Forest Ecology and Management 262 (2011) 1061–1066
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Forest Ecology and Management
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Selective logging in public pine forests of the central Iberian Peninsula: Effects of the recovery process on ant assemblages ⇑ Crisanto Gómez , Sílvia Abril
Department of Environmental Sciences, University of Girona, Montilivi Campus s/n, 17071 Girona, Spain article info abstract
Article history: Pine forests on the northern plateau of the Iberian Peninsula have a long history of use, exploitation, and Received 5 April 2011 management. Current management practices consist of selective logging with relatively short periods of Received in revised form 25 May 2011 time between logging events. The main objective of this study is to detect changes in ant assemblages in Accepted 27 May 2011 the short time periods between selective logging activities. Ants were sampled at 44 sites considering three grouping categories of time periods after the last timber extraction: short (<4 years), medium (4–8 years) and long (>8 years). After selective logging the number of ant species increases as the forest recovers. A look Keywords: at the differences between the assemblages when the analysis shifts from the species-specific level to func- Ants tional groups showed differences between the short and long categories. This indicates that in certain cir- Formicidae Ant assemblages cumstances the functional groups may be more informative of the functional restructuring of the ant Forest management assemblages in a disturbed habitat. Ant species from three functional groups display significant indicative Functional groups values (Opportunist, Hot Climate Specialists and Subordinate Camponotini) in the medium- and long-time- Pine forests after-logging categories: Messor capitatus (HCS) for medium-time category sites; and Aphaenogaster iberica (Op), Camponotus cruentatus (SC) and, Cataglyphis velox (HCS) for long-time category sites. No indicator spe- cies were found for the early stages of recovery. This information may also be of interest to managers because it reduces the number of data elements of the recovery status of these forests, and can be translated into monitoring protocols. The continued exploitation of these forests leads to an ant fauna that reflects this change. The results show that ant assemblages need at least 8 years to recover since only after that much time there is an emergence of Subordinate Camponotinae, a behaviorally dominant and low stress-tolerant functional group. This selective logging maintains the relative diversity and structure of ant assemblages. Ó 2011 Elsevier B.V. All rights reserved.
1. Introduction Given the general poverty of the soils of these pine forests, the underwood is very poor in woody shrubs, presenting a layer of dis- Pine forests (Pinus pinea L. and Pinus pinaster Ait.) on the northern continuous herbaceous mat composed mainly of various species of plateau of the Iberian Peninsula, located in a region known as Tierra xeric grasses. Forest management in the study area is characterized de Pinares (Pine Land) have a long history of use, exploitation and by a relatively low harvest intensity that permits a greater average management (Aránzazu et al., 1997). Information exists about the density of pines during the production cycle (213 pines ha 1). This use and exploitation of pine forests (logging, harvesting pine nuts, management is designed to encourage more timber production, and resin collection) in human settlements of the first Iron Age in although it does not prevent the extraction of pine nuts. The man- the area of study. These species do not sprout, so they are very sen- agement of similar forests to produce pine nuts or combined wood sitive to human disturbance. We understand that there is a docu- and pine nuts needs less pine density (100–175 pines ha 1) or, what mentary record of the region’s management and custody since the is the same, higher intensities of logging. An increase in canopy eleventh century. The pine forests under study are public use forests openness and a reduction in vegetation structure and understory in the province of Valladolid (Castile and León). They have been pre- plant richness can cause great changes to ant communities (Uhl served and managed as public use forests since their listing in 1859. and Vieira, 1989). However, taking into account both aspects, mainly This catalog of forests should be seen as a guarantee that their genet- herbaceous vegetation and relatively low intensity logging, the im- ic structure results from pristine formations, which have been al- pact of logging on the overall structure of the habitat is relatively tered by the story of the human-Mediterranean forest relationship light; except, of course, the partial disappearance of the tree layer. (Aránzazu et al., 1997). Ants are one of the terrestrial invertebrate groups used as bioin- dicators. They have been included in monitoring programs associ-
⇑ Corresponding author. ated with human activities around the world (Andersen et al., E-mail addresses: [email protected] (C. Gómez), [email protected] 2002; Bestelmeyer and Wiens, 1996; Gunawardene et al., 2010; (S. Abril). Majer, 1983; Nakamura et al., 2007; Read and Andersen, 2000;
0378-1127/$ - see front matter Ó 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2011.05.043 1062 C. Gómez, S. Abril / Forest Ecology and Management 262 (2011) 1061–1066
Ottonetti et al., 2006; Stephens and Wagner, 2006). In those pro- The distances between the five pine forests ranged between 1 grams ants have been used to monitor the effects of forest manage- and 5 km. ment practices such as selective logging and clearing, subsequent Ant species were assigned to functional groups according to their habitat recovery processes, or the subsequent land use of forest responses to environmental stress and disturbance, in line with pre- clearings (Gunawardene et al., 2010; Maeto and Sato, 2004; Nakam- vious studies of ants as bioindicators (Andersen, 1995, 1997; Read ura et al., 2007; Palladini et al., 2007; Stephens and Wagner, 2006). and Andersen, 2000; Gómez et al., 2003; Stephens and Wagner, Ants are an important component of the animal biomass and act 2006) and the information about ant functional group assignment as relevant ecosystem engineers (Folgarait, 1998). They have an compiled by Brown (2000). The functional groups considered are important influence on soils (Lobry de Bruyn, 1999), vegetation Dominant Dolichoderinae (DD), Subordinate Camponotini (SC), (herbivores, seed predators, seed dispersers) (Buckley, 198 2), and Hot Climate Specialist (HC), Cold-climate Specialist (CC), Cryptic other faunal groups. Ants are relatively sedentary and responsive Species (Cr), Opportunists (Op), Specialist Predators (SP), and Gener- to changes occurring at relatively small scales in space and time, alized Myrmicinae (GM) (Andersen, 1995, 1997). The Formica spe- most of which are easily sampled and observed, and the ecology of cies were assigned to the Opportunist group (all of them belong to the group as a whole is comparatively well understood (Brown, the fusca group) and the Tapinoma species were assigned to the 2000; Hölldobler and Wilson, 1990; Lach et al., 2010). These features Dominant Dolichoderinae group (Gómez et al., 2003; Castracani have made them focal animals in studies of the effects of all kinds of et al., 2010). ecological disturbances on terrestrial ecosystems. The use of ants and functional group approaches in studies of 2.2. Sampling Mediterranean ecosystems is slowly increasing (Gómez et al., 2003; Ottonetti et al., 2006; Castracani and Mori, 2006; Castracani Sampling was conducted in the warmer season, during June and et al., 2010) and the interesting results add substantial validity to July 2009, when ant activity is high in Mediterranean ecosystems their use as bioindicators. Also, we have relatively good knowledge (Cros et al., 1997). At each site, three sample points were randomly of ant species diversity and taxonomy for the Iberian and the Ital- established and separated by at least 25 m. Ants were sampled at ian peninsulas. Although studies of this type have been few to date, each sample point using two methods: pitfall trapping (3 traps open the increasing knowledge of Mediterranean ants makes them suit- for 48 h; 2.5 cm diameter; partly filled with ethylene glycol as a pre- able as an animal group of reference. servative, and 5 m apart, forming a triangle) and hand collecting (1 The main objective of this study is to detect any changes that person 30 min) around the trap triangle. A total of 396 traps were occur in ant assemblages in the short periods of time between placed in the pine forests (3 traps 3 sample points 44 sites) and selective logging activities in these pine forests. We wonder if 66 h of hand collecting (0.5 h 3 sample points 44 sites) took the ants can inform us of changes that have occurred after logging place. All ants were sorted by species and identified. The presence and during the forest recovery process. Our hypothesis is that this of each ant species in the trapping and hand collecting samples selective logging does not produce dramatic changes and helps to was recorded. All specimens were preserved and deposited in the maintain the relative diversity and structure of ant assemblages. laboratory of the PECAT Research Group, Department of Environ- mental Sciences, University of Girona. 2. Methods 2.3. Data analysis 2.1. Study site For each sample point, the data from the three pitfall traps and The study was carried out in Tierra de Pinares (Pine Land) situ- the hand collecting were combined. Ant species richness (number ated on the northern plateau of the Iberian Peninsula (Castilian of species) was compared for time categories using a one-way AN- Plateau, Castile and León, Central Spain) (Fig. 1). The pine forests OVA (SPSS 15.0). In order to check if the sampling effort was selected are located around the village of Olmedo (41°170N, 4° 4 adequate, accumulation curves for each of the three site group 10W, elevation 750–780 m). This is a zone with large pine forests types were constructed as well, based on the protocol of Brose surrounded by a matrix of arable land, grazing areas, and pine for- et al. (2003) on species richness estimators. Using several non- est fragments. The forests studied have been for public use (timber parametric estimators we obtained a preliminary idea of the and pine nut exploitation) since they were first listed in 1859 expected species richness in a variable range depending on each (Aránzazu et al., 1997). Today, the Environment Service of the Gov- estimator. The estimators used were: Jackknife 1, Jackknife 2, ICE, ernment of Castile and León in Valladolid is the management Chao2, and MM. For each of them, we obtained the proportion of authority. species found in the total inventory over the same estimator. The The climate is continental Mediterranean, with 452 mm of mean (in%) of the values was used as a criterion to choose the most annual rainfall. Mean monthly temperatures reach a high of appropriate estimator (see Brose et al., 2003, Fig. 6). In our case, it 20.1 °C in July and a low of 2.2 °C in January. Soils are quaternary was the Chao2 estimator. The species accumulation curves and diluvial sands. The pine forests studied are dominated by P. pinea species richness estimates were calculated using EstimateS L. and P. pinaster Ait., with a poor underwood of Lavandula stoechas (Colwell, 2009). Lam., Retama sphaerocarpa L., Cytisus scoparius L., Cistus laurifolius Multivariate analyses were carried out to investigate differ- L., Adenocarpus aureus (Cav.), Stipa spp. and Thymus spp. (Romero, ences in the structure of ant assemblages among the time-after- 1990). logging categories. Non-metric multidimensional scaling (NMDS) Ants were sampled at 44 sites. Each one corresponds to a ordinations were performed with PRIMER v.6 software (Clarke tranzón, a quadrangular unit of management. In our case all the and Warwick, 2001) on Bray–Curtis similarity matrices using three tranzones had similar areas (25–30 ha). And all the tranzones of datasets: site-specific species occurrence data, site-specific species the five pine forests (Mohago, Carrascosa, Sacedón, Gallinas, and abundance data, and functional group abundances. Data on the ant Abogadas) (Fig. 1) were grouped in three categories and selected species and functional group abundances were expressed as randomly. The three grouping categories were formed considering frequency scores (from 0 to 3) that represent the number of sample the time after the last timber extraction: short (<4 years, N =16 point occurrences by site. Similarity analysis (ANOSIM, Clarke and sites), medium (4–8 years, N = 13 sites) and long (>8 years, N =15 Warwick, 2001) was used to test the significance of differences in sites). The maximum time after timber extraction was 14 years. assemblage composition between the categories. C. Gómez, S. Abril / Forest Ecology and Management 262 (2011) 1061–1066 1063
Fig. 1. Location of studied pine forests in Tierra de Pinares, Castilla y León, Spain.
In order to detect and describe the value of different ant species (species occurrence data by site, species abundance data by site) as indicators of time after logging categories (short, medium and showed no differences between category sites. long), Indicator Species Analysis (Dufrêne and Legendre, 1997) The Indicator Species Analysis identified nine species as signif- was applied using the PC-ORD 5.0 package (McCune and Mefford, icant indicators (Table 2). Short-time-after-logging sites were not 1999). This method combines information on the concentration characterized by any ant species. Medium-time sites were charac- of species abundance in a particular group of sites and the reliabil- terized by the Hot Climate Specialists M. capitatus. Long-time sites ity of occurrence of a species in a particular group. The analysis were characterized by the Opportunistic Aphaenogaster iberica, the produces indicator values for each species in each group. The max- Hot Climate Specialist species C. velox and, the Subordinate imum indicator values obtained were tested for statistical signifi- Camponotini Camponotus cruentatus. cance using the Monte Carlo randomization procedure (1000 permutations; P < 0.05). For this analysis we considered data on 4. Discussion ant species abundance by site expressed as a frequency score from 0to3. The total number of ant species found (33), even considering each category separately (21–28 species), is not very different from 3. Results the ant species richness found in non-exploited pine forests of the Iberian Peninsula (Lombarte, 1986; Suñer, 1991), and is even great- A total of 33 species were collected in the study. In the pine for- er than that seen in pine reforestation in protected areas in other est sites, a total of 21 species were collected in the short-time cat- parts of the Mediterranean (Groc et al., 2007). In work by Groc egory (S), 25 species in the medium-time category (M) and 28 et al. (2007) the number of species caught per tranzón was similar species in the long-time category (L) (Table 1). The site species to the number caught by site (5–8 species of ants). This result is richness ranged from 3 to 8 (mean ± sd = 6.0 ± 1.5) in S sites, from probably due to the combination of the two most informative 4 to 9 (mean ± sd = 7.0 ± 1.4) in M sites, and from 6 to 13 in L sites collection systems used in similar studies: pitfall trapping and (mean ± sd = 8.5 ± 1.8). The number of species observed by site cat- standardized hand collecting (Gotelli et al., 2011). After selective egory differed between them (F2,30 = 9.37, p < 0.05), being higher in logging the number of ant species increases as the tranzón recov- L sites than in S sites (Tukey post-hoc test) (Fig. 2). The species ers. Although the differences are significant, there are relatively accumulation curves for each time category show that some of small variations from (6 to 8.5 species per tranzón) and a total of the additional species were not recorded, especially in M sites 21–28 species considering the two categories of extreme time (Fig. 3). Chao2 estimates 24 species in S sites, 30 species in M sites, (short vs. long time). 33 species in L sites, and 34 species combined. The exploitation of pine forests in the Pine Land is managed The richest genera were Camponotus (six species), Formica (four through selective logging with relatively short periods of time species), and Messor (four species) (Table 1). The species with the between logging events. Keep in mind that when we compare highest occurrence in sample points were Pheidole pallidula short and long times after logging, the time intervals are 0–4 years (Nylander) (94.7% of sample points, n = 132), Messor capitatus (short) and more than 8 years (long), with a maximum of 14 years. (Latr.) (71.2%), Cataglyphis velox Santschi (68.9%) and Crematogaster In studies that compare different types of forest management prac- scutellaris (Olivier) (59.8%). tices and ant assemblages, periods of time between the extraction NMDS ordinations and ANOSIM Global R values showed that only of timber, or the time difference between the categories being the functional group dataset slightly separated the short, medium, compared are much longer (see Wike et al. (2010) for a managed and long sites (Global R = 0.069, p < 0.05) (Fig. 4). In fact, the pair- pine plantation with harvest cycles of 20–25 years). Maeto and wise test showed that short-time sites were clearly different from Sato (2004) consider second growth native forests (30–70 years long-time sites (R = 0.124, p < 0.01). The other two databases used old) and old growth native forests with no records of clearance 1064 C. Gómez, S. Abril / Forest Ecology and Management 262 (2011) 1061–1066
Table 1 Summary of the ant species occurrences during the study. For each ant species the Functional Group (FG) is indicated: Dominant Dolichoderinae (DD), Subordinate Camponotini (SC), Hot-climate Specialist (HCS), Cold-climate Specialist (CCS), Cryptic Species (Cr), Opportunists (Op), Specialist Predators (SP), and Generalized Myrmici- nae (GM).
Pine forests Time logging categories FG Short Medium Long Sub-family Dolichoderinae Tapinoma madeirense Forel, 1895 DD + + + Tapinoma nigerrimum (Latreille, 1798) DD + + + Sub-family Formicinae Camponotus cruentatus (Latreille, 1802) SC + + + Camponotus foreli (Emery, 1881) SC + + + Camponotus lateralis (Olivier, 1792) SC + Fig. 3. Species accumulation curves of the three time after logging categories: short Camponotus piceus (Leach, 1825) SC + time (solid line), medium time (dashed line) and long time (dotted line). The values Camponotus pilicornis (Roger, 1859) SC + + + on the y-axis correspond to Sobs (Mao Tau) values in Colwell (2009). Camponotus sylvaticus (Olivier, 1792) SC + Cataglyphis cursor (Fonscolombe, 1846) HCS + Cataglyphis velox (Santschi, 1929) HCS + + + Formica cunicularia (Latreille, 1798) Op + + for at least 120 years. Palladini et al. (2007) compared regenerating Formica gerardi (Bondroit, 1917) Op + + forests by establishing a chronosequence of recovery of 5– Formica rufibarbis (Fabricius, 1793) Op + 427 years. Others compared logged and unlogged forests (Nakam- Formica subrufa (Roger, 1859) Op + + + ura et al., 2007). Our goal is to study the effect of the continuous Lasius alienus (Schenck, 1852) CCS + Plagiolepis pygmaea (Latreille 1798) Cr + + + controlled management of selective logging. Polyergus rufescens (Latreille, 1804) SP + + + Despite this, significant changes are already observable at the le- Sub-family Myrmicinae vel of ant assemblage biodiversity. These could be considered subtle Aphaenogaster iberica (Emery, 1908) Op + + + changes, but they may be informative and useful to managers of Chalepoxenus kutteri (Cagniant, 1973) CCS + + these forests. Decreases in species richness of ants have frequently Crematogaster auberti (Emery, 1869) GM + been identified after major alterations of various types of forests, fol- Crematogaster scutellaris (Olivier, 1792) GM + + + lowed by a further increase as time passes and vegetation recovers Gonioma hispanicum (Andrée, 1883) HCS + + + Messor barbarus (Linnaeus, 1767) HCS + + (Puntilla et al., 1991; Vasconcelos, 1999; Watt et al., 2002). Some- Messor bouvieri (Bondroit, 1918) HCS + + + times, though, these differences in species richness in situations Messor capitatus (Latreille, 1798) HCS + + + similar to ours (selective logging) have been small and not signifi- Messor structor (Latreille, 1798) HCS + cant (Gunawardene et al., 2010; Vasconcelos et al., 2000). Oxyopomyrmex sp (Andrée, 1881) HCS + + + Pheidole pallidula (Nylander, 1849) GM + + + Another result that confirms these small changes after a few Solenopsis latro (Forel, 1894) Cr + + years of gradual recovery of the forest is the similarity in the Temnothorax racovitzae (Bondroit, 1918) CCS + + composition of the ant assemblage. There were no significant Temnothorax recedens (Nylander 1856) CCS + + + differences in the ant assemblage composition between the time- Tetramorium caespitum (Linnaeus, 1758) Op + + after-logging categories in the NMDS analysis, using the presence/ Tetramorium forte (Forel, 1904) Op + absence of species and their abundance. But, if we pay attention to Total ant species 33 21 25 28 the differences between the assemblages when the analysis shifts from the species-specific level to functional groups, the analysis shows differences between the short- and long-time categories. This result is remarkable because it indicates that in certain circum- stances functional groups may be more informative, or at least offer another view of the functional restructuring of the ant assemblage in a disturbed habitat. So far, studies in Mediterranean ecosystems of the impact of some human activities on ant assemblages and on functional groups of ants have been considered distinctly different categories of study (Gómez et al., 2003; Ottonetti et al., 2006; Castracani et al., 2010). Clear differences were found in the compo- sition, presence and level indicator values of functional groups of ants. Our results support the successful use of the ant functional group approach in comparative studies of progressive situations, as well as in studies supporting their use in discrete designs or situations. Ant species from three functional groups (Opportunist, Hot Climate Specialists and Subordinate Camponotini) display signifi- cant indicative values in one or two categories over time after log- ging. We found no indicator species for the early stages of recovery. Although the Opportunist functional group could be one of the most indicative of the disturbance (Andersen, 1995), it is striking that there is no indicator species of the same group in the years closest to logging, but there is in the long-time category. Caution Fig. 2. Ant species richness (mean) from the three ‘‘time after logging’’ categories sites. The different letters at the top of the bar indicate significant differences should be used with the Hot Climate Specialists, the functional (Tukey post-hoc test, a < 0.05). group with more indicator species, because they can be associated C. Gómez, S. Abril / Forest Ecology and Management 262 (2011) 1061–1066 1065
Fig. 4. NMDS ordination of short, medium and long time after logging sites based on (a) ant species abundance, (b) presence/absence of ant species, and (c) functional groups. (S = short-time after logging sites, M = medium-time after logging sites, L = long-time after logging sites.)
Of the three functional groups with significant indicator species, the Subordinate Camponotini is, a priori, the group that we would Table 2 Species indicator values (IndVal) for the ant species bigger than 25% (P < 0.05). For expect to be indicators. We are considering just pine forests and each ant species the Functional Group (FG) is indicated: Subordinate Camponotini species of the genus Camponotus forage, not exclusively, but signif- (SC), Hot-climate Specialist (HCS) and Opportunists (Op). icantly in vegetation and trees. It is likely that this functional group Ant species FG IndVal(%) P is one of the ones most affected by logging and the alteration di- rectly affects one of its resources. C. cruentatus, the Subordinate Indicator species for Medium time after logging sites Messor capitatus HCS 33.2 0.034 Camponitini indicator species of the category of more than 8 years Indicator species for Long time after logging sites after logging, is a typical Mediterranean species, distributed Aphaenogaster iberica Op 41.4 0.0002 throughout North Africa and the Iberian and Italic peninsulas (Col- Camponotus cruentatus SC 33.3 0.0004 lingwood, 1978). It is considered primarily a forest species, but can Cataglyphis velox HCS 38.0 0.001 also be found in non-forest areas but with shrub cover. Several authors have highlighted the fact that C. cruentatus is not observed with open, sunny habitats, and not with forests. The probable in disturbed habitats, while it is common in undisturbed forest explanation is that the pine forests we have been studying are areas in the Iberian Peninsula (Suñer, 1991). The results confirm certainly open forests with very underdeveloped understories that C. cruentatus can serve as an important ant species to be con- where the sunlight can easily reach the ground. Therefore, we con- sidered in monitoring the recovery process. This issue is even sider the forests studied near open habitats and not with closed clearer if we consider that it is one of the largest ant species of and cold habitats. We cannot ignore the possible influence of ant the Iberian Peninsula (worker size: 10–16 mm), easy to observe species that inhabit the large cereal steppes surrounding these for- and recognize. The other two indicator species in the same cate- ests as a source of species. Maeto and Sato (2004) found that open gory, A. iberica and C. velox, are thermophilic species and usually habitat specialist species were abundant in disturbed forests, do not forage in the vegetation. Their connection with tree cover whereas the presence of forest specialists decreased. Both groups, is lesser than in C. cruentatus. Opportunists and Hot Climate Specialists, have been associated Finally, this information obtained may also be of interest to with disturbed habitats (Andersen, 1991; Bestelmeyer and Wiens, managers because it reduces the data elements of the recovery 1996; Gómez et al., 2003), and perhaps in this case, we are showing status of these forests, and can be translated into simple monitor- just a continued but controlled level of disturbance of these forests. ing protocols that can be carried out by non-professionals. Another As in other similar situations, selective logging is still practiced and aspect that supports this point is the fact that all species with sig- has had the potential to permanently alter the composition of ant nificant indication values have relatively large sizes, are easy to ob- fauna (Gunawardene et al., 2010). serve and capture, and are easy to identify with a little practice. 1066 C. Gómez, S. Abril / Forest Ecology and Management 262 (2011) 1061–1066
5. Conclusions Colwell, R.K., 2009. Estimates. Statistical estimation of species richness and shared species from samples. Version 8.2