INTRODUCTION
Varying degrees of predation, inter- and intraspecific competition, inter- and intrasex�a� competition and food avai�abi�ity may res��t in individ�a�, sex�a� or geographic variation in size (End�er 1977, Wike�ski & Tri��mich 1997, Lovich et al. 1998). Historica��y many of the �eading papers on avian size variation have been concerned with terrestria� birds (Hami�ton 1961, Se�ander 1966, Grant 1968, James 1970, Johnston & Se�ander 1973) with �itt�e work on seabirds.
The remote �ocation of many seabird co�onies, the genera� trend for monogamy, and the noct�rna� habits of some seabird species have probab�y contrib�ted to the pa�city of s�ch st�dies.
No previo�s comprehensive st�dies of size variation in the shearwater gen�s Puffinus (Proce��ariiformes) are avai�ab�e, yet the gen�s �ends itse�f to a st�dy of size variation in seabirds. The gen�s contains approximate�y 20 species that vary in s�ch aspects as eco�ogy, geographic range, size, migratory habit, and timing of breeding and the c�imatic zone, hemisphere and habitat in which they breed (Warham 1990, de� Hoyo et al. 1992). Differences in s�ch aspects are expected to contrib�te to size variation of a species over its geographic range.
The primary objective of this paper is to describe the major patterns of size and shape variation of Puffinus species over their respective ranges. This objective was achieved by addressing these q�estions:
• Do sympatric congeners differ in size and shape?
• Do the sexes of each Puffinus species differ morphometrica��y?
• Do Puffinus species exhibit interpop��ation variation in their morphometrics?
• Does the degree of sex�a� size dimorphism exhibited by Puffinus species differ over the species range?
METHODS Taxonomy
The taxonomy �sed in this st�dy �arge�y fo��ows that proposed by Sib�ey & Monroe (1990). The Ye�ko�an P. yelkouan and �a�earic P. mauretanicus Shearwaters have been vario�s�y c�assified at the s�bspecific �eve�, most often as s�bspecies of the Manx Shearwater P. puffinus (M�rphy 1952, Jo�anin & Mo�gin 1979, Harrison 1983). We have fo��owed the present consens�s that, based on morpho�ogic, p��mage, behavio�ra�, geographic and genetic differences, treats each taxon as a f��� species (�o�rne et al. 1988, Wa�ker et al. 1990, de� Hoyo et al. 1992, Wink et al.
1993, Heidrich et al. 1996, Heidrich et al. 1998, Sangster et al.
2002). F�rthermore, we have fo��owed the c�assification of Newe��’s Shearwater P. newelli as a f��� species (�irdLife Internationa� 2000) rather than as a s�bspecies of Townsend’s Shearwater P. auricularis (Sib�ey & Monroe 1990). These birds differ in size, proportions, co�o�ration, winter range and breeding season (King & Go��d 1967, Jeh� 1982).
Data collection
Morphometric meas�rements were taken from 2689 m�se�m st�dy skins of 18 Puffinus species (see Tab�e 1 for common names) he�d in major m�se�m ornitho�ogica� co��ections (see Acknow�edgments).
J�veni�e and immat�re specimens were not inc��ded in the data set.
Species samp�e sizes varied beca�se of specimen avai�abi�ity in the co��ections.
The traits meas�red were bi�� �ength (�L), bi�� depth at base (�D�), bi�� depth at nares (�DN), wing �ength (maxim�m f�attened chord, WL), tars�s �ength (TL) and midtoe �ength (MT). A�� meas�rements were taken by LS�. A stee� r��e with an end stop was �sed to meas�re wing �ength to the nearest 0.5 mm, and digita� Vernier
PATTERNS OF SIZE VARIATION IN THE SHEARWATER GENUS PUFFINUS
LEIGH S. �ULL1,2, �EN D. �ELL1 & SHIRLEY PLEDGER3
1 School of Biological Sciences, Victoria University of Wellington, PO Box 600, Wellington, New Zealand (ben.bell@vuw.ac.nz)
2 Current address: Université Paris-Sud XI, Laboratoire Ecologie, Systématique et Evolution, Batiment 362, F-91405 Orsay CEDEX, France
3 School of Mathematical and Computing Sciences, Victoria University of Wellington, PO Box 600, Wellington, New Zealand
Received 3 June 2004, accepted 27 July 2005 SUMMARY
�ULL, L.S., �ELL, �.D. & PLEDGER, S. 2005. Patterns of size variation in the shearwater gen�s Puffinus. Marine Ornithology 33: 27-39.
Using m��tivariate methods, we investigated patterns of trait variation in the shearwater gen�s Puffinus in terms of specific, sex�a� and geographic variation. We fo�nd no significant interaction between sex and pop��ation, indicating that there is no geographica� variation in the magnit�de of sex�a� dimorphism. Species for which a significant difference was fo�nd between the sexes exhibit �ow �eve�s of sex�a� size dimorphism, expressed on�y in bi��-depth dimensions (ma�e bi��s are deeper). On�y species with widespread distrib�tions exhibit significant geographic variation in their morphometrics.
Key words: Shearwaters, Puffinus spp., morpho�ogy, geographic variation, sex�a� size dimorphism, interspecific variation
ca�ipers were �sed to meas�re bi��, tars�s and midtoe to the nearest 0.01 mm. For consistency, specimens were meas�red on the right- hand side of the body. For each trait, each bird was meas�red three times, not consec�tive�y, and the average was �sed in the statistica�
ana�yses.
Pop��ations of shearwaters genera��y have discrete distrib�tions s�ch as archipe�agos with severa� co�onies (is�ands) and s�bco�onies within is�ands (Rabo�am et al. 2000). Samp�e sizes were too sma�� to investigate differences between s�bco�onies on individ�a�
is�ands, and so data were poo�ed into pop��ations (Appendix 1).
Poo�ing was determined by the overa�� distrib�tion of a species and concentrations of co��ecting �oca�ities within certain areas. Poo�ing specimens into a priori s�bspecies obsc�res patterns of geographic variation, and so individ�a�s were ana�ysed on a species basis (Z�si 1982, Zink & Remsen 1986).
Statistical analysis
A�� ana�yses were cond�cted �sing the SAS (version 6.12) statistica�
package. Preparatory methods of the st�dy skins dictated the variab�es that co��d be meas�red. In some cases not a�� of the ear�ier-noted morphometrics (most often �D�) co��d be taken from each specimen. M��tivariate ana�yses req�ire a f��� data set for each individ�a�, and the samp�e sizes were conseq�ent�y great�y red�ced.
Morpho�ogic variation owing to sex and pop��ation was examined for each character by a mixed-mode�, two-way ana�ysis of variance, with sex as a fixed effect and pop��ation as a random effect (MANOVAs and ANOVAs, GLM proced�re). This design provided tests of three n��� hypotheses: i) no sex�a� dimorphism; ii) no effect of pop��ation �ocation; and iii) no geographic variation in sex�a�
dimorphism (as indicated by sex × pop��ation interaction). To test for the effect of sex on the other morphometrics, MANCOVA and ANCOVA (GLM proced�re) were then performed, with
body size (represented by TL) as a covariate. Species were deemed sex�a��y size dimorphic if the average meas�rements of individ�a� morphometrics differed between the sexes by 5% or more. Puffinus bulleri, P. huttoni, P. mauretanicus and P. newelli have very restricted breeding distrib�tions and so were not inc��ded in the pop��ation ana�yses.
Canonica� discriminant ana�yses (CANDISC proced�re) were performed to compare size and shape variation among Puffinus species. To check these proced�res, the data were on each occasion random�y sp�it into two even s�bsets according to the variab�e being tested. One s�bset (training data) was �sed to generate the mode�
and the other (test data) to va�idate it. The res��ts from the test data are presented here.
RESULTS
Interspecific variation
Tab�e 1 shows the samp�e sizes and mean morphometrics for each species inc��ded in this st�dy, and Tab�e 2 shows the res��ts of the canonica� discriminant ana�yses carried o�t on the species data. The differences in factor �oadings indicate differences in the re�ative size and shape of appendages in the species. Canonica� variab�e 1 (CAN1) is genera��y defined by differences in size, and canonica�
variab�e 2 (CAN2) is defined by differences in re�ative size and shape (Go��d & Johnston 1972, S�otow & Goodfriend 1996). On the basis of size (CAN1), the gen�s is divided into sma�� (P. assimilis, P. gavia and P. lherminieri), medi�m (P. puffinus, P. mauretanicus, P. yelkouan, P. huttoni, P. newelli, P. nativitatis, P. opisthomelas and P. auricularis) and �arge (P. tenuirostris, P. pacificus, P. bulleri, P. carneipes, P. creatopus, P. griseus and P. gravis) shearwaters (Fig. 1).
Comparison of sympatric species (Appendix 1) in Fig. 1 revea�s that in on�y one instance (P. nativitatis and P. newelli) is there TABLE 1
Sample sizes (n�� an�� mean �� stan��ar�� ��eviation meas�rements (mm�� of t�e 1��n�� an�� mean �� stan��ar�� ��eviation meas�rements (mm�� of t�e 1���� an�� mean �� stan��ar�� ��eviation meas�rements (mm�� of t�e 1�� Puffinus species
Species n Bill lengt� Bill ��ept�
at base
Bill ��ept�
at nares
Wing lengt� Tars�s lengt�
Mi��toe lengt�
Scientific name Common name
P. pacificus Wedge-tai�ed Shearwater 576 38.47±1.89 12.84±0.80 9.17±0.70 292.99±9.99 48.67±1.82 49.97±2.07 P. bulleri ����er’s Shearwater 93 41.20±1.44 13.91±0.63 10.43±0.72 286.62±9.21 51.75±1.58 52.76±1.71 P. carneipes F�esh-footed Shearwater 127 41.24±1.84 16.01±0.95 11.73±0.76 319.46±7.84 54.40±1.43 56.87±1.86 P. creatopus Pink-footed Shearwater 116 42.22±1.53 16.39±0.99 12.30±0.68 333.40±8.17 55.45±1.32 58.82±1.63 P. gravis Great Shearwater 124 45.61±1.81 15.02±1.06 11.14±0.79 322.01±14.80 59.37±1.81 62.58±1.98 P. griseus Sooty Shearwater 247 41.43±1.71 13.27±0.92 9.74±0.69 291.10±14.30 56.57±2.04 55.46±1.90 P. tenuirostris Short-tai�ed Shearwater 204 31.82±1.37 11.15±0.74 7.97±0.60 267.11±13.06 50.96±1.55 51.50±1.69 P. nativitatis Christmas Shearwater 175 30.96±1.15 10.81±0.65 7.83±0.55 247.85±6.70 44.40±1.29 42.73±1.23 P. puffinus Manx Shearwater 82 34.88±1.41 10.39±0.70 7.91±0.63 235.88±5.34 45.14±1.17 42.75±1.45 P. yelkouan Ye�ko�an Shearwater 50 35.46±1.56 10.46±0.82 8.00±0.75 232.10±7.44 45.61±1.57 42.95±1.59 P. mauretanicus �a�earic Shearwater 12 38.84±1.73 11.61±0.67 8.72±0.64 246.07±5.44 48.34±1.28 45.74±1.11 P. auricularis Townsend’s Shearwater 17 31.21±1.15 9.99±0.34 7.46±0.28 228.02±5.72 45.19±1.08 41.96±1.10 P. newelli Newe��’s Shearwater 64 33.12±1.22 10.76±0.64 7.59±0.53 233.39±9.60 46.91±1.34 43.78±1.21 P. opisthomelas ��ack-vented Shearwater 75 36.59±1.48 11.32±0.68 8.42±0.61 239.95±7.85 45.65±1.38 43.87±1.37 P. gavia F��ttering Shearwater 144 32.94±1.46 9.20±0.67 7.06±0.57 205.83±7.56 42.03±1.43 40.10±1.28 P. huttoni H�tton’s Shearwater 59 36.18±1.33 9.87±0.56 7.37±0.46 220.39±4.65 41.97±1.27 41.15±1.38 P. lherminieri A�d�bon’s Shearwater 333 27.00±1.75 8.61±0.73 6.50±0.60 197.10±7.77 38.30±1.79 36.18±2.05 P. assimilis Litt�e Shearwater 191 24.65±1.24 8.06±0.59 5.97±0.57 182.22±8.15 38.01±2.00 36.73±0.16
considerab�e over�ap in size and shape. In a�� other cases, the size and shape of the sympatric species over�ap on�y s�ight�y or not at a��. A more detai�ed ana�ysis of sympatric species revea�s that other iso�ating mechanisms besides size and shape variation—s�ch as differences in the time of breeding, in the method of feeding, in feeding �ocation or in nest type—may be �sed by Puffinus species to red�ce interspecific competition (Tab�e 3).
Sex�al size ��imorp�ism
Of seven MANOVAs for which the interaction term (sex × pop��ation) was inc��ded and for which data were s�fficient, on�y
one showed a significant interaction (P. griseus: Wi�ks l = 0.12, F24,57 = 1.99, P = 0.02; Tab�e 4). A �onferroni correction for m��tip�e testing indicates effective�y no significant interaction. This res��t indicates that, in Puffinus, sex and co�ony can be treated as non-interactive variab�es.
Significant differences were fo�nd (Tab�e 4) between the sexes of P. assimilis (Wi�ks l = 0.84, F6,73 = 2.33, P = 0.04), P. carneipes (Wi�ks l = 0.48, F6,26 = 4.63, P = 0.003), P. griseus (Wi�ks l = 0.76, F6,68 = 3.59, P = 0.004), P. lherminieri (Wi�ks l = 0.86, F6,94 = 2.54, P = 0.03), P. nativitatis (Wi�ks l = 0.68, F6,49 = 3.92, P = 0.003), P. pacificus (Wi�ks l = 0.74, F6,128 = 7.63, P < 0.0001) and P. tenuirostris (Wi�ks l = 0.73, F6,72 = 4.53, P = 0.0006).
Ma�es tend to be the �arger sex for most morphometrics, b�t this is not invariab�e (Tab�e 5). In on�y one instance of a fema�e being
�arger was the ANOVA significant (P. yelkouan: WL: WL: F1,16 = 9.79, P = 0.0065). Samp�e sizes were genera��y sma�� for those species in which fema�es were fo�nd to be �arger in one morphometric or more; however, this was not the case for P. griseus WL (F n = 80,80, M n = 100) and100) and P. assimilis TL (F n = 69,n = 69,69, M n = 79).79).
In Puffinus species, sex�a� size dimorphism as defined for this st�dy (5% difference between the sexes) was expressed on�y in bi�� depth dimensions, with the bi��s in ma�es being deeper (Tab�e 5). The magnit�de of sex�a� size dimorphism was �ow, with the greatest difference being fo�nd for P. mauretanicus �DN. The samp�e size for this species was very sma�� (F n = 6,n = 6, 6, M n = 4), and this �eve� ofn = 4), and this �eve� of), and this �eve� of sex�a� size dimorphism is �ike�y to be an overestimation for this
Fig. 1. Differences in size and shape of 18 Puffinus species as i���strated by a p�ot of canonica� 1 (differences in size) against canonica� 2 (differences in re�ative size and shape).
TABLE 2
Res�lts of t�e canonical ��iscriminant analysis carrie�� o�t on t�e morp�ometric meas�rements
of t�e 1�� species of t�e gen�s Puffinus
Factor loa��ings Canonical 1 Canonical 2 Canonical 3
�i�� �ength 0.64 –0.53 –0.53
�i�� depth at base 0.54 –0.17 0.17
�i�� depth at nares 0.43 –0.2 0.03
Wing �ength 0.77 –0.12 0.38
Tars�s �ength 0.73 0.39 –0.47
Midtoe �ength 0.77 0.32 –0.13
Eigenvectors 28.71 4.55 2.36
Variance (%) 78.3 12.4 6.4
C�m��ative variance (%)
78.3 90.7 97.1
TABLE 3 Morp�ologic, foraging an�� bree��ing parameters of Puffinus species bree��ing at sympatric locations LocationCoexisting speciesBLBDBBDNWLTLMTFee��ing zone aFee��ing met�o��Nest typeEgg laying ��atesSo�rce Montag�e Is, A�stra�iaP. pacificus37.2512.859.23290.3247.9949.34OSSF, CD, PPL��27–29 NovMarchant & Higgins (1990) P. tenuirostris32.4512.01—276.00—52.99OS+PD��20 Nov – 3 DecSch��tz & K�omp (2000a) Lord Howe IsP. assimilis23.307.735.70175.0336.3735.79OSSD, PPL, PD��J��yH�tton (1991) P. pacificus36.5112.539.00287.1448.1049.26OSSF, CD, PPL��DecemberH�tton (1991) P. carneipes42.3216.6212.17316.8655.3457.21NS, OSSF��Mid-DecH�tton (1991) Kermadec Is, New Zea�andP. assimilis25.128.205.87187.7338.9937.33OSSD, PPL, PD��10 J�ne – mid-J��yMerton (1970) P. pacificus41.2614.4410.39310.3751.5553.52OSSF, CD, PPL��12–28 DecCrockett (1975) Western A�stra�iaP. assimilis24.798.105.93174.5837.6636.94OSSD, PPL, PD��21–26 J�neG�a�ert (1946) P. pacificus38.6412.178.95285.4247.8248.46OSSF, CD, PPL��17–22 NovGarkak�is et al. (1998) P. carneipes41.0615.7911.38320.0053.1155.42NS, OSSF��23–30 NovWarham (1958) Hen & Chicken Is, New Zea�andP. assimilis25.548.566.27189.1341.0938.60OSSD, PPL, PD��23 J�ne – 24 A�g�ooth (2000b) P. gavia34.019.166.93208.4043.2040.98NSPPL��Late Sep – ear�y OctMarchant & Higgins (1990) P. carneipes39.9815.4711.39324.6154.2056.90NS, OSSF��Late Nov – mid-DecFa��a (1934) P. griseus——————OSPD��?Marchant & Higgins (1990) Norfo�k IsP. assimilis24.277.855.94178.3636.6435.96OSSD, PPL, PD��From 7 J��yHermes et al. (1986) P. pacificus39.8912.9810.06303.5150.0652.49OSSF, CD, PPL��Dec – ear�y FebHermes et al. (1986) Tristan da C�nhaP. assimilis25.658.556.39184.2239.7638.58OSSD, PPL, PD��SpringRichardson (1984) P. gravis44.7114.6110.78322.8759.4461.87OSSD, PD��NovemberRowan (1952), E��iot (1957) Seyche��esP. lherminieri26.298.456.57192.7237.6934.79NS, OSSD, PD��, CrOct – MarchFeare (1981) P. pacificus36.6812.688.97281.3947.0548.15OSSF, CD, PPL��End Oct – end NovFeare (1981) Johnston Ato��P. nativitatis30.6810.797.53244.1043.5242.65OSPPLUnLate Mar – ear�y MayAmerson & She�ton (1976) P. pacificus38.5812.308.72288.6947.7849.32OSSF, CD, PPL��Late J�ne – ear�y J��yKing (1974) NW Hawaiian Is.P. nativitatis30.7910.567.72246.3344.4842.80OSPPLUnApri� – J�neAmerson (1971), King (1974) P. pacificus38.8612.738.91293.9948.7549.78OSSF, CD, PPL��, Cr, UnMid-J�neHarrison (1990) Marsha�� IsP. nativitatis30.3811.337.94240.9243.3742.13OSPPLUnApri�Amerson (1969) P. pacificus39.1612.818.98290.1747.9649.39OSSF, CD, PPL��Mid-J�neKing (1974) Phoenix IsP. lherminieri25.118.136.17192.5237.2734.36NS+SD, PD��A�� yearKing (1967, 1974) P. nativitatis30.6910.837.82243.0044.2341.94OSPPLUnKing (1967, 1974) P. pacificus37.4112.849.02289.2047.2348.58OSSF, CD, PPL��Late Nov – ear�y DecGarnett (1984) Christmas IsP. lherminieri26.188.216.30197.8335.5435.01NS+SD, PD��MarchSchreiber & Ashmo�e (1970) P. nativitatis30.6811.148.07246.4943.9442.64OSPPLUnA�� year, peak Oct–JanSchreiber & Ashmo�e (1970) P. pacificus37.2612.098.78286.4146.9448.66OSSF, CD, PPL��, CrLate J�ne – J��yGa��agher (1960) a Schreiber & ��rger (2001). �L = bi�� �ength; �D� = bi�� depth at base; �DN = bi�� depth at nares; WL = wing �ength; TL = tars�s �ength; MT = midtoe �ength; SF = s�rface feeder; CD = contact dipper; PPL = p�rs�it p��nger; �� = b�rrow; OS = offshore feeder; PD = p�rs�it diver; SD = s�rface diver; NS = nearshore feeder; Cr = crevice; Un = �nder tree or b�sh.
species. The observed sex�a� size dimorphism in the bi�� depth was statistica��y significant even after a��owing for overa�� body size (as meas�red by TL) in a�� cases b�t P. mauretanicus �DN (Tab�e 5).
Geograp�ic variation
For species in which a significant difference was fo�nd between the sexes (Tab�e 4), geographic variation of ma�es and fema�es was ana�ysed separate�y. MANOVAs (Tab�e 4) confirmed significant morpho�ogic differences between pop��ations of P. assimilis (M: Wi�ks l = 0.02, F48,112 = 3.02, P < 0.0001; F: Wi�ks l = 0.01, F54,102 = 2.48, P < 0.0001), P. griseus (M: Wi�ks l = 0.02,
F24,29 = 2.44, P = 0.01), P. lherminieri (M: Wi�ks l = 0.02, F60,173 = 3.32, P < 0.0001; F: Wi�ks l = 0.01, F60,162 = 3.93, P < 0.0001), P. nativitatis (F: Wi�ks l = 0.04, F36,73 = 2.18, P = 0.003) and P. pacificus (M: Wi�ks l = 0.03, F78,238 = 2.85, P < 0.0001; F: Wi�ks l = 0.03, F96,267 = 2.38, P < 0.0001).
DISCUSSION Sympatric congeners
As noted by �rooke (2004) and fo�nd in a�� b�t one case in this st�dy, sympatric Puffinus congeners show �itt�e or no over�ap in
TABLE 4
Res�lts of MANOVAs an�� ANOVAs for geograp�ic variation an�� sex�al size ��imorp�ism
Species Test n MANOVA BL BDB BDN WL TL MT
P. assimilis Interaction 120 NS NS NS NS NS NS NS
Sex 80 a NS b b NS NS NS
Pop��ation (m) 36 c b b b c c c
Pop��ation (f) 34 c b a b c b c
P. auricularis Sex 4 — NS NS NS NS NS NS
P. bulleri Sex 18 NS NS NS NS NS NS NS
P. carneipes Interaction 21 NS NS NS NS NS NS NS
Sex 33 b NS c c NS NS a
Pop��ation (m) 11 NS a a a NS NS NS
Pop��ation (f) 10 NS NS NS NS NS NS NS
P. creatopus Sex 13 NS a NS NS NS NS NS
Pop��ation 4 — a NS NS NS NS NS
P. gavia Sex 16 NS NS a a NS NS NS
Pop��ation 6 — NS a NS a a a
P. gravis Sex 29 NS NS NS NS NS NS NS
Pop��ation 7 — a NS NS NS NS NS
P. griseus Interaction 34 a NS NS NS a NS NS
Sex 75 b b a b NS c a
Pop��ation (m) 18 a NS NS NS a NS NS
Pop��ation (f) 16 NS NS NS NS NS NS NS
P. huttoni Sex 37 NS a a NS NS NS NS
P. lherminieri Interaction 94 NS NS NS NS NS NS a
Sex 101 a a a a NS NS NS
Pop��ation (m) 48 c c c c c c c
Pop��ation (f) 46 c c c c c c c
P. mauretanicus Sex 4 — NS a a NS NS NS
P. nativitatis Interaction 54 NS NS NS NS a NS NS
Sex 56 b c c b NS b NS
Pop��ation (m) 26 NS NS NS NS a a NS
Pop��ation (f) 28 b NS NS NS b NS NS
P. newelli Sex 9 NS NS NS NS NS NS NS
P. opisthomelas Sex 16 NS a b a NS NS NS
Pop��ation 6 — NS NS NS NS NS NS
P. pacificus Interaction 129 NS NS NS NS NS NS NS
Sex 135 c b c c NS NS NS
Pop��ation (m) 61 c c c c c c c
Pop��ation (f) 68 c c c c c c c
P. puffinus Interaction 20 NS NS a b NS NS NS
Pop��ation 23 NS NS NS NS NS NS NS
Sex 27 NS NS NS NS b NS NS
P. tenuirostris Sex 79 c a c c NS NS NS
P. yelkouan Sex 18 NS NS NS NS b NS NS
a P < 0.05. b P < 0.01. c P < 0.001
�L = bi�� �ength; �D� = bi�� depth at base; �DN = bi�� depth at nares; WL = wing �ength; TL = tars�s �ength; MT = midtoe �ength; (m) = ma�e; (f) = fema�e; — = ins�fficient data; NS = nonsignificant.
TABLE 5 Comparison of Puffinus mean female (F�� an�� male (M�� morp�ometrics an�� average sex�al size ��imorp�ism calc�late�� as t�e ��ifference between male an�� female means expresse�� as a percent of t�e male mean. Negative val�es in��icate variables in w�ic� t�e female was t�e larger sex. Bol�� text in��icates a significant ANCOVA (a = 0.05��. S�a��e�� cells in��icate sex�al size ��imorp�ism (i.e. >5% ��ifference between t�e means of t�e sexes�� SpeciesBill lengt�Bill ��ept� at base Bill ��ept� at nares Wing lengt� Tars�s lengt� Mi��toe lengt� FM%FM%FM%FM%FM%FM% P. assimilis24.3824.871.977.868.224.385.��16.125.07181.56182.790.6738.0637.97–0.2436.4037.021.67 P. auricularis31.3231.03–0.939.8410.112.677.437.500.93229.33225.83–1.5545.2545.08–0.3841.8542.080.55 P. bulleri40.8241.511.6613.6214.194.0210.1910.624.05283.34289.071.9851.2952.151.6552.6452.870.44 P. carneipes 40.4741.933.4815.4016.526.7811.2712.137.09319.14319.720.1854.1354.640.9356.4257.261.47 P. creatopus41.1242.603.4715.6516.756.5711.9512.393.55332.16333.880.5255.4455.450.0258.8958.900.02 P. gavia32.6833.251.71��.9��9.475.176.957.193.34204.94206.910.9541.8942.200.7339.8240.411.46 P. gravis44.6846.022.9114.4715.245.0510.8611.283.72322.81321.54–0.3958.7759.651.4861.7762.961.89 P. griseus40.6442.023.2813.0813.442.689.529.893.74292.51289.98–0.8756.1356.891.3455.2255.620.72 P. huttoni35.3836.583.289.4��10.055.677.127.515.19219.46220.890.6541.3542.292.2240.8641.311.09 P. lherminieri26.6327.332.568.438.804.206.326.675.25196.11198.040.9738.0738.521.1735.8536.461.67 P. mauretanicus38.4039.452.6611.4211.843.558.469.127.24245.33247.170.7448.1248.560.9145.7645.73–0.07 P. nativitatis30.5231.432.9010.5411.135.307.55��.127.02246.52249.181.0743.9644.932.1642.5042.961.07 P. newelli32.7933.762.8710.6910.811.117.667.46–2.68232.53235.111.1046.7347.291.1843.5744.101.20 P. opisthomelas35.5337.394.9710.��411.636.79��.12��.6��6.45241.01239.26–0.7345.4145.860.9843.6044.101.13 P. pacificus38.0938.841.9312.6113.093.678.989.364.06292.36293.600.4248.5448.810.5549.8850.070.38 P. puffinus34.6035.071.3410.1910.502.957.847.961.51234.11237.021.2344.7145.381.4842.2943.141.97 P. tenuirostris31.4532.192.3010.��511.465.327.74��.195.49264.69269.431.7650.8851.040.3151.2051.791.14 P. yelkouan35.1435.751.7110.2210.674.227.848.143.69234.23230.41–1.6645.3945.851.0042.7343.140.95
size and shape, indicative of a mechanism to red�ce interspecific competition. Those sympatric species that did over�ap in size and shape (P. nativitatis and P. newelli) red�ce interspecific competition by segregation of nesting habitats, with P. nativitatis s�rface-nesting at �ow a�tit�de on is�ets and ato��s and P. newelli b�rrow-nesting in�and at high a�tit�de (Harrison 1990). Other means by which sympatric Puffinus congeners may red�ce interspecific competition for reso�rces inc��de segregation of breeding seasons, foraging zones, prey type and prey size (�rown et al. 1981, Stone et al. 1995, Monteiro et al. 1996, Sch��tz & K�omp 2000). Like a n�mber of seabirds, shearwaters forage opport�nistica��y depending on the avai�abi�ity of prey in their preferred habitat (Harrison et al. 1983, Spear et al. 1995, �a��ance et al. 2001). Conseq�ent�y, differences in habitat are hypothesized as being more important than differences in prey se�ection in enab�ing co-existence (�a��ance et al. 2001).
�ody size can often be �sed to predict the o�tcome of interference competition (�a��ance et al. 2001, Hamer et al. 2001). Historica��y the differences in size between sympatric congeners may have provided a means by which species have been ab�e to co-exist.
Now, however, with red�ced habitat avai�abi�ity for many breeding seabirds, s�ch differences in size may be res��ting in increased interference competition, possib�y at the expense of the sma��er congener. For examp�e, at the Poor Knights Is�ands, New Zea�and, P. bulleri are disp�acing gadf�y petre�s Pterodroma spp. and P. gavia (Harper 1983). Simi�ar�y on the Azores, interference competition among petre�s has res��ted in the sma��er species, inc��ding P. assimilis, being confined to c�iffs (Monteiro et al. 1996, Ramos et al. 1997). S�ch sit�ations may res��t in higher intraspecific competition for nest sites or in decreased breeding s�ccess, or both (Monteiro et al. 1996, Ramos et al. 1997).
Sex�al size ��imorp�ism
Effective�y, no significant interaction was fo�nd between sex and pop��ation, indicating that no geographic variation in the magnit�de of sex�a� size dimorphism occ�rs. The se�ective press�res being exerted on ma�e and fema�e Puffinus therefore do not differ significant�y over the species’ ranges.
In birds, the average size difference between the sexes is 5%–10%
(Amadon 1959). �ased on the res��ts of the present st�dy, Puffinus species exhibit �ow �eve�s of sex�a� size dimorphism. Significant differences in morphometrics were fo�nd between the sexes of P. assimilis, P. carneipes, P. griseus, P. lherminieri, P. nativitatis, P. pacificus and P. tenuirostris. A�tho�gh ma�es were genera��y
�arger in a�� morphometrics, sex�a� size dimorphism (i.e. a 5%
difference) was expressed on�y in the bi��-depth parameters. �i��s are �sed for feeding and aggressive enco�nters and are pres�mab�y m�ch more prone to se�ection for dimorphism than are wings and
�egs, which are �sed for �ocomotion and are �ike�y to be an optim�m physica� dimension in re�ation to body size (Agnew & Kerry 1995).
�eca�se of its d�a� ro�e, the adaptive significance of sex�a� size dimorphism in the bi�� has been the topic of m�ch debate (Hedrick
& Teme�es 1989, Shine 1989).
Nat�ra� se�ection attrib�tab�e to eco�ogic differences between the sexes may ca�se sex�a� size dimorphism (Shine 1989, Andersson 1994). The intersex�a� food-competition hypothesis proposes that sex�a� differences in size might evo�ve from niche partitioning between the sexes as a mechanism to red�ce intersex�a� competition for food (Se�ander 1966, 1972). Sex�a� differences in foraging zones, migration ro�tes, diet composition and prey size have been
reported for seabirds (Gi�ardi 1992, Kato et al. 1996, Weimerskirch et al. 1997, Gonzá�ez-So�ís et al. 2000, Forero et al. 2002). These differences may occ�r at any stage of the breeding and non- breeding seasons.
St�dies of Puffinus foraging and food-provisioning strategies are fair�y we�� represented in the �iterat�re for severa� species (Rick�efs 1984, Montag�e et al. 1986, Lang�ands 1991, Hamer & Hi�� 1997, Hamer et al. 1999, �ooth et al. 2000a, Sch��tz & K�omp 2000, G�icking et al. 2001), a�tho�gh few have investigated the ro�es of the sexes. Perrins & �rooke (1976) identified different foraging gro�nds �sed by the sexes of breeding P. puffinus from Skokho�m and Skomer Is�ands d�ring the pre-�aying exod�s: fema�e P. puffinus foraged in the rich sardine fishery in �iscay �ay, whi�e the ma�es remained c�ose to the co�ony. F�rthermore, Gray & Hamer (2001) fo�nd that, d�ring the breeding season, the mean foraging trip d�ration was significant�y �onger for fema�e P. puffinus than for ma�es, indicating the possib�e �se of different foraging zones.
With regards to sympatric species, Johnson (1966) wrote that “�i��
�ength may be on�y partia��y satisfactory in revea�ing differences in foraging niche ... beca�se divergence in bi�� width and/or bi�� depth between congeners can striking�y a�ter bi�� shape and f�nction when bi�� �ength is constant.” This concept co��d be app�ied to differences in bi�� shape between the sexes. �i�� depth is an important factor in determining the snapping power of a bi��, and it has been hypothesized that ma�es with deeper bi��s sho��d have a better hand�ing performance for powerf�� prey than sho��d fema�es (Ashmo�e 1968, Koffijberg & Van Eerden 1995). However, beca�se of diffic��ties associated with obtaining dietary samp�es (partic��ar�y with respect to rates of digestion), �itt�e information exists abo�t Puffinus prey size. It is therefore �nknown whether sex�a� size dimorphism in Puffinus bi�� morpho�ogy is attrib�tab�e to intersex�a� competition for food items of different size.
The sex�a� se�ection hypothesis proposes that, within one sex, characteristics that confer an advantage in either competition for mates (intrasex�a� se�ection) or mate choice (intersex�a� se�ection) are se�ected for (Darwin 1871). Evidence s�pporting sex�a�
se�ection in Puffinus species wo��d be that, in ma�es, a deeper bi��
confers some advantage (reprod�ctive or s�rviva�) over a sma��er bi��. Ma�e Puffinus genera��y take the predominant ro�e in obtaining and defending a b�rrow (�rooke 1990, Warham 1990). Fights may ens�e over nest ownership, d�ring which the bi�� is the primary weapon (Ne�son 1979). If deeper bi��s in ma�es convey an advantage in nest attainment or defence, we wo��d expect that characteristic to be se�ected for in co�onies in which high intraspecific competition for nest sites occ�rs. �rooke (1990) described high intraspecific competition for P. puffinus nest sites at Skomer Is�and, Wa�es, and fo�nd significant differences between the sexes in bi�� size.
Fema�e mate choice, which may res��t in �ong-term fitness conseq�ences, cannot be e�iminated as a mechanism for the observed sex�a� size dimorphism in Puffinus species (Forero et al.
2001). �eca�se members of Puffinus species, �ike other seabirds, are monogamo�s and exhibit high mate fide�ity, mechanisms for mate choice wo��d be diffic��t to detect (Warham 1990, �arbra�d 2000). However, P. tenuirostris do exhibit significant assortative mating with respect to age and bi�� depth (Meathre� & �rad�ey 2002). Assortative mating may arise from either active mate choice by one or both of the sexes or thro�gh passive contact between phenotypes (Forero et al. 2001). Meathre� & �rad�ey (2002)
s�ggest that beca�se assortative mating based on age and bi�� depth in P. tenuirostris is a predictor of breeding s�ccess, mate se�ection may be adaptive.
�oth sex�a� se�ection and nat�ra� se�ection can inf��ence the evo��tion of the same trait to different degrees (Shine 1989, Wittze��
1991, Fitzpatrick 1999, Forero et al. 2001). F�rthermore, the forces maintaining sex�a� size dimorphism may be different from those that ca�sed it, making ascertainment of the origina� ca�ses of its evo��tion diffic��t (Perry 1996, Szeke�y et al. 2000). Neverthe�ess,
�ong-term morphometric and breeding st�dies, and remote-tracking and feeding st�dies, are necessary to obtain a better �nderstanding of the processes responsib�e for sex�a� size dimorphism in Puffinus bi�� size.
Geograp�ic variation
Typica��y, 50%–90% of the body-size difference between individ�a�s is attrib�tab�e to genetic ca�ses (�oag & van Noordwijk 1987);
the remaining 10%–50% of the difference is attrib�tab�e to environmenta� ca�ses (�rooke 1990). Se�ection press�res vary according to �ocation, beca�se pop��ations of a species m�st adapt to the �oca� conditions, often res��ting in geographic variation in characteristics (Mayr 1963, End�er 1977, Wike�ski & Tri��mich 1997, Lovich et al. 1998). It is �n�ike�y that any sing�e factor may be responsib�e for variation in size, b�t rather a combination. The potentia� for geographic variation increases with the n�mber of is�ands that a species occ�pies (Mayr & Diamond 2001). This appears to be the case in Puffinus species, beca�se significant intraspecific variation was fo�nd on�y in species with widespread breeding distrib�tions (see Appendix 1). Species whose pop��ations are distrib�ted over a wide range are �ike�y to be exposed to differing c�imatic environments.
Once f���y deve�oped, ske�eta� str�ct�res sho��d be �itt�e affected by the environment, b�t d�ring deve�opment, food avai�abi�ity or even temperat�re might inf��ence expression of the genotype (D�ffy 1987). The growth patterns of Puffinus species are simi�ar to those of other petre�s; that is, a rapid growth in tars�s, re�ative�y s�ow increase in bi�� �ength and intermediate growth in wing �ength (Pettit et al. 1984, �rooke 1990, Warham 1990, �ooth et al. 2000b, Saffer et al. 2000). Conseq�ent�y, intraspecific differences in wing and bi�� morpho�ogy may be re�ated to differences in the post- f�edging environment, b�t differences in tars�s morpho�ogy may be attrib�tab�e to s�ch factors as the age and experience of the parents, c�imatic conditions, and the avai�abi�ity and q�a�ity of reso�rces (Saffer et al. 2000).
Ecogeographic r��es imp�y patterns of variation based on corre�ation with environmenta� and c�imatic conditions (Linco�n et al. 1998).
Probab�y the most we��-known and debated are the �ergmann and A��en R��es (McNab 1971, Geist 1987). Proce��ariiform seabirds trave� vast distances and spend extensive periods at sea (Weimerskirch et al. 1988, Spear et al. 1995, K�omp & Sch��tz 2000). Many of them ret�rn to �and on�y to breed and, �n�ike many
�and birds, are not constrained to one set of c�imatic parameters.
Therefore, among proce��ariiform seabirds, patterns of geographic variation are �n�ike�y to be a res��t of a thermoreg��atory response, as is proposed by the �ergmann and A��en R��es. A�tho�gh the
�ergmann R��e has been described for P. pacificus (M�rphy 1951), statistica� methodo�ogy (partic��ar�y m��tivariate ana�ysis) has advanced since that time, and the pattern therefore warrants re- examination (���� 2002).
The magnit�de of variation in morphometrics was simi�ar between the sexes in species (P. assimilis, P. lherminieri and P. pacificus) for which both ma�es and fema�es exhibited geographic variation.
F�rthermore, the geographic variation was attrib�tab�e to a combination of differences in a�� traits of both sexes. This finding may indicate that the se�ective forces shaping the sexes are simi�ar over the species range. In comparison, on�y one sex of P. griseus (ma�es) and P. nativitatis (fema�es) exhibited significant geographic variation. F�rthermore, that variation was a res��t of differences in the wing �ength over each species’ range. Wing morpho�ogy is affected by press�res of migration, foraging, sex�a� se�ection and predation (Ain�ey 1980, A�ata�o et al. 1984, Hedenström & Mø��er 1992, Marchetti et al. 1995, Mø��er et al. 1995, Copete et al.
1999, Voe�ker 2001). Differences in the wing �ength co��d ref�ect differences in the eco�ogic sex ro�es over the species range. Long pointed wings are more cost efficient for �ong-distance f�ights (Savi�e 1957), therefore differences in foraging range between the sexes may res��t in differences in wing morpho�ogy. In Wandering A�batrosses Diomedea exulans breeding in the I�es Crozet, sex�a� size dimorphism in wing morpho�ogy was fo�nd to have a f�nctiona� ro�e in f�ight performance, which in t�rn inf��ences the at-sea distrib�tion of ad��ts and f�edg�ings (Shaffer et al. 2001). Shaffer et al. s�ggested that the differences in wing �oadings made it more optima� for ma�es to forage in the windier s�b-Antarctic and Antarctic regions, with ad��t fema�es and j�veni�es being better adapted to exp�oit the �ighter winds of the s�btropica� and tropica� regions.
ACKNOWLEDGEMENTS
We thank the co��ection managers and c�rators of the bird co��ections in the American M�se�m of Nat�ra� History (New York, USA), the Nationa� M�se�m of Nat�ra� History (Smithsonian Instit�tion, Washington, DC, USA), the Nat�ra� History M�se�m (Tring, UK), the Nationa� M�se�m of New Zea�and Te Papa Tongarewa Te Papa Tongarewa (We��ington, New Zea�and), and the A�stra�ian M�se�m (Sydney, A�stra�ia) for access to specimens and faci�ities. Expenses inc�rred for trave� to these m�se�ms were financed by grants obtained by LS� from the American M�se�m of Nat�ra� History (Co��ection St�dy grant), the Roya� Society of New Zea�and (H�tton F�nd) and the Victoria University of We��ington Science Fac��ty. This work has benefited from disc�ssions with, or comments on ear�ier drafts by, Char�es Da�gherty, John Haywood, �r�ce Norris, Sandy
�art�e, Stephanie Rowe, Kate McA�pine, Phi� Garnock-Jones, Richard C�thbert, St�art �rad�ey, Andrew Styche, and everyone in the “hatchet” gro�p. Last�y, the a�thors thank the editor and two anonymo�s referees for their constr�ctive comments, a�� of which improved this paper.
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APPENDIX 1
Bree��ing localities an�� sample sizes of 1�� Puffinus spp. sample��
P. assimilis P. auricularis P. bulleri P. carneipes P. creatopus P. gavia P. gravis P. griseus P. huttoni P. lherminieri P. mauretanicus P. nativitatis P. newelli P. opisthomelas P. pacificus P. puffinus P. tenuirostris P. yelkouan
A�ck�and Is, SPO 3
Antipodes Is, SPO 6 2
A�stra� Is, SPO + 7 3
Azore Is, NAO 1 2
�erm�da 3
�onin Is, NPO 6
Canary Is, NAO 5 + Caribbean is�ands 51
Caro�ine Is, NPO 4 +
Chatham Is, SPO 7 2
Tierra de� F�ego, Chi�e 8
Campbe�� Is, SPO 9
Cocos-Kee�ing Is, IO 2
Cook Strait is�ands, New Zea�and + 19 +
Corsica, MED 1
Cape Verde Is, NAO 18 10
Easter Is, PO 2
Fa�k�and Is, SAO 1 1 Faroe Is, NAO 3
Fiji, SPO + 30
France 5
Ga�apagos Is 53
Gambier Archipe�ago, PO 17 +
Greece 5
G�ada��pe Is, NPO 10
Ha�raki G��f is�ands, New Zea�and 10 16
Hawaiian Archipe�ago, NPO 66 48 146 Ice�and 2
Irish Sea region 43
Ita�y 8
Johnston Is, PO 6 32
J�an Fernandez Is, SPO 18
Kermadec Is, SPO 43 53
Lord Howe Is, TAS 23 38 33
Kiribati, PO 2 27 22
Macq�arie Is, SO 7
Ma��eira Is, NAO 11 + Ma�dive Is, IO 5
Ma�ta 2
Marc�s Is, NPO 1 3
Marq�esas Is, PO + 17 15
Marsha�� Is, NPO 4 11
Ma�riti�s, IO + 12
Is�a de �a Mocha, SPO 7
Is�a Natividad, SPO 4
Norfo�k Is, TAS 23 +
Ni�e, PO 4 Northern north is�ands, New
Zea�and
20 + 43 4
New So�th Wa�es, A�stra�ia 1 40 1
Panama 11
Pe�ew Is, PO 54
Phoenix Is, PO 61 18 45
Pitcairn Is, SPO 21 +
Q�eens�and, A�stra�ia 3
Ré�nion Is, IO 6 1
Sa�vage Is, NAO 4
Samoa, PO 11 +
Revi��agigedo Is, NPO 13 12
Seyche��es gro�p, IO 25 23
Snares Is, SPO 8
Society Is, PO 2 13
So�thern so�th is�ands, New Zea�and
19
So�th Western A�stra�ia 4 12 3 +
Tasmanian is�ands, A�stra�ia + 3
Tristan da C�nha gro�p, SAO 4 13
T�rkey
Van�at�, SPO 1 4
Victoria, A�stra�ia 18
Vo�cano Is, NPO 9
Wake Is, NPO 3 8
Mariana Is, NPO +
St. Pa�� Is, IO + +
Kaiko�ra, New Zea�and 21
New Ca�edonia, SPO +
So�omon Is, SPO +
So�th A�stra�ia + +
Chagos Archipe�ago, IO + +
Cargados Carajos Shoa�s, IO +
Comoros Is, IO +
�a�earic Is, MED 7
San �enito Is, NPO +
Newfo�nd�and, Canada +
Massach�setts, USA +
Sardinia, Ita�y 1
Tonga, SPO +
SPO = So�th Pacific Ocean; NAO = North At�antic Ocean; NPO = North Pacific Ocean; IO = Indian Ocean; MED = Mediterranean Sea;
PO = Pacific Ocean; SAO = So�th At�antic Ocean; TAS = Tasman Sea; + = breeds at that �ocation, b�t not samp�ed for this st�dy; shaded ce��s = species no �onger breed at those �oca�ities.
P. assimilis P. auricularis P. bulleri P. carneipes P. creatopus P. gavia P. gravis P. griseus P. huttoni P. lherminieri P. mauretanicus P. nativitatis P. newelli P. opisthomelas P. pacificus P. puffinus P. tenuirostris P. yelkouan
APPENDIX 1 (contin�e����
