The bill of evolution : trophic adaptations in anseriform birds Kurk, C.D.

The bill of evolution : trophic adaptations in anseriform birds

Kurk, C.D.

Citation

Kurk, C. D. (2008, May 27). The bill of evolution : trophic adaptations in anseriform birds. Retrieved from https://hdl.handle.net/1887/12867

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Jaw mu

C

uscle size fee

Chapte

e in aqua ding wild

er 3

tic and t dfowl

errestria



al

40 Wi ite an suc fee wh ter fun We ma bu gro jaw jaw the Th co ter an As siz res mo sam the dif for

ildfowl exploit m ems to terrestrial

d especially in fil ch movements m eders. To investig hich species forag rrestrial feeders b nctionally differe e found that tota ass in both troph t total jaw muscl oups contribute t w, the openers of w) are larger in aq

e two remaining e jaw opener mu mpared to a sam rrestrial feeders.

seriform birds th the bill of aquat e of the jaw ope sisting forces in a oment of inertia.

me, having a larg e jaw opener mu fference in bill siz r the larger resist

any trophic reso grazing. Aquatic ter-feeding spec may generate resi gate possible diff ge we categorize based on literatu ent jaw muscle gr al jaw muscle ma ic groups. The ex le mass are 1.5 ti to the difference f the upper jaw a quatic than in ter jaw-closing musc uscle groups of aq mple of non-anser

The pterygoid m han in both anser ic feeders is large ner muscles cann an aquatic enviro

If angular accele ger bill also requi

scles is estimate ze and there is no ting forces in an a

Summary

urces ranging fro feeding birds us ies with fast repe isting forces that ferences in muscl d a number of an ure data and dete

roups.

ss scales negativ xponent is the sa imes higher in aq in total jaw mus and the pterygoid

rrestrial feeding cle groups.

quatic feeding an riform birds, whic muscles, however

riform groups.

er than in terrest not be simply exp onment. Longer a

eration and densi res larger jaw op d to be approxim o indication that aquatic environm

om filter-feeding ually feed with t etitive bill movem t are much larger

le size related to nseriform species ermined the mas

ely allometric wi me for aquatic a quatic feeding spe scle mass. The op d muscles (closer species. No diffe

natids were also h ch did not differ

, were much larg

trial feeders the d plained as an ada

nd wider bills res ity of the environ pener muscles. Th mately sufficient t muscle size incre ment.

Cha

small aquatic foo heir bills submer ment. Under wate r than for terrestr

the environmen s as aquatic or s of several

th respect to bod nd terrestrial fee ecies. Not all mu peners of the low rs of upper and lo rences are found

heavier when from anseriform ger in the non-

difference in rela aptation to large

sult in a larger nment remain the he difference in s to compensate fo eases to compens

apter 3

od ged er rial

t in

dy eders,

scle wer

ower d for

ative

e size of or the sate

Jaw

Wi fee ch ha of mo to the 19 tha (ch cyc tro ter filt res No ma jaw Fo Th pa the esp for mu al., tha of firm off for the inv cat on filt mo be

w muscle size

ildfowl (ducks, ge eding small aqua

aracterized by di s to be secured b the jaw apparatu outh to transport generate a wate e roof of the mou

89; Zweers et al.

an in filter-feede hapter 2 and cha cle in filter-feede ophic morphology

rrestrial grazing h ter-feeding perfo

sults in a low inta ot only bill and to ay be expected to ws open and clos

rces acting on a m e reaction forces rt of the beak plu e beak. The force pecially since the rces are much les uch lower rate, u

, 2003). One may an in terrestrial g jaw closers is les mly in the bill so f, rather than be rces that elevate e other hand aqu vestigate possible tegorized a numb literature data o ter-feeders but a olluscs, fish, etc.

tween the two g

eese and swans) tic food items to fferent types of f by and transporte us. Terrestrial gra t vegetation, whi

rflow through th uth and acts as a , 1977). Similarly rs, resulting theo pter 3), but a larg ers (Van der Leeu

y, in turn, are ref have a low perfor ormance the ineff ake rate (Van der ongue morpholog o be associated w

e at a high rate, moving bill unde s consists of the f us the force requ es generated dur e bill surface area

ss or absent in te p to maximal 2 H y therefore expec grazers. Whether ss clear. In grazing

that when the he pulled out of the

the upper bill, w uatic feeders hav

e differences in m ber of anseriform on their foraging

lso included spec A regression ana roups.

Introduction exploit many tro

terrestrial grazin food as well as a ed through the b azers, for instanc le filter-feeders r he mouth using th piston (Van der y, the bill is shorte oretically in highe

ger volume pump uw et al., 2003 an

flected in foragin rmance for filter- ficient transport r Leeuw et al., 20 gy may be related with resource use up to a frequenc r water are drag force required to uired to accelerat ing bill movemen a of filter-feeders errestrial grazers, Hz for the barnac ct larger opening r aquatic versus t g a forceful closu ead and neck are e bill. The backwa which is moveable e to push water o muscle size betwe m species as aqua

habits. The aqua cies feeding on la alysis was used to n

ophic resources ra ng. These two ext different environ bill. Both require a ce, use short spin

require a bold lin heir tongue, whic Leeuw et al., 200 er and narrower er bite and pullin ped through the nd chapter 6). Th ng performance. S

-feeding, while in of grazed vegeta 003; chapter 5, ch d to resource use e as well. In filter y of 20 Hz (Koolo force plus accele o accelerate the m

te an added mass nts in water may s is relatively larg which also open le goose on shor g muscles in aqua errestrial feeding ure of the bill is n e drawn backwar ard movement of e with respect to out off their beak een aquatic and t atic feeder or terr atic feeding group arger items such o evaluate differe

anging from filte tremes are nment in which f a specific morpho

es on the roof of ning of the oral ca

ch is pressed aga 03; Kooloos et al.

in terrestrial gra g forces in grazer beak per movem hese differences i Species specialize n species with a h ation through the hapter 6).

e but jaw muscle r-feeding species oos et al., 1989).

eration reaction f mass of the movi

s of water movin be of importanc ge. Such resisting n and close the bi t pasture (Duran atic feeding speci g also affects the ecessary to hold rds, the grass will f the head results

the neurocraniu k during closing.

terrestrial feeder restrial grazer ba p was not limited as water plants, ences in muscle s

41 r- food

ology f the avity inst .,

zers rs ment

in ed in high e bill

size the forces.

ng g with e;

ill at a t et es e size

grass snap s in um. On

To rs we ased d to size

42 As 3.1 al., Ma Mo 20 Co co fro Ge jaw de wh ad the 19 To ow an To als ran

signment of spec 1 (Austin et al., 19

, 1995; Hohman allory and Metz, owbray et al., 20 02; Rylander and omplete specimen

mmercial supplie om one side of th ermany). When ju w muscles were s

pressors (opener hich act as opene ductors originati ese muscle comp

74) muscles with increase our dat wn data set from alyses are given allow a compari so used previousl nging from 12 to

Ma cies to trophic gro 998; Drilling et a and Lee, 2001; Ja 1999; Mowbray, 02; Petersen et a d Bolen, 1974; Sa

n or loose heads er. After determi he head and weig

ust the head was subdivided into fi rs) of the mandib ers of the upper j

ng on the quadra plexes encompas h similar lines of a

ta-set we include the study by Goo in table 3.1.

son between the ly published data 12000 g (Burger

aterialandMet oup are based on l., 2002; Dubowy ames and Thomp 1999; Mowbray al., 1994; Reed et vard et al., 1998 of 34 species of ning body mass ( ghed (mg) on a ba

available body m ive groups: the a ble, the protracto aw, and two grou ate) that are able ses several distin action were take ed some of the sp

odman and Fishe e data on Anserif a on jaw muscle m

, 1978; van der M thods

n literature data y, 1996; Dugger e pson, 2001; Johns , 2002; Mowbray t al., 1998; Rober

).

Anseriformes we (g) the jaw muscl alance (Sartorius mass was taken f dductors (closers ors of the quadra

ups (the pterygoi e to close both ja nct muscles (figur n to form a single pecies that were er (1962). All spec formes and non-a mass of 16 bird sp Meij and Bout, 20

Cha

and are listed in et al., 1994; Eadie son, 1995; Kear, y et al., 2000;

rtson and Savard,

ere obtained from es were dissecte , H51, Göttingen rom the literatur s) of the mandibl te and pterygoid id muscles and th ws. Although eac re 3.1 and Zweer

e functional unit not already in ou cies used in the anseriform birds

pecies with body 004).

apter 3

table e et

2005;

,

m a ed

, re. The

le, the d,

he ch of

s, . ur

we y mass

Table3.1. Jaw muscle weights of wildfowl species examined. Species Common name trophic group body mass (g)adductor muscles (mg) quadrate adductor muscles (mg) pterygoid muscles (mg)protractor muscles (mg)

depressor muscles (mg) Anasspecularis Spectacled duck aquatic 1134.01298.6426.5 694.5227.11091.5 Anashottentota Hottentot teal aquatic 200.0223.669.7 116.556.1268.7 Anascarolinensis*Green-winged teal aquatic 350.0291.067.0 128.097.0316.0 Anasplatyrhynchos Mallardaquatic 1206.01375.8404.1 641.9377.11757.4 AnasrhynchotisAustralian shoveler aquatic 320.0267.387.3 168.460.6293.5 Anasclypeata*Northern shoveler aquatic 735.0254.093.0 172.0154.0479.0 AnasformosaBaikal teal aquatic 320.0481.1117.6 228.9105.8432.4 AnasbahamensisWhite-cheeked pintail aquatic 440.0469.7127.4 165.099.9435.1 AnasamericanaAmerican wigeon terrestrial 740.0439.4134.1 205.183.9245.9 Aythyaaffinis*Lesser scaup aquatic 825.0498.0128.0 279.0193.0637.0 Aythyavalisneria*Canvasback aquatic 1178.0932.0244.0 529.0414.01458.0 Aythyanyroca Ferrugineous duck aquatic 520.0487.9104.3 192.778.3448.5 Anseranser Greylag goose terrestrial 4204.03919.2839.3 1762.2430.01233.1 Anserindicus juv Bar-headed goose terrestrial 1140.0928.6339.2 545.3122.8411.7 Ansererythropus Lesser white-fronted goose terrestrial 1640.0909.9264.5 422.7106.9372.3 Ansercaerulescens Snow goose terrestrial 3900.03808.5915.8 1462.9540.21455.3 Ansercygnoides Swan goose terrestrial 2800.02752.0796.6 1567.4303.41025.2 Ansercanagicus juv Emperor goose terrestrial 1060.01231.4308.6 596.9151.7539.6 Brantacanadensis Canada goose terrestrial 3480.02388.5550.4 743.6236.8617.5 Brantaberniclanigricans* Brent goose terrestrial 1424.0739.0145.0 244.0124.0215.0 Brantaruficollis Red-breasted goose terrestrial 920.0470.1110.4 150.035.9196.1 Brantaleucopsis Barnacle goose terrestrial1850.0709.9255.2 292.190.7420.2

Species Common name trophic group body mass (g)adductor muscles (mg) quadrate adductor muscles (mg) pterygoid muscles (mg)protractor muscles (mg)

depressor muscles (mg) Chenonettajubata Maned duckterrestrial 500.0387.598.8 144.348.4146.0 Neochenjubatus Orinoco goose terrestrial 1350.0793.9241.1 254.983.7311.5 Alopochenaegypticus Egyptian goose terrestrial1880.01271.3324.4 558.9163.8791.0 Chloephagahybrida*Kelp goose terrestrial 2324.0791.0266.0 486.0174.0441.0 ChloephagapoliocephalaAshy-headed goose terrestrial 720.0348.7146.7 173.141.0172.0 Bucephalaclangula*Common goldeneye aquatic 906.0573.0130.0 278.0168.0931.0 Clangulahyemalis*Long-tailed duck aquatic 725.0565.0136.0 286.0141.0786.0 DendrocygnaautumnalisBlack-bellied whistling- duck terrestrial 620.0823.9195.7 384.9179.9516.7 DendrocygnaviduataWhite-faced whistling- duck aquatic 480.0815.3202.6 392.7139.2491.9 DendrocygnaeytoniPlumed whistling-duck terrestrial 780.0918.5251.2 359.4125471.1 DendrocygnabicolorFulvous whistling-duck aquatic 600.01211.3234.4 576.2186.6619.6 Melanittaperspicillata*Surf scoter aquatic 950.01226.0310.0 556.0255.01023.0 Lophodytuscucullatus*Hooded merganser aquatic 610.0477.078.0 317.072.0355.0 Mergusmerganser*Common merganseraquatic 1400.01311.0217.0 851.0202.0550.0 TachyerespteneresFlightless steamer- duck aquatic 2620.02587.8830.8 1057.1380.41606.6 TadornacanaSouth-african shelduck aquatic 1660.01179.8318.7 444.2148.9870.3 TadornaferrugineaRuddy shelduckaquatic 1460.0724.0249.0 376.8147.8649.6 CygnusolorMute swan aquatic 6780.03768.31213.8 1850.7579.12570.2 CygnusbewickiBewick’s swan aquatic 5100.03463.21221.1 1858.4900.22915.9 CygnusatratusBlack swan aquatic 4880.02297.3599.3 985.3428.41354.3 NettapeposacaRosy-billed pochard aquatic 910.01163.4260.0 546.7233.9794.6 NettarufinaRed-crested pochard aquatic 1179.0744.2226.4 405.1216.7685.1

Species Common name trophic group body mass (g)adductor muscles (mg) quadrate adductor muscles (mg) pterygoid muscles (mg)protractor muscles (mg)

depressor muscles (mg) Marmaronetta angustirostrisMarbled teal aquatic 480.0452.6114.9 228.6114.3461.7 Non-anseriforms PaddaoryzivoraJava sparrow 30.485.715.8 86.34.123.6 CarduelischlorisGreenfinch 28.3138.721.1 89.510.533.7 MycerobasaffinisCollared grosbeak 70.0322.423.8 212.914.647.1 SerinusmozambicusYellow-fronted canary 12.039.46.9 26.85.19.5 CalidriscanutusKnot 130.941.423.7 54.311.349.0 ColumbapalumbusWoodpigeon 368.566.133.4 104.422.483.1 EmberizacitrinellaYellowhammer 28.947.516.2 43.54.014.1 EuplectusaferYellow-crowned bishop 15.036.88.3 28.62.78.1 FulicaatraEurasian coot 450.1266.569.2 233.230.5142.1 LarusridibundusBlack-headed gull 189.1390.0120.7 385.535.5161.1 ParusmajorGreat tit 15.224.33.6 20.31.87.6 PasserdomesticusHouse sparrow 27.094.622.6 58.011.241.6 PhalacrocoraxafricanusReed cormorant 756.02076.0168.0 896.0232.0348.0 RheaamericanaGreater rhea12500.03600.0600.0 3200.0500.02000.0 SicalisflaveolaSaffron finch 25.140.711.7 48.02.712.4 ViduachalybeataVillage indigobird 11.915.44.9 12.21.615.5 * From Goodman and Fisher (1962)

Q Pa AMP Figure3.1. Bones of the skull (middle figure) and work lines of individual jaw muscles, dotted lines indicate that (part of) a muscle runs behind other structures. Muscle names according to Zweers (1974). A: Skull adductor muscles: ACL, ARM and PS B: Protractor muscles: PPt and PQ C: Quadrate adductors: AMP, AEP, PPr D: Pterygoid muscles: PVL, PVM, PDL, PDM D: Depressors: DGP, DMT and DCM ACL: musculus adductor mandibulae externus pars caudolateralis, AEP: musculus adductor mandibulae externus profundus, AMP: musculus adductor mandibulae posterior, ARM: musculus adductor mandibulae externus pars rostromedialis, DCM: musculus depressor mandibulae, DGP: musculus depressor mandibulae grandis pyramidalis, DMT: musculus depressor mandibulae triangularis, J: jugal, Mn: mandible, O: orbit, Pa: palatine, PDL: musculus pterygoideus dorsalis, lateralis, PDM: musculus pterygoideus dorsalis medialis, PPr: musculus pseudotemporalis profundus, PPt: musculus protractor pterygoidei, PQ: musculus protractor quadrati, Pr.AP: processus angularis posterior, Pr.C: processus coronoideus, Pr.OQ: processus orbitalis quadrati, Pr.PO: processus postorbitalis, PS: musculus pseudotemporalis superficialis, Pt: pterygoid, PVL: musculus pterygoideus ventralis lateralis, PVM: musculus pterygoideus ventralis medialis, Q: quadrate. DCM

DGP DMTPVL PDMPDLPVM

Q PtJ

Pr. OQPr. PO Pr. CMn

ARM PS

ACL

A PPtPQ

B C PPr AEP

D E

Pr. AP

Jaw Da

 All in ma the Ind bra un 19 Ph an

Th in of bo an rel the mu the ma ter To mu Te ad rel an the mu int (de Th

w muscle size ataanalysis

data were log tr SPSS 12.0 (SPSS I ajor axis routine e algorithms dev dependent contr anch lengths set dergone adaptiv 99).

ylogenetic hypot d Donne-Goussé

e data on specie table 3.1. The log each functional m oth aquatic feede

alysis of the tota lationship is not d e two groups of a uscle mass, altho e intercepts do d ass total jaw mus rrestrial feeding a

determine whic uscle mass betwe

rrestrial and aqu ductor muscles ( lative to body ma

d openers of the e adductor musc uscle group are s tercepts are diffe epressors) are ap e pterygoid musc

ransformed to ob Inc. Chicago, IL, U (S)MATR (v1) (Fa eloped by Warto asts were calcula to unit length, as ve radiations thro theses were base é et al. (2002).

s body mass and g-transformed da muscle group (fig rs (n = 27) and te al jaw muscle mas different for the anseriforms is 0.8 ough the 95% con differ significantly scle mass is on av anseriforms, but h functional mus een the two trop atic feeders have table 3.2). Jaw cl ass in aquatic and e upper or lower j

le groups the slo tatistically simila erent. Both the op pproximately 2 tim

cles are on avera

btain normality. B USA). For the ana alster et al., 2003 on and Weber (20

ated with Compa s has been recom ough the occupat

ed on studies by

Results

weights of indiv ata of total jaw m gure 3.1) are all h errestrial grazers ss and body mass two trophic grou 873 and suggests nfidence interval y (p = 0.000; figur verage 1.5 times there is a large o scle groups contr

hic groups each e similar slopes a losing muscles th d terrestrial feed jaw, however, dif pes for the open r but for the jaw peners of the up mes larger in aqu age 1.4 times hea

Basic statistical te alysis of muscle d

) was used. This 002). 

re v4.6b (Martin mmended for clad

tion of diverse nic Livezey (1991, 19

idual groups of ja muscle mass (1-si

highly correlated (n = 18; all p = 0 s shows that the ups (p = 0.072). T s negative allome includes 1, be it re 3.2 and table 3

higher in aquatic overlap between ibute to this diffe muscle group wa and intercepts for herefore seem to

ers. The size of t ffers between th ner muscle group w opener and pter

per (protractors) uatic feeders tha avier in aquatic fe

ests were perform data the standard

routine impleme s, 2004) with all des that have

ches (Mooers et 995, 1996a, 1996

aw muscles are li de; mg) and the with body mass .000). A regressio

slope of this The common slop etric growth of ja

only just. Howev 3.2). For a given b c feeding birds th

groups.

erence in relative as analysed separ r skull and quadr o have the same s he pterygoid mu e two groups. As s and pterygoid rygoid muscles th ) and lower jaw

n in terrestrial gr eeders.

47 med dized ents

al., 6a)

isted mass (g) for on II pe for

w ver,

body han in

e jaw rately.

rate size scles s for he razers.

48



 Fig axi Leg gra (Ay me (An am (De du

2.7 3.0 3.2 3.5 3.7 4.0 4.2

2.0 2.5 3.0 3.5

gure3.2. Regressio s: log muscle mass gend: +: aquatic fee aph (see text). Fille ythyavalisneria), 3 erganser (Lophodyt nasclypeata), 8: Au mericana), 10: black endrocygnaeytoni) ck (Dendrocygnav

2.50 3.00 75

00 25 50 75 00

25 total jaw muscles

2.50 3.00 00

50 00

50 pterygoid muscle total jaw mus

pterygoid mu

n lines for log body s (mg)).

eders, _: terrestri d squares: Anser s : mute swan (Cygn tescuculatus), 6: co ustralian wood duc k-bellied whistling-

), 12: fulvous whist viduata), 14: Egypti

3.50 4.00 2.25 2.50 2.75 3.00 3.25 3.50 3.75

3.50 4.00 s

1.50 2.00 2.50 3.00

scles

uscles

y mass and log jaw ial feeders. Species pecies, 1: mallard ( nusolor), 4: black s ommon merganser ck (Chenonettajub

duck (Dendrocygna tling-duck (Dendro

an goose (Alopoch

2.50 3.00 3.5

skull adductors

2.50 3.00 3.5

protractor muscles skull adductors

protractor muscl

w muscles mass (x-a s of interest are ind (Anasplatyrhyncho wan (Cygnusatrat r (Mergusmergans ata), 9: American w aautumnalis), 11:

cygnabicolor),13:

henaegypticus).

50 4.00

2.00 2.50 3.00

qu

50 4.00

2.10 2.40 2.70 3.00 3.30 3.60 dep

1 13 q a

es d

Cha

axis: log body mass dicated in depresso os), 2: canvasback tus), 5: hooded

ser), 7: northern sh wigeon (Anas

plumed whistling- white-faced whistl

2.50 3.00 3.50

uadrate adductors

2.50 3.00 3.50

pressors

21 10

9 7

6 5

8

11

3 12 14

uadrate adductors

epressors

apter 3



s (g), y- or

hoveler duck ling-

4.00

4.00

3 4

Table3.2. Relationships between (log) body mass and (log) jaw muscle weights (r = Pearson correlation) in aquatic (Aq.) and terrestrial (Terr.) feeding anseriform species and non-anseriform (non-A.) species. Regression has the form y = a (slope) * log x + b (intercept). c. slope = common slope, i.c. = independent contrasts, p1 = probability that slopes are equal for the aquatic and terrestrial group, p2 = probability that intercepts of the two groups are equal for the common slope. n r* slope p1 95% CI intercept Intercept common slope p2 Jaw muscle mass (1-sided)

Aq. Terr. c. slope i.c. non-A.

27 18 45 45 16

0.917 0.839 0.840 0.915

0.812 1.087 0.873 0.901 0.769

0.072

0.690-0.957 0.818-1.446 0.751-1.014 0.730-1.080 0.613-0.965

0.957 -0.072 1.030

0.782 0.605 0.000 Skull adductors Aq. Terr. c. slope i.c. non-A

27 18 45 45 16

0.886 0.847 0.820 0.847

0.893 1.127 0.965 0.901 0.805

0.156

0.737-1.081 0.854-1.488 0.827-1.125 0.720-1.090 0.597-1.084

0.254 - 0.558 (0.005) 0.539

0.041 -0.045 0.104 Quadrate adductors Aq. Terr. c. slope i.c. non-A

27 18 45 45 16

0.902 0.856 0.840 0.935

0.952 1.037 0.978 0.897 0.707

0.582

0.797-1.137 0.791-1.359 0.848-1.128 0.720-1.070 0.578-0.865

-0.501 -0.834 (-0.603) 0.063

-0.579 -0.647 0.167 Pterygoid muscles Aq. Terr. c. slope i.c. non-A

27 18 45 45 16

0.888 0.810 0.810 0.914

0.868 1.187 0.943 0.886 0.763

0.082

0.722-1.044 0.874-1.612 0.800-1.111 0.690-1.080 0.607-0.958

0.024 - 1.115 0.546

-0.199 - 0.346 0.009 Protractor muscles Aq. Terr. c. slope i.c. non-A

27 18 45 45 16

0.871 0.772 0.750 0.935

0.798 1.142 0.875 1.149 0.855

0.064

0.655-0.971 0.820-1.591 0.731-1.047 0.850-1.450 0.698-1.047

-0.115 -1.490 - 0.551

- 0.345 - 0.647 0.000 Depressor muscles Aq. Terr. c. slope i.c. non-A

27 18 45 45 16

0.881 0.768 0.770 0.961

0.740 1.019 0.803 0.907 0.797

0.093

0.610-0.898 0.730-1.421 0.673-0.957 0.680-1.130 0.680-0.933

0.665 - 0.578 0.135

0.479 0.103 0.000 * all p = 0.000

50 So the op Me mu ad mu rhy Ch wh lar the wh To co the ve the no an pte an gra Alt tw

Ma Ou allo ter 1.0 in res fee spe tho clo spe an

me species show e aquatic feeding pener muscles, w

erganser species uscles of the nort ductor muscles, uscle mass of all t ynchotis) did not enonettajubata, hile most Anser a rge jaw opener m e two aquatic fee histling ducks.

evaluate the diff mpared to a sam e relationship be ry similar to the s e opener muscles on-Anseriformes w

d significantly sm erygoid muscles,

seriform group t azing group (p = 0 though the adduc wo anseriform gro

ainresults

ur study strongly ometrically with rrestrial grazers s 014) but differen

aquatic feeders t sult of relatively eders. Compared

ecies, the size of ose of terrestrial osers) are also lar ecies, but the pte seriform species

w large deviations g group Anasplat hile Nettapeposa

have relatively s thern shoveler ar which gives it the the species exam show a high rati , most Branta an nd especially the muscles compared eding whistling-d

ference between mple of non-anser tween muscle gr slope found for t s of the lower jaw were statistically maller than for th however, were m han in both the a 0.000).

ctor muscle grou oups no clear stat

suggests that tot body mass. A co shows that this re

t intercepts for t than in terrestria large jaw opener d to a sample of p the jaw openers grazing anserifo rger in aquatic fe erygoid muscles o

.

s from the muscle tyrhynchos and A aca, Cygnusolor small jaw opener

re not very large e highest ratio of mined, while the o

o. In the terrestr d sheldgeese hav e two grazing wh d to other grazing

ucks, however, a

n the two groups riform species wi roup mass and bo the anseriforms f

w (depressor) an y similar to those e aquatic feeding much larger (2-3x aquatic feeding g ups in non-anserif tistical difference

Discussion

tal jaw muscle m mparison betwee elationship has th he two groups. T l grazers. The dif r muscles in aqua predominantly te s of aquatic feedi rms do not differ eding anseriform of both anserifor

e mass expected Aythyavalisneria and C.atratus, a muscles. Surpris but this species f jaw opener mus other shoveler sp rial grazing group

ve relatively sma istling duck spec g species. The jaw are relatively larg

of anseriforms t ith various foragi ody mass in the n for all muscle gro

d of the upper ja of the terrestria g anseriforms (bo x for the commo group (p = 0.002) forms tend to be e was found.

ass in Anseriform en aquatic feedin he same slope (0 The jaw muscle m fference in total j atic feeders comp errestrial feeding ng wildfowl are l r. The pterygoid m m species than in

rm groups are sm

Cha for their body si

have very large and the two singly, the opene

has relatively sm scle mass / adduc pecies studied (A p Anasamericana ll jaw opener mu ies have relativel w opener muscle ger than in the gr

he data were ng habits. The slo non-Anseriforme oups. The intercep

aw ( protractors) l feeding anserifo oth p = 0.000). Th n slope) in the no and the terrestr e higher than in th

mes scales negati ng species and 0.873, 95% CI 0.75 mass is 1.5 times l

jaw muscle mass pared to terrestri non-anseriform arger as well, wh muscles (upper ja terrestrial grazin maller than in non

apter 3 ze. In

r mall

ctor .

a, uscles,

ly es in

azing

ope of s was pts for

of orms he on- ial he

ve 51- larger is the ial hile

aw ng n-

Jaw In Go hig Th lar mu stu aq stu on Th dif

Sca Da (20 see mu co an Go va ex the un 0.6 Th ma Lee bo an Sch ex cra 0.2 va he mu Fin sim jaw ava

w muscle size another study on oodman and Fishe gher and increase

ey attributed thi rge muscles and l uscles in aquatic udy, but the pres uatic feeders and udy by Goodman

ly species that sp e small sample s fferent conclusio

alingofjawmus ata on jaw muscle

004) found positi ed-cracking finch uscle data from t rmorant species d Bout calculated oodman and Fishe lue reported in th plained by the di e Goodman and derestimate the 68 (95% CI 0.43–1

e exponent for s ay be related to t

euw (2002) foun ody mass (0.7 ± 0 d the brain, also hmidt-Nielsen, 19 pected to scale w anium lengths of 215 (95% CI 0.183 lue. Jaw muscle m ad size. Irrespect uscle mass and b nches have appro milar head size re w muscle size. In ailable for the ins

n the functional a er (1962) found t es faster with bod

s difference to la long force arms f feeders compare ence of large clo d is not significan

and Fisher samp pend part of thei

ize and heteroge n compared to th

sclemass

es in other group ive allometric sca hes (1.29; 95% CL he literature and also tends to sca d for the jaw mus er (1962) was on his study (0.87). T ifference in regre

Fisher data were slope. For the sa 1.07).

caling of jaw mus the scaling of hea d for 8 anatid spe .13). The weights

scale negatively 984). Based on th with an exponent

the anseriform s 3 - 0.249, n = 44) mass in anserifor tive of the refere ody/head size is oximately 4 times elative to body m

finches a large p sertion of muscle

anatomy of the fe that the effective dy mass in strain arge muscles for j for jaw closing. Th ed to terrestrial g

ser muscles is no ntly different from ple size was smal

r time grazing bu eneous combinat

he present study

ps of birds are ver aling of jaw musc L, 1.09–1.50). The d found that jaw ale positive allom

scle mass of 14 a nly 0.45 (95% CI 0 The difference be ession technique e fitted with a mo ame sample mod

scle mass with re ad size (see also v ecies that head m s of the organs co allometric (0.67) his value, linear d t of 0.67/3 = 0.22 species in the pre to body mass (se rms therefore see ence measure the significantly lowe s larger adductor

ass. Apparently, rocess, the proce e fibers. This proc

eeding apparatus e jaw opening an ning species than jaw opening and he presence of la grazers is confirm ot. Adductor size m that in equally l and their graspi ut also fish eating ion of species ma .

ry scarce. Van de cle size with respe ey also calculated muscle mass in a metrically. The exp anseriform specie 0.12–0.77). This is etween the two e used. In van der odel I regression, el II regression e

espect to body m van der Meij and mass scales negat

ontained within t ) to body mass (B dimensions of the 2 to body mass. A

esent study scale ee chapter 4), sim ems to scale posi e slope of the rela

er in anseriforms r muscles than an overall cranium essus zygomaticu cess is absent in A

s of Anseriforme d jaw closing forc

in grasping spec a combination o arge jaw opener med by the presen

varies widely in large grazers. In ing group include g merganser spec

ay explain the

er Meij and Bout ect to body mass d exponents for j a small sample of ponent van der M es reported by

s much lower tha exponents is larg Meij and Bout (2 which tends to stimates a slope

mass in anseriform Bout, 2004). Van tively allometric the cranium, the Brooke et al., 199

e cranium are As in finches, the

d with an expone milar to the expe

itively allometric ationship betwee s than in finches.

nseriforms, but a size is not limitin us, increases the

Anseriformes.

51 s ce is ies.

of nt

the ed not cies.

s in aw f Meij an the gely

2004) of

ms n der

with eyes 99;

ent of ected

to en jaw

ng for area

52 Te 2) att Re we Sta rel str sig An An she rel the de an ha ey oth Th Go fee the ter bil po foo



 Fu It i an wh req str ter mu acc An (20 Th su to mo 24

rrestrial grazers and relative skul tachment of addu elative skull heigh

ell (Claude et al., ayton, 2005; Van lationship betwe raightforward, as gnificantly differe nser and Branta s nser species have eldgeese) specie lationship betwe e size of the depr

pressor (and add d lower cranium s shown that a re e and kinetic hin her traits than ar e higher effectiv oodman and Fishe

eders have longe erefore expected rrestrial grazers i

l, not by a relativ ossibility is that a

od.

nctionalsignifica s tempting to rel seriform groups hich the two grou

quire a larger jaw raining species, w rrestrial foraging uch lower. Howe

celerate water co nseriformes. In th

0 Hz) but their m e drag Fd may be rface area, v the guess but would ovement. When mm) are small F

have a higher-va l height is often t uctor muscle fibe ht has been sugge 2004; Herrel et a Cakenberghe et en skull height an s it seems. Adduc ent from that in e pecies do have a larger adductors s have smaller ad en jaw muscle siz ressor muscles. W ductor) muscles t

than terrestrial g elatively high cra

ge. A high craniu rea for muscle att

e closing force in er (1962) is even er bills than terres d to have lower ja ncrease their bit vely large adducto

short bill has the

ance

late the differenc directly to the di ups forage. The o w opener force to which show fast r species these fo ver, it not clear h ompares to the fo he mallard the up

easured rotation e estimated as 0.5

velocity of the m d be 1 in the case both velocity and Fd will be small to

ulted cranium th thought to increa ers posterior to t ested to improve al., 1999; Herrel e

al., 2002). Howe nd muscle size or ctor size varies wi equally large graz a high-vaulted cra s than expected f dductors than ex

ze and difference While aquatic fee than terrestrial gr grazing species (s nium is correlate um may therefore

tachment.

n strainers compa more unlikely w strial grazers (cha aw closing force a e force compare or muscle compl e additional adva

ces in jaw muscle ifferent physical c opening and closi

o overcome drag epetitive movem rces are much sm how the magnitu

orces produced b pper and lower ja n is small (6 and 3 5  Aw v² Cd, whe movement and Cd of a flat plate m d surface area (lin oo. The mass of w

han straining spec ase the available he orbit (Goodm e bite capacity in et al., 2001; Herr ever, the present r bite capacity m idely in aquatic fe zers. In the grazer anium (chapter 2

for their body siz pected. The abse es in cranial heig eding species (e.g

razers, Anas spec see chapter 2). M ed with a more d

e be the consequ

ared to grazers o when we consider apter 2 and chap at the tip of the b d to aquatic feed ex. Why this is so ntage of a shorte

e size between th characteristics of ng movements d and to accelerat ment cycles (Koolo

maller, because t de of drag force by the jaw openin aw open and clos 3 degrees respect ere  is the densi d is the drag coef oving perpendicu near dimensions water that has to

Cha cies (see also cha

area for the an et al., 1962).

other vertebrate el et al., 2004;

study shows tha ay not be as eeders and is not r group, especial

), but while most ze, most Branta ( ence of a direct

ht is also illustrat g., Anas) have lar cies have a narro Morphometric an orsal position of uence of selection

r graspers report r bill length. Aqua pter 4) and are

bill. Interestingly, ders through a sh o, is not clear. On er transport time

he two trophic f the environmen during feeding in

e water, especia oos et al. 1989).

he density of air or the force to ng muscles of

e at a high frequ tively; Kooloos, 1 ty of water, Aw th fficient. Cd is diffi ular to the direct of the mandible be accelerated d

apter 3 apter

es as at this

t ly t and ted by

ger wer alysis

the n on

ted by atic

, hort

ne e for

nt in water lly in In

is

ency 1989).

he icult tion of

89 x during

Jaw jaw ma ap Ho be tha cra de pa the the cra sha at l²), Th be no Dr bu pro mo ter lar acc mu ter fee suc Fo 1.2 fee the mu Th co for Su gro act up acc be

w muscle size w opening may b allard the depres proximately 60 N owever, the diffe

tween the two g an in terrestrial g anial hinge do no termined by the ssive elastic forc e oral cavity, grav e same angular a anial morphology

ape of the upper the top corner (k , where l, h and w e moment of ine am, which is sim ot differ between ag forces are pro t the moment fro oportional to l⁴ (V oment of inertia rrestrial feeders.

rger protractor m celeration of the uscle data show t rrestrial feeders.

eders are not an ch.

r the opener mu 24 times longer in eder would there e same angular a uscle is estimated

e depressor in aq mpensate for the rces.

rprisingly, the siz oups. The only cl

ts on both the up pper bill opener, t count for more t tween pterygoid

e a much larger c sor muscles are e N, but the openin

rence in force ex roups of anserifo grazers (see chap ot differ between moments exerte es from soft tissu vity, cf Van Wass acceleration of th y, one would exp r bill may be appr kinetic hinge). Fo w are the length, ertia of the lower

ply two times th trophic groups t oportional to the om drag force inc Van Wassenberg

is (1.35)³ = 2.5 tim Given similar mo muscles for the qu upper bill, assum that the protract

This suggests tha adaptation to th

scles of the lowe n aquatic feeders efore require a (1 acceleration of th d to be 2.4 times quatic feeders is e increase in mom

ze of the adducto osing muscle tha pper and lower ja the relative incre han just the incre d muscle size and

component of th each capable of g ng force will decre xerted by the env

orms. The bill is 1 pter 2 (and chapte

the groups. The ed by a number o ues and the bend senbergh et al. (2 he bills were to be

ect larger jaw mu roximated by a tr or such an object height and width r jaw may be app

e expression for the moment of in

surface area of t creases even fast gh et al., 2005). Fo

mes larger in aqu oments an aquat uadrate and ptery ming that muscle

or muscles are 2 at the relatively l e aquatic environ

er jaw the situatio s than in terrestr 1.24)³ = 1.9 times he lower jaw as a larger in aquatic therefore somew ment of inertia a

or muscles does n at seems to differ

aw and is 1.4 tim ease in size of the ease in moment aquatic feeding

e forces resisting generating a max ease with jaw op vironment is not t 1.35 times longer

er 4)). Bill height (angular) accele of different forces ding zone of the u 2005) and by thei

e reached in spec uscles in species riangular prism w the moment of i h of the upper bi roximated by tha the upper bill. As nertia is proportio the bill and (angu

ter than the mom or the upper bill uatic feeders than

ic feeder would a ygoid to produce fibre length rem times larger in a large protractor m nment but are re

on is slightly diffe ial feeders (see c s larger depresso

terrestrial feede c feeders than in what larger than nd may be used t

not differ betwee r in size is the pte es larger in aqua e pterygoid musc of inertia of the b is also unlikely b

g jaw opening. In ximum static forc pening velocity.

the only differen r in aquatic feede and width at the ration of the bills s (muscle forces, upper jaw, pressu

r moment of ine cies with similar with larger bills.

with the rotation nertia is 1/6 hw ll and  is the de at of a rectangula

s height and widt onal to l³ for both ular) velocity squa ment of inertia an this means that t n in similar sized also need 2.5 tim e the same angula mains constant. Th aquatic feeders th muscles in aquat elated to bill size

erent. The mandi chapter 4). An aq r muscle to prod er. The depressor terrestrial feede required to to overcome resi

en the two troph erygoid muscle, w

tic feeders. As fo les seems too sm bills. A relationsh

ecause non-

53 the ce of

ce ers e

s is ure in

rtia. If The axis wl (h² +

nsity.

ar th do h bills.

ared, nd is

the mes

ar he han in

ic as

ble is uatic uce r

rs.

isting

ic which or the mall to

hip

54 an an A p wa dif tha ter fee les bil on str ga (12 du ha str an mo the mu ex du illu rel of

Va

 Fo oft no co tec fee an for ex su en inc D.

so atr fee

seriform terrestr seriform species proper assessme ater and bill size f fferent forces tha at aquatic feedin rrestrial feeding a eders are compa ss wide at the tip

l of aquatic feede jaw acceleration raining geese and pe and straining 2-13 Hz) but relat

cks (mallard, wig ve relatively sma raining frequency gular rotation an ovement of the b e ducks and swan uscles are as larg

pected from its s ck species but its ustrate that an in

lationship may re water to be disp

ariationwithintr r many species u ten depending on ot available. Categ nsiderable degre chniques may be eding group som d/or small invert rmosa,A.baham perience resistin bmerged, but on ding in steep pon clude parts of aqu bicolor) and/or t me consume pre ratus). Aquatic ‘g eding. The velocit

rial species have .

nt of the effect o for feeding move at act on the bill.

g species are not anseriforms. This red under the sa than in aquatic f ers, even when t n in anseriforms a d duck species su

frequency show tively large gapes geon, and tufted all angular rotatio y (11 Hz) but also nd frequency are bill accelerations n. The northern s e as expected fo size. The angular s straining freque

crease in bill size eflect the decreas laced increases.

rophicgroups

used in this study n the season. Det gorizing species a ee of arbitrarines

associated with e of the examine tebrates) year ro mensis,and M.an g forces from the n both bills when

nds as found in E uatic vegetation terrestrial vegeta edominantly aqua grazing’ may in so ty of jaw opening

larger pterygoid

of the differences ements requires b

However, from t t able to produce s may be true eve me (aquatic) con feeders and will p

he bill is immerse are not available

ggest that this m that two geese s s compared to du

duck) use high st ons of the bills. T o a relatively sma used to estimate in the two geese shoveler has a re r its body size an rotations of the ency is much low e may go at the e se in net jaw ope

there is a consid tailed data on foo as ‘aquatic’ or ‘te

s, especially since different forces ed species forage und (A.hottento gustirostris). Dab e water especiall

they forage by ‘u Europe (Nudds et

(A.nyroca,T.can ation (T.ferrugine atic vegetation (A ome respects be

g and jaw closing

muscles than aq

s in drag, reaction biomechanical m the present data e angular accelera

en when aquatic nditions. The bill o

produce less resi ed equally far. De

, but data on a sm may be the case. R

species have low ucks and the mut training frequenc he mute swan ha ll gape compared e maximal accele e species are almo

latively large bill d the jaw closers bill during straini wer (13 Hz). This s expense of straini ening force as bill

derable variation od items taken o errestrial’ feeder e different food i regimes for the j exclusively on sm ta,A.clypeata, A bbling ducks feed y on the lower b up-ending’. Speci t al., 2000). A num

na, N.peposaca,

ea,A.platyrhynch A.valisneria,C.o

more like terrest g during foraging

Cha uatic feeding

n force of displac modelling of all th it would seem lik ations as high as

and terrestrial of terrestrial feed

sting force than t etailed kinematic mall number of Rough estimates

straining freque te swan. A numb cies (18-20 Hz), b as a much lower d to the geese. W eration for sinuso

ost twice as high but the jaw open s are smaller than ing are similar to species seems to ing frequency. Su l size and the am

in food items tak over a year are of

therefore involv items or foraging

aws. In the aqua mall food items ( A.rhynchotis,A.

ding on the surfac ill when it is part ies tend to use u mber of species

N.rufina,D.vidu hos, A.specularis lor,C.bewicki,C.

trial grazing than on aquatic plant

apter 3

ced e kely

ders is the c data

on ncies er of but When

oid as in ner n

other uch a

ount

ken, ften

es a g

tic seeds ce will

ly p- uata,

s), and .

filter- ts may

Jaw be mo ma spe Sev pe pte ma for sw Au al., Th ref de A.

div an Mo Th the she pla ex lar fee tha to htt Go da exc pre to Th Am spe up jaw sim Th rel fee

w muscle size similar to the ve ovements during ay explain the rel

ecies.

veral (diving) spe rspicillata, A.affi eneres). Whethe ay partly depend r a number of the wallowed underw

ustin et al., 1998;

, 1998).

e small size of th flect the smaller tach shellfish or affinisand L.cuc ving species addu d sheldgeese.

ost species in the e major ingredie e geese, Anser sp eldgeese species ant parts, but also

penditure than g rger jaw opening eding behaviour, an did grazing juv grub (references tp://www.birdsk oose.shtml), whic

ta on food items clusively on abov eference for abo

the other Anser e three extant w merican wigeon f ecies is known to pon arrival on the w opener muscle milar to those of t

e two species of latively large jaw eding group bette

elocity for terrest straining (18-20 latively small dep

ecies add large in finis,B.clangula,

r such species oft on where the pr e species mentio

ater. Very large f Eadie et al., 199

he depressor mus drag forces expe hold struggling fi cullatusdo have t uctor muscles are

e terrestrial grazi nt of their diet co pecies tend to ha s. According to lit o on undergroun grazing (Gauthier forces as the bill it was found tha veniles (Jónsson, s in Esselink et al.

orea.org/Birds/S ch may explain th are available, bu ve-ground plant p ve-ground plant geese examined.

wigeon species are eeds the least on o include terrestr eir breeding grou s of this species i terrestrial grazer grazing whistling opener muscles er than the terre

trial grazing and l Hz). Consequent pressor muscles f

nvertebrates or ev C.hyemalis,L.cu ten experience la rey is swallowed,

ned above it has food items are ta 5; Johnson, 1995

scles of the two m erienced by the ve ish one may expe the largest adduc e less prominent,

ng group predom onsists of aerial p ve larger jaw ope terature data Ans nd parts (i.e. grub et al., 1984) and ls push against th at grubbing juven 2005). Four of th ., 1997; Mowbray Significant_Recor

heir heavier musc ut the lesser-whit parts in spring (M parts may explai .

e considered to b n terrestrial veget rial plants in its d

nds (references i is clearly differen rs.

g-ducks (Dendroc compared to oth estrial group. The

ower than the hi tly resisting force found for N.rufin

ven fish to their d ucullatus,M.mer arge resisting for

under water or been reported t aken to the surfac 5; Mallory and M

merganser specie ery narrow bills.

ect relatively larg ctors of the speci , but often larger

minantly use a sin parts of terrestria ener muscles tha ser geese forage bbing). Grubbing d probably anima he mud. In a stud niles had slightly h

he six Anserspec y et al., 2000; Pe ds/New_Birds/B cles. For the bar- te fronted goose Markkola et al., 20

n its lower jaw m

be grazers. Of the tation (Kear, 200 iet during winter in Mowbray (199 nt from the aquat cygnaeytoniand her grazers and s assignment as te

igh frequency es will be less. Th na and the Cygnu

diet (A.crecca, M rganser,andT.

ces is not clear a at the surface. At hat food items m ce (references in etz, 1999; Savard

es is considered t In species that h ge adductor musc

ies examined. In r than in many ge

ngle feeding meth al vegetation. Wi an Branta and

not only on aeria requires larger e ls have to produc dy on snow goose

heavier jaw musc cies studied are k

tersen et al., 199 K-NB-Bar-headed headed goose fe is known to fora 003). A strong muscle sizes comp

ese three species 05). However, thi

r, during migratio 99)). The size of th

tic feeding group D.autumnalis)h seem to fit the aq errestrial grazer w

55 his us

M.

nd t least may be

d et

to ave to cles.

other eese

hod.

ithin al energy

ce e

cles known

94;

d- w age

pared

s the s on and

he p and have quatic

was