brown bears, Ursus arctos, in southeastern Alaska. Can Field-Nat 118:499–503
Willson MF, Whelan CJ (1990) Variation in postdispersal survival of vertebrate-dispersed seeds: effects of density, habitat, location, season, and species. Oikos 57:191–198
Acknowledgments
We would like to thank İlkim Tan, Elif Deniz Ülker, and İsmail Bekar for their help in extracting seeds from feces material and supporting the experimental set-up. We are grateful to Salih Gücel, Barış Özüdoğru, Haşim Altınözlü, and Şinasi Yıldırımlı for their contribution to the taxonomical identification of the plant samples collected in the field. We also would like to thank the two anonymous reviewers for their suggestions to improve the manuscript. The fieldwork of the study was conducted with the permission of the General Directorate of Nature Conservation and National Parks of Turkey (no: 41152, date: 05.09.2012) and the General Directorate of Agricultural Research and Policies of Turkey (no: 2643, date: 26.07.2012).
Funding
This study was financially supported by the Scientific and Technological Research Council of Turkey (TÜBİTAK, project no: 212T042).
Author information
Authors and Affiliations
Contributions
A.S., A.E., and Ç.T. designed the study and collected fecal samples in the field; D.D.K. and C.Ü.D. conducted the lab work, including the germination experiment; Ç.T. analyzed data and wrote the first draft of the manuscript; all authors critically contributed to the final version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Additional information
Communicated by: Dries Kuijper
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
ESM 1
(DOCX 21 kb)
Rights and permissions
About this article
Cite this article
Tavşanoğlu, Ç., Kazancı, D.D., Soyumert, A. et al. Seed dispersal by the brown bear in a mixed temperate forest: fruit type matters. Mamm Res 66, 137–147 (2021). https://doi.org/10.1007/s13364-020-00551-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13364-020-00551-6