Parasitology Today, vol. 4, no. I, 1988

Do Birds use Biological Control against Nest Parasites?

E,H. Bucher

Many mammals and birds build nests. These range from simple temporary platforms to complex communal structures; occupied over several generations (Fig. I). Nest or burrow habitats offer a relatively stabi~ ..... -onment protected from climatic extremes, in which an abundant source Ul iooa - from the vertebrate hosts and their products - is available for nest-dwelling arthropods. It is from such nest communities that many ectoparasitic arthropods are thought to have evolved 1,2.

Long-term occupancy or re.gulor reuse of nests can allow substantial populations of blood-sucking ectoparasites to develop - which can be severely detrimental to the young nestlings. In this article, Enrique Bucher discusses recent evidence that some bird species make use of novel biologlcal control methods to inhibit nest parasites.

Blood-sucking arthropod ectoparasites that live in the nest and attack the host birds intermittently include ticks, fleas, cimicid bugs, flies and fly larvae. Typically such arthropods can survive for several weeks between feeds, and may over- winter in or near the nest during the nonbreeding season when the bird host is absent. In some cases ec:toparasites represent the chief source of mortality among nestling birds, either by weaken- ing the nestlings (eg, through blood loss) or by transmission of pathogens, which may cause the death of entire broods of nestlings 3-s.

Ectoparasites become a particularly important problem for birds in cavity or domed nests which are reused for sev- eral breeding seasons. Cavity nesting is advantageous for birds becaLuse it pro- vides shelter from climatic extremes and conserves energy. Nestlings remain longer in the nest in spe,sies having enclosed nests 6 but long-term occu- pancy of nests does increase the risk of incurring large parasite loads "~,7,8.

Widespread and well known behav- ioural adaptations against arthropod nest parasites include nest sanitation by the ejection of faeces over the side of the nest, removal of the faecal sacs of the young and frequent renovation of the nest lining material. Nests heavily in- fested with ectoparasites may eventually be abandoned for later broods 9. More recently however, some unexpected and rather sophisticated mechanisms of biological control have been proposed, including the use of insecticidal and anti- pathogenic substances from plants, and the introduction of live cleaning devices (snakes) into the nest.

Green Leaves to avoid Parasites

Many species of birds bring sprays of ~)1988, EIsewer Publ<a'~lons, Cambridge 0169-4758/88/$02.00

fresh green leaves to their completed nests 9 (Fig. I). This habit has been the subject of much conjecture, and a novel suggestion is that the green leaves may function as insecticides or insect re- pellents by releasing secondary com- poundst0,1 I. Many plants produce com- pounds acting as a chemical defence against herbivores and pathogens, and naturally occurring insecticides and bac- tericides in plants are widespread j2,13.

Support for the ectoparasite-repel- lent hypothesis now comes from several sources. For example, greenery was found to be significantly correlated with nest reuse in a set of 49 species of North American and European birds of prey (Falconiformes) I°. Also, a review of the composition of nesting material for 137 passerine birds breeding in eastern North America revealed a significant re- lationship between nesting mode and the use of green vegetation. Passerines nesting in enclosed spaces (eg. secondary cavity nesters or species using crevices) were more likely to incorporate green plants into their nests (I 8 against 9), while those passerines that nest in open cup nests and rarely reuse old nest sites were much less likely to incorporate green vegetation into their nests (28 against 82) II . Nevertheless, this proportion does not represent a general pattern in all avian groups. For instance, from a list of 68 South American ovenbird species (Furnaridae and Dendrocolaptidae) that nest in enclosed spaces only four bring green leaves to their nests t4.

The European starling (Sturnus vul- garis) selects a small subset of available plant species for inclusion in nest mat- eriall L Preferred plants possess a greater number and higher concentrations of monoterpenes and sesquiterpenes com- pared with a random subset of available plants. Volatiles from the selected plants were more effective at retarding egg hatching of the louse Menacanthus than

volatiles from a random sample (but were almost ineffective against adult fowl mites). Leaves from the preferred plants were also more effective in inhibit- ing growth of some bacteria found in nests (excluding Escherichia coil) I I.

Several alternative explanations have been offered for the use of fresh vegeta- tion for nest construction. First, greenery may be used as a form of nest sanitation, covering rotten material and excreta- but this does not explain why it should be done with green leaves, rather than with other material, or why the greenery should be brought in some cases long before the eggs are laid and the nest is soiled 15. Second, greenery could be a form of advertisement, denoting an occupied territory. In that way the occupants may reduce the need to expel intruders by more energetic means. But the nest-occupancy hypothesis does not explain why greenery is still brought after there are eggs or nestlings pres- entll, 16. Third, fresh vegeta~on may reduce the rate of desiccation of eggs (and thereby improve their hatching suc- cess) by raising the vapour pressure in the nest environment 16. This humidity- maintenance theory does not explain why the use of green leaves is as com- mon in rainforests and maritime climates as it is in dry ones, at least in raptors Is. No experiments have been carried out to test this hypothesis.

A fourth hypothesis contends that by covering the nestlings green vegetation may help to camouflage the nest and thus minimize the risk of predation 17, while a fifth proposes that leaves may be used to shade the nestlings 18. Both hypotheses fail to explain the presence of greenery in cavity nests or in the nests of forest birds located beneath the canopy, or why the material used to shade should be green. There is no indi- cation that the leafy sprays are placed in the nests of open-dwelling birds in a manner that would shade eggs or nest- ling during the hottest part of the day, when this behaviour would be most beneficial l0

In the end, you may prefer to agree with Gramme ~9 that the birds use greenery to lend "an appearance of artis- try and colour", but none of the above hypotheses appears sufficient to account for the widespread occurrence of this trait in the variety of climates, habitats

Parasitology Today, vol. 4, no. I, 1988

Fig. I. The South American Monk Parakeet (Myiopsitta monachus) (inset) builds large com- munal nests on any toll structure - natural or artificial. The nests are occupied throughout the year and usually host large numbers of arthropod parasites. Parakeets are among those birds that bring fresh green leaves to the nest while breed- ing, and this may help to inhibit ectoparasites.

and circumstances under which it appears.

The available evidence suggests that birds use chemicals in fresh vegetation as fumlganT_s against parasites and patho- gens. but this idea should be interpreted cautiously. Moreover, a primary pur- pose of repellency does not necessarily exclude the possibility of subsidiary func- tions, such as sanitation, maintenance of humidity, or advertisement. Field tests are needed to demonstrate conclusively whether or not greenery actually repels or kills ec~oDarasJ~es in the nest under field conditions to an extent that results in ~mproved nestling survival.

However. accepung that birds select Dlants according to their effects agaLnst parasptes and pathogens, some equally intriguing questions arise: How can birds detect differences between plants - do they rely on visual or chemical cues? Considering that ~lants available for use as nest matena differ throughout the

Parasitology Today, vol. 4, no. I, 1988 3

breeding ranges of many species, how do juveniles learn to select a particular chemical profile? Can they form associa- tions between a given plant material and its effects on parasites or pathogens? And why should this habit be restricted to birds? Mammals living in burrows should benefit from a simiar practice, yet no such case has yet been re- ported,

Snakes for Housekeeping

A more exceptional case of be- havioural adaptation implying the use of biological material to control nest para- sites is suggested by recent studies of North American owls. Nests of elf owls (Microthene whitnegi) and eastern screech owls (Otus asia) sometimes con- tain live blind snakes (Leptotyphlops dul- cis) 20,21. These snakes are normally fosso- rial but readily climb trees where they could enter the owl nests in search of soft- bodied insect prey. However, recent studies by Gehlbach and Baldridge 20 reveal that the screech owls - which nor- mally kill their prey before de.livering it to the nest-frequently carry live blind snakes to their nests where they may survive by eating arthropod larvae living; in the nest detritus. The authors point out that the snakes, besides reducing larval parasitism on the young owls, may also reduce the amount of food eaten by insects, leaving more for the growing birds. They found live snakes in 18% of 77 nests;, with more than half the snakes showing signs of dam- age by the birds. Nestlings from nests with resident snakes grew faster ancl had better rates of survival than snakeless broods.

It remains possible that the snakes were taken to the owl nests as prey (as suggested by the high proportion of snakes showing signs of da.mage), but escaped while being manipulated. In that situation they may have survived by bur- rowing under the nest structure and debris. Under the same circumstances nonfossorial snakes would prefer to slip out of the nest but the fossorial blind snakes appear to find the nest a suitable substitute for their normal subterranean habitat. The higher rate of growth shown by nestlings from nests with snakes may simply reflect a better hunting efficiency by their parents, or it may reflect some degree of specialization in prey capture associated with a higher frequency of encounters in some specific places. Yet the apparent benefit to the owls of bringing an efficient predator of insects to their nest is attractive, and certainly merits further study, although it is diffi- cult to understand why such supposedly advantageous behaviour is so -estricted in

terms of the number of species involved and geographical range.

Overall, the possi- bility of disentangling complex adaptations developed by verte- brates to deal with nest parasites opens a fascinating field of research, particularly at a time when the impact of parasites on the evolutionary biol- ogy of hosts is being actively recast 22, After all, we too are 'nest- building' vertebrates!

Enrique Bucher is Director of the Centro de Zoologia Aplicada, Universidad de Cordoba, Casilla 122, Cordoba, Argentina.

References I Marshall, A.G. (i 981 ) The Ecology of Ectoparasi-

tic Insects, Academic Press 2 Waage, J.K, (1979) BiaLJ. Linn. Sac. 12, 187-224 3 Feare, C.J.(1976)lbisl18, 112-115 4 Powlesand, R.G. ([ 977) NewZeatandJ. 7_oot. 4,

85-94 5 Duffy, D.C. (1983) Ecology 64, 110-119 6 Lack, D. (1968) Ecological Adaptations for

Breeding in Birds, Methuen 7 Smith, G.C. and Eads, R.B. (I 978)]. Washington

Acad. Sci. 68, 23-26 8 Humphrey-Smith, I. and Moorehouse, D.E.

(I 981 ) Ann. Parasitol. (Paris) 56,353-357 9 Callas, N. and Collias, E. (1984) Nest Building

Behavior in Birds, Princeton University Press I 0 Wimberger, P.H. (I 984) Auk 10 I, 61 5-618 I I Clark, L. and Russell Mason, J. (1985) Oecologia

67, 169-176

ke~ ~ Why can't we have a snake like everyo e e se.

12 Rosenthal, G.A. and janzen, D.H. (eds) (I 979) Herbivores; Their Interactions with Secondary Plant Metabolites, Academic Press

13 Secoy, D.M. and Smith, A.E. (I 983) Econ. Bat. 37, 28-57

14 Narosky, S. eto/. (1983) Nidiflcacion de los Ayes Argentinas, Asociacion Ornitologica del Plata, Buenos Aires

I 5 Newton, I. (1979) Population Ecology of Roptors, Buteo Books, Vermilion, South Dakota

16 Sengupta, S. (1968) Prod. Zool. Sac. Calcutta 2 I, 1-27

17 Skutch, A.F. (1976) Parent Birds and Their Young, University of Texas Press

18 Bush, ME. and Gehlbach, F.R. (I 979) Bull. Tex. Ornithol. Sac. I I, 41-43

19 Gramme, O.j, (I 935) Auk 52, 15-20 20 Gelbach, F. and Baldridge, R. (1987)Oecotogia

7 I, 560-563 21 Ligon, J.D. (1968) Mus. Zool. Univ Michigan

Misc. Publ. 136, 5-70 22 Price, P.W. (1980) Evolutionary Biology of Para-

sites, Princeton University Press

W H O Filariasis S e r u m Bank

The Filadasis Serum Bank established by the Filariasis SWG of the WHO Special Pro- gramme (TDR) has a limited number of 0,2 ml alieuots of well-characterized sara from patients with single infections of each of the following parasites (including a few pooled samples):

Wuchereria bancrofti (from India, Sri Lanka. Papua New Guinea. Phil ppines, Fiji, Tahiti) Brug a malayi B. timori ?

(from Indonesia)

Onchocerca volvulu~(from Ivory Coast. Sudan, Guatemala) Loa too (from Congo) Mansonetla ozzardi (from VenezueIa) M perstans (from Congo) Samples from pat~ent_s w~th Drocunculus medinensis ~nfection should also be available s o o n .

Inves~iga~ors may request samples of these sera from: The Secretary Steenng Committee of the Soentific Working Group on Filariasis World Health Organlzat~on 121 I Geneva 27 Switzerlancl

giving the follow~ng details: (a) An outline arotocot for the study using such sera. including detai~s of requirements and justification. (b) An agreement to reimburse the costs of d~spatching the samples. For scientists from developing countries, financlat assistance for this might I::]e arranged. (c) An undertaking to submit a report of the work done using the sera.

In order to expedite approval for release of the sara, copies of the request must also be

varsity, East Lansing, Michigan 48824- 1101. USA.