Austral Ecology (2010) 35, 444–450 Non-lethal foraging by bell miners on a herbivorous insect: Potential implications for forest healthaec_2099 444..450 KATHRYN M. HAYTHORPE1,2 AND PAUL G. McDONALD2* 1School of Environmental and Life Sciences, Newcastle University, Newcastle, New South Wales, and 2Department of Brain, Behaviour and Evolution, Macquarie University, Sydney, NSW 2109, Australia (Email: [email protected]) Abstract Tree health is often negatively linked with the localized abundance of parasitic invertebrates. One group, the sap-sucking psyllid insects (Homoptera: Psyllidae) are well known for their negative impact upon vegetation, an impact that often culminates in the defoliation and even death of hosts. In Australia, psyllid-infested forest in poor health is also frequently occupied by a native honeyeater, the bell miner (Manorina melanophrys; Meliphagidae), so much so that the phenomenon has been dubbed ‘bell miner-associated dieback’ (BMAD). Bell miners are thought to be the causative agent behind BMAD, in part because the species may selectively forage only upon the outer covering (lerp) exuded by psyllid nymphs, leaving the insect underneath to continue parasitizing hosts. As bell miners also aggressively exclude all other avian psyllid predators from occupied areas, these behavioural traits may favour increases in psyllid populations. We examined bell miner foraging behaviour to determine if non-lethal foraging upon psyllid nymphs occurred more often than in a congener, the noisy miner (M. melanocephala; Meliphagidae). This was indeed the case, with bell miners significantly more likely to remove only the lerp covering during feeding, leaving the insect intact underneath. This arose from bell miners using their tongue to pry off the lerp cases, whereas noisy miners used their mandibles to snap at both the lerp and insect underneath. Furthermore, psyllids left behind following a bell miner foraging event were significantly more likely to be viable and regrow a lerp covering than those exposed by noisy miners. Together, this behaviour supports the theory that non-lethal foraging behaviour of bell miners may contribute to high psyllid abundance, consistent with the mechanisms by which BMAD is thought to develop. Key words: bell miner-associated dieback, group living, lerp, Manorina, psyllid. INTRODUCTION 1997). Threatened taxa in these habitats face further challenges in the near future given the grim changes Insect-based herbivory can affect every aspect of a forecast by most climate change models (Dale et al. plant’s performance, leading to a decrease in defences 2001). Given this, it is important that the factors sur- and a vulnerability to declining health and subsequent rounding insect infestation and the ensuing dieback be plant death, a phenomenon known as ‘dieback’. Symp- determined promptly, so that attempts to redress the toms of tree dieback can be varied, but are typically issue can be made in stands set aside for both conser- characterized by the wholesale defoliation of leaves vation and harvesting purposes around the globe. and thus canopy cover, a process that often progresses Numerous insects have been implicated in diminishing through to tree death if left unchecked (Landsberg & tree health and dieback of eucalypts in Australia (for a Wylie 1983). Forests of almost any composition of review see Ohmart & Edwards 1991); however, psyl- species worldwide can be affected by insect infesta- lids (Homoptera: Psyllidae) appear to be among the tions and subsequent dieback, leading to devastating most detrimental (Stone et al. 2008). results (e.g. Vejpustková & Holuša 2006; Carus 2009). The most commonly observed psyllid genus in The impact of insect herbivory looms as a significant dieback areas is Glycaspis, both within Australia (Stone threat to the health of large areas of forest worldwide, et al. 2008) and in plantations where these insects have as habitats are placed under ever increasing levels of been introduced (Brennan et al. 2001).These parasitic anthropogenic stress (Crawley 1989). In Australia invertebrates are small (adults usually <5 mm; Moore many threatened and endangered species are restricted 1961) and resemble aphids (Hemiptera: Aphidoidea) to eucalypt-dominated woodland (Yates & Hobbs in appearance. Adults are winged and mobile, with females laying their eggs on the leaves of eucalypts *Corresponding author. that later hatch into wingless nymphs. Nymphs suck Accepted for publication October 2009. sap directly out of leaves via a specially adapted © 2010 The Authors doi:10.1111/j.1442-9993.2009.02099.x Journal compilation © 2010 Ecological Society of Australia SELECTIVE FORAGING IN BELL MINERS 445 mouthpiece called a stylet. For protection, they exude coverings observed (Poiani 1993), contrary to that a solid, carbohydrate-rich substance that covers the expected if foraging habits of the birds are driving insect in a dome-like structure, termed ‘lerp’ (Moore BMAD. However, the digestion speed of lerp relative 1961).This sugary lerp is a favoured component of the to nymphs in bell miners’ guts was not quantified. diet of many bird species, particularly passerines (Woi- Moreover, psyllid nymphs retain previously moulted narski et al. 1989; Kavanagh & Stanton 2003). One exoskeletons under their lerp coverings, and these species in particular, the bell miner Manorina mel- additional exoskeletons may have potentially been anophrys (Meliphagidae), is heavily dependent upon recorded as entire predated nymphs, complicating lerp as a food source both as adults and nestlings (te interpretation of these results. In any case the key point Marvelde et al. 2009).This species, native to Australia, to the relationship is whether nymphs remaining fol- is an obligate cooperative breeder (e.g. Clarke 1989; lowing bell miner predation are able to continue to McDonald et al. 2008; Wright et al. 2009) that forms parasitize leaves, a factor that has yet to be investigated large colonies of several hundred individuals. Individu- in any study. Given this, while there is correlational als cooperate in a variety of contexts within the colony evidence linking bell miner presence with high (Pacheco et al. 2008), but are best known for their numbers of psyllids and eucalypt dieback (e.g. despotic nature. Aggression directed at other species is Wardell-johnson et al. 2005; Stone et al. 2008) and so severe and effective in this species that potential some experimental evidence (e.g. Loyn et al. 1983; avian predators and food competitors are typically Loyn 1987, but see also Clarke & Schedvin 1999), the excluded from the entire area that colonies occupy causative mechanism has yet to be established (Dare (Loyn et al. 1983; Poiani 1991). et al. 2007). This exclusion of other potential psyllid predators We attempted to clarify bell miner foraging prac- from colonized areas of forest has been suggested to be tices, by assessing the feeding behaviour of captive bell one mechanism by which psyllids may become overly miners on leaves with known numbers of psyllids. If abundant, leading to subsequent eucalypt dieback. bell miners do forage in a specialized manner, we Bell miners are thought to consume mainly the lerp anticipated that they would leave more nymphs behind covering of psyllid insects, leaving the insect sheltering than their congener, the noisy miner (M. melano- underneath intact. This is in contrast to more typical cephala; Meliphagidae). This species has a similar avian predators that consume both the insect and lerp dietary niche and habitat requirements to bell miners, (Loyn 1987). The combination of this specialized for- yet its association with dieback is less widespread and aging strategy and extreme territoriality may then lead is more apparent in small isolated remnants (e.g. Grey to psyllid numbers increasing to the point where tree et al. 1998) as opposed to BMAD that can be found health declines and canopy dieback occurs. The cor- in areas of forest largely undisturbed by humans relation between bell miners and eucalypt dieback has (Wardell-johnson et al. 2005). To verify the veracity of long been suggested (Chandler 1922) and has come to psyllid nymphs remaining on leaves, we further exam- be known as bell miner-associated dieback (BMAD). ined the regrowth potential of nymphs following This process has the potential to affect up to 2.5 removal of their lerp coverings. million hectares of forest in the Australian state of New South Wales (NSW) alone (Wardell-johnson et al. 2005). These areas likely to be affected are home to over 40 threatened species of flora and fauna (NSW METHODS Scientific Committee 2008), a significant portion of the regions biodiversity. Source of animals and husbandry However, the mechanism/s driving BMAD are not well understood. While it has long been proposed that Bell miners (n = 16) were temporarily removed from a local selective consumption of lerp casings by bell miners population at Mount Wilberforce Lookout Reserve, NSW, exists (Loyn et al. 1983), empirical data are lacking Australia (151°02′51.04″E, 33°44′44.38″S). Noisy miners and it remains a matter of some debate (Poiani 1993; (n = 16) were sourced from a colony located on the Macqua- Loyn 1995; Wardell-johnson et al. 2005). Field obser- rie University campus (151°06′48.43″E, 33°46′09.22″S). vations of this phenomenon by foraging birds using Birds were housed at Macquarie University in cages measur- binoculars (e.g. Woinarski 1985; Poiani 1996) are typi- ing 2 ¥ 1 ¥ 1.8 m (l ¥ w ¥ h: hereafter cage A), with a smaller cally considered unreliable because of the difficulty of cage measuring 75 ¥ 44 ¥ 44 cm (hereafter cage B) attached to one side. A sliding door separated the two cages. Birds recording such small insects in a moving tree canopy were fedWombaroo lorikeet and honeyeater mix (Wombaroo (Woinarski et al. 1989). Earlier work examined the Food Products, Adelaide, Australia), nutritional supplements feeding behaviour of captive bell miners, but results and water every morning in cage B, to allow them to grow were inconclusive because of small sample sizes (Tyers accustomed to feeding from this cage.Trials were carried out 1981; Robinson 1982).