Herbivore search behaviour drives associational plant refuge

doi:10.1016/j.actao.2015.05.004

Acta Oecologica

Volume 67, August 2015, Pages 1-7

https://doi.org/10.1016/j.actao.2015.05.004 Get rights and content

Highlights

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Plants can gain refuge from herbivores by association with plant neighbours.
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How do refuge-providing neighbours alter foraging behaviour at the patch-level?
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Swamp wallabies reduced search time in patches with manipulated plant neighbours.
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Palatable seedlings with manipulated neighbours escaped herbivory for longer.
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Palatable plants may persist because neighbours influence patch foraging behaviours.

Abstract

Herbivore foraging decisions leading to consumption of a plant are complex and multi-faceted, shaped both by the plant itself and by its neighbours. Associational plant refuge arises when neighbours reduce focal plant susceptibility to herbivory. The specific foraging behaviours generating refuge patterns have rarely been examined in free-ranging systems, yet these are key to understanding why such refuge works or fails. We aimed to integrate herbivore foraging and associational plant refuge theories by linking foraging decisions directly to browsing outcomes on focal plants and their neighbours. We tested whether obstructive, unpalatable neighbours reduce the number of patch visits and/or interrupt searching, leading to associational refuge of focal plants. We compared visits by and behaviours of free-ranging mammalian browsers, swamp wallabies (Wallabia bicolor), in control and manipulated plant patches using cameras. Patches (7 m²) comprised a central focal plant (palatable native tree seedling, Eucalyptus pilularis) with neighbours of either existing or manipulated vegetation (unpalatable native daisy, Coronidium elatum). Wallabies made fewer visits to control than manipulated patches, but always browsed the focal plant during the first visit to a control patch. In contrast, wallabies often visited manipulated patches multiple times before browsing the focal plant. These ‘futile’ visits were both shorter and involved less searching time than visits when the focal plant was browsed. Focal plants escaped browsing for longer in manipulated than in control patches, and although none had escaped browsing after one year, survival was significantly greater in manipulated patches. We demonstrate that reduced investment in searching during visits to manipulated patches drove the associational plant refuge, but this refuge was eventually surmountable. Understanding the behaviours underpinning refuges allows better prediction of outcomes, and explains why refuge can collapse. By shaping foraging behaviour in patches, neighbouring vegetation can increase the probability that palatable plants persist despite high herbivore pressure.

Introduction

From the herbivore perspective, plants occur in a landscape of vegetation patches varying in quality amongst an inedible matrix. An underlying assumption of foraging theory is that animals forage to optimize their net energy intake per unit time (MacArthur and Pianka, 1966) and for herbivores, such foraging involves searching among and within patches to find and consume plants that provide maximum net benefit. As herbivores deplete the food resources in a patch, returns diminish; and patch quitting is predicted when the cost of staying is greater than the cost of travelling to the next exploitable patch (marginal value theorem, Charnov, 1976). Since the plant neighbourhood affects the cost-to-gain ratio of foraging in a patch, foraging decisions by herbivores are influenced not only by any particular plant's own chemical and physical characteristics, but also those of its neighbours, and of plants in other patches (Stephens and Krebs, 1986). Neighbours can change the perceived profitability of a patch, and therefore how much time herbivores invest in searching for and consuming patch resources (Stephens, 2008).

Where neighbouring plants protect focal plants from herbivory, the phenomenon is termed associational plant refuge (Atsatt and O'Dowd, 1976, Tahvanainen and Root, 1972). There are several mechanisms of associational plant refuge from vertebrate herbivores. Refuge can be generated when focal plants occur in patches of unpalatable or defended neighbours and herbivores select predominantly between rather than within patches (repellent plant defence, Atsatt and O'Dowd, 1976, McNaughton, 1978). This is the most commonly documented mechanism of associational plant refuge from vertebrate herbivory (Milchunas and Noy-Meir, 2002). Alternatively, refuge may occur when neighbours are more palatable or undefended, so that they are consumed preferentially and thus allow focal plants to escape herbivores selecting between plants within patches (attractant-decoy or neighbour contrast defence; Alm Bergvall et al., 2006, Atsatt and O'Dowd, 1976). Neighbours can also protect a focal plant from herbivory by reducing its apparency, and therefore its probability of detection by herbivores (Castagneyrol et al., 2013, Hambäck et al., 2000, Miller et al., 2007).

Associational plant refuges arise, therefore, from foraging decisions made by herbivores in relation to plant patches and individual plants within them. Most studies of associational plant refuge, however, focus on the plant perspective, quantifying outcomes of herbivory such as plant survival, size or damage, or depletion of artificial food in patches of differing quality while inferring the underlying foraging decisions from these outcomes. Baraza et al. (2006), for example, demonstrated that shrubs with greater physical defence (spines) and lower relative palatability provided better protection to saplings from ungulates. From this, they inferred that ungulates selected predominantly between patches rather than between plants within patches – the repellent plant mechanism of associational plant refuge. This inferential approach may tell us the scale of selection dominating herbivore foraging decisions, but we cannot determine how behaviours during visits to patches change as a result of the neighbouring vegetation.

We are aware of only two studies that have directly quantified the behaviour of vertebrate herbivores coupled with associational refuge, and these have assessed animals in captivity. Captive bred fallow deer Dama dama showed no difference in the amount of time spent or the number of individuals visiting patches of different quality, but ate less high tannin (low quality) pellets in patches dominated by low tannin (high quality) pellets – i.e. associational refuge by neighbour contrast defence (Alm Bergvall et al., 2006). In contrast, captive pademelons Thylogale billarierii spent significantly less total time and time consuming neighbouring plants in constructed patches of low quality (herbicided) than high quality (grass), providing refuge for eucalypt seedlings via the repellent plant mechanism (Miller et al., 2009).

Our main aim was to compare the browsing behaviour of free-ranging herbivores in response to a focal plant and its neighbours in vegetation patches, and to quantify the browsing outcomes. In doing so, we unite concepts of foraging theory (the animal perspective) with associational refuge theory (the plant perspective), to provide a mechanistic understanding of the differences in foraging outcomes for focal plants arising from behavioural responses to plant neighbours.

Our study system was a partially degraded area of a national park lacking much of its native eucalypt overstorey, in which native Eucalyptus pilularis tree seedlings were planted as part of restoration efforts. In Stutz et al. (2015), we found that browsing of these highly palatable eucalypt seedlings by free-ranging swamp wallabies Wallabia bicolor was delayed in control vegetation patches with higher cover of understorey vegetation and fewer browsed plant species (as associational refuge) and lower canopy cover (influencing habitat selection). Here, we manipulated vegetation patches with the aim of influencing wallaby foraging behaviour to enhance the associational plant refuge. We used field cameras to directly observe the browsing behaviour of wallabies in control and manipulated vegetation patches with E. pilularis seedlings as the focal plants. Observing behaviour allowed us to directly quantify and elucidate the foraging decisions underpinning any associational plant effects.

Manipulated neighbourhoods were predicted to lower the patch value in two ways; (1) by reducing the perceived net patch quality as a food source, and (2) by masking visual and olfactory cues from the focal plant, thus decreasing the cue-to-noise ratio (Carthey et al., 2011, Schmidt et al., 2010) and so reducing the capacity of wallabies to detect the focal plant. We therefore predicted that refuge in manipulated patches would be driven either by fewer visits to patches or by reduced time spent in a patch once there, specifically with less time spent searching. We expected the former if swamp wallabies perceive patch quality at a distance (deciding to avoid manipulated patches more often), and the latter if they assess patch quality once at a patch (deciding to leave manipulated patches early). Alternatively, if manipulated neighbours did not change the patch value, we predicted that refuge in manipulated patches would be driven by reduced search efficiency in patches; i.e. obstruction by neighbours leading to lower frequency of finding and consuming focal plants for the same absolute visit duration or search time.

Section snippets

Study site

Our study site was a 50 ha area in the western part of Booderee National Park (BNP), Jervis Bay Territory, on the south coast of New South Wales, Australia (35°08″30″S, 150°39″10″E). The area was reclaimed from pine Pinus radiata plantation more than 20 years ago, with current vegetation comprising a mosaic of dense bracken fern Pteridium esculentum, shortly-cropped introduced grasses, sedge-like herbs Lomandra spp. and small scrubby trees Monotoca elliptica, with a sparse overstorey of remnant

Herbivore behavioural response to patch treatments

Motion-triggered cameras recorded 78 visits in total over the five-week period following planting. Swamp wallabies accounted for most of these (51 visits) and were responsible for all visits where the focal plant was browsed. European rabbits, eastern grey kangaroos and red-necked wallabies made the remaining visits. Of the visits by swamp wallabies, 42 occurred before or during browsing of the focal plant. Both swamp wallabies and rabbits browsed C. elatum in manipulated patches (during 14 and

Discussion

Our study demonstrated that the presence of less palatable neighbours provided refuge for focal plants by altering the foraging behaviour of a generalist browser in food patches. Swamp wallabies, the sole browsers of the focal eucalypt seedlings, visited manipulated patches more often than control patches. However most of the visits to manipulated patches were ‘futile’. That is, the visits were relatively short, involved less time spent searching within the patch, little if any browsing of the

Author contributions

All authors designed the experiment; RSS conducted the fieldwork; RSS and CM analysed the data; RSS prepared the manuscript; all authors gave editorial comments on the draft and approved the final manuscript for publication.

Acknowledgements

Booderee National Park provided housing and financial support for this project. We thank Booderee Botanic Gardens, particularly Stig Pedersen, for collecting seeds and raising the plants used. The University of Sydney Animal Ethics Committee approved all procedures (L04/2-2012/3/5696). All research was conducted under a National Parks Permit (BDR12/00001).

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Original articleHerbivore search behaviour drives associational plant refuge

Highlights

Abstract

Introduction

Section snippets

Study site

Herbivore behavioural response to patch treatments

Discussion

Author contributions

Acknowledgements

Theor. Popul. Biol.

Acta Oecol

Trends Ecol. Evol.

Trends Ecol. Evol.

Survival Analysis Using SAS: a Practical Guide

Associational effects of plant defences in relation to within- and between-patch food choice by a mammalian herbivore: neighbour contrast susceptibility and defence

Oecologia

The effect of spatial scale on plant associational defences against mammalian herbivores

Ecoscience

Plant defense guilds

Science

Conditional outcomes in plant–herbivore interactions: neighbours matter

Oikos

Roles of the volatile terpene, 1,8-cineole, in plant–herbivore interactions: a foraging odor cue as well as a toxin?

Oecologia

Transient facilitative effects of heather on Scots pine along a grazing disturbance gradient in Scottish moorland

J. Ecol.

Negotiating a noisy, information-rich environment in search of cryptic prey: olfactory predators need patchiness in prey cues

J. Anim. Ecol.

Plant apparency, an overlooked driver of associational resistance to insect herbivory

J. Ecol.

Mycophagy among Australian mammals

Aust. J. Ecol.

Foraging decisions of bison for rapid energy gains can explain the relative risk to neighboring plants in complex swards

Ecology

Survival analysis: overview of parametric, nonparametric and semiparametric approaches and new developments

SAS Glob. Forum

Response of tree seedlings to the abiotic heterogeneity generated by nurse shrubs: an experimental approach at different scales

Ecography

Associational resistance: insect damage to purple loosestrife reduced in thickets of sweet gale

Ecology

Herbivore avoidance by association: vole and hare utilization of woody plants

Oikos

Ecology of the swamp wallaby (Wallabia bicolor) in northeastern New-South-Wales .1

Diet. Wildl. Res.

Dynamics and Adaptiveness of Grouping in Macropods, Kangaroos, Wallabies and Rat-kangaroos

Original article
Herbivore search behaviour drives associational plant refuge