Aromatic plants in Eurasian Blue Tit nests: the 'Nest Protection Hypothesis' revisited.
|Abstract:||The 'Nest Protection Hypothesis' suggests that some birds add aromatic plants to their nests to repel or kill ectoparasites. This behavior has been described for several species, including the Eurasian Blue Tit (Cyanistes caeruleus). We studied the reproductive performance, based on 26 nests (in nest boxes), of this species in mixed forested areas of Quercus spp. and Pinus pinea in the Parque Florestal de Monsanto, the largest park of Lisbon, Portugal. The frequency of aromatic plants in nests was compared with frequency of these plants in the study area. The three most frequent aromatic plants (Dittrichia viscosa, Lavandula dentata, Calamintha baetica) in nests were used more than expected from their availability in the study area. We could not reject the null hypothesis that nest survival rate is independent of the presence of aromatic plants in the nest.|
Agricultural chemicals industry
(Protection and preservation)
Chemical plants (Protection and preservation)
Pires, Barbara A.
Belo, Anabela F.
Rabaca, Joao E.
|Publication:||Name: The Wilson Journal of Ornithology Publisher: Wilson Ornithological Society Audience: Academic Format: Magazine/Journal Subject: Biological sciences Copyright: COPYRIGHT 2012 Wilson Ornithological Society ISSN: 1559-4491|
|Issue:||Date: March, 2012 Source Volume: 124 Source Issue: 1|
|Product:||Product Code: 2870000 Agricultural Chemicals NAICS Code: 3253 Pesticide, Fertilizer, and Other Agricultural Chemical Manufacturing SIC Code: 2873 Nitrogenous fertilizers; 2874 Phosphatic fertilizer industry; 2879 Agricultural chemicals, not elsewhere classified|
|Organization:||Company Name: Monsanto Co. Ticker Symbol: MON|
|Geographic:||Geographic Scope: Portugal; United States Geographic Code: 4EUPR Portugal|
Some birds use fragments of fresh plants in their nests different
from those used in nest cup construction. For example, raptors include
fragments of resinous conifers (Dykstra et al. 2009) in their nests and
passerines use herbaceous and shrubby species (Wimberger 1984,
Lambrechts and Dos Santos 2000). These fragments are incorporated into
the nest cup (Ontiveros et al. 2007) and several hypotheses have been
presented to explain this behavior (e.g., Banbura et al. 1995, Gwinner
and Berger 2006, Mennerat et al. 2009b). The 'Nest Protection
Hypothesis' (NPH) seems to be the most plausible explanation for
this behavior when the green material is aromatic. This hypothesis
suggests that sprigs of aromatic plants are added to nests because of
the presence of volatile secondary chemical compounds (e.g., Wimberger
1984), namely terpenes (Camacho et al. 2000), to reduce ectoparasite
loads. Clark and Mason (1988) explained that volatile compounds can
affect ectoparasite feeding, even if numbers of ectoparasites in nests
do not decrease with presence of aromatic plants.
The NPH should be more relevant for holenesting birds which may reuse the same cavity for several breeding attempts, thus increasing the probability of detrimental ectoparasite attacks. This trait has been documented for European Starlings (Sturnus vulgaris) (e.g., Gwinner and Berger 2005) and Eurasian Blue Tits (Cyanistes caeruleus) (e.g., Lambrechts and Dos Santos 2000, Mennerat et al. 2009b). Female Eurasian Blue Tits, a few days before egg laying, start to add fresh aromatic plant material to their nest (Mennerat et al. 2009a) and continue this behavior throughout the reproductive cycle (Lambrechts and Dos Santos 2000).
Our objective was to examine if Eurasian Blue Tits nesting in nest boxes use aromatic plants in their nests more than would be expected according to availability of these plants in the study area and, if so, which species are used. An additional objective can be established if aromatic plants are better represented in nests than predicted, indicating a selective plant search: does the presence of aromatic plants in the nests influence Eurasian Blue Tit nest survival rate?
Study Area.--The study was conducted in Parque Florestal de Monsanto, Lisbon, Portugal, the largest park in the city with ~900 ha. The park has extensive forested areas dominated by Quercus spp. (Q. robur, Q. suber, Q. coccifera, Q. rotundifolia, Q. faginea, and Q. pyrenaica), Pinus pinea, P. halepensis, and Eucalyptus globulus. Four Quercus spp. and Pinus pinea mixed stands of ~8 ha each were selected as study sites. We placed 484 (121/stand) pine wood nest boxes (chamber size: internal height X width X depth = 17 X 10.5 X 13.5 cm; entrance hole diameter = 3.5 cm) attached to a branch with a hook or wire away from hard substrate, 3 to 6 m above the ground and oriented south or east to avoid the dominant moderate-strong winds from north and west (e.g., Lambrechts et al. 2010). Nest boxes were equally spaced from each other in a grid arrangement of 25 X 25 m (1 nest box/25 X 25 [m.sup.2]). Nest boxes could not be placed at a few points due to site constraints (lack of trees, ponds, etc.).
Eurasian Blue Tit Breeding Performance.--Fifty nest boxes were randomly selected in each stand in the 2009 breeding season. We searched for reproductive events of cavity nesting birds and monitored the breeding performance of Eurasian Blue Tits. All occupied nest boxes were checked weekly from 1 March to 3 July to ascertain: (1) clutch size, (2) hatching rate (percent of eggs incubated to term that hatched), (3) nest survival rate (percent of fledglings per number of hatched eggs), and (4) breeding success (percent of fledglings per clutch). All nests were removed at the end of the breeding season, individually sealed in plastic bags, and analyzed in the laboratory.
Aromatic Plants Available in Study Area and Nests.--We considered aromatic plants to be all those with an obvious odor, i.e., those rich in volatile compounds (Clark and Mason 1985, Gwinner 1997). The presence of these plants was assessed by conducting line transects along the E-W line of the nest box grids. Plants visible on each side of the transect line were recorded in 140 consecutive sample units of 50 X 50 m. Aromatic plant fragments in the nests were identified through morphological features or scent.
Statistical Analyses.--We used Wilson's 95% Confidence Interval (CI) (following Newcombe 1998) to compare use of aromatic plant species in nests with their availability in the study area. Similarly to Dykstra et al. (2009), we considered that an aromatic species was used more or less than expected if the proportion of sample units containing that species was respectively below or above the 95% CI for the proportion of nests using that same aromatic species. We used [chi square] with contingency tables to test the null hypothesis ([H.sub.o]) that nest survival rate is independent of the presence of aromatic plants in the nest.
We found 26 (34.2%) Eurasian Blue Tit nests in 76 nest boxes with confirmed breeding attempts of cavity nesting species (Table 1).
Aromatic Plants in the Study Area and Nests.--Twelve aromatic plant species were detected on line transects; two others were recorded only in nest contents (Table 2). Another 10 aromatic plants were identified in the study area (Achillea ageratum, Eucalyptus camaldulensis, Juniperus oxycedrus, Lavandula pedunculata, Myrtus communis, Phagnalon saxatile, Pinus halepensis, P. pinea, Rum chalepensis, Thymus sp.). All taxa are autochthonous from the Mediterranean Region except for Eucalyptus camaldulensis. Fragments from aromatic plants in nests represented a small part of the nest material and were placed in the nest cup between other materials (BAP, pers. obs.). We recorded fragments from one herbaceous and seven aromatic shrubby species in 16 of the 26 analyzed nests. The average [+ or -] SE number of aromatic plant species per nest was 0.96 [+ or -] 0.39.
Use vs. Availability.--Wilson's 95% CI assessment indicated that Dittrichia viscosa, Lavandula dentata, and Calamintha baetica were the most frequent aromatic plants identified in nest material and were used by Eurasian Blue Tits more than expected according to availability in the study area (Table 2). Some aromatic fragments recorded in nests were from plant species not detected on transects (Lavandula dentata and Mentha spp.).
Aromatic Plants and Nest Survival Rate of Eurasian Blue Tits.--We detected predation of nestlings in five nests and excluded them from this analysis. We grouped survival rates (SR) from the 21 remaining nests into three classes: SR < 50%, 50% [less than or equal to] SR < 75%, and SR [greater than or equal to] 75%, and tested the null hypothesis that nest survival rate was independent of the presence of aromatic plants in the nest. Use of [chi sqaure] with contingency tables did not allow us to reject [H.sub.o] ([chi square] = 2.87, df = 1, critical value = 3.84, [alpha] = 0.05).
Aromatic species in Eurasian Blue Tit nests were a small proportion of all scented plants in the study area, suggesting non-random use of those species (e.g., Petit et al. 2002, Mennerat et al. 2009b). Mennerat et al. (2009a) found that choice of aromatic plants in nests was related to individual female preferences repeatable both within and across years. The major use of the three aromatic shrubby species most frequently detected in nests (D. viscosa, L. dentata, and C. baetica) suggests Eurasian Blue Tits actively search for plants that give them protection, as demonstrated by Lambrechts and Dos Santos (2000). This major use may be explained by the richness of terpenes with insecticidal properties: D. viscosa has in its chemical composition sesquiterpenes and monoterpenes working as insecticides, bactericides, and fungicides (Ibrahim et al. 2001, Blanc et al. 2006, Mamoci et al. 2011); C. baetica extracts and essential oils have showed positive effects against bacteria, fungi, and insects that affect stocked cereals and seeds (Matos 2011); L. dentata has an intense fragrance produced by oils rich in beta-pinene (Bousmaha et al. 2005), a chemical compound known as a potent insect repellent (Freeman and Beattie 20O8).
Our observations of nest composition and structure indicate dried needles of P. pinea were used as a building material. However, a second function of pine needles as aromatic fragments cannot be ignored due to the richness of Pinus spp. in terpenes. Macchioni et al. (2002) found that 58.9 to 62.5% of the essential oils of needles, branches, and cones of P. pinea are limonene, a compound known to decrease malaria parasite progression (Moura et al. 2001), and to reduce fleas and ticks on domestic animals (Hinkle 2010). We could not reject the null hypothesis that nest survival rate was independent of the presence of aromatic plants in the nest. This may be due to: (1) the small sample size of nests, and (2) because, ultimately, nearly all nests contained fragments of aromatic plants considering the presence of pine needles in 25 of the 26 nests.
We thank Rita S. C. A. Moreira and the Lisbon City Hall for field support and facilities. We are grateful to Adele Mennerat and an anonymous referee for helpful comments improving an earlier version of the manuscript.
Received 17 June 2011. Accepted 17 September 2011.
BANBURA, J., J. BLONDEL, H. WILDE-LAMBRECHTS, AND P. PERRET. 1995. Why do female Blue Tits (Parus caeruleus) bring fresh plants to their nests? Journal of Ornithology 136:217-221.
BLANC, M.-C., P. BRADESI, M. J. GONCALVES, L. SALGUEIRO, AND J. CASANOVA. 2006. Essential oil of Dittrichia viscosa ssp. viscosa: analysis by 13C-NMR and antimicrobial activity. Flavour and Fragrance Journal 21:324-332.
BOUSMAHA, L., F. A. BEKKARA, F. TOMI, AND J. CASANOVA. 2005. Advances in the chemical composition of Lavandula dentata L. essential oil from Algeria. Journal of Essential Oil Research 17:292-295.
CAMACHO, A., A. FERNANDEZ, C. FERNANDEZ, J. ALTAREJOS, AND R. LAURENT. 2000. Composition of the essential oil of Dittrichia viscosa (L.). W. Greuter. Rivista Italiana EPPOS 29:3-8.
CLARK, L. AND J. R. MASON. 1985. Use of nest material as insecticidal and anti-pathogenic agents by the European Starling. Oecologia 67:169-176.
CLARK, L. AND J. R. MASON. 1988. Effect of biological active plants used as nest material and the derived benefit to starling nestlings. Oecologia 77:174-180.
DYKSTRA, C., J. HAYS, AND M. SIMON. 2009. Selection of fresh vegetation for nest lining by Red-shouldered Hawks. Wilson Journal of Ornithology 121:208-211.
FREEMAN, B. C. AND G. A. BEATTIE. 2008. An overview of plant defenses against pathogens and herbivores. The plant health instructor. Iowa State University, Ames, USA. http://www.apsnet.org/edcenter/intropp/topics/ Pages/OverviewOfPlantDiseases.aspx
GWINNER, H. 1997. The function of green plants in nests of European Starlings Sturnus vulgaris. Behaviour 134: 337-351.
GWINNER, H. AND S. BERGER. 2005. European Starlings: nestling condition, parasites and green nest material during the breeding season. International Journal of Ornithology 146:365-371.
GWINNER, H. AND S. BERGER. 2006. Parasite defence in birds: the role of volatiles. Acta Zoologica Sinica 52:280-283.
HINKLE, N. 2010. Animals: pets (companion animals) external parasite control. Georgia pest management handbook. College of Agricultural and Environmental Sciences, University of Georgia, Athens, USA. http://www.ent.uga.edu/pmh/
IBRAHIM, M., P. KAINULAINEN, A. AFLATUNI, K. TIILIKKALA, AND J. HOLOPAINEN. 2001. Insecticidal, repellent, antimicrobial activity and phytotoxicity of essential oils: with special reference to limonene and its suitability for control of insect pests. Agricultural and Food Science in Finland 10:243-259.
LAMBRECHTS, M. M. AND A. DOS SANTOS. 2000. Aromatic herbs in Corsican Blue Tit nests: the 'Potpourri' hypothesis. Acta Oecologica 21:175-178.
LAMBRECHTS, M. M., F. ADRIAENSEN, D. R. ARDIA, A. V. ARTEMYEV, F. ATIENZAR, J. BANBURA, E. BARBA, J.-C. BOUVIER, J. CAMPRODON, C. B. COOPER, R. D. DAWSON, M. EENS, T. EEVA, B. FAIVRE, L. Z. GARAMSZEGI, A. E. GOODENOUGH, A. G. GOSLER, A. GREGOIRE, S. C. GRIFFITH, L. GUSTAFSSON, L. S. JOHNSON, W. KANIA, O. KELPS, P. E. LLAMBIAS, M. C. MAINWARING, R. MAND, B. MASSA, T. D. MAZGAJSKI, A. P. MOLLER, J. MORENO, B. NAEF-DAENZER, J.-A. NILSSON, A. C. NORTE, M. ORELL, K. A. OTTER, CH. R. PARK, CH. M. PERR1NS, J. PINOWSKI, J. PORKERT, J. POTTI, V. REMES, H. RICHNER, S. RYTKONEN, M.-T. SHIAO, B. SILVERIN, T. SLAGSVOLD, H. G. SMITH, A. SORACE, M. J. STENNING, I. STEWART, CH. F. THOMPSON, J. TOROK, P. TRYJANOWSKI, A. J. VAN NOORDWIJK, D. W. WINKLER, AND N. Z1ANE. 2010. The design of artificial nestboxes for the study of secondary hole-nesting birds: a review of methodological inconsistencies and potential biases. Acta Ornithologica 45:1-26.
MACCHIONI, F., P. L. CIONI, G. FLAMIN1, I. MORELLI, S. MACCIONI, AND M. ANSALDI. 2002. Chemical composition of essential oils from needles, branches and cones of Pinus pinea, P. halepensis, P. pinaster and P. nigra from central Italy. Flavour and Fragrance Journal 18:139-143.
MAMOCI, E., I. CAVOSKI, V. SIMEONE, D. MONDELLI, L. ALBITAR, AND P. CABONI. 2011. Chemical composition and in vitro activity of plant extracts from Ferula communis and Dittrichia viscosa against postharvest fungi. Molecules 16:2609-2625.
MATOS, O. 2011. The use of plants to fight toxin producers' pests and microorganisms that cause diseases in animals and humans via food (in Portuguese). Page 7 in I Garcia de Orta Conference--Medicinal plants. Institute of Hygiene and Tropical Medicine, Lisbon, Portugal.
MENNERAT, A., P. PERRET, AND M. M. LAMBRECHTS. 2009a. Local individual preferences for nest materials in a passerine bird. PLoS ONE 4(4):e5104. DOI:10.1371/ journal.pone.0005104
MENNERAT, A., P. PERRET, P. BOURGAULT, J. BLONDEL, O. GIMENEZ, D. W. THOMAS, P. HEEB, AND M. M. LAMBRECHTS. 2009b. Aromatic plants in nests of Blue Tits: positive effects on nestlings. Animal Behaviour 77:569-574.
MOURA, I., G. WUNDERLICH, M. UHR1G, A. COUTO, V. PERES, A. KATZIN, AND E. KIMURA. 2001. Limonene arrests parasite development and inhibits isoprenylation of proteins in Plasmodium falciparum. Antimicrobial Agents and Chemotherapy 45:2553-2558.
NEWCOMBE, R. G. 1998. Two-sided confidence intervals for the single proportion: comparison of seven methods. Statistics Medicine 17:857-872.
ONTIVEROS, D., J. CARO, AND J. M. PLEGUEZUELOS. 2007. Green plant material versus ectoparasites in nests of Bonelli's Eagle. Journal of Zoology 27:99-104.
PETIT, C., M. HOSSAERT-MCKEY, P. PERRET, J. BLONDEL, AND M. M. LAMBRECHTS. 2002. Blue Tits use selected plants and olfaction to maintain an aromatic environment for nestlings. Ecology Letters 5:585-589.
WIMBERGER, P. H. 1984. The use of green plant material in bird nests to avoid ectoparasites. Auk 10:615-618.
Barbara A. Pires, (1) Anabela F. Belo, (2,4) and Joao E. Rabaca (3,4,5)
(1) Avenida 5 de Outubro, 267 2Dto 1600-035 Lisboa, Portugal.
(2) Laboratory of Botany, Department of Biology, University of Evora, 7002-554 Evora, Portugal.
(3) Laboratory of Ornithology, Department of Biology, University of Evora, 7002-554 Evora, Portugal.
(4) Mediterranean Ecosystems and Landscapes Research Group, Institute of Mediterranean Agricultural and Environmental Sciences, University of Evora, 7002-554 Evora, Portugal.
(5) Corresponding author; e-mail: email@example.com
TABLE 1. Breeding parameters (mean [+ or -] SD) of Eurasian Blue Tits using nest boxes in Parque Florestal de Monsanto (n = 26). Clutch size 6.0 [+ or -] 1.6 Eggs hatched 4.6 [+ or -] 2.3 Chicks fledged 3.0 [+ or -] 12.0 Hatching rate, % 71.9 [+ or -] 31.3 Nest survival rate, % 64.0 [+ or -] 36.1 Breeding success, % 47.9 [+ or -] 30.9 TABLE 2. Aromatic species in nests of Eurasian Blue Tits vs. available aromatic species in nesting habitats. Assessment is based on Wilson's 95% CI comparing the percentage of nests with fragments of each aromatic species (Use) with the percentage of sampling units with that species (Availability). Percent of nests with aromatic plant species (Use) Aromatic plant Mean 95% CI Percent of sample species (a) units containing the species (Availability) Calamintha baetica 30.77 12.68-48.86 2.14 Cistus psilosepalus 3.85 0-11.38 0.71 C. salviifolius 3.85 0-11.38 2.14 Daphne gnidium 0 -- 2.86 Dittrichia viscosa 30.77 12.68-48.86 2.86 Foeniculum vulgare 0 -- 0.71 Geranium robertianum 0 -- 7.86 Hypericum perfoliatum 0 -- 2.14 Jumperus phoenicia 0 -- 0.71 Lavandula dentata 15.38 1.24-29.53 0 Lonicera periclymenum 0 -- 0.71 Mentha spp. 7.69 0-18.14 0 Origanum virens 3.85 0-11.38 2.14 Rosmarinus officinalis 0 -- 1.43 Aromatic plant species (a) Use vs. Availability (b) Calamintha baetica More Cistus psilosepalus No difference C. salviifolius No difference Daphne gnidium Less Dittrichia viscosa More Foeniculum vulgare Less Geranium robertianum Less Hypericum perfoliatum Less Jumperus phoenicia Less Lavandula dentata More Lonicera periclymenum Less Mentha spp. No difference Origanum virens No difference Rosmarinus officinalis Less (a) Species are listed in alphabetical order. Only species detected in nests and on line transecu are listed. (b) We consider that an aromatic species was used more or less than expected if the proportion of sample units containing that species was respectively below or above the 95% CI.
|Gale Copyright:||Copyright 2012 Gale, Cengage Learning. All rights reserved.|