Romera et al. Botanical Studies 2013, 54:4 http://www.as-botanicalstudies.com/content/54/1/4 RESEARCH Open Access Reproductive phenology and pre-dispersal fruit predation in Atriplex halimus L. (Chenopodiaceae) Prado Romera1†, Francisca Fernández-Illescas1†, F Javier J Nieva1*, Pilar Rodríguez-Rubio2†, Enrique Sánchez-Gullón3† and Adolfo F Muñoz-Rodríguez1† Abstract Background: The flowering phenology pattern of Atriplex halimus was studied in a Mediterranean habitat in order to analyze protandry effectiveness. Fruit set evolution was recorded over two years and the impact of pre-dispersal predation by insects was also evaluated. Results: The flowering phenology coincided in 2006 and 2007, starting in mid-July and reaching full flowering at the end of August in both years. Inflorescences are composed of glomerules with 8.78 ± 2.79 male flowers and 4.57 ± 2.58 female flowers, with no significant differences in position on the inflorescence. The peaks of male and female flower anthesis were reached in mid-August, but the male maximum occurred one week before the female. Plants at the start of flowering only bear male flowers, but female flowers soon appear. Fruit set starts at the end of August; all the flowers were transformed into fruit by mid-September and their development continued to the beginning of October, when fruit structures had matured and began to drop. Fruit predation started at the end of September and reached maximum intensity in mid-October. Conclusions: At population level, male and female flowers seemed to open in the same weeks, but at plant and glomerule level male flowers opened one week before the females. Fruit predation levels were 62.42 and 43.14% in 2006 and 2007 respectively, with no significant differences between different parts of the inflorescence. And larvae of Coleophoridae were the most abundant predators. Keywords: Atriplex halimus; Flowers; Fruit predation; Insects; Phenology Background Atriplex halimus is a monoecious scrub that produces Atriplex shrub species, known as saltbushes, inhabit arid staminate flowers, with a whorl of 5 green sepals and 5 regions and are frequently found in saline soils stamens, and female flowers with a single carpel (McArthur and Sanderson 1984; Cañadas et al. 2010). enclosed within two opposite bracts which develop into Atriplex halimus L. is a Mediterranean and Macronesian dry fruit (achenes) surrounded by 2 valves, giving rise to scrub that grows in dry saline soils, and is a characte- a fruit structure that disperses as a unit. (Talamali et al. ristic species of halo-nitrophilous vegetation (Pegano- 2001,2003) studied floral polymorphism in the flowers of Salsoletea). It is planted extensively in these areas for this species, observing other types sporadically including ornamental purposes and as a fodder shrub due to its hermaphrodite flowers. Male and female flowers are set tolerance of drought and salinity; it plays an important in glomerules formed by the concrescence of several role in the rehabilitation of degraded zones (Le Houerou dichasial cymes deployed along the axis of the branched 1992; Kinet et al. 1998; Le Houerou 2000; Papanastasis inflorescence. Female flowers mainly develop in the et al. 2008) and has improved the quality of pastures in proximal part and male flowers in the distal part of each arid zones (Osman et al. 2006). glomerule (Talamali et al. 2001), and the sex ratio is affected by day length and light intensity (Talamali et al. 2003). * Correspondence: [email protected] As a rule, in the Chenopodiaceae family plants are pre- † Equal contributors dominantly wind-pollinated (Blackwell and Powell 1981) 1Departamento de Biología Ambiental y Salud Pública, Facultad de Ciencias Experimentales, Campus de El Carmen, 21071-Huelva, Spain and there is no evidence of self-incompatibility (Heyligers Full list of author information is available at the end of the article 2001). Some studies have focused on the phenology of this © 2013 Romera et al.; licensee Springer. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Romera et al. Botanical Studies 2013, 54:4 Page 2 of 10 http://www.as-botanicalstudies.com/content/54/1/4 species in different areas (Talamali et al. 2003), and one the Moguer Meteorological Station, 12 km from the lo- describes protandry (Abbad and Benchaabane 2004) cation (Rivas-Martínez and Rivas-Sáenz 1996–2009) which is consistent with the high levels of outcrossing (Figure 1). The study was carried out during 2006 and found in this species (Haddioui and Baaziz 2001; Ferchichi 2007, in which the annual temperatures were 17.0 and et al. 2006). 16.3°C, and annual rainfall was 663.2 and 366.8 mm, re- In this study we examine the flowering phenology pat- spectively (Figure 1). tern of A. halimus in a Mediterranean habitat, determin- For population phenology, ten plants randomly distrib- ing male and female flower development on three levels uted among the Atriplex population were marked at the (population, plant and glomerule) in order to analyze beginning of 2006 and evaluated weekly to determine protandry effectiveness. flowering stage on a scale of zero to ten that measured The rates of fruit and seed predation are important pa- the proportion of inflorescences with open flowers. Ten rameters of the population dynamic of plants. However, inflorescences from different plants were picked ran- there is a lack of information on fructification and seed domly each week for laboratory analysis with loupe or predation despite their importance as factors for the microscope magnification. Three glomerules were ran- population dynamic of A. halimus. In this study fruit set domly selected from each inflorescence, one from the evolution was recorded over two years and the impact of upper, middle and lower parts, and analyzed independ- pre-dispersal predation by insects was also evaluated. ently to estimate the number of male and female flowers, and the evolution of fructification and predation. Materials and methods Male flower phenology was studied in 2007 by Atriplex halimus plants were studied in a single popula- counting the number of male flowers in each glomerule tion at the “Marismas del Odiel” Natural Park in Huelva which marked three different developmental stages of (SW Spain). This population grows on a saline soil is- the flower: B) male flower bud differentiated, A) male land surrounded by a tidal marsh in a virtually monospe- flower at anthesis liberating pollen, and S) senescent cific shrub community (37°13’53”N 6°57’50”W). See male flowers. As male flower bud differentiation occurs Fernández-Illescas et al. (2010) for cover values. This lo- sequentially, and the male flowers fall from the glomer- cation has a typical Mediterranean climate with an aver- ule and disappear after flower senescence, we estimated age annual temperature of 18.0°C and an average annual the average number of male flowers per glomerule by rainfall of 460.9 mm, calculated from data recorded at calculating the arithmetic mean for the two weeks when Figure 1 Mean values of monthly temperature and precipitation for Moguer, and average monthly temperature and rainfall in 2006 and 2007. Data recorded at the Moguer Meteorological Station. Romera et al. Botanical Studies 2013, 54:4 Page 3 of 10 http://www.as-botanicalstudies.com/content/54/1/4 male flowering peaked (7 and 14 August 2007). The the inflorescence, only values above 0% were used in average values for different levels of inflorescence were analysis. also calculated. Data normality was checked by using the Kolmogorov- Female flower phenology and fruit evolution were Smirnov test. Statistical analysis was done via the studied in 2006 and 2007 by counting the number of fe- ANOVA one-way analysis of variance (when data were male flowers in each glomerule, which yielded three dif- normally distributed) or by a non-parametric test ferent developmental stages of the flower: B) female (Kruskal-Wallis) if not. flower bud differentiated, A) female flower at anthesis protruding stigmas from the flower bracts, and F) Results fruiting female flower, showing prominent bract develop- The flowering phenology pattern in the A. halimus ment. No senescent female flower was recorded as all population in 2006 and 2007 was similar (Figure 2) with the flowers observed had initiated fruit development. the start and full flowering dates virtually coinciding, 17 Once all female flowers are differentiated, and there is July and 21 August respectively; 2006 weekly values were no flower drop, we assume that their numbers will re- higher, which could mean flowering started a little earl- main stable until the onset of flower drop, with possible ier than in 2007. record variations due to sampling. In order to establish The weekly evolution of male and female flowers per an approximate level of female flowers per glomerule, glomerules and their ontogenic phases are shown separ- we considered the week in both years when flowering ately (Figure 3). Male flower buds were differentiated in peaked (28 August 2006 and 18 September 2007) to- mid-July 2007; the first flowers opened in early August gether with the week before and after. The global mean and by 28 August most of the male flowers were senes- values for different levels of the inflorescence were cent. All had fallen from the glomerule by 1 October. calculated. Male flowers reached the peak of anthesis on 14 and 21 Each week the number of male flower per glomerule August that year, with a global mean of 8.78 ± 2.79 at each stage was calculated with the percentage of flowers per glomerules. By position on the inflorescence, plants and glomerules with only male flowers opened, the means were 9.95 ± 4.45, 8.50 ± 2.69 and 7.90 ± 2.43 with only female flowers opened, with both types for upper, medium and lower parts respectively, with no opened, and with no flower opened.