Fruit removal from rowanberry (Sorbus aucuparia) trees at urban and rural areas in Finland: A multi-scale study

Highlights

• Large number of frugivorous birds feed on urban ornamental trees.

• In urban areas the birds consumed the rowanberry fruits later than in rural areas.

• The rowanberry fruit was removed earlier from the tops of trees.

• Urban-related disturbance probably had impacts on the use of fruits by bird species.

• Ornamental trees are important food resources for frugivorous birds in urban environment.

• Rowanberry crop size per tree was higher in urban than in rural areas.

Abstract

Urbanization changes landscape, causes destruction of natural habitats, and reduces species diversity. Urbanization can alter the interaction between fruit-bearing plants and frugivorous birds such as the Fieldfare, Turdus pilaris, and Bohemian waxwing, Bombycilla garrulus, which are the most abundant frugivorous bird species in Finland. Rowanberry, Sorbus aucuparia, is an ornamental tree species used commonly in the urban landscaping. It can promote bird diversity and the pleasantness of the urban environment for humans. The study was conducted on three spatial scales ranging from the macro scale (600 km latitudinal gradient) to the regional scale (rural vs. urban habitats), and to the micro scale (different tree parts) in three towns and their nearby rural areas in Finland. About 25 trees were photographed on each site three times during the autumn until the rowanberry fruit-crop had been used up. At the beginning of the research the crop size was larger on the urban trees than that of rural ones. The fruit removal rate was not related to the geographical location. However, in urban habitats the fruits were consumed later than in rural habitats. At the tree-level, the rowanberry fruits were removed earlier at the tops of trees. Our results suggest that earlier use of rowanberry fruits from rural habitats and tree tops may be related on human and predator-related disturbances. Our results indicated that urban rowanberry fruit crop is important food resource for frugivorous bird species in urban areas.

Introduction

Urban areas are characterized by high levels of disturbance, and only remnants of the original habitats exist in urban centres (Francis and Chadwick, 2013, Schlesinger et al., 2008). These changes may impact also on resource availability as well as the force and frequency of interspecific interactions in the community (Francis & Chadwick, 2013). It has been suggested that due to high amounts of predictable anthropogenic food resources, the temporal variability of urban bird assemblages is lower in urban than in natural areas (Jokimäki and Kaisanlahti-Jokimäki, 2012, Suhonen et al., 2009, Suhonen et al., 2010). However, the abundance of fruits and berries varies a lot between years, and therefore the abundance of frugivorous bird species varies a lot depending on the fruit crop size (Lehikoinen, Väisänen, Hokkanen, 2010). Ornamental trees would provide fruits and berries for frugivorous bird species, and that this should be taken into account in urban landscaping (Aslan and Rejmánek, 2010, Francis and Chadwick, 2013). However, the exploitation of fruit or berry crops of ornamental trees in relation to the urbanization has seldom been studied (but see Aslan and Rejmánek, 2010, Tyrväinen, 1975).

The interaction between fruit-bearing plants and frugivorous birds is an example of widespread mutualism, birds get food and at the same time disperse plant seeds. For example, in temperate forests, the mutualism between fleshy-fruited plants and birds is the main seed dispersal mechanism (Albrecht et al., 2012, Richardson et al., 2000). A variety of factors determine effective seed dispersal; this includes the visitation frequency of frugivorous species (Schupp, Jordano, & Maria Gomez, 2010), their local abundance, and their capacity to remove fruits and berries (Herrera et al., 1994, Jordano and Schupp, 2000). The patterns in fruit removal by frugivorous birds have been studied earlier mainly in fragmented forest environments (Denslow, 1987, Herrera et al., 1994, Malmborg and Willson, 1988) and rural habitats (Albrecht et al., 2012), but seldom in urban environments (but see Aslan & Rejmánek, 2010). Previous studies have indicated that mutualisms, such as frugivorous birds and the plant species may be vulnerable to habitat fragmentation and degradation (Albrecht et al., 2012, Cordeiro and Howe, 2003, Lehouck et al., 2009b, Santos and Telleria, 1994). However, results obtained in natural or rural landscapes do not necessarily apply to urban habitats (e.g. Aronson, Handel, & Clemants, 2007). Human-induced activities such as trade and travel seem to disturb ecosystems in urban landscapes. In addition, the urban heat–island effect, light, and noise pollution can affect both community structure and species composition and resource use (Francis & Chadwick, 2013). However, little is known about how these factors affect frugivorous birds’ preferences and ornamental plant mutual interactions such as a the removal rates of fruits.

Urbanization is known to impact on animals and plants in different ways, depending on the species’ characteristics and the type and scale of habitat modification involved. When urbanization causes a decrease in the abundance or species richness of frugivorous animals, then interactions between plants and the dispersers of their seeds can be constrained by the overall urbanization process. The structural features of habitat urbanization can be important factors explaining the dynamics of the mutualism between ornamental plants and frugivorous bird species. Only a few studies have analyzed the differential responses of frugivorous birds on fruit abundance in human-induced landscapes (Aslan and Rejmánek, 2010, Gonzalez-Varo, 2010, Moran et al., 2004). Studying the way in which urbanization can alter fruit-removal regimes may improve our predictive understanding about the variation in seed-dispersal effectiveness (Dennis and Westcott, 2006, Schupp et al., 2010). Interspecific interaction may also vary across on several spatial scales. Our understanding of how the differential responses of the frugivorous birds in terms of fruit removal changes across spatial scales is inadequate. For example, the mutual interaction between plants and the fruit-removal rates achieved by frugivorous bird species can vary by geographical location, habitat, and even by tree part.

In this study, we studied effects of urbanization on fruit removal from rowanberry (Sorbus aucuparia, Rosaceae) trees in Finland. The rowanberry was chosen as study object because it has regular crop size (Sperens, 1997) and it is used also as an ornamental tree in urban landscaping. In addition, the fruits of rowanberry tree have been indicated as being the main factor explaining the autumn/winter abundance of many frugivorous bird species in northern latitudes (Fox et al., 2009, Lehikoinen et al., 2010, Tyrväinen, 1975). The fresh fruits of rowanberry trees mainly are consumed by the Fieldfare, Turdus pilaris, the Bohemian waxwing, Bombycilla garrulous, and the Bullfinch, Pyrrhula pyrrhula in Finland (Fox et al., 2009, Lehikoinen et al., 2010, Tyrväinen, 1975). We compared the magnitude of removal rates of rowanberry fruits on three spatial scales in relation to latitudinal location, urban and rural habitats, and different parts of trees. Based on observations of plants and avian frugivorous, we addressed the following research questions: (1) Do frugivorous bird abundance varied seasonally and by geographical regions? Many frugivorous bird species move southwards when the fruit crop is used in northern areas (Lehikoinen et al., 2010); therefore it is also important to consider the latitudinal effects on rowanberry fruit-removal when comparing fruit consumption between urban and rural areas. (2) Do removal rates differ by geographical location? We predicted that the fruit removal will follow the abundance of frugivorous bird species, starting from northern areas and moving towards southern areas as a result of avian migration from north to south in the autumn. (3) Do fruit removal rate differ between urban and rural areas? We predicted that the removal rate of rowanberry fruits may be later in the urban than in the rural areas due to the higher level of human-induced disturbance in the urban area as compared to rural areas (Forman and Alexander, 1998, Summers et al., 2011). (4) Do removal rates vary by tree parts? At the tree revel, we predicted that the removal of rowanberry fruits may begin earlier at the top of trees than in the lower parts of trees due to the higher risk of human-induced disturbance (Forman and Alexander, 1998, Schlesinger et al., 2008, Summers et al., 2011) and/or the higher risk of predation in the lower parts of trees (Suhonen, 1993). Birds foraging at the top of trees might detect earlier the possible predators, either human, bird or mammal, and therefore the fruits would be firstly consumed from the more safety tree part, top of the trees, and when the tree tops are empty of fruits, the frugivorous birds are forced to use more disturbed lower parts of the trees.