Received 6 October 2014Received in revised form 11 February 2015Accepted 26 February 2015Available online 21 March 2015
Regime shifts in benthic invertebrates within coastal ecosystems threaten the survival of wading birds(Charadrii). Predicting how invertebrate regime shifts will affect wading birds allows conservation
2005) and can sometimes benet from alterations in the habitatsallowing species to colonise new areas (Herbert, 2001; Hewittet al., 2003). Changes in temperature (Beukema, 1990; Beukemaet al., 2009; Bhaud et al., 1995) and the impact of sewage outows(Alves et al., 2012) are examples of events that impair and benetinvertebrate populations respectively. Such regime shifts are likely
osystem and as a(Fernndezd as sentints, as in
and decreases in their populations have been linked to cin the prey biomass (Furness, 1993).
Regime shifts affecting coastal birds have been described inaddition to moderate population changes associated with the avail-ability of their preferred prey. In theWadden Sea (Netherlands), theloss of mussel beds has been linkedwith declines inmolluscivorousbirds and subsequent increases in worm-eating birds from growthin polychaete numbers (Piersma, 2007; van Roomen et al., 2012;van Roomen et al., 2005; Weijerman et al., 2005). The Wash in
Corresponding author. Tel.: +44 1202 965268.E-mail address: firstname.lastname@example.org (K.M. Bowgen).
Biological Conservation 186 (2015) 6068
Contents lists availab
.e limpact higher trophic levels within an ecosystem (Kraberg et al.,2011). Within marine and intertidal ecosystems, invertebratesexperience both incidences of population loss or range expansionto the potential detriment of other species (Weijerman et al.,
birds are used as indicators of the health of an ecconsequence many feeding areas are protected2005). In particular, wading birds are often useenvironmental change and indicators of pollutahttp://dx.doi.org/10.1016/j.biocon.2015.02.0320006-3207/ 2015 The Authors. Published by Elsevier Ltd.This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).et al.,nels ofcreaseshanges1. Introduction
With an increasing risk of rapidly changing environmentalconditions and extreme weather events, there is a high probabilityof the size of individuals and the magnitude and diversity of eco-logical populations shifting dramatically. These regime shiftsmark the rapid change between different system states and can
to impact upon wading birds (Charadrii) due to the different typesand size of invertebrates that each species forages upon (seeTable 4 and Goss-Custard et al., 2006b). Waders are dependenton specic size categories of invertebrates, with some moregeneralist than others (greater numbers of species and sizes eaten),and any shift in prey species abundance or size range could cause aloss of available food (Cayford, 1993). At the top of the food chainEstuarine systemsIndividual-based modelsShorebirdsSurvivalmanagement and mitigation measures to be implemented, including protection of terrestrial feedingareas. An individual-based model was used to investigate the impact of regime shifts on wading birdsthrough their prey (marine worms and bivalves) in the estuarine system Poole Harbour, (UK). The modelpredicted the number of curlew (Numenius arquata), oystercatcher (Haematopus ostralegus), black-tailedgodwit (Limosa limosa), redshank (Tringa totanus) and dunlin (Calidris alpina) supported in the Harbourduring the non-breeding season (autumn and winter months). The most dramatic declines in birdnumbers were for regime shifts that reduced the abundance of the largest invertebrates, particularlymarine worms. The least adaptable bird species (those with the most restrictive diets) were unable tocompensate by consuming other prey. Generally, as birds adapt to changes by switching to alternativeprey species and size classes, changes in invertebrate size and species distribution do not necessarily affectthe number of birds that the Harbour can support. Our predictions reveal aweakness in using birds as indi-cators of site health and invertebrate regime shifts. Differences in bird populations would not necessarilybe detected by standard survey methods until extreme changes in invertebrate communities hadoccurred, potentially beyond the point at which these changes could be reversed. Therefore, populationsize of wading birds should not be used in isolation when assessing the conservation status of coastal sites. 2015 The Authors. Published by Elsevier Ltd. This is anopenaccess article under the CCBY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).Article history:Predicting the effect of invertebrate regimInsights from Poole Harbour, UK
Katharine M. Bowgen , Richard A. Stillman, Roger J.Centre for Conservation Ecology and Environmental Science, Department of Life and EnvBH12 5BB, UK
a r t i c l e i n f o a b s t r a c t
journal homepage: wwwshifts on wading birds:
Herbertmental Sciences, Faculty of Science and Technology, Bournemouth University, Dorset
le at ScienceDirect
sevier .com/locate /b iocon
ered in this study due to being present in large, though notinternationally important numbers (Holt et al., 2012) and taking
values listed in the original paper and then run several times toconrm that the predictions in the original paper were reproduced.
l Conthe UK has also seen a shift to more worm-eating waders alongsidedeclines in bivalve eating waders after losses in bivalve populations(Atkinson et al., 2010). In addition to anthropogenic causes, coldwinters in the late 1980s reduced invertebrate stocks in theWadden Sea (Beukema, 1990, 1992) and during the 1990s increasesin salinity led to reduction in benthic vegetation in a costal lagoonin western Denmark that decreased bird numbers (Petersen et al.,2008). A regime shift was seen in Alaska where piscivorous birdsreduced after an upwards temperature shift changed sh com-position and the Exxon Valez oil spill put extra pressures on thesystem (Agler et al., 1999). In the mid-2000s large polychaetesincreased near sewage outlets in the Tejo estuary, Portugal increas-ing the numbers of birds that could be supported on these areas(Alves et al., 2012).
In general the specic types of shifts thatmay affectwading birdsinclude the loss of individuals at the lower and upper ends of preysize range (Kraberg et al., 2011), removal of entire prey species orfamily (Atkinson et al., 2010; Strasser et al., 2001) and increases innew or formerly under represented prey (Caldow et al., 2007).Increases in shing for molluscs and bait-collecting for marineworms will also remove the larger sizes of invertebrates and olderbreeding stock and thus potentially reduce the overall populationnumbers (Olive, 1993). In other cases, pollution, toxicity and tem-perature uctuations in an environment can impinge on recruit-ment and cause a loss in the smaller sizes of invertebrates; thoughin the short term it can add nutrients to a system and increase inver-tebrate numbers (Alves et al., 2012; Olive and Cadnam, 1990). Thisinvestigation becomes important when considering the resilienceof a system to such changes, as it has been proposed that to reducethe risk of regime shifts we should investigate gradual changes thatcould potentially lead to catastrophic shifts (Folke et al., 2004).
Understanding how animals might respond to prey regimeshifts can be achieved through eld experiments and observationsbut this can be time consuming and often takes several seasons ofeld work before useful management conclusions can be madeconcerning their impacts on both waders and their habitats(Deyoung et al., 2008; Goss-Custard and Stillman, 2008).Modelling provides an attractive alternative and, in particular,individual-based models (IBMs) have been shown to produce accu-rate predictions that can advise conservation decision making(Goss-Custard et al., 2006a; Grimm and Railsback, 2005; Grimmet al., 1999; Stillman and Goss-Custard, 2010; Stillman et al.,2007). IBMs follow tness-maximising procedures to allowindividual model birds to act independently over the course of aseason and provide an ecosystem view that is closer to reality thananalytical models such as differential-equation or matrix models(Stillman, 2008). They can also be manipulated quickly to provideanswers to a range of conservation questions from only a singleseason of invertebrate data collection.
In this paper we will explore how regime shifts in invertebratepopulations can affect the survival of ve species of wading birdsin Poole Harbour, UK using a validated IBM of the site. We investi-gated the following types of regime shift:
(i) complete loss of a prey species,(ii) directional (loss from either smaller or larger ends of prey
size classes),(iii) divergent and convergent (bi-directional loss of prey size
We predict that birds will respond to invertebrate regime shiftsthrough alterations to the range of prey species and sizes includedin their diets. We also discuss the consequences of regime shifts for
K.M. Bowgen et al. / Biologicathe numbers of birds supported by the site. From our hypothesisedoutcomes we expect to nd that when prey size ranges arereduced, birds will switch to less preferred species which will (a)Many IBMs are developed for a single purpose, such as tounderstand one environmental change event. In this paper, weinto account their regional importance.
2.2. The model
We used a pre-existing model of Poole Harbour (Durell et al.,2006) designed in MORPH (Stillman, 2008) which predicts thenumbers of birds supported at the end of the non-breeding seasondue to the closed nature of the mode