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Begging for a better future: how far can behavioral ecologists go without specifying mechanisms?

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Begging for a better future: how far can behavioral ecologists go without specifying mechanisms?
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  Begging for a better future: how far canbehavioral ecologists go without specifying mechanisms? Uri Grodzinski, a  Roi Dor, b and Arnon Lotem c a Department of Experimental Psychology, University of Cambridge,Downing Street, Cambridge CB2 3EB, UK, b Fuller Evolutionary Biology Program, Cornell Lab of Ornithology, Cornell University,Ithaca, NY 14850, USA, and c Department of Zoology, Tel-Aviv University, Ramat Aviv, Tel-Aviv 69978, Israel Mock et al.’s critical review of the ‘‘honest begging’’ literature iscertainly welcome and constructive. We agree that there aresome problems with Signal of Need (SoN) including its inter-actions with Signal of Quality (SoQ) (Lotem 1998), andthe fact that it makes opposing predictions for different fitness func-tions (Cotton et al. 1999) and ‘‘assumes away’’ the dynamicnature of parent–offspring interactions (Godfray and John-stone 2000). We are obviously pleased with the endorsement of the fuel gauge model (FGM;Grodzinski and Lotem, 2007)but feel that its presentation as a version of the Signaling of Hunger idea (SoH), that is, as an alternative to SoN, gives it a different interpretation than srcinally intended. The dis-tinction may look subtle but it is critical: In our view, the fielddoes not require another normative model but crucially re-quires mechanistic models connecting the theoretical terms‘‘need’’ and ‘‘quality’’ with biological reality. The FGM is there-fore not an alternative to SoN, but a mechanistic model ex-plaining how food deprivation can cause a gradual increase inneed (i.e., in the marginal fitness value of receiving extra re-sources). The first component of the FGM is that sated (full)offspring have a need level of zero simply because they are not receptive to being fed, so food cannot be converted into off-spring fitness. However, this food-receptivity component,termed ‘‘being ready for additional food’’ by Mock et al., isnot sufficient to explain further increases in begging with fooddeprivation (receptivity alone could be indicated by an all-or-none signal or cue). This is where the second component of the FGM becomes essential. The reason that an ‘‘almost empty’’ offspring is needier than a ‘‘half empty’’ offspring isthat although they may be equally ready to receive a meal, thealmost empty one is at greater risk of becoming completely empty, which might temporarily stop its ‘‘digestive engine’’converting food into growth (Grodzinski and Lotem 2007). Alternatively, ‘‘efficiency-based’’ models suggest that fullnessreduces digestive efficiency, providing a different functionalreason for why food-deprived offspring will gain more fitnessfrom being fed (Grodzinski and Lotem 2007;Wright et al. 2010). Importantly, specifying the alternative mechanismsthrough which SoN may work enables us to return to ultimatereasoning with relevant experimental results (Grodzinski et al.2009). If the justified criticism of being ‘‘content with SoN’’leads to this integrating approach, as we suggest, we are not really ‘‘expanding from signal of need,’’ but breaking it downto concrete examples that can be studied and understood at the mechanistic level. In contrast, using ‘‘hunger’’ or ‘‘fullness’’ without clarifying their relation to fitness might not take usmuch further than need or quality. We greatly sympathize with Mock et al.’s call to move beyondthe ‘‘hunger experiment’’ and the honest signaling preoccupa-tion but feel that expanding to SoH or SoQ may not be thebest way. In theory, begging should be adjusted in relation toboth differential costs (quality) and benefits (need), but off-spring must assess those through proximate factors, such asdigestive physiology, hormonal levels, competitive state, andpast experience. Understanding these mechanisms is necessary for decoding the message conveyed by begging and assessingthe extent to which begging is honest and parental response toit is adaptive. On the bright side, it seems that the field isalready moving in this direction with an increasing numberof studies into the genetic and phenotypic mechanisms of par-ent–offspring communication (e.g.,Bell 2008;Grodzinski et al. 2008;Dor and Lotem 2009,2010; Hinde et al. 2009;Wright  et al. 2010). We should perhaps recall that the honest-signalingrevolution was mainly a conceptual one. It provided a stablesolution for the problem of cheating, facilitating the use of normative models like those used for animal foraging to study animal communication. Now that behavioral ecologists gradu-ally stopped asking whether foraging is optimal and are insteadusing optimality as a working hypothesis for studying theevolution of behavioral mechanisms (recently reviewed by McNamara and Houston 2009), we can stop asking whetherbegging is honest as a goal in itself. Instead, we can use work-ing hypotheses about costly signaling and evolutionary stability (implying some general concept of honesty) to study themechanisms that make offspring begging and parental re-sponse to it adaptive. Key words:  animal communication, parent–offspring conflict,parental care, signaling.  Address correspondence to U. Grodzinski. E-mail: ug205@cam.ac.uk.Received 18 February 2011; accepted 20 April 2011.doi: 10.1093/beheco/arr076 REFERENCES Bell MBV. 2008. Strategic adjustment of begging effort by bandedmongoose pups. Proc R Soc Lond B Biol Sci. 275:1313–1319.Cotton PA, Wright J, Kacelnik A. 1999. Chick begging strategies inrelation to brood hierarchies and hatching asynchrony. Am Nat.153:412–420.Dor R, Lotem A. 2009. Heritability of nestling begging intensity in thehouse sparrow ( Passer domesticus  ). Evolution. 63:738–748.Dor R, Lotem A. 2010. Parental effort and response to nestling beg-ging in the house sparrow: repeatability, heritability and parent-offspring co-evolution. J Evol Biol. 23:1605–1612.Godfray HCJ, Johnstone RA. 2000. Begging and bleating: the evolu-tion of parent-offspring signalling. Philos Trans R Soc Lond B BiolSci. 355:1581–1591. Ó The Author 2011. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved.For permissions, please e-mail: journals.permissions@oup.com Commentaries on Invited Review  921   a t   C  am b r i   d  g e U ni  v  er  s i   t   y L i   b r  ar  y  onA  u g u s  t  2  3  ,2  0 1 1  b  eh  e c  o. ox f   or  d  j   o ur n al   s . or  gD  ownl   o a d  e d f  r  om   Grodzinski U, Erev I, Lotem A. 2008. Can hungry nestlings be trainedto reduce their begging? Behav Ecol. 19:116–125.Grodzinski U, Hauber ME, Lotem A. 2009. The role of feeding regu-larity and nestling digestive efficiency in parent-offspring commu-nication: an experimental test. Funct Ecol. 23:569–577.Grodzinski U, Lotem A. 2007. The adaptive value of parental responsive-ness to nestling begging. Proc R Soc Lond B Biol Sci. 274:2449–2456.Hinde CA, Buchanan KL, Kilner RM. 2009. Prenatal environmentaleffects match offspring begging to parental provisioning. Proc R Soc Lond B Biol Sci. 276:2787–2794.Lotem A, 1998. Higher levels of begging behavior by small nestlings:a case of a negatively correlated handicap. Isr J Zool. 44:29–45.McNamara JM, Houston AI. 2009. Integrating function and mecha-nism. Trends Ecol Evol. 24:670–675. Wright J, Karasov WH, Kazem AJN, Braga Goncalves I, McSwan E. 2010.Begging and digestive responses to differences in long-term andshort-termneedinnestlingpiedflycatchers.AnimBehav.80:517–525. 922 Behavioral Ecology    a t   C  am b r i   d  g e U ni  v  er  s i   t   y L i   b r  ar  y  onA  u g u s  t  2  3  ,2  0 1 1  b  eh  e c  o. ox f   or  d  j   o ur n al   s . or  gD  ownl   o a d  e d f  r  om 
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