Arid-zone adaptations of (Aves: Charadiii): • . " ..... ' '; ;! . I ~.; .• !" I:! .' . -;',

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G.L. Maclean Department of Zoology, l:Jniversity of Natal;Pietermaritzburg

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i; :.If-: :/( .:•... ~-y""1 ~ ~J f~ de i.~ :.~ ~? .: 1~-;u f '~f.-~ ": :~\/i H L:j; (ll \ ~~ ..' i ~ : c:;:; f:! j~; . ' ! .' . '\, '. ( , :1'" , ',.' ~

,,','~ " Waders ( of the subdrder Charadrii) have radlate(t~nl~Hhl:f\ sevhai '~oups of ~~dets (th~adriiformes, Charadrii) ''tiliy1'' arid zOnes of the world through the successfuLus&,0f,adaplatiOns given rise to arid-adapted species, or even entire familiCII~lThe' formerly evolved in response to a marine or bracKi~;@~~li~.,,: most notable of these are the (,::;Olt­ These preadaptat;ons are traced thro~g/:l.'1~~, 1'AAjoUl~~ soriinae), the pratincotes '(Glareolidaej'.';,Olareolinae),vthe of wi1d~er radiation, endinq in such highly Sp~?!~H~E1P t~~(\a~ m~ ~n~rouse (family Pter~lidae),. which re~ined~~i~:~i~~ .~~~P,~~; seed (Thinocoridae) and the plovers (Charadriidae),,1fhe t/ons or evolved furth~~ iidaptat/ons to SUIt th~m. to a dIet of '_ phylogeny of these groups within the suborder Char:umi.:tias $SeCts 'i1.r;'Ic;i t~e, need tP'p!ink In ;i~!l el1,\/il.onment JlqPL,~\1~urr'i1G~' ," been the subject of several major studies (Fjeldsa 19'16{Jehl wCI-,ter,,' . ,-: "':, ! ';.'''1:, ·'i.: "'i:'~"".' 1968; Sibley, Corbin & Ahlquist 1968; Strauch 19?8):frofu S. Atr, J. Zool, 1QS4,l9; 78:';" at : which>'it is iiJ.creasmgly clear ~:that certaitl·'features,·'of'tlle • , .. ' ,;",,:_" r .'! r;. .'-;n:;. ' .....IL 1 ,\ 1::-\ . :'I":'! to, -(.;'i;);:;!~·-.; i ," 1 suborder are highly!sigriifieanr'in the\ dael'ttlrhirli6n' '{)'ftela- Waadvo~ls (onderorde CijarCi9.rii) he" i~ dis dQ[re ge9~el~ van- . [ tionshi1Js within it. r. 'l 'J ',J:'.".,,', ", •• "\\,' di~~~r~!~ ver;spr~i ,dew ,d~d>4~~~\IgIJe g~t;lr~i~ ,v~nlaqIJPflr>~ing~, wat vroe~r ontwikkel is in reaksie op see- of brakwater-kushabit?~) It iHLlso clear that theCharadrii as a grouti\hctVe'hlt.'l1q,\\gtrc Hierdie voorafaanpassings kan deur die hooflyne van waad­ origin~ whether marine of freshwater' :,:.... :/ifuath'a't'the\aftd­

~Ievolusie

. nagespoor word tot sulke hooggespesialiseerde

) wne taxa are more recent offshoots from the aquatic an~l7S.

0 groepe soos die sandpatryse (familie Pteroclidae).

1 It is JJlY intention t() show, how the basic anatomkaL..and

0 ,}j~~d~:Ql:oejJd=leJ ~~~~~cI!1:~lWlI,~irg~·y~rlyn, ~ ~~~a!\

2 physiological equipment evolved by the waders iW\the.iWater,­

d side (especially the marine water.nde) are th~\very;samefea1ures e :Va~i~~~~~h~k~~~:;~~~~~~r 'i~'f~-~~~i~i~:~~;~~i~~irJ': ~": t aangepas geraak het." " . . , .. , ' ,.. ..' '. . '-' .1" a that have preadapted tnemHo>the desertN)(;the'.worlck' • d (.'.;

( S.-Atr. T1~C/~r.. [)ierk" 1'?84, 19: 78 - 81 r phylogeny e L' ,_ ,.'':,l[;dj... j h s i , -i'.:" '.,'. Tht;SJit~ria on w9ich family tr~s of waders I;J.JI.,y,~,b~ 4r:~y.:n l ,l!::', .. '.' b up include, most importantly, adult and neonatal plumage pat­ u

P , osteology, anatomy, behaviour and breedingbiotO~. e RelatiOnship with any rriiljor order of birds cari'.be'~Iili1i~rr&l h t with certainty by 'an' analysis of egg-white ptbtelfi.s'(Sibi~Y& y

b ,I.,' ',•. \ , .. " Ahlqwst 1972), on the basis of which tti~"t;tdeI"t:hahitlffi­ d e formes is shown to 'be a n~tural one_ 'OSil!6lokJ'8ll' e\1t1en\k t .'.". ' ....' \", n points10 a major dichotomy hl~o the'S@l&p\id(of~oi'Op~­ a r .. \ .. \ .... "'",. coidea) on the one hand and the g Charadi1i'(ofChfu%ttl~UaM)

,,;,; e on the other (Strauch 1978) with a third branch leading;to.tile c , :. i I j ~,' f n Alcae,(auks) which will noLbe cons~derejiher.e,Another;.arid­ e c i adapted family of birds, the'Ptevoclidail (lWldgroose.) .,falls l

r within the limits of charadriiform egg-whlt.C\p",)teiJ1;~s, e d and sahdgrouse possess mlmy ·other charadriifol'tif. featUres n u

(Maclean 1967a). However ,theitclose oSteoiogibit resembtan& y a • I with the doves [Columbidae, Columbiformes (S'~!J\q,mm)rz ;,! .:,' I;~' w

e [ilt.; ~~egmann 1969)] in,dicates that the san'4viR~ ~l}qm9J~ t a ,_:, i:·.·. regard¢ as an in~erJllediate 9rd~ of their own (Pt~9C;W:qr:m~) G whos~;~haradriiform affinitieso/ilfe very close, andJN,lll~\will t e 1,1/1'.',;',1. ,;,,',' \ \ n therefQfe be includep in this account. i b Of the five taxa to be considered - seedsn.ipe,,(;ouc~rg, a S

, plovers and - the seedsnipe ar,e ex­ y b clusively Neotropical, the coursers,

pr~i11C()lesha.nd ~~ii-6\t~ G.L. Maclean. d Afrotropical, Palaearctic and oriental; )lave e 'whlIe tne plbvers

c Department of Zoology, University of Natal, Pietermaritzburg, u 3201 Republic of South representatives in all the world's deserts. The afrIDities of the d

o seedsnipe within the have long been open to r

p Received 8 August 1983; accepted 5 January 1984 question, but the weight of osteological evidence points to an e R S. Mr,· L Zoo!. 1984. 19(2) 79

early divergence from scolopacoid stock (Strauch,lW;8jt;~y:; are the only arid~adapt~ taxQIl onthatev/illuponary line. The. In sllCtnt) slia)tliCditting is .~ ,to: ~lii inSolatiOn· plovers," coursers: p~~tip~les''aiid' sa~o:~si.'ai~··al .. aerived and low i'ek'lti.ve; humidity i(GiiMt 1982f!GtauILl97~'~iPurdUt' . "." ".. ' .. ':", ':'.;', ,,.,,tJ# .:i'· ,', fr()lll;try.~,ch~~(iI,i(,)iqlin~.". ;: '1!~";., ; "f' ,: 19768" 0; l"Wd~&· H.ain~ .} 001):.' Its! i'ie!.1ffig,erlviidnihenl· ap;; proximates: t~ef6te to i:t::desert·1ri fnattf\\lays-/:Sd that'evefi Basic{~h~mi'driifb"rf~d~p.~lic)riS!. ".. ." '.'" ~ ;: '.' '} :~'.~' .. watersid'e :wader.sf nestuhder' :¢Ondit~ ;that'ireqaire (tneril(to. SiJlfti;~br~.()Cth~.'i~~~,u~~~r;,~~t~~·~;~·~~ri,y~d·;fr()ln!ii' be tbletant ,(jf;heat Joads.·and de5iccatiorr~:tw():emintntly·arid-­ cowm~m, ;Stq~k, ~h,ey,. ~ p~qY,id~iJ!'icj~.c~,f,0f.J;l:~'~ of zone preadaptations;, Thtls latl the·features, for mdeting there:; charadriiform evolutionary trends. The plov~~,(~h¥~4ffulae) ~{In~~ of.~ ~. Q~bj~~,~~,!9Al1~, W~~~ ~t:g~~ ~lley t~dory. th~~hol~Ao,,~.g~f~!·. ~et§~~¢Pt.~m>p1?;, l~n~h.e w.<\t~~~~ !<;>r ~i~ffi!!Q.~Jr~~l~P ~"qEt;{~s~'r~F~ politano Most plovers are aquatic shorebirds iRiJne 1l,rict tfu~'} 4;~j fo~ ~i:th,~ifr;IJ~~~\~~rRf9C~~R.~~:nw.g~ ~()I~~~~e,!~()llle ..1Jl~l~i~ot~r~.fr~h~~~r,. \¥ifB {e:'f; ~~! i~y~~~~~:,p~,;~4,t.mffiIW)1~) \'JMtStL~~~Er~ .. ~~ e~seBHqqs,.b~y, fU"~ 8l~~c.t.~~ 9y,~e~/:l:1~~$1' r~tp~:q~ort' 'r.4t~r;i-thtW:n~~~~~:W~ffWqr.::~~~! fCJf ~~ &fP~s\ anterior toes, reduce4,0{.,~8~n.t :h..i~~ ~dom~·~tech\\l~ngs S~~·JIl,.S~~rt.. !WCl,~~~ ~~~~lP:fRR¥.P~¥:) mcu:~,;~f~%v.#~,pr~i" all(.l~p()W.sh:pms fop,~~~ f~P!sI:1~:p~o9iP.$f:9nJ¥, ~p.r.edt.pi,~i~·,~Rq~!~;i@}ff9tprr,,~~~!W9"'J?~o{Wrd~~ tQ~ m.JQI'fll~j!ly,~~l?I~ b~Y~ ill :~UJ?B,QrJ.jittY; p,~.s~/nWand ~J}i~P~~,~.~~;~!~e4~~"~4js,~~~oW;,~ed ~j~l~;;~!; ~11~l~~~:~'1 ~a~.~~~'9n ~f;:: ,J~~ ;~'i:f;~:';)"',.~ '~'/':,';~' ::.,; :(~';','~ the salt gland (Thomas & Phillips 1~7,IDw~~10tP.~r. ~vers Emrp, 'M~~h~.~~~ ~;~~~t)~P%~,p'w.~~~~,jj~ hJ!r.~,!.~IJJJ~~rqi~a,l: ~.I.'~t .~~ ~~9!~iy~ly:; t;;~~~~t~ i plqy,er,~J~t, ~II)~~c

·.!{iP'~pl8v~Hfejt~f ~qjrHtq Wl.1W~~¥,~~~~~~~~y~~q.l P·lo"'~ts1rt·tHe' . "., difectR%:BP'hbctUfuru'ciCtMty. ,. #tttems, '(Maclean,I . irito a salt gland 9~~!4 ,w.it~;~~JpfPtAAf ~~.,w~t;ers, m"fjtissyWlllch.uanbWYheiiHa refuaii{ili.a~ive'u{theneat' 61'

! . or evolved it in response to such an aquatic habitat, and later dle 'rnty' c:' r icl' g60trtlieritio~Ulat6&'eoondmyi tiheA~uf.e: The )

0 reduced or lost it on becoming freshwater dwellerll>sM~~i ~ged; cOriri£r'.(Ji'tluilC6'jjtenilis erit~tYjhbCtUtrta1;bf 1

0 fOf~; ;l?p~~b!~ ~o, S!-l~!75~ is ,m~lle ~~tfY., fp~ the:pI~v,er~,J~~ ; cieP~cfi'and~lotffetspedtls'faigery s&!ifitbihheebili~ts 2

d deed the occurre%e of~llltg4mq..~;in ~lY:a,I,l ~p~~W;ijfQr.ms tUi~' f~~laft

P ~~~~J~,PYJ~e:Il~~~i!I~.~9tt~~k

e (M~!fjIJlkJ,9.1~p)i!~~)Q~~!#!~ ~~ fWr~Y,Y~~lP ... h t v;"'... ~ r9\«.~CJ"'" i ,r." l·"".+r,,, ..,y .• ;;.,; ,··· .. ·,d ' th .. ,I:lIml't.subf·.. "'il y .-Er""""'-' . "::-~f ~.,., "" ~~: .'f d~ '''''~ ~; .:\';:..:! 1 .~ b Alidzones can' be' loosely: dd'ihed'as 'tht5'seiarid 'slitfacenflat ".>< 09A.ili§W"""i~, . .\qstA9~iW1, ;q~L"J • r'tnw~&'j I :", _ d

e pq~~:i~ A5J!wIy:~~1~J\Wa9~f;lnkGlJ1;tM".~~i~ J t n ~~~~:Ni~~~~~t4~:~~~1~~~~t§~~~L Ime Qf.Qwl!ltiOP..u~hP~t~a~~h I:WH)·J~,~E;Yi~~ ~ . a r w~r!isc.~~ •. t~l;Dperatm"!:li ~·I~l}l:ion.r.ste!\ ~~aJJY, direcrJl';.fi'~~ ~;pIQV~~tJA~Y(~~f9IP~~~ ~~~~ g high. It,thetef01'e·behoves,a,,desert··not tp"r.ely;

r iiilitiri~ '«ra\:ie~,: dferdirtIiffii' WYth (ili~'.ff~tf.ufi,,*h€!it'iU~~Ci: e !ill t6th&' wader;2HIt~s(HciU8PiVfth; t1ieh~d:iffc(t ldii';'thti d :6tl&~~1r~~!~Q~J~~~~:t,~~t~ f" n shbsttate:-/~rt()?-'[l ~·.:~3 c :f~:~';"fHt!) j :-IJ Lh~ fit) {~; :-V)qr':ll~ -; t :·~.11:;1-t w~qeJ:'~ .~Jo ,COl(m.i~i~4~$'Qf~hei \yprJ(tQl¥ln~l

u tlM\t

y !; 'Tbb J"~ietesdtjcida~tea rtfJ"'4ltl~ 'fue-;A~IPi'a¥Dlci)te majOf"step·t().takc :in IthekJeedieg·· eoolog)l"except,that, they Illy f ,Y. . 5JQJ \,.V t, . ~ • a 1

w no longer waded or probed for their food in a wet substrate. Stilrlil' JSiiB€ttfft.ests 061~6hY.ifi?hli~ ~;i!ldifarwater; e t Ho\\r' c6\i1d siiCh cl'cnangein'habitat'h.ti.ie cotne a'66ut? All' usi'iiillyYe'ilip(l,thlj '~'till&idbY" l~' 'i£iWiS') (Nfiitlem a

G aquat\c ~<.tde{s, ,except !pe jascul~, ~~.iP.~'i~~frps91t1<.~9. iI9763).l [the" adlilfbrr~~ ffiiri'ic,"ItP(~ife,~nitiCs :arf fed:=bri1iij] t 2 e a few -pto~ers'and 'scolopa#s':;-pe#'~a~jl~~/R\oW:/w~t?(~,t~ui ~s:\mcfl'todesSi.h~rtb~~ :6~yflUi~:pymdmS;o~~ k'iij:lrii n i wilhin~J~'¥J~\U1Qr..ed.l!1etre§;,oJ;it.,1)leJ)Jt&ic ~lJdet:,~t,i,ng' ofufthl: Salt Waii"f ij~brf&" ~d~' l~6Y?'~:~~iW b a strategy, illustrated typically by the plovers,'oonsists of a. small feptd~nts'fu1 ieVohit\dnifrY S~B~ fri~ehrl~~~~ iliMbf S

y clutcb (maxinihlly'4'@)'ofcryptiCaliy ,tol'dured:eggs ~ia1d{ih:' the true pratincoles (G/afe6'/J); kfu:if~af aFtti~ ')&slffi~rS b a simpl~ scr.a~ in an ~xpo~ site, wit~ a rWnlm~bl ~ ~~8 (MadeaiJ.,:;l976a)~- '," : ,,}., ,,') :,i ,'[;,:c u:;, ,r: ·,:'r; -'lie d e c material. th¢~~Itf#1&\£~~rt:i e~jg~~"~4Qd;.(~!WWtt~J~fel u 6~~~~~~_~,l;,"/ ,,::.:i~.;,:';:, ;' 1'1. :~'~':,~,;;:':;::: ';;J:~~'~i.:~;,;,,:!' d tQj;A~ ~Jy·mJ,b,~ "ijCf;JeX ~,~~J~ ,ff&§~\l§t. o r therefore be inconspicuous, .~lheir Cli)(psia:m"hth!MmalI The two most highly specialized (in a derived sense)Ju.Iadm{ taxa p e R 80 S.-Afr. Tydskr. Dierk. 1984, 19(2)

of the arid zone are the seedsnipe and the sandgrouse. From Conclusions different ancestries (though within the charadriiformes) they Adaptations (including preadaptations) of waders to the arid have converged remarkably in habitat, structure, plumage and zone can conveniently be listed as follows: habits. Both feed largely on plant material, mostly seeds (a) Long legs for rurming; later shortened by highly specialized (Maclean 1969; 1976c). This has led to profound structural sandgrouse and seedsnipe for feeding on the ground on modifications: short legs and bills, robust bodies, small heads small seeds, by taking quick short steps. - indeed an altogether dovelike appearance and method of (b) Short toes for progression over fIrm substrates (in the feeding, and another case of evolutionary convergence. pratincoles and seedsnipe long toes facilitate running over A diet of seeds means a low intake of water, with a resultant stony ground). water deficit in birds, since their kidneys are generally poorly (c) Hind toe reduced or absent (typical cursorial adaptation adapted for water conservation when compared with the kid­ in birds). neys of mammals. This deficit must be made good by the up­ (d) Long wings for strong flight, especially important in take of water in some other form, either as drinking water or nomadic and migratory species, and those that fly frequent­ as preformed water in succulent food. Seedsnipe eat the water­ ly to water to drink (like sandgrouse). rich leaves of succulent or subsucculent green plants. Sand­ (e) Salt-secreting nasal gland for processing saline or hyper­ drink. Seedsnipe are therefore restricted to fog deserts tonic water or body fluids of prey (this gland has on the west coast of South America, or to montane deserts been lost in sandgrouse which drink large amounts of where precipitation, though small, is frequent enough in the relatively fresh water). form of condensed fog or light snowfalls to support a relatively (f) Diet of arthropods; highly specialized forms like seedsnipe substantial growth of water-rich plants. and sandgrouse have become largely seed-eating to capita­ lize on a locally abundant food source. Sandgrouse are not restricted to such desert types and can (g) Open nest site with small clutch of cryptically coloured range widely over the inland continental deserts, provided that eggs. drinking water is available within comfortable flying distance (h) Nocturnal or crepuscular activity patterns. of food resources. This in tum imposes its own kinds of restric­ (i) Secondary dependence on drinking water as a result of a tions which are not the subject of this review, and have been diet of seeds (sandgrouse). dealt with elsewhere (Maclean 1976c). But it is necessary to Transport of water to young in belly plumage of male mention the loss of the salt gland in the sandgrouse; by drinJ(­ G> parent sandgrouse. ing comparatively dilute water and feeding on a salt-poor diet (k) Cryptically coloured dorsal plumage, probably originally of seeds, sandgrouse encounter problems of salt deficit, rather an adaptation to nesting in exposed sites.

than salt loading. The need for a salt-secreting gland falls away, . ) and so does the gland itself. Water conservation remains a high 0 References 1 physiological priority and sandgrouse employ an efficient 0

2 CADE, T.J. & MACLEAN, G.L. 1967. Transport of water by adult method of cloacal water resorption (Thomas & Maclean 1981), d sandgrouse to their young. Condor 69: 323 - 343. e t a process common to many birds so far studied, and therefore FJELDSA. J. 1976. The systematic affinities of , a another preadaptation to an arid habitat. d Pteroclididae. Vidensk. Meddr dansk naturh. Foren. 139: ( 179 - 243. r

e One further preadaptation to the sandgrouse's lifestyle GRANT, G.S. 1982. Avian incubation: egg temperature, nest humidi­ h s deserves mention, namely transport of water in the belly i ty, and behavioral thermoregulation in a hot environment. Orn. l b plumage. Transport of drinking water by male sandgrouse to Monogr. 30: 1-75. u their young is done by soaking the belly feathers in water until GRAUL. W.D. 1975. Breeding biology of the mountain plover. P

e saturated (belly-soaking), then flying to where the young have Wilson Bull. 87: 6 - 31. h

t JEHL, J.R., Jr. 1968. Relationships in the Charadrii (shorebirds): a

been left crouched and letting them drink from the wet plumage y taxonomic study based on color patterns of the downy young. San b (Cade & Maclean 1967; Maclean 1983). Belly-soaking as a Diego Soc. Nat. Hist. Mem. 3: I - 54. d e means of water transport is confined to the Charadriiformes JESSON, R.A. & MACLEAN, G.L. 1976. Salt glands in the neonatal t

n and Pterocliformes and has been extensively reviewed by Australian . Emu 76: 227. a r Maclean (1974) and further discussed by Grant (1982). JOUBERT, C.S.W. & MACLEAN, G.L. 1973. The structure of the g water-holding feathers of the Namaqua sandgrouse. Zool. afro 8: e c As a means of cooling or humidifying eggs and/or young 141-152. n e in a shoreline habitat, belly-soaking is an obviously suitable LOUW, G.N. & SEELY, M.K. 1982. Ecology of desert organisms. c i l mechanism. The feathers of waders are somewhat modified p.41. Longman, New York. r MACLEAN, G.L. 1967a. Die systematische Stellung der Flughiihner e to hold water in their fIlamentous barbules. As a means of d (Pteroclididae). J. Orn. 108: 203-217. n water transport in an arid environment, belly-soaking is ad­

u MACLEAN, G.L. 1967b. The breeding biology and behaviour of the vantageous only if the adults have to drink frequently (daily y double-banded africanus (Temminck). Ibis 109: a or nearly so). It is therefore not slU"prising that sandgrouse have 556-569. w e

t not only retained and refmed belly-soaking as a behaviour pat­ MACLEAN, G.L. 1969. A study of seedsnipe in southern South a , but have undergone considerably greater modification America. Living Bird 8: 33 - 80. G

t of feather structure, especially in the belly region, for just this MACLEAN, G.L. 1974. Belly-soaking in the Charadriiformes. J. e Bombay Nat. Hist. Soc. 72: 74 - 82. n

i purpose (Joubert & Maclean 1973), to the extent that a sand­ MACLEAN, G.L. 1976a. A field study of the