Aromatic plants in bird nests as a protection against blood-sucking flying insects?
Introduction
Animals use different defence mechanisms against parasites such as complex immune systems, resistance genes or specific behaviours (Loye and Zuk, 1991, Clayton and Moore, 1997). One of these mechanisms is self-medication, i.e. a defence against parasites by using substances produced by other organisms (Clayton and Wolfe, 1993). In some bird species, individuals bring green plant material to active nests that contain eggs or nestlings (Wimberger, 1984, Clark and Mason, 1985, Rodgers et al., 1988). Clark (1991) has reviewed the various functional hypotheses to explain this behaviour. The nest-protection hypothesis suggests that some of the fresh plants brought to the nest contain secondary compounds that repel parasites or mask the chemical cues that parasites use to find the host (Wimberger, 1984, Clark, 1991). This hypothesis provides the simplest explanation for why female Corsican blue tits (Parus caeruleus ogliastrae) incorporate into nests with eggs or nestlings, up to five aromatic herb species with distinct odours easily perceived by humans (Lambrechts and Dos Santos, 2000, Banbura et al., 1995). The plants selected represent a small fraction of the species observed in the blue tit territory. Furthermore, blue tits sometimes incorporate into the nest, fragments of plant species not observed in the territory (Lambrechts and Dos Santos, 2000, Petit, 2000). Lambrechts and Dos Santos (2000), therefore, hypothesised that a mixture of plants (the ‘Potpourri effect’) provides more benefits than the presence of a single plant species in the nest; for instance, treatment with a mixture of aromatic plant fragments would be a more efficient defence mechanism against parasites than the treatment with a single plant species (the ‘Potpourri hypothesis’).
Fresh plant material brought to the nest at the end of the evening, as observed in Corsican blue tits (Banbura et al., 1995), may be a defence mechanism against blood-feeding insects at night or dusk, such as ornithophilic mosquitoes (Rothschild and Clay, 1953, Jaenson, 1990). Although host–parasite interactions have been studied extensively in natural bird populations, the effects of blood-sucking flying insects on bird life history traits and behaviour are a neglected subject (Bucher, 1988, Loye and Carroll, 1995). This is probably explained by the relative discretion (nocturnal activity, ephemeral at the nest and small size) of these insects, which are essentially nematocera diptera: black flies (Simulidae), biting midges (Ceratopogonidae) and mosquitoes (Culicidae) (Rothschild and Clay, 1953). However, the insects are probably detrimental to their host by removing some blood, although they also inject toxins and may act as vectors of parasitic diseases (Scott and Edman, 1991, Richner et al., 1995). Some studies indicate that these effects can dramatically affect some life history traits (Anderson et al., 1999), particularly when bites are numerous (e.g. Smith et al., 1998). In northern Europe, 20 species of mosquitoes have been found to feed preferentially or occasionally on birds (Jaenson, 1990), and some viruses such as the sindbis virus (Togaviridae: Alphavirus) or the Nile virus (Flaviviviridae: Flavivirus) are equally found in birds and mosquitoes (Francy et al., 1989, Lundström et al., 1992, Anderson et al., 1999).
The aim of this study was to establish whether aromatic herb species found in Corsican blue tit nests repel blood-sucking flying insects or mask the presence of a host. Experiments were performed using the mosquito Culex pipiens (L.) (Diptera: Culicidae), which is common in Corsica (Raymond and Marquine, 1994) and can be a vector of avian malaria (Vinogradova, 2000). More specifically, experiments have been conducted with this mosquito presented to a bird host in laboratory conditions, with or without a mixture of the Corsican aromatic herb species. For practical reasons, domestic chicks (Gallus gallus) have been used in the experiments, instead of blue tits.
Section snippets
Plants
Four species of aromatic plants found in Corsican nests (Lambrechts and Dos Santos, 2000) were used: Achillea ligustica, Helichrysum italicum, Lavandula stoechas and Cistus creticus. For each experiment, 1 g of fresh material was used which is slightly above the mean, although within the range of natural variation of quantity (Lambrechts, unpublished data), containing either only one plant species or a mixture of all four, depending on the treatment: control (T1), mixture (T2); monospecific
Repellent experiment
Overall, the mixture of aromatic plants had a repellent effect (P<0.01, Table 1). Individual plants had no repellent effect, with the exception of L. stoechas (P<0.0001). Results were heterogeneous for the mixture and L. stoechas, not all repetitions showing a repellent effect (Table 1).
Choice experiment
The mixture of aromatic herbs had a highly significant effect (P<0.0001) to protect chicks from female seeking a blood meal (Table 2). The corresponding minimal probability (pmin) of blood feeding in the control
Discussion
Many birds select fresh plant material that they bring to the nest (Wimberger, 1984, Clark and Mason, 1985, Rodgers et al., 1988, Milton and Dean, 1999). Several studies have investigated the potential anti-ectoparasite or anti-pathogen effect of these fresh plants (Clark and Mason, 1985, Clark and Mason, 1988, Hart, 1997), mainly because they have volatile compounds often considered to have possible repellent or toxic properties against insects, bacteria or herbivores (Jacobson, 1990, Barel et
Acknowledgements
We thank F. Rousset for providing the binomial exact test program, C. Bernard, M. Marquine, P. Perret, A. Dos Santos for technical assistance and C. Berticat, C. Chevillon, D. Heyse, C. Manus for help in mosquito supply, M. Hossaert-McKey for comments. This is contribution no. ISEM 2001.083 (UMR 5554).
References (42)
- et al.
The antimicrobial activity of 3,5,7-trihydroxyflavone isolated from the shoots of Helichrysum aureonitens
J. Ethnopharmacol.
(1997) - et al.
The antimicrobial activity of the essential oil from Achillea fragrantissima
J. Ethnopharmacol.
(1991) Terpene-sensitive receptors in female Culex pipiens mosquitoes: electrophysiology and behaviour
J. Insect Physiol.
(1992)Do birds use biological control against nest parasites?
Parasitol. Today
(1988)- et al.
The adaptive significance of self-medication
Trends Ecol. Evol.
(1993) - et al.
Green plants in starling nests: effects on nestlings
Anim. Behav.
(2000) - et al.
Aromatic herbs in Corsican blue tit nests: the ‘Potpourri’ hypothesis
Acta Oecologia
(2000) - et al.
Birds, bugs and blood: avian parasitism and conservation
Trends Ecol. Evol.
(1995) - et al.
Isolation and identification of the antibacterial compounds from Helychrysum stoechas
J. Ethnopharmacol.
(1991) - et al.
Antifungal activities of Origanum vulgare subsp. Hirtum, Mentha spicata, Lavandula angustifolia, and Salvia fruticosa essential oils against human pathogenic fungi
J. Agric. Food Chem.
(1998)
Isolation of West Nile virus from mosquitoes, crows, and a Cooper's hawk in Connecticut
Science
Why do female Blue Tits (Parus caeruleus) bring fresh plants to their nests?
J. Ornithol.
The nest protection hypothesis: the adaptive use of plant secondary compounds by European starlings
Use of nest material as insecticidal and anti-pathogenic agents by the European starling
Oecologia
Effect of biologically active plants used as nest material and the derived benefit to starling nestlings
Oecologia
Emergence and its diel periodicity in Aedes (O.) communis (DeG.), punctor (Kirby) and hexodontus Dyar in Swedish Lapland
Aquilo Ser. Zool.
Composition and antimicrobial activity of the essential oil of Cistus creticus subsp. eriophalus
Planta Med.
Ecologic studies of mosquitoes and birds as hosts of ockelbo virus in Sweden and isolation of inkoo and batai viruses from mosquitoes
Am. J. Trop. Med. Hyg.
Insecticidal and genotoxic activities of mint essential oils
J. Agric. Food Chem.
Behavioural defence
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