Are Bird Communities Structured by Arthropod Availability?

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Revista Catalana d’Ornitologia 21:17-28, 2005 Post-fire dynamics in Mediterranean shrublands: are bird communities structured by arthropod availability?

Sergi Herrando, Lluís Brotons & Santiago Llacuna

The relationship between arthropod availability and bird energy requirements was studied in Mediterranean shrublands. Specifically, we tested the hypothesis that food availability is a possible constraint in the recovery of bird communities in post-fire dynamics. We used the sweep-net sampling method to collect arthropods, and the point-census method to assess bird abundance. The censuses were carried out during the breeding and wintering seasons in a fire-free zone and in two burned zones (one burned four years before the fieldwork, the other 16 years before it). During the breeding season, we found a positive association between arthropod availability and bird requirements in all three zones. However, compared with the other two zones, the recently burned zone contained fewer birds than expected, based on arthropod availability. Thus, it seems that birds exerted significantly lower predation pressure on arthropod populations in this zone than in the other two zones, which resembled each other in this parameter. These results suggest that arthropod availability does not constrain breeding-bird numbers soon after fire; however, it could do so in later successional stages. During winter, when the studied bird species also feed on fleshy-fruits, there were no conclusive associations between arthropods and birds.

Key words: arthropod availability, bird community, predation pressure, post-fire succession, burned zones, Mediterranean shrublands. Sergi Herrando, Institut Català d’Ornitologia, Museu de Ciències Naturals, Passeig Picasso s/n, 08003 Barcelona. E-mail: [email protected] Lluís Brotons, Àrea de Biodiversitat, Centre Tecnològic Forestal de Catalunya, Pujada del Seminari s/n, 25280 Solsona. Santiago Llacuna, Parc Natural del Garraf, Diputació de Barcelona, c/ Urgell 187, 08036 Barcelona. Received: 02.12.04; Accepted: 02.08.05 / Edited by Jordi Domènech.

The study of avian post-fire dynamics in Medi- vegetation recovery. An association between terranean shrublands has traditionally focused food availability and bird abundance is often on bird-community turnover and its clear asso- detected during the breeding season (as a con- ciation with changes in vegetation structure (e.g. sequence of high food requirements for feeding Lawrence 1966, Prodon et al. 1984, Stanton nestlings) as well as during the winter (when 1986, Prodon et al. 1987, Vicente 1991, Pons & there may be food scarcity). However, there is a Prodon 1996, Izhaki & Adar 1997, Herrando et wide disparity of results over all periods, from al. 2003). Most of these works showed that bird strong associations between bird abundance and abundance usually increases progressively, food availability to no correlation at all (e.g. matching vegetation recovery. However, an as- Newton 1980, Martin 1987, Wiens 1989, Diaz sociation between the vegetation and the avian & Pulido 1993, Morris & Thompson 1998). The community may be due to an indirect effect of lack of a relationship may be found when these the increase in food available to birds following resources are so abundant that they do not im-

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pose any constraint on the exploiters. This is a small valleys located at 100–500 m a.s.l. The common pattern when there is a second, more average annual rainfall is about 500 mm, but limiting resource for individuals, or when the karstic lithology of these hills provides only populations are in a growing stage (Begon et al. skeletic soils, which offer extremely dry condi- 1987). tions for plant communities. The vegetation of In addition, in Mediterranean ecosystems, the study area is dominated by shrubs such as studies on the post-fire dynamics of inverte- Arbutus unedo, Quercus coccifera, Pistacia brates, the main food source for many breeding lentiscus, Ulex parviflorus, Rosmarinus officinalis, passerines, have usually focused on soil arthro- Thymus vulgaris, Chamaerops humilis and Olea pods (Prodon et al. 1987, Athias-Binche et al. europaea, and by Pinus halepensis trees. These 1987, Sgardelis et al. 1995, Broza & Izhaki plant species are widespread in the natural park, 1997), whose numerical responses to fire seem regardless of the frequency of fire, which has to be very variable depending on the soil layer basically affected species abundance but not in which they live, as well as on the severity of species composition, although grasses such as the fire in terms of temperature and duration. Ampelodesmos mauritanica and Brachypodium Only a few studies have dealt with the effects retusum were more abundant in recently burned of fire on foliage invertebrates (e.g. Woinarski zones than in others (Herrando et al. 2003); this & Recher 1997, Pons 1998). As with birds, these is a common pattern in Mediterranean authors reported a fast increase in foliage-ar- shrublands (Trabaud 1981). thropod abundance in the vegetation regener- The area that is the Garraf Natural Park does ating rapidly after fire. However, despite the not now support any economic resources apart trends described for both birds and arthropods from those related to leisure activities. At the after fire, our understanding of the associations end of the nineteenth century, however, the area between these two groups remains poor. was extensively cultivated, and vineyards oc- The main aim of our study was to test the cupied the belts of terraces built into the stony hypothesis that bird communities are structured slopes of the mountains. After the phylloxera by arthropod availability. If this is true, there crisis, most of the human population migrated should be an association between arthropod to nearby urban areas, although livestock and availability and bird numbers. Since succes- timber exploitation continued until the middle sional dynamics show a progressive increase in of the twentieth century. From then on, human the number of interactions between elements activity has sharply decreased, and fire has been of the ecosystem (Margalef 1968, Odum 1969), the main form of disturbance affecting the land- we hypothesized that the association between scape and habitats. A knowledge of this histori- arthropod availability and bird requirements is cal process is essential for understanding the greater in mature unburned areas than in re- current aspect of the Garraf massif. cently burned ones. Most studies conducted on The natural park has had two extensive fires the relationship between arthropods as a food in the last decades: the first burned 10,000 ha resource and birds have, in general, focused on in 1982; and the second, which burned the area one bird species. In contrast, our study attempts again in 1994, affected 5,000 ha. The periphery to consider the entire bird community feeding of the park, about 1,000 ha, has not been dam- on shrub invertebrates. aged by fire in recent years and consists mostly of pine woods grown since the end of the timber exploitation (40–50 years ago). Although Methods we could not directly reconstruct a succession from the synchronic study of these three adja- Study area and design cent zones (Prodon & Pons 1993), the histori- cal processes that occurred throughout the This study was carried out during the breeding whole massif (see above) and the similarity of and wintering seasons of 1998 in the Garraf climate, relief and plant species composition led Natural Park, situated 20 km south of the city us to assume that fire was the main factor of Barcelona (NE Iberian Peninsula). The study involved in the current physiognomy of each of area (41°15’N 1°55’E) consists of low hills and these zones. Other authors have used the syn-

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chronic approach to study successional post-fire to be not significant in 42 out of the 48 tests dynamics (e.g. Vicente 1991, Crête et al. 1995, carried out. Thus, we considered them as true Ding et al. 1997, Imbeau et al. 1999), and we replicates and used means between the two sam- think that our study area provided an appropri- ples for a given taxon as the most reliable indi- ate framework within which to study the rela- cator of its abundance in the given period. tionships between bird and arthropod abun- Samples were dried for 72 hours at 70°C, dance after fire. We established 18 randomly the numbers of individuals were counted, and placed survey zones: 6 within the habitat burned each sample was weighed. Next, we classified in 1982 (referred to as “F82”), 6 within the habi- arthropods to the taxonomic level of order. We tat burned in both 1982 and 1994 (“F94”), and then determined whether the different taxons 6 in the fire-free zone (”Control”). encountered had been detected in previous studies on shrubland bird diets. According to Arthropod sampling the feeding data compiled in Cramp (1988, 1992), Cramp & Perrins (1993) and Hódar We used sweep-net sampling to collect arthro- (1994), the bird species found in our study show pods from shrubs. This method is probably the a notable flexibility in diet depending on the most widely used for sampling arthropods from frequency of the different potential prey types vegetation, and it is especially suitable in eco- in the habitat. All the arthropod orders present systems where the plants of interest are small. on the studied shrubs occur in the diets of the Sweep-netting does not provide a measure of breeding birds found in the area, except absolute density; however, this is not needed Phasmida, which was very rare and accounted when examining the relationships between ar- for less than 0.01% of total arthropod biomass thropods and bird abundance (Cooper & in all zones. Although Wolda (1990) indicated Whitmore 1990). Arthropods are not expected that some arthropod species included in abun- to be uniformly distributed in plants, but, rather, dance estimates may not be potential prey for concentrated in the areas where leaves and birds because they are unpalatable or require branches are especially dense and with the high- excessive time or energy for capture, we assumed est physiological activity, that is, in the most that the total arthropod biomass of each sam- external layers of the shrubs. Hence, although ple could be considered a measure of resource the sampling device only allows surveying these availability for the whole insectivorous bird external layers, we think that the method could community inhabiting this zone. be appropriate for estimating overall arthropod abundance, independent of shrub size. Bird sampling Arthropods were collected in each of the 18 survey zones in a transect that involved beating The point-count method was used to assess the shrubs at intervals of 1 m during a route of 100 abundance of bird species (Bibby et al. 2000). m. Each transect was repeated twice (at inter- In each of the 18 survey zones, five point-count vals of at least 3 weeks) in both the breeding stations were randomly selected. The sampling and wintering seasons. We carried out a total of was carried out twice at each station during the 72 transects and thus obtained 72 samples. Each breeding season (March to June) of 1998 and sample was obtained in just 10–15 minutes to wintering season (November to January) of minimize the effects of temperature and weather 1998/99. Thus a total of 360 point-counts were changes within the sampling time. We assumed performed during the census period. that each arthropod sample was a reliable indi- Birds heard or seen were recorded, and the cator of the foliage arthropod community in the distance between the observer and the bird was survey zone. This assumption was supported by estimated. Following the recommendations of the fact that the transect was relatively long and Fuller & Langslow (1984), sampling time was designed to maximize spatial heterogeneity in 10 minutes. Bird counts were carried out dur- plant species composition and vegetation struc- ing the first three hours after sunrise, during ture. Finally, we analysed differences in arthro- maximum avian activity. Censuses were per- pod order abundance in each of the two sam- formed only in good weather conditions, with- ples in each season and habitat, and found them out heavy rainfall or strong wind (Bibby et al.

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2000). To calculate densities for each species, proposed by Nagy (1987); the FMRS for each we considered the maximum number of indi- species was calculated by multiplying its FMR viduals detected at either of the censuses con- by the proportion of food taken from shrubs. ducted at each station as the most reliable indi- The FMRS of a population was calculated by cator of abundance. We then used the method multiplying the FMRS of each species by its proposed by Reynolds et al. (1980) to estimate abundance and, finally, the overall FMRS of the bird density. bird community was calculated by adding to- We attempted to determine the kind of as- gether the FMRS of each bird species popula- sociation between the availability of arthropods tion inhabiting the study zone. from shrubs and the bird species that gleaned these invertebrates. Therefore, from the total Statistical Analysis bird species recorded in the census, only those that, according to literature and personal ob- We compared arthropod density, arthropod servations, gleaned arthropods from shrub sur- biomass, bird density, bird biomass and FMRS faces were considered. These were as follows: of the three zones studied by means of an Wren Troglodytes troglodytes; Stonechat Saxicola ANOVA. A Newman-Keuls test was used for torquatus; Dartford Warbler Sylvia undata; post hoc comparison. When data transforma- Sardinian Warbler Sylvia melanocephala; Black- tion did not meet the ANOVA assumptions, cap Sylvia atricapilla; Bonelli’s Warbler we used the Kruskal-Wallis test (Sokal & Rohlf Phylloscopus bonelli; Chiffchaff Phylloscopus 1995). A multiple comparison rank extension collybita; Goldcrest Regulus regulus; Firecrest of the Kruskal-Wallis for pairwise comparisons Regulus ignicapilla; Long-tailed Tit Aegithalos was performed (Siegel & Castellan 1988); since caudatus; and Great Tit Parus major. We made there were k = 3 groups, the level of signifi- notes of the feeding activities observed during cance was alfa’ = alfa/k(k-1) = 0.0083 (one- the fieldwork, and took into account the forag- sided Z distribution). For dependent samples, ing substrata reported by Cramp (1988, 1992) the t-test was used to analyse differences be- and Cramp & Perrins (1993) for these bird spe- tween the breeding and wintering season, but cies in Western Mediterranean shrublands and the non-parametric Wilcoxon matched pairs pine woods. The percentage of food taken from test was chosen when data transformations did shrubs by each species has been established as not meet the parametric assumptions (Sokal & follows; 100% for the Wren; 6% for the Stone- Rohlf 1995). Standard linear regression was used chat; 100% for the Dartford Warbler; 100% for to test the relationship between arthropod the Sardinian Warbler; 100% for the Blackcap; biomass and bird requirements (Sokal & Rohlf 10% for Bonelli’s Warbler; 50% for the 1995), and residual analysis was used to ana- Chiffchaff; 20% for the Goldcrest; 20% for the lyse differences in this relationship among the Firecrest; 40% for the Long-tailed Tit; and 60% three zones. The residuals obtained from this for the Great Tit. regression were used as an index of predation To obtain a reliable indicator of the food re- pressure, being negative when there were lower quirements of these birds, we calculated their FMRS than expected from the model and posi- field metabolic rate (FMR), a parameter that tive when they were greater. All statistical analy- shows the amount of food required per day by ses were run with Statistica Statsoft, Inc 1999. birds in a given area. Given our specific interest in the relationships between arthropod abundance in shrubs and the birds that feed on them, Results we calculated the field metabolic rate derived from foraging on shrubs (FMRS). Thus, the FMRS quantified the weight of food required Arthropod community per day by all birds that glean from shrubs in our study plots, and was expressed as g/day/10 Altogether 3,827 individual arthropods were ha. The field metabolic rate (FMR) of each bird collected from the shrubs. The most abundant species was estimated using the allometric re- orders were Araneida, Homoptera, Heteroptera, gression for passerine birds of appropriate size Diptera, Coleoptera and Hymenoptera; these

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Table 1. Shrubland arthropod community descriptors in the breeding and wintering seasons in the three zones. Values: Mean (standard error). We performed a multiple comparisons rank extension of the Kruskal- Wallis test for pairwise comparisons (Siegel & Castellan 1988). Significant differences are marked ***. Descriptors de la comunitat d’artròpodes dels arbustos en la estació reproductora i hivernant en les tres zones. Valors: Mitjana (error típic). Amb l’objectiu de comparar entre parelles es va dur a terme una extensió del test de rangs Kruskal-Wallis per a comparacions múltiples (Siegel & Castellan 1988). Les diferències significatives estan marcades amb el símbol ***.

Kruskal- F94 vs F94 vs F82 vs F94 F 82 Control Wallis P Cont. F82 Cont.

BREEDING SEASON Total individuals 43.50 (3.11) 83.33 (6.58) 128.41 (18.27) 12.78 <0.01 *** *** n.s. Biomass (mg/ transect) 61 (16) 127 (21) 120 (13) 6.89 <0.05 *** *** n.s.

WINTERING SEASON Total individuals 35.00 (9.47) 38.33 (7.75) 54.00 (6.92) 3.80 0.146 n.s. n.s. n.s. Biomasss (mg/ transect) 19 (8) 19 (6) 44 (19) 3.03 0.219 n.s. n.s. n.s.

had more similar relative frequencies in the than in the burned zones (Kruskal-Wallis test breeding season than in winter (Fig. 1). The H’ = 10.43, p<0.01, p<0.0083 for these pair- other orders found were Collembola, Orthop- wise comparisons); and Heteroptera individu- tera, Lepidoptera, Tysanoptera, Phasmida, als were less abundant in F94 than in F82 Psocoptera, Neuroptera, Acari and Opilionida, (Kruskal-Wallis test H’ = 8.74, p<0.05, which together accounted for less than 15% of p<0.0083 for pairwise comparison between F94 the total number of individuals. The abundance and F82). In the breeding season, the total of most of the orders did not show any signifi- number of individuals per transect and arthro- cant difference among the three zones in either pod biomass per transect were significantly breeding or wintering seasons. In the former, higher in the Control and F82 than in F94 (Ta- only Homoptera, Araneida and Heteroptera ble 1). In the wintering season there were even showed significant differences between study fewer significant differences: only Araneida zones: Homoptera numbers were lower in F94 showed the same pattern as in the breeding sea- than in the other habitats (Kruskal-Wallis test son (Kruskal-Wallis H’ = 11.46, p<0.01, H’ = 11.40, p<0.01, p<0.0083 for pairwise p<0.0083 for the two pairwise comparisons be- comparison with both, F82 and the Control); tween the Control and the burned zones). It is Araneida numbers were higher in the Control worth noting that the total number of individu-

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Fig. 1. Percentages of arthropod orders in each study zone in the breeding and wintering seasons. Percentatge de cada ordre d’artròpodes en cada zona d’estudi durant l’estació reproductora i nidificant.

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Fig. 2. Percentages of bird species in each study zone in the breeding and in wintering seasons. Numbers refer only to those species that feed on shrubs. Percentatge de cada espècie d’ocell en cada zona d’estudi durant l’estació reproductora i nidificant. Les xifres fan referència exclusivament a aquelles espècies que s’alimenten als arbusts.

als per transect and arthropod biomass did not Z = 2.20, p<0.05) and in arthropod biomass differ among zones during the winter (Table 1). (Wilcoxon test Z = 1.99, p<0.05; Fig.3). From the breeding to wintering seasons, F94 showed no significant differences in total indi- Bird community viduals (Wilcoxon test Z = 0.94, p = 0.345) or in arthropod biomass (Wilcoxon test Z = 178, We found that, in both the breeding and win- p = 0.074; Fig. 3); F82 showed a significant tering seasons, the shrubland bird communities decrease in total individuals (Wilcoxon test Z were always dominated by: Wren, Dartford = 2.20, p<0.05) and in arthropod biomass Warbler, Sardinian Warbler, Great Tit, Long- (Wilcoxon test Z = 2.20, p<0.05; Fig. 3). The tailed Tit, Stonechat and Firecrest. The two Control also showed a significant decrease in warblers accounted for more than 70% of the the number of total individuals (Wilcoxon test total individuals inhabiting the burned habitats,

Table 2. Shrubland bird community descriptors in the breeding and wintering seasons in the three zones. Values: Mean (standard error). We used the ANOVA and the Newman-Keuls test for pairwise comparisons. Variables were log-transformed in order to fit ANOVA assumptions. Significant differences are marked ***. Descriptors de la comunitat d’ocells dels arbustos en la estació reproductora i hivernant en les tres zones. Valors: Mitjana (error típic). Es va utilitzar l’ANOVA i el test de Newman-Keuls per fer comparacions entre parelles. Les variables es van transformar mitjançant logaritmes per acomplir les assumpcions de l’ANOVA. Les diferències significatives estan marcades amb el símbol ***.

F94 F82 Control F P F94 vs F94 vs F82 vs Cont. F82 Cont.

BREEDING SEASON Total density (ind/10ha) 8.83 (1.07) 24.69 (3.75) 28.42 (1.95) 17.32 <0.001 *** *** n.s. Total biomass (g/10ha) 99.5 (13.5) 274.3 (41.3) 303.3 (27.9) 13.63 <0.001 *** *** n.s. FMRS (g/day 10ha) 19.85 (2.36) 78.56 (10.78) 71.30 (7.52) 17.21 <0.001 *** *** n.s.

WINTERING SEASON Total density (ind/10ha) 39.54 (2.44) 47.00 (3.84) 55.87 (13.96) 0.95 0.408 n.s. n.s. n.s. Total biomass (g/10ha) 448.8 (29.1) 478.2 (24.0) 515.2 (107.2) 0.25 0.777 n.s. n.s. n.s. FMRS (g/day 10ha) 119.8 (7.9) 133.3 (7.0) 104.0 (14.7) 1.95 0.176 n.s. n.s. n.s.

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Fig. 3. Arthropod availability in the breeding and Fig. 4. Field metabolic rate deriving from foraging on wintering seasons in the three zones (n=18). Bars shrubs (FMRS) in the breeding and wintering seasons indicate standard error. in the three zones (n=18). Bars indicate standard error. Disponibilitat d’artròpodes en l’estació reproductora Taxa metabòlica derivada de l’alimentació en arbusts i hivernant en les tres zones (n=18). Les barres indi- (FMRS) durant l’estació reproductora i hivernant en les quen els errors típics. tres zones (n=18). Les barres indiquen els errors típics.

whereas in the Control, the bird species were was six-fold greater in winter than in the breed- more equally distributed (Fig. 2). In our study ing period (Fig. 4). area, Bonelli’s Warbler was only present in the breeding season, whereas the Blackcap, Chiff- Relationships between arthropod chaff and Goldcrest were only present in the availability and birds winter. The comparison of shrubland-bird-commu- In the breeding season, arthropod availability nity descriptors between zones differed depend- was positively correlated with the FMRS (r = ing on the season. During the breeding period, 0.548, p<0.05, n = 18; Fig. 5). In winter, ar- the F94 shrubland bird community had signifi- thropod availability was not correlated with the cantly fewer individuals and lower biomass and FMRS (r = 0.391, p = 0.109, n = 18). The re- FMRS than the shrubland bird communities of sidual analysis of the first of these regressions the other two zones. In contrast, during the wintering season, no significant differences were found between zones (Table 2). From the breeding season to the wintering season, F94 showed a significant increase in total shrubland bird density (t-test = -13.17, df = 5, p<0.001), total shrubland bird biomass (t-test = -12.62, df = 5, p<0.001) and in the FMRS (t-test = 12.53, df = 5, p<0.001; Fig 4). F82 presented significant differences in total bird density (t-test = -3.62, df = 5, p<0.05), total bird biomass (t-test = -3.45, df = 5, p<0.05) and in FMRS (t-test = -3.74, df = 5, p<0.05; Fig. 4). Finally, the Control did not show a significant increase in total shrubland bird density (t-test = -1.88, df = 5, p = 0.117), total shrubland bird biomass (t-test = -1.96, df = 5, p = 0.106) or in the FMRS (t-test = -2.39, df Fig. 5. Relationship between FMRS and arthropod = 5, p = 0.062; Fig. 4). Thus, seasonal varia- availability during the breeding season. tion in the FMRS was greater in F94, where it Relació entre FMRS i disponibilitat d’artròpodes durant l’estació reproductora.

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portion of early-successional insect species overwinter as immature individuals, which is an advantageous strategy because in the initial stages of succession the time for development is often limited by the death of herbaceous species. Therefore, the pattern observed in F94 may be related to the higher quantities of grasses observed there compared with the other two zones. In contrast to arthropods, birds were more abundant in winter than in the breeding season in all of the three zones. To explain the high abundance of wintering birds we should bear in mind that many European birds overwinter in coastal Mediterranean areas, such as the Garraf, Fig. 6. Predation pressure (estimated as the residuals of the linear regression) in the breeding season in where they feed basically on fleshy fruits the three zones. Bars indicate standard error. (Blondel & Aronson 1999). Large quantities of Pressió de depredació (estimada com el residual de fleshy fruits from shrubs such as Pistacia lentiscus, la regressió lineal) en l’estació reproductora en les Phillyrea latifolia and Olea europaea are available tres zones. Les barres indiquen els errors típics. during autumn and winter in the study area. In a study carried out in a similar Mediterranean showed significant differences between habitats plant community in southern Spain, Herrera (F = 3.84, df = 2,15, p<0.05). The average (1984) calculated an annual fruit biomass pro- residual score for F94, F82 and the Control was duction of 98 kg/ha, with a peak in December, used as an index of the predation pressure in when there were more than 100,000 fruits/ha. each zone. Thus, the Newman-Keuls post hoc He also suggested that the presence of a large multiple comparison showed that the index of number of passerines in winter is only possible predation pressure in the Control and in F82 in mild climates with an abundant supply of (which were 8.53 and 12.86 respectively) did energy-rich fruits. not significantly differ (p = 0.753), but the index of predation pressure in F94 (-21.4) differed Successional changes in arthropod and from both the index of predation pressure in F82 bird numbers (p<0.05) and in the Control (p<0.05) (Fig. 6). Our results showed that the relative abundance of arthropod orders varied among zones, although Discussion the most abundant groups were always Araneida, Homoptera, Diptera and Hymenoptera. These results are similar to those found by Pons (1998), Seasonal changes in arthropod and bird who reported Homoptera, Diptera and Hy- numbers menoptera to be the most abundant orders in burned and unburned Mediterranean shrublands In temperate areas, arthropod numbers usually of southern France. In both Pons’s study and ours, have a marked peak in spring and summer and the abundance of foliage arthropods was lower then decrease sharply in winter because the bio- in burned areas than in nearby unburned areas. logical cycles of these invertebrates are strongly This is a typical pattern in most ecosystems when affected by low temperatures and adverse they have recently been affected by fire, and it weather conditions (Berryman 1986). This may provides plants with a short-term release from explain why we detected a significant decrease insect herbivory (Swengel 2001). in arthropod biomass from breeding to winter- Our results showed that shrubland bird den- ing seasons in F82 and in the Control but, sur- sities were lower in the recently burned area prisingly, F94, the most recently burned zone, than in the other two zones during the breed- did not show significant differences between sea- ing season. In contrast with this, if we consider sons. Brown (1986) pointed out that a high pro- the whole bird community and not only that

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linked to shrubs, overall bird abundance did not biomass is greater than bird requirements soon differ between F94 and F82 (Herrando et al. after fire, thus suggesting that birds are not lim- 2002), thus indicating that the abundance of ited by arthropod availability. In such case, birds other species that do not feed on shrubs is par- could be limited by an alternative resource, such ticularly important in the recently burned area. as breeding sites. Pulido & Díaz (1997) found Interestingly, after a controlled fire in a Medi- that the abundance of Blue Tits Parus caeruleus terranean shrubland of southern France, Pons was not constrained by food resources, but by (1998) found that bird abundance did not fol- the availability of tree holes for nesting. In our low a decrease in shrub arthropod abundance study, the presence of this type of structural con- and suggested an increase in flying and terres- straint in F94 would be applicable for the scarce trial invertebrates which might enhance prey Great Tit, but even if this were the case (highly availability, thus contributing to maintaining improbable in a area with an abundance of holes bird densities. among the karstic rocks and walls of abandoned terraces), it is difficult to imagine this forest spe- Bird community and arthropod cies reaching high densities in a burned area. availability Nesting sites for the commonest cup-nesting species are generally presumed to be readily During the breeding season, we found a signifi- available (Wiens 1989) and therefore are likely cant positive association between the arthro- to be highly abundant in our study area, so pod availability from shrubs and the food re- would not limit bird numbers. Other types of quirements of the bird community that gleans potential resource, such as perches, roost loca- these invertebrates. In contrast, during the win- tions or cover from predators were not quanti- tering season, the use of fruits as a food resource fied in this work, but these structural compo- may explain the lack of correlation between bird nents of habitats have not been reported to date requirements and arthropod availability. An as constrictors of shrubland bird communities. association between bird requirements and ar- We suggest that the actual fire dynamics thropod availability is an expected prediction if could be responsible for the disassociation be- a bird community is constrained by food avail- tween bird requirements and arthropod availability (Martin 1987, Wiens 1989). Arthropod ability. Invertebrate life cycles are very short, and abundance is likely to limit bird density because their community characteristics and abundance during breeding individuals forage mostly on may recover sooner than for vertebrates such as these invertebrates for both their own suste- birds, whose responses may take longer. Typi- nance and that of their nestlings. Arthropod cally, bird predation on arthropods shows a availability sets an upper limit on bird abun- sigmoid-shaped curve, that is to say, there is a dance at equilibrium stages and does not allow slow initial response to increasing prey density, bird populations to grow beyond the carrying followed by increased predation until predation capacity of the system. In such conditions, other levels off (Kirk et al. 1996). In our study, during factors, such as competition between similar the first years after fire, the bird community does species for scarce resources, may contribute to not seem to be related to arthropod availability shaping community structure (Wiens 1989). (and predation pressure on the invertebrates is However, after a disturbance event, such as consequently lower), probably because of the a fire, both the bird and arthropod communi- distinct recovery speeds of these two groups. ties undergo a successional process that follows Pons & Prodon (1996) found that some bird vegetation recovery. The residual analysis species colonized a 140-ha burned area from showed that in F94, the most recently burned similar open areas nearby, while others showed zone, there were fewer birds than expected from marked site tenacity and managed to persist in the arthropod availability. In contrast, F82 spite of the drastic modification of the vegeta- (burned 16 years before the fieldwork) and the tion. However, neither of these responses may Control (not damaged by fire) showed the op- be enough to recover five thousand hectares of posite relationship, suggesting a closer depend- burned vegetation rapidly, and successive colo- ence of the bird community on arthropod avail- nization waves should be added to the juveniles ability. These results indicate that arthropod produced in the burned area. The sigmoid-

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shaped theoretical curve is consistent with the sionat per a Universitats i Recerca de la Generalitat increase in density, biomass and the FMRS af- de Catalunya. ter the first years of succession, and the stabiliza- tion of these numbers 16 years after fire (the Control and F82 did not differ in the values of Resum these parameters). Therefore the hypothesis that Dinàmica post-incendi en ambients bird communities are limited by arthropod avail- arbustius mediterranis: la disponibilitat ability seems to be only suitable for middle and d’artròpodes modela la comunitat later successional stages when the interactions d’ocells? between elements of the ecosystem are probably stronger than during initial stages after fire. Es va estudiar la relació entre la disponibilitat It is commonly assumed that early succes- d’artròpodes i els requeriments energètics dels ocells en una zona coberta de brolles, garrigues i màquies. sional habitats are variable in quality and that Específicament es va testar la hipòtesi que la disponi- resources are more patchily distributed than in bilitat d’aliment constituïa un possible limitant en later successional habitats (Helle & Mönkkönen la recuperació de la comunitat d’ocells dins la 1990). Thus, at initial successional stages birds dinàmica de recolonització post-incendi. Es va are often not yet fully adapted to the main fea- utilitzar un sistema de captura estandarditzat amb tures of the vegetation structure (Wiens 1989). salabres per recol·lectar artròpodes i estacions However, in a concurrent study in the same area puntuals per estimar l’abundància d’ocells. Els cen- (Herrando et al. 2003), we found that three years sos es van dur a terme durant la temporada de after fire, vegetation structure was already a re- nidificació i d’hivernada dels ocells en una zona que liable predictor of bird community. This pattern no havia estat afectada pel foc i en dues zones cremades (la primera incendiada 4 anys abans del has repeatedly been reported in several studies treball de camp i la segona 16 anys abans). Durant relating birds and vegetation structure after fire la temporada de nidificació vàrem trobar una in the Mediterranean Basin (Prodon et al. 1987, associació positiva entre la disponibilitat d’artròpodes Vicente 1991, García 1997). The high histori- i els requeriments energètics dels ocells a les tres cal occurrence of perturbations in Mediterra- zones. No obstant això, comparada amb les altres nean ecosystems may have led some species to dues, la zona afectada recentment pel foc contenia include early successional stages as favourable menys ocells que els esperables a partir de la seva habitats. The results of the present study may abundància d’artròpodes. D’aquesta manera sembla help to clarify the dynamics of Mediterranean que els ocells exercien una pressió de depredació bird communities after fire. Even when the bird menor sobre les poblacions d’artròpodes en aquesta zona que a les altres dues, les quals no diferien entre community is highly predictable from vegeta- si respecte a aquest paràmetre. Aquests resultats tion structure soon after fire, it does not seem suggereixen que la disponibilitat d’artròpodes no li- to be limited by food until later stages, when, in mita el nombre d’ocells reproductors pocs anys addition to habitat structure, food abundance després del foc, però sí que ho pot fer en estadis may set an upper limit to bird numbers. posteriors. A l’hivern, quan la comunitat d’ocells estudiada també s’alimenta de fruits, no es va trobar cap associació entre ocells i artròpodes. Acknowledgements

We thank David Requena and Rodrigo del Amo for Resumen their kind help with the fieldwork, Xavier Ruiz and Constantí Stefanescu for their assistance in the de- Dinámica post-incendio en ambientes sign of the arthropod sampling method, and espe- arbustivos mediterráneos: ¿la cially Roger Prodon and Pere Pons for their valuable disponibilidad de artrópodos modela la comments on a previous version of the manuscript. comunidad de aves? This study is part of the research carried out by the Grup de Recerca de Qualitat 1198 of the University Se estudió la relación entre la disponibilidad de ar- of Barcelona, which has financial support from the trópodos y los requerimientos energéticos de las aves project PB 96-0224 from the Ministerio de Educación en una zona cubierta de matorral mediterráneo. y Cultura. Sergi Herrando and Lluís Brotons received Específicamente se testó la hipótesis de que la dis- financial support (FI fellowship) from the Comis- ponibilidad de alimento constituía un posible factor limitante en la recuperación de la comunidad de aves

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dentro de la dinámica de recolonización post-incen- Cramp, S. 1992. The Birds of the Western Palearctic. dio. Utilizamos un sistema de captura estandarizado Vol VI. Oxford: Oxford University Press. con embudos entomológicos para recolectar artró- Cramp, S. & Perrins, C.M. 1993. The Birds of the Western Palearctic. Vol VII. Oxford: Oxford podos y estaciones puntuales para estimar la abun- University Press. dancia de las aves. Los censos se llevaron a cabo Crête, M., Drolet, B., Huot, J., Fortin, M.J. & durante la temporada de nidificación y de invernada Doucet, G.J. 1995. Post-fire stages of mammal de las aves en una zona que no había sido afectada and bird diversity in the north of Quebecois bo- por el fuego y en dos zonas quemadas (la primera real forest. Canadian Journal of Forest Research incendiada 4 años antes del trabajo de campo y la 25 (9): 1509–1518. Díaz, M. & Pulido, F.J. 1993. Relaciones entre la segunda 16 años antes). Durante la temporada de abundancia de artrópodos y la densidad de he- nidificación se encontró una asociación positiva en- rrerillo común Parus caeruleus en dehesas du- tre la disponibilidad de artrópodos y los requerimien- rante el periodo prereproductor. Ardeola 40 (1): tos energéticos de las aves en las tres zonas. No obs- 33–38. tante, comparada con las otras dos, la zona afectada Ding, T.S., Lee, P.F. & Lin, Y.S. 1997. Abundance and distribution of birds in four high elevation recientemente por el fuego contenía menos aves de plant communities in Yushan National Park, las esperables a partir de su abundancia de artrópo- Taiwan. Acta Zoologica Taiwanica 8 (1): 55–64. dos. De esta manera parece que las aves ejercían una Fuller, R.J. & Langslow, D.R. 1984. Estimating presión de depredación menor sobre las poblaciones numbers of birds by point counts: how long should de artrópodos en esta zona que en las otras dos, las counts last? Bird Study 31: 195–202. cuales no diferían entre sí respecto a este parámetro. García, J.A. 1997. Caracterización y uso del hábitat por la avifauna en los bosques quemados de la Estos resultados sugieren que la disponibilidad de provincia de León. PhD thesis. Universidad de artrópodos no limita el número de aves reproductoras León. pocos años después del fuego, pero sí que lo puede Helle, P. & Mökkönen, M. 1990. Forest successions hacer en estadios posteriores. En invierno, cuando and bird communities: theoretical aspects and la comunidad de aves estudiada también se alimen- practical implications. In Keast, A. (ed.). Biogeo- ta de frutos, no se encontró ninguna asociación en- graphy and ecology of forest bird communities. The Hague: SPB Academic Publishing. tre aves y artrópodos. Herrando, S., Brotons, L., del Amo, R. & Llacuna, S. 2002. Bird community succession after fire in a dry Mediterranean shrubland. Ardea 90 (2): 303–310. References Herrando, S., Brotons, L. & Llacuna, S. 2003. Does fire increase the spatial heterogeneity of bird Athias-Binche, F., Briard, J., Fons, R. & Sommer, communities in Mediterranean landscapes? Ibis F. 1987. Study of the ecological influence of fire 145: 307–317. on fauna in Mediterranean ecosystems (soil and Herrera, C.M. 1984. A study of avian frugivores, above ground layer). Patterns of post-fire reco- bird-dispersed plants, and their interaction in very. Ecología Mediterránea 13: 135–153. Mediterranean shrublands. Ecological Monographs Begon, M., Harper, J.L. & Townsend, C.R. 1987. 54 (1): 1–23. Ecology: individuals, populations and commu- Hódar, J.A. 1994. La alimentación de Sylvia undata nities. Oxford: Blackwell Scientific Publications. y Sylvia conspicillata en una zona semiárida del Berryman, A.A. 1986. Forest insects. Principles and sureste peninsular. Ardeola 41(1): 55–58. Practice of Population management. New York: Imbeau, L., Savard, J.P.L. & Gagnon, R. 1999. Plenum Press. Comparing bird assemblages in successional Bibby, J.C., Burgess, N.D., Hill, D.A. & Mustoe, spruce stands originating from fire and logging. S.H. 2000. Bird census techniques. London: Canadian Journal of Zoology 77: 1850–1860. Academic Press. Izhaki, I. & Adar, M. 1997. The effects of post-fire Blondel, J. & Aronson, J. 1999. Biology and wildlife management on bird community succession. of the Mediterranean region. Oxford: Oxford International Journal of Wildland Fire 7 (4): 335– University Press. 342. Brown, V.K. 1986. Life cycle strategies and plant Kirk, D.A., Evenden, M.D. & Mineau, P. 1996. Past succession. In Taylor, F. & Karban, R. (eds.). The and current attempts to evaluate the role of birds Evolution of Insect Life Cycles. Pp. 105–124. New as predators of insect pests in temperate York: Springer-Verlag. agriculture. Current Ornithology 13: 175–269. Broza, M. & Izhaki, I. 1997. Post-fire arthropod Lawrence, G.E. 1966. Ecology of vertebrate animals assemblages in Mediterranean forest soils in Is- in relation to chaparral fire in the Sierra Nevada rael. International Journal of Wildland Fire 7 (4): foothills. Ecology 47: 278–291. 317–325. Margalef, R. 1968. Perspectives in ecological theory. Cooper, R.J. & Whitmore, R.C. 1990. Arthropod Chicago: Chicago University Press. sampling methods in ornithology. Studies in Avian Martin, T. E. 1987. Food as a limit on breeding birds: Biology 13: 29–37. a life-history perspective. Annual Review of Cramp, S. 1988. The Birds of the Western Palearctic. Ecology and Systematics 18: 453–487. Vol V. Oxford: Oxford University Press.

03-Arthropods.p65 27 17/02/2006, 10:22 S. Herrando et al. Revista Catalana d’Ornitologia 21 (2005)

Morris, D.L., & Thompson, F.R. 1998. Effects of Reynolds, R.T., Scott, J.M., & Nussbaum, R.A. habitat and invertebrate density on abundance 1980. A variable circular-plot method for estimat- and foraging behaviour of Brown-headed Cow- ing bird numbers. Condor 82: 390–413. birds. Auk 115 (2): 376–385. Sgardelis, S.P., Pantis J.D., Argyropoulou, M.D. Nagy, K.A. 1987. Field metabolic rate and food & Stamou, G.P. 1995. Effect of fire on soil requirement scaling in mammals and birds. macroinvertebrates in a Mediterranean phryganic Ecological Monographs 57: 111–128. ecosystem. International Journal of Wildland Fire Newton, I. 1980. The role of food in limiting bird 5 (2): 113–121. numbers. Ardea 68: 11–30. Siegel, S. & Castellan, N.J. 1988. Nonparametric Odum, E.P. 1969. The strategy of ecosystem statistics. New York : McGraw-Hill. development. Science 164: 262–270. Sokal, R.R. & Rohlf, J. 1995. Biometry. New York: Pons, P. 1998. Bird site tenacity after prescribed Freeman. burning in a Mediterranean shrubland. In Trabaud, Stanton, P.A. 1986. Comparison of avian community L. (ed.). Fire Management and Landscape Eco- dynamics of burnt and unburnt coastal sage logy. Pp. 261–269. Montpellier: CNRS. scrub. Condor 88: 285–289. Pons, P. & Prodon, R. 1996. Short term temporal Swengel, A.B. 2001. A literature review of insect patterns in a Mediterranean shrubland bird com- responses to fire, compared to other conservation munity after fire. Acta Oecologica 17 (1): 29–41. managements of open habitat. Biodiversity and Prodon, R., Fons, R. & Peter, A.M. 1984. L’impact Conservation 10: 1141–1169. du feu sur la vegetation, les oiseaux et les Trabaud, L. 1981. Man and fire: impacts on Medi- micromamifères dans diverses formations des terranean vegetation. In di Castri, F., Goodall, Pyrénées-Orientales: premiers résultats. Rev. D.W. & Specht, R.T. (eds.). Mediterranean-type Eco. Terre Vie 39: 129-158. Shrublands. Pp. 523-537. Ecosystems of the Prodon, R., Fons, R. & Athias-Binche, F. 1987. World, 11. Amsterdam: Elsevier. The impact of fire on animal communities in the Vicente, A.M. 1991. Algunos aspectos sinecológicos Mediterranean area. In Trabaud, L. (ed.). The Role de los sistemas avifauna-vegetación. Caso de un of Fire on Ecological Systems. Pp. 121–157. The gradiente estructural simplificado. Orsis 6: 167– Hague: SPB Academic Publishing. 190. Prodon, R, & Pons, P. 1993. Postfire bird studies: Wiens, J.A. 1989. The Ecology of Bird Communities. methods, questions and perspectives. In Trabaud, Vols I, II. Cambridge: Cambridge University F. & Prodon, R. (eds.). Fire in Mediterranean Eco- Press. systems. Pp: 332–343. Ecosystems research Woinarski, J.C.Z. & Recher, H.F. 1997. Impact and report 5. Brussels: Commission of the European response: a review of the effects of fire on the communities. Australian avifauna. Pacific Conservation Biology Pulido, F.J., & Díaz, M. 1997. Linking individual 3 (3): 183–205. foraging behaviour and population spatial distri- Wolda, H. 1990. Food availability for an insectivore bution in patchy environments: a field example and how to measure it. Studies in Avian Biology with Mediterranean Blue Tits. Oecologia 111: 13: 38–43. 434–442.

03-Arthropods.p65 28 17/02/2006, 10:22