Abstract
Pollen from olive trees (Olea europaea L.) is one of the main airborne allergens of the Mediterranean region. We have performed a comparative analysis of the behaviour of Olea pollen in the atmosphere at different localities in southern Spain with different biogeographic and climatic characteristics. Sampling over several years with Burkard or Lanzoni volumetric collectors was performed in the four cities of Córdoba, Jaén, Málaga and Granada. The pollen season spans primarily April to June, with the heaviest concentrations in May and peak days registering: 3890 grains/m {\rm ^{3}} (Córdoba), 6730 grains/m {\rm ^{3}} (Jaén), 2819 grains/m {\rm ^{3}} (Málaga), and 1884 grains/m {\rm ^{3}} (Granada). These quantities make these cities prime centres of seasonal allergic rhinitis and bronchial asthma. The main pollen season was defined taking the days registering 95% of the total annual pollen, and by studying the fluctuations between years and seasons in terms of Olea pollen at the different sampling points. Correlation analysis showed that the pollen concentrations on the preceding days, as well as the average accumulated temperature, were the parameters that invariably had significant correlation indices at all sampling points. In addition, the forecast models indicated that these two variables, together with others, predicted a high percentage (up to 80% in Jaén) of the seasonality of this pollen observed in the atmosphere of the different localities studied.
Principal geographic, climatic, bioclimatic and biogeographic characteristics of the sampling sites.
Total annual data and principal characteristics of the MPS of Olea europaea pollen in the air of the sampling stations during the years studied.
Spearman's correlation coefficients between daily Olea europaea pollen during the MPS in Córdoba and other variables: a) pollen concentrations registered on previous days and b) the principal meteorological parameters.
Spearman's correlation coefficients between daily Olea europaea pollen during the MPS in Jaén and other variables: a) pollen concentrations registered on previous days and b) the principal meteorological parameters.
Spearman's correlation coefficients between daily Olea europaea pollen during the MPS in Málaga and other variables: a) pollen concentrations registered on previous days and b) the principal meteorological parameters.
Spearman's correlation coefficients between daily Olea europaea pollen during MPS in Granada and other variables: a) pollen concentrations registered on previous days and b) the principal meteorological parameters.
Forecast equation for each city formulated by linear step regression between the daily concentrations of Olea europaea pollen and the different factors studied.
Spearman's correlation coefficients and comparison of averages by the Wilcoxon test between daily Olea europaea pollen during the MPS of the year 2000 (observed) and data from the linear regression equation (expected).
The genus Olea L. is represented in the Mediterranean region by the single species Olea europaea L. and two varieties, var. sylvestris (wild olive), which forms part of the natural vegetation, and var. europaea, cultivated primarily for oil. Olive tree cultivation probably started about 5000 years ago in the eastern Mediterranean area and spread westwards, reaching the Iberian Peninsula. Today, Spain leads the world in olive production, some Andalusian provinces devote more than 60% of their total surface area to olive cultivation. In fact, the province of Jaén dedicates more than 90% of its surface area to this crop, becoming the zone with the highest production of olive oil in the world.
In southern Spain, olive pollen is the most abundant type within the annual pollen spectrum, so that the levels registered at certain times of year are extremely high, due both to the ubiquity of this crop as well as the intense flowering of the trees, which produce abundant pollen during springtime (Citation Citation Citation Citation Citation CitationGalán et al. Citation1988, Díaz de la Guardia et al. 1993, Recio et al. 1996, González Minero & Candau 1997, Ruiz et al. 1998, Alba et al. 2000, Fornaciari et al. 2000). This airborne pollen, provoking numerous cases of pollinosis among the population, has in recent years prompted a high number of studies throughout the Mediterranean (Citation Citation Citation Citation CitationBousquet et al. Citation1985, D'Amato & Lobefalo 1989, Negrini & Arobba 1992, Macchia et al. 1991, D'Amato & Liccardi 1994, Geller-Bernstein et al. 1996, Licardi et al. 1996). In southern Spain, olive pollen is the principal cause of seasonal allergic rhinitis and bronchial asthma, with high percentages of the population being allergic according to cutaneous tests: 46% in Málaga (Burgos Citation1991), 72% in Córdoba (Domínguez et al. Citation1993), 77% in Granada (Martínez Cañavate et al. Citation1995) and 89% in Jaén (Florido et al. Citation1999).
The areas surrounding the cities sampled () differ markedly in geographic characteristics. The city of Jaén is located in the Guadalquivir river valley, land occupied almost completely by olive cultivation and the abrupt Subbetic cordilleras with Mediterranean forest. Meanwhile, Córdoba is located in the cultivated plain of the Guadalquivir, bordered to the north by the Sierra Morena and to the south by the Campiña and the Subbetic sierras, which are dominated by olive orchards. The city of Málaga is situated on the shore of the Mediterranean Sea, on the alluvial plains of the Guadalhorce and Guadalmedina rivers and bordered by low mountains predominated by Mediterranean scrub and forest, beyond which lie vast tracts of olive orchards. The city of Granada is located in the fertile valley of the Genil river and is surrounded by the Betic, Penibetic and Subbetic mountains, characterized by abrupt cordilleras with degraded oak woodlands and large areas of olive cultivation, generally distributed over a broad altitudinal gradient.
Geographical location of the cities of Córdoba, Jaén, Málaga and Granada.
Biogeographically, all the cities belong to the corological province Betica, located in the different biogeographic sectors with appreciably different climates (). These characteristics influence both the type of natural vegetation near the collector as well as in the distribution and extent of the olive cultivation. Granada and Jaén are included in the Mesomediterranean (Ms) belt and have a continental Mediterranean and Mediterranean continental climate, respectively (Capel Citation1981), with Granada being in the province with the most accentuated continentality. Both Córdoba and Málaga belong to the Thermomediterranean (Tm) belt. However, whereas Córdoba, due to its inland location, has certain aspects of continentality (Mediterranean continental climate type), Málaga has a milder, coastal climate (Mediterranean subtropical climate type).
In the present work, after several years of airborne sampling, we present a comparative aerobiological study of the pollen of Olea europaea pollen from the southern Iberian Peninsula. We have developed forecast models for the seasonality of this pollen, to be used as a preventive measure against allergies in the populations of these cities, as well as similar geographical areas where a high number of the population are afflicted.
MATERIAL AND METHODS
This study was conducted in 4 localities of southern Spain. Three of the sampling stations included in this study (Córdoba, Málaga and Granada) have been operational since 1992, and Jaén since 1993. At all the sites, a volumetric Hirst-type spore-trap was used (Hirst, Citation1952). These traps were located on the roofs of the buildings, at 15–25 m above the ground level, ensuring free air circulation. Daily pollen counts were made using the methodology proposed by the REA (Spanish Aerobiology Network), (Domínguez et al. Citation1991) and the data are expressed as a number of pollen grains per cubic metre of air (grains/m {\rm ^{3}} ).
The main pollen season (MPS) was determined at 95%, following the methodology proposed by Nilsson & Persson (Citation1981). The most relevant data registered at the different sampling stations during the MPS, is shown in : the starting and ending date, the number of days with concentrations between 1 and 50 pollen grains/m {\rm ^{3}} , 51–100 pollen grains/m {\rm ^{3}} and higher than 100 pollen grains/m {\rm ^{3}} , the maximum daily concentration reached and the date on which it was recorded. The tables also include the annual absolute total values for olive pollen recorded in each of the cities. The average daily counts for all the years registered at each station is also shown.
The starting precept of this study is that the pollen data is a temporal series and that the different values reached by olive pollen may be determined by factors intrinsic and extrinsic to the series or else they are due to chance. In this light, we seek to ascertain the degree of association between various known factors and the pollen concentrations by means of Spearman's correlation test. This analysis was applied firstly with dephased values from the series of pollen values (pollen concentrations for 1 or 2 days before), and secondly with meteorological parameters which in turn were subdivided into two categories: a) daily observations (maximum, mean and minimum temperature, relative humidity, rainfall, frequency of the periods of calm and wind direction and velocity) and b) cumulative values (cumulative mean temperature and cumulative rainfall). These variables were calculated, accumulating the mean temperature and the daily precipitation from chilling (or the pre-seasonal cold period to each of the days that make up the pollen series of the MPS). According to Barceló Coll et al. (1987), the cold period of woody plants in the Mediterranean area lasts some 260–1000 hours after temperatures reach 0–5°C and it is essential for the floral buds to resume growth from accumulating warmth. This applies to Málaga from the second week in November (Recio et al. Citation1996), in Córdoba from mid-December to late January (Galán et al. Citation2000) and in Granada and Jaén from early January to the end of February.
To evaluate the parameters that form part of the mathematical model that enable the prediction of the olive-pollen concentrations, we used a multiple step regression, excluding the pollen data from the year 2000 in order to validate the forecast model using the data observed during that year. For this, we used a comparison of averages by the Wilcoxon test, which showed whether there were significant differences between the observed and the expected series. In addition, the Spearman's correlation test estimated the degree of association between these series.
RESULTS
The average of the daily production of olive pollen during the study period is shown in . At the four sampling locations, the pollen season spans basically April to the middle or end of June, and the greatest air concentrations occur in May. The annual total, as well as the MPS analysis are shown in . Although very high annual quantities of pollen were collected in all four cities, strong fluctuations appeared between years and sampling site, with the lowest quantity registered in Málaga (4167 pollen grains in 1995) and the highest in Jaén (67107 pollen grains in 1997). Similarly, the beginning and ending date of the MPS varied considerably, generally from April to June, or exceptionally, July. The peak day usually occurred in May.
Average daily concentration of Olea europaea pollen during the period analysed at each of the sampling stations.
The correlation analysis for each city and year is shown in . In general terms, the daily concentrations of olive pollen correlated significantly and positively with the pollen observations of the previous days, temperature and insolation. The cumulative temperature, the relative humidity, rainfall and cumulative rainfall generally had a significant and negative correlation. With respect to wind, the influence of air current on the levels of pollen varied over the years without a well-defined pattern of association in Córdoba, Jaén and Granada. On the contrary, the proximity of Málaga to the sea caused a negative correlation with the sea winds of the second quadrant (SE) and a positive correlation in the fourth quadrant (NW), where the olive orchards abound.
The forecast equations formulated for each of the cities are listed in . Although all the equations contain a considerable number of independent variables, the most parsimonious and the least complex, but with an appropriate r {\rm ^{2}} , were selected. The four mathematical models coincide on introducing, as independent variables into the first steps, the pollen observations of the preceding days followed by the variable cumulative temperature. The best results of r {\rm ^{2}} corresponded to Jaén. provides a graphic comparison of the results by means of a regression equation and the observed pollen data over the MPS of the year 2000 of each city. In addition, shows the results for the comparison of the averages between the observed and expected mean seasonal concentrations by comparing the two series. Only in the case of Málaga did the Wilcoxon test reveal significant differences.
Representation of the forecast models constructed using linear regression equations (expected) and data for pollen detected during the MPS of the year 2000 (observed) in each of the sampling stations.
DISCUSSION
Seasonal behaviour
The detailed study of the seasonal dynamics revealed that the first pollen grains were detected in March in the coastal zones of Málaga and that the last were registered during July in the highest zones of the province of Granada. The fact that the flowering of the olive tree begins so early in Málaga was observed by Recio et al. (Citation1996), suggesting also that Málaga might serve as an indicator to the onset of the pollination season in western Mediterranean area, at least in the southern Iberian Peninsula. For the same reason, the city of Granada, for its surrounding topographical characteristics, could be used to establish the end of the pollination of the olive in the southern Iberian Peninsula.
The evolution of the total annual counts reveals that in four of the cities studied, there were strong yearly fluctuations, alternating years having accentuated lows followed by high values (i.e. Málaga with 4558 grains in 1996 and 21625 grains in 1997). The highest annual concentration consistently occurred in Jaén (e.g. 67107 grains in 1997), the city with the highest mean values during the MPS, followed in descending order by Córdoba, Granada and Málaga (). The biennial pattern of pollen production reported by some researchers for tree species (CitationGalán et al. Citation1988, Emberlin et al. 1990) has been detected in this study, although quite irregularly. According to other authors (González Minero & Candau Citation1996), the pre-season rains play a major part in the annual production of olive pollen, so that when consecutive years register low rainfall, the reduction in the water reserves of the soil cause severe stress in the tree, leading to highly irregular cycles, as detected in the present study. Nevertheless, two general trends were identified in pollen production: firstly, a decline coinciding with dry period (years 1992–1995) and, secondly, an increase for years with a rainy pre-seasonal period (1997–2000).
The MPS occurred first in coastal areas of Málaga (first fortnight of April), followed by the Thermomediterranean areas of Córdoba (second fortnight of April) and, finally, in the zones with Mesomediterranean and more severe climate of Jaén and Granada (second fortnight of April-early May). This suggests that the olive tree needs a certain amount of heat to initiate the MPS, this occurring later in the coldest areas of Andalusia (Alba & Díaz de la Guardia Citation1998). Also, yearly differences have been found in the onset of the MPS in each city, which many authors (CitationFrenguelli et al. Citation1989, González Minero & Candau 1996) consider to be intimately related to the pre-seasonal climatic conditions, delays occurring when precipitation is registered prior to flowering, and earliness when the pre-seasonal temperatures are warmer. Although the date for the end of MPS varied considerably from one year to another (), it generally lasted until the end of May or beginning of June in the provinces of Málaga, Jaén and Córdoba, while in the province of Granada (with marked continentality and olive orchards distributed over a broad altitudinal gradient) it often lagged to the end of June and, exceptionally, to July.
In the four cities sampled, the duration of the MPS differed notably between years. In agreement with Keynan et al. (Citation1989), the duration of the MPS depends on the meteorological factors during pollen production, and thus when no rainfall is registered and temperatures rise, the MPS shortens (e.g. Córdoba 26 days during 1992). Nevertheless, abundant rainfall, by interrupting the emission of pollen and prolonging flowering, promotes longer pollination periods (e.g. Granada 79 days during 1993). The different ranges of concentrations in each sampling season per year indicate that as the MPS lengthened, the number of days with concentrations of less than 100 grains/m {\rm ^{3}} increased, and, on the contrary, when as the MPS shortened, the number of days with concentrations greater than 100 grains/m {\rm ^{3}} increased considerably, presenting short but intense MPS. In Jaén, this trend was evident, with practically no days having concentrations less than 100 grains/m {\rm ^{3}} , and in Córdoba the same was true, although not as marked. Meanwhile, in Málaga and Granada, characterized by fewer and longer periods of heavy pollen production, registered many days with concentrations of less than 50 grains/m {\rm ^{3}} .
The day of the maximum count usually occurred in May, although in Córdoba, Jaén and Málaga this sometimes came in April, while in Granada, this could lag until June (). Jaén registered the highest peak days, reaching 6730 grains/m {\rm ^{3}} in 1999 (May 14); Córdoba also reached high seasonal maximums, of up to 3890 grains/m {\rm ^{3}} in 1997 (May 1); Málaga and Granada were distinguished by reaching somewhat more moderate peak days.
Correlation analysis
The correlation analysis performed for each of the cities ( ) indicated that the evolution of the airborne pollen consisted of a series of consecutive observations that depended on one another and that proved closely related, so that the pollen quantity collected in one day was determined largely by the values registered on the preceding day. This was reflected in the significant correlation coefficients between the olive pollen concentrations and the concentrations on previous days. However, as shown by the analyses, the dispersion of olive pollen in the air depended not only on the intrinsic factors of the series but also extrinsic ones, such as meteorological variables. Our results coincide with those of numerous aerobiological studies demonstrating that climatic parameters related to warmth, such as temperature and insolation, generally increase the content of airborne olive pollen. These parameters act both on pollen emission by favouring dehydration and dehiscence of the anthers, as well as on dispersion by transporting the particles on thermal currents. On the contrary, humidity and rainfall usually correlated negatively with the amount of pollen in the air by provoking aggregation and deposition of pollen.
The cumulative temperature had a highly significant correlation with the pollen levels. This variable generally gave negative correlation coefficients, an effect due to the fact that, as the pollen values for the post-peak period declined, accumulated temperatures rose. Authors such as Recio et al. (Citation1996) have demonstrated that this variable is among the factors that most favour the level of olive pollen during the pre-peak period, the opposite effect resulting in the post-peak period. Many researchers express particular interest in this parameter, used widely to predict the onset of the MPS (CitationFrenguelli et al. Citation1989, Galán et al. 2000) as well as to construct forecast models on the daily evolution of olive pollen (Recio et al. Citation1997). Similarly, the accumulated precipitation showed significant negative coefficients during the MPS, this influence being positive both on pollen production as well as on the onset of the pollen season (Recio et al. Citation1996).
The relationship line wind - pollen dispersion is strongly heterogeneous ( ). We found no conclusive results on the effect caused by wind direction in the levels of olive pollen, as wind activity depended on many factors, including the wind regime characteristic of each province, the phenological state of the olive flowers during wind activity, the distribution of the crops and the topography near the sampling station (Alba et al. Citation2000). In general terms, the olive-pollen levels increased when the wind direction was favourable to the placement of the olive orchards (e.g. Málaga with winds of the fourth quadrant; ) and their phenological state was suitable and, on the contrary, diminished without wind (e.g. Málaga with winds of the second quadrant) or the phenological state was inappropriate. In Málaga and Granada, moderate wind velocity promoted the emission of pollen into the air and facilitated dispersion.
Forecast models and validation
The forecast models constructed for the daily evolution of Olea europaea pollen at the different sampling points indicate that both the pollen concentrations on the previous days, as well as cumulative temperature, were the most appropriate variables for predicting the variability of olive pollen in the air. This was reflected by the mathematical models of each of the four sampling stations. Nevertheless, other variables form part of the forecast equation of each station, indicating that these also affect the evolution of the pollen in the atmosphere (). In particular, the models developed for Córdoba and Málaga included up to 7 variables in the equation, Granada 6, and Jaén only 5 variables. In terms of seasonal dynamics of olive pollen, prediction proved only 40% accurate in Málaga, 48% in Córdoba and 65% in Granada. The mathematical model that offered the best results was that of Jaén, with 80% forecast power in the year 2000, the year for which the data was not included in the regression equation.
A graphic comparison of the results from the regression equation with the data throughout the MPS of the year 2000 at each station () revealed that the forecast data generally conformed well to the evolution of the pollen season, reflecting a seasonal dynamic similar to the observed one. Nevertheless, we should point out that the model did not offer good results in predicting the highest values. To solve this problem, some researchers, such as De Pablos Alcázar (Citation2001), delete the pollen data that deviate from the seasonal mean.
On comparing the two numerical series (observed and expected) by means of the Spearman's correlation (), we detected that in all sampling stations, there was a significant and positive correlation, confirming that these presented similar behavioural patterns. The result of comparing the averages for the observed and predicted mean seasonal concentrations () by the Wilcoxon test indicated no significant differences between the Córdoba, Jaén or Granada, verifying that the regression models used were valid for predicting pollen activity. However, for Málaga, significant differences were found, the mean and sum of the range observed data prevailing over the predicted, which finally led us to reject the regression model for this sampling station.
Acknowledgements
The authors wish to tank the Andalusian Regional Government (Departatment of Education and Science) and CICYT CO-ordinated I+D Project AMB97-0457-CO7-01-04 for financing this study.
Related Research Data
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