What Weta Want: Colour Preferences of a Frugivorous Insect
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Arthropod-Plant Interactions (2010) 4:267–276 DOI 10.1007/s11829-010-9109-0 ORIGINAL PAPER What weta want: colour preferences of a frugivorous insect Nik Fadzly • K. C. Burns Received: 24 March 2010 / Accepted: 18 October 2010 / Published online: 31 October 2010 Ó Springer Science+Business Media B.V. 2010 Abstract Plants use colours as signals to attract mutual- consistent preferences for colours other than red indicate ists and repel antagonists. Fleshy-fruits are often conspic- that weta might be responsible for the unusual colours of uously coloured to signal different types of information fleshy-fruits in New Zealand. including fruit maturity and spatial location. Previous work on fruit colour selection focus on large diurnal vertebrates, Keywords Colour Á Fleshy-fruits Á New Zealand Á yet fruit colours are perceived differently by frugivores Weta with different types of visual systems. Here, we tested whether a nocturnal, frugivorous, seed-dispersing insect selects fruits based on their pigmentation and whether Introduction different lighting conditions affect fruit colour selection. We captured 20 Wellington tree weta (Hemideina crassi- Most plants are sessile and often rely on animals for the dens) from a forest reserve on the North Island of New movement of seeds and pollen. In order to attract animal Zealand and brought them into laboratory conditions to test mutualists, plants often use colour signals. Fruits and their fruit colour preferences. The fruits of Coprosma flowers are often brightly coloured to attract frugivores and acerosa, a native shrub species that naturally produces pollinators (see van der Pijl 1972; Janson 1983; Willson translucent, blue-streaked fruits, were dyed either red or et al. 1990; Kelber 1996; Burns and Dalen 2002; Raine blue. Fruits were then offered to weta in a binary (y-maze) and Chittka 2007; Pohl et al. 2008). Different lineages of choice test in two light conditions, either at night during a animal mutualists often have unique eye structures with full moon or under artificial light conditions in the lab. different photosensitive receptor cells and spectral sensi- Weta preferred unmanipulated, naturally blue-streaked tivities (Osorio and Vorobyev 2008). Therefore, a fruit fruits and artificially-blue coloured fruits over those dyed colour that is highly conspicuous to birds, might not be as red. Furthermore, their colour preferences were unaffected conspicuous to other frugivores, such as mammals, lizards by light environment. Our results therefore suggest that and insects (Osorio and Vorobyev 2005, 2008). weta can discriminate between colours (using colour Previous work on fruit colour preferences has focused vision) in both light and dark light environments. Their on birds (e.g. Schaefer et al. 2003, 2006; Lomascolo and Schaefer 2010) and mammals (e.g. Endler 1978; Dominy and Lucas 2001; Endler and Mappes 2004; Loma´scolo Handling Editor: Lars Chittka. et al. 2008). Comparatively little work has been conducted on lizards (Whitaker 1987; Lord and Marshall 2001; Lord N. Fadzly (&) School of Biological Sciences, Universiti Sains Malaysia, et al. 2002; Roth and Kelber 2004; Kelber and Roth 2006). 11800 Minden, Penang, Malaysia Although insect colour vision has been discovered over e-mail: [email protected] 100 years ago (Lubbock 1881), most studies focus on plant-pollinator interactions or folivorous insects, without N. Fadzly Á K. C. Burns School of Biological Sciences, Victoria University of any specific consideration of frugivores (Lunau and Maier Wellington, P.O. Box 600, Wellington 6140, New Zealand 1995; Chittka and Wells 2004; Raine et al. 2006; Raine and 123 268 N. Fadzly, K. C. Burns Chittka 2007). Insect frugivores contain diverse taxa from experiments have been conducted in daytime light condi- Orders such as Lepidoptera, Hemiptera, Coleoptera and tions. The effect of varying light environments on fruit Diptera (Sallabanks and Courtney 1992). However, current colour selection is therefore poorly understood. Light understanding of insect frugivore interactions is mostly conditions are known to have a pronounced effect on the simplified because knowledge of insect frugivores outside foraging behaviour of animals (Willmer and Stone 2004; of pollination biology or an agricultural context remains Kelber et al. 2005; Somanathan et al. 2008a, b, 2009a, b; largely untested (Wilson 2008). Little is known about fruit Caine et al. 2009). Daytime environments are illuminated colour selection by frugivorous insects. by either direct or diffuse sunlight. While most available Weta are an entirely unique type of seed disperser that light remains constant at specific solar inclinations, other are endemic to New Zealand. Weta are massive, nocturnal factors such as cloud cover, canopy cover and humidity are orthopterans. Giant Weta (Deinacridia sp.) are known to known to affect the lighting environment. In contrast, grow up to nearly ten centimetres in length and weighting crepuscular and nocturnal light environments are influ- 20–70 g (Gibbs 2001). They are the only insect known to enced by multiple sources with different spectra, such as consume entire fleshy-fruits and pass seeds in viable con- airglow emissions, scattered, low-inclination sunlight and dition after ingestion (Duthie et al. 2006). However, their moonlight (Leinert et al. 1998). Each of these potential importance to plants as seed dispersers is largely unknown influences varies in intensity and spatial extent resulting in and their capacity to select for particular fruit characteris- fluctuating light environments that can change rapidly tics such as colour has been debated (Burns 2006, 2008; (Johnsen et al. 2006). Different light conditions can have a Morgan-Richards et al. 2008; King et al. 2010). Very little substantial effect on the appearance and visibility of is known about their photoreceptor spectral sensitivities. objects and organisms (Endler 1993; Johnsen et al. 2006). However, based on electroretinogram analyses, weta Little is known about how light environments affect colour appear to be blind at the red end of the visible spectrum, preferences in frugivorous animals and in particular how similar to many other insects (Field 2001). Orthopteran crepuscular and nocturnal seed dispersers use colour sig- insects such as weta have rarely been studied with respect nals to make fruit choices. to wavelength selective behavorials, spectral preferences, Here, we investigate how light conditions affect fruit colour vision or colour learning (Zufall et al. 1988; Behmer colour selection by New Zealand weta. We conducted an et al. 2005, but see Wasserman and Kong 1982; Bernays experiment where we dyed the fruits of Coprosma acerosa, and Wrubel 1985). Therefore specific information on weta an endemic plant species that we show is dispersed by weta vision capabilities and colour selection are lacking. after gut passage, either red or blue. Different coloured New Zealand’s fruit colours are unusual from a human fruits were then presented to weta in paired choice tests perspective. There are no green fruits at maturity and white under two light conditions, full moonlight and under arti- fruits, which are comparatively rare elsewhere in the world, ficial lights. Results were then used to determine whether make up 21.2% of the 246 fleshy-fruited floras (Lee et al. weta make consistent fruit choices based on their colour 1988, 1990, 1994; Willson et al. 1989;Lordetal. 2002). In and whether these choices are affected by the ambient light comparison to the other various regions in the world, most environment. fruits are either typically black (34–41% in Costa Rica, Peru and Florida) and/or red (21–27% in Galapagos Islands and Gabon). South African trees with mammal dispersal Materials and methods commonly have yellow (31%), green (20%) or orange (16%) fruits (full list of fruit colour comparison available Weta from Willson et al. 1989). New Zealand is home to an unusual and diverse array of seed dispersers, including New Zealand weta are a group of insects in the order bats, birds, lizards and weta. Because each of these taxa Orthoptera and are related to grasshoppers, locusts, ka- have different visual systems and activity periods, the tydids and crickets (Gibbs 2001; Gorochov 2001). All of unusual fruit colours present in the New Zealand flora may the experiments were conducted using a single species, the be a reflection of differential selection by different types of Wellington tree weta (Hemideina crassidens, Blanchard) frugivores (Lord and Marshall 2001;Lordetal. 2002; (Fig. 1a), a common species of weta, in New Zealand. Wotton 2002; Burns 2006; Duthie et al. 2006). However, Wellington tree weta are nocturnal and spend most of their this explanation for the evolution of fruit colour diversity time foraging arboreally. They are primarily herbivorous, has received little evidence to date (Willson and Whelan feeding on the leaves, flowers and fruit of a wide range of 1990; Herrera 2002). trees and shrubs, but they will also take living or recently Past studies on the fruit colour preferences of frugivores dead invertebrates when they get the opportunity (Gibbs have focused on diurnal seed dispersers and previous 2001). Twenty adult animals (10 male and 10 female) were 123 Weta fruit colour selection 269 C. acerosa belongs to the Rubiaceae family. Coprosma acerosa produces fleshy-fruits that are globose, 7 mm in diameter (Fig. 1b) and each contain two flattened seeds. Coprosma acerosa fruits are translucently white coloured and are sometimes