Floral cognition: Comparative and functional perspectives

In this paper, I begin by presenting a detailed summary and discussion of work that has been conducted in my laboratory investigating how the cognitive mechanisms that underpin foraging may be adapted to maximally exploit resources of different distributions. My study species, the noisy miner (Aves: Meliphagidae, Manorina melanocephala) is a generalist forager that feeds on both nectar and invertebrate prey – resources with quite different natural distributions. Throughout this discussion I draw comparisons between the behaviour and cognition of noisy miners and other relevant species. These include the two other nectarivorous groups that have been the subjects of the most in-depth investigations of the cognition of nectar foraging: hummingbirds (especially rufous hummingbirds, Selasphorus rufus) and bees; and also several species of insectivorous birds. I then consider how the different extant approaches to studying animal cognition lead researchers to ask different questions, apply different types of studies and ultimately draw quite different conclusions about the structure and function of cognitive mechanisms across the Animal Kingdom. In particular, I discuss the implications of these different approaches for interpreting the findings from avian nectarivores and for inspiring the directions of future research. I finish by identifying some of the strengths and weaknesses of the research programs examined. I also suggest some potentially profitable future directions, including the development of more novel paradigms, and the use of formal modeling to guide quantitative predictions of behaviour. * Corresponding author: Email: danielle.sulikowski@ymail.com. The exclusive license for this PDF is limited to personal website use only. No part of this digital document may be reproduced, stored in a retrieval system or transmitted commercially in any form or by any means. The publisher has taken reasonable care in the preparation of this digital document, but makes no expressed or implied warranty of any kind and assumes no responsibility for any errors or omissions. No liability is assumed for incidental or consequential damages in connection with or arising out of information contained herein. This digital document is sold with the clear understanding that the publisher is not engaged in rendering legal, medical or any other professional services. Danielle Sulikowski 108 NOISY MINERS – A TALE OF TWO STRATEGIES Noisy miners (Aves: Meliphagidae, Manorina melanocephala) are a species of Australian honeyeater. They are generalist foragers, feeding on nectar and invertebrates, which they capture using a variety of methods, including gleaning and hawking (Barker and Vestjens, 1984; Dow, 1977). Noisy miners also frequently feed on novel food sources in urban areas (personal obs.) including opening commercial sugar packets (Delgado-V and Correa-H, 2015). Aside from one recent investigation exploring problem-solving in noisy miners (Griffin and Diquelou, 2015), our knowledge of their cognition comes from a series of experiments conducted in our lab examining differences in how these birds use information while foraging for resources with natural distributions: nectar compared to invertebrates. In contrast to the majority of the work with hummingbirds described above, all of the research we have conducted in our lab with noisy miners has been conducted in captivity. Our subjects have all been adult noisy miners of unknown age and sex, although our samples are likely to be strongly male biased, mirroring the sex-ratio of these birds in the wild (Arnold, Griffith and Goldizen, 2001). For all of our studies, wild birds were trapped days (up to several weeks) prior to the experiments and banded and released shortly after. Banding birds prior to release allowed us to confirm that our experimental subjects successfully re-integrated into their social groups post-release (which we were able to observe was the case for the majority of birds), and also ensured that each sample of birds trapped was experimentally naïve. While in captivity, all our birds are held individually in adjacent cages measuring 3m x 3m x 3m. All testing is carried out in each bird's home cage. The majority of our studies' designs have several features in common. Birds are required to search arrays of feeders presented, vertically, on the front wall of their home cage to locate rewards. In some cases, the number of feeders a bird was permitted to probe on any given trial was limited to the number of rewards available in the array, such that probing a non-rewarded feeder (or the same feeder twice) carried the cost of being unable to retrieve all available rewards. In most cases, however, the time a bird was permitted to search the array was ample to allow birds to retrieve all rewards, no matter how many 'incorrect' (unrewarded, or already visited) feeders a bird probed. Feeders are designed such that they are self-closing, so that after a bird has probed a feeder and moved on, the feeder closes again, making it visually indistinguishable from feeders the bird has not yet visited on that trial. To understand how noisy miners' cognitive strategies may have diverged to support efficient foraging on both nectar and invertebrate prey, birds in our studies were rewarded with either a 30% w/v sucrose solution (imitating nectar) or a mealworm (representing invertebrate prey). These food types were usually manipulated between-subjects. Nectar is a resource with a reasonably well-defined distribution. It is found in visually conspicuous, discrete point locations in space (flowers), which are typically clumped (on plants). Thus, there are clear visual cues that indicate the potential locations of nectar and that define the locations and boundaries of patches of nectar. While invertebrates, as a category of prey items, is large and heterogeneous there are some generalisations that we can make about their distribution (at least with respect to the types of prey items that noisy miners typically consume). Unlike nectar, their point locations in space are not usually signaled prior to attack, as they are typically cryptic. They are also mobile. This means that, within the boundaries of a suitable ‘patch’ of microhabitat, invertebrate prey items are potentially continuously Floral Cognition: Comparative and Functional Perspectives 109 distributed (Benhamou, 1992). Only after some period of searching is a prey item located and then typically immediately attacked and consumed. Since the locations of prey are not signaled, a forager has only probabilistic information about the distribution of prey within a patch. If it searches and does not locate a prey item, this could be because prey items are currently at a low density, or it could be because the forager missed them. This can be contrasted with the analogous situation when foraging on flowers. If a forager visits a flower and does not find nectar, it can be certain that the flower does not contain nectar. While the profitability of a whole plant might need to be probabilistically estimated based on the yield from a subset of the flowers, at least the information gleaned from each flower is highly reliable. There are also differences between nectar and invertebrates in terms of the effects of the forager’s behaviour on the distribution of food remaining in a patch. A flower once visited by the forager will be reliably depleted, and so an unprofitable place to which to return for an extended period of time. After such time it will likely replenish and, unless visited by another forager, will again become a profitable place at which to forage. The mobile nature of invertebrate prey items, however, means that a point location at which an invertebrate prey item is located may not be reliably depleted for any length of time. Further, if the invertebrate prey are sparsely distributed, that point location in space may never contain another prey item again. Therefore, the different distributions of nectar and invertebrate prey mean that different foraging strategies may be required to maximize foraging efficiency. It also means that different information becomes available to a bird as it forages on either food source. These two factors combined may have selected for noisy miners to evolve two divergent cognitive foraging systems: one to support foraging on nectar and the other to support foraging on invertebrates. The other evolutionary solution to the problem of foraging on multiple resources with different distributions and different informational properties, is that a single generalist cognitive system could evolve that represents some optimal trade-off in efficiency between the two food types. Data collected in our lab suggest that the former outcome is the case. In the laboratory, noisy miners spontaneously avoid (after a delay of 5 minutes) feeders that they previously visited which contained food rewards, in favour of feeders that did not contain rewards (Sulikowski and Burke, 2007). This behaviour, termed “win-shifting” (as opposed to “win-staying”) or a “win-shift bias” is exhibited also by several other nectarivorous birds tested in the lab (Burke and Fulham, 2003; Cole et al., 1982; Wunderle and Martinez, 1987; although see also Sulikowski and Burke, 2011a), tested in the field (Healy and Hurly, 1995) and observed in the wild (Gill and Wolf, 1977; Kamil, 1978). Noisy miners exhibited this win-shift bias when rewarded with a sucrose solution (mimicking a nectar reward), but not when rewarded in an identical task with a mealworm. The most straightforward conclusion is that win-shifting is a nectar-specific behaviour that reflects a cognitive adaptation to efficiently exploit the depleting nature of flowers. 1 The term cognitive system is used here to indicate a collection of rules describing how the animal uses a subset of the information available in the world to make decisions in a particular context, such as foraging o