Agroforest Syst DOI 10.1007/s10457-010-9359-y Fungal fruitbodies and soil macrofauna as indicators of land use practices on soil biodiversity in Montado Anabela Marisa Azul • Sara Margarida Mendes • Jose´ Paulo Sousa • Helena Freitas Received: 22 January 2010 / Accepted: 28 October 2010 Ó Springer Science+Business Media B.V. 2010 Abstract The impacts of land use on soil biodiver- cutting practices followed by soil tillage (M), in sity are still poorly understood, although soil fungi and comparison with cutting practices with no soil tillage macrofauna are recognized to provide benefits to (Cu) and the control (C). The ECMF Laccaria laccata ecosystems. Here, we tested whether land use practices and Xerocomus subtomentosus exhibited a close used to control shrub density influences the fruiting relation with C and Cu plots while the saprobes, e.g., macromycetes (ectomycorrhizal-forming fungi— Entoloma conferendum, were associated to Ca and M ECMF—and saprobes) and soil macrofauna diversity plots. Most species associated to Cu plots were present and abundance in Montado ecosystems. To address in C plots during the 2 years, but not in Cu after the this influence, we conducted a 2-years’ period mon- cutting practices (in the second year of sampling). itoring of fungi fruitbodies and macrofauna in sixteen Regarding soil macrofauna, higher values of taxa and experimental plots in Montado landscape in southern species richness were observed in C and Cu plots in the Portugal. A total of 4,881 frutibodies (57 taxa of first year of sampling. The ant species Aphaenogaster ECMF and 64 taxa of saprobic fungi) and 3,667 soil senilis and several Staphylinid morphospecies exhib- invertebrates (73 species and morphospecies) were ited a close relation with M plots, whilst most spider monitored in the experimental plots. There was greater families were directly associated to C and Cu plots. losses in sporocarps production and taxa composition, After the shrub cutting practices, higher values of taxa particularly the ECMF, in plots where shrub density and species richness of soil macrofauna were observed was controlled by permanent grazing (Ca) or involving in M and Ca plots; the presence of species with a high competitive ability to colonize disturbed areas faster might explain the results. Contrary to the frutibodies production and diversity, species richness and abun- dance within soil macrofauna were identical between Cu and C in 2004. Thus, fruiting macromycetes and A. M. Azul (&) Á H. Freitas soil macrofauna diversity and abundance in Monta- Department of Life Sciences, Centre for Functional do’s, appear highly sensitive to land use and somewhat Ecology, University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal reflected a trend of severity to the current shrub e-mail: [email protected] management practices. S. M. Mendes Á J. P. Sousa Keywords Fungal fruit-body Á Soil macrofauna Á Department of Life Sciences, IMAR-CMA, University of Coimbra, PO Box 3046, Quercus suber L. Á Ecosystems monitoring Á 3001-401 Coimbra, Portugal Land use Á Montado 123 Agroforest Syst Introduction network that benefits plant communities by facilitating and influencing seedling establishment, by altering Quercus suber L. (cork oak) woodlands cover 23% of plant–plant interactions and by supplying and recy- the total forest area in Portugal (737 9 103 ha; DGRF cling nutrients (van der Heijden and Horton 2009), 2007). The cork oak woodlands are widespread in the while saprobic fungi are more specialized in decom- Mediterranean basin and cover about 2.2 million ha in posing dead organic plant material. In this context, a Europe (Portugal, Spain, France, and Italy) and North previous study reported that ECM fungal community Africa (Morocco, Algeria, and Tunisia). Most of cork associated to cork oak is quite diverse in both oak woodlands in Portugal are under agro-silvo- community structure and species composition, and pastoral exploitation, traditionally called Montado, affected by seasons, land use and cork oak mortality that is characterized by open oak formations of (Azul 2002; Azul et al. 2010). evergreen oaks (Q. suber and Quercus rotundifolia Soil fauna is also gaining importance in biodiversity L.), pastures and agricultural fields as undercover, assessment studies due to its active role on soil traditionally in a rotation scheme that includes fallows. processes and its sensitive response to changes in the The Montados are well adapted to the Mediterranean soil system (Bruyn 1997; Frouz 1999; Knoepp et al. environment and represent a good example of sustain- 2000; Rainio and Niemela¨ 2003; Sauberer et al. 2004). able agroforestry practice in Europe (Council of Soil organisms are representative of soil conditions Europe 1992) by combining two key aspects of land whether it’s physical, chemical or biological processes management: production and conservation, and due to we’re trying to assess (Blakely et al. 2002; Breure et al. their social and economic outcomes (Pinto-Correia 2005). This means that soil organisms could be used as and Vos 2004; Scarascia-Mugnozza et al. 2000). indicators of soil quality; soil invertebrates, one of the Changes in land management over the twentieth most abundant and diverse groups of soil organisms, century are thought to have contributed to Montado for example, often react very quickly to environmental landscape degradation (Joffre et al. 1999; Nunes et al. changes, with very sensitive responses (Bruyn 1997; 2005; Pinto-Correia 1993), with a significant decline Nickel and Hildebrandt 2003; Perner and Malt 2003; in cork oaks and plant and animal biodiversity (Da Rainio and Niemela¨ 2003). Some soil invertebrate Silva et al. 2008; Hector et al. 1999). Although indicators are already being used to assess certain successfully managed Montados remain, others are conditions (Beck et al. 2005; Hodkinson and Jackson increasingly being reforested with other tree species 2005;Ja¨nsch et al. 2005; Knoepp et al. 2000; Lavelle considered more lucrative by forest managers (e.g., et al. 2006; Nahmani et al. 2006; Rombke et al. Pinus pinea for the production of pine acorns; 2005; Ruiz Camacho et al. 2009; Sochova´ et al. 2006; Eucalyptus globulus, for the production of cellulose Souty-Grosset et al. 2005; Tischer 2005; Velasquez for the pulp industry), whilst other Montados are et al. 2007). abandoned and subject to shrub intrusion highly Several studies conducted in cork oak and holm- susceptible to fire (Nunes et al. 2005). In both cases, oak woodlands have been published (Cammell et al. a collapse of this highly-adapted and diverse Mediter- 1996; Da Silva et al. 2008; Deharveng et al. 2000; ranean-type ecosystem is observed. Rego and Dias 2000; Sousa et al. 1997) but none of Evaluating the impacts of management actions on these focused specifically on fungi and macrofauna as forests using bioindicators is widely recommended by indicators of the impacts of land use. European programs (Delbaere et al. 2002; EPBRS Understanding and predicting the consequences of 2002a, b). land use in soil biodiversity is emerging as one of the Plant mutualists, such as mycorrhizal fungi, and grand challenges for sustainable forest management, saprobes are widespread and are thought to maintain under climate change (European Environment Agency the structure and diversity of natural communities, 2004) and heavy mortality of evergreen oaks (Brasier influencing the performance of individual plants but 1996; Brasier and Scott 2008). In this work, we also altering plant community structure, plant produc- propose to investigate the performance of fruiting tivity, and nutrient cycling (Smith and Read 2008). macromycetes of ectomycorrhizal (ECMF) and sapro- Ectomycorrhizal (ECM) develop symbiotic structures bic fungi and soil macrofauna as indicators of land use on fine root tips and form a complex belowground in Montado ecosystems, an approach that can yield 123 Agroforest Syst insight into the link between management practices Montado landscape is dominated by Quercus and diversity descriptors of key soil components: fungi suber (40 to 60 trees per ha), but Quercus rotundi- and macrofauna. folia is also present, shrub strata (mainly Cistus salvifolius L., C. crispus L. and C. ladanifer L.) with plants with 4–5 years of age, occupying 65% of the Materials and methods total vegetation cover density. Cork is the main lucrative economical activity and it is harvested every Study site 9-year period; cattle breeding represent the second profitable activity. Land use is focused on practices to Field-work was conducted in a Montado landscape, control shrubs density to reduce the risk of fire. located in Foros de Vale de Figueira (Montemor-o- Novo, Portugal) (3884101000N, 882002300W) (Fig. 1). Experimental design The climate is typically Mediterranean, with a severe summer drought (2–4 months) and mild Sixteen experimental plots of 20 9 20 m were humid winters, with precipitation mainly from selected randomly among four Montado areas, each autumn to mid spring. The mean temperature ranges one with a different shrub management practice. The from 7.5°C (mean average in January) to 24°C four treatments include: the control (C), with no (mean average in July). Soils are classified as orthic shrub-cutting in the preceding 5 years, including the 2 luvisols with organic layers varying accordingly years (2003 and 2004) study period; the cut plots with land use and the year of perturbation; pH (Cu), with mechanized cutting practices that cut the ranges from 4.5 to 5.7. shoot of the plants and left it on the ground without till the soil afterwards; the cattle plots (Ca), with shrubs artificially maintained at low densities by permanent grazing of cows and sheep; and the mobilized plots (M), with mechanized practices with soil tillage that remove the completely the plants (Fig. 2). Shrub management practices were per- formed in Cu and M plots in the beginning of autumn 2004. Fruiting macromycetes of ECMF and saprobic fungi were monitored every 10 days during the peak fruiting period, from September to December, in 2003 and 2004.